Identifying trophic variation in a marine suspension feeder: DNA- and stable isotope-based dietary analysis in Mytilus spp.

Accurate field data on trophic interactions for suspension feeders are lacking, and new approaches to dietary analysis are necessary. Polymerase chain reaction-denaturing gradient gel electrophoresis (PCR-DGGE) was integrated with stable isotope analysis to examine dietary patterns in suspension-feeding Mytilus spp. from seven spatially discrete locations within a semi-enclosed marine bay (Strangford Lough, Northern Ireland) during June 2009. Results of the two methods were highly correlated, reflecting dietary variation in a similar manner. Variation in PCR-DGGE data was more strongly correlated with the principal environmental gradient (distance from the opening to the Irish Sea), while values of δ ¹³C and δ ¹⁵N became progressively enriched, suggesting a greater dependence on animal tissue and benthic microalgae. Diatoms and crustaceans were the most frequently observed phylotypes identified by sequencing, but specific DNA results provided little support for the trophic trends observed in the stable isotope data. This combined approach offers an increased level of trophic insight for suspension feeders and could be applied to other organisms.     

Contribution of mangrove detritus to juvenile prawn nutrition: a dual stable isotope study in a Malaysian mangrove forest

Dual stable C and N ratio analyses of primary producers and prawns have clarified the important role of mangrove detritus as the primary food source of juvenile prawns inhabiting the upper estuaries of the Matang mangrove swamp in Malaysia. The contribution of mangrove carbon to prawn tissues, as high as 84%, decreased in the offshore direction, as the contribution by phytoplankton became progressively more important. Prawns located 2 km outside the mangrove swamp still exhibited a dependency of 15–25% on mangrove carbon, but farther offshore (7–10 km) in shallow waters, the prawn's food was basically phytoplankton, with some contribution from benthic microalgae. Comparative stable C and N isotope ratios of tissue and gut contents indicate that prawns basically assimilated what they consumed. Received: 29 February 2000 / Accepted: 26 August 2000     

Invasive cordgrass modifies wetland trophic function

Vascular plants strongly control belowground environments in most ecosystems. Invasion by vascular plants in coastal wetlands, and by cordgrasses (Spartina spp.) in particular, are increasing in incidence globally, with dramatic ecosystem-level consequences. We examined the trophic consequences of invasion by a Spartina hybrid (S. alterniflora x S. foliosa) in San Francisco Bay (USA) by documenting differences in biomass and trophic structure of benthic communities between sediments invaded by Spartina and uninvaded sediments. We found the invaded system shifted from an algae-based to a detritus-based food web. We then tested for a relationship between diet and tolerance to invasion, hypothesizing that species that consume Spartina detritus are more likely to inhabit invaded sediments than those that consume surface algae. Infaunal diets were initially examined with natural abundance stable isotope analyses and application of mixing models, but these yielded an ambiguous picture of food sources. Therefore, we conducted isotopic enrichment experiments by providing 15N-labeled Spartina detritus both on and below the sediment surface in areas that either contained Spartina or were unvegetated. Capitellid and nereid polychaetes, and oligochaetes, groups shown to persist following Spartina invasion of San Francisco Bay tidal flats, took up 15N from labeled native and invasive Spartina detritus. In contrast, we found that amphipods, bivalves, and other taxa less tolerant to invasion consumed primarily surficial algae, based on 13C enrichment experiments. Habitat (Spartina vs. unvegetated patches) and location of detritus (on or within sediments) did not affect 15N uptake from detritus. Our investigations support a "trophic shift" model for ecosystem response to wetland plant invasion and preview loss of key trophic support for fishes and migratory birds by shifting dominance to species not widely consumed by species at higher trophic levels.     

