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Functional diversity in amphipods revealed by stable isotopes in an eelgrass ecosystem

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Abstract

Amphipods are often dominant components of benthic marine communities and may exhibit taxon-specific differences in feeding behavior. As a result, variation in the composition of amphipod communities is an important metric for the interpretation of trophic dynamics in benthic marine ecosystems. Though previous studies of amphipod diets indicate functional diversity among taxa, few studies have examined whether these differences are detectible using time-integrated natural tracers of in situ feeding habits. We used stable isotope ratios of nitrogen (delta N-15) and carbon (delta C-13) to examine trophic structure among amphipod taxa belonging to 5 families in an eelgrass (Zostera marina) ecosystem in San Diego Bay, California. The relative contribution of sources of primary production to amphipod diets was further analyzed using a mixing model bracketed by 2 dominant sources of primary production in the system: eelgrass and algae. We detected significant differences in both delta C-13 and delta N-15 among amphipod taxa, indicating family-specific differences in feeding habits that generally agree with previous studies of amphipod diets. Hyalids fed almost exclusively on eelgrass, ischyrocerids and ampithoids tended to feed more on algae and eelgrass, respectively, and caprellids exhibited heterogeneous feeding on both algae and eelgrass. The relatively high delta N-15 value of oedicerotids suggested that this group was likely carnivorous. Our findings are in general agreement with previous descriptions of family-specific amphipod feeding behaviors, suggesting that stable isotopes are a useful tool for describing the functional roles of mesograzers in eelgrass ecosystems.
MARINE ECOLOGY PROGRESS SERIES
Mar Ecol Prog Ser
Vol. 420: 277–281, 2010
doi: 10.3354/meps08873 Published December 16
INTRODUCTION
Trophic interactions structure communities and
influence productivity across multiple trophic levels
(Paine 1980, Heck & Valentine 2007). Most studies
demonstrating such interactions in benthic marine
habitats have focused on the effects of macrograzers
(e.g. fishes, sea urchins and mollusks), whereas
smaller mesograzers (e.g. amphipods) have received
relatively less attention (Thayer et al. 1978, Duffy &
Hay 2000). Mesograzers, however, can exhibit interac-
tion strengths similar to macrograzers (Sala & Graham
2002) and may exert strong top-down effects on the
structure and productivity of benthic macrophyte
assemblages (Duffy & Hay 2000). Amphipods are par-
ticularly important in eelgrass ecosystems because
they are significant consumers of primary production
and graze preferentially on epiphytic algae, which in
turn enhances eelgrass production (Kitting et al. 1984,
Orth & Van Montfrans 1984). Determining whether
© Inter-Research 2010 · www.int-res.com*Email: nilraf@gmail.com
NOTE
Functional diversity in amphipods revealed by
stable isotopes in an eelgrass ecosystem
J. P. Farlin1,*, L. S. Lewis1, 2, T. W. Anderson1, C. T. Lai1
1Department of Biology and Coastal & Marine Institute, San Diego State University, 5500 Campanile Drive, San Diego,
California 92182-4614, USA
2Present address : Center for Marine Biodiversity and Conservation, Scripps Institution of Oceanography,
9500 Gilman Drive, La Jolla, California 92083-0202, USA
ABSTRACT: Amphipods are often dominant components of benthic marine communities and may
exhibit taxon-specific differences in feeding behavior. As a result, variation in the composition of
amphipod communities is an important metric for the interpretation of trophic dynamics in benthic
marine ecosystems. Though previous studies of amphipod diets indicate functional diversity among
taxa, few studies have examined whether these differences are detectible using time-integrated nat-
ural tracers of in situ feeding habits. We used stable isotope ratios of nitrogen (δ15N) and carbon (δ13C)
to examine trophic structure among amphipod taxa belonging to 5 families in an eelgrass (Zostera
marina) ecosystem in San Diego Bay, California. The relative contribution of sources of primary pro-
duction to amphipod diets was further analyzed using a mixing model bracketed by 2 dominant
sources of primary production in the system: eelgrass and algae. We detected significant differences
in both δ13C and δ15N among amphipod taxa, indicating family-specific differences in feeding habits
that generally agree with previous studies of amphipod diets. Hyalids fed almost exclusively on eel-
grass, ischyrocerids and ampithoids tended to feed more on algae and eelgrass, respectively, and
caprellids exhibited heterogeneous feeding on both algae and eelgrass. The relatively high δ15N
value of oedicerotids suggested that this group was likely carnivorous. Our findings are in general
agreement with previous descriptions of family-specific amphipod feeding behaviors, suggesting
that stable isotopes are a useful tool for describing the functional roles of mesograzers in eelgrass
ecosystems.
KEY WORDS: Functional diversity · Stable isotopes · Eelgrass food web · Amphipods · Amphipod
feeding
Resale or republication not permitted without written consent of the publisher
Mar Ecol Prog Ser 420: 277–281, 2010
amphipods are grazing on an algal-based or eelgrass-
based (living or detrital tissue) food source has implica-
tions on their net (positive, negative, or neutral) effects
on ecosystem primary production.
