Decadal shift in foraging strategy of a migratory southern ocean predator.

Rapid anthropogenic environmental change is expected to impact a host of ecological parameters in Southern Ocean ecosystems. Of critical concern are the consequences of these changes on the range of species that show fidelity to migratory destinations, as philopatry is hypothesized to help or hinder adaptation to climate change depending on the circumstances. Many baleen whales show philopatry to feeding grounds and are also capital breeders that meet migratory and reproductive costs through seasonal energy intake. Southern right whales (Eubalaena australis, SRWs) are capital breeders that have a strong relationship between reproductive output and foraging success. The population dynamics of South Africa's population of SRWs are characterized by two distinct periods: the 1990s, a period of high calving rates; and the late 2010s, a period associated with lowered calving rates. Here we use analyses of stable carbon (δ13 C) and nitrogen (δ15 N) isotope values from SRW biopsy samples (n = 122) collected during these two distinct periods to investigate foraging ecology of the South African population of SRWs over a time period coincident with the demographic shift. We show that South African SRWs underwent a dramatic northward shift, and diversification, in foraging strategy from 1990s to 2010s. Bayesian mixing model results suggest that during the 1990s, South African SRWs foraged on prey isotopically similar to South Georgia/Islas Georgias del Sur krill. In contrast, in the 2010s, South African SRWs foraged on prey isotopically consistent with the waters of the Subtropical Convergence, Polar Front and Marion Island. We hypothesize that this shift represents a response to changes in preferred habitat or prey, for example, the decrease in abundance and southward range contraction of Antarctic krill. By linking reproductive decline to changing foraging strategies for the first time in SRWs, we show that altering foraging strategies may not be sufficient to adapt to a changing ocean.

Individual and species-specific traits explain niche size and functional role in spiders as generalist predators.

The function of a predator within a community is greatly based on its trophic niche, that is the number and the strength of feeding links. In generalist predators, which feed on a wide range of prey, the size and position of the trophic niche is likely determined by traits such as hunting mode, the stratum they occur in, their body size and age. We used stable isotope analyses ((13)C and (15)N) to measure the trophic niche size of nine spider species within a forest hedge community and tested for species traits and individual traits that influence stable isotope enrichment, niche size and resource use. The spiders Enoplognatha, Philodromus, Floronia, and Heliophanus had large isotopic niches, which correspond to a more generalistic feeding behaviour. In contrast, Araneus, Metellina and Agelena, as top predators in the system, had rather narrow niches. We found a negative correlation between trophic position and niche size. Differences in trophic position in spiders were explained by body size, hunting modes and stratum, while niche size was influenced by hunting mode. In Philodromus, the size of the trophic niche increased significantly with age. Fitting spiders to functional groups according to their mean body size, hunting mode and their habitat domain resulted in largely separated niches, which indicates that these traits are meaningful for separating functional entities in spiders. Functional groups based on habitat domain (stratum) caught the essential functional differences between the species with species higher up in the vegetation feeding on flying insects and herb and ground species also preying on forest floor decomposers. Interestingly, we found a gradient from large species using a higher habitat domain and having a smaller niche to smaller species foraging closer to the ground and having a larger niche. This shows that even within generalist predators, such as spiders, there is a gradient of specialism that can be predicted by functional traits.

Trophic behaviour of juvenile reef fishes inhabiting interlinked mangrove-seagrass habitats in offshore mangrove islets.

Stable isotope (δ(13)C and δ(15)N) and gut content analyses were used to investigate size-related feeding habits of four reef fishes (the beaugregory Stegastes leucostictus, the french grunt Haemulon flavolineatum, the schoolmaster snapper Lutjanus apodus and the yellowtail snapper Ocyurus chrysurus) inhabiting an offshore (non-estuarine) mangrove islet off Belize, Central America. Comparisons of isotopic niche space and Schoener diet similarity index suggested a low to moderate degree of niche overlap between fish size groups. The δ(13)C gradient between mangrove and seagrass prey as well as results of Bayesian mixing models revealed that sampled fishes relied mostly on seagrass prey items. Only small and large juveniles of the carnivorous species L. apodus derived a part of their diet from mangroves by targeting mangrove-associated Grapsidae crabs and fish prey, respectively. Isotopic niche shifts were particularly obvious for carnivorous fishes that ingested larger prey items (Xanthidae crabs and fishes) during their ontogeny. The utilization of mangrove food resources is less than expected and depends on the ecology and life history of the fish species considered. This research highlights that mangrove-derived carbon contributed relatively little to the diets of four fish taxa from an offshore mangrove islet.

