Isotopic Niche Research Articles

Flexible foraging strategies in a highly pelagic seabird revealed by seasonal isotopic niche variation

Flexible foraging strategies in a highly pelagic seabird revealed by seasonal isotopic niche variation

Trophic Niche Dynamics and Diet Partitioning of King Crab Lithodes santolla in Chile’s Sub-Antarctic Water

The southern king crab Lithodes santolla is one of the most economically important fishery species in the southern waters of the Atlantic and Pacific Oceans. A combination of stomach content and stable isotope analyses was used to reveal the potential dietary characteristics, isotopic niche, overlap among maturity stages and sexes, and trophic relationships of an L. santolla population in the Nassau Bay, Cape Horn region. Stable isotope analyses indicated that L. santolla assimilated energy from a basal carbon source, the giant kelp Macrocystis pyrifera, forming the trophic baseline of the benthic food web. Moreover, the trophic position of L. santolla varied among late juveniles and adults, suggesting that the southern king crab does undergo an ontogenetic diet shift. L. santolla exhibited intraspecific isotopic niche variation, reflecting niche differentiation which allows the species to partition resources. The trophic relationships of L. santolla with the associated fauna suggested some potential interactions for food resources/habitat use when they are limited. This study is the first attempt to characterize the trophic dynamics of the southern king crab in the Cape Horn area and, by generating more data, contributes to the conservation of the king crab population and the long-term management of local fisheries that rely on this resource.

Dynamic trait-niche relationships shape niche partitioning across habitat transformation gradients

Multidimensional approaches examining complex trait-niche relationships are crucial to understand community assembly. This is particularly important across habitat transformation gradients because specialists are progressively substituted by generalists and, despite increasing functional homogenization, in both specialist and generalist communities niche partitioning is apparent. Here, in line with the continuum hypothesis, we expected that divergent trait-niche relationships would arise in passerine assemblages across the natural-to-urban transformation gradient. More specifically, we expected that traits linking form to function would be more important in less transformed habitats, while population density and traits linked to dispersal and dominance would predominate in more transformed habitats. Accordingly, we found that beak length and its interaction with tarsus length correlated significantly with isotopic niches in natural and rural habitats, where specialists predominate. Conversely, body size and aggressiveness only showed significant relationships with isotopic niches with increasing habitat transformation, where generalists prevail. Interestingly, we recorded a mix of these processes in rural habitats, which acted as a frontier between these two domains. Our study is thus important in showing that a complex combination of morphological and behavioral traits determine niche characteristics, and that these relationships are dynamic across habitat transformation gradients.

Using stable isotope chronologies within squid gladii (Doryteuthis gahi) to evaluate dietary differences by fishing region and season

Stable isotopes are a useful tool for understanding diet and migration in squid, which often play an important role in marine food webs. The Patagonian long-finned squid fishery around Falkland Islands waters is managed separately for each of its biannual fishing seasons and 2 sub-areas of the fishing zone. However, factors driving differences in the timing of recruitment and squid size between sub-areas have never been resolved. To investigate whether seasonal and spatial variation in life history parameters of the Patagonian long-finned squidDoryteuthis gahiis driven by differences in diet, stable isotope profiles (δ13C and δ15N) were measured along the gladius—the internal chitinous shell—to reconstruct a chronological record of habitat and feeding variations and to compare fishing seasons and sub-areas using a mixed modelling approach. Here we show that isotopic niche was distinct between the fishing seasons, but negligible differences in isotopic niche were found between sub-areas of the fishing zone. This suggests that spatial differences in life history parameters are not a result of dietary variation. Substantial variation in δ13C and δ15N values along the gladius indicated versatility in feeding behaviours and dietary habits over time. Squid in the second fishing season occupied a lower trophic level (mean = 3.2) than the first season (mean = 3.5). Patterns in δ13C values indicated more complex and substantial migration patterns in the second fishing season. This coincides with the current knowledge of this species’ spawning migrations. We anticipate that these data may be used for future studies investigating the role of squid within the Patagonian Shelf marine ecosystem. Analysis of the squid gladius has applications for other loliginid squid species in future studies.

