Kelp as a trophic resource for marine suspension feeders: a review of isotope-based evidence

Kelp forests are enormously productive, and they and adjacent habitats support large populations of suspension feeders. What do these suspension feeders eat? Intuitively, we might expect that kelp primary production is a key form of trophic support for these animals. Indeed, a large and growing number of studies using carbon stable isotope data, typically collected over short time periods, have asserted that detritus from kelps is an important, and in some cases the main, food source for coastal benthic suspension feeders. This view has been incorporated into several textbooks and review papers covering kelp forest ecosystems, and loss of trophic support for benthic suspension feeders is now often invoked as an ecosystem consequence of top-down or other impacts on kelp forests. More direct evidence, however, suggests that these animals mainly eat phytoplankton and, in some cases, bacteria or zooplankton. Because isotope values of pure coastal phytoplankton, uncontaminated with detritus, are difficult to obtain, present studies have largely relied on single measurements from offshore environments or from the literature, which typically reflects offshore values. We review the evidence showing that phytoplankton isotope values can, and are expected to, vary widely in coastal waters and that inshore phytoplankton may often be enriched in ¹³C compared to offshore phytoplankton. This unaccounted-for variation may have systematically biased the results of such trophic studies toward finding large contributions of kelp detritus to suspension-feeder diets. We review some key stable isotope studies and put forth evidence for alternative explanations of the isotope patterns presented. Finally, we make recommendations for future isotope studies and describe several approaches for progress in this area. New techniques, particularly flow cytometry and compound-specific stable isotope analysis, provide ways to shed light on this interesting and important ecological issue.     

Higher trophic level prey does not represent a higher quality diet in a threatened seabird: implications for relating population dynamics to diet shifts inferred from stable isotopes

Diet quality is a key determinant of population dynamics. If a higher trophic level, more fish-based diet is of higher quality for marine predators, then individuals with a higher trophic level diet should have a greater body mass than those feeding at a lower trophic level. We examined this hypothesis using stable isotope analysis to infer dietary trophic level and foraging habitat over three years in eastern rockhopper penguins Eudyptes chrysocome filholi on sub-Antarctic Campbell Island, New Zealand. Rockhopper penguins are ‘Vulnerable’ to extinction because of widespread and dramatic population declines, perhaps related to nutritional stress caused by a climate-induced shift to a lower trophic level, lower quality diet. We related the stable nitrogen (δ¹⁵N) and carbon (δ¹³C) isotope values of blood from 70 chicks, 55 adult females, and 55 adult males to their body masses in the 2010, 2011, and 2012 breeding seasons and examined year, stage, age, and sex differences. Opposite to predictions, heavier males consumed a lower trophic level diet during incubation in 2011, and average chick mass was heavier in 2011 when chicks were fed a more zooplankton-based, pelagic/offshore diet than in 2012. Contrary to the suggested importance of a fish-based diet, our results support the alternative hypothesis that rockhopper penguin populations are likely to be most successful when abundant zooplankton prey are available. We caution that historic shifts to lower trophic level prey should not be assumed to reflect nutritional stress and a cause of population declines.     

δ 13C and δ 15N variations in organic matter pools, Mytilus spp. and Macoma balthica along the European Atlantic coast