Multi-isotope (δ2H, δ13C, δ15N) feather profiles and morphometrics inform patterns of migratory connectivity in three species of North American swallows.

Aerial insectivorous birds have suffered steep population declines in North America over the last 60 years. A lack of information on migratory connectivity between breeding and non-breeding grounds for these species limits our ability to interpret factors affecting their population-specific trends. We determined likely Latin American non-breeding regions of Bank (Riparia riparia), Barn (Hirundo rustica) and Cliff (Petrochelidon pyrrhonota) swallow from populations across their breeding ranges. We used predicted feather hydrogen (δ2Hf) and carbon (δ13Cf) isoscapes for winter-grown feathers to indicate areas of highest probability of moult origin and incorporated these results into a cluster analysis to determine likely broad non-breeding regions. We also assessed variation in wing length among populations to determine the potential for this metric to differentiate population moult origins. We then investigated patterns of multi-isotopic (δ2Hf, δ13Cf, δ15Nf) and wing-length niche occupancy by quantifying niche size and overlap among populations under the assumption that broad niches were consistent with low within-species migratory connectivity and narrow and non-overlapping niches with higher connectivity. Multivariate assignment identified different non-breeding regions and potential clusters of moult origin generally corresponding to Central America and northern South America, eastern and south-central South America, and the western and southern part of that continent, with variation within and among populations and species. Separate niche space indicated different wintering habitat or areas used by species or populations whereas niche overlap indicated only potential spatial similarity. Wing length varied significantly among populations by species, being longer in the west and north for Bank and Cliff Swallow and longer in eastern Canadian Barn Swallow populations. Barn Swallow occupied consistently larger isotopic and wing length niche space than the other species. Comparisons among populations across species showed variable isotopic and wing-length niche overlap generally being greater within breeding regions and lower between western and eastern breeding populations supporting a general North American continental divide for all species with generally low migratory connectivity for all species. We present a novel approach to assessing connectivity using inexpensive and broad isotopic approaches that provides the basis for hypothesis testing using more spatially explicit expensive techniques.

Isotopic niche overlap between sympatric Australian snubfin and humpback dolphins.

Ecological niche theory predicts the coexistence of closely related species is promoted by resource partitioning in space and time. Australian snubfin (Orcaella heinsohni) and humpback (Sousa sahulensis) dolphins live in sympatry throughout most of their range in northern Australian waters. We compared stable isotope ratios of carbon (δ13C) and nitrogen (δ15N) in their skin to investigate resource partitioning between these ecologically similar species. Skin samples were collected from live Australian snubfin (n = 31) and humpback dolphins (n = 23) along the east coast of Queensland in 2014-2015. Both species had similar δ13C and δ15N values and high (>50%) isotopic niche space overlap, suggesting that they feed at similar trophic levels, have substantial dietary overlap, and rely on similar basal food resources. Despite similarities, snubfin dolphins were more likely to have a larger δ15N value than humpback dolphins, indicating they may forage on a wider diversity of prey. Humpback dolphins were more likely to have a larger δ13C range suggesting they may forage on a wider range of habitats. Overall, results suggest that subtle differences in habitat use and prey selection are likely the principal resource partitioning mechanisms enabling the coexistence of Australian snubfin and humpback dolphins.

Inter- and intra-specific trophic interactions of coastal delphinids off the eastern coast of South Africa inferred from stable isotope analysis.

Dietary tracers, such as bulk stable carbon (δ13C) and nitrogen (δ15N) isotopes, can be used to investigate the trophic interactions of marine predators, which is useful to assess their ecological roles within communities. These tracers have also been used to elucidate population structure and substructure, which is critical for the better identification of management units for these species affected by a range of threats, particularly bycatch in fishing gears. Off eastern South Africa, large populations of Indo-Pacific bottlenose (Tursiops aduncus) and common dolphins (Delphinus delphis) co-occur and are thought to follow the pulses of shoaling sardines (Sardinops sagax) heading north-east in the austral winter. Here we used δ13C and δ15N to investigate the trophic interactions and define ecological units of these two species along a ≈800 km stretch of the east coast of South Africa, from Algoa Bay to the coast of KwaZulu-Natal. Common and bottlenose dolphin dietary niche overlapped by 39.7% overall in our study area, with the highest overlap occurring off the Wild Coast (40.7% at Hluleka). Both stable isotopes were significantly enriched in bottlenose dolphins sampled in the western part of our study area (i.e., Algoa Bay and Amathole) compared to eastern animals (i.e., from Hluleka, Pondoland, and KZN). In areas where genetic information is not available or is insufficient, food web tracers (such as stable isotopes) can be used to group individuals based on trophic ecology, which can provide ecological units for management of populations. The distinct isotope signatures found here for bottlenose dolphins can, therefore, be used as management units for conservation efforts in the future.

