Utah State University
DigitalCommons@USU
All Graduate Theses and Dissertations
Graduate Studies
2015
Population and Community Dynamics of
Freshwater Decapods in Response to Ecological
and Anthropogenic Factors in Subtropical Streams
in the Caribbean
Omar Perez-Reyes
Utah State University
Follow this and additional works at: http://digitalcommons.usu.edu/etd
Recommended Citation
Perez-Reyes, Omar, "Population and Community Dynamics of Freshwater Decapods in Response to Ecological and Anthropogenic
Factors in Subtropical Streams in the Caribbean" (2015). All Graduate Theses and Dissertations. Paper 4501.
This Dissertation is brought to you for free and open access by the
Graduate Studies at DigitalCommons@USU. It has been accepted for
inclusion in All Graduate Theses and Dissertations by an authorized
administrator of DigitalCommons@USU. For more information, please
contact [email protected].
POPULATION AND COMMUNITY DYNAMICS OF FRESHWATER DECAPODS IN
RESPONSE TO ECOLOGICAL AND ANTHROPOGENIC FACTORS IN
SUBTROPICAL STREAMS IN THE CARIBBEAN
by
Omar Pérez-Reyes
A dissertation submitted in partial fulfillment
of the requirements for the degree
of
DOCTOR OF PHILOSOPHY
in
Ecology
Approved:
________________________
Todd A. Crowl
Major Professor
________________________
Alan P. Covich
Committee Member
________________________
Phaedra Budy
Committee Member
________________________
Chris Luecke
Committee Member
________________________
Mark Brunson
Committee Member
________________________
Mark McLellan
Vice President for Research and
Dean of the School of Graduate Studies
UTAH STATE UNIVERSITY
Logan, Utah
2015
ii
Copyright © Omar Pérez-Reyes 2015
All Rights Reserved
iii
ABSTRACT
Population and Community Dynamics of Freshwater Decapods in Response to Ecological and
Anthropogenic Factors in Subtropical Streams in the Caribbean
by
Omar Pérez-Reyes, Doctor of Philosophy
Utah State University, 2014
Major Professor: Dr. Todd A. Crowl
Department: Watershed Sciences
Streams have been impacted by human activities in a variety of ways. Over time, these
ecosystems become dominated by the most resilient species, with significant losses in the natural
components that provide valuable ecosystem services to people. In impacted streams, the loss of
ecosystem services often is not recognized until the stream has already been dramatically altered.
In this study, I provide data on the natural distribution of freshwater decapods and the status of
decapod communities in streams with different land use histories.
I reviewed the decapod distribution for the Caribbean to provide an update of the species
that inhabit the freshwater systems. I determined the presence of 18 species of decapods in
Puerto Rico and concluded that these decapods follow the island-species relationship in the
Caribbean. Also, I present data associated with decapod community dynamics in watersheds with
different urban development. As, expected the highly urban watershed had lower diversity and
density of decapods than the medium and low urban watersheds. The variations in decapod
communities among watersheds correlated with the degradation of the physical-chemical
environments and clearing of the riparian zones. I compare the food webs among streams with
different human impacts. Specific influences of point/nonpoint sources of N could be
iv
distinguished in food web components. This shows to an effect of human activities on the stream
and watershed. In addition, I determined the effect of abiotic and biotic factors on the growth of
A.lanipes (0.27 mm) and X.elongata (0.1 mm) over the 10-year period of study. The results
showed that these species transform a wide range of organic materials into their biomass. Finally,
I developed a series of education projects which promote the understanding and knowledge of
freshwater ecosystems; interactions and the organisms that inhabit these systems. The results
showed an increasing interest about freshwater fauna and ecosystems.
I concluded that: a) the distribution of freshwater decapods in the Caribbean islands
follows the area-species relationship; b) urbanization represents one of the many distinct land
uses that affect habitat structure, energy sources and biotic interactions; and c) it’s necessary to
present the results of our research to the general public in ways that are easily understood.
(193 pages)
v
PUBLIC ABSTRACT
Population dynamics of the freshwater decapods in response to ecological and anthropogenic
factors in subtropical Puerto Rican streams: A Caribbean perspective
Omar Pérez-Reyes
Historically, cities were established in close proximity to the richest agricultural lands
and freshwater resources. In tropical islands, urbanization occupies a large percentage of land use
along streams and rivers and strongly affects the biota and habitat quality. I studied freshwater
decapod population and community dynamics in tropical streams of Puerto Rico across human
and elevational gradients. I found that: 1) streams with less urbanization had higher decapod
species richness and population sizes than the highly urbanized streams; 2) changes in the food
webs in the streams are the result of the influence of changes in land use and environmental
conditions in their watersheds; 3) Atya lanipes and Xiphocaris elongata marked and measured biannually over a 10 year period have a relatively long lifespan (over 15 years) and slow growth
rates (Atya grew an average of 0.27 mm per year while Xiphocaris only 0.1 mm per year). In
order to present the results of our investigations in the Luquillo Forest, we developed an
education plan which includes web sites, field exercises, and training program for teachers and
students. The results suggested that ecological education and outreach efforts should explore the
use of available and trusted methods of dissemination to supplement and encourage use of the
internet as a reliable source of information. I conclude that changes in land use have a direct
impact on streams components and in the terrestrial corridor near the water body. Alterations of
these components can increase the erosion of the stream banks, sedimentation and water flow that
impacts the habitat, abundance, diversity and life cycle of organisms in the stream.
vi
DEDICATION
I dedicate my dissertation work to my family and friends.
I want to extend a special feeling of gratitude to my parents,
Ramón Pérez-Vega and Hipólita Reyes-Nieves,
my brother Ramón A. Pérez-Reyes and sister Jessica Pérez-Reyes.
whose words of encouragement led me in this new step.
I also dedicate this dissertation to my many friends
(Fernando A. Villar-Fornes, Francisco J. Pérez-Rivera, and Gladys Nazario) who have
helped me throughout the research process.
vii
ACKNOWLEGMENTS
I would especially like to thank Drs. Todd A. Crowl and Alan P. Covich for acting as my
advisers, their committed guidance and assistance during the research and preparation of my
thesis was greatly appreciated. I would also like to thank Dr. Mark Brunson for providing
valuable suggestions and comments through the project. I also thank Phaedra Budy and Chris
Luecke for their advice, suggestions and time. Thanks to other graduate students and technicians
who committed their time and effort in the field to help collection of valuable data for the project.
viii
CONTENTS
Page
ABSTRACT.................................................................................................................................... iii
PUBLIC ABSTRACT ..................................................................................................................... v
DEDICATION ................................................................................................................................ vi
ACKNOWLEDGMENTS ............................................................................................................. vii
LIST OF TABLES .......................................................................................................................... ix
LIST OF FIGURES ......................................................................................................................... x
CHAPTER
1.
INTRODUCTION ................................................................................................. 1
2.
FRESHWATER DECAPODS OF PUERTO RICO: A CHECKLIST AND
REPORTS OF NEW LOCALITIES ...................................................................... 5
3.
COMPARISON OF DECAPOD COMMUNITIES ACROSS AN URBANFOREST LAND USE GRADIENT IN PUERTO RICAN STREAMS .............. 41
4.
COMPARISON OF TROPHIC RELATIONSHIPS IN CONTRASTING
TROPICAL STREAMS IN PUERTO RICO ...................................................... 83
5.
EFFECTS OF FOOD SUPPLIES AND WATER TEMPERATURE ON
GROWTH RATES OF TWO SPECIES OF FRESHWATER TROPICAL
SHRIMPS .......................................................................................................... 120
6.
EVALUATION OF A WEB-BASED EDUCATION PROGRAM:
COMMUNICATING ECOLOGICAL KNOWLEDGE TO THE PUBLIC
ABOUT THE LUQUILLO EXPERIMENTAL FOREST ................................ 148
7.
SUMMARY AND DISCUSSION..................................................................... 167
APPENDICES ............................................................................................................................. 173
CURRICULUM VITAE .............................................................................................................. 175
ix
LIST OF TABLES
Table
Page
2-1
Distribution of the 18 freshwater decapod species sampled at the 43 freshwater
bodies (rivers, streams, rivulets, and caves) in Puerto Rico ............................................. 31
2-2
Antillean islands, area, and number of families, genera and species of freshwater
decapods included in the study ......................................................................................... 34
3-1
Mean (+ SE) of physicochemical and environmental parameters of the water in
low, moderate and highly urban development watersheds in Puerto Rico.
Measurements were made per sampling site (n=3) in each watershed (n=3)
during 24 hours in 2010–2011 ......................................................................................... 73
3-2
Mean decapod species density (+ SE) in the different watersheds of the low,
moderate and high urban watersheds during 2010-2011 .................................................. 74
3-3
Minimum, mean (+ SE) and maximum number of embryos per female, regression
equations showing relationship between female size (CL) and fecundity (FEC)
for each land use section in the Low, Moderate, and High impact watersheds
during the wet season. ....................................................................................................... 75
4-1
Feeding habits of the studied species based, the δ13C and δ15N values (mean + SE) and
the sample size of the macroinvertebrates and fish communities from the LUW, MUW,
and HUW (Sabana, Bayamón, and Rio Piedras) ............................................................ 113
5-1
Range, mean and standard deviation of chemical variables of the stream water in
Quebrada Prieta. Long-term chemical data from Luq-LTER (1999-2007) ................... 142
6-1
List of the frequently used-keywords to search information and the number of sessions
observed in the REP and PER websites during 2012-2013 ............................................ 162
6-2
Landing pages for the user of the websites and the percentage of sessions in the
REP and PER during the years 2012 and 2013............................................................... 163
x
LIST OF FIGURES
Figures
Page
2-1
Geographic distribution of shrimp species from the family Atyidae sampled
and reported for the major rivers of Puerto Rico and their tributaries .............................. 37
2-2
Geographic distribution of shrimp species from the family Palaemonidae sampled
and reported for the major rivers of Puerto Rico and their tributaries .............................. 38
2-3
Geographic distributions of Epilobocera sinuatiforns and Xiphocaris elongata
in the major rivers of Puerto Rico ..................................................................................... 39
2-4
Species-area relationships of freshwater decapods in the Antilles ................................... 40
3-1
Location of the Low (Río Sabana), Moderate (Río Bayamón), and Highly urban
(Río Piedras) watersheds of the studied streams in the north coast of Puerto Rico .......... 77
3-2
Comparison of predominant land use/land cover groups among watersheds (Low,
Moderate, and High urban development). Watersheds analyses include all the area from
the headwaters to the mouth of the streams ...................................................................... 78
3-3
Mean (+ SE) species number (S) a), Shannon-Weiner Diversity Index (H’) b),
Evenness (J) c), and Density d) of the freshwater decapod communities for each
watershed (Low-Sabana, Moderate-Bayamón and High-Río Piedras urban categories)
during the rainfall season (HRF-High Rainfall and LRF-Low Rainfall) ......................... .79
3-4
Nonmetric multidimensional scaling (NMDS) results from ordination of decapod
family densities ................................................................................................................. 80
3-5
Multiple regressions showing the relation between female cephalothorax length
(mm) and reproductive output. ......................................................................................... 81
3-6
Mean (+ SE) larvae drift densities and discharge in 24-hour (H-hour, M-minutes, Sseconds) sampling period in the Low (Sabana) (a), Moderate (Bayamón) (b) and in the
High (Rio Piedras) (c) urban watersheds .......................................................................... 82
4-1
Proportions of food items in stomachs of Atya innocuous (Ai), A.lanipes (Al),
A.scabra (As), Micratya poeyi (Mp), Macrobrachium acanthurus (Ma),
M.faustinum (Mf), Xiphocaris elongata (Xe), and Palaemon pandaliformis (Pp)
shrimp from the Sabana (a), Bayamón (b) and Rio Piedras (c) rivers ............................ 117
4-2
δ13C and δ15N stable isotope biplots for primary, secondary and tertiary consumers
collected from LUW (a), MUW (b) and HUW (c). ...................................................... 119
5-1
Percentage of gravid females of Atya lanipes and Xiphocaris elongata across time
xi
(1997-2007), rainfall periods (HRF and LRF), and pools (Upper,
Middle and, Low altitude) in Quebrada Prieta................................ ................................ 143
5-2
Annual frequencies of size classes in populations of a) Atya lanipes and b) Xiphocaris
elongata during 1997 to 2007 ......................................................................................... 144
5-3
Relationship between average growth (+ SE) of the shrimp Atya lanipes (n = 10) and
Xiphocaris elongata (n = 12) and the years of the experimental period in Quebrada
Prieta ............................................................................................................................... 145
6-1
Monthly number of sessions and pageviews of the users of the websites during the
years 2012 and 2013: a) River Education Program, b) Programa Educativo sobre
Ríos. .............................................................................................................................. 164
6-2
Average monthly sessions (+ Standard Error) and bounce rates (+ SE) for the REP
(a) and PER (b) during the years 2012 and 2013 ........................................................... 165
6-3
Percentage of sessions per country or territories in the REP (a) and PER (b) websites
during 2012 (open bar) and 2013 (closed bar) ................................................................ 166
CHAPTER 1
INTRODUCTION
Urbanization represents one of the distinct land uses that disproportionately affect streams.
Increases in human population size have often generated an urban sprawl that results in increased
pollution, depletion of water resources, and destruction of wilderness and wildlife habitats.
Transition from forested to urban landscapes represents a significant threat to sustaining functions
of stream ecosystem.
Urbanized streams have been impacted, modified, and often degraded by human
activities in a variety of ways. Over time, these freshwater ecosystems become dominated by the
most resilient species, resulting in the loss of many natural components that provide valuable
ecosystem services to people. In urban and sub-urban streams, the loss of freshwater ecosystem
services often is not recognized until the stream has already been dramatically altered or
impacted. Numerous anthropogenic stressors and their effects on streams have been identified:
channel modification; loss of riparian vegetation; water withdrawal; addition of alien taxa;
changing land use; and pollutant generation (Paul and Meyer 2001). These stressors directly
impact the physical integrity (loss of large woody debris, canopy opening, stream hydrology,
geomorphology, and sedimentation), the physiochemical elements (nutrient enrichment,
contaminant pollution, water quality and toxicity) and the biological components (biotic
interactions, habitat structure, energy source, and alterations in trophic structure) of the stream
(Booth and Jackson 1997, Meyer et al. 2005). As a result, these stressors change the ecological
integrity (removal of native species and decline in abundance and richness of macroinvertebrates) and ecosystem services (variation of ecosystem processes and trophic structure that
affect water quailty); this characteristic pattern is termed the “Urban Stream Syndrome” (Walsh
et al. 2005).
2
The effects of watershed land use on streams and rivers are well-documented and these
alterations produced a community structure, sometimes totally or partially degraded, that is
significantly different from previous conditions or from similar un-degraded streams. Recent
studies have illustrated these effects. For example, there is often a reduction in shade from
removal of riparian forest that increases water temperature, promoting algal growth in the stream
(Allan 2004). Riparian clearing also decreases bank stability, input of organic matter and
increases channel erosion. Other consequences of the removal of land cover are that the soil
surface becomes more compacted and impervious, the infiltration decreases and the surface
runoff increases. In addition, sedimentation increases turbidity, scouring, abrasion, and changes
in the substrate that leads to changes in periphyton and biofilm production, an important food
source for most stream communities. The impervious surfaces transport fertilizers and
contaminants directly into the streams where the excess nutrients increase the algae production.
Contaminants impact the fauna through deformities, disruption of internal systems, and
ultimately, mortality rates.
Diverse studies have shown negative relationship among stream communities and land
use. Larger deforested patches in the riparian forest have been associated with a decrease in
abundance of benthic-dependent species that have been replaced by sediment-tolerant and/or
exotic species. Long-term studies have shown the impacts of urbanization on streamsthrough: 1)
decreases in the abundance and species diversity; 2) removal of sensitive species and increases in
more tolerant species; 3) greater flood frequencies. The magnitude of land use influences on
these characteristics depends on slope, soil type, and riparian vegetation of the watershed (Paul
and Meyer 2001).
Aquatic insects are the most widely used group of organisms in biomonitoring studies
(Allan 2004). Their importance resides in their sensitivity to represent changes in the
environment. Moore and Palmer (2005), Cuffney et al. (2010), among many others have
3
demonstrated a strong relationship between the catchment land cover and the stream biota; taxa
richness, abundance and diversity decrease in stream with low riparian forest cover. A decrease
in invertebrate diversity can be explained by diverse factors such as: habitat loss (sedimentation
and loss of woody debris); pollution and chemical contamination (nutrient inputs from agriculture
in riparian zones, toxins and reduction in dissolve oxygen concentration) (Allan 2004); and
replacement of species (shifts and eliminates important species in the food web for non-necessary
ones) (Sudduth and Meyer 2006).
This study had 5 objectives. In the first chapter, I describe the distribution of freshwater
decapods in Puerto Rico and the Caribbean. In Chapter 2, I examined changes in decapod
assemblages, water quality, and habitat quality along two streams with varied land uses and one
forested stream that served as a reference stream. I predicted that decapod diversity and
abundance would be greater in streams within high percentages of forest cover compared to sites
with limited forest. In Chapter 3, I evaluated the decapod and fish communities in forested and
urban streams in Puerto Rico in order to compare food webs from streams with different degrees
of human impact. I hypothesized that the effects of anthropogenic stressors on freshwater food
webs would be less dramatic in forested streams compared to urban ones. In Chapter 4, I
reported the growth rates of marked shrimp in the headwaters of the Luquillo Mountains.
Comparisons in growth were observed in long-term changes under natural conditions, in response
to hurricane-driven disturbances, temperature, and seasonal inputs of leaf litter. Finally in
Chapter 5, I proposed and developed some educational tools (e.g., web sites, workshops, field
activities) to present the ecological information derived from research in Luquillo Experimental
Forest to the general public.
4
LITERATURE CITED
Allan, J.D. 2004. Landscapes and riverscapes: the influence of land use on stream ecosystems.
Annual Review of Ecology, Evolution, and Systematics 35: 257-284.
Booth, D,B, and C.R. Jackson. 1997. Urbanization and aquatic systems: degradation thresholds,
stormwater detection, and the limits of mitigation. Journal of American Water Resources
Association 33: 311-323.
Cuffney, T. F., R. Kashuba, S.S. Qian, I. Alameddine, Y.K. Cha, B. Lee, J.F. Coles and G.
McMahon. 2011. Multilevel regression models describing regional patterns of
invertebrate and algal responses to urbanization across the USA.Journal of North
American Benthological Society Journal 30: 797-819.
Meyer, J.L., M.J. Paul, and W.K.Taulbee. 2005 Stream ecosystem function in an urbanizing
landscape. Journal of North American Benthological Society Journal 24: 602-612.
Moore, A.A. and M.A.Palmer. 2005. Invertebrate biodiversity in agricultural and urban
headwater streams: implications for conservation and management. Ecological
Applications 15: 1169-177.
Paul, M.J. and J.L.Meyer. 2001 Streams in the urban landscape. Annual Review of Ecology,
Evolution, and Systematics 32: 333-365
Sudduth, E. B., and J.L. Meyer. 2006. Effects of bioengineered streambank stabilization on bank
habitat and macroinvertebrates in urban streams. Environmental Management 38(2):
218-226.
Walsh, C.J., A.H. Roy, J.W. Feminella, P.D. Cottingham, P.M. Groffman, R.P. III Morgan. 2005.
The urban stream syndrome: current knowledge and the search for a cure. Journal of
North American Benthological Society Journal 24: 706-723.
5
CHAPTER 2
FRESHWATER DECAPODS OF PUERTO RICO: A CHECKLIST
AND REPORTS OF NEW LOCALITIES1
Abstract
An updated checklist of the freshwater decapod fauna of Puerto Rico is presented based on
records of shrimp and crab species whose presence has been confirmed in Puerto Rico as a result
of extensive field collections, examination of carcinological collections, literature review, and
personal communications from researchers.
The freshwater decapod fauna of Puerto Rico
consists of 18 species of shrimp belonging to eight genera and three families, and one species of
crab belonging to the family Pseudothelphusidae.
Introduction
The freshwater decapod fauna of Puerto Rico is relatively well known for their role in the
ecological process as shredders and for nutrient cycling (Crowl et al. 2001). However, relatively
little work has been done on shrimp and crab diversity, distribution and inventory in a systematic
way in Puerto Rico.
Juan Gundlach (1887) reported many species of decapods on the island but Schmitt
(1935) in the Scientific Survey of Porto Rico and the Virgin Island, was the first to report the
presence of freshwater decapods.
Macrobrachium acanthurus (Weigmann), M. carcinus as
“Periclimenes portoricencis” (Linnaeus 1758), and M. faustinum (De Saussure), Xiphocaris
elongata (Guérin-Méneville), Atya scabra (Leach, 1815), A. innocuous (Herbst) and Micratya
poeyi (Guérin-Méneville) were reported by Schmitt. In 1954, Chace reported the first troglobitic
1
Coauthored by Omar Pérez-Reyes, Todd A. Crowl, Pablo J. Hernández-García, Ricardo Ledesma-Fusté,
Fernando A. Villar-Fornes, and Alan P. Covich
6
species for the Archipelago of Puerto Rico: Typhlatya monae (Chace 1954). Typhlatya has been
reported in caves on Mona Island, Guánica Dry Forest-Puerto Rico, Dominican Republic,
Curacao, Barbuda and Lesser Antilles (Debrot 2003). In 1967, Vélez made the first checklist of
freshwater and terrestrial decapods of Puerto Rico and reported the presence of Atya innocuous as
“A. occidentalis” and Atya scabra as “Atyia scabra”. Based on their own collections in 19641966 and material provided by others, Chace & Hobbs (1969) documented distribution, ecology
and taxonomy of the freshwater decapods of the Caribbean; but they did not identify the precise
location or collection date of the specimens. Canals (1977; 1979) reported collecting specimens
of Macrobrachium crenulatum (Holthuis) in the Espíritu Santo River and classified this location
as the only one in the island for this shrimp. Villamil and Clements (1976) working in the same
river described the ecology and distribution of the freshwater shrimp in the upper parts of the
river. In their report, Villamil and Clements concluded that some species of atyids showed intraspecific habitat selection based on water flow, type and size of the substrate. The effects of
abiotic factors on distribution and development of palaemonids were studied by Santiago (1979),
and Ching and Vélez (1985).
Hobbs and Hart (1982) did a comprehensive analysis of the distribution, taxonomy and
classification of the Atya genus globally. Their report of Atya included the three species of Atya
present in Puerto Rico: A. lanipes, A. innocuous and A. scabra, but the report was incorrect in
relation to the locations for these shrimp in the island. They reported these species only in 10
streams and rivers around the island.
Montero (1987), Johnson et al. 1998, and Pérez-Reyes (1999) described the general
ecology, reproductive biology and fecundity of atyids species in the island. Montero (1987)
described the fecundity of Micratya poeyi (Guérin-Méneville) and Jonga serrei (Bouvier) in the
Tanamá and Río Grande de Arecibo rivers and concluded that adults of these species showed
sexual dimorphism, where female are bigger than males. Johnson et al. (1998) sampled Atya
7
lanipes at the Luquillo Experimental Forest and associated the egg production with high flows
and high food availability. Pérez-Reyes (1999) in his work regarding the abundance, diversity
and life histories of freshwater decapods in Puerto Rico, concluded that there were no differences
in species diversity, fecundity and density in rivers that flow through different ecological life
zones. In addition, Pérez-Reyes reported new localities for Macrobrachium crenulatum Tanamá,
Cerrillos, Loco and Camuy rivers.
The upstream migration of Xiphocaris elongata,
Macrobrachium spp., and Atya spp. was studied by Kikkert (2009) at the Espiritu Santo River.
He reported that massive migration occurs at night and when the water flow is minimal. New
records on Potimirim and a new species of Micratya were reported by Holmquist et al. (1998)
(Potimirim glabra Kingsley 1878) and Pérez-Reyes (1999; 2010 unpublished data) (Potimirim
americana Guérin-Méneville 1855), and Karge et al. (2013) (Micratya cooki) respectively.
Recently a new Potimirim species from the Guayanes River in the municipality of Yabucoa was
discovered by Fernando Mantelatto, they are working in the molecular and morphological
description (F.Mantelatto pers. com.).
The endemic potamonid crab, Epilobocera sinuatifrons (A.Milne-Edwards, 1866) was
described by Milne-Edwards (1866) and Rivera (1996), who when describing the distribution of
this freshwater crab found that Epilobocera occurs in all kinds of habitats, elevations and
environments.
The distribution of the Buruquena in the Luquillo streams was studied by
Zimmerman and Covich (2003) reporting that the distribution and abundance of Epilobocera
correlated with the physical habitat (pool depth, volume, high water velocity, substrate type and
size, and high water flow) and previous use of the forest. The growth rate and diets of this
freshwater crab were described by Fraiola (2004). He found that E. sinuatifrons feeds on a wide
variety of plants and animals in the stream and in the riparian forest, where the growth rate was
-1
limited to 0.02 mg mg per day, and that they reached reproductive maturity in their 7th year. The
8
genetic status of E. sinuatifrons was described by Cook et al. 2008a. They reported that the
populations are differentiated among rivers but have a natural history to be recently derived, since
these species have not experienced population expansions or bottlenecks.
Knowledge of freshwater decapods diversity in the Caribbean has increased rapidly in
recent years as a result of studies that describe their role in aquatic ecosystems, as part of the food
chain and as recyclers of organic material. The most recent works and the long term experiments
on the ecology of the freshwater decapods from Puerto Rico have been done at Luquillo
Experimental Forest. The research has focused on the ecological interactions of the decapods
with other species (Pringle et al. 1993; 1996; Crowl & Covich 1994; Johnson et al. 2000; March
et al. 1998; 2002; Cook et al. 2008b; Covich et al. 2009; Hein et al. 2010), the effects of natural
(Covich et al. 1991; 1996; 2003; 2006) and anthropogenic disturbances on the populations
(Benstead et al. 1999; 2000; Greathouse et al. 2005; 2006; Hein et al. 2010; March et al. 1998;
2003), and in the nutrient recycling importance for the species (Pyron et al. 1999; March et al.
2001; March & Pringle 2003; Wright & Covich 2005; Covich & McDowell 1996, Crowl et al.
2001; 2006; Cross 2008; Benstead et al. 2010).
The goal of this study is to contribute knowledge of the freshwater decapod fauna found
in the Puerto Rico archipelago describing their distributions, and to clarify which are the valid
shrimp and crab species in the island. The list contained herein is a comprehensive list of the
decapod fauna found in Puerto Rico based on a revision of previously published data, museum
collections, personal collections and research. Additionally, in this study a newly taxonomic key,
distribution maps and recorded species have been added to the information of the freshwater
decapod fauna of the island. Representative specimens were deposited in the Zoology Museum at
the University of Puerto Rico, Río Piedras Campus, Museo Nacional de Historia Natural de
República Dominicana and in the reference collection at El Verde Field Station, University of
Puerto Rico.
9
Study Area
The Archipelago of Puerto Rico is located in between the Atlantic Ocean and the
Caribbean Sea and comprises 3 inhabited islands; Puerto Rico, Vieques and Culebra, 4 natural
reserve islands (Mona, Monito, Desecheo, and Caja de Muerto) and more than 100 cays. With an
area of 9,104 km2, Puerto Rico is the third largest island in the United States. Six ecological life
zones have been described for Puerto Rico and ranging from dry to rain forest (Ewel & Whitmore
1973; Helmer et al. 2002). Subtropical Lower Montane Rain Forest occupies the smallest area
with 12.3 km2 while the Subtropical Moist Forest is the prevailing life zone, covering more than
5,482 km2 (Ewel & Whitmore 1973; Helmer et al. 2002). Numerous rivers and streams flow
down from the mountains of the Cordillera Central but only 41 reach the coastal plains; rivers
from the north coast are larger, with tranquil waters, and have higher flow capacity in comparison
to the southern rivers that have extensive drought periods. The characteristics present on each
river, in combination with the conditions of the ecological life zones, provide the environment for
diverse mesohabitats that the different species of decapods can exploit.
Material and Methods
The following list is based on preserved specimens for most species. Sporadic collecting
was mainly undertaken from 1970–2011. Decapods were sampled by hand using aquatic nets,
minnow traps or electroshocker. The material collected was identified by one of us (OPR) and is
housed in the Zoological Collections of the Biological Museum at the University of Puerto Rico,
Río Piedras Campus and El Verde Field Station, University of Puerto Rico, Río Piedras Campus.
In addition, parts of the data that formed the basis of the checklist were obtained from the
literature cited in the introduction and collections at the National Museum of Natural History,
Smithsonian Institution, and Museum of Comparative Zoology of Harvard University.
10
Nomenclature, classification and common name (McLaughlin et al. 2005) of taxa follows
the Chace and Hobbs (1969), Chace (1972), Holthuis (1980), Hobbs and Hart (1982)
descriptions.
Some common names are derived from the native Taíno languages or local
fisherman.
Results and Discussion
A total of 18 species of freshwater decapods from 4 families were found to inhabit the
freshwater systems of the Puerto Rico Archipelago (Table 2-1; Fig. 2-1, 2-2, and 2-3). The
families represented include Atyidae (10 taxa or 56% of the biota), Palaemonidade (6 taxa or
33%), Xiphocarididae (1 taxa or 5%), and Pseudothelphusidae (1 taxa or 5%) (Table 2-1). Three
species of shrimp, Potimirim glabra, Potimirim americana, and Palaemon pandaliformis, are
new records for the island. Micratya cooki represents the new species for Puerto Rico.
The diversity of freshwater carcinological fauna is expected for an island of its size
(Table 2-2; Fig. 2-4), although the list is expected to grow with more intensive surveys,
particularly in the estuarine portions of the rivers and subterranean streams in the karst area of the
island. Decapod species richness and composition of the area surveyed suggest healthy stream
environments. The diversity here reported is comparable to that of Hispaniola (Pérez-Gelabert
2008), which has 19 taxa reported and Jamaica with 21 species of freshwater decapods (Schubart
& Koller 2005). Detailed examination indicates that the species-area relation among the Greater
and Lesser Antilles results because larger islands have more number and diverse habitats in
contrast with the smaller ones (Losos & Losos 1996). The diversity of the freshwater decapod
group in the Caribbean Archipelago tends to be controlled primary by the size of the island and
the dispersion of the organisms. Habitat and vegetation types in the Lesser Antilles are primary
catalogued as xerophytic and mesophytic, only Guadeloupe, Dominica, Martinique and St. Lucia
(Isaac & Bourque 2001) have abundant rainfall and higher densities of streams and rivers capable
11
to sustain hydrophytic vegetation and abundant freshwater fauna (Ricklefs & Lovette 1999).
Similar distribution, diversity and abundance has been observed in lizards (Anolis) (Losos &
Losos 1996; Losos & Schluter 2000), birds (Coereba) (Ricklefs & Lovette 1999; Ricklefs 2000),
bats (Ricklefs & Lovette 1999), butterflies (Heliconious & Dryas) (Davies & Spencer-Smith
1998; Ricklefs & Lovette 1999; Davies & Bermigham 2002) (McDowell et al. 2012). The life
cycle histories of these species influence the distribution and abundance through the Caribbean
Archipelago. All freshwater shrimp in the Caribbean exhibit an amphidromous life cycle where
adults reproduce in the high elevation sections of the stream and the larvae need to spend time in
the estuary until metamorphose and migrate to the upper locations of the freshwater bodies. This
results in a common species pool in the estuaries and the sea capable to colonize and migrate
among the islands.
Freshwater decapods were found across all ecological life zones, with the richest systems
(Río Bayamón, Río Mameyes and Río Sabana) were located in the north part of the island or in
the Subtropical Moist Forest. What is more significant, however, is the presence of all the
seventeen native species in most of the rivers specifically in the highly forested streams of El
Yunque National Forest (Río Mameyes, Río Sabana & Río Espiritu Santo) and in the highly
urbanized Río Bayamón (Table 2-1; Fig. 2-2 & 2-3).
The relatively rich and unaltered
environment, presence of organic matter, longitudinal connectivity and the physical-chemical
variables may provide the conditions for which these streams are important areas for the
conservation of these aquatic animals.
Although this checklist is richer in Atyidae and Palaemonidae species than previously
reported by Vélez (1967) and Chace and Hobbs (1969); the reports by Holmquist et al. 1994,
Pérez–Reyes (1999), and Kwak et al. 2007, which were largely from field collections, appear to
reveal a bias towards big and larger species.
12
Checklist of freshwater decapods species collected in Puerto Rico.
Family ATYIDAE
Genus Atya Leach, 1816
1. Atya scabra (Leach, 1815) - Gata shrimp, camacuto shrimp, Gata, Guábara
2. Atya innocuous (Herbst, 1792) - Basket shrimp, Gata, Guábara
3. Atya lanipes Holthuis, 1963 – Spinning basket shrimp, Guábara
Genus Jonga Hart, 1961a
1. Jonga serrei Hart, 1961a- Estuarine tiny basket shrimp, Guabarita
Genus Micratya Bouvier, 1913
1. Micratya poeyi Bouvier, 1913 - Caribbean dwarf filter shrimp, Guabarita
2. Micratya cooki Karge, 2013 – Puerto Rico dwarf filter shrimp, Guabarita
Genus Potimirim Holthuis, 1954
1. Potimirim americana (Guérin-Méneville, 1855) – American potimirim,
Guabarita
2. Potimirim mexicana (De Saussure, 1857) – Mexican potomirim, Guabarita
3. Potimirim glabra (Kingsley, 1878) - Smooth potimirim, Guabarita
Genus Typhlatya Creaser, 1936
1. Typhlatya monae Chace, 1954 - Eastern Caribbean cave shrimp, Camarón Ciego
Family XIPHOCARIDIDAE
Genus Xiphocaris Ortmann, 1895
1. Xiphocaris elongata (Guérin-Méneville, 1856) - Yellow-nose shrimp, Salpiche,
Piquines
13
Family PALAEMONIDAE
Genus Macrobrachium Bate, 1868
1. Macrobrachium carcinus (Linnaeus 1758) – Painted river prawn, Big claw river
shrimp, Camarón Palancú
2. Macrobrachium acanthurus (Wiegmann, 1836) - Cinnamon river shrimp,
Tuberculoso
3. Macrobrachium heterochirus (Wiegmann, 1836) - Cascade river prawn,
Camarón Palancú
4. Macrobrachium faustinum (De Saussure, 1857) - Caribbean long arm shrimp,
Zurdito, Camarón Bocú
5. Macrobrachium crenulatum Holthuis, 1950 - Striped river shrimp, Zurdito,
Camarón Bocú
Genus Palaemon Weber, 1795
1. Palaemon pandaliformis (Stimpson, 1871) - Grass shrimp, Potitinga shrimp
Family PSEUDOTHELPHUSIDAE
Genus Epilobocera Stimpson 1860
1. Epilobocera sinuatifrons (A. Milne-Edwards, 1866) - Puerto Rican freshwater
crab, Buruquena (Taino name), jaiba
14
Taxonomic Key for the Atyidae and Xiphocarididae families in Puerto Rico
(Modified from Chace & Hobbs 1969; Chace 1972)
1 Chelae of first and second pereiopods without tufts of long hairs at ends of fingers
XIPHOCARIDIDAE ... Xiphocaris elongata
- Chelae of first and second pereiopods with tufts of long hairs at ends of fingers ATYIDAE...2
2 Eyes reduced, cornea limited to distolateral pigment spot on eyestalk; subterranean species ...
Typhlatya monae
- Eyes normal, cornea nearly as broad as or broader than eyestalk; pereiopods without exopods …
3
3 Compressed rostrum with teeth on the dorsal margin ... 4
- Depressed rostrum without teeth on the dorsal margin ... 5
4 Appendix masculina with spinulation near the distal end, tip of appendix interna does not reach
the spinulated part of the appendix masculine … Micratya poeyi
- Appendix masculina with spines extending more proximally, tip of the appendix interna reaches
the spinulated part of the appendix masculine … Micratya cooki
5 Carpus of second pereiopod broader than long ... 6
- Carpus of second pereiopod much longer than broad ... 8
6 Adults without horizontal lateral lobe or tooth on either side of rostrum; third pereiopod not
bearing horny scales or tubercles and only slightly more robust than fourth pereiopods ... Atya
lanipes
- Adults with distinct horizontal lateral lobe or tooth on either side of rostrum; third pereiopod
bearing prominent horny scales or tubercles and considerably larger and more robust than fourth
pereiopods ... 7
7 Lateral lobes of adult rostrum obtuse; pleuron of second abdominal somite without blunt
marginal spines although pleura of third to fifth somites may bear acute marginal denticles …
15
Atya innocuous
- Lateral lobes of adult rostrum subacute and directed anteriorly; ventral margins of pleura of
second to fifth abdominal somites armed with row of small blunt spines … Atya scabra
8 Orbital margin minutely serrate; appendix masculina on second pleopod of male slender,
terminating in sharp point … Jonga serrei
- Orbital margin not serrate; appendix masculina on second pleopod of male broad, rounded
distally … 9
9 Appendix masculina widening distally, about three-fourths as wide as long, posterior margin
slightly and evenly convex ... Potimirim americana
- Appendix masculina widest proximally, not more than half as wide as long, posterior margin
sinuous ... 10
10 Dorsal margin of rostrum curving downward at tip; appendix masculina with deep, unarmed
sinus in posterior margin ... Potimirim glabra
- Dorsal margin of rostrum nearly straight; appendix masculina without deep, unarmed sinus in
posterior margin ... Potimirim mexicana
16
Taxonomic Key for the Palaemonidae family in Puerto Rico
(Modified from Chace & Hobbs 1969; Chace 1972)
1 Carapace with two spines on anterolateral margin, antennal and branchiostegal … Palaemon
(Palaemon) pandaliformis
- Carapace with hepatic spine on lateral surface and with no more than one spine on anterolateral
margin, branchiostegal and rarely antennal spines absent; rostrum with ventral teeth … 2
2 Rostrum long, unramed throughout dorsal length, posterior tooth usually separated from second
by distance greater than that between second and third, usually reaching beyond end of antennal
scale, with 5-11 dorsal teeth, no more than 2 of which originate on carapace posterior to level of
orbital margin; second pereiopod of adult male spinulose, carpus shorter than chela, fingers
densely furred ... Macrobrachium acanthurus
- Rostrum short, reaching at most slightly beyond end of antennular peduncle, with 10-15 dorsal
teeth, at least 4 of which originate on carapace posterior to level of orbital margin; second
pereiopods robust, chela less than seven times as long as broad ... 3
3 Rostrum with sinuous dorsal margin, tip slightly upturned; second pereiopods of adult subequal
in form but not in size, with short pubescence and short spines along outer margin of fixed finger
and continued onto palm, but spines not forming distinct crest and not hidden by pubescence … 4
- Rostrum with nearly straight dorsal margin, tip not upturned; second pereiopods of adult
unequal in both form and size with dense long fur partially concealing crest-like row of long
spines on margin of palm ... 5
4 Posterior teeth of dorsal rostral series not especially erect or noticeably more widely spaced
than others; second pereiopods of adult subequal, carpus shorter than merus and about half as
long as palm, fingers only slightly shorter than palm, prominent tooth near end of proximal third
of opposable margin of fixed finger … Macrobrachium carcinus
- Three or four posterior teeth of dorsal rostral series more erect and more widely spaced than
17
anterior ones; second pereiopods of adult usually unequal in length, major one with carpus about
as long as merus and about three-fourths as long as palm, fingers about two-thirds as long as
palm, none of teeth on opposable margin of fixed finger greatly enlarged … Macrobrachium
heterochirus
5 Major second pereiopod of adult male with carpus usually longer than merus and fingers
distinctly longer than palm, row of spines along mesial margin of palm and fixed finger rather
long on proximal portion of palm, becoming shorter near middle of palm, longer near base of
finger, and decreasing again distally on finger … Macrobrachium faustinum
- Major second pereiopod of adult with carpus shorter than merus and fingers slightly longer or
slightly shorter than palm, row of spines along mesial margin of palm and fixed finger forming
regular series, not decreasing in length along middle portion of palm … Macrobrachium
crenulatum
Pseudothelphusidae
(Modified from Chace & Hobbs 1969)
Carapace not very convex longitudinally or transversely, broad, less than three-fifths as long as
wide; cervical groove distinct, concave forward; anterolateral margin denticulate, marked by two
obscure notches, one at end of cervical groove, one near outer orbital angle; front delimited
dorsally by strong transverse crest hiding entire true frontal margin from dorsal view. Third
maxilliped with merus subquadrate, lateral margin feebly convex, distal margin somewhat
concave; exopod extending beyond ischiomeral articulation. Pereiopods not unusually long or
slender. Chela without prominent, swollen protuberance on outer surface near base of fingers ...
