J OURNAL OF C RUSTACEAN B IOLOGY, 34(2), 144-156, 2014
DIFFERENTIAL USE OF THALASSIA TESTUDINUM HABITATS BY SYMPATRIC
PENAEIDS IN A NURSERY GROUND OF THE SOUTHERN GULF OF MEXICO
Marco Antonio May-Kú 1,∗ , Maria M. Criales 2 ,
Jorge Luis Montero-Muñoz 1 , and Pedro-Luis Ardisson 1
1 Departamento
de Recursos del Mar, Cinvestav, 97310 Merida, Yucatan, Mexico
School of Marine and Atmospheric Science, University of Miami,
4600 Rickenbacker Causeway, Miami, FL 33149, USA
2 Rosenstiel
ABSTRACT
Density of Penaeidae was assessed in habitats of Thalassia testudinum with different relative location (inshore zone and coastal lagoon)
and sediment type (fine sand and coarse sand) during three weather seasons in the Yucatan peninsula, Mexico. A total of 26,847 penaeids
were collected on a fortnightly basis from June 2001 to May 2002. A differential habitat use was observed in juveniles of three species of
penaeids. Densities of Farfantepenaeus brasiliensis (mean size ± SD: 8.3 ± 3.8 mm CL, carapace length) and Farfantepenaeus notialis
(5.5 ± 2.2 mm CL) were highest in the coastal lagoon in T. testudinum on fine sand, while density of Metapenaeopsis goodei (6.7 ± 1.7 mm
CL) was also highest in T. testudinum on fine sand, but in the inshore zone. This spatial distribution pattern varied little during the three
sampling seasons. A unimodal temporal distribution pattern was observed for juveniles of each species of penaeid, the abundance peaks of
F. brasiliensis and M. goodei overlap in the nortes season, while the abundance peak of F. notialis was distinct, peaking in the rainy season.
In contrast to juveniles, epibenthic Farfantepenaeus spp. postlarvae (3.2 ± 0.5 mm CL) had a more uniform spatial distribution with a
bimodal temporal distribution pattern, a highest abundance peak in the late rainy-early nortes seasons and other minor in the dry season.
A redundancy analysis indicated that densities of penaeids were related primarily with water salinity, sediment grain size, and aboveground
biomass and structural complexity of T. testudinum, which are variables closely linked with the spatial arrangement of the habitats along
the inshore zone and coastal lagoon. The use of different T. testudinum habitats allows coexistence of sympatric penaeids in the nursery
ground with minimal inter-specific interactions.
K EY W ORDS: Gulf of Mexico, nursery grounds, Penaeidae, population density, Thalassia testudinum,
shellfish
DOI: 10.1163/1937240X-00002214
I NTRODUCTION
Nearshore ecosystems such as seagrass meadows, marshes,
and mangrove forests provide nursery habitats for several
marine species, including exploited fishes and invertebrates
(Beck et al., 2001). Among these, penaeid shrimp are one
of the most valuable fishery resources in tropical and subtropical regions (Gillett, 2008). The distribution and abundance of juvenile penaeids in estuaries and coastal lagoons
can be variable depending, among other factors, on environmental gradients, type of submerged aquatic vegetation,
distance from the mouth, and species interactions. For example, the abundance of Melicertus plebejus (Hess, 1865)
(in this article, the binomials we use for Penaeidae are according to Pérez Farfante and Kensley, 1997) within Zostera
capricorni Ascherson, 1876 meadows is mainly determined
by the location of the seagrass meadow with respect to the
site where larval shrimp enter the estuary (Bell et al., 1988).
Similarly, the distribution of juvenile Penaeus esculentus
Haswell, 1879 and Penaeus semisulcatus de Haan, 1844 (in
De Haan, 1833-1850) is influenced by the relative location
of seagrass type and morphometric characteristics of seagrass (Loneragan et al., 1994, 1998; Haywood et al., 1995;
∗ Corresponding
Kenyon et al., 1997). For Farfantepenaeus aztecus (Ives,
1981), Farfantepenaeus brasiliensis (Latreille, 1817), Farfantepenaeus duorarum (Burkenroad, 1939) and Farfantepenaeus notialis (Pérez Farfante, 1967) the seagrass type,
seagrass biomass and the distance from the mouth were important factors determining their spatial distribution along
the estuarine habitat (Pérez-Castañeda and Defeo, 2004).
There are three shrimp-fishing areas in the Mexican portion of the Gulf of Mexico, with different target species and
production levels (SAGARPA, 2012). In the shrimp-fishing
area of Contoy, in the northeastern Yucatan peninsula, the
catch consists mainly of F. brasiliensis and Sicyonia brevirostris Stimpson, 1871 (cf., Porrás-Ruíz et al., 1998). Historically, this area ranks third in shrimp production, with 200 to
500 t per year, which accounts for 5 to 10% of the total production of the Gulf of Mexico (Mexico) (SAGARPA, 2012).
The turtlegrass Thalassia testudinum Banks et Soland. ex
K. D. Koenig is the dominant species of seagrass in this area,
forming extensive meadows in the inshore sublittoral zone,
coastal lagoons, estuaries, and coral reef lagoons (Short et
al., 2007). Densities of juvenile penaeids are higher in T.
testudinum compared to other available habitats (Sánchez,
author; e-mail: [email protected]
© The Crustacean Society, 2014. Published by Brill NV, Leiden
DOI:10.1163/1937240X-00002214
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MAY-KÚ ET AL.: THALASSIA AS A NURSERY FOR PENAEIDS
1997; Arrivillaga and Baltz, 1999; Sheridan and Minello,
2003), indicating their importance as nursery habitat.