Improving stable isotope assessments of inter- and intra-species variation in coral reef fish trophic strategies.

Fish have one of the highest occurrences of individual specialization in trophic strategies among Eukaryotes. Yet, few studies characterize this variation during trophic niche analysis, limiting our understanding of aquatic food web dynamics. Stable isotope analysis (SIA) with advanced Bayesian statistics is one way to incorporate this individual trophic variation when quantifying niche size. However, studies using SIA to investigate trophodynamics have mostly focused on species- or guild-level (i.e., assumed similar trophic strategy) analyses in settings where source isotopes are well-resolved. These parameters are uncommon in an ecological context. Here, we use Stable Isotope Bayesian Ellipses in R (SIBER) to investigate cross-guild trophodynamics of 11 reef fish species within an oceanic atoll. We compared two- (δ 15N and δ 13C) versus three-dimensional (δ 15N, δ 13C, and δ 34S) reconstructions of isotopic niche space for interpreting guild-, species-, and individual-level trophic strategies. Reef fish isotope compositions varied significantly among, but also within, guilds. Individuals of the same species did not cluster together based on their isotope values, suggesting within-species specializations. Furthermore, while two-dimensional isotopic niches helped differentiate reef fish resource use, niche overlap among species was exceptionally high. The addition of δ 34S and the generation of three-dimensional isotopic niches were needed to further characterize their isotopic niches and better evaluate potential trophic strategies. These data suggest that δ 34S may reveal fluctuations in resource availability, which are not detectable using only δ 15N and δ 13C. We recommend that researchers include δ 34S in future aquatic food web studies.

Fish isotopic niches associated with environmental indicators and human disturbance along a disturbed large subtropical river in China.

Stable isotopes are increasingly used to detect and understand the impacts of environmental changes on riverine ecological properties. The δ13C and δ15N signatures of fish with different feeding habits were measured in a large subtropical river to evaluate how fish isotopic niches respond to environmental gradients and human disturbance. From basal resources to fish consumers, the high values of epilithic periphyton (biofilm) δ13C and suspended particulate organic matter δ15N concurrently determined the niche ranges and space (e.g., convex hull area) of fish communities. Along a longitudinal gradient (except in the industrial zone), the number of fish trophic guilds identified by Bayesian ellipses continuously increased; meanwhile, higher trophic diversity and less redundancy were observed near the lower reaches and estuary. Variance inflation factors were estimated to detect the multicollinearity of 40 environmental variables, 14 of which were selected as indicators. Relative importance (RI) analysis was used to evaluate the explanatory power of these indicators for the spatial variation in isotopic niche metrics; the results showed that riffle habitat area, water nitrate concentration, gravel-cobble substrate, and riparian buffer width were the 4 key environmental indicators (average RI > 12%) that determined the longitudinal pattern of fish isotopic niches. These findings suggested that community-level δ13C signatures are more responsive to changes in habitats (e.g., riffle) and substrates (e.g., gravel-cobble) supporting the productivity of autochthonous diatoms while δ15N signatures respond to water quality altered by nitrogen pollution from manure-fertilized farming and poultry livestock effluent. Furthermore, δ15N may be more robust and interpretable than δ13C as an isotopic indicator of ecosystem change in rivers exposed to multiple or complex anthropogenic stressors.

Trophic Ecology of Endangered Gold-Spotted Pond Frog in Ecological Wetland Park and Rice Paddy Habitats.