Epilobocera sinuatifrons
18
References
Alvarez, F., Iliffe, T. M., & Villalobos, J. L. (2005) New species of the genus Typhlatya
(Decapoda:Atyidae) from anchialine caves in Mexico, the Bahamas, and Honduras.
Journal of Crustacean Biology, 25(1), 81-94.
Barnish, G. (1984) The Freshwater Shrimp of Saint Lucia, West Indies (Decapoda, Natantia).
Crustaceana, 47, 314-320.
Bauer, R. (2011a) Amphidromy and migrations of freshwater shrimp. I. Costs, benefits,
evolutionary origins, and an unusual Case of amphidromy. In: Asakura A (Ed.) New
Frontiers in Crustacean Biology. Proceedings of The Crustacean Society summer
meeting, Tokyo, 20-24 September 2009. Brill, Leiden, The Netherlands, pp 145-156.
Bauer, R. (2011b) Amphidromy and migrations of freshwater shrimp. II. Delivery of hatching
larvae to the sea, return juvenile upstream migration, and human impacts. In: Asakura A
(ed) New Frontiers in Crustacean Biology. Proceedings of The Crustacean Society
summer meeting, Tokyo, 20-24 September 2009. Brill, Leiden, The Netherlands, pp 157168.
Bauer R.T. (2013) Amphidromy in shrimp: a life cycle between rivers and the sea. In:
Wehrtmann IS & Bauer RT (eds) Studies on Freshwater Decapods in Latin America.
Latin American Journal of Aquatic Research, 41, 633-650.
Bass, D. (2003a) Freshwater macroinvertebrates of Barbados. Journal of the Barbados Museum
and Historical Society, 49, 269-280.
Bass, D. (2003b) A survey of freshwater macroinvertebrates in Tobago, West Indies. Living
World,Journal of Trinidad and Tobago Field Naturalists’ Club, 2003, 64-69.
Bass, D. (2004a) Diurnal stream drift of benthic macroinvertebrates on the small oceanic island of
Dominica, West Indies. Caribbean Journal of Science, 40, 245-252.
19
Bass, D. (2004b) A survey of freshwater macroinvertebrates on Grenada. Living World, Journal
of Trinidad and Tobago Field Naturalists’ Club, 2004, 26-31.
Bass, D. (2005) A survey of freshwater macroinvertebrates from Antigua. Living World, Journal
of Trinidad and Tobago Field Naturalists’ Club, 2005, 11-14.
Bass, D. (2006) A comparison of the freshwater macroinvertebrate assemblages of St. Kitts and
Nevis, West Indies. Living World, Journal of Trinidad and Tobago Field Naturalists’
Club, 2006, 30-37.
Bass, D. (2007) Freshwater macroinvertebrates and their habitats in Dominica. Living World,
Journal of Trinidad and Tobago Field Naturalists’ Club, 2007, 21-30.
Bate, C.S. (1868) On a new genus, with four new species, of freshwater prawns. Proceedings of
the Zoological Society of London, 1868, 363-368.
Benstead, J.P., March, J.G., Pringle, C.M. & Scatena, F.N. (1999) Effects of a low-head dam
and water abstraction on migratory tropical stream biota. Ecological Applications, 9, 656668.
Benstead, J.P., Cross, W.F., March, J.G., McDowell, W.H., Ramírez, A. & Covich, A.P. (2010)
Biotic and abiotic controls on the ecosystem significance of consumer excretion in two
contrasting tropical streams. Freshwater Biology, 55, 2047-2061.
Benstead, J.P., March, J.G. & Pringle, C.M. (2000) Estuarine larval development and upstream
post- larval migration of freshwater shrimp in two tropical rivers of Puerto Rico.
Biotropica, 32, 545-548.
Bouvier, E.L. (1913) Les variations d’ une crevette de la famille des Atyidées, l’ Atyaephyra
desmaresti.Bulletin du Muséum national d'histoire naturelle, Paris, 19, 65-74.
Canals, M. (1977) Nuevo record para Puerto Rico de dos especies de decápodos: Macrobrachium
crenulatum (Holthuis, 1950) Palaemonidae y Panaeus schmitti (Burkenroad, 1936)
Penaeidae. Science-Ciencia, 5, 6-8.
20
Canals, M. (1979) Some ecological aspects of the biology of Macrobrachium crenulatum
(Holthuis,1950) Palaemonidae, Decapoda in Puerto Rico including notes on its
taxonomy. Science-Ciencia, 6, 130-132.
Carvacho, A. (1982) Sur une petite collection de crevettes de la Martinique. Caribbean Journal of
Science, 17, 15-20.
Chace, F.A., Jr. (1954) Two new subterranean shrimp (Decapoda: Caridea) from Florida and the
West Indies, with a revised key to the American species. Journal of the Washington
Academy of Sciences, 44, 318-324.
Chace, F.A., Jr. & Hobbs, H. H. Jr. (1969) The freshwater and terrestrial decapod crustaceans of
the West Indies with special reference to Dominica. United States national Museum
Bulletin, 292, 1-258.
Chace, F.A., Jr. (1972) The Shrimp of the Smithsonian-Bredin Caribbean Expeditions with a
Summary of the West Indian Shallow-water Species (Crustacea:Decapoda: Natantia).
Smithsonian Contributions to Zoology, 98, 179 pp.
Chace, F.A. (1975) Cave shrimp (Decapoda: Caridea) from the Dominican Republic.
Proceedings of the Biological Society of Washington, 88, 29-44.
Ching, C. A. & Vélez, M. J.Jr. (1985) Mating, incubation and embryo number in the freshwater
prawn Macrobrachium heterochirus (Wiegmann, 1836) (Decapoda, Palaemonidae) under
laboratory conditions. Crustaceana, 49, 42-48.
Cook, B.D., Pringle, C.M. & Hughes, J. M. (2008a) Phylogeography of an island endemic, the
Puerto Rican freshwater crab (Epilobocera sinuatifrons). Journal of Heredity, 257-268.
Cook, B. D., Pringle, C.M. & Hughes, J. M. (2008b) Molecular evidence for sequential
colonization and taxon cycling in freshwater decapod shrimp on a Caribbean island.
Molecular Ecology, 17, 1066-1075.
21
Covich, A. P., Crowl, T.A., Johnson, S.L., Varza, D. & Certain, D. L. (1991) Post-Hurricane
Hugo increases in atyid shrimp abundances in a Puerto Rican montane stream. Biotropica
23, 448-454.
Covich, A. P., Crowl, T.A., Johnson, S.L. & Pyron, V. (1996) Distribution and abundance of
tropical freshwater shrimp along a stream corridor: response to disturbance. Biotropica,
28, 484-492.
Covich, A. P. & McDowell, W. H.(1996). The stream community. In: Waide, R.B. & Reagan, W.
B. (Eds.), The food web of a tropical rainforest. University of Chicago Press, Chicago,
pp. 434-459.
Covich, A.P., Crowl, T.A. & Scatena, F.N. (2003). Effects of extreme low flows on freshwater
shrimp in a perennial tropical stream. Freshwater Biology, 48, 1199-1206.
Covich, A. P., Crowl, T.A. & Heartsill-Scalley, T. (2006). Effects of drought and hurricane
disturbances on headwater distributions of palaemonid river shrimp (Macrobrachium
spp.) in the Luquillo Mountains, Puerto Rico. Journal of the North American
Benthological Society, 25, 99-107.
Covich A.P., Crowl, T.A., Hein, C.L., Townsend, M.J. & McDowell, W.H. (2009) Predator-prey
interactions in river networks: comparing shrimp spatial refugia in two drainage basins.
Freshwater Biology, 54, 450-465.
Creaser, E. P. (1936) Crustaceans from Yucatan. Carnegie Institute of Washington Publications,
457, 111-132.
Cross, W. F., Covich, A.P., Crowl, T.A, Benstead, J.P. & Ramírez, A. (2008). Secondary
production, longevity and resource consumption rates of freshwater shrimp in two
tropical streams with contrasting geomorphology and food web structure. Freshwater
Biology, 53, 2504-2519.
22
Crowl, T. A. & Covich, A. P. (1994) Responses of a freshwater shrimp to chemical and tactile
stimuli from a large decapod predator. Journal of the North American Benthological
Society, 13, 291-298.
Crowl, T.A., McDowell, W.H., Covich, A.P. & Johnson, S. L. (2001) Freshwater shrimp effects
on detrital processing and nutrients in a tropical headwater stream. Ecology, 82, 775-783.
Crowl, T. A., Welsh, V., Heartsill-Scalley, T. & Covich, A. P. (2006) Effects of different types of
conditioning on rates of leaf-litter shredding by Xiphocaris elongata, a Neotropical
freshwater shrimp. Journal of the North American Benthological Society, 25, 198-208.
Debrot, A. O. (2003) The freshwater shrimp of Curacao, West Indies (Decapoda, Caridea).
Crustaceana, 76, 65-76.
De Saussure, H. (1857) Diagnoses de quelques Crustaces nouxeaux de 1' Amerique tropicale.
Revue el Magasin de Zoologie Pure et Applique'e, 2(9), 501-505.
Davies, N. & Spencer-Smith, S. (1998) Munroe revisited: a survey of West Indian butterfly
faunas and their species‐area relationship. Global Ecology and Biogeography Letters,
7(4), 285-294.
Davies, N. & Bermingham, V. (2002) The historical biogeography of two Caribbean butterflies
(Lepidoptera: Heliconiidae) as inferred from genetic variation at multiple loci. Evolution,
56(3), 573-589.
Ewel, J. J. & Whitmore, J. L. (1973) The ecological life zones of Puerto Rico and the Virgin
Islands. Institute of Tropical Forestry, San Juan, Puerto Rico. Forest Service Research
Paper ITF, 18, 1-72.
Felix, C.M.L. (1991) Freshwater shrimp of Barbados: some aspects of their biology, ecology
and culture. PhD. Thesis University of the West Indies, Barbados, West Indies.
23
Fièvet, É., Bonnet-Arnaud, P. & Mallet, V. (1999) Efficiency and sampling bias of electrofishing
for freshwater shrimp and fish in two Caribbean streams, Guadeloupe Island. Fisheries
Research, 44, 149-166.
Fraiola, K.M.S. (2004) Juvenile Epilobocera sinuatifrons growth rates and ontogenetic shifts in
feeding in wild populations. M.S. Thesis University of Georgia, Athens, Georgia, United
States of America.
Fryer, G. (1977) Studies on the Functional Morphology and Ecology of the Atyid Prawns of
Dominica. Philosophical Transactions of the Royal Society of London. Series B,
Biological Sciences, 277, 57-129.
Greathouse, E. A., March, J.G. & Pringle, C. M. (2005) Recovery of a tropical stream after a
harvest- related chlorine poisoning event. Freshwater Biology, 50, 603-615.
Greathouse E.A., Pringle,C.M., McDowell, W.H. & Holmquist, J.G. (2006) Indirect upstream
effects of dams: consequences of migratory consumer extirpation in Puerto Rico.
Ecological Applications, 16, 339-352.
Guérin-Méneville, F.E. (1855-1856. 1856 1857) Crustaces. In: de la Sagra, R.(Eds.) Histoire
physique,politique et naturelle de Vile de Cuba,7:vii Ixviii; 8 atlas: 3 plates. Paris:
Arthus Bertrand.
Guérin-Méneville, F.E. (1856- 1857b) Crustaceos. In: de la Sagra,R. (Eds.) Historm física
politico y natural de la isla de Cuba,7 :vii xxiii; 8[atlas]: 3 plates. Paris: Arthus
Bertrand.
Gundlach, J. (1887-1894) Fauna puertorriqueña. Anales de la Sociedad Española de Historia
Natural, 16-22, 347-658.
Hart, C.W., Jr. (1961a) Jonga, a New Genus of Freshwater Atyid Shrimp (Decapoda, Atyidae).
Notulae Naturae, Academy of Natural Sciences of Philadelphia, 342, 1-3.
24
Hart, C.W. (1961b) The freshwater shrimp (Atyidae and Palaemonidae) of Jamaica, W.I., with a
brief discussion of their relation to the ancient geography of the western Caribbean area,
Proceedings of the Academy Natural Sciences Philadelphia, 113, 61-80.
Hein, C. L., Pike, A.S., Blanco, J.F., Covich, A.P., Scatena, F.N., Hawkins, C.P. & Crowl, T. A.
(2011) Effects of coupled natural and anthropogenic factors on the community structure
of diadromous fish and shrimp species in tropical island streams. Freshwater Biology, 56,
1002-1015.
Helmer, E. H., Ramos, O., del M López, T., Quiñónez, M., & Diaz, W. (2002). Mapping the
forest type and land cover of Puerto Rico, a component of the Caribbean biodiversity
hotspot. Caribbean Journal of Science, 38, 165-183.
Herbst, J.F.W. (1791-1796). Versuch einer Naturgeschichte der Krabben und Krebse nebst einer
systemalischen Beschreibung ihrer verschiedenen Arten, 2, 266 Berlin: Gottlieb August
Lange.
Hobbs, H. H. & Hart, C. W. (1982) The shrimp genus Atya (Decapoda: Atyidae). Smithsonian
Contribution to Zoology, 364, 1-143.
Holthuis, L.B. (1950) Preliminary Descriptions of Twelve New Species of Palaemonid Prawns
from American Waters (Crustacea: Decapoda). Proceedings of the Koninklijke
Nederlandse Akademie van Wetenschappen, 53, 93-99.
Holthuis, L. B. (1954) On a collection of decapod Crustacea from the Republic of El Salvador
(Central America). Zoologische Verhandelingen, 23, 1-43.
Holthuis, L.B. (1977) On some freshwater and terrestrial Crustacea Decapoda from Cuba. In:
Résultats des expéditions biospéologiques Cubano-Roumaines à Cuba, 271-275.
Holthuis, L. B. (1980). FAO species catalogue. Shrimp and prawns of the world. An annotated
catalogue of species of interest to fisheries. FAO Fisheries Synopsis 125(1) pp 261.
25
Holmquist, J. G., Schmidt-Gengenbach, J.M. & Yoshioka, B. B. (1998) High Dams and Marinefreshwater Linkages: Effects on Native and Introduced Fauna in the Caribbean.
Conservation Biology, 12, 621-630.
Hynes, H. B. N. (1971) Zonation of the invertebrate fauna in a West Indian stream.
Hydrobiologia, 38, 1- 8.
Isaac, C. & Bourque, C.P.A. (2001) Ecological life zones of Saint Lucia. Global Ecology and
Biogeography, 10(5), 549-566.
Johnson .SL., Covich, A.P., Crowl, T.A., Estrada, A., Bithorn, J. & Wurtsbaugh, W.A. (1998) Do
seasonality and disturbance influence reproduction in freshwater atyid shrimp in
headwater streams, Puerto Rico?. Proceedings of the International Association of
Theoretical and Applied Limnology, 26, 2076-2081.
Johnson, S. L. & Covich, A. P. (2000) The importance of night-time observations for determining
habitat preferences of stream biota. Regulated Rivers: Research and Management, 16,
91-99.
Karge, A., Page, T.J. & Klotz, W. (2013) A new species of freshwater shrimp of the genus
Micratya (Decapoda: Tyidae: Caridea) from Puerto Rico. Zootaxa, 3608(5), 357-368.
Kikkert, D. A., Crowl, T.A. & Covich, A. P. (2009) Upstream migration of amphidromous
shrimp in the Luquillo Experimental Forest, Puerto Rico: temporal patterns and
environmental cues. Journal of the North American Benthological Society, 28, 233-246.
Kingsley, J.S. (1878) Notes on the North American Caridea in the Museum of the Peabody
Academy of Science at Salem, Massachusetts. Proceedings of the Academy of Natural
Sciences of Philadelphia, 30, 89-98.
Kwak, T.J., Cooney, P.B. & Brown, C.H. (2007) Fishery population and habitat assessment in
Puerto Rico streams: phase 1 final report. San Juan, Federal Aid in Sport Fish
26
Restoration, Final Report, Submitted to the Department of Natural and Environmental
Resources.
Leach, W.E. (1815) A tabular view of the external characters of four classes of animals,
which linn arranged under insecta: with the distribution of the genera composing three of
these classes into orders, and descriptions of several new genera and species.
Transactions of the Linnaean Society of London, 11, 306-400.
Leach, W.E. (1816, 1816, 1824). Atya. In Encyclopaedia Britannica, supplement to the fourth,
fifth, and sixth editions, 1(1):421, plate 21. Edinburgh: Archibald Constable and
Company.
Linnaeus, C. (1758) Systema naturae per regna tria naturae, secundum classes, ordines, genera,
species, cum characleribus, differentiis, synonymis, locis. Edition 10, 1: iii + 824 pages.
Holmiae [Stockholm].
Losos, J. B. & Losos, J.B. (1996) Ecological and evolutionary determinants of the species-area
relation in Caribbean anoline lizards. Philosophical Transactions of the Royal Society of
London. Series B: Biological Sciences, 351(1341), 847-854.
Losos, J. B. & Schluter, D. (2000) Analysis of an evolutionary species–area relationship. Nature,
408(6814), 847-850.
March, J. G., Benstead, J.P., Pringle, C.M. & Scatena, F. N. (1998) Migratory drift of larval
freshwater shrimp in two tropical streams, Puerto Rico. Freshwater Biology, 40, 261-273.
March, J.G., Benstead, J.P., Pringle, C.M. & Ruebel, M.W. (2001) Linking shrimp assemblages
with rates of detrital processing along an elevational gradient in a tropical stream.
Canadian Journal of Fisheries and Aquatic Sciences, 58, 470-478.
March, J. G., Pringle, C.M., Townsend, M.J. & Wilson, A. I. (2002) Effects of freshwater shrimp
assemblages on benthic communities along an altitudinal gradient of a tropical island
stream. Freshwater Biology, 47, 377-390.
27
March, J. G. & Pringle, C. M. (2003) Food Web Structure and Basal Resource Utilization along a
Tropical Island Stream Continuum, Puerto Rico. Biotropica, 35, 84-93.
March, J. G., Benstead, J.P., Pringle, C.M. & Scatena, F. N. (2003) Damming Tropical Island
Streams: Problems, Solutions, and Alternatives. BioScience, 53, 1069-1078.
Martínez-Iglesias, J.C. (2006) Lista de especies crustáceos decápodos registrados para Cuba.
McDowell, W.H., Scatena, F.N., Waide, R.B., Brokaw, N., Camilo, G.R., Covich, A.P., Crowl,
T.A.,González, G., Greathouse, E.A., Klawinski, P., Lodge, D.J., Lugo, A.E., Pringle,
C.M., Richardson, B.A., Richardson, M.J., Schaefer, D.A., Silver, W.L., Thompson, J.,
Vogt, D.J., Vogt, K.A., Willig, M.R., Woolbright, L.L., Zou, X., & Zimmerman,
J.K.(2012) Geographic and ecological setting of the Luquillo Mountains. In: Brokaw,N.,
Crowl,T.A., Lugo, A.E., McDowell, W.H., Scatena, F.N., Waide, R.B. & Willig, M.R.
(Eds.), A Caribbean forest tapestry: the multidimensional nature of disturbance and
response. New York: Oxford University Press.
McLaughlin, P. A., Camp, D. K., Angel, M. V., Bousfield, E. L., Brunel, P., Brusca, R. C., &
Cadien, D.(2005). Common and scientific names of aquatic invertebrates from the United
States and Canada: crustaceans. American Fisheries Society, 120 pp.
Milne Edwards, A. (1866) Description de trois nouvelles especes du genre Boscia, Crustaces
Brachyures de la tribu des Telpheusiens. Annales de la Societe Entomologique de France,
(4)6, 203- 205.
Montero, J.C. (1987). Reproductive biology, general ecology and the altitudinal distribution of
the atyid shrimp Crustacea, Decapoda, Atyidae on the Tanamá and Río Grande de
Arecibo rivers on the north coast of Puerto Rico. Ms. Thesis, University of Puerto Rico,
San Juan, Puerto Rico, 84pp.
Nemeth, D. & Platenberg, R. (2007) Diversity of freshwater fish and crustaceans of St. Thomas
28
watersheds and its relationship to water quality as affected by residential and commercial
development. Water Resources Research Institute Project 2006VI73B, University of the
Virgin Islands, St. Thomas.
Ortmann, A. E. (1894) A Study of the Systematic and Geographical Distribution of the Decapod
Family Atyidae Kingsley. Proceedings of the Academy of Natural Sciences of
Philadelphia, 46, 397-416.
Pérez-Gelabert, D.E. (2008) Arthropods of Hispaniola (Dominican Republic and Haiti): A
checklist and bibliography. Zootaxa, 1831, 1-530.
Pérez-Reyes, O. (1999) Abundance, diversity and life histories of freshwater decapods in Puerto
Rico. MS Dissertation, University of Puerto Rico, Río Piedras Campus, San Juan, Puerto
Rico.
Pringle, C. M., Blake, G.A., Covich, A.P., Buzby, K.M. & Finley, A. (1993) Effects of
omnivorous shrimp in a montane tropical stream: sediment removal, disturbance of
sessile invertebrates and enhancement of understory algal biomass. Oecologia, 93, 1-11.
Pringle, C. M. (1996) Atyid shrimp (Decapoda: Atyidae) influence the spatial heterogeneity of
algal communities over different scales in tropical montane streams, Puerto Rico.
Freshwater Biology, 35, 125-140.
Pyron, M., Covich, A.P. & Black, R. W. (1999) On the relative importance of pool morphology
and woody debris to distributions of shrimp in a Puerto Rican headwater stream.
Hydrobiologia, 405, 207-215.
Ricklefs, R. E. (2000) The relationship between local and regional species richness in birds of the
Caribbean Basin. Journal of Animal Ecology, 69(6), 1111-1116.
Ricklefs, R. E. & Lovette, I.J. (2001) The roles of island area per se and habitat diversity in the
species–area relationships of four Lesser Antillean faunal groups. Journal of Animal
Ecology, 68(6), 1142-1160.
29
Rivera, M. (1996) The biology of the Puerto Rican freshwater crab Epilobocera sinuatifrons
(Crustacea,Decapoda, Pseudothelphusidae). MA Thesis, University of Colorado,
Colorado, United States of America.
Rodríguez, G. & Williams, A.B. (1995) Epilobocera wetherbeei, a new species of freshwater crab
(Decapoda: Brachyura: Pseudothelphusidae) from Hispaniola. Proceedings of the
Biological Society of Washington, Lawrence, 108 (1), 76-83.
Rodríguez, G. & López, B. (2003) Insular species of Neotropical freshwater crabs (Crustacea:
Brachyura). Journal of Natural History, London, 37 (21), 2599-2614.
Rodríguez, G. & Magalhes, C. L. (2005) Recent advances in the biology of the Neotropical
freshwater crab family Pseudothelphusidae (Crustacea, Decapoda, Brachyura). Revista
Brasileira de Zoologia, 22, 354-365.
Santiago, A. T. (1979) Estudio biogeográfico de los camarones en los ríos Yauco y Grande de
Arecibo y algunos estudios poblacionales sobre estos animales. Ms. Thesis, University of
Puerto Rico, San Juan, Puerto Rico.
Schmitt, W. L. (1935) Crustacea macrura and anomura of Porto Rico and the Virgin Islands.
Scientific Survey of Porto Rico and the Virgin Islands, New York Academy of Sciences,
15, 125-227.
Schubart, C.D. & Koller, P. (2005) Genetic diversity of freshwater crabs (Brachyura:Sesarmidae)
from central Jamaica with description of a new species. Journal of Natural History, 49,
469-481.
Stimpson, W. (1871) Notes on North American Crustacea, in the Museum of the Smithsonian
Institution.No 3. Annals of the New York Lyceum, 10, 92-136.
Thorpe, T. & Lloyd, B. (1999) The macroinvertebrate fauna of St. Lucia elucidated by canonical
correspondence analysis. Hydrobiologia, 400, 195-203.
Vélez, M. J. Jr. (1967) Checklist of the terrestrial and freshwater Decapoda of Puerto Rico.
30
Caribbean Journal of Science, 7, 41-44.
Villamil, J. & Clements R.G. (1976) Some aspects of the ecology of freshwater shrimp in the
upper Espíritu Santo river at El Verde, Puerto Rico. Puerto Rico Nuclear Center,
University of Puerto Rico, San Juan Puerto Rico (United States Energy Research and
Development Administration) Publication, 206, 1-62.
Weber, F. (1795) Nomenclator entomologicus secundum Entomologiam systematicam ill.
Fabricii adjectis speciebus recens detectis et varietatibus: i-viii, 1-171. Chilonii et
Hamburgi.
Wiegmann, A.F.A. (1836) Beschreibung einiger neuen cruslaceen des Berliner Museums aus
Mexiko und Brasilien. Archiv fur Naturgeschichte, 2(1), 145-151.
Wright, M. S. & Covich, A. P. (2005) Relative importance of bacteria and fungi in a tropical
headwater stream: leaf decomposition and invertebrate feeding preference. Microbial
Ecology, 49, 536-546.
Zimmerman, J. K. H. & Covich, A. P. (2003) Distribution of juvenile crabs (Epilobocera
sinuatifrons) in two Puerto Rican headwater streams: Effects of pool morphology and
past land-use legacies. Archiv fur Hydrobiologie, 158, 343-357.
31
Table 2-1 Distribution of the 18 freshwater decapod species sampled at the 43 freshwater bodies (rivers, streams, rivulets, and caves) in Puerto
Rico.
Species list
Macrobrachium
faustinum
Macrobrachium
heterochirus
Xiphocaris elongata
Epilobocera
sinuatifrons
X
X
X
X
X
X
11
2- Herrera
X
X
X
X
X
X
X
X
X
X
X
11
3- Espíritu
Santo
X
X
X
X
X
X
X
X
X
X
X
11
4- Mameyes
X
X
X
X
X
X
X
X
X
X
X
11
5- Sabana
X
X
X
X
X
X
X
X
X
X
X
14
X
X
X
X
X
X
X
8
X
X
X
X
8
6- Juan
Martín
X
7- Fajardo
X
X
X
X
X
X
X
Palaemon
pandaliformis
Macrobrachium
crenulatum
X
Macrobrachium
acanthurus
X
Typhlatya monae
X
Rivers
Potimirim glabra
X
Micratya cooki
X
Micratya poeyi
1- Loíza
Jonga serrei
Total
Species
/Location
Species
Macrobrachium
carcinus
Pseudothelphusidae
Atya scabra
Xiphocarididae
Atya innocuous
Potimirim mexicana
Palaemonidae
Potimirim americana
Atyidae
Atya lanipes
Family
8- Daguao
9- Santiago
0
X
X
10- Blanco
X
X
X
X
X
X
X
X
X
X
X
X
10
X
X
X
X
8
11- Antón
Ruiz
0
12- Humacao
13Guayanes
14- Maunabo
15- Jaraboa
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
8
X
X
13
X
5
0
31
32
16- Patillas
X
17- Salinas
X
X
X
X
X
X
X
2
X
X
X
18- Jueyes
9
0
19- Coamo
X
X
X
X
20Descalabrado
X
X
X
X
X
X
X
X
X
X
X
21- Jacaguas
X
X
X
11
X
X
9
X
22- Inabón
1
X
1
23- Bucaná
X
X
X
X
X
X
X
X
X
X
X
X
12
24Portugues
X
X
X
X
X
X
X
X
X
X
X
X
12
25- Matilde
X
X
X
X
X
X
X
X
9
26- Tallaboa
X
X
X
X
X
27Guayanilla
X
X
X
X
X
X
X
6
X
X
7
28- Yauco
X
X
X
X
X
X
X
X
X
X
X
X
X
13
29- Loco
X
X
X
X
X
X
X
X
X
X
X
X
X
13
30Guanajibo
X
X
X
X
X
X
X
X
X
X
X
13
X
X
6
31- Yagüez
32- Añasco
33Culebrinas
34Guajataca
X
X
X
X
X
X
X
X
X
X
X
10
X
X
X
X
X
X
11
X
X
4
X
X
X
X
X
X
X
X
X
X
X
35- Camuy
X
X
X
36- Arecibo
X
X
X
37- Manatí
X
X
X
X
38- Cibuco
X
X
X
X
39- La Plata
X
X
X
X
X
X
X
X
X
X
X
X
X
X
12
X
X
X
X
X
X
X
X
X
13
X
X
X
X
9
X
X
X
X
X
9
X
X
X
X
7
X
32
33
40- Bayamón
41- Río
Piedras
42- Mona
Island- Cave
43- Guanica
Dry ForestCave
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
15
X
X
6
X
1
X
1
33
34
Table 2-2 Antillean islands, area, and number of families, genera and species of freshwater
decapods included in the study. Primary data sources for the decapod species presence in the
studied Caribbean islands.
Island
Area (km2) Families Genera Species Literature
Chace and Hobbs 1969
Holthuis 1977
Cuba
105806
5
13
48
Martínez-Iglesias 2006
Rodríguez and Megalhaes 2005
Chace 1975
Hispaniola
73929
5
9
20
Rodríguez and Williams 1995
Pérez-Gelabert 2008
Bahamas
13878
1
1
2
Jamaica
10991
4
7
21
Alvarez et al. 2005
Hart 1961b
Schubart and Koller 2005
Vélez 1967
Chace and Hobbs 1969
Puerto Rico
9100
4
9
18
Holmquist et al. 1998
Pérez-Reyes 1999
Karge et al. 2013
Trinidad
4709
3
4
12
Rodríguez and López 2003
Guadeloupe
1628
3
5
11
Fièvet et al. 1999
Martinique
1128
2
6
8
Carvacho 1982
Rodríguez and López 2003
Margarita
1020
1
2
2
750
3
6
12
Rodríguez 1967
Fryer 1977
Dominica
Rodríguez and López 2003
35
Bass 2004 a
Bass 2007
Barnish 1984
St. Lucia
622
4
8
13
Thorpe and Lloyd 1999
Rodríguez and López 2003
Curacao
444
3
5
9
Debrot 2003
440
2
2
2
Bass 2005
Antigua and
Barbuda
Hobbs and Hart 1982
Barbados
431
5
6
9
Felix 1991
Bass 2003a
Hobbs and Hart 1982
Grenada
346
3
6
10
Bass 2004 b
Hobbs and Hart 1982
U.S. Virgin Islands
346
3
3
8
Nemeth and Platenberg 2007
Rodríguez and López 2003
St. Vincent
340
2
2
6
Hobbs and Hart 1982
Hynes 1971
Tobago
300
5
8
13
Bass 2003 b
Saint Kitts and
Chace and Hobbs 1969
271
3
5
6
Nevis
Bass 2006
British Virgin
153
2
2
2
Chace and Hobbs 1969
102
1
1
3
Hobbs and Hart 1982
Islands
Montserrat
36
Bermuda
53
3
3
3
Chace and Hobbs 1969
37
Fig. 2-1 Geographic distribution of shrimp species from the family Atyidae sampled and reported for the major rivers of Puerto
Rico and their tributaries. The number in the triangle represents the number of atyid species collected in the river. Typhlatya
monae was recorded in caves from the Mona Island Reserve and in the xerophytic forest of Guánica. Numbers outside the map
represent the number of rivers in the island.
37
38
Fig. 2-2 Geographic distribution of shrimp species from the family Palaemonidae sampled and reported for the major rivers of
Puerto Rico and their tributaries. The number in the diamond represents the number of palaemonid species collected in the
river. Numbers outside the map represent the number of rivers in the island.
38
39
Fig. 2-3 Geographic distributions of Epilobocera sinuatiforns and Xiphocaris elongata in the major rivers of Puerto Rico. Open
triangles represent Epilobocera sinuatifrons, closed triangles represent Xiphocaris elongata and open-close triangles the
occurrence of both species. Numbers outside the map represent the number of rivers in the island.
39
40
4
Cuba
3.5
Jamaica
3
Hispaniola
LN Freshwater Decapod Species
Puerto Rico
St.Lucia
Tobago
Dominica
Trinidad
Guadeloupe
Grenada
Curacao
Barbados
U.S. Virgin Islands
Martinique
2.5
2
St.Kitts and Nevis
St.Vincent
1.5
Bermuda
Montserrat
Bahamas
1
Antigua
and Margarita
Barbuda
British Virgin Islands
0.5
y = 0.264x + 0.199
R² = 0.3908
0
0
2
4
6
8
10
12
LN Island Area (km2)
Fig. 2-4 Species-area relationships of freshwater decapods in the Antilles. Species richness of
decapods as a function of island area shows a species–area (LN–LN) relationship with a slope of
0.264±0.05 (R2=0.3908). Solid line represents the regression line for all islands in the Caribbean.
Closed diamonds represent Lesser Antilles and open diamonds Greater Antilles.
41
CHAPTER 3
COMPARISON OF DECAPOD COMMUNITIES ACROSS AN URBAN-FOREST LAND USE
GRADIENT IN PUERTO RICAN STREAMS 2
Abstract
Urbanization influences a range of factors related to stream health, including the
hydrologic regime, water quality, and riparian conditions that lead to negative effects on
terrestrial and aquatic ecosystems. However, impacts on freshwater decapods from urbanization
of tropical streams have not been reported. We hypothesized that changes in decapod
communities in watersheds with different levels of urbanization are related to changes in physical
stream habitats caused by different land uses and their effects on water discharge. The impacts of
land use on the physico-chemical characteristics of streams and freshwater decapod communities
were evaluated in three watersheds characterized by low, moderate and high-intensities of
urbanization in Puerto Rico. For the low and moderately developed urban watersheds, decapod
species richness ranged from 10-11 species; the highly urbanized watershed only had 4 species.
Macrobrachium faustinum and Xiphocaris elongata were the most ubiquitously species and were
found in all watersheds. Multivariable analysis of physical characteristics and densities of the
decapod families resulted in one axis that explained 80 % of the total variation among the
watersheds and was correlated with stream discharge. The effect of discharge is likely a result of
frequent high flows that sustain habitats with high concentrations of dissolved oxygen and low
concentrations of pollutants. An increase in physico-chemical parameters were observed from
the LUW to the HUW. These results indicate that the decapod communities were most likely
influenced by land use and environmental conditions that affected erosional aspects related to
water discharge and water quality in the highly impacted watersheds.
2
Coauthored by Omar Pérez-Reyes, Todd A. Crowl, and Alan P. Covich
42
Keywords Atya, Epilobocera, Macrobrachium, species diversity, urban streams, Xiphocaris
Introduction
Urbanization can disproportionately affect flow regime (Walsh et al. 2012; Braud et al.
2013), water quality (Mallin et al. 2009; Line 2013; Wang et al. 2013), energy sources (Zeni and
Cassati 2014), habitat (Engman and Ramírez 2012; Fogaca et al. 2013), and biotic interactions
(Wenger et al. 2010; Kaushal and Belt 2012; McDonald et al. 2013). Collectively, changes in
these aspects alter the stream health and modify ecosystem goods and services provided by biotic
communities. Over time, freshwater ecosystems in urban watersheds generally become
dominated by the most resilient species. These patterns are described as the “Urban Stream
Syndrome” (Meyer et al. 2005; Walsh et al. 2005).
Tropical streams are rarely studied across urbanization gradients (Victor and Ogbeibu
1991; Buckup et al. 2007; Nemeth and Platenberg 2007; Zhang et al. 2010; Valle et al. 2013).
Most previous studies in tropical streams have focused on terrestrial-aquatic interactions and the
roles of diverse freshwater species in forested areas (Pringle et al. 1993; Covich et al. 1996;
March and Pringle 2003; Crowl et al. 2001; Greathouse et al. 2006a, 2006b; Covich et al. 2009).
In general, abundance and species diversity decrease in streams with loss of riparian
forest cover. Aquatic insects are most frequently used in stream biomonitoring studies to assess
land-use impacts because of their sensitivity to changes. A strong relationship between watershed
land cover and stream insect biota is well established (Chinnayakanahalli et al. 2011; Chadwick
et al. 2012; Vander Laan et al. 2013). Although previous studies of Caribbean urban streams
have evaluated species responses of aquatic insects to environmental changes (e.g., de Jesús and
Ramírez 2011; Ramírez et al. 2012), none have focused on freshwater decapod community
structure or their roles in urban stream ecosystems.
43
Tropical island streams, in contrast to continental streams, are often dominated by
diadromous decapod species rather than by aquatic insects (Covich and McDowell 1996; Crowl
et al. 2012). Caridean shrimp (Atyidae, Palaemonidae, and Xiphocarididae) and crabs (Grapsidae,
Pseudothelphusidae) are potentially vulnerable to the physical and ecological effects of
urbanization. A decrease in decapod diversity can result from: habitat loss (sedimentation and
loss of woody debris); pollution and chemical contamination (nutrient inputs from agriculture in
riparian zones, toxins and reduction in dissolved oxygen concentration); replacement of native
species by exotics; and a decrease in allochthonous food resources that shift the trophic structure
from allocthonous to autochthonous food resources and consumers. These decapod species (Atya,
Macrobrachium, Xiphocaris and Epilobocera) influence primary production, leaf-litter
breakdown, and the benthic community structure (Pringle et al. 1993; Covich et al. 1999; Crowl
et al. 2001; Synder et al. 2011, Crowl et al. 2012). Moreover, these consumers are important food
sources for predators including large species of freshwater shrimp and crabs, fish, aquatic birds,
snakes and turtles (Hein et al. 2010).
The diadromous shrimp in this study have larval stages that complete their development
in estuarine or marine environments. Consequently, these species are vulnerable at different
stages of their complex amphidromous life cycle to a range of stressors such as low dissolved
oxygen or toxins as well as fish, decapod and bird predators. Individuals grow, mate, and spawn
in the river but the planktonic larvae develop in brackish estuaries or marine waters. After
completion of larval metamorphoses, the post-larvae migrate upstream to the headwaters and
migrate back to the headwaters to complete their life cycle (Benstead et al. 2000; Kikkert et al.
2009; Bauer 2011a, 2011b, 2013).
We hypothesized that species loss in watersheds with different degrees of urbanization
would result because different taxa could be affected by changes in their habitat as consequence
of the land use. We compared the freshwater decapod community composition among
44
watersheds with different urban land cover levels (low, moderate, and high) and between
different periods of rainfall [Low Rainfall- (LRF) and High Rainfall- (HRF)]. We expected to
find lower abundance and diversity of decapods in watersheds with a higher percentage of urban
land cover than in watersheds with moderate and low urban impact because of lower water
quality and high peak flows characteristic of most urban ecosystems. We also hypothesized that
the effects of the low rainfall would further reduce the abundance and diversity of decapods in
watersheds with moderate and high percentage of urban land use by exacerbating the physical and
chemical effects of urbanization such warmer water and lower dissolved oxygen.
Material and Methods
Site selection and classification
Three watersheds that represent different gradients of human impact in Puerto Rico were
selected to test our hypotheses. The Sabana, Bayamón and Río Piedras watersheds represent low,
moderate and high levels of urbanization based on the percentage of urban cover, respectively
(Fig. 3-1). The streams were classified by the percentage of urban land use in their watersheds
based on the results obtained by the Puerto Rico Gap Project (Gould et al. 2008) (Fig. 3-2). The
drainage areas for these watersheds were 10.3 km2 in the low urban watershed, 108.3 km2 for the
moderate and 39.7 km2 for the highly urban. In each watershed, three sampling sites were
selected from the river mouth to the headwaters to maximize the diversity of habitat types (i.e.
pools, runs, and riffles) in different land use settings. At each site, three, 10m sampling reaches
were randomly selected to sample decapod communities and measure the physico-chemical data
(9 sampling location across watersheds). All the sampling reaches were located downstream the
reservoirs in the Bayamón and Río Piedras streams. The two small dams in the coastal valleys of
Río Piedras and Río Bayamón do not represented a barrier or have any direct impacts on
45
freshwater species because they are inundated during floods and post-larval shrimp can migrate
around and over these low dams (Fig. 3-1).