Thalassia testudinum can have considerable intraspecific
morphological variation mainly as response to environmental variability (van Tussenbroek, 1995; Hackney and Durako,
2004; May-Kú et al., 2010); however, there is little knowledge about the influence of intra-habitat variability of this
species of seagrass on the distribution and abundance of
sympatric species of penaeids. In addition, the rapidly developing touristic in this region has negatively impacted the
ecological attributes of T. testudinum, e.g., decline in shoot
density and leaf growth (Herrera-Silveira et al., 2010), which
may affect their function as nursery habitat and consequently
the natural productivity of penaeids. Identify factors that create site-specific variations in nursery value can help the identification and conservation of seagrass nurseries (Beck et al.,
2001).
Differences in water quality, sediment type, and structural
characteristics of T. testudinum located in the inshore sublittoral zone and Yalahau Lagoon (Tran et al., 2002; May-Kú
et al., 2010), may help explain preliminary observations of
differential habitat utilization between these areas by several
species of penaeid shrimp (May-Kú and Ardisson, 2012).
The objective of this study was to assess the influence of
intra-habitat variability of T. testudinum on the spatial and
temporal distribution of sympatric penaeids.
M ATERIALS AND M ETHODS
Study Area
The northeastern Yucatan peninsula is a transitional area between the Gulf
of Mexico and the Caribbean Sea. It is a “karst” region characterized by
sinkholes, underground streams, and a lack of surface watercourses that
cause the absence of estuaries. The Yalahau Lagoon (21°26 -21°36 N,
87°06 -87°24 W) in the State of Quintana Roo, Mexico, has an area of
275 km2 and a water depth ranging from 0.3 to 4 m (Fig. 1). The Yalahau
Lagoon and its adjacent inshore sublittoral zone (<2 km from the shoreline;
<2 m depth) are dominated by monospecific T. testudinum meadows. In
the inshore zone, T. testudinum have lower biomass and shoot density,
along with longer and wider leaves than in Yalahau Lagoon (May-Kú et
al., 2010). In the inshore zone, the salinity (approx. 35) is relatively stable
year-round while in the Yalahau Lagoon the salinity has temporal and
spatial fluctuations. The northern part of the Lagoon has a trend toward
hypersalinity (approx. 40) because of the limited current circulation, which
results in a high residence time of water, while the southern part has a
slightly lower salinity (ranging between 25 and 30) due to the presence
of freshwater springs and surface runoff (Tran et al., 2002). Near the inlet
and in the southern part of the Lagoon, sand constitutes above 80% of
the sediment while the northern part of the Lagoon is dominated by finer
sediments nearly half of which consist of silt/clay (Tran et al., 2002).
Sampling Design
Eight T. testudinum sites were selected in the inshore zone and Yalahau
Lagoon and located in shallow waters (mean depth = 0.8 m; minimum =
0.25 m; maximum = 1.8 m), where no stratification of the water column
occurs (Tran et al., 2002). Sampling sites were grouped into four habitat
types according to their relative location and sediment type as: inshore T.
testudinum on fine sand (Ifine, T1-T2), inshore T. testudinum on coarse
sand (Icoarse, T3-T4), lagoon T. testudinum on fine sand (Lfine, T5-T6)
and lagoon T. testudinum on coarse sand (Lcoarse, T7-T8) (Fig. 1).
Fig. 1. Location of the sampling sites (") in the inshore zone and Yalahau Lagoon, Yucatan peninsula (YP), Mexico. Four habitat types were selected:
inshore Thalassia testudinum on fine sand (Ifine); inshore T. testudinum on coarse sand (Icoarse); lagoon T. testudinum on fine sand (Lfine) and lagoon T.
testudinum on coarse sand (Lcoarse).
146
JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 34, NO. 2, 2014
Penaeids were collected at night on a fortnightly basis around the full
and new moons from June 2001 to May 2002. This period includes the
three main weather seasons of the region: rainy (June-October), cold fronts
or ‘nortes’ (November-February) and dry (March-May). Two trawls per
sampling site were carried out with a Renfro beam trawl (1.6 × 0.5 m
mouth, 1.5 m total length, and 1.0 mm mesh size), covering a sampling area
of 50 m2 per trawl tow. For penaeids, the catch efficiency of the Renfro
beam trawl has been estimated at 15% in T. testudinum meadows (Gracia
et al., 1994). Although catch efficiency of this gear is low, is easy to use,
produces clean samples, allows for a large sampling area and is a relatively
non-destructive method of the benthic habitat (Rozas and Minello, 1997).
In October 2001 and January 2002 sampling was monthly and in August
2001 no sampling was carried out.
The penaeids were sorted from the seagrasses, preserved in 10%
formalin and identified to species (Pérez Farfante, 1971a, b; May-Kú et al.,
2006). The carapace length (CL, distance from postorbital margin to middorsal posterior margin of the carapace) was measured for each individual.
Epibenthic postlarvae (CL < 4 mm) of the genus Farfantepenaeus were
not possible to identify to species because of the lack of specific diagnostic
characteristics at these sizes (May-Kú et al., 2006).