The gold-spotted pond frog (Pelophylax chosenicus) is an endangered amphibian species in South Korea. In order to obtain ecological information regarding the gold-spotted pond frog's habitat environment and biological interactions, we applied stable isotope analysis to quantify the ecological niche space (ENS) of frogs including black-spotted pond frogs (P. nigromaculatus) and bullfrogs (Lithobates catesbeianus) within the food web of two different habitats-an ecological wetland park and a rice paddy. The gold-spotted pond frog population exhibited a broader ENS in the ecological wetland park than in the rice paddy. According to the carbon stable isotope ratios, gold-spotted pond frogs mainly fed on insects, regardless of habitat type. However, the results comparing the range of both carbon and nitrogen stable isotopes showed that gold-spotted pond frogs living in the rice paddy showed limited feeding behavior, while those living in the ecological wetland park fed on various food sources located in more varied trophic positions. Although the ENS of the gold-spotted pond frog was generally less likely to be overlapped by that of other frog species, it was predicted to overlap with a high probability of 87.3% in the ecological wetland park. Nevertheless, gold-spotted pond frogs in the ecological wetland park were not significantly affected by the prey competition with competitive species by feeding on other prey for which other species' preference was low. Since these results show that a habitats' food diversity has an effect on securing the ENS of gold-spotted pond frogs and prey competition, we recommend that the establishment of a food environment that considers the feeding behavior of gold-spotted pond frogs is important for the sustainable preservation of gold-spotted pond frogs and their settlement in alternative habitats.

Metapopulation dynamics and foraging plasticity in a highly vagile seabird, the southern rockhopper penguin.

Population connectivity is driven by individual dispersal potential and modulated by natal philopatry. In seabirds, high vagility facilitates dispersal yet philopatry is also common, with foraging area overlap often correlated with population connectivity. We assess the interplay between these processes by studying past and current connectivity and foraging niche overlap among southern rockhopper penguin colonies of the coast of southern South America using genomic and stable isotope analyses. We found two distinct genetic clusters and detected low admixture between northern and southern colonies. Stable isotope analysis indicated niche variability between colonies, with Malvinas/Falklands colonies encompassing the species entire isotopic foraging niche, while the remaining colonies had smaller, nonoverlapping niches. A recently founded colony in continental Patagonia differed in isotopic niche width and position with Malvinas/Falklands colonies, its genetically identified founder population, suggesting the exploitation of novel foraging areas and/or prey items. Additionally, dispersing individuals found dead across the Patagonian shore in an unusual mortality event were also assigned to the northern cluster, suggesting northern individuals reach southern localities, but do not breed in these colonies. Facilitated by variability in foraging strategies, and especially during unfavorable conditions, the number of dispersing individuals may increase and enhance the probability of founding new colonies. Metapopulation demographic dynamics in seabirds should account for interannual variability in dispersal behavior and pay special attention to extreme climatic events, classically related to negative effects on population trends.

The dynamic trophic niche of an island bird of prey.

Optimal foraging theory predicts an inverse relationship between the availability of preferred prey and niche width in animals. Moreover, when individuals within a population have identical prey preferences and preferred prey is scarce, a nested pattern of trophic niche is expected if opportunistic and selective individuals can be identified. Here, we examined intraspecific variation in the trophic niche of a resident population of striated caracara (Phalcoboenus australis) on Isla de los Estados (Staten Island), Argentina, using pellet and stable isotope analyses. While this raptor specializes on seabird prey, we assessed this population's potential to forage on terrestrial prey, especially invasive herbivores as carrion, when seabirds are less accessible. We found that the isotopic niche of this species varies with season, age, breeding status, and, to a lesser extent, year. Our results were in general consistent with classic predictions of the optimal foraging theory, but we also explore other possible explanations for the observed pattern. Isotopic niche was broader for groups identified a priori as opportunistic (i.e., nonbreeding adults during the breeding season and the whole population during the nonbreeding season) than it was for individuals identified a priori as selective. Results suggested that terrestrial input was relatively low, and invasive mammals accounted for no more than 5% of the input. The seasonal pulse of rockhopper penguins likely interacts with caracara's reproductive status by constraining the spatial scale on which individuals forage. Niche expansion in spatially flexible individuals did not reflect an increase in terrestrial prey input; rather, it may be driven by a greater variation in the types of marine prey items consumed.

Stable isotopes reveal effects of natural drivers and anthropogenic pressures on isotopic niches of invertebrate communities in a large subtropical river of China.