The Río Sabana watershed (with low level urbanization- LUW) is located in the
northeastern portion of the Luquillo Experimental Forest (LEF), where there is little seasonal
variation in rainfall. The river’s headwaters are located in the eastern portion of El Yunque
National Forest (also known as the Luquillo Experimental Forest) and this watershed (28,000 ha)
is managed by the U.S. Forest Service to sustain the riparian forest cover. The Puerto Rico
Environmental and Natural Resources Department manages the suburban and urban reaches of
this watershed (approximately 1,083 ha). Humans have impacted the meanders and valleys in the
middle and lower watershed for hundreds of years (Thomlinson and Rivera 2000). The
headwater portion of the Rio Sabana watershed is dominated by patches of secondary forest with
some sections considered primary forests (51 %) (Fig.3-2). The middle elevations have moderate
densities of native and introduced trees in contrast with the lower sections where the valleys have
high densities of non-native grasses and fruit trees. Non-native species are scarce in the forested
sites but increase downstream to the urban reaches. Urban reaches (6.2 %) are characterized by
riparian zones primarily composed of grasses where the most common species are Panicum
aquaticum and Bambusa vulgaris rather than forested riparian buffers.
The Río Bayamón watershed (with moderate level of urbanization- MUW) is one of the
largest in Puerto Rico. The river’s headwaters are located in the Cordillera Central at an
elevation of 500 m above sea level and flow through Subtropical Moist and Subtropical Wet
Forests (Ewel and Whitmore 1973; Helmer et al. 2002). The land cover for the Bayamón
watershed consists of 41 % secondary forests, 26 % grassland, 7 % suburban and 24 % urban
development (Gould et al. 2008) (Fig. 3-2). The vegetation communities in the forested sections
of the watershed are dominated by exotic trees species and the urban sections by grasses. The
46
meanders in the lower and coastal valleys have been heavily modified due to construction of
earthen channels with raised levees for flood control.
The Río Piedras watershed (with high level urbanization- HUW) has several tributaries
and flows through the center of the metropolitan area of San Juan. This watershed has more than
60 % of urban cover, 5 % suburban development, and 18.5% of secondary forest (Fig. 3-2)
(Ortíz-Zayas et al. 2006; Gould et al. 2008; de Jesus and Ramírez 2011). The headwaters are
located 70 m above sea level and regulated by outflow from the Las Curias Reservoir. The Río
Piedras flows from Las Curias Reservoir (200 m above sea level) through several residential
areas, the Botanical Garden of The University of Puerto Rico, and into San Juan Bay. Within the
city of Río Piedras, some reaches and tributaries have been modified by channelization or
reinforced with rock embankments. The riparian vegetation is characterized by exotic species of
trees and grasses.
Data Collection
Stream Habitat Data
Each stream was visited in random order and sampled twice each year for 2 years (20102011), during the Low Rainfall (LRF) period (December-May), and the High Rainfall (HRF)
period (June-November). To characterize the habitat at each sampling reach, several physical
characteristics of the pools (length, width, depth, maximum depth, and substrate), and biotic
factors (organic matter in the stream, pool canopy cover, and riparian canopy cover) were
measured. Composition of the substrate was characterized from a location near each sampling
site where decapods were collected. One hundred rocks from four samples of 0.5 m2 were
selected randomly to characterize the substrate composition using a gravelometer. The categories
were expressed as percent bedrock, boulders, cobble, coarse gravel, fine gravel, and sand/fines.
The percentage categories were converted to a Substrate Index (SI) using the following formula:
47
SI = [(0.08) (% bedrock) + (0.07) (% boulder) + (0.06) (% coble) + (0.05) (% gravel) + (0.04) (%
fine gravel) + (0.03) (% sand and fines)]. The composition of the dominant riparian vegetation
was determined by recording the most abundant species along the banks of the streams. The
riparian and pool canopy cover were measured six times annually (three times during the two
periods per year) using a spherical densitometer directly in the middle of the stream and in the
riparian forest (10 m from the stream). Four samples of 0.5 m2 of submerged organic matter in
the selected pools were collected every time the pools were visited. The organic matter was
collected in labeled plastic bags, frozen, dried in an oven at 25 oC for 24 h. Once dried, the
organic matter was weighted to determine the total amount of organic matter in the pool. The
water discharge for each watershed was obtained from the United States Geological Service
(USGS) gauging station located nearest the stream sampling sites (Sabana- USGS 50067000;
Bayamón- USGS 50047850; Río Piedras- 50049100). The discharges for each watershed were
standardized by drainage area. Standard water parameters (conductivity, pH, DO, turbidity, and
temperature) were recorded during 24-h with three DS 5X Hydrolab Multiparameter Sondes
(Hatch Hydromets Colorado, USA) set at each sampling site (river mouth, mid location and
headwaters) (Fig. 3-1) Additional chemical data from the LUW and the HUW were obtained
from the long-term data sets of the Luquillo Long Term Ecological Research program, the Sabana
Station- Forest Service, and the San Juan Urban Long Term Research Area Project.
Decapod sampling and processing
Decapod distributions were collected from all sites using a backpack electrofisher (Model
12-B, Smith-Root, Vancouver, Washington, USA). Collections consisted of three upstream
electrofishing passes in each sampling reach that was bounded by a 6.4 mm mesh net to limit the
emigration or immigration of decapods and fish during sampling. Hand nets were used to collect
the organisms; macro-invertebrates (small decapods, insects, and mollusks) were transferred to
48
labeled plastic bags and placed on ice for transport to the laboratory. The habitats sampled
included riffle, run, pool and the aquatic vegetation. Decapods were identified and classified
according to species, counted, and their reproductive condition was recorded (gravid or nongravid). Large decapods were measured in the field and released. Small specimens were
identified by the reproductive appendages (1st and 2nd pleopods). When the individuals were too
small or immature to be identified, they were classified to genus or family. Taxonomic
identification followed Chace and Hobbs (1969) and Pérez-Reyes et al. 2013. The cephalothorax
length (CL) of each decapod was measured from the post-orbital region to the end of the carapace
with a dial caliper (0.01 mm precision); the measurement from the tip of the rostrum was not used
because the rostrum was missing in some individuals. Length of the rostrum among Xiphocaris
elongata varies among individuals related to the presence of fish predators below waterfalls
(Covich et al. 2009; Ocasio-Torres et al. 2014; 2015).
Eggs from ovigerous females were stripped from the pleopods using fine forceps; setal
material and extraneous matter was removed. The egg mass was placed in a square Petri dish
with water and split into 36 equal portions. Eggs from 8 of 36 squares from the Petri dish were
counted and the total number of eggs from each female was calculated using the following
formula: Total egg number = ((Σ X)/8) (36); where X= number of eggs on each sub-sample.
Freshwater shrimp larval drift
Invertebrate drift at each watershed was sampled at 30 min intervals over a 24 hr period,
at the lowest reach of each river. Drifting decapod larvae were collected by placing 3 plankton
nets (153 µm mesh with dimensions of 30 cm mouth diameter x 90 cm length) in the channel; one
in the middle and two equidistant on each side of the stream (25% and 50% of the stream width
taken from each bank). The nets were located in sites where water depth was sufficient to
completely cover the net opening and were set for periods of 30 min. Depth and flow velocity
49
were measured to calculate the volume of water that passed through each net. Depth was
measured to the nearest 0.5 cm and the water flow was measured (to the nearest 0.01 ms-1) at a
point directly in front of each net using a Marsh McBirney 2000 Flo-Mate Flow Meter. Samples
were labeled and preserved immediately in 4% formalin and transported to the laboratory, where
they were counted using a dissecting microscope. Samples with high larval densities were subsampled and the total number of larvae was estimated by volume. Preserved samples were
diluted in water until reaching 100 ml; then 5 sub-samples of 1 ml were extracted and the larvae
counted. The number of larvae in the sub-samples was averaged and multiplied by the total
volume (ml) in order to estimate total number of larvae in the sample. The drift densities of
shrimp larvae (number of larvae m-3) were calculated by dividing the number of organisms
collected in the net by the amount of water that passed through the net. The volume of water
sample in a 30-min survey period was calculated as V (m3) = S(m2) (v(m/s)) (1800 (s)), where S
is the area of the net mouth submerged in the water and v is the average flow velocity measured
in front of the net. The sampling of shrimp larvae was conducted in random order in July 2009
during the HRF period.
Data analysis
Community composition in streams
The environmental variables and the physico-chemical measurements (24-hr sampling)
from the three sampling sites in each stream were compared among watersheds using one-way
ANOVAs. The totals of these variables were also compared with pairwise comparisons tests
(Tukey) among watersheds. Species diversity was characterized by the number of taxa (S),
Shannon-Weiner Index of Diversity (H’), evenness (J) (Magurran 2003),total density, and
densities of decapod family groups (Atyidae, Palaemonidae, Xiphocarididae, and
Pseudothelphusidae). Differences in decapod community diversity, richness, evenness, and total
50
density among watersheds (LUW, MUW, HUW) and between the two rainfall periods (LRF and
HRF) were examined using nested ANOVAs and a Tukey post-hoc test. The average and
standard error (SE) of each variable measured by each land use reach and rainfall period were
calculated as a way to characterize their variability previous the analyses. Density data were
transformed (LN X+1) prior to being compared among watersheds. Non-metric
multidimensional scaling (NMDS) was used to describe the relationship among densities of
decapod family groups and environmental variables (pool area, pool volume, pool cover, riparian
cover, standardized discharge, substrate index, organic matter in the stream, and maximum
depth). The densities of the decapod families and the corresponding environmental variables
were averaged for each sampling site in each watershed prior to analysis. Family densities of the
primary vector representing environmental variables were plotted with the ordination
configuration. Prior to analysis, the environmental and decapod abundance data were SQRT(X)
transformed. Densities of family groups were used instead of total density per specie due to some
of the specimens could not be fully identified because they were juveniles. The Bray-Curtis
Dissimilarity Index (Bray and Curtis 1957) was used as the distance variable for NMDS
ordination.
Drift density and Fecundity
Statistical differences in aquatic drift density among sites were tested using one-way
ANOVA with a Tukey post-hoc test. Drift densities were (LN X+1) transformed before the
analysis. Linear regressions were used to examine possible relationships between egg production
and shrimp size. We used analysis of covariance (ANCOVA) to test for differences in the mean
numbers of embryos among females of the same species but from different streams. In order to
evaluate possible differences in fecundity among populations, an ANCOVA (with CL as the
51
covariate) was applied to the slopes for the relationship between egg number and body size (Zar
1999).
Results
Characteristics of the watersheds
The one way ANOVAs comparing water discharge from the watersheds demonstrated
significant differences among streams (F2,33=10.4; p<0.0001). The pairwise comparison test
showed that the LUW (0.06+0.01 m3s-1) and HUW (0.05+0.01 m3s-1) had high, similar mean
discharge compared to the MUW where the mean discharge was 0.02+0.002 m3s-1. The lowest
monthly mean discharges were observed during the LRF period (February and January) as
expected. One-way ANOVAs comparing pool area, pool volume, riparian and pool canopy
cover, maximum depth, and the substrate index among watersheds showed no significant
differences among watersheds. One-way ANOVAs comparing pool area, pool volume, riparian
and pool canopy cover, maximum depth, and the substrate index among watersheds showed no
significant differences among watersheds.
One-way ANOVAs for the 24-hr physico-chemical parameters of water showed
significant differences in water temperature, salinity, pH and conductivity among the watersheds
(Table 3-1). Water temperature increased from the LUW to the HUW. The lowest average water
temperature was recorded in the LUW (26+0.08 oC) while the MUW and HUW had average
values of 28.3+0.1 oC and 27.5+0.1 oC, respectively. Concentrations of the dissolved oxygen
varied among streams (Table 3-1). The DO concentrations in the LUW ranged between
111.7+0.5 to 78.2+0.5 mgL-1, in the MUW between 140.0+1.0 to 55.2+1.0 mgL-1, and in HUW
between 94.6+0.5 to 71+0.5 mgL-1. Significant differences in TDS were observed among
watersheds (Table 3-1). The LUW had the lowest concentrations in TDS with an average value
of 0.07+0.002 g L-1 while the highest values were observed in the MUW (0.3+0.003 g L-1).
52
Conductivity and salinity also showed significant differences among streams (Table 3-1). The
MUW and HUW showed higher conductivities and salinities than the LUW (Table 3-1).
Decapod diversity and abundance
A total of 14,833 specimens from the Atyidae, Palaemonidae, Pseudothelphusidae,
Xiphocarididae, and Grapsidae were collected in the watersheds (Table 3-2). The most common
species found in all of the streams were Xiphocaris elongata (n=5164), Macrobrachium
faustinum (n=1276), and Epilobocera sinuatifrons (n=11). Micratya poeyi, Atya lanipes,
Potimirim glabra, Macrobrachium carcinus, and Epilobocera sinuatifrons were present in larger
proportions in the LUW compared to the other watersheds. Conversely, X. elongata, M.
faustinum, and Atya scabra were present in larger proportions in the MUW. Palaemon
pandaliformis was the most abundant shrimp in the HUW (Table 3-2); this species represented
the 77% (530) of all the individuals collected in this watershed during study.
Thirteen species of the 18 native freshwater decapods that are known to occur on the
island (Pérez-Reyes et al. 2013) were collected during the study. The LUW and MUW had
similar numbers of species (11 and 10 respectively) in comparison with the HUW with only 4
species. The nested ANOVA comparing the number of species among watersheds and between
rainfall periods showed significant differences in species richness among watersheds (F2,3=35.3;
p<0.008), but not between rain periods (F2,3=0.3; p>0.825) (Fig. 3-3a). The highest mean number
of species was observed in LUW (7.0+1.1), while the MUW and HUW had 5.0+1.0 and 2.5+0.2
species, respectively. The Tukey pairwise tests to compare average of species number among
watersheds showed that the LUW- HUW differed significantly in their number of species (p<
0.001) than the LUW-MUW (p>0.063) and the MUW-HUW (p>0.09). The most diverse
watershed was LUW with a mean diversity indices of 1.3+0.04 and 1.2+0.1 during the LRF and
HRF, respectively. The mean diversity indices in the HUW were 0.09+0.03 (LRF) and
53
0.3+0.1(HRF) (Fig. 3-3b). The nested ANOVA to compare the diversity index (H’) per rainfall
period and watersheds showed significant differences among watersheds (F2,3=44.6; p<0.006),
but was not significant among rain periods (F2,3=0.6; p<0.718). Higher values in evenness were
observed in the LUW in comparison with the MUW and the HUW (Fig. 3-3c). The nested
ANOVA showed no significant differences in evenness were observed between rainfall periods or
watersheds (Fig. 3-3c). A post hoc Tukey test for evenness showed that the LUW-HUW group
differed from the LUW-MUW and MUW-HUW; no differences in evenness were observed
between seasons.
Higher mean densities of decapods were observed in the LUW and MUW than HUW.
The LUW had a highest average density of decapods (1.7+0.7 decapods m-2) during the LRF in
comparison with the MUW (1.1+0.4 decapods m-2) where the highest average density was
observed in the HRF (Fig.3-3d). The lowest abundance of decapods was observed in HUW
during the HRF with 0.5+0.2 decapods m-2. Significant differences in decapod densities were
found among watersheds (F2,3=101.2; p<0.002), but no significant differences in decapod
densities were found between rain periods (F2,3=0.054; p>0.983) (Fig. 3-3d). The most abundant
species in the LUW were Micratya poeyi and Xiphocaris elongata with average densities of 1.0
+0.2 and 1.1+0.1 shrimp m-2 respectively. The LUW had the largest density of atyids (1.2+0.1
atyids m -2) and xiphocarids (0.7+0.1 Xiphocaris m-2). Palaemonids were abundant in HUW
(0.6+0.2 palaemonids m-2), while the largest average densities of Epilobocera were observed in
LUW (0.004+0.003 crabs m-2) (Table 3-2). Highly significant differences in atyid densities were
observed among watersheds (F2,3=14.7; p< 0.0001), but not between LRF/HRF periods.
Significant differences in xiphocarid densities were found between seasons (F2,3=4.6; p< 0.02) but
not among watersheds. Higher densities of xiphocarids were observed during the LRF period in
the LUW in contrast with the MUW and HUW where the highest densities were observed in the
HRF period (Table 3-2). The post-hoc test showed no differences among watersheds or rain
54
season. No significant differences in palaemonids, xiphocarids and pheudothelphusids were
observed between rainfall periods or watersheds.
Multivariable Analysis
NMDS ordination of decapod abundance assemblages yielded 2 major axes; Axes 1 and
2 explained most of the variation. Axis 1 and 2 were highly related to the discharge (0.8) and
pool volume (0.03), respectively (Fig. 3-4). Stream with positive values on NMDS axis 1 and 2
were located in the HUW. Discharge represented the environmental variable with better
explained the variation in species abundance. The environmental variable that best explained the
variation on axis 2 was pool volume. The sites with larger pools were observed in the MUW
(10.7 m-3) and low (10.3 m-3) HUW. The pool area and the maximum depth of the pools were
also important factors with direct influence in the decapod densities.
Fecundity and Drift density
Ovigerous females of Atya innocuous, Micratya poeyi, Macrobrachium faustinum, and
Xiphocaris elongata were collected in all the watersheds. Ovigerous Palaemon pandaliformis
were collected in the HUW. The largest brood sizes were reported for Atya innocuous where the
maximum number of eggs were observed in the MUW (6,587 eggs) and LUW (1,256) and the
smallest was for Micratya poeyi from LUW with 12 eggs. Positive linear regressions between
cephalothorax length and fecundity were observed for the species in all the watersheds (Fig. 3-5).
No significant differences in the slopes between body size and fecundity among watersheds in
Micratya poeyi. The ANCOVA analyses demonstrated no significant effect of locality on female
fecundity for Atya innocuous (F=1.4; df=1; p>0.2) and Xiphocaris elongata (F=1.6; df=1;
p>0.2), but were significant for Macrobrachium faustinum (F=17.8; df=2; p<0.001) (Fig 3-2b, c,
d). A post-hoc Tukey test for comparison of fecundity among watersheds in M. faustinum
showed similar fecundities between the LUW-HUW than with the LUW-MUW or MUW-HUW.
55
The analyses of covariance detected effects of female CL on fecundity in Atya innocuous (F=214;
df=1; p<0.0001), Macrobrachium faustinum (F=52; df=1; p<0.0001) and Xiphocaris elongata
(F=53; df=1; p<0.0001).
Lower mean hourly drift densities (larvae m-3) were observed at 10:30 hr and 13:30 hr in
the LUW (2.0+0.36 larvae m-3) and HUW (2.0+0.65 larvae m-3), respectively. The largest mean
drift density occurred in the MUW with 2552+7.8 larvae m -3 (Fig. 3-6). Mean drift density in the
LUW over the course of the study was 370±133.2 larvae m -3, while the mean for the MUH and
HUW were 263±105.6, and 344±111.1 larvae m -3. No significant differences in mean drift
densities were observed among watersheds (F2,68=2.06, p=0.13). Diel periodicity in the drift
densities was observed where a reduction in larvae release occurred from 6:30 to 16:30 (Fig. 3-6).
Discussion
Our results show a general negative impact of urbanization on species richness and
abundance of freshwater decapods along the urban-forested gradient in the tropical streams of
Puerto Rico. The decapod communities were less diverse and less abundant in HUW than in the
MUW and LUW. This difference suggests that watersheds with high percentage of forested landuse are important to sustain the freshwater decapod diversity. These observations agree with
previous patterns associated with the “Urban Stream Syndrome” where streams are degraded by
complex and multiple physico-chemical and ecological stressors (Meyer et al. 2005; Walsh et al.
2005; Wenger et al. 2009). The effects of urbanization on rivers can decrease ecological integrity
and associated ecosystem services (Walsh et al. 2005; Wallace and Eggert 2009). Nonetheless,
the HUW retained 4 of the 13 total species observed in the LUW. Although the number of
species is relatively low in the urbanized river, these organisms, especially Xiphocaris, can still
function as shredders in the ecosystem.
56
The diversity and abundance of freshwater decapods among watersheds were best
explained by an increase in water discharge in the HUW relative to the MUW and LUW. A
disproportionate increase in water discharge in the HUW in comparison with the LUW and
MUW, as result from changes in the land use patterns among these watersheds, appeared to
determine a reduction in the number of decapods in each stream. Even though the HUW had
fewer species than the LUW, this urbanized watershed had a higher diversity of decapod species
than expected. The presence of some species of palaemonids, xiphocarids and the endemic crab
Epilobocera sinuatifrons in the HUW demonstrates that these ecosystems can support species that
are critical for sustaining ecological processes such as shredding of leaf litter. Most of the shrimp
apparently benefited from high discharge during their spawning by having rapid downstream
transport of their larvae to the estuary as part of their amphidromous life cycle (Bauer 2011a;
2011b; 2013). However, extremely high discharge events can wash out some macroinvertebrates,
organic matter and cause changes in the morphology of the pools in headwater streams (Covich et
al. 1991; 1996; 2006). In urban streams, high-discharge events have been associated with the
reduction on diversity in the lower valleys of the watersheds (Urban et al. 2006). An increase in
sedimentation, alteration of river banks, and changes in the physico-chemical environment of the
stream can result in the reduction of the habitat heterogeneity and the loss of sensitive species.
The HUW has been developed over many years (Lugo et al. 2011) and has the largest
percentage of impervious surfaces, pipes, and culverts that transport water (precipitation or
wastewater overflow) to the stream (Potter et al. 2013). These effluents, the channelization of the
main channel and some of the tributaries resulted in an increase of the river discharge in these
reaches. Such modifications in the watersheds together with the reduction of the riparian forest
can increase discharge that disrupts the natural conditions of pools, increase sedimentation, and
decrease food quality. The HUW (Río Piedras) tends to be a “flashy” stream as result of
frequent, brief rainfall events, and changes in land use. The geomorphology of the Río Piedras
57
headwaters is steeply sloped along a gradient of elevation from 200 to 0 masl. The urban areas
are located in the coastal valleys while the land uses on the steep slopes are suburban areas with
secondary forests. Changes in discharge in the urban and suburban zones occur as a result of the
combined effects of changes in land use, increases in impervious surface, rapid runoff, and
overflows of the sewage systems. Headwaters in the HUW also exhibit flashiness as result of
saturated soils and a network of natural drainage channels (Ramírez et al. 2009; 2012). The soils
can retain water before the excess runoff flows to the stream in contrast to coastal and lower
valleys where the rainwater rapidly runs off the impervious surfaces increasing the water
discharge. Frequent and intense flashiness in these valleys exert a strong effect on the freshwater
biota and in the quality and quantity of energy derived from the riparian organic matter (Paul and
Meyer 2001; Walsh et al. 2005; Braud et al. 2013). Heavy rainstorms remove the small amount
of organic matter deposited in the stream by the urban riparian vegetation as well the human
derived-organic matter (fecal coliform and Streptococcus) and export it to the ocean (Larsen and
Webb 2009; Bachoon et al. 2010).
Macrobrachium faustinum, Palaemon pandaliformis and Xiphocaris elongata were the
only shrimp species collected in the HUW, suggesting that these species are highly tolerant to
changes in water discharge, temperature and water chemistry. In the headwaters, P.
pandaliformis was the dominant species and responded more positively to uniform conditions, a
variety of habitats, and access to food resources. Paschoal et al. (2013) suggest that palaemonids
seek locations with sufficient organic matter for food and as refuge to avoid fish predation. The
high abundance of Palaemon in these headwater reaches is related to their detritivorous feeding
(Campaneli et al. 2009), a role shared with Xiphocaris (Crowl et al. 2001). Xiphocaris elongata
process leaves and produces fine, medium and coarse particulates that can be used by filterfeeding species (Crowl et al. 2001). Species like Macrobrachium faustinum are generally more
abundant in the lower and shallow reaches with low-flow conditions (Hunte and Mahon 1983;
58
Thorpe and Lloyd 1999). These results are consistent with those of Nemeth and Platenberg
(2007) who reported similar species richness and distribution in streams with different degrees of
human impact in the St. Thomas U.S. Virgin Islands. They found M.faustinum and X.elongata in
the low, moderate and highly impacted streams while Atya species were restricted to the low and
moderate-impacted urban streams.
The lowest densities of X. elongata and M. faustinum in the headwaters might be the
result of inter-specific competition with P. pandaliformis. These observations are consistent with
the results of an exclusion experiment developed in artificial streams of Puerto Rico, where P.
pandaliformis displaced individuals of X. elongata and M. faustinum when they were in the same
cage; neither Xiphocaris nor M. faustinum exhibited this behavior when they were interacting in
the same location. Palaemon pandaliformis is a shrimp species from lowlands and shallow
aquatic systems that is tolerant of changes in salinity and water flows in estuaries (Campaneli et
al. 2009).
The absence of filter feeder species of shrimp in the HUW may represent the result of
direct or indirect disturbances in this stream as well the replacement of sensitive species by more
tolerant species. The higher concentrations of oxygen and rocky substrate and submerged wood
could be related to the presence of larger populations of these shrimp. Hobbs and Hart (1982)
reported that the absence of atyids in certain streams in the Caribbean and Central America were
the results of the absence of rocks, debris and macrophytes. Previous studies in the headwater
tributaries of this watershed have reported the presence of some adults of Atya lanipes (A.
Ramírez, personal communication). These findings could represent a previous population of this
species in the stream that was temporarily able to remain in a particular location with adequate
cover; watersheds with diverse habitats and relatively low normal flow conditions tend to have
diverse population of atyids. Similar to Palaemon pandaliformis, Atya lanipes prefers pools with
natural substrate, high concentration of organic matter and stable flow conditions.
59
Small numbers of Epilobocera sinuatifrons, the endemic freshwater crab of Puerto Rico,
were observed in the headwater and suburban reaches of all the watersheds. Previous collections
documented their presence in almost all types of freshwater bodies, from pristine montane
streams to wetlands, karsts, and caves of the island (Pérez-Reyes et al. 2013). The amphibious
movement of adults and their direct development makes Epilobocera relatively resistant to
changes in discharge and land use but sensitive to water pollution. The presence of E.
sinuatifrons in the forested headwaters of the HUW demonstrates the importance of these reaches
as refuges for the conservation of sensitive species (Thorpe and Lloyd 1999; Yeo et al. 2008;
Cumberlidge et al. 2009).
Biota and water quality. A decrease in water quality tends to relate land use with
increases in temperature, pH, TDS, conductivity and salinity with increased urbanization. Higher
water temperatures were observed in the MUW and HUW than in the LUW likely because of
reduced riparian forest cover. Increased water temperatures in higher-latitude urban streams are
often associated with the removal of riparian forest that reduces the shade in the streams (Meyer
et al. 2005). In the HUW, more than 60 % of the watershed is residential land while in the MUW
nearly 30 % of the watershed is urbanized. Concrete buildings, roads, culverts, and channels can
store and transfer heat (during rainstorms) to warm the stream water and affect the stream biota
(Somers et al. 2013). Higher water temperatures in the streams reduce the percentage of
dissolved oxygen in the water, and accelerate decomposition rates, nutrition release, and animal
metabolism. Palaemonids in the highly urban watershed tolerate high water temperatures,
salinity, and changes in oxygen concentrations. Atyids are sensitive to warm temperatures and
low dissolved oxygen (González-Ortegón et al. 2012; 2013).
Reductions in oxygen concentrations at urban watersheds can result from the combined
effects of organic pollution and changes in the land use in the watersheds. Meanders and
channels in the coastal valleys of the high and moderately urban watersheds have been modified
60
to prevent flood and to transport stream water rapidly to the ocean. Replacing the natural,
complex substrate with uniform concrete channels, increased channel width and channel
straightening all combine to reduce the turbulence that in turn decreases the dissolved oxygen
concentration (Miller 2013). Studies on macroinvertebrates have demonstrated that reduction in
DO concentrations affect the emergence of insects and produce the mortality of sensitive groups
(Connolly et al. 2004).
In natural streams, conductivity generally increases from headwater to downstream and is
affected by geology, but in urban systems the highly variable discharges can rapidly change the
conductivity. Leaks in the sewage system, run-off or soil erosion can raise the conductivity
because of the increased input of chloride, phosphate, and nitrate (Paul and Meyer 2001).
Conductivity was higher in the MUW and HUW than in the LUW. These watersheds have both
point and non-point pollution from agriculture, septic tanks, and run-off due to the large amounts
impervious surface.
Decapods in Impacted Streams. Urbanization is known to decrease the abundance and
diversity of organisms living in streams, but it is not clear which forcing factors (e.g. changes in
discharge, sediment, and pollutant concentrations), are most important for causing these
reductions. Our results suggest a negative effect of the physico-chemical and environmental
impacts on the diversity and abundance of freshwater decapods in the urban watersheds.
Hydrologic changes, physico-chemical factors and land use appear to be the main stressors that
influence the abundance and diversity of decapods in the streams. Higher stream discharge
reduced the densities and diversity of macroinvertebrates regardless of whether they were in LRF
and HRF periods, discharges representing press or pulse disturbances. Tropical streams with
LRF and HRF periods are characterized by the relatively high frequency and intensity of stormflow events.
61
Riparian vegetation had positive effect on species richness and abundance by providing
food, shelter and substrate for aquatic organism as well by reducing the water temperature. The
riparian vegetation in the headwater reaches in the highly urbanized watershed of Río Piedras is
characterized by non-native trees that provide input of leaf litter to the detritivores. Also, these
reaches have closed canopies, relatively slower flow conditions, lower water temperature, and a
more diverse community of other macroinvertebrates (freshwater sponges, flatworms, snails,
clams, and insects) than the urbanized sections of the stream. Increased urbanization, impervious
surfaces, channelization, and forest clearing can reduce lateral subsidies of leaf litter that are
needed to support the higher taxonomic richness and abundance. The loss of species richness and
abundance during high discharge is consistent with other studies in temperate (Boulton et al.
1992; Bogan and Lytle 2007) and tropical (de Jesús and Ramírez 2011) streams, where high
discharge removes the living and non-living biota from the stream reach. Ramírez et al. (2009)
and de Jesús and Ramírez (2011) observed that diversities of Ephemeroptera and Trichoptera
decreased from the forested to urban reaches, while the densities of Chironomidae increased
because of a lack of hard substrata. The patterns of changes on diversity of decapods and insects
were also observed in the fish communities in this stream. Engman and Ramírez (2012)
demonstrated that natural and low impacted reaches have more native species of aquatic insects
than reaches in highly urbanized reaches.
The HUW has all the 9 native species of fishes present on the island in addition to some
exotic species. Native fish are sensitive to habitat alterations and studies in Puerto Rico (e.g.,
Engman and Ramírez 2012; Cooney and Kwak 2013), and Hawai’i (e.g., Brasher 2003; Keith
(2003) have shown that Sicydium, Eleotris and Gobiomorus species prefer natural channels and
spawn in streams with low amounts of silt substrate, larger coarse substrate, closed canopy, unaltered channels, and cool water temperatures.
62
The decapod community in the MUW contrasts with our observations in LUW. The
decapod communities in the MUW resemble the communities observed in the LUW and many
other streams in the island (Pérez-Reyes et al. 2013). Only 10 out the 18 decapods species
present in the island were found in this stream. The differences in species richness and
abundance among sites are likely affected by the presence of barriers caused by two dams (The
San Juan and Cidra Lake Dam) that isolate the decapod communities in the headwater reaches
from the communities in the urban and coastal reaches in this stream. Smaller densities of
decapods (Atya scabra, A. innocuous, Micratya poeyi, and Macrobrachium faustinum) collected
in the headwater reaches, located above the dams, contrast with the densities observed in the
urban reaches where densities were higher. In tropical and temperate streams where freshwater
fauna have life cycles dependent on the marine environment, dams have restricted the migration
of fish and shrimp, and disrupted the longitudinal connectivity in the stream resulting in
detrimental effects on the freshwater environment above and below the dam (Holmquist et al.
1998; Greathouse et al. 2006a; Cooney and Kwak 2013). However, the increase in shrimp
density in these sites could represent the effect of the dam located upstream that prevents the
migration of the faunal biota to the upper parts of the stream. Headwaters of the LUW had the
higher densities of decapods among streams. That high density most likely represents the
massive upstream migration of post-larvae (juveniles) shrimp from the estuary during the LRF
period.
The LUW was the most diverse in freshwater fauna among the studied streams with 11 of
the 18 species of freshwater decapods reported for the island. The abundance and species
richness showed no variations between rain periods (LRF/HRF). Atyids and xiphocarids were the
most abundant; palaemonids and pseudothelphusids were present but in lower densities. In this
stream, in contrast to the others, all the shrimp families were represented in all the sampling
reaches. Higher densities of decapods during the low rainfall period can be attributed to the
63
upstream migration of post-larval shrimp from the estuary. Amphidromous shrimp reproduce
during the HRF period (June-November) that concurs with the hurricane season and the increased
of the allochthonous input from the forest (Heartsill-Scalley et al. 2012). This input of litter
increases food resources during the period when most reproduction occurred. Macroinvertebrate
diversity and abundance were significantly lower in the HUW than at the LUW and MUW. This
difference among the three rivers can probably be explained by limited food availability, habitat
loss, and warmer water temperature in conjunction with the flashy discharge regimes; low
invertebrate production can be a consequence of high water discharges (Heino et al. 2004; Girard
et al. 2013).
Shrimp fecundity in urban streams. The drift of shrimp larvae was similar among
watersheds in terms of the density of larvae drifted and the time of release. All the shrimp
species exhibited positive relationship between size and egg number and no differences among
watersheds were observed. Fecundity in decapods is determined primarily by body size and
energy allocation. The larvae releases coincide with high-discharge events; shrimp release larvae
after an increase in stream discharge. The larval drift started at 18:00 and drift densities peaked
2-h later, except for the low impacted watershed that had a prolonged larval drift 5 h later. The
concentration of larvae released at this time can reach a maximum of 2500 larvae m -3. This
concentration is consistent with the breeding pattern that peaks during the warmest months with
high-flow conditions, and warmer water temperatures (Heartsill-Scalley et al. 2012). In general,
drift usually increases from sunset to darkness (March et al. 1998), continues at low densities
after the initial peak throughout the night and ends with a reduction in drift densities at dawn
(Ideguchi et al. 2007). Shrimp are active at night and avoid visual predators (Johnson and Covich
2000; Kikkert et al. 2009). The reproductive patterns in freshwater decapods are apparently
synchronized by physical and environmental factors as water temperature, photoperiods, rainfall,
nutrients availability, and phases of the moon. Tropical and subtropical shrimp can breed
64
throughout the year, but mostly during warm months and high-flows events which transport the
larvae to the estuarine zone. After the larvae are released they spend 30-90 days (depend on the
species) in estuarine or marine waters where after several molts they transform into post-larval
shrimp that migrate to headwaters (Bauer 2011a; 2011b; 2013).
Conclusion
Anthropogenic stressors increase the environmental pressure on macroinvertebrate
communities that can alter biotic distributions in tropical streams. Changes in the riparian
vegetation can increase the erosion of the stream banks, sedimentation, and water flow that
decreases the habitat heterogeneity and the abundance and diversity of decapods in the stream.
Complete or partial removal of riparian forests greatly decreases the input of allochthonous
material, a major source of energy for decapods and other macroinvertebrates. These removals
also increase the water temperature that raise rates of animal metabolism and deplete oxygen
concentrations. The relatively rich and unaltered environment, presence of organic matter,
longitudinal connectivity and the physical-chemical variables can provide the conditions for
which these streams are important areas for the conservation of these aquatic animals.
In general, urbanization in tropical regions decreases the species richness and abundance
of decapod communities in highly urbanized watersheds when compared to watersheds with low
or moderate urbanization. Previous studies of macroinvertebrates in temperate-zone streams
(Paul and Meyer 2001; de Jesús and Ramírez 2011) have demonstrated that poor quality waters
are often a result of urbanization that decreases the species richness and abundance. Urban
streams reflect the impact of human activities in their hydrology, geomorphology, water quality
and aquatic biota. The effect of a combination of all or some of these variables impacts on the
species assemblages as well on the energy inputs in the stream. Our study suggests that the loss
of species richness and abundance of freshwater decapods in tropical insular urban streams is the
65
result of a series of stressors that degrade decapod habitat. The alterations of the terrestrial
environment as well the construction of barriers to migration change the local energy inputs as
well the longitudinal connectivity among streams sections. These changes affect the organization
and functions of the stream communities in the upper reaches of insular river drainages and are
similar to effects initially outlined in the river continuum concept for larger watersheds (Vannote
et al. 1980; Greathouse et al. 2006b; Tomanová et al. 2008; Gorbach et al. 2014).
Acknowledgments
We thank the people who assisted us, with special appreciation for the fieldwork done by
Pablo J. Hernández-García, Carlos A. Rosado Berríos, Francisco J. Pérez and José A. Rivera.
Our urban studies benefited from collaborations with research groups organized by Alonso
Ramírez, University of Puerto Rico, and Ariel E. Lugo, International Institute of Tropical
Forestry. This research was supported by grants BSR-8811902, DEB 9411973, DEB 0080538,
DEB 0218039, and DEB 0620910 from National Science Foundation (NSF) to the Institute for
Tropical Ecosystem Studies, University of Puerto Rico, and to the International Institute of
Tropical Forestry, United States Department of Agriculture (USDA) Forest Service, as part of the
Long-Term Ecological Research Program in the Luquillo Experimental Forest. Also this study
was partially supported by the San Juan- ULTRA Project (NSF Grant 0948507), USDA Forest
Service and the University of Puerto Rico.
66
References
Bachoon DS, Markand S, Otero E, Perry G, Ramsubaugh A (2010) Assessment of non-point
sources of fecal pollution in coastal waters of Puerto Rico and Trinidad. Marine Pollution
Bulletin 60:1117-1121
Bauer R (2011a) Amphidromy and migrations of freshwater shrimp. I. Costs, benefits,
evolutionary origins, and an unusual Case of amphidromy. In: Asakura A (ed) New
frontiers in crustacean biology. Brill, Leiden, The Netherlands, pp 145-156
Bauer R (2011b) Amphidromy and migrations of freshwater shrimp. II. Delivery of hatching
larvae to the sea, return juvenile upstream migration, and human impacts. In: Asakura A
(ed) New frontiers in crustacean biology. Brill, Leiden, The Netherlands, pp 157-168
Bauer RT (2013) Amphidromy in shrimp: a life cycle between rivers and the sea. In: Wehrtmann
IS, Bauer RT (eds) Studies on freshwater decapods in Latin America. Latin American
Journal of Aquatic Research 41:633-650
Bogan MT, Lytle DA (2007) Seasonal flow variation allows time-sharing by disparate aquatic
insect communities in montane desert streams. Freshwater Biology 52:290-304
Boulton AJ, Peterson CG, Grimm NB, Fisher SG (1992) Stability of an aquatic macroinvertebrate
community in a multiyear hydrologic disturbance regime. Ecology 73:2192-2207
Brasher AMD (2003) Impacts of human disturbances on biotic communities in Hawaiian streams.
BioScience 53:1052-1060
Bray JR, Curtis JT (1957) An ordination of the upland forest communities of southern Wisconsin.
Ecological Monograph 27:325-349
Braud I, Breil P, Thollet F, Lagouy M, Branger F, Jacqueminet C, Kermadi S, Michel K (2013)
Evidence of the impact of urbanization on the hydrological regime of a moderate-sized
periurban catchment in France. Journal of Hydrology 485:5-23
Buckup L, Bueno AA, Bond-Buckup G, Casagrande M, Majolo F (2007) The benthic
macroinvertebrate fauna of highland streams in southern Brazil: composition, diversity
and structure. Revista Brasileira de Zoologia 24:294-301
Campaneli Mortari R, Nunes Pralon BG, Negreiros-Fransozo ML (2009) Reproductive biology of
Palaemon pandaliformis (Stimpson, 1871) (Crustacea, Decapoda, Caridea) from two
estuaries in southeastern Brazil. Invertebrate Reproduction and Development 53:223-232
Chace FAJr, Hobbs HH (1969) The freshwater and terrestrial decapod crustacean of the West
Indies with special references to Dominica. United States National Museum Bulletin 292:1258
67
Chadwick MA, Thiele JE, Huryn AD, Benke AC, Dobberfuhl DR (2012) Effects of urbanization
on macroinvertebrates in tributaries of the St. Johns River, Florida, USA. Urban Ecosystems
15:347-365
Chinnayakanahalli KJ, Hawkins CP, Tarboton DG, Hill RA (2011) Natural flow regime,
temperature and the composition and richness of invertebrate assemblages in streams of
the western United States. Freshwater Biology 56:1248-1265
Connolly NM, Crossland MR, Pearson RG (2004) Effect of low dissolved oxygen on survival,
emergence, and drift of tropical stream macroinvertebrates. Journal of the North
American Benthological Society 23:251-270
Cooney PB, Kwak TJ (2013) Spatial extent and dynamics of dam impacts on tropical island
freshwater fish assemblages. BioScience 63:176-190
Covich AP, McDowell WH (1996) The stream community. In: Reagan DP, Waide RB (eds) The
Food Web of a Tropical Rain Forest. The University of Chicago Press, Chicago, pp 433459
Covich AP, Crowl TA, Johnson SL, Pyron M (1996) Distribution and abundance of tropical
freshwater shrimp along a stream corridor: response to disturbance. Biotropica 28:484492
Covich AP, Palmer MA, Crowl TA (1999) Role of benthic invertebrate species in freshwater
ecosystems. BioScience 49:119-127
Covich AP, Crowl TA, Hein CL, Townsend MJ, McDowell WH (2009) Predator–prey
interactions in river networks: comparing shrimp spatial refugia in two drainage basins.