Water salinity, water temperature, and dissolved oxygen were recorded
fortnightly in the middle of the water column using a YSI model 85-25
FT at each sampling site. For each T. testudinum site we estimated the
aboveground biomass, shoot density and leaf morphology (for a detailed
procedure see: May-Kú et al., 2010) and used this data to calculate an index
(modified from Tolan et al., 1997) that defines a multiplicative total value
of the aboveground structural complexity as:
Structural complexity index = (Sd × Ls × La )/100,
where Sd = shoot density (shoots m−2 ), Ls = number of leaves per
shoot (3, according to Herrera-Silveira et al., 2010) and La = leaf area
(leaf length × leaf width, cm−2 ). Sediment samples were analyzed using
standard Ro-tap procedures (Ingram, 1971) with the following mesh sizes:
−1.25, 0, 1, 2, 3, 4, and 5 phi ( = − log2 d, where d is sediment grain
diameter in mm). The mean grain size was calculated by the graphical
method (Folk and Ward, 1957) and classified according to the UddenWentworth scale (Udden, 1914; Wentworth, 1922).
Statistical Analyses
To test for differences in environmental variables among the four habitats
for T. testudinum, we performed for each season a two-way ANOVA
(F ) with location (inshore zone and coastal lagoon), sediment type (fine
sand and coarse sand) and location × sediment type interaction as
sources of variation. When significant differences were detected, multiple
comparisons were performed using the Bonferroni test (P < 0.05). To meet
ANOVA assumptions of normality and homoscedasticity, environmental
variables were log-transformed. To test for differences in density of
penaeids among the four habitats for T. testudinum, we performed for
each species a Generalized Linear Model (GLM) to conduct an analysis
of deviance (ANODEV) using Poisson distribution and a log-link function,
in the statistical package R version 1.9.0 (Zuur et al., 2009). Sources of
variation were: location (inshore zone and coastal lagoon), sediment type
(fine sand and coarse sand), season (rainy, nortes, dry), location × sediment
type, and location × season. The analyses performed in this way have
the minimum amount of replication needed to avoid pseudoreplication
(Hurlbert, 1984). Metapenaeopsis smithi (Schmitt, 1924) and Rimapenaeus
constrictus (Stimpson, 1871) were excluded from statistical analysis owing
to their low relative abundance (<0.1%).
Multivariate ordination methods (Ter Braak and Šmilauer, 2002) were
performed to assess the influence of intra-habitat variability of T. testudinum
on the distribution of penaeids. Detrended correspondence analysis (DCA)
was used to detect the environmental gradient length. Redundancy analysis
(RDA) was applied after DCA since the length of environmental ordination
axes was <2.0 SD, indicating that the dataset had short gradients and that
the linear model was appropriate. Shoot density was excluded a priori from
RDA because was highly correlated with structural complexity index. After
a preliminary RDA, only those explanatory variable combinations with
variance inflation factors < 10 (water salinity, sediment grain size, aboveground biomass and structural complexity) were included in the final RDA
to reduce multicollinearity (ter Braak and Šmilauer, 2002). Analyses were
performed for each season using transformed
data of explanatory variables
√
(log x + 1) and densities of penaeids ( x + 0.375) registered at each T.
testudinum site. The scaling option for RDA was based on inter-species
correlations and the species data were standardized by error variance (Lepš
and Šmilauer, 2003). The automatic forward selection procedure was used
to determine the importance of each explanatory variable in the RDA model
in accordance with the Monte Carlo permutation test with 999 permutations.
R ESULTS
Environmental Variation
For sediment grain size, significant effects of the sediment
type were detected in the two-way ANOVAs for each season
(rainy: F1,32 = 70.32, P < 0.0001; nortes: F1,32 = 90.19,
P < 0.0001; dry: F1,24 = 109.33, P < 0.0001), confirming
that mean grain size was higher in Ifine and Lfine habitats
(>1.5 ø; i.e., fine to very fine sand) than in Icoarse and
Lcoarse habitats (<1.5 ø; i.e., coarse to very coarse sand)
during the three seasons (post hoc Bonferroni test, P <
0.05; Table 1). Water salinity was lower and more stable
in the inshore zone (mean ± SE = 35.8 ± 0.2; range =
28.3-38.2; coefficient of variation (CV) = 4.7%) than in the
coastal lagoon (38.5 ± 0.4; 29.2-46.2; 10.5%, respectively).
Significant effects of the location were detected for water
salinity in the two-way ANOVAs for each season (rainy:
F1,56 = 279.66, P < 0.0001; nortes: F1,64 = 4.41, P =
0.039; dry: F1,48 = 3.14, P = 0.083), indicating that during
the three seasons mean water salinity was higher in the
coastal lagoon than in the inshore zone (post hoc Bonferroni
test, P < 0.05). Significant interactions between location
and sediment type were detected by two-way ANOVA
during the rainy (F1,56 = 6.71, P = 0.0124) and nortes
seasons (F1,64 = 12.88, P = 0.0007), with the highest mean
water salinity at Lfine habitat during both seasons (post hoc
Bonferroni test, P < 0.05; Table 2). For water temperature,
the two-way ANOVAs only detected significant differences
between sediment types during the rainy season (F1,56 =
5.6, P = 0.022). However, mean water temperatures tended
to increase during the rainy season and decrease during the
nortes season, and generally water temperature was similar
for all habitats within each of the three seasons (Table 1).
For dissolved oxygen, significant effects of the location were
detected in the two-way ANOVAs for each season (rainy:
F1,56 = 21.03, P < 0.0001; nortes: F1,64 = 16.58,
P = 0.0001; dry: F1,48 = 6.93, P = 0.011), indicating
that during the three seasons mean dissolved oxygen was
higher in the inshore zone than in the coastal lagoon (post
hoc Bonferroni test, P < 0.05). Two-way ANOVAs did not
find any significant differences in mean dissolved oxygen in
the interaction of location × sediment type for each season
(rainy: F1,56 = 0.83, P = 0.366; nortes: F1,64 = 0.87,
P = 0.354; dry: F1,48 = 0.4, P = 0.531), indicating that
within each of the three seasons, mean dissolved oxygen no
varied among the four habitat types.