Perspectives and challenges on isotopic ecology of terrestrial birds in Brazil

Although stable isotopes have been increasingly used in ornithology since 1980 in many places, Brazil has been slow in adopting this methodology, especially when it comes to terrestrial birds. The most common elements in bird ecology studies are carbon, nitrogen, hydrogen, and oxygen stable isotopes, which provide information on diet, trophic interactions, habitat use, migration, geographic patterns, and physiology. It is important that Brazilian ornithologists become aware of the potential of stable isotope analysis in ecological studies, and the shortcomings of this tool. The use of stable isotopes to study bird ecology has great potential in Brazil, since many ecological questions about Neotropical birds can be addressed by it (e.g., resource and habitat use, migratory routes, isotopic niches, anthropogenic impacts, individual specialization). Brazilian museums and other Natural History collections can provide samples to study long-term temporal dynamics in bird ecology. Additionally, the integration of avian tissue sample information into a database may increase the collaboration among researchers and promote sample reuse in a variety of studies. All biomes in Brazil have been under pressure from anthropogenic impacts (e.g., land-use change, habitat loss, fragmentation, intensive agriculture), affecting several taxa, including terrestrial birds. Considering the negative effects of human expansion over natural areas and that stable isotopes provide useful ecological information, ornithologists in Brazil should increase their use of this tool in the future.

Using stable isotope to compare the habitat use and trophic level between the new and old breeding range of wild Crested Ibis in the early breeding season

The concept of foraging niche provides an insight into habitat use and dietary information of animals. Knowing intraspecific variation in foraging niche and trophic level is critical to the understanding of the species response to environmental changes during the process of range expansion, as well as the habitat management for conservation of threatened species. Using stable isotopic values of eggshell membranes (δ13C and δ15N), we examined whether there are differences in habitat use, trophic level, foraging niche width between the new and old breeding habitats (plains vs. mountains) of wild Crested Ibis (Nipponia nippon) in the early breeding season. Crested Ibis exhibited high variability in both δ13C and δ15N values, δ13C and δ15N varied as a function of habitat types. Birds breeding in plains had significantly higher δ13C but lower δ15N values compared to the birds breeding in mountains. Higher δ15N suggested that individuals in mountains consumed a great proportion of higher trophic level prey species in the early breeding season. Moreover, the isotopic niches were distinctly different in positions and showed small overlap between the two habitat types. The niche width was wider in old habitat than in the expanded new habitat. Our results demonstrated that the wild Crested Ibis had a high intraspecific variation in habitat uses and trophic levels in the early breeding season, and they could be divided into mountain and plain groups based on their different foraging niches. The difference in δ15N and niche width revealed that high trophic level food resources might be insufficient in plains. These findings stressed the importance of protecting foraging grounds in mountains and the necessity of improving foraging grounds in plains during winter and spring. Our study highlights the feasibility of investigating intraspecific variation in foraging ecology of birds through non-invasive isotopes of eggshell membranes. Understanding foraging niche variation gives us an insight into the food resource diversity in local areas and provides important information regarding particular foraging habitats that require protection.

Trophic ecology and resource partitioning of Haemulidae species along the Northeastern Brazilian continental shelf

Abstract In the Southeastern Tropical Atlantic, Haemulidae family play an important role both environmentally, acting as a link between lower and higher trophic levels, and socioeconomically, being widely caught by artisanal fleets. This study aimed to describe the trophic ecology of three grunt species (Haemulon aurolineatum, H. plumierii and H. squamipinna) considering spatial, temporal and ontogenetic aspects, integrating stomach content and stable isotopes analysis. Sampling occurred in 26 stations along the Northeast of Brazil (04°– 09°S), in August 2015 and April 2017, using bottom trawling net. There was greater feeding intensity at night, at latitudes below 08°S and in the inner continental shelf. Higher values of δ¹⁵N were reported for H. aurolineatum and H. plumierii collected near coastline. The isotopic niche breadth indicated that H. aurolineatum has a narrower diet thanH. plumierii. For the three species, the trophic level ranged between three and four. Considering stomach content and isotopic niche, diet was similar comparing species. This trophic ecology pattern reveals a likewise use of the habitat, which may be essential for identifying priority areas for conservation on an ecosystem basis, especially in rich reef zones that are subject to several increasing pressures, such as those in Northeast Brazil.

