Diet variation in a critically endangered marine predator revealed with stable isotope analysis.

Understanding the foraging ecology of animals gives insights into their trophic relationships and habitat use. We used stable isotope analysis to understand the foraging ecology of a critically endangered marine predator, the Maui dolphin. We analysed carbon and nitrogen isotope ratios of skin samples (n = 101) collected from 1993 to 2021 to investigate temporal changes in diet and niche space. Genetic monitoring associated each sample with a DNA profile which allowed us to assess individual and population level changes in diet. Potential prey and trophic level indicator samples were also collected (n = 166; 15 species) and incorporated in Bayesian mixing models to estimate importance of prey types to Maui dolphin diet. We found isotopic niche space had decreased over time, particularly since the 2008 implementation of a Marine Mammal Sanctuary. We observed a decreasing trend in ∂13C and ∂15N values, but this was not linear and several fluctuations in isotope values occurred over time. The largest variation in isotope values occurred during an El Niño event, suggesting that prey is influenced by climate-driven oceanographic variables. Mixing models indicated relative importance of prey remained constant since 2008. The isotopic variability observed here is not consistent with individual specialization, rather it occurs at the population level.

Trophic Dynamics and Feeding Ecology of Skipjack Tuna (Katsuwonus pelamis) off Eastern and Western Taiwan.

The skipjack tuna (Katsuwonus pelamis) is a mesopredator fish species with seasonal abundance in waters off Taiwan. Regional ecological and life-history information has been historically lacking for this species. In recent years, stable isotope analysis (SIA) of carbon and nitrogen has been used to assess predator feeding ecology and broader ecosystem trophic dynamics. This study evaluated comparative skipjack feeding ecology in distinct regions off Taiwan, combining traditional stomach content analysis with SIA of individuals off western (n = 43; 2020) and eastern (n = 347; 2012-2014 and n = 167; 2020) Taiwan. The stomach content analysis showed the most important prey to be ponyfish (Photopectoralis bindus) in western Taiwan and epipelagic squids (Myopsina spp.) and carangids (Decapterus macrosoma;) in eastern Taiwan from 2012 to 2014 and epipelagic carangids (Decapterus spp.) and flying fishes (Cheilopogon spp.) in eastern Taiwan in 2020, suggesting that the skipjack tuna is a generalist predator across regions. In contrast, time-integrated diet estimates from Bayesian mixing models indicated the importance of cephalopods and crustaceans as prey, potentially demonstrating more mesopelagic feeding in less productive waters during skipjack migrations outside the study regions. Skipjack off western Taiwan had a slightly higher estimated trophic position than in the waters off eastern Taiwan, potentially driven by the varying nutrient-driven pelagic food web structures. Skipjack SI values increased with body size off eastern Taiwan but not in western waters, suggesting that opportunistic predation can still result in different predator-prey size dynamics between regions.

Refining trophic dynamics through multi-factor Bayesian mixing models: A case study of subterranean beetles.

Food web dynamics are vital in shaping the functional ecology of ecosystems. However, trophic ecology is still in its infancy in groundwater ecosystems due to the cryptic nature of these environments. To unravel trophic interactions between subterranean biota, we applied an interdisciplinary Bayesian mixing model design (multi-factor BMM) based on the integration of faunal C and N bulk tissue stable isotope data (δ13C and δ15N) with radiocarbon data (Δ14C), and prior information from metagenomic analyses. We further compared outcomes from multi-factor BMM with a conventional isotope double proxy mixing model (SIA BMM), triple proxy (δ13C, δ15N, and Δ14C, multi-proxy BMM), and double proxy combined with DNA prior information (SIA + DNA BMM) designs. Three species of subterranean beetles (Paroster macrosturtensis, Paroster mesosturtensis, and Paroster microsturtensis) and their main prey items Chiltoniidae amphipods (AM1: Scutachiltonia axfordi and AM2: Yilgarniella sturtensis), cyclopoids and harpacticoids from a calcrete in Western Australia were targeted. Diet estimations from stable isotope only models (SIA BMM) indicated homogeneous patterns with modest preferences for amphipods as prey items. Multi-proxy BMM suggested increased-and species-specific-predatory pressures on amphipods coupled with high rates of scavenging/predation on sister species. SIA + DNA BMM showed marked preferences for amphipods AM1 and AM2, and reduced interspecific scavenging/predation on Paroster species. Multi-factorial BMM revealed the most precise estimations (lower overall SD and very marginal beetles' interspecific interactions), indicating consistent preferences for amphipods AM1 in all the beetles' diets. Incorporation of genetic priors allowed crucial refining of the feeding preferences, while integration of more expensive radiocarbon data as a third proxy (when combined with genetic data) produced more precise outcomes but close dietary reconstruction to that from SIA + DNA BMM. Further multidisciplinary modeling from other groundwater environments will help elucidate the potential behind these designs and bring light to the feeding ecology of one the most vital ecosystems worldwide.