For above-ground biomass of T. testudinum, significant interactions between location and sediment type were detected
by two-way ANOVAs for each season (rainy: F1,64 = 16.11,
P = 0.0002; nortes: F1,64 = 4.67, P = 0.035; dry:
F1,48 = 4.61, P = 0.037), with the highest mean aboveground biomass at Ifine habitat during the three seasons
(post hoc Bonferroni test, P < 0.05; Table 1). For shoot
density of T. testudinum, the two-way ANOVAs detected
significant differences between locations during the rainy
(F1,64 = 10.31, P = 0.002) and nortes seasons (F1,64 = 9.8,
147
MAY-KÚ ET AL.: THALASSIA AS A NURSERY FOR PENAEIDS
Table 1. Mean ± SE for environmental variables in four habitats of Thalassia testudinum with different relative location and sediment type during three
weather seasons. For abbreviations of habitat type see Fig. 1.
Variable
Inshore zone
Ifine
Rainy
Sediment grain size ()
Water
Salinity
Temperature (°C)
Dissolved oxygen (mg l−1 )
Thalassia testudinum
Aboveground biomass (g dry w m−2 )
Shoot density (shoots m−2 )
Structural complexity index
Nortes
Sediment grain size ()
Water
Salinity
Temperature (°C)
Dissolved oxygen (mg l−1 )
Thalassia testudinum
Aboveground biomass (g dry w m−2 )
Shoot density (shoots m−2 )
Structural complexity index
Dry
Sediment grain size ()
Water
Salinity
Temperature (°C)
Dissolved oxygen (mg l−1 )
Thalassia testudinum
Aboveground biomass (g dry w m−2 )
Shoot density (shoots m−2 )
Structural complexity index
Coastal lagoon
Icoarse
Lfine
Lcoarse
2.7 ± 0.2
0.9 ± 0.2
1.9 ± 0.2
0.8 ± 0.1
37.2 ± 0.2
29.8 ± 0.3
5.0 ± 0.5
36.4 ± 0.3
29.5 ± 0.2
4.2 ± 0.5
43.8 ± 0.5
29.8 ± 0.2
3.0 ± 0.3
41.1 ± 0.4
28.8 ± 0.3
2.0 ± 0.3
930 ± 183
848 ± 87
826 ± 61
436 ± 24
549 ± 37
368 ± 47
526 ± 64
1017 ± 122
437 ± 81
1016 ± 74
903 ± 70
552 ± 37
2.4 ± 0.1
0.5 ± 0.2
1.9 ± 0.2
0.7 ± 0.1
35.3 ± 0.2
25.5 ± 0.4
6.7 ± 0.3
33.9 ± 0.5
25.5 ± 0.4
6.9 ± 0.3
37.8 ± 0.5
25.4 ± 0.3
5.7 ± 0.2
33.7 ± 0.6
25.1 ± 0.3
5.6 ± 0.3
1138 ± 232
688 ± 52
569 ± 51
396 ± 56
601 ± 75
404 ± 59
568 ± 59
915 ± 100
450 ± 79
530 ± 40
794 ± 52
394 ± 30
2.7 ± 0.2
0.3 ± 0.1
2.0 ± 0.3
0.7 ± 0.1
36.6 ± 0.3
28.2 ± 0.3
4.7 ± 0.5
35.8 ± 0.5
27.7 ± 0.3
4.2 ± 0.3
38.5 ± 0.7
27.9 ± 0.4
3.6 ± 0.3
36.8 ± 1.1
27.2 ± 0.4
3.1 ± 0.5
1203 ± 262
883 ± 142
797 ± 66
471 ± 42
1080 ± 103
682 ± 61
613 ± 48
1066 ± 93
543 ± 59
651 ± 55
867 ± 62
465 ± 40
P = 0.002); between sediment types during the rainy season
(F1,64 = 4.31, P = 0.042) and for the interaction of location × sediment type during the dry season (F1,48 = 5.19,
P = 0.027). In general, the mean shoot density was greater
in the coastal lagoon, with the highest mean value during
the dry season in the Lfine habitat (post hoc Bonferroni
test, P < 0.05; Table 1). For the structural complexity index of T. testudinum, the two-way ANOVAs detected sig-
nificant differences between locations during the dry season
(F1,48 = 18.21, P = 0.0001) and between sediment types
and in the interaction of location × sediment type during
the rainy season (F1,64 = 4.23, P = 0.044; F1,64 = 33.52,
P < 0.0001; respectively). In general, the mean structural
complexity was greater in the inshore zone at Lfine habitat,
with the maximum value during the rainy season (post hoc
Bonferroni test, P < 0.05; Table 1).
Table 2. Species of penaeid shrimps ranked by numerical abundance in 336 trawl tows performed at the inshore zone and Yalahau Lagoon, from June 2001
to May 2002. a Only the 20,704 shrimps identified to species category were considered.
Species
Farfantepenaeus brasiliensis
Farfantepenaeus notialis
Metapenaeopsis goodei
Metapenaeopsis smithi
Rimapenaeus constrictus
Epibenthic Farfantepenaeus spp. postlarvae
Total
Carapace length (mm)
(mean ± SD (min-max))
8.3 ± 3.8 (4-32.5)
5.5 ± 2.2 (4-16)
6.7 ± 1.7 (3-10.1)
6.1 ± 1.4 (4.1-9)
5.7 ± 1.7 (3.6-8)
3.2 ± 0.5 (1.6-3.9)
Abundance
Frequency of
ocurrence
Total
Relative (%)a
No.