In studies of marine food webs, amphipods are often
grouped into a single trophic guild based on the
assumption that they are functionally redundant
(Thayer et al. 1978, Kitting et al. 1984, Bell 1991, Fre-
driksen 2003, Nagelkerken et al. 2006, Davenport &
Anderson 2007). This assumption, however, has been
challenged due to contrary evidence provided by feed-
ing assays and gut content analyses (Poore 1994, Duffy
& Harvilicz 2001). Though such studies provide valu-
able insight into feeding behaviors of amphipods, they
are limited to observing individual grazing behaviors
as snapshots in time (e.g. gut contents) or under less
realistic conditions (e.g. laboratory assays and meso-
cosms).
The diversity of amphipod feeding behaviors in the
wild remains an important gap in our knowledge of
benthic ecosystems (Duffy & Hay 1991) and is crucial
to our understanding of food web dynamics in these
systems (Poore et al. 2008). One method of exploring
the feeding history and trophic diversity of wild organ-
isms is through the use of stable isotope ratios of car-
bon (13C/12C) and nitrogen (15N/14N), whereby carbon
is used to trace primary production and nitrogen to
infer trophic level (Peterson & Fry 1987). Our objective
was to use stable isotopes to examine the feeding his-
tory of 5 amphipod taxa, each within a different family
(Ampithoidae, Caprellidae, Hyalidae, Ischyroceridae,
and Oedicerotidae) within an eelgrass (Zostera marina)
ecosystem in San Diego, California. We selected these
5 amphipod families because they were common in the
study area (Lewis 2009), were readily identified using
taxonomic keys (e.g. Chapman 2007), and were
expected to exhibit different modes of feeding based
on previous research and jaw morphology (Chapman
2007). We then examined whether our findings based
on stable isotope ratio analyses agreed with previous
descriptions of family-specific feeding behaviors.
MATERIALS AND METHODS
Study area and collection. Amphipods, filamentous
epiphytic algae, eelgrass, and eelgrass detritus were
collected haphazardly during low tide from ca. 100 m2
of eelgrass habitat adjacent to Shelter Island in San
Diego Bay, California. This site was chosen to take
advantage of the existing infrastructure associated
with ongoing research (Lewis 2009). At low tide,
researchers waded into the eelgrass bed to a depth of
approximately 0.5 m prior to collecting samples. Eel-
grass samples, containing epiphytic algae and epi-
fauna, were pulled by hand and immediately placed in
500 μm mesh bags. The benthos was then skimmed to
collect detritus and benthic amphipods. A total of 9
grab samples and 8 benthic samples were collected on
18 October and 13 November, 2008. All samples were
immediately placed on ice and transported to the labo-
ratory for processing. In the lab, epiphytic algae and
fresh young eelgrass leaves were isolated from grab
samples. The remaining eelgrass samples were thor-
oughly rinsed with deionized water over a 500 μm
sieve to isolate amphipods from other material. Benthic
samples were also rinsed over a 500 μm sieve, and
amphipods and detrital (i.e. dead and decaying) eel-
grass were removed and isolated. All samples were
frozen (–20°C) until preparation for stable isotope
analysis. We intended to sample macroalgae, but none
were present in the eelgrass bed during sampling. Epi-
phytic filamentous algae were analyzed and inter-
preted as a general ‘algal signature’ on the basis of the
assumption that macroalgae and filamentous algae
have similarly depleted δ13C values (approximately
10‰ less) than those of eelgrass (Currin et al. 1995,
Moncreiff & Sullivan 2001).
Amphipod identification. Amphipods were sorted to
family according to Chapman (2007). We used this tax-
onomic category because identification of amphipods
to genus and species was not feasible for all sexes and
stages of specimens used in our study (Chapman
2007). We later identified the numerically dominant
genus within each family (Table 1) by further examin-
ing identifiable voucher specimens with taxonomists
from the San Diego City Metropolitan Waste Water
District.
Sample preparation and stable isotope analysis.
Samples were thawed, sorted in clean Petri dishes, and
then rinsed with deionized water to remove residual
salt water. Amphipods were sorted to family and indi-
viduals were pooled (n 5 to 45 per replicate sample;
Table 1) to attain adequate material for isotope analy-
ses (1.0 to 2.0 mg dry wt). Young eelgrass leaves, detri-
tal eelgrass, and epiphytic algae were cleaned of all
fouling material prior to processing and analysis. All
samples were placed in a drying oven at 60°C for 48 h,
homogenized, placed into tin capsules and weighed.
Isotopic ratios were measured by combustion using
continuous-flow isotope-ratio mass spectrometry at
San Diego State University’s (SDSU) Ecology Analyti-
cal Facility (Thermo Scientific DeltaPlus Advantage
IRMS, n = 66) and the Stable Isotope Facility at the
University of California, Davis (PDZ Europa 20-20
IRMS, n = 33). Stable carbon and nitrogen isotope
ratios of a sample were measured against laboratory
reference materials selected to be compositionally sim-
ilar to the samples being analyzed in both analytical
laboratories. At SDSU, laboratory reference materials
278
Farlin et al.: Stable isotopes of amphipods
were calibrated against NIST standard reference
materials USGS40 and USGS41. Delta (δ) values for C
and N were calculated using standard delta notation:
(1)
where Ris the molar ratio of the heavy to light isotopes.