Stable carbon (δ ¹³C) and nitrogen (δ ¹⁵N) isotope (SI) values of sedimentary organic matter (SOM), seston and two dominant bivalves, Mytilus spp. and Macoma balthica, were studied at 18 stations along the European coast in spring and autumn 2004. Three main regions, the Baltic Sea (BS), the North Sea and English Channel (NS), and the Bay of Biscay (BB), were tested for possible geographic (latitudinal) differences in the SI values. In spring, only BS showed lower δ ¹³C values of seston and Mytilus spp., and higher δ ¹⁵N values of SOM, than NS and BB. No significant differences between the 3 regions were found in autumn. Irrespective of season and regions, Mytilus spp. was more ¹³C-depleted than M. balthica. δ ¹³C values of M. balthica, but not those of Mytilus spp., were significantly correlated with SOM. These results are consistent with differences in feeding behavior of Mytilus spp. and M. balthica, as the two species are known as obligatory-suspension and facultative-deposit feeders, respectively. In contrast, no differences in the δ ¹⁵N values of Mytilus spp. and M. balthica were found at individual stations, indicating the same trophic level of the two bivalves within the food webs. At some stations, irrespective of geographic location, both bivalves showed δ ¹⁵N values up to 18–20 ‰. These were two trophic levels higher than those found at the other stations, indicating local and/or episodic eutrophic conditions, probably due to waste water discharge, and the effectiveness of both Mytilus spp. and M. balthica as bio-indicators of anthropogenic eutrophication. Overall, our results suggest that pathways of energy flow from OM pools to dominant bivalves is more related to local environmental conditions than to geographic regions across the European coastline. This has implications for food web studies along the Atlantic coast because most of the values are consistent over a large area and show no significant differences. Therefore, the present study can be used twofold for the determination of trophic baselines and for the correction of the trophic position of consumers higher up in the food web in the case of differences in waste water discharge.     

Trophic relationships of hydrothermal vent and non-vent communities in the upper sublittoral and upper bathyal zones off Kueishan Island,Taiwan: a combined morphological,gut content analysis and stable isotope approach

This study used morphological, gut content analysis and carbon- and nitrogen-stable isotope analysis to investigate the trophic structure of upper sublittoral (15–30 m deep) and upper bathyal (200–300 m deep) hydrothermal vents and the adjacent non-vent upper bathyal environment off Kueishan Island. The sublittoral vents host no chemosynthetic fauna, but green and red algae, epibiotic biofilm on crustacean surfaces, and zooplankton form the base of the trophic system. Suspension-feeding sea anemones and the generalist omnivorous vent crab Xenograpsus testudinatus occupy higher trophic levels. The upper bathyal hydrothermal vent is a chemoautotrophic-based system. The vent mussel Bathymodiolus taiwanensis forms a chemosynthetic component of this trophic system. Bacterial biofilm, surface plankton, and algae form the other dietary fractions of the upper bathyal fauna. The vent hermit crab Paragiopagurus ventilatus and the vent crab X. testudinatus are generalist omnivores. The vent-endemic tonguefish Symphurus multimaculatus occupies the top level of the trophic system. The adjacent non-vent upper bathyal region contains decapod crustaceans, which function as either predators or scavengers. The assemblages of X. testudinatus from sublittoral and upper bathyal vents exhibited distinct stable isotope values, suggesting that they feed on different food sources. The upper bathyal Xenograpsus assemblages displayed large variations in their stable isotope values and exhibited an ontogenetic shift in their δ¹³C and δ¹⁵N stable isotope signatures. Some individuals of Xenograpsus exhibited δ¹⁵N values close to those of non-vent species, suggesting that the highly mobile Xenograpsus may transfer energy between the upper bathyal hydrothermal vents and the adjacent non-vent upper bathyal environment.     

Important organic matter sources and trophic pathways for the nutrition of Hilsa kelee (Cuvier, 1829) and Valamugil buchanani (Bleeker, 1853) in Pangani macro-tidal estuary,Tanzania

The study investigated the spatial variation in the main sources of organic matter (OM) and trophic pathways for zooplanktivorous Hilsa kelee and phytodetritivorous Valamugil buchanani in fresh-water-influenced zone versus sea-water-dominated zone of Pangani estuary. The findings indicated significant inter-specific variations in δ¹³C and δ¹⁵N values (ANOVA, F?≥?84.3, p?F?≥?9.4, p?=?0.001) in both estuarine zones. Results also showed significant zonal-intraspecific variations in stable isotopes (δ¹³C and δ¹⁵N), FA profile and marginal differences in diet for the V. buchanani while no considerable differences were observed for H. kelee from two estuarine zones. The isotope mixing models and FA biomarkers revealed that the most important carbon sources to the nutrition of H. kelee were derived from microphytobenthos, macro-algae and sea grasses transferred through phytoplankton and detrital trophic pathways. In contrast, C₃ terrestrial plants and microphytobenthos were the main carbon source to the diet of V. buchanani; and were transferred via the benthic and detrital trophic pathways. Therefore, both terrestrial and in-situ OM sources were the main trophic resources base fuelling the planktonic and benthic food webs in Pangani estuary.     