Stable-isotope analysis reveals sources of organic matter and ontogenic feeding shifts of a mangrove-dependent predator species, New Granada sea catfish, Ariopsis canteri.

To gain a better understanding on the trophic ecology of New Granada sea catfish, Ariopsis canteri, and their linkage to mangroves, nitrogen and stable carbon isotopes (δ15 N and δ13 C), as well as Bayesian mixing models, were used to explore trophic dynamics and potential ontogenic feeding shifts across different size classes: class I (8-20 cm), class II (21-32 cm) and class III (>32 cm). The study area was the estuary of the Atrato River Delta, where information about fish ecology is scarce. The δ13 C of size class I was lower (mean ± s.d. = -24.96 ± 0.69‰) than that of size classes II (-22.20 ± 0.90‰) and III (-22.00 ± 1.96‰). The δ15 N of size class I was lower (mean ± s.d. = 8.50 ± 0.67‰) than that of size classes II (9.77 ± 0.60‰) and III (10.00 ± 0.66‰). Body size was positively and significantly correlated to δ15 N and δ13 C. Individuals with LT > 32 cm presented the highest estimated trophic position (3.8). Five-source mixing models indicated that for class I, the mean estimated contribution of macroalgae was the highest (6%-57% c.i.), and for classes II and III, the mean estimated contribution of macrophytes was the highest (3%-53% c.i. and 4%-53% c.i., respectively). Ontogenetic feeding shifts of A. canteri were confirmed evidencing decreasing intraspecific competition between small and large individuals. Results suggest that mangroves are a nursery and feeding ground habitat for this species and that mangroves support A. canteri mainly due to the substrate/habitat that supports sources in the food webs. These results can be used in ecosystem-based fishery management focused on the protection of extensive mangrove areas in the southern Caribbean Sea.

Determining tributary sources of increased sedimentation in East-African Rift Lakes.

Temporal and spatial sediment dynamics in an East-African Rift Lake (Lake Manyara, Tanzania), and its river inputs, have been evaluated via a combination of sediment tracing and radioactive dating. Changes in sedimentation rates were assessed using radioactive dating of sediment cores in combination with geochemical profile analysis of allogenic and autogenic elements. Geochemical fingerprinting of riverine and lake sediment was integrated within a Bayesian mixing model framework, including spatial factors, to establish which tributary sources were the main contributors to recent lake sedimentation. The novel application of Bayesian source attribution on sediment cores and subsequent integration with sedimentation data permitted the coupling of changes in the rate of lake sedimentation with variations in sediment delivery from the tributaries. These complimentary evidence bases demonstrated that Lake Manyara has experienced an overall upward trajectory in sedimentation rates over the last 120 years with distinct maxima between 0.80 and 0.85 g cm-2 yr-1 in the 1960s and between 0.84 and 1.81 g cm-2 yr-1 in 2010. Increased sedimentation rates are largely a result of a complex interaction between increased upstream sediment delivery following changes in land cover and natural rainfall fluctuations. Modelling results identified two specific tributaries as responsible for elevated sedimentation rates, contributing 58% and 38% of the recently deposited lake sediment. However, the effects of sedimentation were shown to be spatially distinct given the domination of different tributaries in various areas of Lake Manyara. The application of source-tracing techniques constrained sedimentation problems in Lake Manyara to specific tributary sources and established a link between upstream land degradation and downstream ecosystem health. This novel application provides a solid foundation for targeted land and water management strategies to safeguard water security and environmental health in Lake Manyara and has potential application to fill knowledge gaps on sediment dynamics in other East-African Rift Lakes.

New light in the dark - a proposed multidisciplinary framework for studying functional ecology of groundwater fauna.