Carbon and nitrogen isotope ratios are reported rela-
tive to the Vienna PDB scale (Coplen et al. 2006) and
atmospheric N2(Mariotti 1983), respectively.
A 2-source mixing model was used to estimate
dietary composition of amphipod families using the
equation:
(2)
where fis the fraction of the diet derived from algae.
The average δ13C values of producers used in the cal-
culation were –9.2 ± 1.35‰ for eelgrass (aver-
age of live and detrital eelgrass) and –17.2 ±
4.5‰ for algae. Trophic enrichment was cal-
culated as the mean difference between δ15N
values of each amphipod family and the aver-
age δ15N value of primary producers (10.7 ±
1.7‰).
Statistical analysis. Outliers greater than
1.5 ×IQR (inter-quartile range) were identi-
fied and removed prior to analyses, resulting
in less than 3% exclusion of data in analyses.
Differences among amphipod families in δ13C
and δ15N values were examined using 1-way
ANOVA. When significant, pairwise multiple
comparisons among amphipod taxa were
conducted using Tukey’s HSD test. All
statistical analyses were conducted using
SYSTAT 12.01.02. We used ‘IsoError’ (Phillips
& Gregg 2001) and a 2-source mixing model
to estimate the proportion of the diet of the
amphipod families derived from eelgrass- vs.
algae-based carbon sources. Errors were
propagated and reported as 95 % confidence intervals
for the mixing-model results using IsoError software.
RESULTS
Carbon isotope signatures of eelgrass (mean of live
and detrital) and algae differed by 8 ‰ and bracketed
all amphipod δ13C values (Fig. 1). Significant differ-
ences in δ13C were detected among amphipod taxa
(F4,45 = 5.7, p = 0.001), with hyalids showing a signifi-
cantly higher δ13C than all other families. Oedicerotids
were enriched in δ15N relative to hyalids (F4,45 = 4.055,
p = 0.007) and appeared to be partially carnivorous as
suggested by their higher, but slightly overlapping,
δ15N values (Fig. 1) and greater trophic enrichment
(Table 1). Caprellids, ischyrocerids, and ampithoids all
exhibited intermediate δ13C and δ15N values (Fig. 1,
fCC
C
=
δδ
δδ
13 13
13
amphipods eelgrass
algae 113Ceelgrass
δ= −
×
R
R
sample
standard
1 1000
279
Family Genus δ15N δ13C Reps Ind./rep. % algae δ15N enrichment
Ampithoidae Ampithoe 12.4 ± 0.5 –12.4 ± 1.0 10 11.5 39.2 ± 16% 1.7
Caprellidae Caprella 11.6 ± 0.3 13.2 ± 0.5 10 12.9 49.7 ± 13% 0.9
Hyalidae Protohyale 11.5 ± 0.4 –9.7 ± 0.3 11 16.5 5.2 ± 6 % 0.8
Ischyroceridae Erichthonius 12.4 ± 0.2 –14.0 ± 0.9 10 42.3 59.8 ± 18% 1.7
Oedicerotidae Hartmanodes 14.0 ± 0.7 12.1 ± 1.3 4 4.5 35.9 ± 19% 3.3
Primary producers
Live eelgrass 10.7 ± 0.5 –8.3 ± 0.4 8 1
Detrital eelgrass 10.5 ± 0.4 –10.2 ± 0.2 8 1
Filamentous algae 11.0 ± 0.5 –17.2 ± 1.8 6 >100
Table 1. Isotopic ratios of amphipod groups and primary producers from an eelgrass bed in San Diego Bay, California. Also shown
are no. of replicates, average no. of individuals per replicate, proportion of algae in the diet (± 95 % CI) and trophic enrichment
of amphipods
Fig. 1. Mean stable isotope ratios (±1 SE) of amphipod families (filled
symbols), and primary producers (open symbols) from an eelgrass bed in
San Diego Bay, California
Mar Ecol Prog Ser 420: 277–281, 2010
Table 1). The mixing model indicated that eelgrass
production (live or detrital) constituted 94.8% and
60.8% of the diet of hyalids and ampithoids, respec-
tively. Algal production constituted 59.8% of the diet
for ischyrocerids, whereas the mixing model indicated
a relatively equal contribution of algae and eelgrass to
the diet of caprellids.
DISCUSSION
We employed stable isotopes to explore time-
integrated differences in the diets of amphipod taxa in
situ. Our findings are in general agreement with previ-
ous descriptions of family-specific feeding habits
(Brawley & Fei 1987, Dewey 1970, Dixon & Moore
1997, Poore 1994, Duffy & Harvilicz 2001, Chapman
2007, Poore et al. 2008). For example, intermediate
δ13C signatures for ampithoids, caprellids and ischyro-
cerids agree with previous reports of heterogeneous
feeding behaviors (Brawley & Fei 1987, Dewey 1970,
Duffy & Harvilicz 2001), with our mixing model deter-
mining that ampithoids consume more eelgrass and
ischyrocerids favor microalgae. Hyalids have previ-
ously been described as feeding on brown algae (Poore
2004). Our δ13C measurements suggest that hyalids
were supported by eelgrass-derived carbon, which
was in agreement with a macrophagous diet, but not in
agreement with the source of carbon. Based on jaw
morphology (adapted for consuming macrophytes),
consumption of eelgrass in the absence of macroalgae
in our study is a likely alternative feeding response.