Freshwater Biology 54:450-465
Crowl TA, McDowell WH, Covich AP, Johnson SL (2001) Freshwater shrimp effects on detrital
processing and nutrients in a tropical headwater stream. Ecology 82:775-783
Crowl TA, Brokaw N, Waide RB, González G, Beard K, Greathouse E, Lugo AE, Covich AP,
Lodge DJ, Pringle C, Thompson J, and Belovsky GE (2012) When and where biota
matter: Linking disturbance regimes, species characteristics and dynamics of
communities and ecosystems. pp. 272-304, In: Brokaw N, Crowl TA, Lugo AE,
McDowell WH, Scatena FN, Waide RH, Willig MR (eds.), A Caribbean forest tapestryThe multi-dimensional nature of disturbance and response. Oxford University Press,
Oxford.
Cumberlidge N, Ng PKL, Yeo DCJ, Magalhaes C, Campos MR, Alvarez F, Naruse T, Daniels
SR, Esser LJ, Attipoe FYK, Clotilde-Ba FL, Darwall W, McIvor A, Ram M, Collen B
(2009) Freshwater crabs and the biodiversity crisis: importance, threats, status, and
conservation challenges. Biological Conservation142:1665-1673
de Jesús-Crespo R, Ramírez A (2011) Effects of urbanization on stream physicochemistry and
macroinvertebrate assemblages in a tropical urban watershed in Puerto Rico. Journal of
the North American Benthological Society 30:739-750
68
Engman AC, Ramírez A (2012) Fish assemblage structure in urban streams of Puerto Rico: the
importance of reach- and catchment-scale abiotic factors. Hydrobiologia 693:141-155
Ewel JJ, Whitmore JL (1973) The ecological life zones of Puerto Rico and the Virgin Islands.
Institute of Tropical Forestry, San Juan, Puerto Rico. Forest Service Research Paper ITF18:1-72
Fogaça FNO, Gomes LC, Higuti J (2013) Percentage of impervious surface soil as indicator of
urbanization impacts in Neotropical aquatic insects. Neotropical Entomology 42:1-9
Girard V, Monti D, Valade P, Lamouroux N, Mallet JP, Grondin H (2013) Hydraulic preferences
of shrimps and fishes in tropical insular rivers. River Research and Applications 30:766779
González-Ortegón E, Rodríguez A, Drake P (2012) The freshwater shrimp Atyaephyra
desmarestii (Millet, 1831) as a bioindicator of hypoxic event effects on temperate
freshwater systems. Ecological Indicators 18:236-242
González-Ortegón E, Pascual E, Drake P (2013) Respiratory responses to salinity, temperature
and hypoxia of six caridean shrimp from different aquatic habitats. Journal of
Experimental Marine Biology and Ecology 445:108-115
Gorbach KR, Shoda ME, Burky AJ, Benbow ME (2014) Benthic community responses to water
removal in tropical mountain streams. River Research and Applications 30:791-803
Gould WA, Alarcón C, Fevold B, Jiménez ME, Martinuzzi S, Potts G, Quiñones M, Solórzano
M, Ventosa E (2008) The Puerto Rico Gap Analysis Project, Volume 1: Land cover,
vertebrate species distributions, and land stewardship, pp165
Greathouse EA, Pringle CM, Holmquist JG (2006a) Conservation and management of migratory
fauna: dams in tropical streams of Puerto Rico. Aquatic Conservation of Marine and
Freshwater Ecosystems 16:695-712
Greathouse EA, Pringle CM (2006b). Does the river continuum concept apply on a tropical
island? Longitudinal variation in a Puerto Rican stream. Canadian Journal of Fisheries
and Aquatic Sciences 63:134-152
Heartsill-Scalley T, Scatena FN, Moya S, Lugo AE (2012) Long-term dynamics of organic matter
and elements exported as coarse particulates from two Caribbean montane watersheds.
Journal of Tropical Ecology 28:127-139
Hein CL, Pike AS, Blanco JF, Covich AP, Scatena FN, Hawkins CP, Crowl TA (2010) Effects of
coupled natural and anthropogenic factors on the community structure of diadromous fish
and shrimp species in tropical island streams. Freshwater Biology 56:1002-1015
Heino J, Louhi P, Muotka T (2004) Identifying the scales of variability in stream
macroinvertebrate abundance, functional composition and assemblage structure.
Freshwater Biology 49:1230-1239
69
Helmer EH, Ramos O, del M López T, Quiñónez M, Diaz W (2002) Mapping the forest type and
land cover of Puerto Rico, a component of the Caribbean biodiversity hotspot. Caribbean
Journal of Science 38:165-183
Hobbs HH Jr, Hart CW Jr (1982) The shrimp genus Atya (Decapoda: Atyidae). Smithsonian
Contributions to Zoology 364:1-143
Holmquist JG, Schmidt-Gengenbach JM, Yoshioka BB (1998) High dams and marine–freshwater
linkages: effects on native and introduced fauna in the Caribbean. Conservation Biology
12:621-630
Hunte W, Mahon R (1983) Life history and exploitation of Macrobrachium faustinum in a
tropical high gradient river. Fishery Bulletin 81:654-660
Johnson SL, Covich AP (2000) The importance of night-time observations for determining
habitat preferences of stream biota. Regulated Rivers: Research and Management 16:9199
Kaushal SS, Belt KT (2012) The urban watershed continuum: evolving spatial and temporal
dimensions. Urban Ecosystems 15:409-435
Keith P (2003) Biology and ecology of amphidromous Gobiidae of the Indo-Pacific and the
Caribbean regions. Journal of Fish Biology 63:831-847
Kikkert DA, Crowl TA, Covich AP (2009) Upstream migration of amphidromous shrimp in the
Luquillo Experimental Forest, Puerto Rico: temporal patterns and environmental cues.
Journal of the North American Benthological Society 28:233-246
Larsen MC, Webb RM (2009) Potential effects of runoff, fluvial sediment, and nutrient
discharges on the coral reefs of Puerto Rico. Journal of Coastal Research 25:189-208
Line DE (2013) Effect of development on water quality for seven streams in North Carolina.
Environmental monitoring and assessment 185:6277-6289
Lugo AE, González OMR, Pedraza CR (2011) The Río Piedras watershed and its surrounding
environment. International Institute of Tropical Forestry; USDA Forest Service pp 52
Mallin MA, Johnson VL, Ensign SH (2009) Comparative impacts of stormwater runoff on water
quality of an urban, a suburban, and a rural stream. Environmental Monitoring and
Assessment 159:475-491
Magurran AE (2003) Measuring biological diversity. Blackwell Publishing, Oxford
March JG, Benstead JP, Pringle CM, Scatena FN (1998) Migratory drift of larval freshwater
shrimps in two tropical streams, Puerto Rico. Freshwater Biology 40:261-273
March JG, Pringle CM (2003) Food web structure and basal resource utilization along a tropical
island stream continuum, Puerto Rico. Biotropica 35:84-93
70
McDonald RI, Marcotullio PJ, Güneralp B (2013) Urbanization and global trends in biodiversity
and ecosystem services. In: Elmqvist T, Fragkias M, Goodness J, Güneralp B,
Marcotullio PJ, McDonald RI, Parnell S, Schewenius M, Sendstad M, Seto KC,
Wilkinson C. (eds). Urbanization, biodiversity and ecosystem services: Challenges and
opportunities. Springer Netherlands pp. 32-52
Meyer JL, Paul MJ, Taulbee WK (2005) Stream ecosystem function in urbanizing landscapes.
Journal of the North American Benthological Society 24:602-612
Miller EM (2013) Local- and landscape-level controls on coarse particulate organic matter
retention in urban and forested small streams of central Massachusetts. Freshwater
Science 32:576-585
Nemeth D, Platenberg R (2007) Diversity of freshwater fish and crustaceans of St. Thomas
watersheds and its relationship to water quality as affected by residential and commercial
development. Water Resources Research Institute Project 2006VI73B, University of the
Virgin Islands, St. Thomas
Ocasio-Torres ME, Crowl TA, Sabat AM (2014) Long rostrum in an amphidromous shrimp
induced by chemical signals from a predatory fish. Freshwater Science 33:451-458
Ocasio-Torres ME, Giray T, Crowl TA, Sabat AM (2015) Antipredator defence mechanism in the
amphidromous shrimp Xiphocaris elongata (Decapoda: Xiphocarididae): rostrum length.
Journal of Natural History doi: 10.1080/00222933.2015.1005716
Ortíz-Zayas J, Cuevas E, Mayol-Bracero O, Donoso L, Trebs I, Figueroa-Nieves D, McDowell
WH (2006) Urban influences on the nitrogen cycle in Puerto Rico. Biogeochemistry
79:109-133
Paul MJ, Meyer JL (2001) Streams in the urban landscape. Annual Review of Ecology and
Systematics 32:333-365
Pérez-Reyes O, Crowl TA, Hernández-García P, Ledesma-Fuste R, Villar-Fornes FA, Covich AP
(2013) Freshwater decapods of Puerto Rico: a checklist and reports of new localities.
Zootaxa 3717:329-344
Potter JD, McDowell WH, Helton AM, Daley ML (2013) Incorporating urban infrastructure into
biogeochemical assessment of urban tropical streams in Puerto Rico.
Biogeochemistry12:1-16
Pringle CM, Blake GA, Covich AP, Buzby KM, Finley A (1993) Effects of omnivorous shrimp
in a montane tropical stream: sediment removal, disturbance of sessile invertebrates and
enhancement of understory algal biomass. Oecologia 93:1-11
Ramírez A, de Jesús-Crespo R, Martinó-Cardona DM, Martínez-Rivera N, Burgos-Caraballo S
(2009) Urban streams in Puerto Rico: what can we learn from the tropics? Journal of the
North American Benthological Society 28:1070-1079
71
Ramírez A, Engman A, Rosas KG, Pérez-Reyes O, Martinó-Cardona DM (2012) Urban impacts
on tropical island streams: some key aspects influencing ecosystem response. Urban
Ecosystems 15:315-325
Somers KA, Bernhardt ES, Grace JB, Hassett BA, Sudduth EB, Wang S, Urban DL (2013)
Streams in the urban heat island: spatial and temporal variability in temperature.
Freshwater Science 32:309-326
Synder MN, Anderson EP, Pringle CM (2011) A migratory shrimp’s perspective on habitat
fragmentation in the neotropics: extending our knowledge from Puerto Rico. In: Asakura
A (ed) New frontiers in crustacean biology. Brill, Leiden, The Netherlands, pp 169-182
Thomlinson JR, Rivera LY (2000) Suburban growth in Luquillo, Puerto Rico: some
consequences of development on natural and semi-natural systems. Landscape and Urban
Planning 49:15-23
Thorpe T, Lloyd B (1999) The macroinvertebrate fauna of St. Lucia elucidated by canonical
correspondence analysis. Hydrobiologia 400:195-203
Tomanová S, Tedesco PA, Campero M, Van Damme PA, Moya N, Oberdorff T (2008)
Longitudinal and altitudinal changes of macroinvertebrate functional feeding groups in
Neotropical streams: A test of the River Continuum Concept. Archiv für Hydrobiologie
170:233-241
Urban MC, Skelly DK, Burchsted D, Price W, Lowry S (2006) Stream communities across a
rural–urban landscape gradient. Diversity and Distributions 12:337-350
Valle IC, Buss DF, Baptista DF (2013) The influence of connectivity in forest patches, and
riparian vegetation width on stream macroinvertebrate fauna. Brazilian Journal of
Biology 73:231-238
Vander Laan JJ, Hawkins CP, Olson JR, Hill RA (2013) Linking land use, in-stream stressors,
and biological condition to infer causes of regional ecological impairment in streams.
Freshwater Science 32:801-820
Vannote RL, Minshall GW, Cummins KW, Sedell JR, Cushing CE (1980) The river continuum
concept. Canadian Journal of Fisheries and Aquatic Sciences 37:130-137
Victor R, Ogbeibu AE (1991) Macroinvertebrate communities in the erosional biotope of an
urban stream in Nigeria. Tropical Zoology 4:1-12
Wallace JB, Eggert SL (2009) Benthic invertebrate fauna, small streams. Encyclopedia of inland
waters 2:173-190
Walsh CJ, Roy AH, Feminella JW, Cottingham PD, Groffman PM, Morgan RP II (2005) The
urban stream syndrome: current knowledge and the search for a cure. Journal of North
American Benthological Society 24:706-723
72
Walsh CJ, Fletcher TD, Burns MJ (2012) Urban stormwater runoff: A new class of environmental
flow problem. PLoS ONE 7:e45814
Wang R, Xu T, Yu L, Zhu J, Li X (2013) Effects of land use types on surface water quality across
an anthropogenic disturbance gradient in the upper reach of the Hun River, Northeast
China. Environmental Monitoring and Assessment 185:4141-4151
Wenger SJ, Freeman MC, Fowler LA, Freeman BJ, Peterson JT (2010) Conservation planning for
imperiled aquatic species in an urbanizing environment. Landscape and Urban Planning
97:11-21
Yeo DC, Ng PK, Cumberlidge N, Magalhaes C, Daniels SR, Campos MR (2008) Global diversity
of crabs (Crustacea: Decapoda: Brachyura) in freshwater. In: Balian EV (ed) Freshwater
animal diversity assessment. Springer Netherlands pp. 275-286
Zar JH (1999) Biostatistical analysis. Prentice Hall International, New Jersey
Zeni JO, Casatti L (2014) The influence of habitat homogenization on the trophic structure of fish
fauna in tropical streams. Hydrobiologia 726:259-270
Zhang Y, Dudgeon D, Cheng D, Thoe W, Fok L, Wang Z, Lee JH (2010) Impacts of land use and
water quality on macroinvertebrate communities in the Pearl River drainage ba sin,
China. Hydrobiologia 652:71-88
73
Table 3-1 Mean (+ SE) of physicochemical and environmental parameters of the water in low, moderate and highly urban development
watersheds in Puerto Rico. Measurements were made per sampling site (n=3) in each watershed (n=3) during 24 hours in 2010–2011.
TDS
Watershed type Water Temperature (oC) % Dissolved Oxygen (mg L-1)
pH
Salinity (ppt)
(g L-1)
Low
Conductivity
26.1 ± 0.1
94.4 ± 0.5
7.3 ± 0.01 0.06 + 0.003
28.3 ± 0.1
97 ± 1
8 ± 0.01
27.5 ± 0.1
83.3 ± 0.5
***
***
(µS cm-1)
114.5 ± 2
0.04 + 0.001
0.2 + 0.003
361 ± 5
0.18 + 0.003
7.7 ± 0.01
0.2 + 0.003
357 ± 3
0.8 + 0.002
***
***
***
***
(Sabana)
Moderate
(Bayamón)
High
(Río Piedras)
ANOVA
NS- not significant at p = 0.05; * p < 0.05; ** p < 0.01;*** p < 0.001
73
74
Table 3-2 Mean decapod species density (+ SE) in the different watersheds of the low, moderate and high urban watersheds during 2010-2011.
Low urban
Moderate urban
High urban
Taxa
LRF
HRF
LRF
HRF
LRF
HRF
0
0
0
0
0.5+0.4
0.1+0.4
Macrobrachium faustinum
0.3+0.2
0.1+0.03
0.2+0.1
0.2+0.02
0.1+0.1
0.1+0.03
Xiphocaris elongata
0.8+0.1
0.6+0.3
0.3+0.2
0.5+0.3
0.003+0.002
0.02+0.02
0.0001+0.0001
0.01+0.01
0.001+0.001
0
0
0.002+0.002
0.2+0.1
0.2+0.1
0.3+0.2
0.1+0.1
0
0
0.04+0.03
0.03+0.02
0.1+0.1
0.03+0.03
0
0
0.7+0.2
0.7+0.3
0.001+0.001
0.1+0.1
0
0
0.01+0.01
0.01+0.01
0
0
Atya lanipes
0.3+0.2
0.3+0.2
0
0.2+0.2
0
0
Potimirim mexicana
0.1+0.1
0.02+0.01
0
0.01+0.01
0
0
Sesarma roberti
0
0
0
0.001+0.001
0
0
Macrobrachium carcinus
0
0.003+0.003
0
0
0
0
0.06+0.06
0
0
0
0
0
Palaemon pandaliformis
Epilobocera sinuatifrons
Atya innocuous
Atya scabra
Micratya poeyi
Macrobrachium acanthurus
Potimirim glabra
0.002+0.001 0.004+0.004
74
75
Fecundity
Species
Regression Equation
Min Mean (SE)
R2
F
0.8
197
p
N
Max
Atya innocuous
25
360 (40)
1256 FEC = 103.4 CL – 784.5
Micratya poeyi
12
65.9 (3)
153
FEC = 19.2 CL – 24.3
0.13 10.6 *** 75
Xiphocaris elongata
55
228 (13)
446
FEC = 42.6 CL – 205.7
0.5
42.2 *** 50
Macrobrachium faustinum
16
179 (42)
827
FEC = 72.26 CL - 331.1
0.5
19.4 *** 25
Atya innocuous
132
1321 (206) 6587
FEC = 352.4 CL – 3812
0.9
310
Micratya poeyi
32
70.6 (5.3)
FEC = 20.27 CL – 24.07
0.2
6.1
*** 43
Moderate
Low
Watershed
Table 3-3 Minimum, mean (+ SE) and maximum number of embryos per female, regression equations showing relationship between female size
(CL) and fecundity (FEC) for each land use section in the Low, Moderate, and High impact watersheds during the wet season.
154
*** 50
*
25
75
76
Xiphocaris elongata
54
147 (19)
413
FEC = 60.3 CL - 403.8
0.5
22.2 *** 25
Macrobrachium faustinum
47
98 (8)
258
FEC = 7.5 CL – 39.8
0.2
7.3
Macrobrachium faustinum
96
302 (33)
601
FEC = 52.61 CL - 151.3
0.5
17.1 *** 19
Palaemon pandaliformis
12
49 (3)
91
FEC = 23.4 CL -68.1
0.6
34
High
**
76
*** 43
NS- not significant at p= 0.05; * p < 0.05; ** p < 0.01;*** p < 0.001
76
77
Río Piedras
Cu
L
Río
Bayamón
Río Sabana
Ci
L
Puerto Rico
Fig. 3-1 Location of the Low (Río Sabana), Moderate (Río Bayamón), and Highly urban (Río
Piedras) watersheds of the studied streams in the north coast of Puerto Rico. The gray area
represents El Yunque National Forest; closed circles- the sampling sites (low, medium and high
elevation), horizontal bar – large dam with a vertical wall, open left triangle- small dam with
acute vertical wall, and the closed left triangle- small broken dam. CiL represents Cidra Lake and
CuL- Las Curias Lake.
78
100
Percentage of Land Use Cover
80
High-density urban development
60
Grasslands and pastures
Secondary Forest
Low-density urban development
Artificial barrens
Mangrove forest
40
Freshwater
Riparian forest
Mature primary Tabonuco, Palo Colorado, Sierra
20
0
Low
Moderate
High
Watershed
Fig. 3-2 Comparison of predominant land use/land cover groups among watersheds (Low, Moderate, and High urban development).
Watersheds analyses include all the area from the headwaters to the mouth of the streams.
78
79
Low Rainfall
High Rainfall
***
7
NS
5
4
3
NS
2
1
Shannon-Weiner Diversity Index (H')
NS
6
Species (S)
***
1.6
0
1.4
NS
1.2
NS
1.0
0.8
0.6
NS
0.4
0.2
0.0
NS
1.0
***
2.5
NS
Evenness (J)
0.6
NS
0.4
0.2
0.0
Decapod Density (LN X + 1)
NS
0.8
2.0
NS
NS
1.5
NS
1.0
0.5
0.0
Low
Moderate
Watershed
High
Low
Moderate
High
Watershed
Fig. 3-3 Mean (+ SE) species number (S) a), Shannon-Weiner Diversity Index (H’) b), Evenness
(J) c), and Density d) of the freshwater decapod communities for each watershed (Low-Sabana,
Moderate-Bayamón and High-Río Piedras urban categories) during the rainfall season (HRFHigh Rainfall and LRF-Low Rainfall). Closed bar- HRF, open bar- LRF, Horizontal line over the
bars represents the nested Anova test differences among streams/ urban intensity categories. NSnot significant at p = 0.05; * p< 0.05; ** p<0.01; *** p< 0
80
Fig. 3-4 Nonmetric multidimensional scaling (NMDS) results from ordination of decapod family densities.
Stream habitat variables measured at the different sampling sites (LU-Low Urban-Sabana, MU-Moderate
Urban-Bayamón and HU-High Urban- Río Piedras)(1-Headwater, 2-mid elevation, and 3- river mouth
sampling sites) are plotted as vectors. Vector length and direction reflects strength and direction of
relationship between the stream habitat variables (Disch- discharge, Omatter-Organic matter in the stream,
%Pcov- %Pool cover, %Rcov- % Riparian cover, %SI- % Substrate Index, Mdepth- Maximum depth,
Pvol- Pool volume,Parea- Pool area) and decapod family densities (Palaemonidae, Atyidae,
Xiphocarididae, and Pseudothelphusidae). Stress value = 0.04; Axis 1 R2 = 0.79 and Axis 2 R2= 0.03.
81
Low Urban
Moderate Urban
180
High Urban
7000
a)
160
b)
6000
140
5000
120
100
4000
80
3000
60
2000
40
1000
20
0
0
3
4
5
6
7
500
5
10
15
20
25
30
1000
d)
c)
Fecundity
35
400
800
300
600
200
400
100
200
0
0
7
8
9
10
11
12
13
14
15
4
6
8
10
12
14
16
18
20
Cephalothorax Length (mm)
100
e)
80
60
40
20
0
3
4
5
6
7
Cephalothorax Length (mm)
Fig. 3-5 Multiple regressions showing the relation between female cephalothorax length (mm)
and reproductive output. a) Micratya poeyi; b) Atya innocuous, c) Xiphocaris elongata, d)
Macrobrachium faustinum, and e) Palaemon pandaliformis in the Low (closed circle), Moderate
(open circle) and High (closed inverted triangle) urban watersheds. Regression lines: Straight lineLow Urban, Dashed line- Moderate Urban, and Dotted line- High Urban streams.
82
3000
2500
0.25
Shrimp Larvae
Discharge
a)
0.24
0.23
2000
0.22
1500
0.21
1000
0.20
500
0.19
0.18
0.64
3000
2500
b)
Shrimp Larvae
Discharge
0.62
2000
1500
0.60
1000
0.58
500
0
0.56
1.00
3000
2500
Shrimp Larvae
Discharge
c)
0.95
2000
0.90
1500
0.85
1000
0.80
500
0.75
0
23:00:00
0.70
07:00:00
15:00:00
23:00:00
Time (HH:MM:SS)
Fig. 3-6 Mean (+ SE) larvae drift densities and discharge in 24-hour (H-hour, M-minutes, Sseconds) sampling period in the Low (Sabana) (a), Moderate (Bayamón) (b) and in the High (Rio
Piedras) (c) urban watersheds. The larvae density and discharge were collected near the estuary
in each stream. Solid lines represent the discharge and the closed circle, open circle and closed
inverted triangle represent mean (+SE) larvae drift in the studied watersheds.
Discharge (m3 s-1)
Mean larvae density + SE (larvae m -3)
0
83
CHAPTER 4
COMPARISON OF TROPHIC RELATIONSHIPS IN CONTRASTING TROPICAL STREAMS
IN PUERTO RICO3
Summary
1. In tropical islands, urbanization occupies a large percentage of land use along streams and
rivers and strongly affects the biota and habitat in them.
2. Clearing of riparian vegetation, increased impervious surface, and channelization results in
changes in water quality and quantity that affect the assemblage of the freshwater biota, and
the health and services of the ecosystem.
3. Stomach analysis and natural abundances of the stable isotopes δ 13C and δ 15N of shrimp,
fishes, snails, plants, and algae were used to determine the influence of anthropogenic
nutrients on food web dynamics in forested and urban tropical streams in Puerto Rico.
4. Primary production (biofilm, algae and plant detritus of terrestrial origin) showed distinct δ 13C
signatures, which provided a clear discrimination of carbon sources. The C-sources for the
primary, secondary and tertiary consumers were similar among streams; enrichment with 15N
was observed in the urban streams. δ 15N values for all food web components varied
significantly among streams.
5. These results demonstrate the importance of organic matter and the dependence of freshwater
biota on terrestrial inputs.
Keywords Stomach content, Atya, Xiphocaris elongata, Macrobrachium, food web
3
Coauthored by Omar Pérez-Reyes, Todd A. Crowl, and Alan P. Covich
84
Introduction
Streams in islands constitute one of the freshwater sources for the people living in these
islands, in some cases the only source of freshwater. Similar to continental counterparts, streams
in islands have been impacted by urbanization and the health of the ecosystem has been degraded.
In these locations, the effects of urban development (Urban Stream Syndrome: Walsh et al.,
2005) tend to impact the whole ecosystem due to the low order and small size streams. Islands
have restricted options when developing their freshwater resources. Many islands are vulnerable
to extreme climatological periods of heavy/low rains, contamination, saline intrusion, and soil
erosion; but the freshwater biota in the islands consists of species adapted to exploit these
hydrological and environmental conditions.
In tropical islands, urbanization occupies a large percentage of land use along streams
and rivers and strongly affects the biota and habitat in them (e.g. urbanization in Puerto Rico
represent 10% of the land use). Removal of the riparian vegetation, increased of impervious
surface, channel destabilization and widening results in an increased in water pollution (changes
in ionic concentrations, inputs of toxins, wastewater discharge, increase in water temperature,
increase in sedimentation and suspended solids, and reduce of oxygen concentrations) which is
recognized as the main problem in tropical streams (Ramírez et al., 2012). Density, diversity and
assemblages of the freshwater biota change with an increase in water pollution in the streams.
Studies in urban streams have demonstrated that some groups of macroinvertebrates are sensitive
to pollution and had been replaced by tolerant taxa. The aquatic insect taxa (de Jesus-Crespo &
Ramírez, 2011), ostracods (Hartland et al., 2011), annelids and flaworms (Pinilla 2010), and
shrimp (personal observation) seem to be the most impacted by urbanization and water pollution
in tropical urban streams.
Similar to other tropical countries, Puerto Rico went through an intensive agriculture that
took place in the watersheds of all the streams. During the second half of the 20th century, the
85
economy of the island changed from agriculture to industrialize as result of the intervention of the
local government. New urban settlements were developed near the main cities and the natural
resources were endangered or extirpated. The infrastructure in the cities did not grew as the same
rate of the houses and buildings then problems with water distribution, and wastewater are visible
everywhere. Then fertilizers and sewage effluents, sources of nutrients and particulates of
organic matter, invade the freshwater systems of the island with the results of a disruption in the
natural nutrient balance and alteration the biota assemblages in the urban streams.
Four families of decapods (Atyidae, Palaemonidae, Pseudothelphusidae and
Xiphocarididae), fish (Eleotridae, Gobiidae, Anguillidae, and Mugilidae), and snails (Neritidae)
compose the freshwater endemic biota in the Caribbean (Covich & McDowell, 1999; Debrot,
2003; Coat et al., 2009). Most of the members in these families present an extended life cycle
that included two aquatic environments, as adult, in the freshwater system and as larvae short
time in the ocean. Shrimp, snails, and river gobies are diadromous species which reproduce in
the headwaters where they release planktonic larvae that are transported by the water to the
estuary where they go through a serial morphological changes in order to reach the
metamorphosis stage, then a juvenile is formed and the upstream migrations began (Bell et al.,
1995; Blanco & Scatena, 2005; Bauer, 2011 a; 2011 b; 2013). Big mouth and Cheek spiny
sleepers, mountain mullets, and eels are catadromous. These migration patterns play an important
role in the longitudinal distribution of the species as well in the use of different types of marine
and freshwater resources (Coat et al., 2009; 2011). Similar to their counterpart in the continents
(e.g. salmons), these migrations provide an exchange of nutrients between the stream and the
ocean (Kohler et al., 2013; Reisinger et al., 2013). In the tropics, the lower valleys and sections
near the river mouth received a direct impact from the marine environment and these areas are
preferred by some representative species of shrimp (Macrobrachium acanthurus, Jonga serrei),
crabs (Callinectes and Sesarma), and fish (Eleotris perniger and Gobiomorus maculatus). In
86
addition, these localities host juveniles of shrimp, fish, and snails in their travel to the upper parts
of the stream. During the migrations these animals are exposed to different environmental
conditions, and variable sources of nutrients (March and Pringle 2003; Coat et al., 2009; 2011).
Migratory fauna has shown important roles in the food webs in the tropics as filter feeders,
scrappers, shredders, and predators (Brasher et al., 1997; Covich & McDowell, 1996; McDowall,
2003; March & Pringle, 2003).
We studied the fish and decapod communities in three watersheds that represent a
gradient of urbanization in Puerto Rico in order to propose and compare food webs, estimated the
relative importance of the food sources supporting them, and determined the trophic positions of
their dominant species. These comparisons are of great relevance and interest because urban
streams are surrounded by an extensive gradient of urbanization in contrast to forested or low
impacted streams, which are rarely exposed to urban stressors. We hypothesized that the effects
of anthropogenic stressors on freshwater biota would be less dramatic in forested streams
compared with urban ones. How the food web structures change with increased levels of
disturbance?
Methods
Site selection and classification.
Three streams that represent different conditions of human impact in Puerto Rico were
used to conduct this study. The Sabana, Bayamón and Rio Piedras watersheds were classified as
low (LUW), moderate (MUW) and high (HUW) urban watersheds based on the percentage of
land use. These classifications were based on the results obtained by the Puerto Rico Gap Project
(Gould et al., 2008). On each stream, nine, 10 m reaches were selected to collect organisms and
the physico-chemical data. The sampling reaches were distributed along a longitudinal gradient
of elevation from the river mouth to the headwaters.
87
Río Sabana (low urban watershed- LUW) is located in the northeastern portion of the
Luquillo Experimental Forest. In the headwaters, the annual mean precipitation can reach the
3250 mm year-1, whereas in the coast, the precipitation can range up to 2616 mm year-1 (Scatena,
1989; Zou & Gonzalez, 1997; Quiñones & Torres, 2005). This stream has a mean annual
discharge of 13.1 m3 s-1 · km2, and an annual mean temperature of 25°C (Brown et al., 1983).
The headwaters of this stream are protected by the National Forest Service of the U.S.
Department of Agriculture (28,000 ha). The Puerto Rico government, through the Puerto Rico
Environmental and Natural Resources Department, protect the mid-elevation and coastal valleys
(approximately 1083 ha). The headwaters of the Sabana stream are dominated by primary forests
of Tabonuco, Palo Colorado and Sierra Palm. Native trees and exotic grasses are the most
common plants in the watershed.
Río Bayamón (moderate urban watershed- MUW) has a medium influenced basin due to
human activities in its watershed and riparian zones. Estimates show that 22% of this basin had
been affected by human activities (Ortíz-Zayas et al., 2004; 2006). This river is one of the largest
rivers of the island and its watershed comprised by six municipalities (Toa Baja, Cataño,
Bayamón, Guaynabo, Aguas Buenas, and Cidra) and several tributaries. The headwaters are
located in the Cordillera Central at an elevation of 500 m above sea level (asl). The land cover
for the Bayamón stream consisted of secondary forests and grasses those dominate sub-urban and
urban land use reaches. The mean annual precipitation in the watershed ranges between 1854 to
1625 mm year-1 (Quiñones & Torres, 2005) and the mean annual discharge is 1.13 m3 s-1. The
Río Bayamón has three dams (Los Filtros-Guaynabo, San Juan Dam-Aguas Buenas, and Cidra
Reservoir Dam-Cidra) and a reservoir (Cidra Reservoir) that provides water to the metropolitan
area (Ortíz-Zayas et al. 2004, 2006; Quiñones and Torres 2005). San Juan Dam a concrete
gravity-arch structure with a vertical wall of 50 feet hight constitutes an impediment in the
upstream migration.
88
The Río Piedras (high urban watershed- HUW) has several tributaries, and flows through
San Juan City (with a population density of 3200 people km-2). The watershed is located in the
center of the metropolitan area and is the most urbanized watershed with more than a 60% of
urban cover (Ortíz-Zayas et al., 2004; 2006; de Jesus & Ramírez, 2011). The headwaters are
located in the southern part of the San Juan municipality at the elevation of 70 masl where Las
Curias Reservoir is located. Río Piedras flows from Las Curias Reservoir through several
residential areas, and ends into the marine zone of the San Juan Bay. The mean annual disharge
for ver is 20.6 m3s-1 with a mean annual precipitation that range between 1879 to 1651 mm year-1
in the headwater and coastal valleys respectively (Quiñones & Torres 2005). The riparian
vegetation in this stream is characterized by native, exotic trees, and exotic grasses.
Animal samples
Adult individuals of shrimp, snails, and fish were collected for stomach and stable
isotopes analyses in the streams where the studies were done; during the high rainfall period of
2009 (June- November). All organisms were collected using a backpack electro shocker (Model
12-B Battery Powered Backpack Electrofisher, Smith-Root, Vancouver, Washington, USA). The
animal collections consisted of three upstream passes backpack electrofishing long pool that was
bounded by 6.4 mm mesh net to limiting the emigration of decapods and fish during sampling.
Hand nets were used to collect the organisms; macro-invertebrates and fish were transferred to
labeled plastic bags, preserved in ice, and identified in the laboratory. The reach sampled
included riffle, run, pool and the aquatic vegetation. Identifications were based Pérez-Reyes
(2013) and Erdman (1981).
Gut content analysis
Individuals of shrimp and fishes from the studied streams were collected for gut analysis.
The samples were preserved in 95% ethyl alcohol in the laboratory. Stomachs were dissected,
89
emptied in a Petri dish, diluted in 75% ethyl alcohol, and the content identified under a
stereoscope. The stomach content was separated and identified as: unicellular algae, filamentous
algae, coarse organic matter (> 1mm), seeds/spores, spicules, insects, spiders, shrimp/crabs, fish,
mollusk (snail), rotifers, and sand. Fine organic matter was present in all the stomach and was
removed from the analysis due to difficulties in the identification. Algae and animal parts were
identified to lowest taxonomic group using taxonomic keys available for each group.
Stable Isotopes samples
At the laboratory, shrimp were dissected and a section of the abdominal muscle (flexor
muscle) was removed, cleaned, preserved in ethyl alcohol (95%) and deposited in sterile
Eppendorf vials previously labeled. To collect tissue from the snail it was necessary to break the
shell and remove the foot. The epidermis and the operculum were removed from the foot before
preserving and placed in the labeled vial. The fish were dissected and a piece of the light muscle
tissue from the lateral side of the body was removed, cleaned and preserved. Approximately 2 g
of muscle tissue was removed from each organism and preserved prior to isotopic analysis.
Periphyton samples were collected from rocks in the streams; rock surface was scrapped using a
tooth brush and the sample collected with a dropper and deposited in Eppendefor vials. Leaves
and CPOM were collected directly from the stream, deposited in labeled sample plastic bags and
identified in the laboratory. We dried the samples at 60–75 °C for 24–48 h, ground them into a
fine powder with mortar and pestle, and packed them into acid-washed 5 mm × 8 mm tin capsules
for carbon and nitrogen isotope analysis.
The University of California Stable Isotope Facility performed all isotope analyses.
Carbon and N stable isotope ratios were determined on CO2 and N2 gases, produced by
combustion of samples in an elemental analyzer coupled to a continuous flow isotope ratio mass
spectrometer (ANCA-CFIRMS; Europa Scientific Crewe, England; ANCA combustion unit and
90
20–20 mass spectrometer). Stable isotope ratios are expressed in delta (δ) notation, defined as the
parts per thousand (‰) deviations from a standard material: δ13C or δ15N = ([Rsample·Rstandard –1] –
1) × 1000 where R = 13C/12C or 15N/14N. For C, the international standard is the Peedee
Belemnite (PDM) limestone formation; N, the standard is atmospheric N (AIR). Rsample and
Rstandard are the fractions of heavy to light isotopes in the sample and standard, respectively.
We used δ 13C and δ 15N stable isotope data to determine the energy source and trophic
position of shrimp relative to fish. Carbon and nitrogen stable isotope ratios (δ13C and δ15N) are
tracers of energy flow in aquatic food webs (Peterson & Fry, 1987; Fry, 1988; Pinnegar &
Polunin, 2000). There is typically a three- to four-fold increase in δ15N from prey to predator,
such that δ15N can be used to estimate consumer trophic position.
Estimation of trophic positions
The δ15N values of primary producers are highly variable; δ15N values of primary
consumers (shrimp, fish, and snails) were used as a baseline to estimate the trophic positions of
other consumers. The formula adheres to that of Cabana and Rasmussen (1996): trophic position
of consumers = [(higher level consumers δ15N − primary consumers δ15N)/3.4] + 2; where 3.4
represents an increment in δ15N per each increase in trophic position, and + 2 represents the
trophic position of primary consumers that is one position higher than primary producers, a basal
group counted as trophic position 1 (Vander Zanden & Rasmussen, 2001; Post, 2002; Leclerec et
al., 2013).
We expected that the carbon signatures of consumer organisms would be closely aligned
with their source of carbon. We do not present a mixing model applied to the data due to we
were unable to sample the source of algae, organic matter, and all the exotic fish species present
in the stream; these cases a mixing model would give anomalous results.
91
Statistical analyses
We compared the shrimp δ15N and δ13C values to the values of primary producers
(leaves, CPOM, and periphyton) and primary consumers (shrimp, fish and snails), to estimates
the food sources of shrimp, since isotopes values of primary producers indicate potential food
sources and primary consumers provide an isotope baseline for the food web (Post, 2002).
Biplots of δ15N and δ13C values for each species were used to compare patterns of isotopic
variation among streams. To view overlap of consumers, predators and preys in the bi-plot, we
only plotted δ15N and δ13C values of the animal species; the δ15N and δ13C values of the CPOM,
periphyton and plant species were removed from the comparison. One way ANOVAs were used
to compare the means of δ 13C and δ 15N of primary producers and consumers among streams.
Isotopic metrics of δ13C and δ15N were and the corrected stable isotope data were then used to
calculate the standard ellipse area (SEA) as measure of niche width for each species in each
treatment using the SIAR package in the R computing program. SEA is a bivariate measure of
the distribution of individuals in trophic space; each ellipse encloses 40% of the data and,
therefore, represents the core dietary niche, indicating typical resource use within a species or
population.
Results
Shrimp and fish stomach analyses. Moss, ferns, seeds/spores, wood, trichomes, roots and
leaves, filamentous (Chaetophora, Spirogyra, Oedogonium) and unicellular algae (Navicula and
other diatoms) constituted the main components in the shrimp stomachs. For the filter feeder
shrimp (Atya innocuous, A. scabra, and Micratya poeyi) these components represented the main
organic material in their stomach (Figs. 4-1a, b). Insect parts were identified in the guts of A.
scabra and A. lanipes but these represented less than 3% of the total of the total stomachs
analyzed. Palaemonids and xiphocarids showed more diverse stomach content than the atyids.
92
The organic material in their stomach were plant and algae (> 80%), and animal-derived matter
(insects, spiders, snails, ostracods, freshwater sponges, rotifers, and fish) (< 12%) (Figs. 4-1a, b).
Insects were the main prey for Macrobrachium faustinum; legs, mouth parts and claws were
found in the analyzed stomachs. Sand grains were found in stomachs of M. acanthurus, P.
pandaliformis, and A. lanipes (Figs. 4-1a, b).
Fish stomachs were constituted mainly by algae, CPOM, snails, insects, crabs, shrimp
and fish. Gobiomorus dormitor was the fish predator with a most rich diet. Sleepers feed on
snails, [Tarebia (Thiara) graniferea, Melanoides tuberculata, and Marisa cornuarietis] as well
on Sesarma crab, M. faustinum, poecilids, Eleotris perniger and juveniles of their own species.
