Marine Pollution Bulletin xxx (2013) xxx–xxx
Contents lists available at SciVerse ScienceDirect
Marine Pollution Bulletin
journal homepage: www.elsevier.com/locate/marpolbul
Watershed discharge patterns, secondary consumer abundances, and seagrass
habitat condition in Yap, Micronesia
Peter Houk a,b,⇑, Yimnang Golbuu c, Berna Gorong e, Thomas Gorong e, Christina Fillmed d
a
University of Guam Marine Laboratory, Mangilao, GU, United States
Pacific Marine Resources Institute, Saipan, MP, United States
c
Palau International Coral Reef Center, Koror, Palau
d
Yap Environmental Protection Agency, Colonia, Yap, Federated States of Micronesia
e
Kaday Community and Cultural Development Organization, Weloy, Yap, Federated States of Micronesia
b
a r t i c l e
Keywords:
Water quality
Watersheds
Seagrass
Nutrients
Sea cucumbers
Fisheries
i n f o
a b s t r a c t
Watershed discharge, water quality, and seagrass assemblages were examined along the western coast of
Yap Proper, Micronesia. Submarine groundwater discharge (SGD) during low tides associated with new
and full moons contributed disproportionally to freshwater delivery where compromised Thalassia habitats existed. Despite SGD influence, nutrient sampling indicated that one characteristic regime may be a
net import of new nitrogen and phosphorous (NO3 and PO4) from offshore to inshore waters, agreeing
with sparse watershed development. Biologically recycled nitrogen (NH4), however, was highest where
SGD contribution was largest. Time-and-tide-limited sampling likely precluded generalized relationships
between SGD and NH4 across the entire study area, however, spatial profiling of SGD during low-tide
events (i.e., a proxy to nutrient input) was strongly associated with seagrass habitat condition (defined
within). Concomitantly, sea cucumber densities were over a magnitude of order lower than in regionally
comparable Thalassia habitats, and negatively correlated with seagrass condition. Both top-down and
bottom-up considerations are discussed.
Ó 2013 Elsevier Ltd. All rights reserved.
1. Introduction
Seagrass beds represent highly productive ecosystems that can
sustain a variety of fisheries, and facilitate the transfer of energy
through marine food webs (de la Torre-Castro and Rönnbäck,
2004; Dorenbosch et al., 2005; Heck et al., 2008). However, as watershed development and urbanization grow, seagrass ecosystems
become overwhelmed by excessive nutrient addition, and opportunistic organisms that can rapidly uptake available nutrients become established (Cardoso et al., 2004; Schaffelke et al., 2005).
Many of these faster growing organisms, such as macroalgae, also
decay rapidly, and the resultant boom-and-bust cycles greatly alter
nutrient availability and recycling dynamics (Zimmermann and
Montgomery, 1984; Duarte, 1995; Flindt et al., 1999). These concepts, in part, form the basis for the paradox of enrichment (Rosenzweig, 1971), whereby increasing the supply of limiting nutrients
has a tendency to first stabilize populations, but continued enrichment leads to unstable population dynamics. The end result is that
most species of seagrass cannot survive in extremely productive
environments through a variety of mechanisms associated with
⇑ Corresponding author at: University of Guam Marine Laboratory, Mangilao, GU,
United States. Tel.: +1 671 735 2175.
E-mail address: [email protected] (P. Houk).
competitive exclusion (mainly due to light acquisition) (Burkholder et al., 2007), and macroalgal stands with unstable population cycles, and faster nutrient recycling rates, invade (Duarte, 1995). A
corollary of these trends is that fish and invertebrate populations
play a critical role in the processing of primary production and
detritus, and any changes in their abundances also impacts energy
flow through seagrass ecosystems (Heck and Valentine, 2006; Unsworth and Cullen, 2010; Baden et al., 2012). However, insight into
the complex relationships between watershed pollution, seagrass
dynamics, and fisheries remains limited (Baden et al., 2012). Meanwhile, the impacts of both land-based pollution and fishing are
increasing in severity across Micronesia (Golbuu et al., 2008,
2011; Houk and van Woesik, 2008; Houk et al., 2012b), as conservation strategies cite both as priority threats to marine resources
(Richmond et al., 2007).