Insights into the trophic ecology of white-beaked dolphins Lagenorhynchus albirostris and harbour porpoises Phocoena phocoena in Iceland

Sympatric organisms can avoid competition by occupying different ecological niches, a mechanism known as niche partitioning. In Iceland, white-beaked dolphinsLagenorhynchus albirostrisand harbour porpoisesPhocoena phocoenaare the most common small cetaceans observed but their trophic ecology remains understudied, including the potential for resource competition. In this study, we measured δ15N and δ13C values from white-beaked dolphin (n = 28) and harbour porpoise (n = 29) muscle samples collected over a 33 yr period (1987-2019) to compare isotopic niche width and overlap of both species, as well as diet composition. We also tested for within-species effects of sex, age class, body length, year of sampling and origin (bycatch vs. stranding) on the δ13C and δ15N values. Intra-species variations included differences between stranded and bycaught white-beaked dolphins and ontogenetic variations in both species, but further studies are necessary to investigate the factors that might explain these results. Inter-species comparisons showed that harbour porpoises and white-beaked dolphins had non-overlapping isotopic niches, with harbour porpoises exhibiting smaller niche widths (corrected standard ellipse area, SEAc: 1.25 vs. 2.13‰2). While white-beaked dolphins had a broader diet, composed primarily of gadoids but with contributions of other fish species, harbour porpoises fed almost exclusively on capelinMallotus villosus, suggesting niche segregation and width is largely maintained by targeting different prey resources. Both species also showed no long-term changes in trophic ecology, despite recent ecosystem changes in this region, possibly a result of adapting to spatial changes in prey distribution or shifts to other prey at similar trophic levels.

Assessing commercial fishery bait in Dungeness crab Cancer magister feeding ecology: δ13C and δ15N stable isotope and gut content analysis

Dungeness crabsCancer magistersupport the largest fishery in Oregon (USA), which inputs millions of pounds of bait into the coastal ocean every year. We assessed evidence for seasonal consumption of commercial Dungeness crab fishery bait off the Oregon coast by that target species through δ13C and δ15N stable isotope and gut content analysis. Using Dungeness crab samples collected on the Oregon inner to mid-continental shelf, variation in δ13C and δ15N values were assessed according to sex, size class, region, and season using nested ANOVA, Euclidean vector statistics, and Bayesian standard ellipse areas corrected for sample size (SEAc) in R. The isotopic signatures of sampled crabs showed statistically significant variation by sex, region, and season; the differences in the isotopic niches of large male versus female crabs (carapace width ≥159 mm) were especially pronounced. δ15N in female crabs peaked in spring and declined toward fall with similar mean δ13C, which could be indicative of higher trophic level bait consumption in the winter when the fishery is the most active, while δ13C varied seasonally in males with similar mean δ15N. The approximated trophic niches (based on SEAc) of both male and female crabs were greatest in fall, suggesting broader foraging in the absence of bait inputs. This work provides a step towards understanding the ecological role of fishery activities on one of the most economically valuable species on the US west coast.

Millennial-Scale Drivers of Small Mammal Isotopic Niche Dynamics in Southern California

Millennial-Scale Drivers of Small Mammal Isotopic Niche Dynamics in Southern California

Feeding of Atlantic bluefin tuna Thunnus thynnus around the Canary Islands assessed from stomach content and stable isotope analyses

The Canary archipelago, which is part of the Atlantic biogeographical region of Macaronesia, provides suitable habitat for tropical and temperate-water large pelagic species. Atlantic bluefin tuna (ABFT) Thunnus thynnus occur year round in the Canary Islands. Life history traits of ABFT, specifically foraging patterns, have not been studied thus far in this region. We investigated ABFT trophic biology, combining stomach content and stable isotope analyses. A high proportion (~77%) of the stomachs contained prey, indicating active foraging. The diet primarily consisted of fishes, among which the snipefish Macroramphosus sp. was the major prey. Cephalopods and crustaceans were less important diet components. Moreover, a well-preserved specimen of Cory’s shearwater Calonectris borealis was found in a stomach sampled in 2018. Besides natural prey, 16.7% of the stomachs contained plastic debris. Inter-annual isotopic differences were detected in liver tissue samples, reflecting a dietary shift in 2018, where δ15N values were lower than in 2016 and 2017. Isotopic niche width estimations from stable isotope Bayesian ellipse in R and kernel utilization density analyses suggested a more diverse diet in 2017. Corrected and Bayesian standard ellipse area values from muscle and liver data indicated that the diet of ABFT in the Canary Islands is more euryphagous than in the Strait of Gibraltar (East Atlantic) but more stenophagous than it is in the Gulf of Saint Lawrence (West Atlantic). The present results show that the Canary archipelago represents a foraging ground for ABFT in spring.