Snails apparently constituted the most important source of nutrients for Agonostomus monticola,
G. dormitor, E. perniger, and the exotic Lepomis auritus. Stomach analyses for the Agonostomus
showed that this species had an omnivore diet that consisted on algae, snails, aquatic insects and
small fish; no shrimp were found in their guts. American eels were present in the streams but the
stomach analyses showed the presence of algae and plant organic matter.
Stable isotopes analysis. For all streams, shrimp and fish consumer taxa had δ13C
isotopes ratios heavier (higher δ13C values) than the mean of basal sources samples. In the LUW,
the δ13C for the producers ranged from -29.82‰ (Syzygium jambos) to -27.69‰ (periphyton),
ratios for primary consumer values ranged from -30.8‰ to -18.94‰ (X. elongata), and for
secondary consumer were distributed from -30.13‰ (M. faustinum) to -18.29‰ (A. rostrata)
(Fig. 4-2a; Table 4-1). The stable ellypsis analyses for the animal species in the LUW showed
three main groups: herbivores, omnivores and carnivores. The hervibore ellypsis grouped the
filter feeders (Atya) and the shredder (Xiphocaris elongata) but not the scrappers (Nereina and
Sycidium plumieri). The omnivore group was composed by the Macrobrachium species. The
predators group only included the sleepers (Eleotris and Gobiomorus).
93
In the MUW, primary producer showed a δ13C that ranged from -30.38 (Bambusa
vulgaris) to -27.24‰ (periphyton). Primary and secondary consumers showed ratios of δ13C that
ranged from -26.79‰ (A. scabra) to -19.23‰ (H. plecostomus) and -27.74‰ (G. dormitor) to 20.71‰ (G. dormitor) respectively (Fig. 4-2b; Table 4-1). The herbivore, omnivore and
carnivore groups showed overlapped ellyssis; but only the filter feeders and the predator fish had
a distinctive signature.
The HUW had δ13C mean values for producers that ranged between -31.33‰ (Bambusa
vulgaris) to -23.41(periphyton). The primary consumers had values from -29.52‰ (P.
pandaliformis) to -17.37‰ (P. pandaliformis) and secondary consumers showed values between 32.60‰ (A. rostrata) to -17.37‰ (P. pandaliformis) (Fig. 4-2c; Table 4-1). The δ 13C values for
CPOM samples in the studied streams revealed heavier δ 13C signatures in Sabana (-29.6‰) than
Rio Piedras (-31.33‰) and Bayamón (-30.15‰). Periphyton samples from Rio Piedras showed
heavier δ 13C (-24.7‰ + 0.5) in comparison with Sabana (-28.8‰ + 0.6) and Bayamón (-30‰ +
1.4). The herbivore, omnivore and carnivoure groups showed overlapped ellyssis.
All the shrimp species and some fish were identified as grazers based on the isotopes
analysis as well in the observations of vegetative organic matter in their stomachs. These grazers
included Atya lanipes, A. innocous, A. scabra, Micratya poeyi, Xiphocaris elongata,
Macrobrachium faustinum, M. acanthurus, Palaemon pandaliformis, Sicydium plumieri, and
Awaous taijasica. Other species identified as grazers were the native snail Nereina punctulata
(LUW = -22.4‰ + 1.5) and the exotic catfish Hypostomos plecostomus (HUW = -28.26‰; MUW
= -19.77‰ + 0.27). No significant differences were observed in the δ 13C signatures of the
shrimp species among the streams. The one-way ANOVAs’ for comparison of δ 13C signatures
among streams were significant for Gobiomorus dormitor (F2, 36 = 34.15, P < 0.0001) and
Anguilla rostrata (F2, 6 = 8.26, P = 0.04). Similar means in δ 13C signature for Gobiomorus were
94
found in the LUW -21.7‰ + 0.5 and the MUW -22.26‰ + 0.6; the HUW had a δ 13C mean value
of -27.46‰ + 0.5.
Trophic positions (TP) for the primary consumers collected in the LUW revealed that the
filter feeders (atyids), shredders and scrappers (snails and river gobies) had lower values (ranged
between 1-Nereina punctulata to 1.99- S. plumieri). Secondary consumers in these streams were
represented by M. acanthurus (TP- 2.9), M. faustinum (TP- 2.5), and A. rostrata (TP-2.9). The
tertiary consumers were represented by Gobiomorus dormitor (TP-3) and Eleotris perniger (TP3), and Anguilla rostrata (TP- 3). Organisms with heavier isotopes (δ 15N) in this stream were E.
perniger (δ 15N- 12.3), G. dormitor (δ 15N- 11.4), A. rostrata (δ 15N- 10.7), and M. acanthurus (δ
15
N- 10.7). Primary consumer species in the MUW had higher values in the TP in comparison
with the LUW; A. innocous (TP- 2.8), A. scabra (2.7), A. tajasica (3.7), H. plecostomus (2.7), S.
plumieri (3.9), and X. elongata (3.0). Secondary and tertiary consumers showed TP that ranged
between 1.6 (M. acanthurus) to 4.2 (E. perniger). The primary consumers at the HUW showed
TP that ranged between 2 (A. tajasica) to 4.4 (H. plecostomus) and the secondary and tertiary
consumers trophic positions were A. rostrata (TP - 2.3), G. dormitor (2.6), M. faustinum (2.9), A.
monticola (3), and E. perniger (3.3).
For the MUW and HUW the δ15N values were higher than the values obtained from the
reference stream. These values likely capture enrichment with nitrogen. Comparison of the δ15N
enrichments between the LUW and the MUW and HUW showed that the organisms from MUW
had higher levels of δ 15N than HUW. Atya innocuous (increment of 5.5), A. scabra (5.13),
Xiphocaris elongata (5.3), and S. plumieri (12.44) showed increments in δ 15N levels when were
compared with LUW. The secondary and tertiary consumers also had increments in δ 15N levels
(M. faustinum- 3.32, M. acanthurus- 0.91, A. rostrata- 3.5, and G. dormitor- 2.8). Organisms in
the HUW showed increments in the δ 15N levels in relation to LUW. Gobiomorus dormitor
(0.19), M. faustinum (1.9), X. elongata (0.4), and S. plumieri (9.0) had higher δ 15N levels in
95
comparison with the LUW but were lower than MUW. Significant differences in δ 15N signatures
among streams were found in Macrobrachium faustinum (F2,49 = 23.02; P < 0.001), Xiphocaris
elongata (F2,39 = 16.14; P < 0.001), Atya scabra (F1,26 = 132.47; P < 0.001), and Atya innocuous
(F1,27 = 227.9; P < 0.001). Urban streams showed higher values in δ 15N than the reference
stream. Significant differences in δ 15N signatures among streams were observed in Gobiomorus
dormitor (F2, 36 = 9.27; F < 0.001) and Anguilla rostrata (F2, 6 = 11.65; P = 0.021).
Discussion
Our results showed that δ15N values in the tissues of the freshwater shrimp and fish
varied remarkably among streams. Based in the position of the consumers relative to producers,
periphyton, CPOM, and allochthonous matter can be important sources of carbon to many
freshwater invertebrates and fish in the tropical streams. The stomach analyses observed in
shrimp suggested that the diets of these organisms are mainly composed of aquatic primary
producers (> 80%) (filamentous and unicellular algae) and allochthonous organic matter (CPOM,
seeds, spores); however regardless of the food item each group used and exploited the available
sources of nutrients in different ways.
This study suggests that filter feeders (Atya lanipes, A. scabra, A. innocous, and Micratya
poeyi) shared the same autochthonous carbon sources (Navicula, Oedogonium, Pinnularia,
Closterium, and Spirogyra) and allochthonous material (pollen, roots, trichomes, etc.). There
were no clear distinctions in δ 13C values of Atya from Sabana and Bayamón streams. Atyids
have modified chelipeds with a brush of bristles that use to filter the water column or scrape the
surface of the substrate in order to obtained organic matter. The bristles are armed with denticles
that facilitate the sweeping, scrapping, plucking, and capture the food from the substrate surface.
The stomachs of the atyids are adapted for the movements of fine particles into the gut than for
crushing or grinding (e.g. Macrobrachium) (Fryer, 1977; Felgenhauer & Abele, 1983; Bailey-
96
Brock & Brock, 1993). Hobbs and Hart (1982) and Fryer (1977) considered Atya lanipes as the
most ancestral shrimp among Atya (exploit the resources in two ways filter feeding and
scrapping) while A. scabra and A. innocous were considered the most specialized and
ecologically restricted species (Girard et al., 2013) due to their filter feeding habits. These types
of feeding can result in the consumption of large amounts of FPOM, filamentous, and unicellular
algae. These organisms change their feeding behavior from filter feeding to scrapping; this
permits the capture and incorporation of large amounts of CPOM in their diets.
The presence of insect parts in the stomach Atya suggests that these animals are not
selective in their food consumption. Previous studies (Pringle et al., 1993; March & Pringle,
2003) have shown that insects did not constitute an important aspect of the diet of Atya and only
represent less than 1% of the total stomach content. Apparently insects are captured by the bristle
in the periopods and incorporated as part of the food mass when the shrimp scrape a rock or plant
matter in the stream. The absence of larger amounts of CPOM and animal parts in the stomach of
Micratya poeyi was due to the size of shrimp. Micratya poeyi represents one of the smaller
members in the Atyidae family. This species reach a maximum body size of 3 centimeters and
their feeding consist in filtering the water column in the riffle to collect micro-organic particles.
Atyids constitute a carbon sources for palaemonids, crabs, eels, and sleepers (Chace & Hobbs,
1969; Covich & McDowell, 1996).
The shredder shrimp (Xiphocaris elongate) was reported in the three streams with mean δ
13
C values of -24.31‰ + 0.57 (LUW), -21.76‰ + 0.50 (MUW), and -22.58‰ + 1.23 (HUW).
Xiphocaris is likely a keystone species in Caribbean streams due to its role in the recycling and
decomposition of the organic matter. This species inhabits calm habitats close to the river banks
where detritus is abundant (March et al., 2001; March & Pringle, 2003; Coat et al., 2009).
Xiphocaris has tiny pincers that allow him to break down leaves in fine particulate organic matter
and capture small macro-invertebrates. These shrimp showed a diverse stomach content that
97
included unicellular and filamentous algae, fine and coarse organic matter (leaves, moss, wood,
trichomes) (Fryer, 1977; Covich & McDowell, 1996; Crowl et al., 2001), amoebas, insect parts
(March & Pringle, 2003), and micro-crustacea (ostracods). The fine particulate organic matter
produced as a result of the feeding of Xiphocaris became available to other consumers such as
filter feeding shrimp, snails, clams, fish and insects (Crowl et al., 2001; 2006). In addition,
Xiphocaris constitutes the source of carbon for other decapods (e.g. Macrobrachium and
Epilobocera) and native fish (e.g. Eleotris and Gobiomorus). Our study suggests no change in
food preferences and trophic position of Xiphocaris between reference and urban streams. This
corroborates the idea presented by Crowl et al. (2006) that suggested that Xiphocaris is highly
dependent on terrestrial carbon resources, especially native tree species as Cecropia, Dacryodes
and Manilkara.
Palaemonids are omnivores, and the isotopic signatures δ 15N positioned Macrobrachium
faustinum and M. acanthurus in the secondary or tertiary trophic levels. In tropical studies they
are classified as primary consumer in early stages and secondary or tertiary consumers when
adults (Covich & McDowell, 1996; March & Pringle 2003; Coat et al., 2009). Macrobrachium
faustinum, the most common and eurytopic freshwater shrimp, inhabits slow flowing rivers at low
elevation sites and fast flowing streams in mountain area (Girard et al., 2013). It has a diverse
diet compose of shrimp, snails, insects, spiders, crabs, fish, filamentous algae and detritus.
Macrobrachium acanthurus presents a limited distribution restricted to the lower valleys and
elevations near the estuaries. The stomach content of M. acanthurus consists of grass, seeds,
filamentous algae and insects; plants and organisms accessible in the urban reaches.
Macrobrachium spp. ingests larger pieces of organic material and some animal parts compared to
the finer particles in the guts of the atyids. They exploit a wide and diverse range of food items in
the streams. Palaemonids have very strong pincers that use to break and crunch the chitinous
exoskeleton of insects (Carvalho et al., 2011), crustaceans, and the shell of snails (Mantel et al.,
98
2004; Blanco & Arroyave, 2009) or fruits. Palaemonids constitute an important component in the
diet of other shrimp, crabs, fishes, birds, and snakes.
The coupled analyses of gut content and stable isotopes demonstrated different feeding
strategies in the fish communities among the LUW, MUW, and HUW. The δ13C values for the
algaevores and detritivores Sycidium plumieri ranged between -22.6 to -26 ‰, compared to other
fish species. In LUW the δ 13C value for Sycidium was -22.6‰ closer to the scrapper snail
Nereina. These species feed on similar resources. The carbon signatures for this species from the
urban streams (MUW and HUW) relate it with the omnivorous and carnivorous fishes
(Oreochromis, Lepomis and Gobiomorus). Sycidium derived their carbon nutrients from the algae
and desmids scraped from the substrate surface (Gillet, 1983). Its mouth parts are adapted to
grazing slime algae (desmids) that grow on the surface of rocks and stones in the fast-moving
water. The jaw of this fish has a ridge-like structure in the front which probably aids in scraping
algae off the rock surfaces, teeth will regularly be replaced so as to allow grazing and the
intestines are long and coiled to digest the vegetative organic matter (Erdman, 1961; 1986; Keith,
2003; Maie et al., 2008). Similar results were observed in S. punctatum by Gillet (1983), but
differ from the observations done by Maciolek (1977) in the sibling species Lentipes concolor.
Lentipes can change its diet from herbivore to carnivore when the goby increase in size. Awaous
tajasica and Agnostomus monticola were classified as omnivores. Isotopic similarities between
consumers with different feeding strategies suggest similar food sources. Studies with sibling
species of Awaous showed that the diet of these gobies consisted on filamentous algae, diatoms,
and insects (Ego, 1956; Sabino & Correa, 1990; Kido et al., 1993; Watson, 1996; Kido, 1997;
Debrot, 2003). Isotopic signatures and gut analysis of Agonostomus monticola identified this fish
as an omnivorous. In our study the isotopic values δ 13C placed this planktonic fish with the
benthic species G. dormitor and H. plecostomus; this supports the idea of a mixed diet. Studies
from Costa Rica (Winemiller, 1983), Honduras (Cruz, 1987; Matamoros, personal
99
communication), Jamaica (Aiken, 1998), Mexico (Torres-Navarro & Lyons, 1999), Trinidad
(Phillip, 1993), Puerto Rico (Ramírez, personal communication), and the United States (Loftus et
al., 1984) characterized Agonostomus monticola as omnivore fish. Aiken (1998) and CottaRibeiro and Molina-Ureña (2009) supported the idea of omnivory because the mountain mullet
changes its diet from insectivorous (juveniles stage) to herbivores when adult (leaves and
filamentous algae). Also with the change in diet an increase in the length of the intestine has
been observed.
The carnivorous guild was represented by benthic consumers. Eleotris, Gobiomorus, and
Anguilla constitute the top freshwater predators in these streams. The feeding behaviors, stomach
content analyses, and the δ 13C signatures for these species reveal diets that consist primarily on
snails, shrimp, fish, insects, and some plant detritus. Eleotris, Gobiomorus and Anguilla are
benthic fishes with a sit-and-wait behavior to capture their slow moving prey (shrimp, small
sleepers, and snails). Variation in the isotopic signal can be the result of a mixed diet or an
ontogenic shift in prey utilization. Bacheler et al. (2002; 2004) reported changes in diet between
juveniles and adult sleepers. Small individuals (< 100 mm) prefer insects, plankton, and
ostracods while larger bigmouth sleepers (> 200 mm) feed on fish and crabs. These studies
differed markedly with the results from Nordlie (1981) and Winemiller and Ponwith (1998) that
reported a diet based mainly on shrimp. Our results support the idea of a mixed diet in bigmouth
sleepers. Eleotris perniger feed on Tarebia (Thiara) granifera and Marisa cornuarietis snails
(shell lengths > 10 mm), which in some occasions seemed disproportionate in size for ingestion
and by the number of snails in the gut. These observations in Eleotris spp. agree with the reports
from Brazil (Teixeira, 1994), Costa Rica (Nordlie, 1979; 1981; Winemiller & Ponwith, 1998),
and Japan (Suzuki & Senou, 1981; 1982; Maeda & Tachihara 2004). The stomach analyses for
Eleotris showed that the introduced melanoid snails constitute the first source of nutrients for this
fish. There no clear idea about how Eleotris got the nutrients from the snails due to all the snails
100
in the stomach and gut had unbroken shells, operculum closed and the internal body been
complete. This might suggest that the spiny sleeper ingests snails but derive the nutrients from
the algae that grow in the external surface of the shell. The stomach contents of Anguilla rostrata
observed in this study were congruent with previos analyses done by Ogden (1970), Wenner &
Musick (1975), Waldt et al. (2012). These studies showed that Anguilla has a diet based in
bottom organisms and its change as the animal grows. In juvenile stages, the stomachs reflect the
presence of insects while adults consumed mostly crustaceans and fishes.
The description of the overall feeding relationships of the dominant species in the
reference and urban streams in Puerto Rico were developed by integrating the stomach content
data and the isotope data described in this study. The food web described for the LUW contains
four trophic positions moving carbon from the primary producer (periphyton, CPOM, vegetative
matter) through three or four trophic levels occupied by omnivorous and carnivorous fishes. In
this food web algaevores fish (S. plumieri), freshwater snail (N. punctulata), filter feeder atyids
(Atya and Micratya) and the shredder shrimp (X. elongata) consume CPOM, debris, and leaves at
the TP 2 or close to 2 (herbivores). Vegetative organic matter is incorporated by adults of M.
faustinum, which are consumed by larger palaemonids (M. acanthurus), and the American eel (A.
rostrata) (omnivores). Macroinvertebrates and some juvenile fishes are consumed by predatory
fishes (E. perniger and G. dormitor) in TP 4 (carnivores). The primary and secondary omnivore
consumers obtain their carbon directly from the periphyton, CPOM and allochthonous sources.
Then the carbon is transported from macroinvertebrates (juvenile shrimp and crabs, and snails) to
macroinvertebrates (adult shrimp and crabs) and fishes, which in turn are eaten by top consumers
(predatory fishes).
In the urban streams the absence of important components of the food web (i.e. filter
feeders) and the addition of new predators resulted in changes in the trophic levels and guilds. In
the medium impact stream of Bayamón the number of animal species and the carbon sources
101
available were similar to the reference stream. The shrimp community in the highly impacted
stream decreased (from 12 species to 4) in comparison with the middle and reference streams.
The variation in δ 13C for Gobiomorus dormitor and Anguilla rostrata can be related with the
carbon sources available in each stream and the ontogenic shift of the species (Waldt et al.,
2013). The animal communities in the LUW and MUW were similar in contrast to HUW. In the
highly impacted watershed the absence of filter feeder shrimp and the lower number of
palaemonids and xiphocarids suggest an increase of inter and intra specific predation in the fish
community. This behavior was observed in the stomachs analyses of Gobiomorus and Anguilla
where larger individuals fed on smaller. The nonexistence of filter feeder shrimp in the HUW
redounded in the accumulations of FPOM and sedimentation. The accumulation of fine
particulate and the incorporation of human derived organic matter reduce the surface available for
insects, algae, plants and other organisms that use substrates for attachments. In this stream, the
absence of atyids represented the change in diets for Xiphocaris elongata and Macrobrachium
faustinum. Xiphocaris elongata changed the preferred carbon sources CPOM and filamentous
algae to unicellular and filamentous algae. Macrobrachium faustinum also diversified their diets.
In the reference stream it was based on CPOM, unicellular and filamentous algae, but in the
highly urban stream incorporated animal-derived material (spiders, sponges, insects, seeds, and
micro-crustaceans).
The presence of exotic fish species (e.g. Cichla ocellaris, Lepomis auritus, Oreochromis
mossambicus, Micropterus salmoides) may result in alterations on the food web. These species
were introduced by the government as game fishes and biological control of invasive snails,
parasites and insects. The incorporation of piscivores and omnivores fishes to the freshwater
ecosystem represents an alteration of a balanced food web due to an overlap with the diet of the
native G. dormitor (Bacheler et al., 2004).
102
Animals in the medium and highly impacted streams had higher δ 15N values than the
reported in the reference stream. An increase in δ 15N stable isotope ratios in primary producers
in the urban streams suggests the influence of wastewater or fertilizers into the stream water that
might be related with changes in land use in the watersheds (Potter et al., 2013). The increase in
δ 15N of the primary producers is passed on to consumers in the food webs of these streams.
Consumers from MUW and HUW had higher δ 15N signatures than their counterparts in the
reference stream of LUW. There are no discernible correlations between feeding mode and the
magnitude of difference in δ 15N signatures between streams. Previous studies (Chang et al.,
2002; Houhou et al., 2010; Bucci et al., 2011; Winemiller et al., 2011) reported that higher levels
in δ15N have been associated to inputs of fertilizers and sewer waste in the rivers, mangrove, and
costal zones. The land use in MUW is mostly private (99.9%) and only 0.1 % is on government
hands (Gould et al., 2008). The urban and sub-urban developments constitute 30% of the land
use and the remaining are forest, grasslands, wetlands, and agriculture lands. Municipalities
those share the watershed of this stream used more than 40% of their lands as croplands and
livestock lands which represent an increase in fertilizers and manure that reach the stream
(Census of Agriculture, 2007). Ramos-Gines (1997) estimated that the amount of nitrogen that
enter and leave the Rio Bayamón Reservoir was 18,863 kg/year and 8,600 kg/year respectively;
most of the nitrogen inputs came from surface-water runoff (agricultural area- 9,780 kg/yr,
forested area- 1900 kg/yr) and urban areas (sewered- 591 kg/yr; unsewered 2,280 kg/yr).
The HUW has a smaller watershed area than MUW, but a larger proportion of the
watershed is urbanized. The water quality varies by location and season, and receives both point
and nonpoint sources of pollution that occurs upstream. This pollution contributes excessive
nutrient and contaminants in the lower valleys and the estuary resulting in eutrophication and
biomagnifications problem in animals (crabs, mussels, fishes) (Webb & Gómez-Gómez, 1998;
Delgado-Morales et al., 1999). Point and nonpoint pollution in combination with other effects of
103
urban land use have a direct impact on sensitive aquatic biota resulting in changes in the food
web (Walsh et al. 2005; Wenger et al. 2009; Kininkova 2012).
Urban streams located in cities near the metropolitan areas tend to be impacted directly or
indirectly by human activities. Higher enrichment of δ 15N may occur with high Nitrogen loading
in streams from human activities and illegal wastewater discharge. The species present in the
urban streams showed higher levels of δ 15N in their tissues than records that have been reported
for pristine streams. Previous studies that have examined the influence of wastewater inputs to
rivers, reservoirs and estuaries have also reported enriched δ 15N in primary producers,
macroinvertebrates and fish (McClelland et al., 1997; 1998; Piola et al., 2006; Eitzman &
Paukert, 2009; Xu & Zhang, 2012). In this study δ 15N enrichments were evident in the primary
(Xiphocaris elongata and Sycidium plumieri), secondary (Macrobrachium faustinum), and
tertiary consumers (Gobiomorus dormitor) of MUW and HUW. Also the periphyton and CPOM
were enriched with δ 15N. The primary consumers had the largest enrichments of δ 15N in their
tissues. The MUW and HUWs streams had the greatest input of anthropogenic δ 15N derived
from sewer and septic leakages (Quinones & Torres, 2005; Potter et al., 2010; 2013 de JesusCrespo & Ramírez, 2011; Personal observation) which discharge solid matter into the stream that
can be incorporated as source of nitrogen by the organism in the stream. Studies on δ 15N
signatures of the major sources of nitrogen (fertilizers and sewage) have shown that the nitrogen
derived from human activities (sewage) have a distinctive value δ 15N (range between 10 - 25‰)
than other sources which have values that are relatively low (-5 to 5‰). Previous studies also
concluded that the higher values in δ15N can be attributed to the fractionation process during the
ammonification and subsequent volatilization of nitrogenous waste products (Cabana &
Rasmussen, 1996). Nitrogen or related compounds can enter the stream water and being
assimilated by the phytoplankton and subsequently consumed and incorporated by
macroinvertebrates. Other studies correlate the amounts of δ 15N in the stream water with the land
104
use in the watershed and have shown a difference in δ 15N between forested and non-forested
streams. There do not appear to be differences between agricultural and urban catchments
however (Peipoch et al., 2012).
Based on our results, we concluded that there is significant variation in the food webs
among low, medium and highly impacted streams in Puerto Rico. The variations consisted
mainly in the amount of δ 15N. Carbon source for the primary, secondary and tertiary consumers
showed no differences. This demonstrates the importance of the organic matter in the ecosystem
and the dependence of the freshwater biota on the terrestrial inputs. Independent of human inputs
of Nitrogen, the aquatic organisms show the same dependence on carbon from allochthonous
inputs. Autochthonous and allochthonous inputs subside in the primary, secondary and tertiary
consumer directly or indirectly. Grazers and carnivorous use, or used these resources in different
ways throughout their life cycle. The urban food webs presented in this study represent a
generalized food web for urban streams in the tropics where the water pollution has an effect in
the freshwater biota. This research provides further evidence for the importance of anthropogenic
inputs on the organization of aquatic food webs. Excess in δ 15N results in significant differences
in trophic levels of the food webs from urban streams in comparison with the reference stream
where the anthropogenic inputs are minimal. The enrichment in δ 15N had an impact in all the
tropic levels by increasing the trophic position of all consumers and decreasing the differences
among feeding groups in terms of trophic level (Fig. 4-2). The urban rivers of Bayamón and Rio
Piedras have similar fish communities, riparian vegetation and have polluted waters (fertilizer and
wastewater). The amounts of δ 15N were higher than normal and in some occasions were three
times the values observed in the reference stream. This research further confirms the significant
impacts of human activities on stream and watershed health and services of the ecosystem. In
addition, we suggest that local authorities and researchers focus more on the management and
105
restoration highly impaired watersheds and make informed decisions about the wastewater
treatment.
Acknowledgments
We thank the people who joined us in the field for deployment, with special appreciation
to the fieldwork done by Francisco J. Pérez and José A. Rivera. This research was supported by
grants BSR-8811902, DEB 9411973, DEB 0080538, DEB 0218039, and DEB 0620910 from
National Science Fundation (NSF) to the Institute for Tropical Ecosystem Studies, University of
Puerto Rico, and to the International Institute of Tropical Forestry, United States Department of
Agriculture (USDA) Forest Service, as part of the Long-Term Ecological Research Program in
the Luquillo Experimental Forest. Also was supported by the San Juan- ULTRA Project (NSF
Grant 0948507). The USDA Forest Service and the University of Puerto Rico gave additional
support.
106
References
Aiken K.A. (1998) Reproduction, diet and population structure of the mountain mullet,
Agonostomus monticola, in Jamaica, West Indies. Environmental Biology of Fishes, 53,
347-352.
Bacheler N.M., Neal J.W. & Noble R.L. (2004) Diet overlap between native bigmouth sleepers
(Gobiomorus dormitor) and introduced predatory fishes in a Puerto Rico reservoir.
Ecology of Freshwater Fish, 13, 111-118.
Bailey-Brock J.H. & Brock R.E. (1993) Feeding, reproduction, and sense organs of the Hawaiian
anchialine shrimp Halocaridina rubra (Atyidae). Pacific Science 47, 338-355.
Bauer, R. (2011a) Amphidromy and migrations of freshwater shrimp. I. Costs, benefits,
evolutionary origins, and an unusual Case of amphidromy. In: Asakura A. (ed) New
Frontiers in Crustacean Biology. Proceedings of The Crustacean Society summer
meeting, Tokyo, 20-24 September 2009. Brill, Leiden, The Netherlands, pp 145-156.
Bauer, R. (2011b) Amphidromy and migrations of freshwater shrimp. II. Delivery of hatching
larvae to the sea, return juvenile upstream migration, and human impacts. In: Asakura A.
(ed) New Frontiers in Crustacean Biology. Proceedings of The Crustacean Society
summer meeting, Tokyo, 20-24 September 2009. Brill, Leiden, The Netherlands, pp 157168.
Bauer RT (2013) Amphidromy in shrimp: a life cycle between rivers and the sea. In: Wehrtmann
I.S. & Bauer R.T. (eds) Studies on Freshwater Decapods in Latin America. Latin
American Journal of Aquatic Research 41, 633-650.
Bell K.N.I., Pierre, P. & Brown J.A. (1995) Seasonal, inverse cycling of length-and age-atrecruitment in the diadromous gobies Sicydium punctatum and Sicydium antillarum in
Dominica, West Indies. Canadian Journal of Fisheries and Aquatic Sciences, 52, 15351545.
Blanco J.F. & Scatena F.N. (2005) Floods, habitat hydraulics and upstream migration of Neritina
virginea (Gastropoda: Neritidae) in northeastern Puerto Rico. Caribbean Journal of
Science, 41, 55-74.
Blanco-Libreros, J. F. & Arroyave-Rincón, A. (2009) Predator damage and shell size on the
diadromous snail Neritina virginea (Gastropoda: Neritidae) in the Mameyes River,
Puerto Rico. Revista de Biología Tropical, 57, 1069-1080.
Brasher A.M. (1997) Habitat use by fish ('o'opu), snails (hihiwai), shrimp ('opae) and prawns in
Two Streams on the Island of Moloka'i. Cooperative national park resources studies unit,
University of Hawai'i at Manoa. pp. 1-98.
Brown S., Lugo A.E., Silander S., & Liegel L. (1983) Research history and opportunities in the
Luquillo Experimental Forest. General Technical Report SO-44. New Orleans: US
Department of Agriculture, Forest Service, Southern Forest Experiment Station. pp. 1128.
107
Brown L.R., Gray R.H., Hughes R.M. & Meador R.M. (2005) Introduction to effects of
urbanization on stream ecosystems. American Fisheries Society Symposium, 47, 1-8.
Bucci J. P., Levine J. F., & Showers W. J. (2011) Spatial variability of the stable isotope (δ 15N)
composition in two freshwater bivalves (Corbicula fluminea and Elliptio complanata).
Journal of Freshwater Ecology, 26, 19-24.
Carvalho, D. A., Collins, P. A. & De Bonis, C. J. (2011) Gut evacuation time of Macrobrachium
borellii (Caridea: Palaemonidae) feeding on three types of prey from the littoral-benthic
community. Journal of Crustacean Biology, 31, 630-634.
Chang C. C., Kendall C., Silva S. R., Battaglin W. A., & Campbell D. H. (2002) Nitrate stable
isotopes: tools for determining nitrate sources among different land uses in the
Mississippi River Basin. Canadian Journal of Fisheries and Aquatic Sciences, 59, 18741885.
Clark J.J. & Wilcock P.R. (2000) Effects of land-use change on channel morphology in
northeastern Puerto Rico. Geological Society of America Bulletin, 112, 1763-1777.
Coat S., Monti D., Bouchon C., & Lepoint G. (2009) Trophic relationships in a tropical stream
food web assessed by stable isotope analysis. Freshwater Biology, 54, 1028-1041.
Coat S., Monti D., Legendre P., Bouchon C., Massat F., & Lepoint G. (2011) Organochlorine
pollution in tropical rivers (Guadeloupe): Role of ecological factors in food web
bioaccumulation. Environmental Pollution, 159, 1692-1701.
Cotta-Ribeiro T. & Molina-Ureña H. (2009) Ontogenic changes in the feeding habits of the fishes
Agonostomus monticola (Mugilidae) and Brycon behreae (Characidae), Térraba River,
Costa Rica. Revista de Biologia Tropical, 57, 285-290.
Covich A.P., & McDowell W.H. (1996) The stream community. In: Reagan D.P. & Waide R.B.
(eds) The Food Web of a Tropical Rain Forest. The University of Chicago Press,
Chicago, Ilinois, pp 433-459.
Crowl T.A., McDowell W.H., Covich A.P. & Johnson S.L. (2001) Freshwater shrimp effects on
detrital processing and nutrients in a tropical headwater stream. Ecology, 82, 775–783.
Crowl T.A., Welsh V., Heartsill-Scalley T., Covich A.P. (2006) Effects of different types of
conditioning on rates of leaf-litter shredding by Xiphocaris elongata, a Neotropical
freshwater shrimp. Journal of the North American Benthological Society, 25, 198-208.
Cruz G. A. (1987) Reproductive biology and feeding habits of cuyamel, Joturus pichardi and
tepemechín, Agonostomus monticola (Pisces: Mugilidae) from Río Plátano, Mosquitia,
Honduras. Bulletin of Marine Science, 40, 63-72.
Cummins K.W. & Klug K.W. (1979) Feeding ecology of stream invertebrates. Annual Review of
Ecology and Systematics, 10, 14-172.
108
de Jesus-Crespo R. & Ramírez A. (2011) Effects of urbanization on streams physicochemistry
and macroinvertebrate assemblages in a tropical urban watershed in Puerto Rico. Journal
of North American Benthological Society, 30, 739-750.
De Niro & Epstein S. (1981) Influence of diet on the distribution of nitrogen isotopes in animals.
Geochimica et Cosmochimica Acta, 45, 341-351.
Debrot A.O. (2003) A review of the freshwater fishes of Curacao, with comments on those of
Aruba and Bonaire. Caribbean Journal of Science, 39, 100-108.
Delgado-Morales D., Rodríguez C.J. & Jiménez D.B. (1999) Heavy metal evaluation in aquatic
organisms from the San José Lagoon. Center for Environmental and Toxicological
Research, Medical Sciences Campus-UPR. Report submitted to the Department of
Natural and Environmental Resources.
Ego K. (1956) Life history of freshwater gobies. Freshwater game fish management research.
Department of Land and Natural Resources. Territory of Hawai'i, Honolulu. Project No
F-4-R.
Engman A.C. & Ramírez A. (2012) Fish assemblage structure in urban streams of Puerto Rico:
the importance of reach-and catchment-scale abiotic factors. Hydrobiologia, 693, 141155.
Erdman D.S. (1961) Notes on the biology of the Gobiid fish Sicydium plumieri in Puerto Rico.
Bulletin of Marine Science of the Gulf and Caribbean, 11, 448-456.
Erdman D.S. (1986) The green stream goby, Sicydium plumieri, in Puerto Rico. Tropical Fish
Hobbyist, February, 70-74.
Ewel J. J. & Whitmore J. L. (1973) The ecological life zones of Puerto Rico and the Virgin
Islands. Institute of Tropical Forestry, San Juan, Puerto Rico. Forest Service Research
Paper ITF-18:1-72.
Felgenhauer B. E. & Abele L.G. (1983) Ultrastructure and functional morphology ff feeding and
associated appendages in the Tropical freshwater shrimp Atya innocuous (Herbst) with
notes on its ecology. Journal of Crustacean Biology, 3, 336-363.
Fry B. (1988) Food web structure on Georges Bank from stable C, N, and S isotopic
compositions. Limnology and Oceanography, 33, 1182-1190.
Fry B. (1991) Stable isotopes diagrams of freshwater food web. Ecology, 72, 2293-2297.
Fryer G. (1977) Studies on the functional morphology and ecology of the atyid prawns of
Dominica. Philosophical Transactions of the Royal Society, Series B: Biological
Sciences, 277, 57-129.
Gillet C. (1983) Les peuplements de poisons et de crevettes des rivieres de Guadeloupe: quelques
donnees sur la biologie, la reproduction, la repartition des especes. Revue
d’Hydrobiologie Tropicale, 16, 327-340.
109
Girard V., Monti D., Valade P., Lamouroux N., Mallet J. P., & Grondin H. (2013) Hydraulic
preferences of shrimp and fishes in tropical insular rivers. River Research and
Applications DOI: 10.1002/rra.2675
Gould W.A., Alarcón C., Fevold B. Jiménez M.E., Martinuzzi S., Potts G., Quiñones M.,
Solórzano M., & Ventosa E. (2008) The Puerto Rico Gap Analysis Project Volume 1:
Land Cover, Vertebrate Species Distributions, and Land Stewardship. pp. 1-165.
Hartland A., Fenwick G.D., & Bury S.J. (2011) Tracing sewage-derived organic matter into a
shallow groundwater food web using stable isotope and fluorescence signatures. Marine
and Freshwater Research, 62, 119-129.
Hobbs H.H. & Hart C.W. (1982) The shrimp genus Atya (Decapoda:Atyidae). Smithsonian
Contribution to Zoology, 264, 1-143.
Houhou J., Lartiges B. S., France-Lanord C., Guilmette C., Poix S., & Mustin C. (2010) Isotopic
tracing of clear water sources in an urban sewer: A combined water and dissolved sulfate
stable isotope approach. Water Research, 44, 256-266.
Keith P. (2003) Biology and ecology of amphidromous Gobiidae of the Indo-Pacific and the
Caribbean Regions. Journal of Fish Biology, 63, 831-847.
Kido M. H., Ha P. & Kinzie R.A.III. (1993) Insect introductions and diet changes in an endemic
Hawaiian goby, Awaous stamineus (Pisces: Gobiidae). Pacific Science, 47, 143-50.
Kido, M. H. (1997) Food relations between coexisting native Hawaiian stream fishes.
Environmental Biology of Fishes, 49, 481-494.
Kohler A.E., Kusnierz P.C., Copeland T., Venditti D.A., Denny L., Gable J., Lewis B.A., Kinzer
R., Barnett B., Wipfli M.S. (2013) Salmon-mediated nutrient flux in selected streams of
the Columbia River basin, USA. Canadian Journal of Fisheries and Aquatic Sciences,
70, 502-512.
Komínková D. (2012) The Urban Stream Syndrome a Mini-Review. Open Environmental and
Biological Monitoring Journal, 5, 24-29.
Loftus W.A., Kushlan J.A., & Voorhees S.A. (1994) Status of the mountain mullet in southern
Florida. Florida Scientist, 47, 256-263.
Maeda K. & Tachihara K. (2004) Instream dostributions and feeding habits of two species of
sleeper, Eleotris acanthopoma and Eleotris fusca, in the Teima River, Okinawa Island.
Ichthyological Research, 51, 233-240.
Maciolek J. A. (1977) Taxonomic status, biology, and distribution of Hawaiian Lentipes, a
diadromous goby. Pacific Science, 31, 355-362.
110
Maie T., Wilson M.P., Schoenfus H.L., & Blob R.W. (2008) Feeding kninematics and
performance of Hawaiians stream gobies, Awaous guamensis and Lentipes concolor:
linkage of functional morphology and ecology. Journal of Morphology, 270, 344-356.
March J., Benstead J., Pringle C., & Ruebel M. (2001) Linking shrimp assemblages with rates of
detrital processing along an elevational gradient in a tropical stream. Canadian Journal of
Fisheries and Aquatic Sciences, 58, 470-478.
March J.G, & Pringle C.M. (2003) Food web structure and basal resource utilization along a
tropical island stream continuum, Puerto Rico. Biotropica, 35, 84-93.
Mantel, S. K. & Dudgeon, D. (2004) Dietary variation in a predatory shrimp Macrobrachium
hainanense (Palaemonidae) in Hong Kong forest streams. Archiv für Hydrobiologie, 160,
305-328.
McDowall R.M. (2003) Hawaiian biogeography and the islands’ freshwater fish fauna. Journal of
Biogeography, 30, 703-710.
Minagawa M. & Wada E. (1984) Stepwise enrichment of 15N along food chains: Further evidence
and the relation between δ15N and animal age. Geochimica et Cosmochimica Acta, 45,
1135-1140.
Nordlie F.G. (1981) Feeding and reproductive biology of eleotrid fishes in a tropical estuary.
Journal of Fish Biology, 18, 97-110.
Ogden, J. C. (1970) Relative abundance, food habits, and age of the American eel, Anguilla
rostrata (LeSueur), in certain New Jersey streams. Transactions of the American
Fisheries Society, 99, 54-59.
Ortíz-Zayas J. & Scatena F. (2004) Integrated water resources management in the Luquillo
mountains, Puerto Rico: an evolving process. International Journal of Water Resources
Development, 20, 387-398.
Ortíz-Zayas J., Cuevas E., Mayol-Bracero O., Donoso L., Trebs I., Figueroa-Nieves D., &
McDowell W.H. (2006) Urban influences on the nitrogen cycle in Puerto Rico.
Biogeochemistry, 79, 109-133.