Both surface and groundwater discharge can be strong contributors to nearshore nutrient dynamics and ecological assemblages
(Umezawa et al., 2002; Schaffelke et al., 2005; Paytan et al.,
2006), yet their expected influences differ. Groundwater input provides freshwater addition to marine environments through tidal
seeps, sink holes, and benthic substrates (Corbett et al., 1999; Rutkowski et al., 1999; Burnett et al., 2003), often in a cyclical manner
tied with low tides during new and full moon periods (Simmons,
1992). Submarine groundwater discharge (SGD) is known to be a
0025-326X/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.marpolbul.2013.03.012
Please cite this article in press as: Houk, P., et al. Watershed discharge patterns, secondary consumer abundances, and seagrass habitat condition in Yap,
Micronesia. Mar. Pollut. Bull. (2013), http://dx.doi.org/10.1016/j.marpolbul.2013.03.012
2
P. Houk et al. / Marine Pollution Bulletin xxx (2013) xxx–xxx
strong contributor of dissolved forms of nitrogen and phosphorous
to nearshore ecosystems (i.e., NO3, NH4, PO4) (Corbett et al., 1999;
Paytan et al., 2006). In contrast, centralized surface runoff following rainfall provides intermittent, seasonal freshwater input that
is similarly associated with dissolved nutrient addition, but coupled with organic detritus and sediments that have longer residence times and can disperse varying distances due to wind and
wave patterns (Devlin and Brodie, 2005). While increased macroalgal proliferation has been noted in response to both types of discharge (Lapointe et al., 2004; Schaffelke et al., 2005; Houk and
Camacho, 2010), added evidence into their relative contribution
to nearshore seagrass assemblages may help to explain observed
spatial dynamics of seagrass and macroalgal growth.
This study offers insight into complex watershed discharge patterns and their association with nearshore ecological assemblages.
We first evaluated the relative contribution of SGD and centralized
watershed discharge to seagrass assemblages adjacent to a locallymanaged marine conservation area in Yap, Micronesia. Building
upon an improved understanding of the nature and magnitude of
freshwater input, we examined nutrient concentrations to determine if alongshore gradients existed in accordance with watershed
discharge patterns, or if offshore-to-inshore gradients existed
across major habitats. Both watershed discharge and water quality
patterns were examined for their association with Thalassia seagrass habitat integrity. Sea cucumber densities and fish abundances were also quantified to explore whether secondary
consumers of primary biological growth may be contributing (or
responding) to the observed patterns in seagrass and macroalgal
growth.
2. Methods
2.1. Study area
Fieldwork was conducted within two municipalities along the
west coast of Yap Proper, a relatively small island complex within
the Federated States of Micronesia (6300 people, Fig. 1). Yap Proper
consists of a network of volcanic and limestone bedrock islands.
The study area had a limestone bedrock foundation with welldeveloped soils used for agriculture and agroforestry. Given these
characteristics, both surface and groundwater discharges were perceived to influence nearshore lagoon waters. The two municipalities associated with our study were Weloy and Dalipebinaw (446
and 397 people respectively).
Fig. 1. A map of the western lagoon of Yap Proper, Federated States of Micronesia, showing the study boundary (solid black line), no fishing marine conservation area (black
dashed line), Thalassia habitat (green polygon below salinity profile), and non-secondary forest land within the watershed (dark yellow polygons overlying terrestrial
vegetation). Legends indicate sampling sites and salinity gradient. (For interpretation of the references to color in this figure legend, the reader is referred to the web version
of this article.)
Please cite this article in press as: Houk, P., et al. Watershed discharge patterns, secondary consumer abundances, and seagrass habitat condition in Yap,
Micronesia. Mar. Pollut. Bull. (2013), http://dx.doi.org/10.1016/j.marpolbul.2013.03.012
P. Houk et al. / Marine Pollution Bulletin xxx (2013) xxx–xxx
In 2006, a no-take marine conservation area (MCA) was established within the study area to protect fishery resources within
the migratory channel that separates the inner seagrass and outer
coral habitats, encompassing 77.5 hectares. Despite much success
in enhancing fishery resources within the MCA (Houk et al.,
2012a), community member and elder fishermen concerns continue to grow over macroalgal proliferation in the nearshore seagrass beds, forming the basis for the present investigation. Our
goals were to characterize watershed discharge into the adjacent
lagoon and examine associations within Thalassia seagrass habitats
that represent desirable grounds for fishing and recreation.
2.2. Water quality data collection
Three types of water quality profiling were performed in order
to determine the nature and extent of watershed discharge: spatial, vertical, and temporal profiles. Spatial water-quality profiles
were conducted on numerous occasions that varied in lunar period
and rainfall intensity. In each instance, a continuously recording
YSI-6600 water quality instrument was secured to the bottom of
a small boat that was driven at a consistent, slow speed (1 m/s)
along pre-defined transects (Atkinson and Mabe, 2006). Salinity
data were collected across nearshore seagrass beds following this
procedure (Fig. 1). In addition to spatial profiles, depth profiles
were conducted at 100 m intervals extending from the two largest watershed discharge points to the inner boundary of the MCA
to characterize freshwater input during, or shortly after, storm
events.
Results from spatial water quality profiles indicated that submarine groundwater discharge (SGD) through Thalassia seagrass
habitats during full and new moon periods was a disproportional
driver of nearshore salinity patterns. Building upon these findings,
YSI instruments were installed at three sites to observe temporal
SGD patterns (i.e., temporal profiles). Two sensors were placed in
Thalassia seagrass beds that were expected to differed in SGD magnitude (sampling sites B and C, Fig. 1), and one was placed in Enhalus seagrass beds inshore of sampling site C, in front of the
mangrove stands. In each instance, sensors were fastened to concrete blocks and set to record at 10-min intervals for a time period
of 3–4 weeks that encompassed full and new moon periods. YSI
sensor availability limited their simultaneous deployment at all
three sites, however, each deployment encompassed new and full
moon periods and significant rainfall events within a three month
period. Sensors were observed to be submerged throughout their
deployment period.