The foraging ecology of Arctic cod (Boreogadus saida) during open water (July–August) in Allen Bay, Arctic Canada

Arctic cod (Boreogadus saida) is a schooling fish providing a critical link between lower and upper trophic levels in the Arctic. This study examined foraging of Arctic cod collected from Allen Bay, Cornwallis Island, Canada (~75 N 95 W), during summer 2010 using temporal indicators of diet including stomach content, and carbon (δ¹³C) and nitrogen (δ¹⁵N) stable isotopes of liver and muscle. Foraging at the time of capture reflected sympagic and epi-benthic habitats indicated by the prevalence of cyclopoid and harpacticoid copepods in stomachs, whereas stable isotope data, which provide an estimate of feeding over a longer period, indicated pelagic prey as important. Prey selection of juveniles differed from adults based on stable isotopes, while large adults showed the most separation based on stomach contents, suggesting size-related diet shifts. Compared to studies near Resolute in the 1970s, 1980s, and 1990s, growth and pre-spawning gonadal conditions of Arctic cod have not changed.     

Stable isotopes identify an ontogenetic niche expansion in Antarctic krill (Euphausia superba) from the South Shetland Islands, Antarctica

Antarctic krill (Euphausia superba) occupy a key position in the Southern Ocean linking primary production to secondary consumers. While krill is a dominant grazer of phytoplankton, it also consumes heterotrophic prey and the relative importance of these two resources may differ with ontogeny. We used stable isotope analyses to evaluate body size-dependent trophic and habitat shifts in krill during the austral summer around the South Shetland Islands, Antarctica. We found evidence for an asymmetric, ontogenetic niche expansion with adults of both sexes having higher and more variable δ¹⁵N values but consistent δ¹³C values in comparison with juveniles. This result suggests that while phytoplankton likely remains an important life-long resource, krill in our study area expand their dietary niche to include higher trophic food sources as body size increases. The broader dietary niches observed in adults may help buffer them from recent climate-driven shifts in phytoplankton communities that negatively affect larval or juvenile krill that rely predominately on autotrophic resources.     

Biological and environmental influences on the trophic ecology of leatherback turtles in the northwest Atlantic Ocean

Understanding the causes and consequences of variability in trophic status is important for interpreting population dynamics and for identifying important habitats for protected species like marine turtles. In the northwest Atlantic Ocean, many leatherback turtles (Dermochelys coriacea) from distinct breeding stocks throughout the Wider Caribbean region migrate to Canadian waters seasonally to feed, but their trophic status during the migratory and breeding cycle and its implications have not yet been described. In this study, we used stable carbon and nitrogen isotope analyses of bulk skin to characterize the trophic status of leatherbacks in Atlantic Canadian waters by identifying trophic patterns among turtles and the factors influencing those patterns. δ¹⁵N values of adult males and females were significantly higher than those of turtles of unknown gender (i.e., presumed to be subadults), and δ¹⁵N increased significantly with body size. We found no significant differences among average stable isotope values of turtles according to breeding stock origin. Significant inter-annual variation in δ¹⁵N among cohorts probably reflects broad-scale oceanographic variability that drives fluctuations in stable isotope values of nutrient sources transferred through several trophic positions to leatherbacks, variation in baseline isotope values among different overwintering habitats used by leatherbacks, or a combination of both. Our results demonstrate that understanding effects of demographic and physiological factors, as well as oceanographic conditions, on trophic status is key to explaining observed patterns in population dynamics and for identifying important habitats for widely distributed, long-lived species like leatherbacks.     