Pérez-Reyes O., Crowl T.A., Hernández-García P., Ledesma-Fusté R., Villar-Fornes F.A., Covich
A.P. (2013) Freshwater decapods of Puerto Rico: a checklist and reports of new
localities. Zootaxa 3717, 329-344.
Peterson B.J. & Fry B. (1987) Stable isotopes in ecosystem studies. Annual review of ecology and
systematic, 18, 293-320.
Phillip D. A. T. (1993) Reproduction and feeding of the mountain mullet, Agonostomus
monticola, in Trinidad, West Indies. Environmental Biology of Fishes, 37, 47-55.
Pinnegar J.K. & Polunin N.V. (2000) Contributions of stable-isotope data to elucidating food
webs of Mediterranean rocky littoral fishes. Oecologia, 122, 399-409.
111
Pinilla, G. (2010) An index of limnological conditions for urban wetlands of Bogota city,
Colombia. Ecological Indicators, 10, 848-856.
Post D.M. (2002) Using stable isotopes to estimate trophic position: Models, methods, and
assumptions. Ecology, 83, 703-718.
Potter J. D., McDowell W. H., Merriam J. L., Peterson B. J. & Thomas, S. M. (2010)
Denitrification and total nitrate uptake in streams of a tropical landscape. Ecological
Applications, 20, 2104-2115.
Potter J.D., McDowell W.H., Helton A.M. & Daley M.L. (2013) Incorporating urban
infrastructure into biogeochemical assessment of urban tropical streams in Puerto Rico.
Biogeochemistry, 1-16.
Pringle C.M., Blake G.A., Covich A.P., Buzby K.M. & Finley A. (1993) Effects of omnivorous
shrimp in a montane tropical stream: sediment removal, disturbance of sessile
invertebrates and enhancement of understory algal biomass. Oecologia, 3,1-11.
Quiñones F. & Torres S. (2005) Las Cuencas principales de Puerto Rico. Unpublished.
Ramírez A., Engman A., Rosas K.G., Pérez-Reyes O., & Martinó-Cardona D.M. (2012) Urban
impacts on tropical island streams: some key aspects influencing ecosystem response.
Urban Ecosystems, 15, 315-325.
Ramos-Gines O. (1997) Water balance and quantification of total phosphorus and total nitrogen
loads entering and leaving the Lago de Cidra, Central Puerto Rico. US Geological
Survey, Water-Resources Investigations Report 96-4222. San Juan, Puerto Rico. pp. 128.
Reisinger A.J., Chaloner D.T., Rüegg J., Tiegs S.D. & Lamberti G.A. (2013), Effects of spawning
Pacific salmon on the isotopic composition of biota differ among southeast Alaska
streams. Freshwater Biology, 58, 938–950.
Sabino J. & Corrêa e Castro R. M. (1990) Feeding biology, activity period and spatial distribution
of fishes in an Atlantic forest stream in southeastern Brazil. Revista Brasileira de
Biologia, 50, 23-36.
Scatena F.N. (1989) An introduction to the physiography and history of the Bisley Experimental
Watersheds in the Luquillo Mountains of Puerto Rico. U.S. Forest Service.General
Technical Report SO-pp 1-72.
Suzuki T. & Senou H. (1982) The inland water fishes of the Yaeyama Islands, Okinawa
Prefecture, Japan VI. Nanki-Seibutsu, 24, 12-18.
Teixeira R.L. (1994) Abundance, reproductive period, and feeding habits of eleotrid fishes in
estuarine habitats of north‐east Brazil. Journal of Fish Biology, 45, 749-761.
112
Torres-Navarro C.I. & Lyons J. (1999) Diet of Agonostomus monticola (Pisces: Mugilidae) in the
Rio Ayuquila, Sierra de Manantlan Biosphere Reserve, Mexico. Revista de Biologia
Tropical, 47, 1-7.
Vander Zanden M.J. & Rasmussen J.B. (2001) Variation in δ15N and δ13C trophic fractionation:
implications for aquatic food web studies. Limnology and Oceanography, 46, 2061-2066.
Waldt E. M., Abbett R., Johnson J. H., Dittman D. E., & McKenna, J. E. (2012) Fall diel diet
composition of American eel (Anguilla rostrata) in a tributary of the Hudson River, New
York, USA. Journal of Freshwater Ecology, 28, 91-98.
Walsh C.J., Roy A.H., Feminella J.W., Cottingham P.D., Groffman P.M., Morgan R.P.II. (2005)
The urban stream syndrome: current knowledge and the search for a cure. Journal of
North American Benthological Society, 24, 706-723.
Watson R.E. (1996) Revision of the subgenus Awaous (Chonophorus) (Teleostei: Gobiidae).
Ichthyological Exploration of Freshwaters, 7, 1-18.
Webb R.M.T. & Gómez-Gómez F. (1998) Synoptic survey of water quality and bottom
sediments, San Juan Bay Estuary System, Puerto Rico, December 1994 - July 1995.
Prepared in cooperation with the PR Environmental Quality Board and U.S.
Environmental Protection Agency for the San Juan Bay Estuary Program WRIR 97-4144,
pp. 1-69.
Wenger S.J., Roy A.H., Jackson C.R., Bernhardt E.S., Carter T.L., Filoso S., Gibson C.A.,
Hession W.C., Kaushal S.S., Martí E., Meyer J.L., Palmer M.A., Paul M.J., Purcell A.H.,
Ramírez A., Rosemond A.D., Schofield K.A., Sudduth E.B., Walsh C.J. (2009) Twentysix key research questions in urban stream ecology: An Assessment of the State of the
Science. Journal of the North American Benthological Society, 28, 1080-1097.
Wenner, C. A., & Musick, J. A. (1975) Food habits and seasonal abundance of the American eel,
Anguilla rostrata, from the lower Chesapeake Bay. Chesapeake Science, 16, 62-66.
Winemiller K. O. (1983) An introduction to the freshwater fish communities of Corcovado Río
National Park, Costa Rica. Brenesia, 21, 47-66.
Winemiller K.O. & Ponwith B.J. (1998) Comparative ecology of eleotrid fishes in Central
American coastal streams. Environmental Biology of Fishes, 53, 373-384.
Winemiller K.O., Hoeinghaus D.J., Pease A.A., Esselman P.C., Honeycutt R.L., Gbanaador D.,
Carrera E., & Payne J. (2011) Stable isotope analysis reveals food web structure and
watershed impacts along the fluvial gradient of a Mesoamerican coastal river. River
Research and Applications, 27, 791-803.
Zou X. & Gonzalez G. (1997) Changes in earthworm density and community structure during
secondary succession in abandoned tropical pastures. Soil Biology and Biochemistry, 29,
627-629.
113
Table 4-1 Feeding habits of the studied species based, the δ13C and δ15N values (mean + SE) and
the sample size of the macroinvertebrates and fish communities from the LUW, MUW, and HUW
(Sabana, Bayamón, and Rio Piedras).
Watershed
Mean δ13C
N
Mean δ15N
n
Ai
-24.79 + 0.11
20
6.31 + 0.19
20
Al
-24.89 + 0.17
20
6.44 + 0.26
20
Species
Code
Atya innocuous
Atya lanipes
Description
Herbivore
Atya scabra
As
-24.68 + 0.06
20
6.36 + 0.24
20
Micratya poeyi
Mp
-24.31 + 0.09
38
7.28 + 0.25
38
Ma
-22.46 + 0.91
5
10.71 + 0.34
5
-23.53 + 0.43
20
9.43 + 0.41
20
Macrobrachium
acanthurus
LUW (Sabana)
Omnivore
Macrobrachium
Mf
faustinum
Xiphocaris elongata
Xe
Herbivore
-24.31 + 0.57
31
7.57 + 0.31
31
Anguilla rostrata
Ar
Carnivorous
-18.97 + 0.35
3
10.69 + 0.32
3
Eleotris perniger
Ep
-22.36 + 0.63
2
12.28 + 0.48
2
-21.77 + 0.51
6
11.41 + 0.28
6
Carnivorous
Gobiomorus
Gd
dormitor
Sicydium plumieri
Sp
Herbivorous
-22.59
1
2.98
1
Nereina punctulata
Np
Herbivorous
-22.41 + 1.55
2
5.23 + 0.19
2
114
Periphyton
-28.25 + 0.55
2
9.08 + 2.4
2
CPOM
-29.58 + 0.16
3
3.01 + 0.55
3
-24.66 + 0.32
8
11.82 + 0.33
8
-25.02 + 0.48
8
11.5 + 0.25
8
Atya innocuous
Ai
Atya scabra
As
Xiphocaris elongata
Xe
-21.76 + 0.50
4
12.87 + 0.27
4
Ma
-21.07 + 0.17
3
11.62 + 0.24
3
Mf
-23.43 + 0.3
13 12.75 + 0.28 13
Awaous tajasica
At
-21.4
1
14.72
1
Sicydium plumieri
Sp
-25.48
1
15.42
1
-19.76 + 0.27
4
11.72 + 1.29
4
-23.29
1
15.59
1
-21.68 + 0.21
2
14.16 + 0.12
2
-21.6 + 0.33
4
12.77 + 0.41
4
Herbivore
Macrobrachium
acanthurus
Omnivore
MUW (Bayamón)
Macrobrachium
faustinum
Herbivorous
Hypostomus
Hp
plecostomus
Oreochromis
Om
Omnivorous
mossambicus
Anguilla rostrata
Ar
Carnivorous
Eleotris perniger
Ep
115
Gobiomorus
Gd
-22.26 + 0.58
12
14.20 + 0.4
12
La
-24.74 + 1.4
3
14.93 + 1
3
Periphyton
-28.6 + 1.36
2
8.95 + 3.02
2
CPOM
-30.15 + 0.17
3
9.36 + 1.84
3
-22.58 + 1.23
5
7.98 + 1.06
5
-24.17 + 0.44
17 11.33 + 0.25 17
Pp
-25.79 + 0.76
21
9.56 + 0.56
21
Awaous taisajica
At
-25.19 + 1.89
3
10.54 + 0.97
3
Sicydium plumieri
Sp
-25.9 + 3.15
2
12.01 + 0.7
2
Hp
-28.26
1
11.80
1
Am
-27.98 + 1.34
10
11.5 + 0.54
10
-27.87 + 0.46
7
9.47 + 0.43
7
dormitor
Lepomis auritus
Xiphocaris elongata
Xe
Herbivore
Macrobrachium
Mf
faustinum
Omnivore
Palaemon
HUW (Rio Piedras)
pandaliformis
Herbivore
Hypostomus
plecostomus
Agonostomus
monticola
Omnivorous
Oreochromis
Om
mossambicus
116
Gobiomorus
Gd
-27.46 + 0.49
19 11.61 + 0.49 19
-28.85 + 3.75
2
8.98 + 1.44
2
dormitor
Anguilla rostrata
Ar
Cichla ocellaris
Co
-23.67
1
13.98
1
Eleotris perniger
Ep
-22.34 + 0.42
2
9.54 + 2.19
2
Periphyton
-24.67 + 0.49
4
10.23 + 0.85
4
CPOM
-31.33
1
3.61
1
Carnivorous
117
a) LUW
c) HUW
b) MUW
Volumetric proportion (%)
100
Uni Algae
Filamentous Algae
CPOM
Seeds/Spores
Spicules
Spiders
Insects
Mollusks
Crustacea
Rotifer
Fish
Sand
80
60
40
20
0
Ai
Al
As
Ma
Mf
Mp
Xe
Ai
As
Ma
Mf
Mp
Xe
Mf
Pp
Xe
Shrimp species
Fig. 4-1 Proportions of food items in stomachs of Atya innocuous (Ai), A.lanipes (Al), A.scabra (As), Micratya poeyi (Mp),
Macrobrachium acanthurus (Ma), M.faustinum (Mf), Xiphocaris elongata (Xe), and Palaemon pandaliformis (Pp) shrimp from the
LUW (Sabana) (a), MUW (Bayamón) (b) and HUW (Rio Piedras) (c) rivers.
117
118
14
a)
Ep
12
Gd
Ma
Ar
10
15
 N
Mf
8
Xe
Al
Mp
Ai
6
As
Np
4
Sp
2
-26
-24
-22
-20
-18
 C
13
16
b)
Om
Sp
15
La
At
15
 N
14
Gd
Ar
13
Xe
Mf
Ep
12
Ai
Hp
Ma
As
11
10
-27
-26
-25
-24
-23
 C
13
-22
-21
-20
-19
119
c)
14
Co
12
Hp
Sp
Gd
15
 N
Am
Mf
At
10
Pp
Om
Ep
Ar
8
Xe
6
-34
-32
-30
-28
-26
-24
-22
-20
 C
13
Fig. 4-2 δ13C and δ15N stable isotope biplots for primary, secondary and tertiary consumers
collected from LUW (a), MUW (b) and HUW (c). Shrimp filter feeders closed circle, shrimp
omnivores as closed circle, herbivore fish as closed diamond, predator fish as open diamond, and
snail as coled triangle. Continous line represents herbivore, dotted line as omnivores, and long
dashed line as predators. Values are mean + Standard Error (SE).
120
CHAPTER 5
EFFECTS OF FOOD SUPPLIES AND WATER TEMPERATURE ON GROWTH RATES OF
TWO SPECIES OF FRESHWATER TROPICAL SHRIMPS4
Summary
1. Growth rates of individual freshwater shrimp of the species Atya lanipes and Xiphocaris
elongata were measured in a second-order stream in the Luquillo Experimental Forest in
Puerto Rico over 10 years (1997-2007). Shrimp living at lower altitudes in warmer water and
wider stream channels with more algal and detrital foods were predicted to grow and
reproduce more rapidly.
2. Shrimp were marked and re-captured periodically in pools located at three altitudes to
determine if temperature affected growth rates among individual A. lanipes and X. elongata.
3. Mean annual water temperatures ranged from 20 to 24oC with the uppermost pool being
cooler than the lower- pools. Mean annual growth rates for Atya and Xiphocaris were 0.27
and 0.1 mm carapace length, respectively for all three populations.
4. Differences in growth were partially influenced by how each species obtains its food. Atya is
a filter-feeder and scraper and has continuous access to suspended organic particles and
biofilms. The slower growth rate for Xiphocaris elongata is most likely a result of the wider
range in quality and accessibility of food resources.
5. Differences in pool morphology and depths probably affected differences in food availability.
Increased leaf litter retention in the deeper upper and lower pools probably increased shrimp
growth rates while washout of leaf litter from the relatively shallow, elongate mid-altitude
pool decreased Atya lanipes growth rates.
4
Coauthored by Omar Pérez-Reyes, Todd A. Crowl, and Alan P. Covich
121
6. These long-lived, slow-growing shrimp species transform a wide range of organic materials
into their biomass. Because of the slow growth rates of these detritivores shrimp, tropical
storms, hurricanes, droughts or other disturbances could have persistent, long-term impacts
on detrital processing and on the populations of their predators.
Keywords. amphidromous, Atya lanipes, environmental factors, reproduction, Xiphocaris
elongata
Introduction
Progress with identification of the decapod species diversity in Caribbean fresh waters
(e.g. Karge et al., 2013; Pérez-Reyes et al., 2013) has stimulated more ecological research now
that investigators can study the dispersal (Kikkert et al., 2008) and evolution of co-occurring
species (Page et al., 2008; Bauer, 2013). Understanding of the primary controls on growth rates
(Bright, 1982; Yam & Dudgeon, 2006; Vogt, 2012) and predator-prey dynamics (e.g. Crowl &
Covich, 1994; Hein et al., 2010; Ocasio-Torres et al., 2014) is accelerating. Recent studies of
growth (Cross et al., 2008), dispersal (Kikkert et al., 2008; Covich et al., 2009), feeding (Covich,
1988a; 1988b; Pringle, 2003; Crowl et al., 2001; 2006) and nutrient cycling (Benstead et al.,
2010) by decapods in Puerto Rican streams provide additional information on the life histories
and ecological dynamics of these taxa (Atya and Xiphocaris) and their decapod predators
(Macrobrachium and Epilobocera) in Neotropical insular rivers and coastal headwaters.
Decapod growth and reproduction can occur year round due to the rather uniform
temperatures of warm tropical streams. Water temperature (Mantelatto & Barbosa, 2005; Chun et
al., 2008), food resource availability (Cross et al., 2008) and possibly population density
(Araneda et al., 2008) are considered the major factors that influence the growth rates of
freshwater decapods (Collins & Petriella, 1999). The growth of decapods is complicated due to
122
variations in the number and timing of molts, differences in size increment between molt events,
differential growth among different ages and sexes, reproductive effort, and variations in
susceptibility to predation (Hartnoll, 1983; 2001; Crowl & Covich, 1994; Cross et al., 2008;
Chang et al., 2012).
Here we report growth rates of marked individuals of the two most abundant shrimp
species (Xiphocaris elongata and Atya lanipes) in the headwaters of the Luquillo Mountains to
compare changes in growth under natural conditions over 10 years and in response to stormdriven disturbances. In addition to temperature, the relatively continuous inputs of leaf litter
(main source of detrital energy in these forested headwaters), are considered important drivers of
shrimp growth (Crowl et al., 2012). The large pulse of leaf-litter input resulting from high winds
and the high discharge that washed leaf-litter downstream during Hurricane Georges (September
1998) provided an opportunity to determine if this altered food availability affected individual
growth rates of shrimp in different pools along an altitudinal gradient (Luq-LTER Algae data)
(Crowl et al., 2012). Previously, we established that these freshwater shrimp species can respond
relatively quickly to large-scale disturbances such as Hurricane Hugo in September 1989 (Covich
et al., 1991), change their timing of reproduction at different altitudes (Johnson et al., 1998), have
relatively long life spans, and have growth rates possibly influenced by inter- and intra-specific
densities in headwater pools (Cross et al., 2008). Using data from this long-term study we here
evaluate two hypotheses: 1) warmer water in downstream pools increases shrimp growth rates in
a montane drainage network; and 2) access to higher quantity and quality of food in downstream
pools (where channel widths are greater, increased light levels enhance algal growth, and leaf
litter retention is longer) increases shrimp growth rates.
123
Material and Methods
Study site
The study took place in Quebrada Prieta, a second-order stream located in the Luquillo
Experimental Forest (also known as the El Yunque National Forest) in the Luquillo Mountains
(LM) of Puerto Rico (latitude 18o18’ N, longitude 65o47’ W). The headwaters of Quebrada Prieta
are located at 550 m above the sea level and flow into Quebrada Sonadora at approximately 300
m altitude. The riparian forest has a closed canopy dominated by yagrumo (Cecropia
schreberiana), tabonuco (Dacryodes excelsa) and the sierra palm (Prestoea montana) (Laurence,
1996; Crowl et al., 2012; McDowell et al., 2012). Although these dominant rainforest trees
provide a relatively continuous input of organic matter (leaf litter, twigs, flowers, stems and
fruits) to the stream, this input increases during high-rainfall periods from May to June and from
September to November (Crowl et al., 2001; Heartsill-Scalley et al., 2012; McDowell et al.,
2012). The steeply sloped stream channel is lined with cobbles and boulders with variable
amounts of sediments from bank erosion and landslides. Pools tend to have finer substrata of
sand and silt. The mean annual water temperature is 22 oC and the mean annual precipitation is
3,600 mm. Stream water temperature is affected by season and rainfall; temperature is lower
from November to March and briefly after large rainfall events. Rainfall is generally lower from
December to May (Low Rainfall- LRF). The wettest months coincide with the hurricane season
in the Atlantic that starts in June and ends in November (High Rainfall- HRF) with a peak storm
activity from mid-August to late October (Ewel & Whitmore, 1973; Helmer et al., 2002; Gould et
al., 2008; McDowell et al., 2012).
The decapod community is dominated by a filter-feeder/scraper, Atya lanipes Holthuis
1963, and a shredder/grazer, Xiphocaris elongata (Guérin-Méneville 1856). Other decapod
species such as A. scabra (Leach 1815), A. innocous (Herbst 1792), Macrobrachium carcinus
(Linnaeus 1758), M. faustinum (de Saussure 1857), M. crenulatum (Holthuis 1950), M.
124
heterochirus (Wiegmann 1836) and Epilobocera sinuatifrons (A. Milne-Edwards 1866) were
occasionally collected at low numbers.
Sampling and growth measurements
Surveys of decapod species distributions in Quebrada Prieta have been carried out since
1988 as part of the Luquillo Long Term Experimental Research (LUQ-LTER) Program.
Distribution, abundance and reproductive status of freshwater decapods in six pools along a 1200
m stretch of stream channel were sampled at least bi-annually. Three pools distributed along an
altitudinal gradient (305 m, 360 m, and 433 m) were selected for our current studies on growth
rates and were during 1997-2007.
Gee’s Minnow traps were baited and left overnight in each pool as in previous long-term
studies (Covich et al., 1996; Covich et al., 2009). The overnight period was necessary to capture
the largest number of shrimp due to the nocturnal activity of these species (Johnson & Covich,
2000). The number of traps per pool was based on the superficial area of the pool (0.5 traps . m2).
Growth rates of Xiphocaris elongata (N = 209) and Atya lanipes (N = 437) shrimp in
Quebrada Prieta were determined using mark-recapture. Visible Elastomeric Implant Tags
(Northwest Marine Technologies, Tumwater, WA, U.S.A.) were inserted laterally below the
integument of the fifth and sixth abdominal segment of the measured shrimp. This numeric tag
allowed for individual identification. These tags generally have over 88% retention over several
years and have no significant effect on growth or mortality (Isely & Stockett, 2001; Buřič et al.,
2008; Dinh et al., 2011). The initial size of the tagged shrimp ranged between 10.6-14.5 mm.
Batch markings were also employed using different colours for shrimp in each of the three pools.
These individuals ranged between 9.9-10.5 mm CL. Different elastomeric tag colours were
assigned to each pool: low (green), mid (red), and high (yellow) altitude. Shrimps were marked
in July (high rainfall period) of 1997.
125
During bi-annual sampling, shrimp were identified by species, counted and their
reproductive status recorded (gravid or/and mature, non-gravid). Carapace length (CL) and
presence of coloured tags were also recorded on site. Shrimp were measured from the tip of the
rostrum to the post-median edge of the cephalothorax to the nearest 0.01 mm with a dial caliper.
The CL measurements were used instead of the post-orbital length due to the absence from the
stream of fish that induce variable enlargement of the rostrum in the shrimp (Covich et al., 2009;
Ocasio-Torres et al., 2014; 2015). All shrimp were returned to their respective pool.
Identifications were based on Chace & Hobbs (1969). If storm flows occurred during the
sampling, traps were removed, shrimp released and the sampling re-scheduled for the next day
that had base-flow conditions. Physical parameters measured for the pools included three width
measurements, five random depths, maximum water depth, and pool length. Pool area and
volume were derived from these data. Shrimp densities (shrimp. m-2) were determined from each
pool during sampling. Values for precipitation, together with air and water temperature, were
obtained from the long-term data sets of the LUQ-LTER. We calculated growth rate (GR) as:
Growth Rate (mm . year-1) = (final length – initial length)*(time)-1. All calculations of length
were based on CL.
Statistical analysis
Long-term data from the LUQ-LTER that comprise the years 1997-2007 were used to
estimate the bi-annual density of marked and unmarked shrimp in each pool. To determine
variations in population density, Two-Way ANOVAs were performed for each pool using the low
rainfall (LRF) and high rainfall (HRF) periods and the time (years 1997-2007) as factors. Prior to
the analysis all the density data were tested for their fit to normal distribution and for
homogeneity of variance, and were transformed using the natural log transformation for
population data [Ln (X + 1)]. Adult shrimp were sorted into size classes based on carapace
126
length; Atya lanipes in five 5.0 mm size classes and Xiphocaris elongata in six 3.0 mm size
classes. Percentages of breeding (gravid) females of both species in the LRF and HRF months
were plotted as annual histograms per pool during the 10 year period. Two-Way ANOVAs were
performed to determine if there were significant differences in the mean cephalothorax length for
each species per pool (lower, middle and upper altitudes) and year (1997-2007), and to determine
variation in shrimp densities across time and rainfall periods (Low Rainfall- LRF and High
Rainfall- HRF) per pool. Linear regressions (Mean CL versus Time) for each species were
performed to compare the growth rates of the shrimp among pools; the slopes were compared
using analyses of covariance (ANCOVA).
Results
Environmental factors
The mean annual water temperature ranged between 20 and 24 oC among the three pools.
The coldest temperatures were recorded during the months of November to March in the
uppermost pool, while the warmest were recorded from July to September in the lowermost pool.
Differences among the monthly mean temperatures (F11,505 = 70.99; P < 0.00001) and throughout
the years (F10,505 = 8.38; P < 0.0001) were both significant. The lowest temperature was recorded
in January 2005 (19.6 oC) and the lowest monthly mean water temperature was for January (21 oC
+ 0.07 standard error). The warmest water temperature was recorded in September of 1997 (24
o
C), while the highest mean monthly temperature was for September (23 oC + 0.05). Monthly
total rainfall ranged from 9.4 mm . month-1 (March 2005) to 1076 mm . month-1 (May 2004); the
lowest monthly mean was for March (166.5 + 42.9 mm) and the highest (453.2 + 64.0 mm)
during Hurricane Georges in 1998. Precipitation differences were significant on a monthly basis
(F11,110 = 2.22; P < 0.018), but these differences were not significant across years (F10, 110 = 1.78;
P > 0.07).
127
All of the three pools had low concentrations of dissolved nutrients (DOC 1.5 + 0.83 mg .
L-1; DON 0.06 + 0.04 mg . L-1; TDN 0.15 + 0.11 mg . L-1) and low conductivity (75.2 + 13.3
micromhos . cm-1) with moderate hardness and a range of pH 6.2 to 8.0 (Table 5-1). The nitrogen
and phosphorus concentrations were also low and typical of other Luquillo streams (McDowell et
al., 2012).
Shrimp abundance and growth
A total of 42,563 shrimp was captured from the three pools in Quebrada Prieta from 1997
to 2007. The percentage of tagged shrimp recaptured annually from 1997 to 2007 ranged
between 0.02 (2006) to 20.0 % (1999). No significant differences in the Atya densities across
time and rainfall periods were observed in any of the pools. Densities of X. elongata varied
significantly across time (F10,10 = 12.33; P < 0.0001) and rainfall periods (F1,10 = 24.63; P =
0.001) in the mid-altitude pool, and no significant variations were observed in the upper and
lower pools. Inter-site differences in A. lanipes abundance showed higher densities of shrimp in
the highest pool than in the middle and lower pools (F2,65 = 4.00; P = 0.028), but no significant
differences were observed across time. Significant differences were observed in the Xiphocaris
elongata densities across pools (F2,65 = 9.92; P < 0.0001) and time (F10,65 = 2.33; P = 0.033).
Breeding females of Xiphocaris elongata were more frequently observed during the HRF
periods than the LRF, whereas Atya lanipes showed no preference between the LRF and HRF
periods for reproduction. Only individuals in the lower pool showed a similar percentage in
gravid females across time (Fig. 5-1).
The annual mean CL of A. lanipes showed significant differences among pools (F2,32 =
15.03; P < 0.0001) and across years (F10,32 = 3.11; P = 0.015) (Fig. 5-2a). The largest mean CL
(17.2 + 0.27 mm) was observed in the lower pool during 1997, while the smallest mean was 12.9
+ 0.16 mm from middle pool in 2007. After Hurricane Georges in September 1998, large
128
reductions in mean CL of Atya lanipes were observed in all the pools during 2000. The shrimp in
the lower and upper pools increased their mean CL after the decrease in 2000, but the mean size
of the organisms in the middle pool continued to decrease until 2007. Significant differences in
mean CL of Xiphocaris elongata were observed across time (F10,32 = 3.99; P = 0.004), but not
among pools. Mean CL of X. elongata ranged between 13.1 + 0.15 mm (lower pool during 2000)
to 15.1 + 0.27 mm (upper elevation pool during 1997) (Fig. 5-2b).
A total of 329 shrimp (203 A. lanipes and 126 X. elongata) was measured, captured,
marked and released in the three pools in 1997. The mean CL of the re-captured A. lanipes in 10
years ranged between 11.91 + 0.92 and 15.56 + 0.72 mm, while for X. elongata the mean CL
ranged between 12.1 + 0.07 and 14.23 + 0.62 mm. Different growth between the two species
revealed that individuals of Atya lanipes grew more than Xiphocaris elongata (Fig. 5-3). The
filter feeder, A. lanipes, had a mean growth rate of 0.27 mm year-1 (CL = 0.2726*Time – 532.75;
r2 = 0.687; P < 0.003), while the shredder/grazer, X. elongata, had an overall mean growth rate of
0.1 mm year-1 (CL = 0.0843*Time – 155.88; r2 = 0.2105; P = 0.156). The comparison of the
slopes shows significant differences in CL across time (F1,18 = 13.31; P < 0.002) but not between
species (F1,18 = 0.06; P = 0.807).
Discussion
Populations of Atya lanipes and Xiphocaris elongata in the Quebrada Prieta are widely
distributed among headwater pools (Covich et al., 1996; Crowl et al., 2001). Comparison of the
mean growth of both species among pools revealed faster growth of A. lanipes, a filter feeder and
scraper, while the mean growth of X. elongata, a shredder and grazer, was similar among pools
and across time. As expected, shrimp in warmer waters grew faster than those in cooler waters.
These observations are the first to document a significantly higher growth rate for A. lanipes than
X. elongata over a range of temperatures, pools, densities and time.
129
The size distributions in the populations of Atya lanipes and Xiphocaris elongata
followed the distribution observed in previous studies in Puerto Rico (Covich et al., 2003, Cross
et al., 2008) where more than 60% of the shrimp in these populations have a CL between 12-17
mm. The Atya lanipes populations in these locations can be divided into three main cohorts:
cohort 1 (< 11 mm CL) comprised new recruitments with active growth but not mature enough to
be reproductive adults; cohort 2 (12-17 mm CL) comprised adults with high reproductive outputs
and active growth; and cohort 3 (> 18 mm CL) comprised mature and older adult shrimp with
low reproductive output, slow growth rate, and which tended to be permanent residents of the
pools. These size distributions and population structures are similar to those reported for A.
scabra in Brazil (Oliveira-Almeida et al., 2010; Herrera-Correa et al., 2013). Like the A. lanipes
populations in Puerto Rico, the middle class size of A. scabra in Brazil contained the most gravid
individuals. Appreciable differences in size between gravid females and larger adults were
observed in the Luquillo populations of A. lanipes. Individuals with a CL larger than 19 mm
were males and most of the gravid females had a CL between 5-18 mm. In this study, no females
or gravid females with a CL larger than 19 mm were observed; it appears that Atya lanipes has a
marked sexual dimorphism (Martínez-Mayen et al., 2000; Sanchez et al., 2008).
The filter-feeding planktonic larvae of shrimp spend 60 to 90 days (depending on the
species) in estuaries. After their metamorphosis in the estuary, the post-larvae begin an upstream
migration until they reach headwater pools. During the migration the post-larvae mature into
juveniles and reach reproductive status in the upstream adult habitat (Bauer, 2011a; 2011b; 2013).
Generally, most individuals reach lower and mid-altitude pools when they are still small juveniles
and sub-adults. These shrimp appear to synchronize their complex life cycle with the changes in
temperature, precipitation and nutrient availability. Adult shrimp can breed throughout the year,
but most of the reproduction occurs during the HRF period. This timing increases the chances for
the rapid downstream transport of the first-stage larvae to an estuary during periods of high-water
130
discharge (Hoffmann & Negreiros-Fransozo, 2010; Heartsill-Scalley et al., 2012). Initiation of
reproduction in the drier months may increase access to large amounts of available food resources
(leaves, fruits, detritus and fungi) for the breeding females, because washout of litter is less
during periods of low flows (Johnson et al., 1998; Covich & McDowell, 1996; Hoffmann &
Negreiros-Fransozo, 2010). These results reinforce earlier observations that Xiphocaris elongata
tends to be relatively seasonal in its reproduction when sufficient food is accessible (Johnson et
al., 1998). Reproductive seasonality is apparently associated with the amount of food available
for shredding by Xiphocaris elongata. Inputs of coarse particulate organic matter (CPOM)
increase from March to August with an extended period until November (hurricane season)
(Heartsill-Scalley et al., 2012). These inputs coincide with the reproductive timing of Xiphocaris
elongata. Atya lanipes, primarily a filter feeder, uses different resources than Xiphocaris. During
base flows, Atya is effective in filtering suspended FPOM derived from the decomposition of
CPOM (Crowl et al., 2001; 2012). Suspended FPOM varies in concentration over time and
space, but some food resources are always available for biofiltration in these streams during base
flows. In contrast, Xiphocaris is an active swimmer and shredder that can use resources not
available to Atya.
During 2000 Atya lanipes and Xiphocaris elongata increased in frequency in the size
classes of 6-11 and 8-11 mm CL respectively. This increase in size during 2000 suggests that
these individuals represent the new cohort of shrimp after the washout of Hurricane Georges.
Moreover, the number of gravid females also showed an increase in the years after the hurricane.
Similar changes in shrimp densities were observed after Hurricane Hugo in 1989. The shrimp
densities decreased soon after Hurricane Hugo, but months later the shrimp densities reached
maximum densities that were greater than previously recorded, apparently as a result of the large
pulse of wind-transported leaf litter that was available along with more algal production as a
short-term result of canopy loss in Quebrada Prieta (Covich et al., 1991).
131
In the last decades, the number and intensity of tropical storms and hurricanes that pass
through the Caribbean have increased. In 1998, Hurricane Georges made landfall in Puerto Rico
as a category 3-hurricane with sustained winds of 115 mph (Ostertag et al., 2003). During
Hurricane Georges, LM had rainfalls of 75.4 mm and a peak discharge in the Rio Espiritu Santo
of 64.9 m3. seconds-1 (USGS-Rio Grande Gauge Station- 50063800). As a consequence of the
intense winds, precipitation, and floods during the hurricane, the riparian forest was defoliated
and stream discharge transported some shrimp and leaf litter from the headwaters to the
downstream pools. The winds increased input of leaf litter in one day that represented
approximately 0.9 times the annual rates reported in pre-hurricane standings (Ostertag et al.,
2003). Defoliation of the riparian forest increased sunlight to the stream resulting in an increase
in sunlight and water temperature. The increased light probably increased algal production that
contributed to higher growth of periphyton and biofilm that were available to filter-feeding Atya
(Crowl et al. 2012); Lefrancois et al. (2011) demonstrated that biofilm (aggregates of
microorganisms) can be an important source of nutrients for atyids and xiphocarids in the
Caribbean. In streams with wider channels, the light conditions increase algal production,
resulting in higher numbers of shredders, grazers and scrappers (P Torres, unpublished data).
An increase in water temperature was expected to increase growth rates. This effect was
evident in the size increase observed in Atya lanipes during 1999. A similar increased size was
observed from 2004 to 2007 when the individuals in the upper and lower pools increased in CL as
the water temperature increased. The highest water temperatures observed in Quebrada Prieta
occurred during May to September, which coincide with the HRF and the hurricane season in the
Caribbean. Studies on crayfish (Geddes et al., 1988; Verhoef & Austin, 1999; Tropea et al.,
2010; Paglianti & Gherardi, 2004) and freshwater shrimp (Stephenson & Knight, 1980; Chen &
Kou, 1996; Niu et al., 200; Yam & Dudgeon, 2006) have shown a direct relation between the
increase in size and increase in temperature. In general, growth rate is observed to increase as the
132
water temperature increases until the maximum growth rate is reached, after which the growth
rate declines at higher water temperatures beyond a threshold (Hart, 1980).
During the LRF period, previous Hurricane Georges (1998) densities of Atya in the
upper, middle and lower pools were 52.0, 10.1 and 26.1 shrimp. m-2 respectively; months later the
densities decreased to 24.3, 10.8 and 8.5 shrimp . m-2. The decline in shrimp densities after the
hurricane in the upper and lower pools most likely resulted from the washout during high flows
during Hurricane Georges. Shrimp densities in the mid-altitude pool were not affected by the
high discharge because this elongate pool (length > 15 m) was less subject to washout.
Xiphocaris, in contrast to Atya, is an active swimmer that can be removed easily from the pool
with a high discharge event.
The variations in densities of Xiphocaris elongata in the upper and lower pools reflect the
variability in environmental conditions. Pools at higher altitude generally have confined reaches,
smaller size and shallow depths. Lower pools generally are larger and deeper but also have
confined reaches. The uppermost, shallow pools are affected more than deeper pools by
droughts, extreme discharges and high inputs of organic matter. Extensive removal of leaf litter
occurs during storm flows (Covich et al., 2003) Extreme environmental conditions can decrease
or increase the shrimp densities (i.e. concentrate individuals by inwash during storm flows or
reduce pool volume during dry periods). These effects were observed in the lowest and highest
pools in this study.
The mean annual growth rate of Atya lanipes was moderate in the mid-altitude pool,
apparently as a result of less variable shrimp densities and lower retention of leaf litter. The data
on growth rates and densities suggest that pools with variable densities, like the higher and lower
pools in Quebrada Prieta, promote growth in Atya lanipes in contrast to pools with stable
densities. This discrepancy among growth rates is possibly explained by the amount and type of
133
available food resources (FPOM and CPOM) in each pool as well the differences in water
temperature.
Due to differences in pool sizes and locations, shrimp in the uppermost pool are exposed
to more variability in pool volume. The uppermost pool was located in a reach where the riparian
forest produced a large, continuous input of Cecropia leaf litter which represented the main
source of energy for these shrimps (Crowl et al., 2001; Wright & Covich, 2005a; 2005b). The
shallow mid-altitude pool was located in a Prestoea montana (Sierra Palm) forest. Palm fronds
are generally not high-quality sources of food for Atya because most of the litter decomposition
occurs while the fronds remain attached to the tree and relatively little leaf litter enters the stream
food web (Zimmerman & Covich, 2007). Atyids and xiphocarids in deeper pools can use
available food resources over a longer period before the storm-flows remove the microbially
processed litter from the pool. A relatively continuous input of Dacryodes leaf litter assured
some level of food resources for the upstream migrants in all pools. Wright & Covich (2005a)
showed that Xiphocaris preferred to feed on microbially conditioned Dacryodes over Cecropia
leaves. This food preference among shrimp can result from the different conditioning processes
by dominant micro-organisms (fungi and bacteria) and the relative greater toughness of the
Cecropia leaves (Wright & Covich, 2005b).
Shrimp in the uppermost pool tended to be mature adults near to the maximum CL size
(cohort 3) where the growth rate and reproduction output generally decline. Cross et al. (2008)
described the growth pattern for Atya in this stream and suggested that Atya has an active growth
phase from 5 mm CL until it reaches the maximum size of 20 mm CL 7 years later. After this
period, the growth rate is reduced dramatically and the shrimp function as mature, reproductive
adults. This shift coincides with the range of growth rate observed in decapods, when they
exhibit an active growth rate during their first years of life. When the adult stage is reached, the
134
growth rate and moulting process are typically reduced to a minimum of 2 or 3 moults per year
(personal observation, OPR).
Shrimp in the lower pool were part of the new cohort (cohort 1) of post-larvae and
juveniles that were in the process of migrating to the upper pools as part of their amphidromous
life cycle. These shrimp were in their active growing phases. In this stage of development the
shrimp appendages were not sufficiently sclerotized (Fryer, 1977) to readily breakdown the more
lignified Cecropia leaves and the juvenile shrimp preferred softer, microbe-enriched leaves
(Wright & Covich, 2005b). In contrast, adult shrimp in the uppermost pools (cohort 3) generally
had an excess of Cecropia leaf litter available that was readily decomposed, and fewer postlarvae reached these upper pools (Kikkert et al., 2009).
The average annual growth rates for Atya lanipes and Xiphocaris elongata during the 10
years of the study were 0.28 and 0.1 mm . year-1 respectively. The mean growth for these shrimp
in the current field experiment is consistent with current models for these species, (Cross et al.,
2008). The model predicted that Atya continue to grow until they reach the maximum size of 20
mm CL, when the growth rate declines. For Xiphocaris, the model predicted a rapid growth rate
between the 5-11 mm CL with the growth rate declining after that threshold until it reaches the
maximum CL of 17 mm is reached, after which the growth rate is further reduced.
As expected, the growth rates of Atya lanipes and Xiphocaris elongata were positive and
associated with differences in water temperature and food supplies in different pools in Quebrada
Prieta; effects of a hurricane increased leaf-litter input that also affected growth rates. Additional
manipulative experiments in the field and laboratory are needed to increase knowledge of the
growth rates among individual shrimp in the early and late stages in their life history. The
important roles that these long-lived, slow-growing species play in headwater stream food webs
also need to be considered when managing watersheds to sustain the ecosystem functions and
services that these key species provide.