Isotopic Niches of Coral Reef Fishes at Early Stages of Development on Guadeloupean Coral Reefs (Lesser Antilles)

Isotopic Niches of Coral Reef Fishes at Early Stages of Development on Guadeloupean Coral Reefs (Lesser Antilles)

Trophic ecology of sympatric juvenile stingrays within a nursery area

Nursery areas are crucial for many elasmobranch species, providing advantages such as increased access to prey and reduced predation risk. This study investigated the trophic interactions of two juvenile stingray species within a coastal communal nursery using stable isotope analysis. Muscle, plasma and red blood cells samples were taken from the mangrove whipray Urogymnus granulatus and the cowtail stingray Pastinachus ater, and δ15N, δ13C and δ34S measured. Urogymnus granulatus had higher mean δ13C, δ15N and δ34S than P. ater. General linear models showed no significant trends between δ13C, δ15N or δ34S and body size or sex. Low isotopic niche overlap, combined with previous data on movement patterns, provided evidence of niche partitioning between stingrays that likely reflect differences in feeding grounds and prey selection. Despite the differences in feeding grounds and prey selection, previous studies showed that U. granulatus and P. ater share sand and reef flat areas for most of the day (~20 h). δ13C and δ34S values suggested that mangrove-derived carbon had little importance to stingrays’ diets in the study area. Results presented in this study bring new insights to the feeding ecology of two sympatric stingray species and their trophic interactions within a communal nursery area.

At-sea behavioural ecology of the endangered MacGillivray’s prion from Saint Paul Island: combining tracking and stable isotopes

Seabirds play important roles as marine ecosystem sentinels. Studying their at-sea ecology is essential for understanding how environmental variability affects their populations. However, the at-sea ecology of small-sized temperate seabirds remains poorly studied. We explored the at-sea ecology of the Critically Endangered MacGillivray’s prion Pachyptila macgillivrayi breeding on the subtropical Saint Paul Island. Using global location sensor loggers and stable isotope analysis, we investigated movements, migratory strategies, at-sea activity and moulting period, and characterized the isotopic niche of tracked individuals. During incubation, MacGillivray’s prions remained in temperate waters north of the Subtropical Front, possibly feeding on prey caught in cold eddies. During the inter-breeding period, individuals wintered almost equally to the north and south of the Subtropical Front in 2 distinct sectors (Tasman Sea and Southwest Indian Ridge). Daily activity varied seasonally, and individuals overwintering in the Tasman Sea spent more time flying at night when moonlight intensity was high. Moulting occurred after the breeding period and lasted longer compared to other prion species. Isotopic data suggest a higher dietary proportion of low trophic-level prey for MacGillivray’s prions than for Antarctic and slender-billed prions, highlighting trophic segregation in relation to bill width. Our study provides new evidence to understand the suite of adaptations allowing the abundant prion species to coexist by feeding on prey of different sizes. Contrary to the majority of seabird species, MacGillivray’s prions from Saint Paul Island exhibited 2 migratory tactics with associated differences in at-sea activity, leading to questions about the origin of these differences.

Foraging trips and isotopic niche of chick-rearing South Georgian diving petrels from the Kerguelen Islands

Seabirds are central place foragers, relying on prey that is patchily distributed and of variable predictability. Species travelling at a high energetic cost are more strongly dependent on spatially predictable prey. This is the case for diving petrels Pelecanoides spp., which are small Procellariiformes that feed by pursuit diving and travel by flapping constantly. Despite their abundance and importance as zooplankton consumers, information on the foraging strategy of diving petrels is still lacking. The detailed at-sea movements and the trophic niche of the South Georgian diving petrel P. georgicus was investigated for the first time using miniaturized GPS and the stable isotope method, respectively. Overall, South Georgian diving petrels from the Kerguelen Islands performed unexpected, direct and long-distance trips (mean foraging range: 191-217 km) to the Antarctic Polar Front, south of the archipelago. This foraging ground is a productive and predictable area, where the birds stopped and fed at the distal part of their trip. Blood isotopic values indicate that the tracked birds fed consistently on macrozooplankton. Such a distant oceanic feeding strategy contrasts with the coastal foraging patterns of the closely related common diving petrel P. urinatrix. Commuting to a more distant but easily accessible resource allows South Georgian diving petrels to cope with their high commuting costs, and to segregate spatially from the sympatric common diving petrel during the breeding season.