Evidence for benthic primary production support of an apex predator–dominated coral reef food web

Five hundred and ninety-nine primary producers and consumers in the Papahānaumokuākea Marine National Monument (PMNM) (22°N–30°N, 160°W–180°W) were sampled for carbon and nitrogen stable isotope composition to elucidate trophic relationships in a relatively unimpacted, apex predator–dominated coral reef ecosystem. A one-isotope (δ¹³C), two-source (phytoplankton and benthic primary production) mixing model provided evidence for an average minimum benthic primary production contribution of 65 % to consumer production. Primary producer δ¹⁵N values ranged from ?1.6 to 8.0 ‰ with an average (2.1 ‰) consistent with a prevalence of N₂ fixation. Consumer group δ¹⁵N means ranged from 6.6 ‰ (herbivore) to 12.1 ‰ (Galeocerdo cuvier), and differences between consumer group δ¹⁵N values suggest an average trophic enrichment factor of 1.8 ‰ Δ¹⁵N. Based on relative δ¹⁵N values, the larger G. cuvier may feed at a trophic position above other apex predators. The results provide baseline data for investigating the trophic ecology of healthy coral reef ecosystems.     

Determination of δ13C and δ15N and trophic fractionation in jellyfish: implications for food web ecology

Application of stable isotope analysis (SIA) in jellyfish allows definition of trophic patterns not detectable using gut content analysis alone, but analytical protocols require standardization to avoid bias in interpreting isotopic data. We determined δ¹³C and δ¹⁵N in Aurelia sp. from the northern Gulf of Mexico (30°00′N, 89°00′W–30°24′N, 88°00′W) to define differences in stable isotope composition between body parts and whole body, the effect of lipid extraction on δ¹³C in tissues, and fractionation values from medusa to prey. The isotopic composition of bell and whole Aurelia sp. was not different. The increase in δ¹³C values after lipid removal suggested a correction is needed. To aid future analyses, we derived a correction equation from empirical data for jellyfish samples. Laboratory feeding experiments indicated medusae increased +4 ‰ in δ¹³C and +0.1 ‰ in δ¹⁵N compared to their diet. These results suggest protocols commonly applied for other species may be inaccurate to define Aurelia sp. trophic ecology. Because Aurelia spp. are commonly found in marine ecosystems, accurately defining their trophic role by use of SIA has implications for understanding marine food webs worldwide.     

Shift in foraging grounds and diet broadening during ontogeny in southern elephant seals from Kerguelen Islands

Highly dimorphic species like southern elephant seals (Mirounga leonina, SES hereafter) frequently exhibit resource partitioning according to sex and/or age classes. We measured carbon and nitrogen stable isotopes (δ¹³C and δ¹⁵N) of 404 blood samples (136 males and 268 females from Kerguelen Islands, 49°21′S, 70°18′E) from 2004 to 2011. Assuming that the distribution of carbon isotopes (δ¹³C value) reflects the two main foraging grounds (Polar Frontal and Antarctic Zones), we quantified the proportion of SES foraging within each zone in relation with size, a proxy for their age. We found a clear shift from Polar Frontal to Antarctic waters as male SES aged, but no relation as far as females is concerned. We also observed a widening range of nitrogen isotopic (δ¹⁵N) values, suggesting that both males and females expanded their diet spectra with age. Whereas males increased their trophic level, females remained constant on average, with some adult females feeding both at lower and at higher trophic levels than juveniles.     

Microscale variations of food web functioning within a rocky shore invertebrate community

The assessment of relevant spatial scales at which ecological processes occur is of special importance for a thorough understanding of ecosystem functioning. In coastal ecosystems, the variability of trophic interactions has been studied at different spatial scales, but never at scales from centimetres to metres. In the present study, we investigated the link between habitat structure and small-scale variability of food web functioning on intertidal boulder field ecosystems. Two microhabitats, boulder-top and boulder-bottom, were considered, and the trophic ecology of invertebrate consumers was studied using stable isotope tracers. We found for two of the main suspension feeders of northern Atlantic rocky shores (the sponges Halichondria panicea and Hymeniacidon sanguinea) consistent ¹⁵N enrichment for individuals sampled under boulders, suggesting that these consumers relied on different trophic resource according to the microhabitat inhabited, at a centimetre scale. The high δ¹⁵N signatures found underneath boulders suggested higher use of highly decomposed organic matter in this microhabitat. The isotopic difference between the two microhabitats decreased in higher trophic level consumers, which likely foraged at a spatial scale including both microhabitats. Finally, our results reveal that in highly heterogeneous habitats such as boulder fields, trophic interactions are likely to vary strongly in space, which should be considered in future researches. The link between habitat physical structure and food web variability might also contribute to the high biological diversity characterizing heterogeneous ecosystems.     