Relative (%)
19,201
1108
367
15
13
6143
26,847
92.7
5.4
1.8
0.07
0.06
325
136
60
9
7
169
96.7
40.5
17.9
2.7
2.1
48.8
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JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 34, NO. 2, 2014
Penaeids
During the study period, 336 trawl tows were completed and
26,847 penaeids belonging to three genera and five species
were collected. The commercial shrimp F. brasiliensis was
the most abundant and frequently caught species, and
small non-commercial shrimp such as M. goodei and R.
constrictus were less common (Table 2).
There was considerable variation in shrimp densities between locations, sediment types and seasons (Table 3).
About 63% and 37% of juvenile F. brasiliensis were caught
in the coastal lagoon and the inshore zone, respectively.
The ANODEV detected significant differences between locations, sediment types and in the interaction of location ×
sediment type (Table 3), with the highest mean densities
occurring in the coastal lagoon (Fig. 2A) and on fine sediments (Fig. 3A). F. brasiliensis occurred year-round, with
the largest peaks in November and December (nortes season)
(Fig. 4A). The ANODEV detected significant differences in
the mean density among seasons and in the interaction of location × season (Table 3), indicating that mean density of
F. brasiliensis during the nortes season was higher than in
the other seasons, with the highest mean density occurring
during this season at Lfine habitat (Fig. 5A).
About 80% and 20% of juvenile F. notialis were caught
in the coastal lagoon and the inshore zone, respectively.
The ANODEV detected significant differences between
locations and sediment types (Table 3), with the highest
mean densities occurring in the coastal lagoon (Fig. 2B) on
fine sediments (Fig. 3B). F. notialis occurred year-round,
with the largest peak in September (rainy season) (Fig. 4B).
The ANODEV detected significant differences in the mean
density among seasons, indicating that mean density of F.
brasiliensis during the rainy season was higher than in the
other seasons. During the three seasons, the mean densities
of F. notialis were usually high at Lfine habitat (Fig. 5B),
but the interaction of location × season was not significant
(Table 3).
About 95% and 5% of juvenile M. goodei were caught
in the inshore zone and the coastal lagoon, respectively.
The ANODEV detected significant differences between locations and sediment types (Table 3), with the highest mean
densities in the inshore zone (Fig. 2C) on fine sediments
(Fig. 3C). Major peaks of M. goodei occurred from November to January (nortes season) and were practically absent
from June to September (Fig. 4C). The ANODEV detected
significant differences in the mean density among seasons,
indicating that mean density of M. goodei during the nortes
season was higher than in the other seasons. During the three
seasons, the mean densities of M. goodei were high at Ifine
(Fig. 5C), but the interaction of location × season was not
significant (Table 3).
Table 3. Summary of analysis of deviance (ANODEV) to evaluate differences in density of species of penaeid shrimps among habitats of T. testudinum with
different location and sediment type. ANODEV was performed using Generalized Linear Model, Poisson distribution and a log-link function. ∗ Significant
probability.
Species
Source of variation
df
Residual deviance
Pr > χ 2
Null
A: Location
B: Sediment type
C: Season
A×B
A×C
NA
1
1
2
1
2
641.96
616.03
585.05
459.15
418.45
355.28
NA
0.000∗
0.000∗
0.000∗
0.000∗
0.000∗
Null
A: Location
B: Sediment type
C: Season
A×B
A×C
NA
1
1
2
1
2
74.31
67.45
66.21
63.92
63.86
63.57
NA
0.000∗
0.069∗
0.046∗
0.701
0.678
Null
A: Location
B: Sediment type
C: Season
A×B
A×C
NA
1
1
2
1
2
32.11
24.81
18.69
12.72
12.70
12.67
NA
0.000∗
0.000∗
0.000∗
0.510
0.894
Null
A: Location
B: Sediment type
C: Season
A×B
A×C
NA
1
1
2
1
2
406.69
406.44
401.44
373.16
369.51
340.39
NA
0.711
0.103
0.001∗
0.164
0.000∗
Farfantepenaeus brasiliensis
% Total deviance explained
44.66
Farfantepenaeus notialis
14.44
Metapenaeopsis goodei
60.55
Epibenthic Farfantepenaeus spp. postlarvae
16.30
MAY-KÚ ET AL.: THALASSIA AS A NURSERY FOR PENAEIDS
149
Fig. 2. Mean density (±SE) of juvenile shrimp in habitats of Thalassia testudinum with different relative location. The P -values are derived from quasiPoisson GLM analyses. A, Farfantepenaeus brasiliensis; B, Farfantepenaeus notialis; C, Metapenaeopsis goodie; D, benthic postlarvae of Farfantepenaeus
spp.
The percentage of epibenthic Farfantepenaeus spp. postlarvae caught at the inshore zone (52%) was similar to that of
the coastal lagoon (48%). The ANODEV did not detect any
significant differences in mean density between locations
(Fig. 2D), sediment types (Fig. 3D) and in the interaction
of location × sediment type (Table 3). Epibenthic Farfan-
Fig. 3. Mean density (±SE) of juvenile shrimp in habitats of Thalassia testudinum with different sediment type. The P -values are derived from quasiPoisson GLM analyses. A, Farfantepenaeus brasiliensis; B, Farfantepenaeus notialis; C, Metapenaeopsis goodie; D, benthic postlarvae of Farfantepenaeus
spp.