Groundwaters provide the vast majority of unfrozen freshwater resources on the planet, but our knowledge of subsurface ecosystems is surprisingly limited. Stygofauna, or stygobionts -subterranean obligate aquatic animals - provide ecosystem services such as grazing biofilms and maintaining water quality, but we know little about how their ecosystems function. The cryptic nature of groundwaters, together with the high degree of local endemism and stygofaunal site-specific adaptations, represent major obstacles for the field. To overcome these challenges, and integrate biodiversity and ecosystem function, requires a holistic design drawing on classical ecology, taxonomy, molecular ecology and geochemistry. This study presents an approach based on the integration of existing concepts in groundwater ecology with three more novel scientific techniques: compound specific stable isotope analysis (CSIA) of amino acids, radiocarbon analysis (14C) and DNA analyses of environmental samples, stygofauna and gut contents. The combination of these techniques allows elucidation of aspects of ecosystem function that are often obscured in small invertebrates and cryptic systems. Carbon (δ13C) and nitrogen (δ15N) CSIA provides a linkage between biogeochemical patterns and ecological dynamics. It allows the identification of stygofaunal food web structures and energy flows based on the metabolic pathway of specific amino groups. Concurrently, 14C provides complementary data on the carbon recycling and incorporation within the stygobiotic trophic webs. Changes in groundwater environmental conditions (e.g. aquifer recharge), and subsequent community adaptations, can be pinpointed via the measurementof the radiocarbon fingerprint of water, sediment and specimens. DNA analyses are a rapidly expanding approach in ecology. eDNA is mainly employed as a biomonitoring tool, while metabarcoding of individuals and/or gut contents provides insight into diet regimes. In all cases, the application of the approaches in combination provides more powerful data than any one alone. By combining quantitative (CSIA and 14C) and qualitative (eDNA and DNA metabarcoding) approaches via Bayesian Mixing Models (BMM), linkages can be made between community composition, energy and nutrient sources in the system, and trophic function. This suggested multidisciplinary design will contribute to a more thorough comprehension of the biogeochemical and ecological patterns within these undervalued but essential ecosystems.

Does food partitioning vary in leaf-eating crabs in response to source quality?

Mangroves have a relevant ecosystem function due to their efficiency in blue carbon sequestration. Autotrophic carbon conservation in mangroves remains controversial. In this sense, autotrophic nutrient assimilation by crabs can highlight their ecosystem function. This study aims to identify the relationship between quality sources and food partitioning in two leaf-eating crabs, Ucides cordatus and Goniopsis cruentata. Quantification of the litterfall biomass, analysis of the soil, the C/N ratio and stable isotopes (δ13C and δ15N) were used to evaluate food sources and crab tissues in two mangrove forests. The litterfall and soil C contents and C/N ratios of the Pacoti River (PR) were higher than those of the Jaguaribe River. The higher C/N ratios of the litterfall of the PR led to higher nitrogen ingestion from complementary food sources (soil and omnivorous invertebrates). The nutritional requirements and food partitioning behavior of both species emphasize the ecosystem functions of leaf-eating crabs concerning the assimilation and conservation of autotrophic carbon and nitrogen in mangroves.

Unexpected dietary preferences of Eurasian Spoonbills in the Dutch Wadden Sea: spoonbills mainly feed on small fish not shrimp.

After an historical absence, over the last decades Eurasian Spoonbills Platalea leucorodia leucorodia have returned to breed on the barrier islands of the Wadden Sea. The area offers an abundance of predator-free nesting habitat, low degrees of disturbance, and an extensive intertidal feeding area with increasing stocks of brown shrimp Crangon crangon, the assumed main prey of P. leucorodia leucorodia. Nevertheless, newly established and expanding colonies of spoonbills have surprisingly quickly reached plateau levels. Here we tested the often stated assertion that spoonbills mainly rely on brown shrimp as food, by quantifying the diet of chicks on the basis of regurgitates and by analysis of blood isotopes using stable isotope Bayesian mixing models. Both methods showed that, rather than brown shrimp being the staple food of spoonbill chicks, small flatfish (especially plaice Pleuronectes platessa) and gobies (Pomatoschistus spp.) were their main prey. Unlike shrimp, small flatfish have been reported to be rather scarce in the Wadden Sea in recent years, which may explain the rapid saturation of colony size due to food-related density-dependent recruitment declines of growing colonies. By way of their diet and colony growth characteristics, spoonbills may thus indicate the availability of small fish in the Wadden Sea. We predict that the recovery to former densities of young flatfish and other juvenile/small fish in the Wadden Sea will be tracked by changing diets (more fish) and an increase in the size of Eurasian Spoonbill colonies across the Wadden Sea.