Short- and long-term importance of small sharks in the diet of the rare deep-sea shark Dalatias licha

Knowing the trophic ecology of marine predators is essential to develop an understanding of their ecological role in ecosystems. Research conducted on deep-sea and threatened shark species is limited. Here, by combining analyses of individual stomach contents and stable isotope values, we examined the trophic ecology (dietary composition and trophic position) of the kitefin shark Dalatias licha, a deep-sea shark considered as near threatened globally and as data deficient in the Mediterranean Sea. Results revealed the importance of small sharks in the diet of the kitefin shark at short- and long-term scales, although fin-fish, crustaceans and cephalopods were also found. Predation on sharks reveals the high trophic position of the kitefin shark within the food web of the western Mediterranean Sea. Stable isotope values from liver and muscle tissues confirmed our results from stomach content analysis and the high trophic position.     

Food web structure of a restored macroalgal bed in the eastern Korean peninsula determined by C and N stable isotope analyses

Loss of macroalgae habitats has been widespread on rocky marine coastlines of the eastern Korean peninsula, and efforts for restoration and creation of macroalgal beds have increasingly been made to mitigate these habitat losses. Deploying artificial reefs of concrete pyramids with kelps attached has been commonly used and applied in this study. As a part of an effort to evaluate structural and functional recovery of created and restored habitat, the macroalgal community and food web structure were studied about a year after the establishment of the artificial macroalgal bed, making comparisons with nearby natural counterparts and barren ground communities. Dominant species, total abundance, and community structure of macroalgal assemblage at the restored macroalgal bed recovered to the neighboring natural bed levels during the study period. The main primary producers (phytoplankton and macroalgae) were isotopically well separated. δ¹³C and δ¹⁵N values of consumers were very similar between restored and natural beds but varied greatly among functional feeding groups. The range of consumer δ¹³C was as wide as that of primary producers, indicating the trophic importance of both producers. There was a stepwise trophic enrichment in δ¹⁵N with increasing trophic level. A comparison of isotope signatures between primary producers and consumers showed that, while suspension feeders are highly dependent on pelagic sources, invertebrates of other feeding guilds and fishes mainly use macroalgae-derived organic matter as their ultimate nutritional sources in both macroalgal beds, emphasizing the high equivalency of trophic structure between both beds. Isotopic signatures of a few mollusks and sea urchins showed that they use different dietary items in macroalgal-barren grounds compared with macroalgal beds, probably reflecting their feeding plasticity according to the low macroalgal biomass. However, isotopic signatures of most of the consumers at the barren ground were consistent with those at the macroalgal beds, supporting the important trophic role of drifting algae. Our results revealed the recoveries of the macroalgal community and trophic structure at the restored habitat. Further studies on colonization of early settlers and the following succession progress are needed to better understand the process and recovery rate in the developing benthic community.     

Short- and long-term consistency in the foraging niche of wandering albatrosses

The wandering albatross (Diomedea exulans) is regarded as a generalist predator, but can it be consistent in its foraging niche at an individual level? This study tested short- and long-term consistency in the foraging niche in terms of habitat use, trophic level and, by inference, prey selection. Fieldwork was carried out at Bird Island, South Georgia, in May–October 2009, during the chick-rearing period. Blood (plasma and cells) and feathers for stable isotope analyses (δ¹³C and δ¹⁵N) were sampled from 35 adults on their return from a foraging trip during which they carried stomach temperature, activity and global positioning system loggers. Results suggest short-term consistency in foraging niche in relation to both oceanic water mass and trophic level, and long-term consistency in use of habitat. Consistent differences between individuals partly reflected sex-specific habitat preferences. The proportion of consistent individuals (i.e., with a narrow foraging niche) was estimated at c. 40?% for short-term habitat and trophic level (prey) preferences and 29?% for longer-term habitat preference, suggesting this is an important characteristic of this population and potentially of pelagic seabirds in general. Foraging consistency was not related to body condition or level of breeding experience; instead, it may reduce intraspecific competition.     