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Fig. 4. Mean fortnightly density (±SE) of juvenile shrimp. A, Farfantepenaeus brasiliensis; B, Farfantepenaeus notialis; C, Metapenaeopsis goodei; D,
benthic postlarvae of Farfantepenaeus spp. 0, no shrimp caught; ns: no sampling.
tepenaeus spp. postlarvae occurred year-round with a major
peak from September to November (late rainy-early nortes
seasons) and a minor peak in March (dry season) (Fig. 4D).
The ANODEV detected significant differences in the mean
density among seasons and in the interaction of location ×
season (Table 3). The highest mean density of Epibenthic
Farfantepenaeus spp. postlarvae occurred during the rainy
season at Icoarse habitat, but high densities also occurred
during the rainy season at Ifine and Lfine habitats, and during the nortes and dry seasons at Lfine and Ifine habitats,
respectively (Fig. 5D).
Relationships Between Species of Penaeids and
Explanatory Variables
During the rainy season, the RDA indicated that the first
and second canonical axes explained 50.5% and 36.9%,
respectively, of the variability of the density of the species
explained by the environmental variables considered in the
analysis; during the nortes season, 80.2% and 19.6%, and
during the dry season 65.5% and 33.5% (Table 4). During
the rainy season (Fig. 6A), the most important variables in
axis 1 were aboveground biomass (r = 0.79) and structural
complexity (r = 0.52). Density of M. goodei increased
MAY-KÚ ET AL.: THALASSIA AS A NURSERY FOR PENAEIDS
151
Fig. 5. Mean density (±SE) of juvenile shrimp in four habitat types with Thalassia testudinum during three seasons. 0, no shrimp caught. For abbreviation
of habitat type see Fig. 1. A, Farfantepenaeus brasiliensis; B, Farfantepenaeus notialis; C, Metapenaeopsis goodie; D, benthic postlarvae of Farfantepenaeus
spp.
along increasing gradients of aboveground biomass and
structural complexity and was primarily associated with the
sampling site T2 (inshore zone). The second ordination axis
was more correlated with water salinity (r = 0.72) and
sediment grain size (r = −0.54). Densities of F. brasiliensis,
F. notialis, and epibenthic postlarvae of Farfantepenaeus
spp. tended to decrease at higher water salinities (because
their arrows point in opposite directions) and increase with
the increased of grain sizes (fine sand) and were primarily
associated with the sampling sites T1 and T3 (inshore zone)
and T4 and T5 (coastal lagoon). During the nortes season
(Fig. 6B), the most important variables in axis 1 were
structural complexity (r = 0.73) and aboveground biomass
(r = 0.47). Density of M. goodei increased along increasing
gradients of aboveground biomass and structural complexity
and was primarily associated with the sampling sites T1 and
T2 (inshore zone). The second ordination axis was more
correlated with water salinity (r = 0.72) and sediment grain
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JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 34, NO. 2, 2014
Table 4. Summary of the redundancy analysis (RDA) between explanatory variables (salinity, sediment grain size, above-ground biomass and structural
complexity index) and density of juvenile Farfantepenaeus brasiliensis, F. notialis, Metapenaeopsis goodei and epibenthic Farfantepenaeus spp. postlarvae,
in Thalassia testudinum sites.
Rainy
Eigenvalues
Species-environment correlation
Cumulative percentage variance
Species data
Species-environment relation
Sum of all canonical eigenvalues
Nortes
Dry
Axis 1
Axis 2
Axis 1
Axis 2
Axis 1
Axis 2
0.358
0.822
0.261
0.976
0.639
0.934
0.156
0.826
0.614
0.987
0.314
0.987
35.8
50.5
61.9
87.4
0.708
size (r = 0.64). Densities of F. brasiliensis, F. notialis
and epibenthic postlarvae of Farfantepenaeus spp. tended
to increase along increasing gradients of water salinity and
grain size (i.e., fine sand) and were primarily associated
with the sampling sites T5 and T6 (coastal lagoon). During
the dry season (Fig. 6C), the most important variable in
axis 1 was sediment grain size (r = 0.59). Densities of
63.9
80.2
79.5
99.8
0.796
61.4
65.5
92.9
99.0
0.938
F. brasiliensis and epibenthic postlarvae of Farfantepenaeus
spp. increased along increasing gradients of grain size (i.e.,
fine sand) and were primarily associated with the sampling
site T1 (inshore zone). The second ordination axis was
more correlated with aboveground biomass (r = 0.87)
and structural complexity (r = 0.54). Density of M.
goodei tended to increase along increasing gradients of
Fig. 6. Redundancy analysis ordination triplot for each sampling season (A, rainy; B, nortes; C, dry) showing sampling sites of Thalassia testudinum
("), species vectors (dashed arrows: Fb, Farfantepenaeus brasiliensis; Fn, F. notialis; Mg, Metapenaeopsis goodei; PLs, epibenthic Farfantepenaeus spp.
postlarvae) and explanatory variable vectors (solid arrows: salinity; phi, sediment grain size; biomass, aboveground biomass; complex, structural complexity
index). A positive correlation is expressed by relatively long vectors roughly pointing into the same direction, whereas a negative correlation is indicated
by arrows pointing into opposite directions. Perpendicular arrows indicate that there is no correlation. Angles between species vectors represent correlation
between the species.
MAY-KÚ ET AL.: THALASSIA AS A NURSERY FOR PENAEIDS
aboveground biomass and structural complexity and was
primarily associated with the sampling site T2 (inshore
zone).