135
Acknowledgments
We thank the many people who helped in the field, with special appreciation of the
fieldwork done by many undergraduate and graduate students. This research was supported by
grants BSR-8811902, DEB 9411973, DEB 0080538, DEB 0218039 and DEB 0620910 from the
National Science Foundation (NSF) to the Institute for Tropical Ecosystem Studies, University of
Puerto Rico, and to the International Institute of Tropical Forestry, United States Department of
Agriculture (USDA) Forest Service, as part of the Long-Term Ecological Research Program in
the Luquillo Experimental Forest. The USDA Forest Service and the University of Puerto Rico
gave additional support.
136
References
Araneda M., Pérez E.P. & Gasca-Leyva E. (2008) White shrimp Penaeus vannamei culture in
fresh water at three densities: condition state based on length and weight. Aquaculture,
283, 13-18.
Bauer R.T. (2011a) Amphidromy and migrations of freshwater shrimp. I. Costs, benefits,
evolutionary origins, and an unusual Case of amphidromy. In: New frontiers in
crustacean biology (Ed. A. Asakura), pp. 145-156. Brill, Leiden, The Netherlands.
Bauer R.T. (2011b) Amphidromy and migrations of freshwater shrimp. II. Delivery of hatching
larvae to the sea, return juvenile upstream migration, and human impacts. In: New
frontiers in crustacean biology (Ed. A. Asakura), pp. 157-158. Brill, Leiden, The
Netherlands.
Bauer R.T. (2013) Amphidromy in shrimp: a life history pattern between rivers and the sea. Latin
American Journal of Aquatic Research, 41, 633-650.
Benstead J.P., Cross W.F., March J.G., McDowell W.H., Ramirez A. & Covich A.P. (2010)
Biotic and abiotic controls on the ecosystem significance of consumer excretion in two
contrasting tropical streams. Freshwater Biology, 55, 2047-2061.
Bright G.R. (1982) Secondary benthic production in a tropical island stream. Limnology and
Oceanography, 27, 472-480.
Buřič M., Kozák P. & Vích P. (2008) Evaluation of different marking methods for spiny-cheek
crayfish (Orconectes limosus). Knowledge and Management of Aquatic Ecosystems, 389,
1-8.
Chace F.A. & Hobbs H.H. (1969) The freshwater and terrestrial decapod crustaceans of the West
Indies with special reference to Dominica. Smithsonian Institution Press: Washington,
D.C.
Chang Y.J., Sun C.L., Chen Y. & Yeh S.Z. (2012) Modelling the growth of crustacean species.
Reviews in Fish Biology and Fisheries, 22, 157-187.
Chen J.C. & Kou T.T. (1996) Effects of temperature on oxygen consumption and nitrogenous
excretion of juvenile Macrobrachium rosenbergii. Aquaculture, 145, 295-303.
Chun J.K., Ma C.W., Oh C.W. & Paik S.G. (2008) Reproduction and growth of the freshwater
prawn, Palaemon paucidens (Decapoda; Palaemonidae) in a lake of Korea. Journal of
Environmental Biology, 29, 163-168.
Collins P.A. & Petriella A. (1999) Growth pattern of isolated prawns of Macrobrachium borellii
(Crustacea, Decapoda, Palaemonidae). Invertebrate Reproductive Development, 36, 1-3.
Covich A.P. (1988a) Geographical and historical comparisons of Neotropical streams: Biotic
diversity and detrital processing in highly variable habitats. Journal of the North
American Benthological Society, 7, 361-386.
137
Covich A.P. (1988b) Atyid shrimp in the headwaters of the Luquillo Mountains, Puerto Rico:
Filter feeding in natural and artificial streams. Verhandlungen der Internationale
Vereinigung für Theorestische und Angewandte Limnologie, 23, 2108-2113.
Covich A.P. & McDowell W.H. (1996) The stream community. In: The food web of tropical rain
forest (Eds. D.P. Reagan & R.B. Waide), pp 433-459. The University of Chicago Press,
Chicago.
Covich A.P., Crowl T.A. & Scatena F.N. (2003) Effects of extreme low flows on freshwater
shrimp in a perennial tropical stream. Freshwater Biology, 48, 1199-1206.
Covich A.P., Crowl T.A., Hein C.L., Townsend M.J. & McDowell W.H. (2009) Predator-prey
interactions in river networks: comparing shrimp spatial refugia in two drainage basins.
Freshwater Biology, 54, 450-465.
Covich A.P., Crowl T.A., Johnson S.L., Varza D. & Certain D.L. (1991) Post-hurricane Hugo
increases in atyid shrimp abundance in a Puerto Rican montane stream. Biotropica, 23,
448-454.
Covich A.P., Crowl T.A., Johnson S.L. & Pyron M. (1996) Distribution and abundance of
tropical freshwater shrimp along a stream corridor: response to disturbance. Biotropica,
28, 484-492.
Cross W.F., Covich A.P., Crowl T.A., Benstead J.P. & Ramírez A. (2008) Secondary production,
longevity and resource consumption rates of freshwater shrimp in two tropical streams
with contrasting geomorphology and food web structure. Freshwater Biology, 53, 25042519.
Crowl T.A. & Covich A.P. (1994) Responses of a freshwater shrimp to chemical and tactile
stimuli from a large decapod predator. Journal of the North American Benthological
Society, 13, 291-298.
Crowl T.A., McDowell W.H., Covich A.P. & Johnson S.L. (2001) Freshwater shrimp effects on
detrital processing and nutrients in a tropical headwater stream. Ecology, 82, 775-783.
Crowl T.A., Welsh V., Heartsill-Scalley T. & Covich A.P. (2006) Effects of different types of
conditioning on rates of leaf-litter shredding by Xiphocaris elongata, a Neotropical
freshwater shrimp. Journal of the North American Benthological Society, 25, 196-206.
Crowl T.A., Brokaw N., Waide R.B., González G., Beard K.H., Greathouse E., Lugo A.E.,
Pringle C. & Belovsky G.E. (2012) When and where biota matter- linking disturbance
regimes. In: A Caribbean Forest Tapestry: The multidimensional nature of disturbance
and response (Eds N. Brokaw, T.A. Crowl, A.E. Lugo, W.H. McDowell, F.N. Scatena,
R.B. Waide & M.R. Willing), pp. 272-304. Oxford University Press, Oxford, UK.
Dinh H., Coman G., Hurwood D.A. & Mather P.B. (2011) Experimental assessment of the utility
of visible implant elastomer tags in a stock improvement programme for giant freshwater
prawn (Macrobrachium rosenbergii) in Vietnam. Aquaculture Research, 1-9.
138
Ewel J.J. & Whitmore J.L. (1973) The ecological life zones of Puerto Rico and the Virgin
Islands. Institute of Tropical Forestry, San Juan, Puerto Rico. Forest Service Research
Paper ITF 18, 1-72.
García-Martinó A.R., Warner G.S., Scatena F.N. & Civco D.L. (1996) Rainfall, runoff and
elevation relationships in the Luquillo Mountains of Puerto Rico. Caribbean Journal of
Science, 32, 413-424.
Geddes M.C., Mills B.J. & Walker K.F. (1988) Growth in the Australian freshwater crayfish,
Cherax destructor Clark, under laboratory conditions. Marine and Freshwater Research,
39, 555-568.
Gould W.A., Alarcon C., Fevold B., Jimenez M.E., Martinuzzi S., Potts G., Quiñones M.,
Solórzano M. & Ventosa E. (2008) Puerto Rico GAP Analysis Project. General
Technical Report IITF-GTR-39, 1, pp. 189.
Hart R.C. (1980) Embryonic duration and post-embryonic growth rates of the tropical freshwater
shrimp Caridina nilotica (Decapoda: Atyidae) under laboratory and experimental field
conditions. Freshwater Biology, 10, 197-315.
Hartnoll R.G. (1983) Strategies of crustacean growth. In: Papers from the Conference on Biology
and Evolution of Crustacea (Ed. J.K. Lowry), pp. 121-131. The Australian Museum
Memoir 18, Australian Museum, Sydney, Australia.
Hartnoll R.G. (2001) Growth in Crustacea-twenty years on. In: Paula J.P.M., Flores A.A.V. &
Fransen C.H.J.M. (eds) Advances in Decapod Crustacean Research. Springer
Netherlands pp 111-122.
Heartsill-Scalley T., Scatena F.N., Moya S. & Lugo A.E. (2012) Long-term dynamics of organic
matter and elements exported as coarse particulates from two Caribbean montane
watersheds. Journal of Tropical Ecology, 28, 127-139.
Hein C.L., Pike A.S., Blanco J.F., Covich A.P., Scatena F.N., Hawkins C.P. & Crowl T.A. (2010)
Effects of coupled natural and anthropogenic factors on the community structure of
diadromous fish and shrimp species in tropical island streams. Freshwater Biology, 56,
1002-1015.
Helmer E.H., Ramos O., López T. Del M., Quiñones M. & Díaz W. (2002) Mapping the forest
type and land cover of Puerto Rico, a component of the Caribbean biodiversity hotspot.
Caribbean Journal of Science, 38, 165-183.
Herrera-Correal J., Mossolin E.C., Wehrtmann I.S. & Mantelatto F.L. (2013) Reproductive
aspects of the caridean shrimp Atya scabra (Leach, 1815) (Decapoda: Atyidae) in São
Sebastião Island, southwestern Atlantic, Brazil. In: Studies on Freshwater Decapods in
Latin America (Eds. I.S. Wehrtmann & R.T. Bauer). Latin American Journal of Aquatic
Resources, 41, 676-684.
139
Hoffmann P. & Negreiros-Fransozo M.L. (2010) Reproductive cycle and fecundity of Potimirim
glabra (Kingsley, 1954) (Caridea, Atyidae) from a littoral stream. Invertebrate
Reproduction and Development, 54, 133-141.
Isley J.J. & Stockett P.E. (2001) Tag retention, growth and survival of red swamp crayfish
marked with a visible implant tag. North American Journal of Fisheries Management, 21,
422-424.
Johnson S.L., Covich A.P., Crowl T.A., Estrada-Pinto A., Bithorn J. & Wurtsbaugh W.A. (1998)
Do seasonality and disturbance influence reproduction in freshwater atyid shrimp in
headwater streams, Puerto Rico? Verhandlungen der Internationale Vereinigung für
Theorestische und Angewandte Limnologie, 26, 2076-2981.
Johnson S.L. & Covich A.P. (2000) The importance of night-time observations for determining
habitat preferences of stream biota. Regulated Rivers: Research and Management, 16,
91-99.
Karge A., Page T.J. & Klotz W. (2013) A new species of freshwater shrimp of the genus
Micratya (Decapoda: Atyidae: Caridea) from Puerto Rico. Zootaxa, 3608, 357-368.
Kikkert D.A., Crowl T.A. & Covich A.P. (2008) Upstream migration of amphidromous shrimp in
the Luquillo Experimental Forest, Puerto Rico: temporal patterns and environmental
cues. Journal of the North American Benthological Society, 28, 233-246.
Lawrence W.T. Jr. (1996) Plants: The food base. In: The food web of tropical rain forest (Eds
D.P. Reagan & R.B. Waide) pp. 17-51. The University of Chicago Press, Chicago.
Lefrançois E., Coat S., Lepoint G., Vachiery N., Gros O. & Monti D. (2011) Epilithic biofilm as a
key factor for small‐scale river fisheries on Caribbean islands. Fisheries Management
and Ecology, 18, 211-220.
Mantelatto F.L.M. & Barbosa L.R. (2005) Population structure and relative growth of freshwater
prawn Macrobrachium brasiliense (Decapoda, Palaemonidae) from São Paulo State,
Brazil. Acta Limnol Bras, 17, 245-255.
Martínez-Mayén M., Román-Contreras R., Rocha-Ramírez A. & Chazaro-Olvera S. (2000)
Relative growth of Atya margaritacea A. Milne-Edwards, 1864 (Decapoda, Atyidae)
from the southern Pacific coast of Mexico. Crustaceana, 73, 525-534.
McDowell, W.H., F.N. Scatena, R.B. Waide, N. Brokaw, G.R. Camilo, A.P. Covich, T.A. Crowl,
G. González, E.A. Greathouse, P. Klawinski, D.J. Lodge, A.E. Lugo, C.M. Pringle, B.A.
Richardson, M.J. Richardson, D.A. Schaefer, W.L. Silver, J. Thompson, D. Vogt, K.
Vogt, R.B. Waide, M. Willig, L. Woolbright, X. Zou, & Zimmerman, J. K. (2012)
Geographic and ecological setting of the Luquillo Mountains. In: A Caribbean Forest
Tapestry: The multidimensional nature of disturbance and response (Eds N. Brokaw,
T.A. Crowl, A.E. Lugo, W.H. McDowell, F.N. Scatena, R.B. Waide & M.R. Willing),
pp.72-163. Oxford University Press, Oxford, UK.
140
Niu C., Lee D., Goshima S. & Nakao S. (2003) Effects of temperature on food consumption,
growth and oxygen consumption of freshwater prawn Macrobrachium rosenbergii (de
Man 1879) post larvae. Aquaculture Research, 34, 501-506.
Ocasio-Torres M.E., Crowl T.A. & Sabat A.M. (2014) Long rostrum in an amphidromous shrimp
induced by chemical signals from a predatory fish. Freshwater Science, 33, 451-458.
Ocasio-Torres M.E., Giray T., Crowl T.A., & Sabat A.M. (2015) Antipredator defence
mechanism in the amphidromous shrimp Xiphocaris elongata (Decapoda:
Xiphocarididae): rostrum length. Journal of Natural History, doi:
10.1080/00222933.2015.1005716
Oliveira-Almeida A., Contreira-Mossolin E. & Rocha-Luz J. (2010) Reproductive biology of the
freshwater shrimp Atya scabra (Leach, 1815) (Crustacea:Atyidae) in Ilhéus, Bahia,
Brazil. Zoological Studies, 49, 243-252.
Ostertag R., Scatena F.N. & Silver W.L. (2003) Forest floor decomposition following hurricane
litter inputs in several Puerto Rican forests. Ecosystems, 6, 261-273.
Page T.J., Cook B.D., von Rintelen T., von Rintelen K. & Huges J.M. (2008) Evolutionary
relationships of atyid shrimp imply both ancient Caribbean radiations and common
marine dispersals. Journal of the North American Benthological Society, 27, 68-83.
Paglianti A. & Gherardi F. (2004) Combined effects of temperature and diet on growth and
survival of young-of-year crayfish: a comparison between indigenous and invasive
species. Journal of Crustacean Biology, 24, 140-148.
Pérez-Reyes O., Crowl T.A., Hernández-García P., Ledesma-Fusté R., Villar-Fornes F.A. &
Covich A.P. (2013) Freshwater decapods of Puerto Rico: a checklist and reports of new
localities. Zootaxa, 3717, 329-344.
Pringle C.M. (2003) Atyid shrimp (Decapoda: Atyidae) influence the spatial heterogeneity of
algal communities over different scales in tropical montane streams, Puerto Rico.
Freshwater Biology, 35, 125-140.
Sánchez-Palacios J., Beltrán-Álvarez R. & Ramírez-Lozano J.P. (2008) Crecimiento y
reproducción del camarón Atya margaritacea (Decapoda: Atyidae) en el Río Presidio,
Sinaloa, México. Revista de Biología Tropical, 56, 513-522.
Stephenson M.J. & Knight A.W. (1980) The effect of temperature and salinity on oxygen
consumption of post-larvae of Macrobrachium rosenbergii (de man) (Crustacea:
Palaemonidae). Comparative Biochemistry and Physiology Part A. Physiology, 67, 699703.
Tropea C., Piazza Y. & Greco L.S.L. (2010) Effect of long-term exposure to high temperature on
survival, growth and reproductive parameters of the “redclaw” crayfish Cherax
quadricarinatus. Aquaculture, 302, 49-56.
141
Verhoef G. & Austin C. (1999a) Combined effects of temperature and density on the growth and
survival of juveniles of the Australian freshwater crayfish Cherax destructor (Clark) part
I. Aquaculture, 170, 37-47.
Verhoef G. & Austin C. (1999b) Combined effects of temperature and density on the growth and
survival of juveniles of the Australian freshwater crayfish Cherax destructor (Clark) part
II. Aquaculture, 170, 49-57.
Vogt G. (2012) Ageing and longevity in the Decapoda (Crustacea): A review. Zoologischer
Anzeiger, 251, 1-25.
Wright M.S. & Covich A.P. (2005a) Relative importance of bacteria and fungi in a tropical
headwater stream: leaf decomposition and invertebrate feeding preference. Microbial
Ecology, 49, 536-546.
Wright M.S. & Covich A.P. (2005b) The effect of macroinvertebrate exclusion on leaf
breakdown rates in a tropical headwater stream. Biotropica, 37, 403-408.
Yam R.S.W. & Dudgeon D. (2006) Production dynamics and growth of atyid shrimp (Decapoda:
Caridina spp) in 4 Hong Kong streams: The effects of site, season, and species. Journal
of the North American Benthological Society, 25, 406-416.
Zimmerman J.K.H. & Covich A.P. (2007) Damage and recovery of riparian Sierra Palms after
Hurricane Georges: Influence of topography and biotic characteristics. Biotropica, 39,
43-49.
142
Table 5-1 Range, mean and standard deviation of chemical variables of the stream water in
Quebrada Prieta. Long-term chemical data from Luq-LTER (1999-2007)
Chemical variables
Minimum Maximum Mean Std. Dev.
pH (pH units)
4.1
7.9
7.1
0.32
Conductivity (micromho . cm-1)
19
127.4
75.2
13.3
Chloride (Cl) (mg . L-1)
1.6
20.5
8.1
10.6
Nitrate (NO3-N) (mg N . L-1)
2.5
662.6
68.5
50.1
Sodium (Na) (mg . L-1)
0.9
10.8
6.3
1.13
Potassium (K) (mg . L-1)
0.02
1.6
0.4
0.14
Magnesium (Mg) (mg . L-1)
0.15
6.2
3.1
0.8
Calcium (Ca) (mg . L-1)
0.17
8.7
4.0
1.1
Ammonium (NH4-N) (mg N . L-1)
2.5
153.4
6.4
9.6
2
89.1
4.9
5.7
Sulphate (SO4-S) (mg S . L-1)
0.05
2.05
0.6
0.2
Dissolved Organic Carbon (DOC) (mg . L-1)
0.4
5.8
1.5
0.8
Total Dissolved Nitrogen (TDN) (mg . L-1)
0.03
0.9
0.15
0.1
Dissolved Organic Nitrogen (DON) (mg . L-1)
0.01
0.3
0.06
0.04
Phosphate (PO4-P) (mg P . L-1)
H.Georges
LRF
HRF
80
60
40
20
0
1996 1998 2000 2002 2004 2006 2008
Atya lanipes Gravid (%) Middle Pool
100
c)
80
60
40
20
0
1996 1998 2000 2002 2004 2006 2008
Atya lanipes Gravid (%) Lower Pool
100
e)
80
60
40
20
0
1996 1998 2000 2002 2004 2006 2008
Time (Years)
Xiphocaris elongata Gravid (%) Upper Pool
a)
100
Xiphocaris elongata Gravid (%) Middle Pool
Atya lanipes Gravid (%) Upper Pool
100
100
Xiphocaris elongata Gravid (%) Lower Pool
143
100
b)
H.Georges
80
LRF
HRF
60
40
20
0
1996 1998 2000 2002 2004 2006 2008
d)
80
60
40
20
0
1996 1998 2000 2002 2004 2006 2008
f)
80
60
40
20
0
1996 1998 2000 2002 2004 2006 2008
Time (Years)
Fig. 5-1 Percentage of gravid females of Atya lanipes and Xiphocaris elongata across time
(1997-2007), rainfall periods (HRF and LRF), and pools (Upper, Middle and, Low altitude) in
Quebrada Prieta. Vertical line during 1998 represents the impact of Hurricane Georges. a) Atya
lanipes upper pool; b) Xiphocaris elongata upper pool; c) Atya lanipes middle pool; d)
144
Xiphocaris elongata middle pool; e) Atya lanipes lower pool, and f) Xiphocaris elongata lower
pool.
145
100
1997
1998-H.Georges
1999
2000
2001
2002
2003
2004
2005
2006
2007
Total
a) Atya lanipes
Annual Frequency (%)
80
60
40
80
60
40
20
20
Total Frequency (%) 1997-2007
100
0
0
0-5
6-11
12-17
18-23
24-29
Class Size (mm)
100
1997
1998- H.Georges
1999
2000
2001
2002
2003
2004
2005
2006
2007
Total
b) Xiphocaris elongata
Annual Frequency (%)
80
60
40
80
60
40
20
20
Total Frequency (%) 1997-2007
100
0
0
0-3
4-7
8-11
12-15
16-19
20-23
Class Size (mm)
Fig. 5-2 Annual frequencies of size classes in populations of a) Atya lanipes and b) Xiphocaris
elongata during 1997 to 2007. Bars represent frequency of shrimp per year and line represents
146
total frequency of shrimp during 10 years of sampling.
147
17
H.Georges
Atya lanipes
Xiphocaris elongata
16
Mean CL (mm)
15
14
13
12
11
1996
1998
2000
2002
2004
2006
2008
Time (Years)
Fig. 5-3 Relationship between average growth (+ SE) of the shrimp Atya lanipes (n = 10) and
Xiphocaris elongata (n = 12) and the years of the experimental period in Quebrada Prieta.
Vertical line represents the impact of Hurricane Georges. Solid (Atya lanipes) and dotted
(Xiphocaris elongata) lines represent linear regressions (cephalothorax- CL). Atya lanipes, CL =
0.2756*Time - 532.75; r2 = 0.69, P < 0.003; Xiphocaris elongata, CL = 0.0843*Time - 155.88, P
= 0.156; r2 = 0.21.
148
CHAPTER 6
EVALUATION OF A WEB-BASED EDUCATION PROGRAM: COMMUNICATING
ECOLOGICAL KNOWLEDGE TO THE PUBLIC ABOUT THE LUQUILLO
EXPERIMENTAL FOREST 5
Abstract
Increasing local knowledge about freshwater biota and enhancing communication
between the scientific community and local populations were the main objectives for developing
an educational program about the ecology of rivers in Puerto Rico. Two websites (River
Education Program and Programa Educativo sobre Rios) with posters, fact sheets, taxonomic
keys, scientific articles, plots, and pictures were developed to present ecological information
regarding the Luquillo mountain streams to Spanish and English-speaking audiences. This study
reports visitors’ behavior over 24 months after the release of the two websites. In total there were
12,343 sessions were reported for the websites. Both websites were used by Spanish and English
speakers from diverse local, national and international locations. Most of the connections were
from locations in Puerto Rico with universities and/or research centers with active research on the
island. Keyword searches were the most common method to reach the websites; ‘Abiotic and
Biotic Factors’, ‘Taxonomic Key’, and ‘El Yunque Rainforest’ were the pages with the most
sessions and pageviews. This educational program provided the opportunity to develop a
complete and integrative educational program that presents new scientific findings in the Luquillo
Mountains in order to increase knowledge about the freshwater biota. This information pathway
can help in highlighting the value of conserving these resources.
5
Coauthored by Omar Pérez-Reyes, Mark Brunson, Todd A. Crowl, and Alan P. Covich
149
Keywords. biodiversity, decapods, El Yunque National Forest, Puerto Rico, river education,
tropical streams, website
Introduction
The Internet reaches increasingly large numbers of people in many countries and
provides up-to-date information in a wide range of formats. The combination of text, multimedia,
and user-interactive technology makes the Internet extremely effective for the dissemination and
acquisition of knowledge (Flanaging and Metzger 2001; Morris and Ogan 1996; Dworak et al.
2014). The results of peer-reviewed field and experimental studies can have a profound impact in
the lives of citizens given the increased accessibility and relatively low cost. The use of the
Internet to support scientific communication is one of the major developments in the practice of
ecology (Hurd 2000; van Raan 2001).
The public today is more aware of the many ecological and environmental issues that
impact everyday life than ever before. A main barrier in the acquisition of this new knowledge
remains a lack of sufficient scientific literacy (Rickinson 2001; Bickford et al. 2012). People
obtain limited or oversimplified information about environmental and conservation issues from
sources that are sometime biased, leading to misconceptions and wrong or incomplete
interpretations of the ecological and environmental problems (Coyle 2005; Ladle et al. 2005).
Communicating ecological science to non-scientists is one of the most important challenges
(Sunderland et al. 2009).
Puerto Rico’s population has increased at a high rate with most of the growth in the major
metropolitan areas (Ramirez et al. 2012; Gould et al. 2012). This growth results in a significant
increase in both residential and industrial development and a corresponding decrease in habitat
for fish and wildlife (Gould et al. 2012). One of the significant habitat alterations has been to
wetlands and watersheds. Puerto Rico has lost and continues to lose wetlands at an alarming rate
150
(Martinuzzi et al. 2009). Riparian forests and wetlands are especially important as they provide
habitats for freshwater shrimp (Pérez-Reyes 2014), fishes, and wildlife (Ramos-Scharron et al.
2015). These ecosystems also produce important services such as flood control, groundwater
recharge, filtration of organic materials, storage and recycling of nutrients, control of erosion as
well as reduced transport of sediment and pollutants. It is especially important for the public and
policy makers to protect the island's remaining wetlands and riparian forests. These habitats used
by diverse species help provide clean water that is essential to maintaining recreational fisheries
and other freshwater benefits (Lugo et al. 2011).
In Puerto Rico, the El Yunque National Forest in the Luquillo Mountains (also known as
the Luquillo Experimental Forest –LEF) represents a location where scientists, technical experts,
and the general public converge daily. The LEF serves as a site for research by scientists from
the United States, especially Puerto Rico, and many other countries around the world. The LEF
is uniquely suited for research in tropical rainforests because the ecological life zones are
representative of the many other tropical forests. The LEF has served as a living laboratory since
1942 when the land was recognized as important for watershed protection and later for
experimentation about forest productivity following disturbances (Odum and Pigeon 1970),
effects of hurricanes on the biota (Covich et al. 1991), nutrient cycling in the ecosystem
(Heartsill-Scalley et al., 2012), effects of urbanization (Ramirez et al. 2009; 2012; Thomlinson
and Rivera 2000), hydrological cycles and water budgets (Scatena 1989; Covich et al., 2003),
meteorology (Jennings et al. 2013; 2014), recreational use of the forest (Kartchner 2002; Santiago
and Loomis 2009), and many other initiatives funded by governmental agencies and universities.
The data and results of this research are in academic and research libraries that are largely
inaccessible to the general public or the local inhabitants. Moreover, the lack of communication
between scientists and the general public, frequent misconceptions, and absence of general
151
information about environmental and ecological issues have often resulted in degradation of the
natural resources of the island.
Our experiences with the island’s community, general public, graduate and undergraduate
students led us to develop an outreach program that includes two educational websites: River
Education Program and Programa Educativo sobre Ríos. This study investigates the use of these
websites to answer the following research questions: 1) How often do visitors use the websites,
from which countries, number of page views and how much time spend on each one?, and 2)
Does language represent a problem for users of the websites?
Methods
The River Education Program (REP) has a version in English as well as one in Spanish
named Programa Educactivo sobre Ríos (PER). These websites present a synthesis of
information from field observations and laboratory experimental results based on the scientific
literature in colloquial language so that the scientific and non-scientific public can find the
answers to most common issues related to freshwater ecosystems in Puerto Rico. The REP and
PER were designed as web-based learning environments with an interactive learning interface
(Khalifa and Lam 2002) where the learner can interact and explore informational materials based
on the many ecological findings in the Luquillo Experimental Forest. The material is organized
into 13 sections (main menu) such as Archeology, Biological Resources, Ecosystems and
Landscapes, Education, El Yunque Tropical Rainforest, Literature, Luquillo-Long Term
Educational Research (Luq-LTER), Physical Resources, Researchers, River and Stream
Terminology, River and Streams, Species List , and Taxonomic Key. Each section is
accompanied by a brief description of the main topic with a series of pictures, hyperlinks, and
educational materials that can be downloaded and printed. The materials in the REP/PER have
explanations of ecological processes (e.g. amphidromous migration of shrimp and fishes),
152
descriptions of native and exotic species (e.g. plants, invertebrates, vertebrates, and fungi),
diagrams of the forest (forest vegetation types), streams (anatomy and morphology of the stream),
and descriptions of the interactions between the organisms in the food webs (food web of a
tropical rain forest). The pictures in each section show a descriptive representation of the
organisms and their interactions with other organisms. These pictures were selected to represent
the uniqueness of the Puerto Rican biota. Hyperlinks on the web pages are linked to websites of
different universities, local and federal agencies, and those individuals who collaborate with the
researchers at the LEF. In addition some hyperlinks connect to other relevant sections within the
website.
Data Collection
To assess usage of the websites we used Google Analytics (GA), a web analytic tool that
provides data summaries and visualizations about visitors and users to facilitate evaluation of
website performance (Clifton 2012).
Data on website sessions were collected during two years (2012 and 2013) after the
release of the sites. The period of 24 months was selected to ensure enough data and time to
identify trends in the site usage. To analyze the usage of the websites the number of sessions,
pageviews, users, and bounce rate were measured (Burby and Brown 2007; Booth and Jansen
2009). For the analyses, “sessions” were defined as the number of individual sessions initialed by
the visitors to the site. “Users” were those visitors who viewed or interacted with the content
within a specific date range. “Pageviews” were the visitors who viewed a page on the site and
tracked from the beginning to end of their visit. “Bounce rate” was defined by the percentage of
visitors who enter the website and leave the site (single page sessions). All the data were
generated using GA.
153
Data were graphed and sorted to identify patterns of the use over time. Visitors to the
websites were characterized by geographic distribution (country and city), language, and
keywords used. Differences in the number of sessions, pageviews, and bounce rate were
compared between years (2012 and 2013) and among months with Two-way ANOVAs.
Results
River Education Program. Since the REP was released in January 2012, it received 7219
sessions that viewed 12316 pages (Fig. 6-1a). A total of 12.5 % of the visitors were classified as
returning visitors (906), while 87.5 % were new visitors to the website. During 2012 the monthly
number of visits ranged from 81-326 while in 2013 the monthly visits ranged from 190-868. The
highest number of visits was registered during September 2013. The site is visited most heavily
during January-May and August-November (Fig. 6-2a). New visitors viewed an average of 1.49
pages with an average time expended in the site of 55 seconds; returning visitors viewed 3.2
pages with an average time of 205 seconds. The largest visit had duration of 45 minutes. A twoway ANOVA to compare the number of visitors per year and among months showed significant
differences in the number of visits between years (F1,11= 33.6; p< 0.0001) and among months
(F1,11= 4.9; p= 0.007). Significant differences in the page views were observed between years
(F1,11 = 681; p=0.02) and among months (F1,11 = 3.5; p=0.02).
Visitors from 119 countries or territories visited the REP; most were from the United
States mainland, Puerto Rico, Australia, United Kingdom, Canada, India, Philippines, Colombia,
Indonesia, and Mexico (Fig. 3a). Visitors from United States mainland accessed the web page
more frequently than any other country with more than 4676 visits in two years. The average
bounce rate for these countries ranged between 92 (Mexico) to 61 % (Puerto Rico).
The percentage of users who accessed the site through search engines was 93 %; only 4
% reached the website through a referral site and only 3 % as a direct URL (Uniform Resource
154
Locator). Thirteen keywords were used at least 10 times to locate the site (Table 6-1). The most
common keywords used to reach the web pages were ‘Abiotic and biotic factors’, ‘Taxonomic
key’ and ‘Freshwater insects.’
Visitors in different nations chose different pages to visit. Comparison of the flow data
for the United States, Puerto Rico, Australia and Canada showed that the starting pages were
similar among the countries (Home Page, Physical Resources-Water, Rain Forest, Luquillo LTER
and Abiotic and Biotic Factors). However, visitors from Australia and Canada moved to
Archeology and River and Streams pages, while the visitors from the US and Puerto Rico also
visited the Rain Forest, Biological Resources, and Luquillo-LTER.
The analysis of the visitors by their origin showed that in the United States the most visits
were from Texas (N=879 sessions), California (N=270), Florida (N=257), Georgia (N=221),
Illinois (N=219), and New York (N=207). Visitors from these states spent between 51 to 110
seconds on the site and visited 1.4 to 2.1 pages per session. North Dakota (N=5), South Dakota
(N=5), and Delaware (N=1) were the states with the lower number of sessions in the REP.
The numbers of visits from Puerto Rico to the REP site were 205 in 2012 and 408
sessions in 2013; 248 of these sessions were originated in the San Juan Metropolitan Area, which
included the municipalities of San Juan, Cataño, Bayamón, Carolina, Trujillo Alto, and
Guaynabo; the other 365 visits came from additional cities around the island. The cities with the
highest number of visitors registered were San Juan (N=148), Río Piedras (N=66), Caguas
(N=44), Bayamón (N=25), Mayagüez (N=20), and Luquillo (N=19). The cities with the lower
bounce rate and higher number of pages per session were Luquillo and Carolina, the cities nearest
to the LEF. Users from Luquillo visited 3.2 pages per session for a 32% of bounce rate while
users from Carolina visited 4.0 pages per session, resulting in a bounce rate of 40%. San Juan,
Rio Piedras, Caguas, Bayamon and Mayaguez had averaged bounce rates that ranged between 52
155
to 75%. In general each visitor viewed an average of 2.6 pages per session and spent an average
of 128 seconds per session.
Programa Educativo sobre Rios. The PER was designed to reach the Spanish-speaking
communities. Since it was released in 2012, the webpage received 5116 sessions, where 4656
were new visits and 460 returning (Fig. 6-1b). The average number of pages viewed per visit was
1.3 pages per session and the average visit time was 57 seconds. In the PER an increase in the
average monthly sessions were observed from February to July and from August to December.
The smallest number of sessions was observed during January 2012 (N=24) and the largest in
December 2013 (N=527). Higher numbers of page views were observed during NovemberDecember of each year (2012- 609 and 2013- 671 page views) (Fig. 6-1b). Highly significant
differences were observed in the number of visitors to the website among months (F1,11=9.7; p<
0.0001) and between years (F1,11=36.7; p< 0.0001). The monthly page views ranged between 38
to 609 in 2012 and 168 to 665 during 2013. The comparisons of monthly page views between
years (F1,11=35.7; p< 0.0001) and among months (F1,11=12.5; p< 0.0001) were also highly
significant (Fig.6-1b, 6-2b).
Visitors from 48 countries reached the Programa Educativo sobre Rios during 2012 and
2013. The most common visitors were from Mexico (N = 1340), Colombia (N = 1101), Puerto
Rico (N = 656), Venezuela (N = 435), United States (N = 291), Spain (N = 232), El Salvador
(N=168), Peru (N=161), Argentina (N=153), Ecuador (N=103), and Guatemala (N=98) (Fig. 63b). Visits from another 37 countries were observed in the PER. Most of these visitors (95%)
reached the website after a search in their preferred browser, 4% from direct traffic, and 1% from
referral traffic. Of the 5116 sessions, 744 reached PER using the following keywords: “Factores
Abióticos y Bióticos del Río” (Abiotic and Biotic factors of the Stream), “Claves Taxonómicas”
(Taxonomic Keys), “Bosque Lluvioso el Yunque” (EL Yunque Rain Forest), “Terminología de
Ríos” (Stream Glossary), and “Petroglifos Taínos” (Taíno Petroglyph) (Table 6-1). The visitors
156
from Puerto Rico were primarily from San Juan (N=187), Caguas (N=127), Bayamón (N=44),
Ponce (N=44), and Mayagüez (N=25). More than 40% of visits (N=277) were from the San Juan
metropolitan area.
Discussion
The River Education Program and the Programa Educativo sobre Ríos websites were
developed to make ecological information from research at the Luquillo Experimental Forest
easily accessible to local people and the general public. Our analyses clearly show that people
from Puerto Rico and other countries are interested in obtaining this information to understand
the importance of ecological resources of a tropical rainforest. Education about the streams and
rivers of Puerto Rico plays an important role in the understanding more about these ecosystems
(Reagan and Waide 1996; Brokaw et al. 2012). The information provided to the visitors to these
websites likely helped them to understand the ecosystems, their services and the importance of
sustaining these ecosystems. Current efforts contribute to making the general public more
successful in searching available resources.
Overall, the results of this study point to a positive use of the web-based education
program by the visitors. These websites were designed to reach the local public of Puerto Rico,
but the impacts were observed internationally. Not only do local individuals who use the
websites tend to have higher number of sessions, they also are more likely to explore more pages,
and tend to search deeper into the content of the websites. The high number of visits suggests
that the River Education Program and Programa Educativo sobre Rios have useful content. These
results are encouraging signs that web-based communication technologies can have a positive
impact on a wide audience. The analyses of keywords and the major search engines show that the
number of visits was increasing through time and may be likely to continue doing so.
157
The numbers of visits suggest that many people view the content; most visits to the sites
are of very short duration. The low number of pages viewed per visit and the low amount of time
spent on each page probably reflect either that visitors find the information quickly in their first
visit, or that the website does not sufficiently reflect their interest. This observation supports
previous reports where Internet users tend to move quickly from one site to another, clicking on
the first thing that draws their attention (Krug 2006). The increasing access to the REP/PER sites
through search engines reflected that the public is looking for information about freshwater
ecosystems. The tendency to search information through search engines is now commonplace in
Internet users.
The most popular content areas were the web pages about water and abiotic and biotic
factors. Most of the users arrived to these web pages after a search using the keywords “abiotic
biotic factors”, “taxonomic keys”, “El Yunque Rainforest”, and “freshwater insects”. Other
keywords can be separated by technical topics (e.g. Hirudinae, river ecosystem, Atyidae, food
web) and vernacular or local words (e.g. taíno petroglyph, snails, streams and rivers, Yukiyu, and
buruquena). This result reflects the behavior of two focal groups: 1) people with knowledge in
ecological process (e.g. students, investigators), and 2) people interested in recreation (e.g.
tourists and local individuals). The research and focused web visitors use technical terminology,
visit different pages in the website, look for a deeper search and repeat the visit returning directly
to the page of interest (direct traffic) (Booth and Jensen 2009). Meanwhile, users looking for
tourist information (browsing visitors) are people who search the site for specific information
about an activity or location. This type of visit would likely result in higher bounce rates, lower
numbers of page views, and shorter sessions.
The second group of website visitors appears to be looking for general information about
El Yunque and its resources. This group is composed of local people and tourists who search to
identify recreational sites in the forest. These findings are congruent with observations by
158
Kartchner (2003) that most of the people who visit the El Yunque National Forest are looking for
a site to relax, spend time with family, and enjoy the natural setting. People who visit the streams
at El Yunque seek to identify the appropriate pools or areas around streams for different types of
use (Santiago and Loomis 2009). Both studies showed an interest in the water as a recreational
resource.
Most visits to the websites occurred during the months of January to May and August to
November. These users reached the websites through a search engine with precise keywords.
These visitors discovered the selected web pages, and likely obtained the ecological information
they wanted and then exited the websites. The duration of the visits was relatively short. The
times of high use in the websites are congruent with the academic semesters of the universities
and schools in United States and Puerto Rico. During these months the students start looking up
information for their research, projects, laboratories or exams. Higher average of use of the
sessions and the lower bounce rates in the PER during the months of June and July coincide with
the Luquillo-LTER Research Education for Undergraduates Program (REU). In the REU
program the students develop research projects and the mentors promote the use of the website as
source of scientific information and articles (personal observation).
The geographical origin of the visitors coincides with the usage of the web pages during
the academic semester. Most of the visits to the websites were from states of the United States
(e.g. Texas, California, New York, Illinois, Florida, Georgia) with higher concentrations of
Hispanics (including Puerto Ricans) and universities with connections to research centers in
Puerto Rico. The users from Puerto Rico came from cities with higher concentrations of people,
and higher-education centers: San Juan, Bayamón, Mayagüez, Caguas, and Cayey.
The websites and their resources were used primary by people from outside of Puerto
Rico rather than local residents. The differences may be the results of low knowledge locally
about the Internet as well as language problems. English speakers used the River Education
159
Program more frequently than those who speak other languages; meanwhile as expected, the
Programa Educativo sobre Rios was used primarily by visitors from Spanish-speaking countries.