Assessing marine ecosystem complexity: isotopic integration of the trophic structure of seabird communities from the Southern Ocean

Understanding the processes structuring communities is a fundamental goal in ecology and conservation biology. Seabirds are commonly used as sentinels of marine ecosystems, but there is a lack of quantitative information providing a synoptic view of their community structure and of its underlying mechanisms. We used stable isotope analysis of chick feathers to investigate the structure of 2 communities that are representative of the subantarctic (Kerguelen) and Antarctic (Adélie Land) seabird diversity. Total area of the convex hull (a measure of the total δ13C-δ15N niche space) was 8.4-fold higher at the Kerguelen Islands than in Adélie Land, a consequence of the higher seabird diversity at the former locality. Kerguelen seabirds grouped into 2 clusters of oceanic and inshore species, with the latter group not represented in Adélie Land. Communities are primarily structured by the availability of foraging habitats (δ13C) and then of trophic resources (δ15N), with body size being a major driving force of trophic position. Ecological characteristics are more important than phylogeny to shape seabird isotopic niche breadth (standard ellipse area corrected for small sample size, SEAc), with no significant differences between Sphenisciformes, Procellariiformes, and Charadriiformes. By contrast, SEAc varies according to foraging guilds, diet, and a specialist-generalist gradient, with ubiquitous seabirds having a 10-fold larger mean SEAc than pelagic divers. This study sets a baseline against which the effects of long-term environmental changes on seabird community structure can be studied across years and conditions, and provides a relevant starting point for the investigation into the effect of climate change on Southern Ocean ecosystems.

Trophic ecology of an abundant kelp forest echinoderm, the bat star Patiria miniata

Echinoderms often play key roles in structuring marine ecosystems. The bat star Patiria miniata is an abundant echinoderm in the kelp forests of the northeastern Pacific coast whose trophic ecology has been understudied. Understanding the trophic role of P. miniata is important given the recent declines of many sea star populations due to wasting disease. Patiria miniata was largely unaffected by these outbreaks and could potentially fill the trophic niches left by other ecologically important sea star species. In this study, we used a combination of feeding experiments and stable isotope analysis to provide new insights into the trophic ecology of P. miniata. Given that P. miniata is considered an omnivorous generalist, we conducted a series of feeding experiments in which we quantified consumption rates for a wide range of reported prey items. Consumption rates were highest for different types of carrion, lower for sessile invertebrates, and negligible for all species of macrophytes. In a series of follow-up experiments, we found that food deprivation did not lead to demonstrable consumption of macrophytes by P. miniata, but that the presence of epiphytes significantly increased consumption rates (presumably of the epiphytes plus incidental consumption of macrophytes). Finally, we compared the isotopic niche of P. miniata with that of a carnivore (the giant sea star Pisaster giganteus), an herbivore (the purple sea urchin Strongylocentrotus purpuratus), and a detritivore (the warty sea cucumber Parastichopus parvimensis) and found that P. miniata occupied the highest relative trophic level and was isotopically most similar to P. giganteus. Altogether, our results suggest that the diet of P. miniata is narrower and more carnivorous than previously expected.

Dietary expansion facilitates the persistence of a large frugivore in fragmented tropical forests