Oedicerotids are known to feed as predators on
meiobenthic animals such as harpacticoid copepods
(Yu & Suh 2002), consistent with the enriched δ15N val-
ues observed in our study. Assuming these oedicero-
tids were mostly carnivorous, our data suggest
ca. 1.2‰ trophic enrichment, in agreement with the
mean δ15N enrichment (1.0 to 1.5 ‰) observed in simi-
lar ammonotelic marine crustaceans (McCutchan et al.
2003, Vanderklift & Ponsard 2003).
Stable isotope analysis has been widely used for
tracing the flow of carbon and nitrogen through food-
webs (Fry 2006). In light of its utility and common use
in ecology, it is surprising that so few studies have used
this tool to explore the functional roles of amphipods in
nature. Gut contents of amphipods are often highly
degraded and difficult to evaluate, and although feed-
ing assays provide excellent information on what
organisms prefer to eat in a laboratory, they are limited
by the less realistic settings and reduced variety of
food items offered (Duffy & Hay 1991). By using stable
isotopes, we were able to determine the relative
importance of algal versus eelgrass production to feed-
ing in amphipods, and their trophic position, in nature.
Furthermore, these signatures provide time-integrated
diet histories (e.g. weeks to months) rather than instant
snapshots in time (Kaufman et al. 2008). Though iso-
topic turnover can be influenced by temperature and
several other factors (McIntyre & Flecker 2006), stable
isotopes have been shown to be fairly conserved
throughout adult invertebrate life cycles (Fry & Arnold
1982).
Our conclusions regarding the relative importance of
eelgrass- versus algae-derived carbon and trophic
position among amphipod taxa are likely robust and
informative. We have demonstrated that stable iso-
topes can be used to assess the function of amphipods
with respect to the dominant trophic pathways used
while in their natural habitat. Such information is criti-
cal to our understanding of trophic dynamics in eel-
grass ecosystems, for example, of how changes in top-
down and bottom-up forcing are transmitted across
trophic levels. In addition, by scaling studies such as
ours to include a more comprehensive food web, ecol-
ogists can assess the relative importance of eelgrass
and algal production in eelgrass ecosystems and how
this importance may vary in space or time, or as a con-
sequence of environmental change.
Acknowledgements. This research was supported by a grant
from the Unified Port of San Diego, and we thank E. Maher
and D. Merck. We also thank L. Thurn at the San Diego State
University Ecology Analytical Lab for assistance with stable
isotope analysis and R. Velarde and E. Moore at the San
Diego City Metropolitan Waste Water District for assistance
with identification of voucher specimens. A. Bohonak and
P. Canning provided constructive comments on the manu-
script, along with the anonymous reviewers whose comments
improved the manuscript. This is Contribution No. 6 of the
Coastal and Marine Institute Laboratory, San Diego State
University.
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Editorial responsibility: Joseph Pawlik,
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Submitted: December 28, 2009; Accepted: October 13, 2010
Proofs received from author(s): November 30, 2010
... Also within grazer assemblages of angiosperm habitats there are isotopic divergences, e.g. among amphipod families (Farlin et al. 2010), in line with the effects of grazer richness, composition and interactions on ecological functions revealed through diversity manipulations (Duffy & Harvilicz 2001;Duffy et al. 2003). Our analysis merits some caveats. ...
... Secondly, our assessment assumes similar trophic enrichment factors for the different mesograzers. Trophic enrichment factors are critical for the interpretation of stable isotope data and their potential further use in mixing models, but in spite of the known variability in trophic shifts and tissue turnover times among taxa and different species, enrichment factors often remain experimentally unverified for specific study organisms (as in the current study) (McCutchan et al. 2003;Farlin et al. 2010;Mancinelli 2012). ...
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... In general, amphipods feed on diatoms attached to surfaces and are known to be fragment feeders (Hosomi et al. 2006). It is thought that upright diatoms are consumed first in comparison with prostrate types; however, as little is known about the feeding habits of these amphipods (Farlin et al. 2010), we examined the stomach contents of amphipods under a microscope and observed only C. moniligera fragments (Fig. 6). This suggests that amphipods might have a feeding preference, which influences the population of Type F diatoms (C. ...