Geographical variations in the trophic ecology of Japanese anchovy, Engraulis japonicus, inferred from carbon and nitrogen stable isotope ratios

Carbon and nitrogen stable isotope ratios of Japanese anchovy (Engraulis japonicus) and their stomach contents were examined and compared among various regions around Japan. Geographical variations in the isotope ratios were found between inshore and Pacific offshore regions. While most of the anchovy samples had isotope ratios around −17.6‰ for δ¹³C and 10.0‰ for δ¹⁵N as median values, higher (more enriched) isotope values were found in the anchovy sampled from inshore regions. On the contrary, lower (more depleted) values were found mostly in the anchovy from the Pacific offshore region including the Kuroshio Extension and Kuroshio-Oyashio transition zones. Higher carbon isotope ratios in the inshore regions may reflect a carbon source from benthic primary producers in addition to phytoplankton possibly through the consumption of the larvae of benthic organisms such as bivalves or decapods, which were found in the stomach contents of the inshore anchovy. Variations in the nitrogen isotope ratio may reflect not only differences in the trophic level of prey species, but also variations in the baseline level of food webs. Stable isotope ratios are potentially a useful tool for understanding the stock/population structure and migration of anchovy. The present findings indicate the potential importance of the “inshore–offshore” variations in the biology of Japanese anchovy populations in the northwestern Pacific waters.     

Relative importance of benthic microalgae,phytoplankton, and mangroves as sources of nutrition for penaeid prawns and other coastal invertebrates from Malaysia

Carbon, sulfur, and nitrogen stable isotope ratio techniques were used in 1989 and 1990 to evaluate the relative importance of algae and of mangrove detritus in the nutrition of two penaeid prawn species on the west coast of Peninsular Malaysia. Mangrove detritus was found to contribute to the nutrition of juvenile Penaeus merguiensis de Man living within tidal creeks, but not to adult P. merguiensis and juvenile and adult Parapenaeopsis sculptilis (Heller) captured offshore. Results from radiotracer feeding studies, with refractory ¹⁴C mangrove lignocellulose as the food source, indicated that juvenile P. merguiensis from tidal creeks assimilated mangrove carbon with an efficiency of 13.4%. This did not differ significantly (P=0.05) from the assimilation efficiencies of juvenile and adult P. sculptilis living offshore (10.0 and 10.9%, respectively); these values were significantly higher (P<0.001) than for adult P. merguiensis (2.1%). Thus, the differential contribution of mangrove material to the nutrition of prawns in the tidal creeks and offshore was not related to differences in the prawn's ability to utilize detritus. Instead, our analysis of C stable isotopes in sediments indicated that mangrove detritus was generally more abundant within the tidal creeks than offshore. Juvenile prawns in the tidal creeks may also utilize mangrove material indirectly by feeding on small detritivorous invertebrates. Stable isotope analyses suggest that benthic microalgae constitute the other major dietary component for prawns living in tidal creeks. Prawns offshore were utilizing mainly phytoplankton-based material.     

Temporal and spatial variability in stable isotope ratios of SPM link to local hydrography and longer term SPM averages suggest heavy dependence of mussels on nearshore production

Temporal changes in hydrography affect suspended particulate matter (SPM) composition and distribution in coastal systems, potentially influencing the diets of suspension feeders. Temporal variation in SPM and in the diet of the mussel Perna perna, were investigated using stable isotope analysis. The δ¹³C and δ¹⁵ N ratios of SPM, mussels and macroalgae were determined monthly, with SPM samples collected along a 10 km onshore–offshore transect, over 14 months at Kenton-on-Sea, on the south coast of South Africa. Clear nearshore (0 km) to offshore (10 km) carbon depletion gradients were seen in SPM during all months and extended for 50 km offshore on one occasion. Carbon enrichment of coastal SPM in winter (June–August 2004 and May 2005) indicated temporal changes in the nearshore detrital pool, presumably reflecting changes in macroalgal detritus, linked to local changes in coastal hydrography and algal seasonality. Nitrogen patterns were less clear, with SPM enrichment seen between July and October 2004 from 0 to 10 km. Nearshore SPM demonstrated cyclical patterns in carbon over 24-h periods that correlated closely with tidal cycles and mussel carbon signatures, sampled monthly, demonstrated fluctuations that could not be correlated to seasonal or monthly changes in SPM. Macroalgae showed extreme variability in isotopic signatures, with no discernable patterns. IsoSource mixing models indicated over 50% reliance of mussel tissue on nearshore carbon, highlighting the importance of nearshore SPM in mussel diet. Overall, carbon variation in SPM at both large and small temporal scales can be related to hydrographic processes, but is masked in mussels by long-term isotope integration.     