D ISCUSSION
We found that in habitats with T. testudinum from the
northeastern Yucatan peninsula, about 93% of the total
shrimp caught were F. brasiliensis. This percentage is
higher than that reported in other nursery grounds across its
geographic distribution range, for example, near the studied
area, at Río Lagartos, F. brasiliensis represents about 80%
(May-Kú and Ordóñez-López, 2006), while in the other
region of the Yucatan peninsula, at Celestun, represents
25% (Pérez-Castañeda and Defeo, 2001). In Biscayne Bay,
Florida, F. brasiliensis represents about 13 to 25% (Saloman
et al., 1968; Criales et al., 2000). In Laguna Joyuda, Puerto
Rico, this species represents only 7% (Stoner, 1988) and
on the Atlantic coast of Brazil it accounts for about 45
to 60% (Costa et al., 2008; Luchmann et al., 2008). The
absence of estuarine ecosystems in the northeastern Yucatan
may be favorable to F. brasiliensis because laboratory
experiments and field studies have observed that this species
is less resistant to low salinity waters than other species
of penaeids and grows better at high salinities (Criales
and Chung, 1979; Brito et al., 2000; Pérez-Castañeda and
Defeo, 2001, 2005), which may explain their absence in
estuaries, such as Terminos Lagoon, in the Gulf of Mexico
(Gracia and Soto, 1990), and the Indaiá Estuary, in the
Atlantic coast of Brazil (Costa et al., 2008). The numerical
dominance of F. brasiliensis in the northeastern Yucatan also
agrees with their spawning and fishing areas in the western
Caribbean Sea (Mexico) (Porrás-Ruíz et al., 1998; SandovalQuintero and Gracia, 2002), highlighting the importance of
T. testudinum habitats as nursery ground for this valuable
species of the Contoy shrimp-fishery.
To our knowledge, there is no comparative information
concerning the population density of F. brasiliensis in T.
testudinum habitats with different spatial arrangement. Mean
densities of F. brasiliensis in the inshore zone (0.85 ind
m−2 ) and Yalahau Lagoon (1.44 ind m−2 ) are about 3- to 4fold higher than the reported for this species in Celestún in
the seagrass Halodule beaudettei (den Hartog) den Hartog,
1964, formerly known as H. wrightii (Pérez-Castañeda and
Defeo, 2001) and in Río Lagartos in a mixed seagrass
(T. testudinum, H. beaudettei) and macroalgae [Laurencia
poiteaui (J. V. Lamouroux) M. A. Howe] habitat (MayKú and Ordóñez-López, 2006). In unvegetated habitats
the densities of F. brasiliensis are 8- to 36-fold lower
(Lüchmann et al., 2008; May-Kú and Ardisson, 2012) than
that reported in the present study, indicating the importance
of vegetated habitats for this species. By comparing our
results of F. brasiliensis densities with other species of
penaeids that inhabit in T. testudinum meadows, we observed
that these are almost similar to that reported for F. aztecus
(mean: 1.1 ind m−2 ) and F. duorarum (mean: 1.7 ind m−2 ) in
Lower Laguna Madre, Texas (Sheridan and Minello, 2003),
although in that study was used a drop trap, a sampling
gear that had a higher catch efficiency than the Renfro beam
trawl (Rozas and Minello, 1997). On the Atlantic coast of
Guatemala, Arrivillaga and Baltz (1999) also using a drop
153
trap reported a mean density for F. notialis of 0.33 ind
m−2 , lower to the observed for F. brasiliensis in the present
study. In contrast, our densities of F. brasiliensis are low
compared to those for F. duorarum in Terminos Lagoon,
Mexico, where Gracia et al. (1994) and Sánchez (1997)
using a Renfro beam trawl, reported mean densities of 9.9
and 49.7 ind m−2 , respectively. Besides the sampling gear
and their catch efficiency, other factors such as lunar cycle,
seasonal and inter annual variations in abundance could have
contributed to the differences in reported shrimp densities
between our study and others (Stoner, 1991; Vance et al.,
1996).
The three penaeids collected in the present study, F.
brasiliensis, F. notialis, and M. goodei had higher densities in T. testudinum on sand fine than in T. testudinum on
coarse sand, but F. brasiliensis and F. notialis had greater
densities within the Yalahau Lagoon, while M. goodei had
greater density in the inshore zone. Interspecies biotic interactions such as interference competition e.g., aggression,
often play an important role in determining coexistence between sympatric shrimp, allowing the efficient utilization of
common resources such as space and food (Thorp, 1976).
Differences in feeding habits between species as well as differential predation pressure between habitats may also result in habitat segregation (Minello and Zimmerman, 1985,
1991; McTigue and Zimmerman, 1998). In the present study,
shrimp densities were related primarily with water salinity,
sediment grain size, and biomass and complexity of T. testudinum, which are biotic and abiotic factors closely linked
with the spatial arrangement of the habitats along the inshore
zone and Yalahau Lagoon (Tran et al., 2002; May-Kú et al.,
2010).
In the field, positive, negative, and no relationships have
been observed between density of penaeids and salinity
(Howe et al., 1999; Howe and Wallace, 2000; Rozas and
Zimmerman, 2000; May-Kú and Ordóñez-López, 2006),
probably because of inter-specific differences in osmoregulatory ability to cope with changes in salinity (Dall, 1981;
Brito et al., 2000). Salinity is not the only factor that determines the distribution and abundance of juvenile shrimp.
Fine sediments are typically found in seagrass meadows because the canopy structure reduces hydrodynamic motion
and increases sedimentation (Hemminga and Duarte, 2000).