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We present a descriptive account of the dynamics of epiphytic diatoms, epifauna, and the leaf surface area of Zostera marina in a shallow water ecosystem. We hypothesized that the growth stage of the host macrophyte (i.e., leaf surface area) influenced the presence of epiflora and epifauna, as well as that the leaf surface area and epifaunal population density affected the cell density and species composition of epiphytic diatoms. To evaluate this hypothesis, we quantified the leaf surface area of a host macrophyte (Zostera marina), the presence of epifauna, and the community of epiphytic diatoms that could be observed on the leaves of Z. marina during the period from May 2017 to December 2018. We conducted a descriptive analysis of the time-series observations of leaf surface area, epiphytic diatom density, and epifauna population density. Epiphytic diatom density was low and epifauna density was high during the growing season of Z. marina. Epiphytic diatom density was high and epifauna density was low during the maturation and senescence periods of Z. marina. Our analysis shows that epifauna densities lagged epiflora densities by at least four months, and that epiflora densities lagged leaf area by four months. Therefore, we hypothesized that herbivorous gastropods and amphipods could alter species composition via their preference of food items (active choice) or by ingesting more of the species that were structurally more available (passive preference).
... However, echinoderms A. depressus and P. bidentata displayed more enriched δ 13 C than H. ovalis, which may be because both echinoderms fed on seagrass detritus instead of fresh seagrass. Seagrass detritus is usually more enriched in δ 13 C than fresh tissue (Farlin et al., 2010;Marco-Méndez et al., 2012), though there are some exceptions (Fellerhoff et al., 2003;Lebreton et al., 2011). ...
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The current paradigm emphasizes the trophic role of epiphytic algae in seagrass-based food webs. However, a growing body of literature demonstrates that grazers would directly cause considerable damage to seagrass rather than targeting epiphytes, perhaps depending on seagrass traits. Here, we analyzed δ¹³C and δ¹⁵N signatures of macrozoobenthos, nekton and their potential organic carbon sources in Halophila ovalis seagrass bed and adjacent waters on the Hepu coast (Beihai, China) to test the hypothesis that Halophila with high nutritive values and fragile leaf-fracture traits may be a key carbon source. The δ¹³C values of most consumers either fell between H. ovalis (−14.7 ± 0.7‰) and benthic microalgae (microphytobenthos and Halophila’s epiphytes, −19.9 to −19.3‰), or approached the δ¹³C of H. ovalis, suggesting that H. ovalis and microalgae is basal carbon sources in Halophila-based food web. Further quantification based on a 4-end-member MixSIAR model showed that H. ovalis is the most important basal carbon source, supporting 4 out of 6 trophic groups of macrozoobenthos, and 4 out of 7 nektonic trophic groups (a total of 22 species, accounting for 84.6% in nekton). The mean contribution was 37.2–75.3% for macrozoobenthos and 51.1–64.4% for nekton, respectively. Most macrozoobenthos directly or indirectly assimilated H. ovalis or its detritus and were then mainly utilized by nekton except for bivalves which largely fed on suspended microphytobenthos and particulate organic matter (POM), and porifera filtered POM. Our results re-examined the trophic function of seagrass in seagrass-based food web and emphasize the importance of protecting Halophila resources.
... Future studies using selective removal or molecular marker analyses could help to confirm this hypothesis by identifying the dietary preferences of the most abundant invertebrate taxa. Stable isotope ratios of carbon (δ 13 C), nitrogen (δ 15 N) and sulphur (δ 34 S) from animal tissue could be compared with those of likely food items (e.g., seagrass leaves, epiphytes, macroalgae, seston, microphyobenthos) using mixing models to determine the relative contributions of each source to their diet [62,63]. Combining this with analyses of the fatty acid composition of key consumers and looking for biomarkers of major food sources increases the predictive power for identifying their dietary components [64,65]. ...
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Consumer communities play an important role in maintaining ecosystem structure and function. In seagrass systems, algal regulation by mesograzers provides a critical maintenance function which promotes seagrass productivity. Consumer communities also represent a key link in trophic energy transfer and buffer negative effects to seagrasses associated with eutrophication. Such interactions are well documented in the literature regarding temperate systems, however, it is not clear if the same relationships exist in tropical systems. This study aimed to identify if the invertebrate communities within a tropical, multispecies seagrass meadow moderated epiphyte abundance under natural conditions by comparing algal abundance across two sites at Green Island, Australia. At each site, paired plots were established where invertebrate assemblages were perturbed via insecticide manipulation and compared to unmanipulated plots. An 89% increase in epiphyte abundance was seen after six weeks of experimental invertebrate reductions within the system. Using generalised linear mixed-effect models and path analysis, we found that the abundance of invertebrates was negatively correlated with epiphyte load on seagrass leaves. Habitat species richness was seen to be positively correlated with invertebrate abundance. These findings mirrored those of temperate systems, suggesting this mechanism operates similarly across latitudinal gradients.
... In addition to variation in abundance, changes in the structure of herbivore communities can also greatly influence their ecological function (Duffy et al. 2003, Farlin et al. 2010, Brandt et al. 2012. As a re sult, herbivorous fishes on coral reefs are often grouped into discrete functional groups (Sandin et al. 2008, Williams et al. 2011) and intra-guild diversity has been examined in observational (Cheal et al. 2010, Edwards et al. 2014) and manipulative (Burkepile & Hay 2008 studies. ...