Spatial profiles also provide guidance for selecting 30 sites
within the project boundary for exploratory nutrient sampling (nitrate-NO3-N, ammonium-NH4-N, and orthophosphate-PO4-P;
Fig. 1). During each of four boat-based sampling events, surface
waters (0.3 m depth) were collected, filtered, and stored on ice
for shipment to the University of Guam Water and Environmental
Research Institute. Sampling was conducted twice during the rainy
season (October 2010 – December 2011), and twice during the dry
season (January – March 2012) at varying lunar periods, but always
during high tide to facilitate boat access.
2.3. Ecological data collection
Ecological data were collected within Thalassia seagrass habitats during June 2012 (Fig. 1). Thalassia habitats were subjectively
delineated from Quickbird satellite imagery (1 m pixel resolution)
using a series of ground validation points that marked the habitat
boundaries (Fig. 1). Comparative sampling sites were then established within six sub-watersheds. The team of investigators used
standard protocols to collect fish, macroinvertebrate, and benthic
substrate data along a series of 5, 25 m transect lines during each
3
survey event. Fish biomass was estimated using a modified stationary point count (SPC) technique (Bohnsack and Bannerot, 1986),
whereby observers recorded the name and size of all food fish
within a 5 m radius for a period of 3 min. During each survey, 10
SPC’s were conducted by each of two observers at 15 m intervals,
who recorded the local names and sizes of all food fish observed
(mainly small snappers, emperorfish, parrotfish, and wrasse).
Macroinvertebrate densities were estimated by counting all sea
cucumbers, sea urchins, and shellfish within 2 m of either side of
the transect lines, yielding five replicate estimates of density per
100 m2 for each site. For comparative purposes, sea cucumber density data from a seagrass monitoring program in the Republic of Palau, an island archipelago southwest of Yap with similar marine
habitats, were also summarized (YG, unpublished monitoring data
from the Palau International Coral Reef Research Center). Palau
surveys estimated sea cucumber densities using the same protocols noted above. For both fish and macroinvertebrates, local
names were translated into scientific names using reference books
and field photos.
Benthic substrate abundances were estimated from
0.5 m 0.5 m string quadrats placed at 1 m intervals along the
transect lines. The substrates under each of six intersecting points
were recorded by observers. All substrates (seagrass and macroalgae mainly) were identified to the species level with the assistance
of trained scientists. These protocols resulted in 150 data points
per transect and five replicate transects per site upon which percent cover estimates were generated.
2.4. Data analyses
Spatial water quality profiles were characterized in the vicinity
of each sub-watershed monitoring site by generating area-based
statistics within 100 m of the ecological sampling sites. Temporal
profiles were analyzed in accordance with tide height and rainfall.
Tide data originated from the Tamil Harbor tide gauge, and cyclical
forecasts for the study period were generated using the Xtides software package (http://www.flaterco.com/xtide/files.html). Rainfall
data originated from the Yap airport meteorological station, and
are available through the National Oceanic and Atmospheric
Administration
Satellite
and
Information
Service
(www7.ncdc.noaa.gov). Probit regression analyses were used to
test if freshwater input events (i.e., binary, yes or no based upon
salinity profiles) were dependent upon minimum daily tidal
heights or rainfall (R Development Core Team, 2005).
Nutrient data were site-averaged prior to examination in order
to attenuate the relative differences between sampling sites. Statistical examinations then explored whether a net import or export of
nutrients may be present in the study area (i.e., east to west gradient, site-averaged data pooled by habitats), as well as if sub-watersheds may be influential to nutrient concentrations (i.e., north to
south gradient, data pooled across habitats by sub-watersheds).
Extending oceanward, the four major reef zones where nutrient
sampling was conducted were: (1) inner sand and Enhalus adjacent
to mangrove stands, (2) Thalassia seagrass beds, (3) reef flat coral
assemblages, and (4) offshore, outer reef waters. In all instances,
a minimum value was used for nitrate and orthophosphate concentrations below detection limits (0.001 mg/l NO3 and 0.1 ug/l
PO4). Due to a lack of normality with and without data transformations, non-parametric comparative tests were used to examine
both along shore and across shore gradients (Kruskal–Wallis tests,
post hoc Mann–Whitney tests with Bonferroni corrections).