We observed that about 65% of shrimp were collected in T.
testudinum growing on fine sand. Juvenile shrimp might prefer fine sediments because it provide suitable habitat for burrowing, which help them avoid predators (Dall et al., 1990).
Also, fine sediments generally harbor higher abundance of
benthic organisms than the coarser sediments, which are potential food for shrimp (Pech et al., 2007).
The relative location of seagrass meadows and their
structural characteristics could contribute to the differences
in spatial distribution and abundance of juveniles (Bell et
al., 1986; Loneragan et al., 1994, 1998; Kenyon et al.,
1997), although the relative importance of each of these
factors it can be difficult to determine because both are often
interrelated, e.g., the intra-specific morphological variation
of seagrass may be linked to exposure gradients according
their relative location (Schanz and Asmus, 2003; May-Kú
et al., 2010). Therefore, our results about the consistent
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JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 34, NO. 2, 2014
positive relationships between density of M. goodei and
high biomass and complexity of T. testudinum from the
inshore zone, can be also explained by the increase in
physical structure that improve protection against predators
reducing mortality in these small penaeids (see review by
Heck and Orth, 2006). In addition, for M. goodei the salinity
probably influence their distribution because in contrast to
F. brasiliensis and F. notialis their juvenile stages do not
enter the coastal lagoon but remain in T. testudinum habitats
from the inshore zone. Most species of Metapenaeopsis
are more adapted to marine salinities and have a Type 3
life cycle according to the four types of life cycle for
penaeids described in Dall et al. (1990). During the juvenile
stage, species of Metapenaeopsis use the inshore zone with
relatively high salinity and seagrasses as nursery grounds,
similar to the observed in the present study.
In penaeids, the temporal partitioning among species is
an important mechanism to reduce potential interspecific
competition (Young and Carpenter, 1977; Lüchmann et al.,
2008). We observed that juveniles of F. brasiliensis and
F. notialis, both with highest abundances within Yalahau
Lagoon, occur all months of the year but at different times,
the former species had high abundances from November
to December (nortes season) and the second species in
September (rainy season). In Celestun, both species also
have temporal segregation in peak abundances of juveniles,
but F. brasiliensis peaked from September to October
(rainy season), whereas F. notialis peaked from February
to May (dry season) (Pérez-Castañeda and Defeo, 2001).
To the best of our knowledge, there is no information
about temporal distribution patterns of juvenile M. goodei
in nursery grounds. In the present study, the presence of
juveniles of M. goodei was episodic, with an abundance peak
from November to January and a tendency to disappear from
June to September. In Biscayne Bay, Florida, juveniles of
Metapenaeopsis spp. had almost the same temporal pattern
with the highest densities between December and February
and lowest between May and October (Criales et al., 2000).
In contrast in Puerto Rico Metapenaeopsis spp. juveniles
increase in number from July to October and decrease
from April to June (Bauer, 1985). Temporal differences
in distribution of juvenile stages have also been observed
in other penaeids, being mainly related to spawning stock
dynamics and hydrographic conditions taking place during
the advection of larvae and postlarvae towards the nursery
grounds (Crocos and van der Velde, 1995; Vance et al., 1996;
Criales et al., 2003).
In contrast to juveniles, epibenthic postlarvae of Farfantepenaeus spp. had a more uniform spatial distribution (regardless the location and sediment type of T. testudinum
habitats) and a bimodal temporal distribution pattern. The
settlement model proposed by Bell and Westoby (1986) suggests that larvae of decapods do not discriminate between
different seagrass types at the time of settlement, because
the refuge obtained in seagrass would be more advantageous
than further exposure to predation in the water column. Our
results about the temporal stability of aboveground biomass
of T. testudinum suggest that both the inshore zone and Yalahau Lagoon provide year-round suitable nursery grounds for
epibenthic postlarvae. This result agrees with Duarte et al.
(2006) who suggest that seagrasses in tropical regions provide a stable biomass and habitat for the associated fauna
throughout the year due to the small seasonal variations in
water temperature and light. In the other hand, near the study
area, at Contoy, Sandoval-Quintero and Gracia (2000) found
that ripe females of F. brasiliensis were present throughout
the whole year with a unimodal peak of abundance in March
and April, which mismatch with the minor abundance peak
of epibenthic postlarvae of Farfantepenaeus spp. in these
months. In addition, RDA results indicated that this life stage
was consistently associated with juveniles of F. brasiliensis.
However, the cause of the highest abundance peak of postlarvae of Farfantepenaeus spp. during the rainy and nortes seasons is unclear. Probably strong seasonal winds could favor
the advection of larvae and postlarvae towards the nursery
ground as observed in postlarvae of the pink shrimp, F. duorarum (Criales et al., 2006, 2010). A more complete understanding of the population dynamics of penaeids in the study
area could become apparent after complementary studies
that analyze the temporal variation in size distribution of
each species, which may indicate the presence of distinct
age groups in the population, mortality or migration (PérezCastañeda and Defeo, 2000; Baker and Minello, 2010).
ACKNOWLEDGEMENTS
Financial support was provided by a doctoral scholarship from CONACYT
(Mexico) to M. A. May-Kú. The authors are grateful to M. Ornelas-Roa,
from the Plankton Laboratory, Cinvestav, for her assistance in obtaining
morphometric shrimp data. We also thank two anonymous reviewers for
suggested improvements to the manuscript.
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ACCEPTED: 30 November 2013.
AVAILABLE ONLINE: 22 January 2014.