Microplastics in the benthic invertebrates from the coastal waters of Kochi,Southeastern Arabian Sea

This study examined microplastic particles present in the benthic invertebrates Sternaspis scutata, Magelona cinta (deposit feeders) and Tellina sp. (suspension feeder) from the surface sediments of off-Kochi, southwest coast of India. The microplastic particles and thread-like fibres detected in these organisms were identified to be polystyrene by using DXR Raman microscope. Examination of the microplastic particle in Sternaspis scutata by epifluorescent microscopy showed fragmentation marks on the surface suggesting that the microplastic particle was degraded/weathered in nature. The study provides preliminary evidence of the presence of microplastics in benthic fauna from the coastal waters of India. However, further studies are required to understand the sources, distribution, fate and toxicity of the different types of microplastics in benthic invertebrates in order to identify any potential threats to higher trophic level organisms.     

Arthropod food web restoration following removal of an invasive wetland plant.

Restoration of habitats impacted by invasive plants is becoming an increasingly important tool in the management of native biodiversity, though most studies do not go beyond monitoring the abundance of particular taxonomic groups, such as the return of native vegetation. Yet, the reestablishment of trophic interactions among organisms in restored habitats is equally important if we are to monitor and understand how ecosystems recover. This study examined whether food web interactions among arthropods (as inferred by abundance of naturally occurring stable isotopes of C [delta13C] and N [delta15N]) were reestablished in the restoration of a coastal Spartina alterniflora salt marsh that had been invaded by Phragmites australis. From patterns of C and N stable isotopes we infer that trophic interactions among arthropods in the native salt marsh habitats are characterized by reliance on the dominant marsh plant Spartina as a basal resource. Herbivores such as delphacid planthoppers and mirid bugs have isotope signatures characteristic of Spartina, and predatory arthropods such as dolicopodid flies and spiders likewise have delta13C and delta15N signatures typical of Spartina-derived resources (approximately -13 per thousand and 10 per thousand, respectively). Stable isotope patterns also suggest that the invasion of Phragmites into salt marshes and displacement of Spartina significantly alter arthropod food web interactions. Arthropods in Phragmites-dominated sites have delta13C isotope values between -18 per thousand and -20 per thousand, suggesting reliance on detritus and/or benthic microalgae as basal resources and not on Phragmites, which has a delta13C approximately -26 per thousand. Since most Phragmites herbivores are either feeding internally or are rare transients from nearby Spartina, these resources do not provide significant prey resources for other arthropod consumers. Rather, predator isotope signatures in the invaded habitats indicate dependence on detritus/algae as basal resources instead of the dominant vegetation. The reestablishment of Spartina after removal of Phragmites, however, not only returned species assemblages typical of reference (uninvaded) Spartina, but stable isotope signatures suggest that the trophic interactions among the arthropods were also similar in reestablished habitats. Specifically, both herbivores and predators showed characteristic Spartina signatures, suggesting the return of the original grazer-based food web structure in the restored habitats.     

Organic detritus of a tropical estuary

Organic detritus of the Cochin Backwater (India) is largely composed of fine silt and sand particles around which organic matter adheres and forms aggregates. In addition to plankton, large quantities of benthic algae, rooted plants, animal matter, suspended soft mud and the material brought down by the rivers and land runoff constitute the main sources of detritus. Detritus sedimentation in the estuary attains its maximum from April to June. Detritus forms a major portion of seston, while phytoplankton productivity constitutes 0.1 to 1.0% of settled detritus. Detrital pigments include degraded chlorophyll (phaeophytin), which has a marked seasonal variation; detrital carbon, phosphorus and nitrogen show little change during the year. The caloric value of detritus, calculated from protein, carbohydrate and lipid fractions and also from total carbon, indicates that sedimented detritus does not have a high nutritional value. However, being a readily available material, its entry into the food chain seems to increase the efficiency of energy transfer from one trophic level to another.     