Seagrass and macroalgal data were examined with respect to
watershed discharge patterns, nutrients, and secondary consumer
abundances. Our premise was that high watershed discharge volume and high nutrient concentrations may have negative associations with seagrass habitat condition because of new nutrient
Please cite this article in press as: Houk, P., et al. Watershed discharge patterns, secondary consumer abundances, and seagrass habitat condition in Yap,
Micronesia. Mar. Pollut. Bull. (2013), http://dx.doi.org/10.1016/j.marpolbul.2013.03.012
P. Houk et al. / Marine Pollution Bulletin xxx (2013) xxx–xxx
addition into the nearshore lagoon waters (i.e., NO3) (Cardoso et al.,
2004; Lapointe et al., 2004). Concomitantly, we also posit that low
secondary consumer abundances may be associated with macroalgal proliferation due to reduced nutrient storage and enhanced cycling of NH4 in the absence of secondary consumers (Vanni, 1996;
Baden et al., 2012). Two measures of benthic substrate data were
generated to represent indicators of seagrass habitat condition.
First, a benthic substrate ratio was calculated by the percent cover
of seagrass divided by the cover of macroalgae. Second, macroalgal
evenness was assessed using Margalef’s d-statistic, depicting both
the extent of macroalgal coverage and its distribution across taxa.
In the case of seagrass assemblages, high macroalgal evenness and
low benthic substrate ratio’s indicated poor condition. Average values of both indices were calculated from the five replicate transect
lines. Correlation examinations were performed to determine the
nature and strength of associations between salinity (i.e., SGD),
NH4 concentrations (i.e., nutrient availability), sea cucumber and
fish abundance (i.e., a proxy of nutrient retention within secondary
consumers), and both measure of seagrass habitat condition. Salinity measurements were derived from area-based statistics generated during horizontal profiles at low-tide (Fig. 1).
3. Results
Spatial water quality profiles indicated a strong influence of
submarine groundwater discharge (SGD) across Thalassia seagrass
habitats (Fig. 1). SGD was more pronounced in the northern study
area compared to the southern, with the lowest salinity levels recorded at site C adjacent to the MCA (Fig. 2). Temporal salinity profiles showed a strong dependence of SGD upon low tides events
during new and full moon periods at this site (z-value = 2.39,
32.6
32.4
32.2
32.0
31.8
31.6
31.4
31.2
31.0
30.8
A
North
B
C
D
E
F
------------------------- South
Fig. 2. Salinity statistics associated with each ecological sampling site derived from
horizontal water quality profiling. The black line represents the median, the boxes
indicate the 25th (lower) and 75th (upper) percentiles, and the error bars indicate
the 5th (lower) and 95th (upper) percentiles.
P = 0.016, Probit analysis, Fig. 3). Model predictions indicated that
50% probability thresholds for significant SGD occurred when tidal
heights fell below 0.36 m and pulsed events lasted between 10 and
30 min. Tidally influenced SGD was less frequently observed at site
B, and absent within Enhalus beds located inshore of site C (nonsignificant Probit analyses results for both). In contrast with SGD,
vertical profiles during significant rain events suggested that freshwater plumes remained within the top 0.5 m of the water column,
and were poorly mixed until turbulent outer reef or channel set-
2.0
35
1.5
20
1.0
Salinity (ppt)
Tide height (m)
(a)
32.8
salinity (ppt)
4
0.5
5
4/2/12
3/26/12
3/19/12
3/12/12
3/5/12
0.0
35
1.5
20
1.0
Salinity (ppt)
Tide height (m)
(b) 2.0
0.5
5
12/25/11
12/21/11
12/17/11
12/13/11
0.0
Fig. 3. (a and b) Temporal freshwater discharge patterns associated with (a) ecological sampling site C where submarine groundwater discharge was most pronounced, and
(b) site B located in Thalassia beds to the north (Fig. 1). Probit regression analysis indicated a significant relationship between freshwater input events and minimum low tide
at site C.
Please cite this article in press as: Houk, P., et al. Watershed discharge patterns, secondary consumer abundances, and seagrass habitat condition in Yap,
Micronesia. Mar. Pollut. Bull. (2013), http://dx.doi.org/10.1016/j.marpolbul.2013.03.012
5
P. Houk et al. / Marine Pollution Bulletin xxx (2013) xxx–xxx
Nitrate (mg/l)
(a)
A
0.009
0.006
E
B-D-F
C
D-E
A
B-C
0.003
0.000
(b)
C
Ammonium (mg/l)
0.5
F
0.4
0.3
0.2
0.1
E
F
A-C-F
D
B
F
D
B-C-E
B
D-E
B
D
A
A
0.0
Inner
Seagrass
Reef Flat
A-C-E
Outer Reef
Inshore -------------------- Offshore
Fig. 4. Nitrate (NO3) and Ammonium (NH4) concentrations across the study area.
Means (±SE) are shown for data aggregated across major habitat types to highlight
significant inshore-to-offshore trends. Letters indicate the spread of individual data
points, with reference to their north–south location (sampling sites A–F).
tings were encountered (Supplemental Fig. S1). Rainfall was not an
influential predictor of temporal salinity patterns at any of the
monitoring sites.