Isotopic niches reflect the basic structure and functioning of river food webs; however, their response to riverine environments remains unclear. We used stable isotope analysis and community-wide metrics to quantify how invertebrate niches vary with environmental changes along a large subtropical river in China. Eight niche metrics, which had higher values in the wet than in the dry season, increased from headwaters to the middle river and decreased sharply near the estuarine industrial zones. The δ13C value of > - 23.8‰, which indicated consumption of epilithic diatoms, separated the invertebrates between the upper and mid-lower reaches. The δ15N values > 9.4‰ identified site-specific nitrogen sources from manure (e.g., animal effluent) and domestic sewage in agricultural area. The output of mixing models showed a downstream shift in carbon utilization by invertebrates from autochthonous periphyton and submerged hydrophytes to allochthonous C3 plants. Principle component (PC) and cluster analysis decomposed and grouped 40 environmental variables into 4 PCs that explained 84.5% of the total variance. Hierarchical partitioning revealed that the second and first PCs, which were driven mainly by biological indicators and habitat characteristics, had the highest explanatory power for niche ranges and areas (e.g., Bayesian ellipse), respectively. Our results suggest that reducing anthropogenic pressures (e.g., habitat loss and water pollution) on river ecosystems through measures, such as protecting diatom-dominated biofilms in riffles and controlling nitrogen loading in rural regions, may produce the greatest impact for river management. Graphical abstract.

Ecological implications of purple sea urchin (Heliocidaris crassispina, Agassiz, 1864) enhancement on the coastal benthic food web: evidence from stable isotope analysis.

A responsible approach to marine stock enhancement is an effective approach to restore fishery resources. While the release strategy of target species has been well investigated, the impacts on local ecological equilibrium and habitat qualities have only been poorly considered. In the present study, we evaluated how the macro-benthic food web in Daya Bay was affected by purple sea urchin (Heliocidaris crassispina (Agassiz, 1864) stock enhancement using stable isotope analyses (δ13C and δ15N). Our results indicated that the distribution of local species and trophic diversity were influenced to a certain degree by release of purple sea urchins and changes in the feeding habit of the urchins were observed in line with food abundance, which seasonally varied. When food is abundant, the main food source of sea urchins was microphytobenthos and no significant differences were observed among sites; significant differences in the diet of purple sea urchins were detected when food is less abundant. These results suggested that optimization of the release strategy should include information on seasonal productivity of local recipient sites, food web structure and feeding habits of released species. Such information is essential for building a responsible release approach to maximize production enhancement.

A Linnaeus NG interactive key to the species of Glomera (Orchidaceae, Coelogyninae) from Southeast Asia.

We present a multilingual interactive key available online (http://glomera.linnaeus.naturalis.nl) that can be used on any web browser without the need for installing additional software. The key includes 169 species of Glomera, a genus within the necklace orchids (Coelogyninae) not yet comprehensively treated in any recent field guide or web-based survey. With this key, plants can be identified using a combination of vegetative and floristic characters in addition to distribution and ecology as a first step to further taxonomic revisions. We urge anyone with an interest in wild orchids in Southeast Asia to contribute new observations to update current information on the distribution of these overlooked plants as a first step for a taxonomic revision and to gain more insight into their conservation status.

Isotopic niches of fin whales from the Mediterranean Sea and the Celtic Sea (North Atlantic).

The fin whale (Balaenoptera physalus) is the most abundant and widespread mysticete species in the Mediterranean Sea, found mostly in deep, offshore waters of the western and central portion of the region. In the Mediterranean, this species is known to feed mainly on krill, in contrast to its Atlantic counterpart, which displays a more diversified diet. The International Whaling Commission recognizes several managements units in the Atlantic and the Mediterranean Sea and the connectivity between these populations is still being debated. Questions remain about inter-individual feeding strategies and trophic ecology. The goal of this study was to compare isotopic niches of fin whales from the Mediterranean Sea and the Celtic Sea (North Atlantic). δ13C and δ15N values were analysed in 136 skin biopsies from free-ranging Mediterranean fin whales sampled in 2010 and 2011 during campaigns at sea. δ13C and δ15N values ranged from -20.4 to -17.1‰ and from 5.9 to 8.9‰, respectively. These values are in good agreement with those estimated previously from baleen plates from Mediterranean and North Atlantic fin whales. The narrow isotopic niche width of the Mediterranean fin whale (Standard Ellipses area SEAc) compared to the North Atlantic fin whale raises many concerns in the context of global changes and long-term consequences. One could indeed expect that species displaying narrow niches would be more susceptible to ecosystem fragmentation and other anthropogenic impacts.