Responses to extreme seasonality in food supply: diet plasticity in Antarctic brachiopods

The ice gouged, shallow, polar seabed is a challenging place to live, but suspension feeders are particularly rich and abundant there. The extreme seasonality of food supply from phytoplankton at high latitudes, combined with very stable temperatures has not, however, reduced the range of life history adaptations. Some species extend feeding and growing periods by concentrating on smaller, lower biomass but longer duration, fractions of phytoplankton. Here we show that shallow-water Antarctic brachiopods can switch from pelagic to benthic food sources when required. Like most suspension feeders they utilise the extremely abundant summer phytoplankton blooms, but unlike many other groups brachiopods do not appear to become dormant in winter. In shallow sites around the world wind and wave action resuspend benthic material, making it available to filter feeders. Widespread ice disturbance at polar latitudes may also cause resuspension enhancing local food supply. Articulate brachiopods have blind-ended guts and probably feed little once a large bolus of food has been collected, so a resuspension event may represent a significant enhancement of yearly food availability. The key to their ability to utilise unpredictable food sources is the same trait responsible for their polar success; very low maintenance costs and a catholic diet. Utilising resuspended material could be an important factor in global brachiopod distributions. Previously difficult to explain high brachiopod densities in New Zealand, Northwest Europe and the Canadian Pacific Coast may occur because these areas are all in the worlds windiest, and hence strongest resuspension, latitudes.Communicated by J.P. Thorpe, Port Erin     

Trophic structure of coastal Antarctic food webs associated with changes in sea ice and food supply

Predicting the dynamics of ecosystems requires an understanding of how trophic interactions respond to environmental change. In Antarctic marine ecosystems, food web dynamics are inextricably linked to sea ice conditions that affect the nature and magnitude of primary food sources available to higher trophic levels. Recent attention on the changing sea ice conditions in polar seas highlights the need to better understand how marine food webs respond to changes in such broad-scale environmental drivers. This study investigated the importance of sea ice and advected primary food sources to the structure of benthic food webs in coastal Antarctica. We compared the isotopic composition of several seafloor taxa (including primary producers and invertebrates with a variety of feeding modes) that are widely distributed in the Antarctic. We assessed shifts in the trophic role of numerically dominant benthic omnivores at five coastal Ross Sea locations. These locations vary in primary productivity and food availability, due to their different levels of sea ice cover, and proximity to polynyas and advected primary production. The delta15N signatures and isotope mixing model results for the bivalves Laternula elliptica and Adamussium colbecki and the urchin Sterechinus neumeyeri indicate a shift from consumption of a higher proportion of detritus at locations with more permanent sea ice in the south to more freshly produced algal material associated with proximity to ice-free water in the north and east. The detrital pathways utilized by many benthic species may act to dampen the impacts of large seasonal fluctuations in the availability of primary production. The limiting relationship between sea ice distribution and in situ primary productivity emphasizes the role of connectivity and spatial subsidies of organic matter in fueling the food web. Our results begin to provide a basis for predicting how benthic ecosystems will respond to changes in sea ice persistence and extent along environmental gradients in the high Antarctic.     

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.     

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.     