Nutrient sampling highlighted low nitrate and below detectable
orthophosphate concentrations across the study area (mean values
<0.004 mg/l NO3 and <0.1 ug/l PO4). However, there was a steady
increase in nitrate moving from inshore to offshore waters
(P < 0.05, outer reef versus inner seagrass habitats, post hoc
Mann–Whitney U-Tests; Fig. 4). Ammonium concentrations were
comparatively higher and more variable than nitrate or phosphate.
The most notable finding was a disproportionally high NH4 concentration found in the Thalassia habitat associated with site C, corresponding with the largest contribution of SGD (Fig. 4b). In
addition, there was a non-significant increase in NH4 concentrations moving from inshore to offshore waters.
Collectively, water quality profiling results served as a basis to
focus ecological sampling upon Thalassia habitats. Seagrass habitat
condition was strongly associated with both salinity and secondary
consumer abundances (r > 0.77, P < 0.05 for all correlations), but
not ammonia concentrations (NH4) (Table 1). One exception to
the non-significant relationships between ammonia and seagrass
assemblages existed at site C, where the lowest seagrass coverage
corresponded with the highest NH4 concentrations. The percent
cover and evenness of macroalgae increased with freshwater input
(strongest, most consistent correlate), and decreased with sea
cucumber density and fish biomass (Fig. 5). Overall, seagrass coverage ranged between 39% and 68%, with sites A and C being disproportionally lower than others (Fig. 5). Macroalgal coverage
was low across the study area (5–20%) with the exceptions of site
C, where temporal profiles found highest SGD, and site A. Site A
had the greatest coverage and diversity of macroalgae, but was also
in close proximity to the larger, northern channel associated with
the Weloy municipality where flushing occurs (Fig. 5). The variation in macroalgal assemblages stemmed from increased abundances of Caulerpa, Laurencia, and several blue-green algae where
low salinity existed. Halimeda represented ubiquitous macroalgae
that varied less across study sites.
Low sea cucumber densities of 1.6–3.9 individuals per 100 m2
(overall mean of 2.6 across the study area) were reported from
Thalassia habitats, and were almost entirely comprised of the small
black cucumber Holothuria atra. Sea cucumber densities across the
study area were over a magnitude of order lower than in comparative Thalassia beds in Palau (mean of 115 individuals per 100 m2).
Fish biomass varied widely among the sites, ranging between 0.1
and 1.0 kg/SPC mean biomass, with the differences attributed to
whether or not small snapper or emperorfish were abundant
(Lethrinus harak and Lutjanus gibbus).
4. Discussion
This study reported a disproportional contribution of SGD in
delivering freshwater to the nearshore ecosystems along the western coast of a limestone island in Yap Proper, Micronesia. SGD was
maximal when tide heights were lowest during new and full moon
periods. In contrast, freshwater surface discharge following storm
events remained in the upper 0.5 m of the water column, and
had limited vertical mixing within lagoon waters. The negative
relationship between SGD and seagrass habitat condition suggested its strong influence upon the nearshore Thalassia beds.
However, a critical intermediary relationship between SGD and
nutrient concentrations was only seen for site C, where extensive
SGD and high NH4 concentrations existed. Elsewhere, the lack of
a generalized association between nutrients and seagrass condition across the study area supported the findings, and doctrine,
describing that pulsed SGD occurred over short-time periods
(Schaffelke, 1999; Rutkowski et al., 1999), representing a timeframe when boat-access for nutrient sampling across the entire
study area was not possible during the present study (i.e., low
tides). However, given the strong association between salinity derived from spatial profiling during low tides and both measures of
seagrass habitat condition, we purport that salinity served as a useful proxy of nutrient addition from SGD (Johannes and Hearn,
1985). Enhanced nutrient sampling during low tides would be
needed to further develop this association.
Despite SGD influence and its coupling with ammonia concentrations at site C, nutrient sampling suggested that a net import
Table 1
Pearson correlation coefficients describing the association between Thalassia habitat-condition metrics, secondary consumer abundances, and proxies to SGD input and nutrient
availability (right). The left half of the table provides ordinal rankings describing which water quality and secondary consumer variables had strongest associations with condition
metrics.
Seagrass–macroalgae ratio
Seagrass–macroalgae ratio
Macroalgal evenness
Salinity
Fish biomass
Sea cucumber density
Ammonia (NH4)
Macroalgal evenness
Salinity
–
1
3
1
ns
1
2
ns
ns
Fish biomass
0.90**
0.94**
0.72
0.78*
0.85*
0.89*
–
–
–
Sea cucumber density
Ammonia (NH4)
0.89**
ns
ns
ns
ns
ns
ns
ns
ns
–
–
–
*
P < 0.05.
**
P < 0.01.