AbstractHow species persist in fragmented habitats is essential to understanding species resilience in response to increasing anthropogenic pressures. It has been suggested that expansion in dietary niche allows populations to persist in human‐modified landscapes, yet this hypothesis has been poorly tested in highly diverse ecosystems such as tropical forests where frugivory is ubiquitous. Here, we measured dietary niche expansion of a large forest‐dwelling mammal, the white‐lipped peccary (Tayassu pecari), in the Atlantic Forest, Brazil, by comparing its diet using stable carbon (δ13C) and nitrogen (δ15N) isotopes. We collected hair of white‐lipped peccaries in three continuous and three fragmented forests and compared δ13C and δ15N values, resource use and isotopic niches among populations and between forest types. We also tested the relationship between isotopic values of the populations and the forest cover percentage. White‐lipped peccaries fed mainly on forest sources (C3 resources), especially in continuous forests, but 28% of the individuals in fragmented sites also incorporated C4 resources to some extent. In fragmented forests, the populations had isotopic niches from 3‐ to 3.6‐fold the size of those in continuous forests. This niche expansion was due to the consumption of food items with higher δ15N values and C4 crops. Differences among populations were larger among fragmented forests, suggesting variable site‐specific strategies to cope with habitat loss. The mean isotopic values of white‐lipped peccary populations were negatively correlated with the loss of forest cover. Some small forest fragments might still retain relatively high habitat quality, and white‐lipped peccaries might be able to capitalize on such variety of resources, shifting their diets from those observed in continuous forests. We suggest that high dietary flexibility and dietary expansion toward consumption of non‐forest resources might facilitate the persistence of large frugivores in fragmented habitats.

Characterization of Trophic Structure of Fish Assemblages in the East and South Seas of Korea Based on C and N Stable Isotope Ratios

The aim of this study was to assess seasonal variation in the food-web structure of fish assemblages in the East (two sites) and the South (one site) Seas of Korea, and to compare the isotopic niche areas between the regions. To do this, we analyzed the community structures and the δ13C and δ15N values for fish assemblages, and their potential food sources collected during May and October 2020. There were spatial differences in the diversity and dominant species of fish assemblages between the two seas. The fish assemblages in the South Sea had relatively wide ranges of δ13C and δ15N (−22.4‰ to −15.3‰ and 7.4‰ to 13.8‰, respectively) compared to those (−22.1‰ to −18.0‰ and 9.8‰ to 13.6‰, respectively) in the East Sea. The δ13C and δ15N values of suspended particulate organic matter, zooplankton, and fish assemblages differed significantly among sites and between seasons (PERMANOVA, p < 0.05, in all cases). Moreover, isotopic niche indices were relatively higher in the South Sea compared to those in the East Sea. Such differences in food-web characteristics among sites are likely due to the specific environmental effects (especially, major currents) on the differences in the species compositions and, therefore, their trophic relationships. Overall, these results allow for a deeper understanding of the changing trophic diversity and community structure of fish assemblages resulting from climate variability.

Diet and isotopic niche dimensions of predatory fish in two estuaries with different degrees of anthropogenic disturbances: a case study of Wami and Pangani Tanzanian coastal estuaries

Diverse anthropogenic activities including alteration of hydrological regime and agricultural development in the upstream of the river catchments modify the structural components and ecological roles of the species in estuarine ecosystems. The present study compared the diet, carbon (δ13C) and nitrogen (δ15N) isotopic signals, trophic niches and metrics of trophic redundancy of predatory fish and their potential phytodetritivore prey-fish between two estuaries with different degrees of anthropogenic disturbances. The δ13C and δ15N signals, Bayesian mixing models and stomach content analyses were adopted. It was revealed that the diet among the predators Arius africanus, Epinephelus coioides, Sillago sihama and Pomadasys argenteus and their isotopic signals including their phytodetritivore-prey, Valamugil buchanani were significantly different between Wami and Pangani estuaries (PERMANOVA, Pseudo –F ≥ 3.1, p = 0.05). The total isotopic niche area between estuaries accounted by the comparable Bayesian standard ellipse area (SEAb) was significantly smaller in Wami than that of Pangani (t-test, t = 4.3, p < .001). The ANOVA test further confirmed significant variation in SEAb among fish populations in two estuaries (F = 27.84, p < 0.001). The Layman metric indices of trophic diversity and redundancy of Wami estuary were substantially smaller than those observed at Pangani estuary. These findings mean that despite Wami estuary being under conservation status, the extent of disturbances in the upstream is high enough to induce the ecological changes at the base of the food web, subsequently cascading its effect up to the higher-order consumers of the ecosystem. As a result, the ecological redundancy and ecosystem complexity of Wami is somewhat compromised relative to that of Pangani estuary. Therefore, the degree of anthropogenic disturbances in river catchments affect differently the trophic niches of predatory and phytodetritivore fish and hence overall food web structures, trophic redundancy and complexity of estuarine ecosystems.