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Herbivores influence the structure and function of ecosystems, especially in the marine environment where ecosystems have rapidly transformed due to the presence or absence of a single important grazer or grazing community. Intraguild variation in the ecological functions of herbivores, however, likely determines their ultimate effects on benthic dynamics. For example, echinoids (sea urchins) can facilitate the growth of stony corals by consuming fleshy algal competitors, yet our understanding of taxonomic variation in their grazing behaviors remains limited. Here, we examined the trophic functions of five herbivorous echinoids on a coral reef in Maui, Hawaii. We conducted field-based assays to compare grazing rates and consumption profiles using several key algal functional groups and contrasted the results with reported differences in echinoid metabolism. Grazing rates varied among species by up to 10-fold, with taxonomic differences explaining 77-85% of the variation among individual urchins and metabolic rate explaining 81-98% of the taxonomic variation in mean biomass and energy ingestion rates. Though all species consumed several algae, they also exhibited distinct grazing behaviors. Species with lower metabolic rates exhibited the largest intraspecific variation in diets and no clear algal preferences. In contrast, species with higher metabolic rates consistently consumed or avoided specific macroalgae, indicating a positive relationship between metabolic rate and diet specificity. This phylogenetic variation in grazing and metabolism aligns with classic metabolic and foraging theory and suggests that species identity, community structure, and complementarity are likely key to understanding the functional roles of herbivorous echinoid communities on coral reefs.
... Aquatic organisms such as amphipods and many isopods are particularly unusual records from bird nests, as nests of most other bird species are too dry to contain aquatic taxa. They are unlikely to be preferentially associated with nests and are probably consumers of vegetation or detritus in general (Farlin et al. 2010). Comparison of these results with invertebrates extracted from non-nest accumulations of saltmarsh vegetation could reveal the extent to which invertebrates selectively use bird nests and for what purposes. ...
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The detrimental effects of nest ectoparasites on breeding birds have been well documented, but interactions between birds' parasites and their environment are less well understood. The Saltmarsh Sparrow, Ammodramus caudacutus is a ground-nesting bird endemic to tidal wetlands in the eastern USA, where the majority of nests are lost to tidal flooding. This study examined evidence that Saltmarsh Sparrows face a trade-off between flood-risk and ectoparasite exposure in nest-site selection and nest initiation. We monitored nesting attempts during the breeding season, and collected 23 nests from which we extracted, described and analyzed the invertebrate communities. Many invertebrate taxa were present in nests, especially Acari, Amphipoda and Isopoda. Flooding-failure was by far the best predictor of nest parasite load (specifically Acari), superior to the investigated characteristics of habitat, nest construction, phenology and research methods. Nests that failed because of flooding had 15% fewer ectoparasites per gram of material. Nests made of smooth cordgrass, Spartina alterniflora had parasite loads 16% lower than those made of other materials, but this variable was confounded with flooding-failure. These results suggest that selecting flood-prone sites has benefits, by reducing exposure to ectoparasites, in addition to the often severe costs of flooding. This study improves understanding of bird nest-parasite interactions in a habitat in which they have been little studied.
... Many species have shown high dietary plasticity (Saunders 1966;Caine 1977Caine , 1980, and detritivorous species can opportunistically prey on small crustaceans (Guerra-García and Tierno de Figueroa 2009). Many other amphipod taxa (e.g., many gammarideans) are also primarily detritivores, but feeding strategies vary by species (Cruz-Rivera and Hay 2000;Farlin et al. 2010). Herbivorous taxa (e.g., Ampithoidae) are important grazers in seagrass and macroalgae-based systems (Duffy and Hay 2000;Pérez-Matus and Shima 2010). ...
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Amphipods are abundant in marine ecosystems worldwide and are important as prey and as consumers of macrophytes and detritus in food webs. Due to the spatially complex and dynamic nature of giant kelp (Macrocystis pyrifera) forests, assessment of the abundances of giant kelp and amphipods through time and space should provide insight into their potential interactions within the system. In an extensive field study within the surface canopy of giant kelp, the abundance of amphipods was quantified on artificial substrates at an array of 18 sites within kelp forests along Point Loma, California, USA, from July to October 2009 and 2010. Biomass of giant kelp canopy was estimated using remotely sensed imagery, and the spatial synchrony (autocorrelation through time) of kelp canopy was compared with synchrony of caprellid and non-caprellid amphipods. Caprellids exhibited high spatial synchrony that did not decrease with distance, while non-caprellids were synchronous on local scales, indicating high spatial heterogeneity in abundance through time. Gammarids showed a rapid exponential decrease in synchrony within the first 550 m that was consistent with synchrony of giant kelp. This suggests a local-scale biotic link between non-caprellids and giant kelp canopy, whereas caprellid synchrony is more likely to be influenced by regional-scale environmental variables. Caprellids and other amphipods are important prey resources for common kelp forest fishes, so these differences may in turn affect the spatial distributions of these predators. Moreover, excretion by amphipods may be an important source of nitrogen to giant kelp during periods of nitrogen limitation.