Please cite this article in press as: Houk, P., et al. Watershed discharge patterns, secondary consumer abundances, and seagrass habitat condition in Yap,
Micronesia. Mar. Pollut. Bull. (2013), http://dx.doi.org/10.1016/j.marpolbul.2013.03.012
6
P. Houk et al. / Marine Pollution Bulletin xxx (2013) xxx–xxx
Fig. 5. Spatial patterns in seagrass and macroalgal percent cover, sea cucumber densities, and watershed sizes across the study area. Graphs and symbols are sized in
proportion to percent cover and density reported in the results. Letters (A–F) indicate the ecological sampling sites.
of new nitrogen and phosphorous (NO3 and PO4) from offshore to
inshore waters was one characteristic regime of our study area. The
low and often undetectable concentrations of NO3 and PO4 were
consistent with tropical marine waters under limited pollution
influence, regardless of sampling regime (Devlin and Brodie,
2005; DiDonato et al., 2009). These findings question the extent
to which new nutrient addition may have contributed to the nearshore lagoon habitats, and highlighted a need to focus upon cycled
nutrients as well (i.e., ammonia). Our reported ammonium (NH4)
concentrations in Thalassia seagrass beds were a magnitude of order higher than offshore waters, similar to those reported in Thalassia beds elsewhere (Ziegler and Benner, 1999), and a magnitude
of order lower than reported from direct SGD pore-water samples
in Thalassia beds (Zimmermann and Montgomery, 1984). The high
concentrations reported at site C were consistent with rapid nutrient cycling rates from macroalgal mats compared to slower cycling, and greater storage, in seagrass beds (Zimmermann and
Montgomery, 1984; Ziegler and Benner, 1999; Cornelisen and Thomas, 2006). Thus, our findings resonate with ecological theory suggesting that enhanced nutrient cycling and less nutrient storage
leads to unstable population dynamics (Rosenzweig, 1971), and
can lead to eutrophication in seagrass beds (Burkholder et al.,
2007). We report more chaotic macroalgal growth dynamics (i.e.,
higher evenness) and lower seagrass coverage in association with
both NH4 concentrations (at site C) and SGD proxies to NH4 (across
the entire study area). Yet, specific to our study area are the potential secondary consequences of enhance NH4 delivery to the adjacent marine conservation area through tidal flushing.
Given the sparse human population and urban development in
the study watersheds, it is appropriate to consider the role of secondary consumers in regulating nutrient availability and cycling (Vanni,
2002). Several lines of evidence support the contribution of sea
cucumbers in regulating primary biological production in our study
area: the sedentary nature of adult sea cucumbers, a history of commercial sea cucumber harvesting in Yap with limited documentation
in 1995, and 2003 to 2007 (Friedman et al., 2008), disproportionally
lower sea cucumber densities compared with Thalassia habitats in
Palau, slow recover times reported for holothurian populations
(Uthicki et al., 2004), and food web studies highlighting the influence
of secondary consumer deficiencies on nutrient cycling and algal
growth (Vanni, 1996, 2002). While correlations inferred associations
and not causality, the nature and strength of correlations indicate
interaction pathways that are most pertinent for further study. Similar to SGD, intermediary associations with cycled nutrients (NH4 in
particular) remain lacking but clearly represent desirable focal areas
for research to assess the contribution of sea cucumbers in regulating nutrient cycling dynamics.
Fish also play a critical role in storing, processing, and redistribution nutrients (Vanni, 2002), yet obviously have a higher mobility in seagrass ecosystems compared with sea cucumbers.
Please cite this article in press as: Houk, P., et al. Watershed discharge patterns, secondary consumer abundances, and seagrass habitat condition in Yap,
Micronesia. Mar. Pollut. Bull. (2013), http://dx.doi.org/10.1016/j.marpolbul.2013.03.012
P. Houk et al. / Marine Pollution Bulletin xxx (2013) xxx–xxx
Associations between fish biomass and seagrass condition metrics
were weakest overall, supporting that fish abundances may have
more bi-directional interactions with habitat integrity as compared with sedentary sea cucumbers that typically attain high population densities in Thalassia habitats.
5. Conclusions
This study reported a disproportional contribution of SGD in
delivering freshwater to the nearshore seagrass ecosystems associated with the limestone island of Yap Proper. SGD represented
short-lived, pulsed events that were best detected from spatial
and temporal profiling. In comparison to stormwater discharge,
SGD events had a greater influence on seagrass habitats due to
the predictable nature of discharge with low tides, and the limited
mixing of stormwater runoff. Thus, we conclude that SGD was an
influential source of new nutrient addition to these systems, but
ambient concentrations of NO3 and PO4 were low. Negative relationships between seagrass condition and sea cucumber populations suggested that the processing and storage of nutrients
within secondary consumers may also contribute to nutrient cycling dynamics. A better understanding of how top-down and bottom-up processes contributed to seagrass–macroalgal dynamics
can come through further study NH4 dynamics in relation to both
SGD and sea cucumber densities.
Acknowledgments
Funding for this project originated from the University of Guam
Water and Environmental Research Institute, the Micronesian Conservation Trust, and NOAA Coastal Oceans Program NA160P2920.