Particulate Organic Matter Composition in A Semi-Enclosed Marine System

Spatial and temporal changes in the biochemical composition of particulate organic matter in a semi-enclosed marine system (Stagnone di Marsala, Mediterranean Sea) were studied, on a monthly basis, from January to December 1994, in order to assess nutritional value of suspended particles for benthic suspension feeders. According to previous findings, the study site displayed a strong oligotrophy. Chlorophyll-a accounted for a very low fraction of the total suspended matter pool (0.1%), whereas at least 75% of POC was of detrital/heterotrophic origin. POC: PON ratio values indicate that bacterioplankton biomass accounted for a significant fraction of the total POC pool, displaying values comparable to those of the phytoplankton biomass (phytoplankton to bacterial biomass ratio was about (1). Temporal and spatial changes in the biochemical composition of particulate organic matter were rather limited and related to its sources, the main of which is represented by detrital particles released by the Posidonia oceanica (L.) beds. the comparison between our results and those encountered in other coastal lagoons indicates that the low abundance of suspension-feeding organisms observed in the study area is related to the “quality depression” of particles due to the dilution of high quality compounds (i.e., biopolymeric carbon) in a largely inorganic matrix. This result leads us to conclude that, to reach the same amount of high quality particulate food, a suspension feeder mollusc in the Marsala lagoon would need to filter a sea water volume around 3 times higher than in other Mediterranean coastal lagoons.     

Particulate Organic Matter Composition in A Semi-Enclosed Marine System

Spatial and temporal changes in the biochemical composition of particulate organic matter in a semi-enclosed marine system (Stagnone di Marsala, Mediterranean Sea) were studied, on a monthly basis, from January to December 1994, in order to assess nutritional value of suspended particles for benthic suspension feeders. According to previous findings, the study site displayed a strong oligotrophy. Chlorophyll-a accounted for a very low fraction of the total suspended matter pool (0.1%), whereas at least 75% of POC was of detrital/heterotrophic origin. POC: PON ratio values indicate that bacterioplankton biomass accounted for a significant fraction of the total POC pool, displaying values comparable to those of the phytoplankton biomass (phytoplankton to bacterial biomass ratio was about (1). Temporal and spatial changes in the biochemical composition of particulate organic matter were rather limited and related to its sources, the main of which is represented by detrital particles released by the Posidonia oceanica (L.) beds. the comparison between our results and those encountered in other coastal lagoons indicates that the low abundance of suspension-feeding organisms observed in the study area is related to the “quality depression” of particles due to the dilution of high quality compounds (i.e., biopolymeric carbon) in a largely inorganic matrix. This result leads us to conclude that, to reach the same amount of high quality particulate food, a suspension feeder mollusc in the Marsala lagoon would need to filter a sea water volume around 3 times higher than in other Mediterranean coastal lagoons.     

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.     

Is kelp detritus a good food for suspension feeders? Effects of kelp species, age and secondary metabolites

The food quality of detrital particles derived from three species of kelps was evaluated in a laboratory feeding experiment utilizing two species of suspension feeders, the serpulid polychaete Pseudochitonopomaoccidentalis and the mussel Mytilustrossulus. Fresh and aged kelp particles were also evaluated, and growth in all treatments was compared to growth on ad libidum phytoplankton rations. Fresh particles from Laminariagroenlandica, aged particles from Agarumfimbriatum and Alariamarginata, and mixed phytoplankton promoted the highest growth rates in both consumers. Growth was inversely related to total polyphenolic concentration in the fresh kelp particles. The increase in quality of both Agarumfimbriatum and Alariamarginata particles with age corresponded with a rapid loss of polyphenolic secondary metabolites and an increase in total nitrogen. Received: 26 November 1996 / Accepted: 9 January 1997     

Trophic significance of kelps in kelp communities in Brittany (France) inferred from isotopic comparisons

The relative contribution of kelps and other food sources to the diet of consumers in shallow coastal communities has been hotly debated in recent years. It has been suggested that considering proxies instead of phytoplankton isotopic signatures can lead to an overestimation of kelp contribution through isotopic mixing models. We analysed spatial patterns in carbon isotopic ratios of the dominant primary sources and consumers at two subtidal sites in Brittany (France) prior to the anticipated 2011 phytoplankton bloom to determine which of kelp and phytoplankton is the dominant food source in Laminaria hyperborea forests. We found simultaneous spatial variations for consumers, kelps and deposited particulate organic matter, suggesting that kelp-derived organic matter is a key component of associated food webs for at least part of the year.     

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.