Ecological niche segregation among five toothed whale species off the NW Iberian Peninsula using ecological tracers as multi-approach

This study aims to assess niche segregation among the five main toothed whales that frequent the NW Iberian Peninsula waters: the common dolphin, the harbour porpoise, the bottlenose dolphin, the striped dolphin and the long-finned pilot whale. We used cadmium (Cd) and stable isotope ratios (δ¹³C and δ¹⁵N) as ecological tracers to assess degree of segregation in diet/trophic level and in foraging habitat, over various time-scales. δ¹³C values highlighted different habitats, while Cd concentrations highlighted feeding differences between oceanic and neritic species. Moreover, δ¹⁵N values suggest different trophic levels of prey targeted within oceanic and neritic species. Hence, results revealed long-term ecological segregation among five toothed whales that coexist in the NWIP and demonstrated the ability of ecological tracers to discriminate ecological niches among closely related species.     

Trophic specialisation of metazoan meiofauna at the Håkon Mosby Mud Volcano: fatty acid biomarker isotope evidence

We report the results of a detailed investigation on the trophoecology of two dominant meiofaunal species at the Håkon Mosby Mud Volcano (HMMV), a deep-sea cold methane-venting seep. Analyses of fatty acids (FAs) and their stable carbon isotopes were used to determine the importance of chemosynthetic nutritional pathways for the dominant copepod species (morphologically very similar to Tisbe wilsoni) inhabiting the volcano’s centre and the abundant nematode Halomonhystera disjuncta from the surrounding microbial mats. The strong dominance of bacterial biomarkers (16:1ω7c, 18:1ω7c and 16:1ω8c) coupled with their individual light carbon isotopes signatures (δ¹³C ranging from ?52 to ?81‰) and the lack of symbiotic relationships with prokaryotes (as revealed by molecular analyses and fluorescent in situ hybridisation) indicated that chemosynthetically derived carbon constitutes the main diet of both species. However, the copepod showed a stronger reliance on the utilisation of methanotrophic bacteria and contained polyunsaturated FAs of bacterial origin (20:5ω3 and 22:6ω3 with isotope signatures δ¹³C < ?80‰). Instead, the FA profiles of H. disjuncta suggested that sulphide-oxidising bacteria constituted the main diet of this nematode. Therefore, HMMV can be regarded as a persistent deep-sea cold seep, allowing a chemosynthesis-based trophic specialisation by the dominant meiofaunal species inhabiting its sediments. The present investigation, through the determination of the fatty acid profiles, provides the first evidence for trophic specialisation of meiofauna associated with sub-habitats within a cold seep.     

Trophic segregation between sexes in the Black Skimmer revealed through the analysis of stable isotopes

The degree of individual or gender variation when exploiting food resources is an important aspect in the study of foraging ecology within a population. Previous information on non-breeding skimmers obtained through conventional methodologies suggested sex-related differences in prey species. In this study, stable isotope techniques were used to investigate the intraspecific segregation in diet and foraging habits of the Black Skimmer (Rynchops niger intercedens) at Mar Chiquita Coastal Lagoon (37°40′S, 57°22′W), Argentina. These results were compared with contemporary data on the trophic composition obtained by conventional methodologies. Blood samples were taken from birds captured with mist-nets during their non-breeding season. The isotopic signatures of skimmers showed a diet mainly composed of marine prey with some degree of estuarine fish intake. When comparing diet between sexes, males showed enrichment in ¹⁵N compared to females, while no differences were observed in ¹³C. The use of mixing models revealed differences in the relative composition of prey in the diet of male and female skimmers. This study highlights stable isotope analysis as a valuable tool to test inter-individual differences and sexual segregation in trophic ecology of Black Skimmers as compared to conventional methodologies. The results show a trophic segregation in the Black Skimmer during the non-breeding season that can be explained by differences in prey species and larger prey sizes of male skimmers. Our findings have significant implications for conservation since any environmental change occurring at wintering areas might have profound effects on several avian life-history traits, and could be different for males and females due to trophic segregation.