The authors are grateful for extensive cooperation from community members from Weloy and Dalipebinaw municipalities, the Palau International Coral Reef Research Center, Dr. Robert Richmond,
Yap State Environmental Protection Agency, and Yap Community
Action Program. Finally, Arius Merep, Mike Gaag, Joe Nam, and
Jesse Googdow were all essential leaders for field data collection.
Appendix A. Supplementary material
Supplementary data associated with this article can be found, in
the
online
version,
at
http://dx.doi.org/10.1016/
j.marpolbul.2013.03.012.
References
Atkinson, S.F., Mabe, J.A., 2006. Near real-time monitoring and mapping of specific
conductivity levels across Lake Texoma. USA. Environ. Monit. Assess. 120, 449–
460.
Baden, S., Emanuelsson, A., Pihl, L., Svensson, C.J., Aberg, P., 2012. Shift in seagrass
food web structure over decades is linked to overfishing. Mar. Ecol. Prog. Ser.
451, 61–73.
Bohnsack, J.A., Bannerot, S.P., 1986. A stationary visual census technique for
quantitatively assessing community structure of coral reef fishes. National
Oceanic and Atmospheric Administration Technical Report NMFS 41.
Washington.
Burkholder, J.A.M., Tomasko, D.A., Touchette, B.W., 2007. Seagrasses and
eutrophication. J. Exp. Mar. Biol. Ecol. 350, 46–72.
Burnett, W.C., Bokuniewicz, H., Huettel, M., Moore, W.S., Taniguchi, M., 2003.
Groundwater and pore water inputs to the coastal zone. Biogeochemistry 66, 3–
33.
Cardoso, P., Pardal, M., Lillebø, A., Ferreira, S., Raffaelli, D., Marques, J., 2004.
Dynamic changes in seagrass assemblages under eutrophication and
implications for recovery. J. Exp. Mar. Biol. Ecol. 302, 233–248.
Corbett, D.R., Chanton, J., Burnett, W., Dillon, K., Rutkowski, C., Fourqurean, J.W.,
1999. Patterns of groundwater discharge into Florida Bay. Limnol. Oceanogr. 44,
1045–1055.
Cornelisen, C.D., Thomas, F.I.M., 2006. Water flow enhances ammonium and nitrate
uptake in a seagrass community. Mar. Ecol. Prog. Ser. 312, 1–13.
de la Torre-Castro, M., Rönnbäck, P., 2004. Links between humans and seagrasses –
an example from tropical East Africa. Ocean Coast. Manage. 47, 361–387.
7
Devlin, M., Brodie, J., 2005. Terrestrial discharge into the Great Barrier Reef Lagoon:
nutrient behavior in coastal waters. Mar. Pollut. Bull. 51, 9–22.
DiDonato, G.T., DiDonato, E.M., Smith, L.M., Harwell, L.C., Summers, J.K., 2009.
Assessing coastal waters of American Samoa: territory-wide water quality data
provide a critical ‘‘big-picture’’ view for this tropical archipelago. Environ.
Monit. Assess. 150, 157–165.
Dorenbosch, M., Grol, M., Christianen, M., Nagelkerken, I., Van Der Velde, G., 2005.
Indo-Pacific seagrass beds and mangroves contribute to fish density and
diversity on adjacent coral reefs. Mar. Ecol. Prog. Ser. 302, 63–76.
Duarte, C.M., 1995. Submerged aquatic vegetation in relation to different nutrient
regimes. Ophelia 41, 87–112.
Flindt, M.R., Pardal, M.Â., Lillebø, A.I., Martins, I., Marques, J.C., 1999. Nutrient
cycling and plant dynamics in estuaries: a brief review. Acta Oecol. 20, 237–
248.
Friedman, K., Ropeti, E., Tafileichig, A., 2008. Development of a management plan for
Yap’s sea cucumber fishery. SPC Beche de Mer Information Bulletin 28, 7–13.
Golbuu, Y., Fabricius, K., Victor, S., Richmond, R.H., 2008. Gradients in coral reef
communities exposed to muddy river discharge in Pohnpei. Micronesia. Estuar.
Coast. Shelf S. 76, 14–20.
Golbuu, Y., Van Woesik, R., Richmond, R.H., Harrison, P., Fabricius, K.E., 2011. River
discharge reduces reef coral diversity in Palau. Mar. Pollut. Bull. 62, 824–831.
Heck, K.L., Carruthers, T.J.B., Duarte, C.M., Hughes, A.R., Kendrick, G., Orth, R.J.,
Williams, S.W., 2008. Trophic transfers from seagrass meadows subsidize
diverse marine and terrestrial consumers. Ecosystems 11, 1198–1210.
Heck, K.L., Valentine, J.F., 2006. Plant–herbivore interactions in seagrass meadows. J.
Exp. Mar. Biol. Ecol. 330, 420–436.