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Changes in the relative importance of the 27 component functional groups (FGs) of seagrass-associated macrobenthos were assessed up the long axis of an estuarine system. Although previously observed division of the estuary into two sections with respect to species diversity was confirmed, this did not correspond to any functional compartmentalisation. Functionally, division was into the terminal extremes and the large intervening marine/lagoonal/lower-estuarine zone, within which no linear segregation of sites occurred. 40% of individual FGs in the latter showed no variation at all, and variation in the remainder was only axially related in two cases, one positive and one negative. Overall structure of the dominant FGs at each locality remained uniform, although rank orders of proportional importance varied widely. Only one major marine/lagoonal FG failed to penetrate the upper estuary at the time of sampling. Estuarine components may change spatially, sometimes dramatically, but overall functional pattern shows considerably less change than the species numbers usually used in characterisation.
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Secondary production of the amphipod Synchelidium lenorostralum was examined on a temperate sandy shore, southern Korea, on the basis of monthly samples from July 1996 to June 1997. Secondary production was estimated by the size-frequency method. Biomass structure showed two peaks in fall and spring, with maximum biomass in April. Biomass in the spring breeding period was higher than that in the fall. The annual secondary production of S. lenorostralum was 1.09 g DW m−2 yr−1 with an annual P/B ratio of 5.68. Secondary production of S. lenorostralum fell within the range observed for other amphipods from intertidal sandy shores, whereas the P/B ratio was higher than that recorded previously. The combination of high abundance and a high P/B ratio suggests an important role for S. lenorostralum in the sandy shore ecosystem as a trophic link from primary producers to higher consumers.
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Secondary production of the amphipod Synchelidium lenorostralum was examined on a temperate sandy shore, southern Korea, on the basis of monthly samples from July 1996 to June 1997. Secondary production was estimated by the size-frequency method. Biomass structure showed two peaks in fall and spring, with maximum biomass in April. Biomass in the spring breeding period was higher than that in the fall. The annual secondary production of S. lenorostralum was 1.09 g DW m-2 yr-1 with an annual P/B ratio of 5.68. Secondary production of S. lenorostralum fell within the range observed for other amphipods from intertidal sandy shores, whereas the P/B ratio was higher than that recorded previously. The combination of high abundance and a high P/B ratio suggests an important role for S. lenorostralum in the sandy shore ecosystem as a trophic link from primary producers to higher consumers.
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Stable isotope analyses are often used to quantify the contribution of multiple sources to a mixture, such as proportions of food sources in an animal's diet, or C3 and C4 plant inputs to soil organic carbon. Linear mixing models can be used to partition two sources with a single isotopic signature (e.g., δ(13)C) or three sources with a second isotopic signature (e.g., δ(15)N). Although variability of source and mixture signatures is often reported, confidence interval calculations for source proportions typically use only the mixture variability. We provide examples showing that omission of source variability can lead to underestimation of the variability of source proportion estimates. For both two- and three-source mixing models, we present formulas for calculating variances, standard errors (SE), and confidence intervals for source proportion estimates that account for the observed variability in the isotopic signatures for the sources as well as the mixture. We then performed sensitivity analyses to assess the relative importance of: (1) the isotopic signature difference between the sources, (2) isotopic signature standard deviations (SD) in the source and mixture populations, (3) sample size, (4) analytical SD, and (5) the evenness of the source proportions, for determining the variability (SE) of source proportion estimates. The proportion SEs varied inversely with the signature difference between sources, so doubling the source difference from 2‰ to 4‰ reduced the SEs by half. Source and mixture signature SDs had a substantial linear effect on source proportion SEs. However, the population variability of the sources and the mixture are fixed and the sampling error component can be changed only by increasing sample size. Source proportion SEs varied inversely with the square root of sample size, so an increase from 1 to 4 samples per population cut the SE in half. Analytical SD had little effect over the range examined since it was generally substantially smaller than the population SDs. Proportion SEs were minimized when sources were evenly divided, but increased only slightly as the proportions varied. The variance formulas provided will enable quantification of the precision of source proportion estimates. Graphs are provided to allow rapid assessment of possible combinations of source differences and source and mixture population SDs that will allow source proportion estimates with desired precision. In addition, an Excel spreadsheet to perform the calculations for the source proportions and their variances, SEs, and 95% confidence intervals for the two-source and three-source mixing models can be accessed at http://www.epa.gov/wed/pages/models.htm.