According to available data, the Internet in the United States is used by 78% of all English
speakers, 77% of Latinos who are English dominant or bilingual, but only 32 % of the Spanishdominant Latinos (Fox and Livingston 2007). Only two-thirds of the population in Puerto Rico
use or have access to the internet; most of the users tend to be younger and educated (Internet
World Stats Miniwatts Marketing Group 2011). Puerto Rico is among the most advanced
telecommunication markets in America, with 2 million Internet users, and there is a large Spanish
speaking population in the mainland United States. Internet users on the island apparently prefer
to visit local websites and previously known web pages (SME Digital and Mobile Behavioral
Study Puerto Rico 2014). Increasing Spanish language content available online removes a barrier
to access and will increase the use among Spanish-speaking populations.
Geographic variability in the website users was considerable in Puerto Rico. Users
seeking information occurred most frequently in the regions surrounding the San Juan
Metropolitan Area. Not surprisingly, we observed a pattern of a higher prevalence of Internet use
in regions with a greater proportion of people with higher education. This observation is also
likely exacerbated by the fact that the most rural communities in Puerto Rico still have limited or
poor Internet access. In Puerto Rico 60% of the population has Internet access, and 80% of the
users connect to the Internet from their jobs or universities (SME Digital and Mobile Behavioral
Study Puerto Rico 2014).
In conclusion, we demonstrate rapid uptake of multimedia tools designed to present the
ecological information derived from research at LEF to the general public. The use of these tools
showed a gradually increase with positive results and comments. Most users of the sites were
people with knowledge of the Internet, seeking information about ecological aspects, and English
speaking. Ecological education and outreach efforts should continue to explore the use of
160
available methods of dissemination, as well as community based programs or activities, and
organizations, to supplement and encourage use of the internet as a source of information. To
further increase the number of visitor on the websites it may be valuable to create links to social
media. Web-based scientific information offers important opportunities for access to an
increasing amount of knowledge and information. One role of professional researchers is to
ensure that the learning environment provided takes account of users’ needs and ensures that they
effectively understand the ecological information. Online learning has advantages, but webbased learning should not always be viewed as the method of choice because barriers (such as
inadequate equipment) can easily detract from student learning. The technology can be applied
appropriately for most users but cannot be used everywhere because some people still have
particular limitations to access the Internet.
Acknowledgments
We thank the many people who helped in the field, with special appreciation of the
fieldwork done by many undergraduate and graduate students. This research was supported by
grants BSR-8811902, DEB 9411973, DEB 0080538, DEB 0218039 and DEB 0620910 from the
National Science Foundation (NSF) to the Institute for Tropical Ecosystem Studies, University of
Puerto Rico, and to the International Institute of Tropical Forestry, United States Department of
Agriculture (USDA) Forest Service, as part of the Long-Term Ecological Research Program in
the Luquillo Experimental Forest. The USDA Forest Service and the University of Puerto Rico
gave additional support.
161
Literature Cited
Bickford, D., Posa, M.R.C., Qie, L., Campos-Arceiz, A., Kudavidanage, E.P. (2012). Science
communication for biodiversity conservation. Biological Conservation. 151,74-76.
Booth, D., Jansen, B. J. (2009). A review of methodologies for analyzing websites. Web
Technologies: Concepts, Methodologies, Tools, and Applications: Concepts,
Methodologies, Tools, and Applications, 145.
Brokaw, N. (Ed.) (2012). A Caribbean forest tapestry: the multidimensional nature of
disturbance and response. Oxford University Press.
Burby, J., Brown, A. (2007). Web analytics definitions. Washington DC: Web Analytics
Association.
Clifton, B. (2012). Advanced web metrics with Google Analytics. John Wiley and Sons.
Covich, A.P., Crowl, T.A., Johnson, S.L., Varza, D., Certain, D.L. (1991). Post-hurricane Hugo
increases in atyid shrimp abundance in a Puerto Rican montane stream. Biotropica, 23,
448-454.
Covich, A.P., Crowl, T.A., Scatena, F.N. (2003). Effects of extreme low flows on freshwater
shrimp in a perennial tropical stream. Freshwater Biology ,48,1199-1206.
Coyle, K. (2005). Environmental Literacy in America. The National Environmental and Training
Foundation, Washington, D.C.
Dworak, B.J., Lovett, J., Baumgartner, F.R. (2014). The Diversity of Internet Media: Utopia or
Dystopia? Midwest Political Science Association Meeting, pp 42.
Flanagin, A.J., Metzger, M.J. (2001). Internet use in the contemporary media environment.
Human Communication Research 27,153-181.
Fox, S., Livingston, G. (2007). Latinos online: Hispanics with lower levels of education and
English proficiency remain largely disconnected from the Internet. Pew Hispanic Center,
Washington, DC, 16 p.
Gould, W. A., Martinuzzi, S., Parés-Ramos, I. K. (2012). Land use, population dynamics, and
land-cover change in Eastern Puerto Rico. In S.F. Murphy, R.F. Stallard (Eds), Water
Quality and Landscape Processes of Four Watersheds in Eastern Puerto Rico.
Professional Paper 1789–B
Heartsill-Scalley, T., Scatena, F.N., Moya, S., Lugo, A.E. (2012). Long-term dynamics of organic
matter and elements exported as coarse particulates from two Caribbean montane
watersheds. Journal of Tropical Ecology, 28,127-139.
Hurd, J.M. (2000). The transformation of scientific communication: A model for 2020. Journal of
the American Society for Information Science, 51,1279-1283.
162
Internet World Stats Miniwatts Marketing Group (2011. Website Usage and Population Statistics
http://www.internetworldstats.com/
Jennings, L.N., Treasure, E.A., McNulty, S.G. (2013). Climate Change and Your National Forest:
Assessing the potential effects of climate change on the El Yunque National Forest (peer
reviewed fact sheet), 1-4 p.
Jennings, L.N., Douglas, J., Treasure, E., González, G. (2014). Climate change effects in El
Yunque National Forest, Puerto Rico, and the Caribbean region. General Technical
Report SRS-GTR-193. Asheville, NC: USDA-Forest Service, Southern Research Station,
47 p.
Kartchner, S.C. (2003). Recreational shrimping in montane streams of the Puerto Rico. Acta
Científica, 17,39-57.
Khalifa, M., Lam, R. (2002). Web-based learning: effects on learning process and outcome.
Education, IEEE Transactions on, 45.350-356.
Krug, S. (2009). Don't make me think: A common sense approach to web usability. Pearson
Education.
Ladle, R.J., Jepson, P., Whittaker, R.J. (2005). Scientists and the media: the struggle for
legitimacy in climate change and conservation science. Interdisciplinary Science
Reviews, 30,231–240.
Lugo, A.E., González, O.M.R., Pedraza, C.R. (2011). The Río Piedras watershed and its
surrounding environment. International Institute of Tropical Forestry, USDA Forest
Service 52 p.
Martinuzzi, S., Gould, W. A., Lugo, A. E., Medina, E. (2009). Conversion and recovery of Puerto
Rican mangroves: 200 years of change. Forest Ecology and Management, 257,75-84.
Morris, M., Ogan, C. (1996). The Internet as Mass Medium. Journal of Computer-Mediated
Communication, 1: 0. doi: 10.1111/j.1083-6101.1996.tb00174.x
Odum, H. T., Pigeon, R.F. (1970). A tropical rain forest: a study of irradiation and ecology at El
Verde, Puerto Rico. R. F. Pigeon (Ed.). Division of Technical Information, US Atomic
Energy Commission.
Pérez-Reyes, O. (2014). Population dynamics of the freshwater decapods in response to
ecological and anthropogenic factors in Puerto Rican tropical streams. PhD Dissertation.
Ramírez, A., de Jesús-Crespo, R., Martinó-Cardona, D.M., Martínez-Rivera, N., BurgosCaraballo, S. (2009). Urban streams in Puerto Rico: what can we learn from the tropics?
Journal of the North American Benthological Society, 28,1070-1079.
Ramírez, A., Engman, A., Rosas, K.G., Pérez-Reyes, O., Martinó-Cardona, D.M. (2012). Urban
impacts on tropical island streams: some key aspects influencing ecosystem response.
Urban Ecosystems, 15,315-325.
163
Ramos-Scharrón, C. E., Torres-Pulliza, D., Hernández-Delgado, E. A. (2015). Watershed-and
island wide-scale land cover changes in Puerto Rico (1930s–2004) and their potential
effects on coral reef ecosystems. Science of the total environment, 506, 241-251.
Reagan, D. P., Waide, R. B. (Eds.) (1996). The food web of a tropical rain forest. University of
Chicago Press.
Rickinson, M. (2001). Learners and learning in environmental education: a critical review of the
evidence. Environmental Education Research, 7,207–320.
Santiago, L.E., Loomis, J. (2009). Recreation benefits of natural area characteristics at the El
Yunque National Forest. Journal of Environmental Planning and Management, 52,535547.
Scatena, F.N. (1989). An introduction to the physiography and history of the Bisley Experimental
Watersheds in the Luquillo Mountains of Puerto Rico. US Forest Service. General
Technical Report SO-72.
Sunderland, T., Sunderland-Groves, J., Shanley, P., Campbell, B. (2009). Bridging the gap: how
can information access and exchange between conservation biologists and field
practitioners be improved for better conservation outcomes? Biotropica, 41,549–554.
SME Digital and Mobile Behavioral Study Puerto Rico. (2014).
https://ddblatinapuertorico.wordpress.com/2014/05/19/sme-digital-mobile-behavioralstudy-2014-puerto-rico/
Thomlinson, J. R., Rivera, L. Y. (2000). Suburban growth in Luquillo, Puerto Rico: some
consequences of development on natural and semi-natural systems. Landscape and
Urban Planning, 49,15-23.
van Raan, A.F. (2001). Bibliometrics and Internet: Some observations and expectations.
Scientometrics, 50,59-63.
164
Table 6-1 List of the frequently used-keywords to search information and the number of sessions
observed in the REP and PER websites during 2012-2013.
Number
Number
Keywords (REP)
of
Keywords (PER)
of
Sessions
Sessions
Biotic and abiotic factors of
rivers
1710
Factores bioticos y abioticos/Biotic
and Abiotics Factors of Rivers
433
Taxonomic key
57
Claves taxonómicas/Taxonomic Keys
259
Freshwater insects
53
Bosque Lluvioso El Yunque/El
Yunque Rain Forest
30
Hirudinidae
45
Terminología ríos/River Terminology
22
Taino petroglyphs
40
Taíno petroglifo/ Taíno Petroglyphs
21
Streams and rivers in El
Yunque
33
Crustáceos de agua dulce/Freshwater
Crustacea
17
River Education Program
28
Caracoles/ Snails
13
River ecosystem plants and
animals
14
Rios y quebradas en El Yunque/ River
and Streams from El Yunque
12
Luquillo LTER
12
Bacterias/ Bacteria
11
El Yunque monthly
temperature
11
Yukiyu
11
River habitats
11
Hongos/ Fungi
9
Bacteria in El Yunque
10
Oro en los ríos de El Yunque/Gold in
Rivers of El Yunque
9
Rivers and streams food web
10
Bosque de Tabonuco/Tabonuco
Forest
8
165
Table 6-2 Landing pages for the user of the websites and the percentage of sessions in the REP
and PER during the years 2012 and 2013.
River Education Program
Landing Page
Programa Educativo en Ríos
Sessions (%) Landing Page
Sessions (%)
Physical Resources-Water
65.0
Abiotic and Biotic Factors
37.2
Abiotic and Biotic-Factors
5.0
Taxonomic Keys
34.5
Home
4.1
Water
6.7
El Yunque Tropical Rain Forest
3.4
El Yunque Rain Forest
4.7
Luquillo-LTER
3.2
Glossary
4.4
Archeology
2.4
Archeology
3.1
Taxonomic Keys-Annelida Leeches
2.2
Fungi
2.5
Ecosystems and Landscapes
2.0
Shrimps and Crabs
1.5
Taxonomic Keys-Freshwater Insects
1.8
Home
1.4
El Yunque Rivers and Streams
1.8
Geology
1.0
Vegetation
1.7
Vegetation
0.8
Glossary
1.6
Ecosystems and landscapes
0.6
Taxonomic Keys
1.6
Insects
0.6
Literature
1.5
Rivers and streams
0.4
Rivers and Streams
1.4
Arachnids
0.3
166
1200
1000
a)
Visits
Pageviews
800
Number of Sessions or Pageviews
600
400
200
0
b)
600
400
200
0
12 12 12 12 12 12 12 12 12 12 12 12 13 13 13 13 13 13 13 13 13 13 13 13
n- eb- ar- pr- ay- un- Jul- ug- ep- ct- ov- ec- an- eb- ar- pr- ay- un- Jul- ug- ep- ct- ov- eca
J F M A M J
A S O N D J F M A M J
A S O N D
Time:Month-Year
Fig. 6-1 Monthly number of sessions and pageviews of the users of the websites during the years
2012 and 2013: a) River Education Program, b) Programa Educativo sobre Ríos. Gray area
represent number of pageviwes and black area number of visits to the REP and PER.
167
100
800
Sessions
Bounce Rate
a)
80
600
60
400
200
20
0
500
0
100
Sessions
b)
400
80
300
60
200
40
100
20
0
y
y
ch
ar
ar
ar
ru
nu
M
b
a
e
J
F
A
il
pr
M
ay
ne
Ju
J
uly
r
r
r
r
st
be
be mbe mbe
gu
o
m
t
u
e
A
ce
ve
Oc
pt
De
No
Se
Average Bounce Rate
Average Monthly Sessions
40
0
Time:Months
Fig. 6-2 Average monthly sessions (+ Standard Error) and bounce rates (+ SE) for the REP (a)
and PER (b) during the years 2012 and 2013. Closed circle represent bounce rate, open square
the sessions in the REP and closed gray square the sessions in the PER.
168
United States
a)
Puerto Rico
Australia
United Kingdom
Canada
India
Philippines
Colombia
Country/Territories
Indonesia
2012
2013
Mexico
Percentage of sessions in the REP web site
Mexico
b)
Puerto Rico
Colombia
United States
Venezuela
El Salvador
Spain
Peru
Argentina
Ecuador
0
20
40
60
Percentage of sessions in the website (%)
Fig. 6-3 Percentage of sessions per country or territories in the REP (a) and PER (b) websites during 2012
(open bar) and 2013 (closed bar).
169
CHAPTER 7
SUMMARY AND DISCUSSION
The symptoms of the “Urban Stream Syndrome” (Walsh et al. 2005) flashy hydrographs,
elevated concentration of nutrients and contaminants, altered channel morphology, reduced
biodiversity and incorporation of non-native-tolerant species were found in the tropical streams of
Puerto Rico. The increase in urbanization as a threat to aquatic ecosystems, particularly tropical
island stream ecosystems, is of growing concern due to small amount of space available for
development. Urbanization within the riparian zone was considerably high in the lower valleys
near the coast compared to those upstreams or in the mountains where the urbanization was
minimum.
Insular tropical freshwater ecosystems are dominated by an unique native fauna of
macroinvertebrates and fishes adapted to survive flashiness (Ramírez et al. 2009), frequent
floods, and droughts (Covich et al. 2006). For example atyids shimps have modified hairy-chelae
to capture fine organic particcules and strong legs that permit the exploitation and survival of
flashy and steep streams. The other three families of decapods (Palaemonidae, Xiphocarididae,
and Pseudothelphusidae) are adapted to survive under these conditions but do not show
modifications in their appendages.
In the Caribbean the decapod freshwater fauna is represented by 5 families (Atyidae,
Palaemonidae, Pheudothelphusidae, Astacidae, and Xiphocarididae). All the shrimp and crab
families were found across all ecological life zones in Puerto Rico. The richest rivers, Río
Bayamón, Río Mameyes and Río Sabana, were located in the north part of the island. The
relatively rich and unaltered environment, presence of organic matter, longitudinal connectivity
and the physical-chemical variables may provide the conditions for which these streams are
important areas for the conservation of these aquatic animals. The diversity of freshwater
170
decapod fauna found in Puerto Rico was expected for an island of its size. It is comparable to
that of Hispaniola (19 taxa) and Jamaica (21 taxa). Detailed examination indicated that the
species-area relation among the Greater and Lesser Antilles was observed; larger islands have
more number and diverse habitats in contrast with the smaller ones (Losos & Losos 1996). The
diversity of the freshwater decapod group in the Caribbean Archipelago tends to be controlled
primary by the size of the island and the dispersion of the organisms. All freshwater shrimp in
the Caribbean exhibit an amphidromous life cycle where adults reproduce in the high elevation
sections of the streams and the larvae need to spend time in the estuary until metamorphose and
migrate to the upper locations of the freshwater bodies. This results in a common species pool
capable to colonize and migrate among the islands (Chapter 2).
The anthropogenic stressors increase the environmental pressure on macroinvertebrate
communities that can alter the biota in tropical streams (Ramírez et al. 2012). Urbanization
decreased the species richness and abundance of decapods communities in highly urbanized
valleys when were compared to forested headwaters or suburban reaches in different streams.
Also, the abundance of species and community structures in each stream showed variations
among different land-uses. However, the species richness was still relatively species rich even in
the urbanized watershed (11 of the 18 species that occur in Puerto Rico). Macrobrachium
faustinum and Xiphocaris elongata were the most tolerant species in the impacted sections of the
streams. Our study suggested that the loss of species richness and abundance of freshwater
decapods in urban streams was the result of a series of human stressors that degrade decapod
habitat. Urban streams reflected the impact of human activities in their hydrology,
geomorphology, water quality and aquatic biota. The effect of these stressors had an impact in
the species assemblages as well in the energy inputs in the stream. Changes in the land use
increased the erosion, sedimentation and water flow that changed the habitat heterogeneity and
the abundance and diversity of decapods in the stream. The relatively rich and unaltered
171
environment, presence of organic matter, longitudinal connectivity and the physical-chemical
variables may provide the conditions for which these streams are important areas for the
conservation of these aquatic animals. The alterations of the terrestrial environment as well the
construction of barriers to migration changed the local energy inputs and the longitudinal
connectivity among streams sections. These changes affected the organization and functions of
the stream communities (Paul and Meyer 2001) (Chapter 3).
Alterations and changes in the local input of organic matter in the streams resulted in
altered food web among low-impact, mid-impact and high-impact streams in Puerto Rico. The
carbon source for the primary, secondary and tertiary consumers were similar among streams;
variations were observed mainly in the amount of δ 15N. The enrichment in δ 15N had an impact
in all the tropic levels but primary change the order of the consumers positioning all together.
The urban rivers of Bayamón and Rio Piedras had concentrations of δ 15N higher than the normal
and in some occasions were three times the values observed in the reference stream of Sabana.
An excess in δ 15N marked a difference in trophic levels of the food web from urban streams in
comparison with the reference stream where the anthropogenic inputs are minimal. This showed
the importance of the organic matter in the ecosystem and the dependence of the freshwater biota
on the terrestrial inputs. Apparently the impact of the human activities on the stream and
watershed had a direct influence in the health and services of the ecosystem (Chapter 4).
Comparison of growth patterns of Atya lanipes and Xiphocaris elongata in 2nd order
streams of Luquillo Mountains showed that these tropical shrimp have: a) a relatively long live (>
15 years) with a slow growth rate; b) annual growth rates for Atya and Xiphocaris were 0.27 and
0.1 mm carapace length over the 10 year period; c) difference in growth rates between individuals
of A. lanipes and X. elongata over a range of temperatures, and time. In these streams water
temperature and food were the most important factors that influenced the growth rate. Inter-site
differences in growth rate could also be attributed to variability in retention of the leaf-litter
172
inputs from the riparian forest. Also, we found that hurricane and leaf-litter input affected growth
rates in some pools (Chapter 5).
Communicate results of any research is alwaysdifficult. Scientific investigations have
become more specialized and complicated to be trasmited and understood by the general public
(Bucchi 1996). Luquillo Mountains is the living laboratory for diverse researches that cover from
the effect of radiation on the forest (Odum 1970) to climate change and global warming models
(Comarazamy et al. 2013). Based in our experiences with the scientific community and the
general public we developed some educational tools those present the scientific information in a
common language and accessible for the general public (e.g. website, field activities, and training
program for teachers and students). In the present study we demonstrated the necessity to
increase the sources of ecological information available to the general public and the interest of
the local people to learn and understand their natural resources. We found a gap of information
between the scientists and the general public. The usage of these tools showed a gradually
increase with positive results and comments. Our results suggest that ecological education and
outreach efforts should explore the use of available and trusted methods of dissemination, as well
as community based programs or activities, and organizations, to supplement and encourage use
of the internet as a source of information (Chapter 6).
173
LITERATURE CITED
Bucchi M (1996) When scientists turn to the public: Alternative routes in science communication.
Public Understanding of Science, 5: 375-394
Comarazamy DE, González JE, Luvall JC, Rickman DL, Bornstein R D (2013) Climate Impacts
of Land-Cover and Land-Use Changes in Tropical Islands under Conditions of Global
Climate Change. Journal of Climate, 26:1535-1550
Covich AP, Crowl TA, Heartsill-Scalley T (2006) Effects of drought and hurricane
disturbances on headwater distributions of palaemonid river shrimp (Macrobrachium
spp.) in the Luquillo Mountains, Puerto Rico. Journal of the North American
Benthological Society, 25: 99-107
Losos JB, Losos JB (1996) Ecological and evolutionary determinants of the species-area
relation in Caribbean anoline lizards. Philosophical Transactions of the Royal Society of
London. Series B: Biological Sciences, 351: 847-854
Odum HT (1970) A tropical rain forest. A study of irradiation and ecology at El Verde, Puerto
Rico (No. PRNC--138; TID--24270). North Carolina University, Chapel Hill. Puerto
Rico Nuclear Center, Rio Piedras
Paul MJ, Meyer JL (2001) Streams in the urban landscape. Annual Review of Ecology and
Systematics 32:333-365
Ramírez A, de Jesús-Crespo R, Martinó-Cardona DM, Martínez-Rivera N, Burgos-Caraballo S
(2009) Urban streams in Puerto Rico: what can we learn from the tropics? Journal of the
North American Benthological Society 28:1070-1079
Ramírez A, Engman A, Rosas KG, Pérez-Reyes O, Martinó-Cardona DM (2012) Urban impacts
on tropical island streams: some key aspects influencing ecosystem response. Urban
Ecosystems 15: 315-325
174
Walsh CJ, Roy AH, Feminella JW, Cottingham PD, Groffman PM, Morgan II RP (2005) The
urban stream syndrome: current knowledge and the search for a cure. Journal of North
American Benthological Society Journal 24: 706-723
175
APPENDICES
176
Permission to reprint: Zootaxa (received July 7, 2015)
Dear Omar:
I herein grant the permission (one-off) for you to reproduce Zootaxa, 3717(3), 329-344 in your
dissertation at the Utah State University. The only condition is that you attribution is prior
publication in Zootaxa [sic].
Good luck,
Zhi-Qiang Zhang
Chief editor, Zootaxa
Permission to reprint: Freshwater Biology (received July 7, 2015)
Omar,
You do not actually need written permission to reproduce your article in your dissertation. See the
Permissions section on the journal website where it states “AUTHORS - If you wish to reuse
your own article (or an amended version of it) in a new publication of which you are the author,
editor or co-editor, prior permission is not required (with the usual acknowledgements).”
Roger Jones
177
CURRICULUM VITTAE
OMAR PÉREZ-REYES
Watershed Sciences Department, and The Ecology Center
Utah State University
5210 Old Main Hill, NR 210, Logan, UT 84322-5210
Phone: (435) 797-2459
E-mail: [email protected]
EDUCATION
2013
Ph.D. in Ecology
Dissertation: Population dynamics of the freshwater decapods in response to
ecological and anthropogenic factors in Puerto Rican tropical streams.
Utah State University, Logan, Utah (Advisor: Todd A. Crowl)
1999
M.Sc. in Biology
Dissertation: Abundances, Richness and Life Histories of Freshwater Decapods
of Puerto Rico
University of Puerto Rico, Rio Piedras (Advisor: Alberto Sabat)
1994
B.S. in Biology
Magna Cum Laude
University of Puerto Rico, Rio Piedras
RESEARCH INTERESTS
I am interested in biogeography, conservation, taxonomy, and systematics of freshwater
crustacean invertebrates of the Neotropics. I use two approaches to understand tropical diversity
and to answer questions about their biogeographic patterns, natural history, and evolutionary
history. I work on the most diverse groups of freshwater decapods (Atyidae, Palaemonidae, and
Pseudothelphusidae) in the Caribbean. I am also interested in the question of the effect of
anthropogenic factors on the diversity, abundance, distribution of other native and exotic
freshwater invertebrates (phenology, longitudinal connectivity, habitat, niche, and life cycle) in
urban and forested streams.
RESEARCH AND WORK EXPERIENCE
Teaching Experience
2013
Instructor. Center for Environmental Research and Conservation, Columbia
University, New York, New York.
2011-2012
Teaching Assistant (International Forestry & Natural Resources Management),
Utah State University, Logan, Utah.
2011
Instructor. Center for Environmental Research and Conservation, Columbia
University, New York, New York.
2011
Teaching Assistant (General Ecology), Utah State University, Logan Utah
2000-2007
Instructor (Zoology, Invertebrate Zoology, and General Biology), Department of
Biology, University of Puerto Rico, Rio Piedras.
2000-2007
Laboratory Coordinator (Zoology and Botany Labs), Department of Biology,
University of Puerto Rico, Rio Piedras.
178
1994-1999
1992-1994
Teaching Assistant (Zoology, Invertebrates, Ecology, General Biology, Topics in
Modern Biology, Freshwater Invertebrates of Puerto Rico) Department of
Biology, University of Puerto Rico, Rio Piedras.
Undergraduate Teaching Assistant (Zoology and General Ecology), Department
of Biology, University of Puerto Rico.
Research Experience
2007-2013
Research Assistant. Luquillo-Long Term Experimental Research (Luq-LTER).
Institute of Tropical Ecosystems, University of Puerto Rico, Rio Piedras.
Primary Investigators: Todd A. Crowl (Utah State University) and Alan P.
Covich (University of Georgia).
2007-2013
Research Assistant. San Juan Urban Long Term Research Area (San Juan Ultra).
USDA Forest Service International Institute of Tropical Forestry (IITF). Primary
Investigator: Ariel E. Lugo (International Institute of Tropical Forestry)
2007-2013
Research Assistant. “Population dynamics of the freshwater decapods in
response to ecological and anthropogenic factors in subtropical streams in the
Caribbean”. Supervisor: Todd A. Crowl.
2005-2007
Research Assistant. “Anatomy, arrangements and distribution of the motor
nerve in the pereiopods of Atya lanipes and Atya scabra”. Supervisor: Eduardo
Rosa-Molinar.
2002
Research Assistant. “Observations of sipunculid species of Puerto Rico”.
Supervisor: Eduardo Rosa-Molinar
1994-1999
Research Assistant. “Abundances, Richness and Life Histories of Freshwater
Decapods of Puerto Rico’. Supervisor: Alberto Sabat.
POSITIONS HELD__________________________________________________________
2012-2013
2012-2013
2000-2013
2010- 2012
1999-2007
Architects
2006- 2007
2005- 2007
2002-2005
1997- 1998
iUTAH, Education, Outreach and Diversity-Communication Team
Guest Editor. Acta Cientifica.
Environmental Scientist. Ferdinand Quiñones, PE, Consulting Water Resources
and Environmental Engineer
Graduate Student Representative Luquillo LTER
Environmental Scientist. Custodio Suarez and Associates Engineer and
(CSA). San Juan, Puerto Rico.
Academic Assistant, Department of Biology. UPR-RP
Representative, Biology Department at UPR, Middle States Association
Invertebrate Curator, Zoology Museum, Department of Biology, University of
Puerto Rico, Rio Piedras.
Graduate Student Representative, Graduate Biology Committee, UPR-RP.
179
PUBLICATIONS
Peer reviewed
Pérez-Reyes, O., Crowl, T.A., Hernández-García, P., Ledesma-Fuste, R., Villar-Fornes, F.A.,
Covich, A.P. (2013). Freshwater decapods of Puerto Rico: a checklist and reports of new
localities. Zootaxa 3717 (3): 329-344.
Ramírez, A., Engman, A., Rosas, K. G., Pérez-Reyes, O., & Martinó-Cardona, D. M. (2012).
Urbanimpacts on tropical island streams: some key aspects influencing ecosystem response.
Urban Ecosystems, 15(2), 315-325.
Pérez-Reyes, O., Brunson, M. Crowl, T. A. and Covich, A.P. (2011). Living in a watershed.
Network News Fall 2011: Vol 24: 2.
Publications in preparation
Pérez-Reyes, O., Crowl, T.A., Covich, A.P. Comparison of Neotropical decapod communities
across an urban-forest land use gradient in Puerto Rican streams. (Urban Ecosystems).
Pérez-Reyes, O., Crowl, T.A., Covich, A.P. Comparison of trophic relationships in contrasting
tropical streams in Puerto Rico: a stable isotopic study of food webs in urban and forested
watersheds. (Freshwater Biology).
Pérez-Reyes, O., Crowl, T.A., Covich, A.P. Effects of elevation, food supplies, and water
temperature on growth rates of freshwater topical shrimp in stream pools in the Luquillo
Mountains, Puerto Rico. (Freshwater Biology).
Pérez-Reyes, O. (editor) Ecosistemas de agua dulce de Puerto Rico. Acta Cientifica.
(December 2015).
Web Publications
2012 River Education Program- Educational website about how to live downstream.
(https://sites.google.com/a/ites.upr.edu/luquillo-lter/)
2013 Programa Educativo sobre Ríos- Pagina web educativa sobre como vivir agua abajo.
(https://sites.google.com/a/ites.upr.edu/programa-educativo-sobre-rios-luquillo-lter/)
Technical Reports
2009 Biological Consultant (Flora and Fauna Survey)- Cayo Vistas, Fajardo.
2008 Biological Consultant (Freshwater Fauna and Flora Survey)- Department of Public
Living, Vieques.
2006 Biological Consultant (Freshwater Flora and Fauna Survey) Rio Grande de Arecibo,
Utuado. http://www.gobierno.pr/NR/rdonlyres/4AB7B3B4-787D-4193-8BB5E2D95FA29647/0/3RioGADIAPEstudiodeFlorayFauna.pdf
2006 Biological Consultant (Fauna and Flora Survey)- Improvements Patillas-Arroyo
Puerto Rico Aqueduct and Sewer Authority.
2006 Biological Consultant (Fauna and Flora Survey)- Improvements San
Lorenzo and Caguas Water Supply Systems. Puerto Rico Aqueduct and Sewer Authority.
2005 Biological Consultant (Freshwater Fauna Survey)- Puerto Rico Aqueduct and
Sewer Authority, Río Grande, Puerto Rico.
2005 Biological Consultant (Tree Inventory and Mitigation Plan)- Marina Las Gaviotas
180
2005
2004
2004
2004
2003
2003
2002
1997
Development, Urbanización San Tomás, Naguabo.
Biological Consultant (Tree Inventory and Mitigation Plan)- Landfill Technologies
Corporation, Fajardo, Puerto Rico.
Biological Consultant (Flora and Fauna Survey; and Tree Inventory and Mitigation Plan)Betterroads- Empresas Diaz, El Olímpico, Salinas, Puerto Rico.
San Miguel Resort Wetland Delineation (Freshwater Fauna Survey), Luquillo, PR
Biological Consultant (Flora and Fauna Survey)- Department of Transportation, PR22, Arecibo- Aguadilla
Biological Consultant (Flora and Fauna Survey)- Department of Transportation, PR2, Arecibo- Aguadilla.
Biological Consultant (Flora and Fauna Survey)- Betterroads- Empresas Díaz, Los
Úcares, Salinas Puerto Rico.
Biological Consultant (Freshwater Fauna Survey)- Development of the Río
Grande de Arecibo Estuary Model. SuperAqueduct, Puerto Rico Aqueduct and Sewer
Authority.
Environmental Report, Agrichemical Caribe Inc. Manatí.
HONORS, AWARDS AND FELLOWSHIPS
2013
2013
2012
2012
2011
2010
2009
2007
2005
2002
2001
1999
1998
1997
1994
PhD Award, Graduate Studies Office, Utah State University.
Travel Award (North American Benthological Society, Florida), Dean Office, Natural
Resources College, Utah State University.
iUTAH Graduate Fellowship.
Travel Award (Congreso Latinoamericano de Macroinvertebrados Acuaticos, Costa
Rica), Dean Office, Natural Resources College, Utah State University.
Utah State University, Watershed Department and Ecology Center. Graduate Support
and Assistantship.
Travel Award (Society of Integrative and Comparative Biology, Seattle), Utah State
University, Watershed Department and Ecology Center.
Travel Award (North American Benthological Society, New Mexico), Watershed
Department and Ecology Center, Utah State University.
Utah State University, Watershed Department and Ecology Center. Graduate Support
and Assistantship.
Who’s Who Among America’s Teacher
Who’s Who Among America’s Teacher
Howard Hughes Foundation. Use of Multimedia in Botany and Zoology Laboratories.
Dr. José Ramón Ortiz Award- Graduate School of Biology, Department of Biology,
University of Puerto Rico, Río Piedras Campus.
Travel Award from President Office of the University of Puerto Rico- Annual
Meeting of the Society of the British Ecological Society, United Kingdom.
Travel Award from President Office of the University of Puerto Rico- Annual
Meeting of the Society of the British Ecological Society, United Kingdom.
Dean List, University of Puerto Rico, Rio Piedras.
GRADUATE AND UNDERGRADUATE STUDENTS
Graduate
2012 Javier Sánchez-Cáceres, MS-Candidate, commitee member, Universidad de Costa Rica,
San José. Expected Graduation May 2014.
181
Undergraduates
2012 Tyler Nelson. Utah State University, REU.
2012 Kristina Krome, Williams College, REU.
2011 Ashley Simone Curry, California State Polytechnic University, REU.
2009 Tanner J. Williamson, University of Vermont, REU.
1999 Alfredo Tirado, University of Puerto Rico.
1999 Ernesto J. Ayala, University of Puerto Rico.
PROFESSIONAL SERVICES
Journal Manuscript Review
 Latin American Journal of Aquatic Research
 Acta Cientifica
Research Collaborations
 Rennata Manconi- Università degli Studi di Sassari · Dipartimento di Scienze della Naturae
del Territorio, Italy.
 Fernando Mantellato- Universidad de São Paulo, Brazil
 Yogani Govender- Conservation Trust of Puerto Rico
PROFESSIONAL ORGANIZATIONS
British ecological Society (BES)
Society of Integrative Comparative Biology (SICB)
Invertebrate Biology (IB)
The Crustacen Society (TCS)
North American Benthological Society (NABS)
Macroinvertebrados Latinos y Ecosistemas (Macrolatin@s)
PRESENTATIONS AND ABSTRACTS
Crowl, T.A., Pérez-Reyes, O., Covich, A.P. (2013). Understanding the complexity of physical
and human interactions on tropical island water and ecosystem sustainability. Association for
Tropical Biology and Conservation, Costa Rica
Pérez-Reyes, O., Crowl, T. and Covich, A. (2013) Trophic relationships in natural and urban
neo-tropical streams in Puerto Rico. North America Benthological Society
Pérez-Reyes, O., Crowl, T. and Covich, A. (2012) Experimental and observational data on
migration patterns, density and growth rates of Atya lanipes and Xiphocaris elongata in tropical
streams in the Luquillo mountains, Puerto Rico. Congreso de Macroinvertabrados Acuaticos,
Costa Rica
Pérez-Reyes, O., Crowl T.A. (2010) How are decapod populations influenced by urbanization?
North America Benthological Society
Pérez-Reyes, O., Crowl, T.A. (2010) Comparisons of the decapod communities structure in
urban and natural streams in Puerto Rico. Society of Integrative and Comparative Biology
182
Pérez-Reyes, O., Suárez, D., Rosa-Molinar, E. (2007) Neurosystematics of Atya and Anostraca.
Society of Integrative and Comparative Biology
Sánchez-Cáceres, J., Pérez-Reyes, O. (2007) Asiatic Freshwater Clam, Corbicula fluminea (O. F.
Müller, 1774): Density, Distribution, Predation, Fecundity and Growth Rate in Puerto Rico.
Society of Integrative and Comparative Biology
Hernández-García, P., Pérez-Reyes, O., Ramírez, A. (2007) Diversity and abundance of benthic
aquatic insects among rivers in Puerto Rico. Society of Integrative and Comparative Biology
Rivera Colom, Natalia M., Cuevas Padró, A., Ackerman , J. D., Pérez-Reyes, O. (2007) The
fragrance composition of a new Scaevola sp. record in Puerto Rico. Society of Integrative and
Comparative Biology
Ledesma-Fuste, R. J., Pérez-Reyes, O., Hernández-García, P., Thomas, R. (2007) Colonization
and stratification patterns among web-building spider species along the banks of several rivers in
Puerto Rico. Society of Integrative and Comparative Biology
Gomez-Carrasquillo, J. E., Pérez-Reyes, O., Hernandez-García, P., Thomas, R. (2007) General
diet of the exotic species Iguana iguana on North Puerto Rican mangrove. Society of Integrative
and Comparative Biology
Hernández-Pasos, J., Pérez-Reyes, O. (2007) Influences of environmental factors on egg sack
production: progeny, developmental time and sexual ratio of Black widows Latrodectus mactans
and L. geometricus in Puerto Rico. Society of Integrative and Comparative Biology
Pérez-Reyes, O., Hernández-García, P., Rosa-Molinar, E. (2006) The motor neurons innervating
the pereiopods of Atya lanipes and Atya scabra. Society of Integrative and Comparative Biology
Pérez-Reyes, O., Muñoz P. M., Rivera, N. Renher, S. (2002) Observations of sipunculid species
of Puerto Rico. British Ecological Society, United Kingdom
Pérez-Reyes, O., Tirado, A. (1999) Differences in eggs size and clutch size of the prawn Atya
lanipes. British Ecological Society, United Kingdom
Tirado, A., Pérez-Reyes, O. (1999) Biological and pathological aspects of parasitism in the
branchial chamber of Macrobrachium spp. by infestation with Probopyrus sp. British Ecological
Society, United Kingdom
Ayala, E.J., Pérez-Reyes, O. (1999) Density and sexual dimorphism in Poeciliids of Puerto Rico.
British Ecological Society, United Kingdom
Pérez-Reyes, O., Tirado, A. (1997) Environmental effects on the fecundity in three Atya species
(Decapoda: Atyidae) (Atya lanipes, Atya innocuous, and Atya scabra. British Ecological Society,
United Kingdom
Tirado, A., Pérez-Reyes, O. (1997) Interactions between the parasite Probopyrus oviformis with
its host Macrobrachium spp. (Decapoda: Palaemonidae). British Ecological Society, United
Kingdom
183
WORKSHOPS ATTENDED
 Ensemble Models: Extending Species Distribution Models to Forecast Environments.
Presenter: Thomas C. Edwards
 The Zais Model for Curriculum Design. Presenter: Gregory A. Cajete
 Designing Effective Educational Signage for Schoolyard Gardens and Habitats. Presenter:
Zackery Zdinak
 Elements of Effective Diverse Education: Getting the Numbers to Dance for American
Indian Students. Presenter: Jim Barta
 Great Tips for Teaching Kids Outside. Presenter: Miriam Grahm
 Exploration of Landforms through Text Features and Hands-on Experiences Presenters:
Amy Taylor and Marilyn Watland-Wright
 Making Science Real. Presenter: Dr. Carla Endres
MEDIA COVERAGE
2013
2008
2008
BBC- London. Shrimp Migration. In: Hurricanes (3D)
Nueva especie de camarón en río metropolitano. Masslive.com
Nuevo Camaron. Primera Hora. http://www.youtube.com/watch?v=6ihxWmoc4Gg
OUTREACH


How many animals are out there?. Bioblitz, University of Puerto Rico, Bayamón
Campus.
Schoolyard, Luq-LTER. Decapodos de Puerto Rico: Importancia y Distribución.
MAIN REFERENCES
Todd A. Crowl, Ph.D.
Utah State University, Logan, UT
Watershed Sciences Department and the Ecology Center
(435) 760-1335
e-mail: [email protected]
Alan P. Covich, Ph.D.
University of Georgia
Odum School of Ecology
(706) 542-6006
e-mail: [email protected]
Ariel E. Lugo, Ph.D
International Institute of Tropical Forestry
University of Puerto Rico
Botanical Garden
(787) 766-5335
e-mail: [email protected]
184
Tamara Heartsill-Scalley, Ph.D
International Institute of Tropical Forestry
University of Puerto Rico
Botanical Garden
(787) 766-5335
e-mail: [email protected]