Houk, P., Benavente, D., Fread, V., 2012a. Characterization and evaluation of coral
reefs around Yap Proper, Federated States of Micronesia. Biodivers. Conserv. 21,
2045–2059.
Houk, P., Rhodes, K., Cuetos-Bueno, J., Lindfield, S., Fread, V., McIlwain, J.L., 2012b.
Commercial coral-reef fisheries across Micronesia: a need for improving
management. Coral Reefs 31, 13–26.
Houk, P., Camacho, R., 2010. Dynamics of seagrass and macroalgal assemblages in
Saipan Lagoon, Western Pacific Ocean: disturbances, pollution, and seasonal
cycles. Bot. Mar. 53, 205–212.
Houk, P., van Woesik, R., 2008. Dynamics of shallow-water assemblages in the
Saipan Lagoon. Mar. Ecol. Prog. Ser. 356, 39.
Johannes, R., Hearn, C., 1985. The effect of submarine groundwater discharge on
nutrient and salinity regimes in a coastal lagoon off Perth. Western Australia.
Estuar. Coast. Shelf S. 21, 789–800.
Lapointe, B.E., Barile, P.J., Matzie, W.R., 2004. Anthropogenic nutrient enrichment of
seagrass and coral reef communities in the Lower Florida Keys: discrimination
of local versus regional nitrogen sources. J. Exp. Mar. Biol. Ecol. 308, 23–58.
Paytan, A., Shellenbarger, G.G., Street, J.H., Gonneea, M.E., Davis, K., Young, M.B.,
Moore, W.S., 2006. Submarine groundwater discharge: an important source of
new inorganic nitrogen to coral reef ecosystems. Limnol. Oceanogr. 51, 343–
348.
R Development Core Team, 2005. R: A language and environment for statistical
computing, reference index version 2.2.1. R Foundation for Statistical
Computing, Vienna, Austria. ISBN 3-900051-07-0, URL <http://www.Rproject.org>.
Richmond, R.H., Rongo, T., Golbuu, Y., Victor, S., Idechong, N., Davis, G., Kostka, W.,
Neth, L., Hamnett, M., Wolanski, E., 2007. Watersheds and coral reefs:
conservation science, policy, and implementation. BioScience 57, 598–607.
Rosenzweig, M.L., 1971. Paradox of enrichment: destabilization of exploitation
ecosystems in ecological time. Science 171, 385–387.
Rutkowski, C.M., Burnett, W.C., Iverson, R.L., Chanton, J.P., 1999. The effect of
groundwater seepage on nutrient delivery and seagrass distribution in the
northeastern Gulf of Mexico. Estuar. Coast. 22, 1033–1040.
Schaffelke, B., 1999. Short-term nutrient pulses as tools to assess responses of coral
reef macroalgae to enhanced nutrient availability. Mar. Ecol. Prog. Ser. 182,
305–310.
Schaffelke, B., Mellors, J., Duke, N.C., 2005. Water quality in the Great Barrier Reef
region: responses of mangrove, seagrass and macroalgal communities. Mar.
Poll. Bull. 51, 279–296.
Simmons, G.M., 1992. Importance of submarine groundwater discharge (SGWD)
and seawater cycling to material flux across sediment/water interfaces in
marine environments. Mar. Ecol. Prog. Ser. 84, 173–184.
Umezawa, Y., Miyajima, T., Kayanne, H., Koike, I., 2002. Significance of groundwater
nitrogen discharge into coral reefs at Ishigaki Island, southwest of Japan. Coral
reefs 21, 346–356.
Unsworth, R.K.F., Cullen, L.C., 2010. Recognising the necessity for Indo-Pacific
seagrass conservation. Conserv. Lett. 3, 63–73.
Uthicki, S., Welch, D., Benzie, J.A.H., 2004. Slow growth and lack of recovery in
overfished holothurians on the Great Barrier Reef: Evidence from DNA
fingerprints and repeated large-scale surveys. Conserv. Biol. 18, 1395–1404.
Vanni, M.J., 1996. Nutrient transport and recycling by consumers in lake food webs:
implications for algal communities. In: Food Webs: Integration of Patterns and
Dynamics. Chapman and Hall, New York, pp. 81–95.
Vanni, M.J., 2002. Nutrient cycling by animals in freshwater ecosystems. Annu. Rev.
Ecol. Syst. 33, 341–370.
Ziegler, S., Benner, R., 1999. Nutrient cycling in the water column of a subtropical
seagrass meadow. Mar. Ecol. Prog. Ser. 188, 51–58.
Zimmermann, C.F., Montgomery, J.R., 1984. Effects of a decomposing drift algal mat
on sediment pore water nutrient concentrations in a Florida seagrass bed. Mar.
Ecol. Prog. Ser. 19, 299–302.
Please cite this article in press as: Houk, P., et al. Watershed discharge patterns, secondary consumer abundances, and seagrass habitat condition in Yap,
Micronesia. Mar. Pollut. Bull. (2013), http://dx.doi.org/10.1016/j.marpolbul.2013.03.012