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Small, grazing invertebrates often benefit seagrasses by cropping their epiphytic algal competitors. Yet predictive relations between grazer abundance and seagrass performance are elusive, in significant part because of poorly understood diversity in mesograzer feeding biology. We conducted experiments in eelgrass Zostera marina microcosms to explore how differences in feeding between 2 common grazing amphipod taxa affected accumulation and species composition of epiphytes on eelgrass, as well as amphipod population growth, competition and production, over a 4-week period in summer. Gammarus mucronatus and ampithoids (a mixture of Cymadusa compta and Ampithoe longimana) were stocked, singly and in combination, along with a grazer-free control treatment. Amphipod population growth rates indicated that the 2 taxa competed for a common limiting resource, presumably periphyton, which was essentially eliminated in all grazer treatments. Final abundances of both amphipod taxa were 53 to 68% lower in treatments where the other grazer was present than in single-species grazer treatments. A common carrying capacity was also indicated by the nearly identical final biomass of amphipods across treatments, despite 2-fold variation in initial amphipod densities. These results support the hypothesis that the 2 amphipod taxa are roughly equivalent in terms of resource requirements and production rates. Despite this equivalence, subtle differences in diet breadth between amphipod taxa translated into substantial differences in biomass and composition of the fouling assemblage among treatments. Whereas grazer-free eelgrass became heavily fouled with periphyton and tunicates, eelgrass exposed to G. mucronatus alone was overgrown by the red alga Polysiphonia harveyi, which reached a biomass equal to the total fouling mass of grazer-free controls. P. harveyi was nearly absent from all other treatments. In contrast, eelgrass with ampithoids was virtually devoid of all fouling material. Thus, similar mesograzer species can have markedly different impacts on fouling assemblages, and these occur despite strong similarity in grazer energetics and primary food sources. Our results may help to reconcile evidence of diet overlap and diffuse competition among mesograzer species with the different feeding preferences and community impacts shown for several mesograzers in experimental studies.
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Segregation of resources is supposed to be a mechanism for coexistence of species and/or life stages when resources are limiting and competition between species occurs. In seagrass beds, fish species richness is lower than on coral reefs, but food abundance is in general higher. In this case, food segregation may not occur. Here, the null hypothesis is tested that species show no segregation in feeding with respect to time, space and diet. The structure of the food web in a tropical seagrass bed revealed that the seagrass fish community consisted of species feeding at 3 trophic levels: (1) herbivores, (2) omnivores, zoobenthivores and zooplanktivores, and (3) piscivores. The data suggest that herbivores partitioned food by specialising on seagrass epiphytes, seagrass leaves or macroalgae from the seagrass bed, with 1 species presumably feeding in adjacent mangroves. Fishes at the second trophic level showed temporal segregation in feeding habits between fish families, while species within families showed segregation in food type and source. At the third trophic level, 1 piscivorous species was found. The majority of fish species showed a very narrow diet breadth with a significant segregation in resource-use. The null hypothesis was rejected since feeding segregation was not random for time, space and diet, viz. feeding time and diet (33.3%), diet only (25.5%), time, habitat and diet (15.2%), habitat and diet (13.4%), time only (3.5%) and habitat only (2.6%). Segregation in resource use was present along 1 to 3 resource axes simultaneously, which could support coexistence of species that favour comparable food types if food were limiting.
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Multiple stable isotope analyses were employed to examine food web dynamics in a northern Gulf of Mexico seagrass system in which epiphytic algae were the single most important primary productivity component, being responsible for 46 and 60% of total system and benthic primary production, respectively. The seagrass Halodule wrightii Ascherson contributed only 13% to total system primary production on an annual basis. Stable isotope ratios of carbon (delta C-13), nitrogen (Omega N-15), and sulfur (delta S-34) Were measured for producer and consumer samples collected from May 1989 through November 1992. Epiphytes and leaves of H, wrightii had distinct delta C-13 values (-17.5 vs -12 parts per thousand, respectively) as well as distinct delta S-34 values parts per thousand (+18 vs +11 parts per thousand, respectively). delta C-13 values for the sand microflora, occasional macroalgae, and phytoplankton were -16, -17, and -22 parts per thousand, respectively; delta N-15 values were lowest for epiphytes and H. wrightii (+6 parts per thousand) and highest for phytoplankton (+100 parts per thousand). Virtually all consumers had delta C-13 values that fell within a narrow range of -20 to -15 parts per thousand, which included all delta C-13 values of epiphytes and the sand microflora but none of those for either H, wrightii or phytoplankton. Values for delta N-15 for consumers fell within a range of +8 to +16 parts per thousand, spanning herbivorous species with diets of microalgae to carnivorous species feeding at secondary to tertiary levels in the local food webs. Consumer values for delta S-34 ranged from +4 to +20 parts per thousand (mean = 14.2 parts per thousand), and indicate a stronger influence of seawater-derived sulfate than sediment-associated sulfides. The stable isotope data, in combination with measured high biomass and primary production rates of the epiphytic algae, strongly suggest that these algae are the primary source of organic matter for higher trophic levels in seagrass beds of Mississippi Sound. The contribution of H. wrightii to the food web appears to be minimal. The overall picture that has emerged based on the present and previous stable isotope studies is one of the major trophic importance of benthic microalgae (i.e, epiphytic and sediment-associated) in seagrass beds.
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Using natural-abundance 13C/12C ratios as tracers, carbon turnover rates were determined for postlarval brown shrimp, Penaeus aztecus, in five laboratory growth experiments. Although tissue turnover in adult animals generally occurs during maintenance metabolism and is a function of time, turnover for young postlarval shrimp was accelerated during growth, and was primarily a function of weight gained rather than time. Metabolic loss of tissue carbon during growth was usually approximated by the function, Fraction lost=1-(initial weight/final weight). For shrimp that switch diets in the sea, model calculations show that this high turnover rate coupled with a four-fold weight increase suffices for shrimp to achieve a close isotopic resemblance of 1‰ or less (d13C units) to the new diet.