Understanding trophic relationships among Caribbean sea urchins

ResumenLas especies Echinometra lucunter, Echinometra viridis, Lytechinus variegatus, Tripneustes ventricosus, and Diadema antillarum son los erizos de mar más comunes en los hábitat litorales del Caribe. Los erizos de mar T. ventricosus y L. variegatus habitan generalmente los pastos marinos mientras que las otras tres especies se encuentran asociadas a sustratos rocosos. Los hábitos alimentarios de estas especies han sido bien documentados y son reconocidas como herbívoros - omnívoros; sin embargo, pocas de estas especies han sido caracterizadas isotópicamente. Utilizamos los isótopos estables para caracterizar estas cinco especies de erizos y establecer las posiciones tróficas para las especies que cohabitan los mismos ecosistemas. También cuantificamos la contribución de los recursos alimentarios para E. lucunter. Los erizos T. ventricosus y D. antillarum mostraron los mayores valores de δ15N y valores similares de δ13C que variaron desde -11.6 ± 0.63 a -10.4 ± 0.99 %; donde el erizo E. lucunter mostró los valores más negativos con -15.40 ± 0.76 %. Las comunidades de algas no mostraron diferencias en valores promedio de δ15N (F= 1.300, df= 3, p= 0.301), pero sí mostraron variaciones en los valores de δ13C (F= 7.410, df= 3, p= 0.001). Los estudios de amplitud de elipses de nicho determinaron que las especies de los biotopos rocosos (D. antillarum, E. lucunter y E. viridis) no mostraron solapamiento de nicho. Similar resultado también se encontró en las especies de erizos que habitan en los pastos marinos. Sin embargo, la distancia entre estas dos especies fue menor respecto a la distancia entre las especies de erizos que habitan en los sustratos rocosos. Nuestros resultados muestran que las especies que habitan en los pastos marinos mostraron valores más elevados de δ13C en comparación con las especies de los sustratos rocosos. No se encontraron diferencias espaciales para E. lucunter en δ15N, pero sí en δ13C. Los modelos de mezcla bayesianos demuestran la plasticidad alimentaria de E. lucunter, especie capaz de utilizar múltiples recursos algales dependiendo de la disponibilidad por sitio. Semejanzas en δ15N entre D. antillarum y T. ventricosus parecen indicar similitudes tróficas entre ambas especies. Si bien T. ventricosus es reconocido como omnívoro, D. antillarum siempre ha sido considerado un herbívoro generalista. Finalmente, la falta de solapamiento entre las especies en los dos biotopos parece indicar una estrategia de partición de recursos para evitar la competencia de nicho entre especies concurrentes.

AbstractThe species Echinometra lucunter, Echinometra viridis, Lytechinus variegatus, Tripneustes ventricosus, and Diadema antillarum are the most common sea urchins of littoral habitats in the Caribbean. T. ventricosus and L. variegatus are associated with seagrass beds, while the other three species usually inhabit hardground substrates. Food preferences of these species are well documented and they are commonly accepted as being primarily herbivorous-omnivorous; nevertheless, few of them have previously been characterized isotopically. We used this approach for assessing the isotopic characterization of five echinoids. We established the trophic position of two groups of co-occurring species and quantified the contribution of food resources in the diet of Echinometra lucunter, considered the most common sea urchin in the Caribbean region. The species T. ventricosus and D. antillarum showed the highest values of δ15N. Sea urchins exhibited similar values of δ13C varying from -11.6 ± 0.63 to -10.4 ± 0.99%. The echinoid E. lucunter displayed the lowest values of carbon, from -15.40 ± 0.76%. Significant differences among species were found for δ15N and δ13C. Seaweed communities exhibited no differences among sites for overall δ15N (F= 1.300, df= 3, p= 0.301), but we found spatial differences for δ13C (F= 7.410, df= 3, p= 0.001). The ellipse-based metrics of niche width analysis found that the hardground biotope species (D. antillarum, E. lucunter, and E. viridis) did not overlap each other. Similar results were obtained for the co-occurring species of the seagrass biotope; however, the distance between these species was closer than that of the hardground biotope species. The Bayesian mixing models run for E. lucunter at all four localities found differences in food resources contribution. The algae D. menstrualis, C. crassa and B. triquetrum dominated in CGD; whereas C. nitens, Gracilaria spp., and D. caribaea represented the main contributor algae to the diet of E. lucunter at LQY. In Culebra Island, no dominance of any particular algae was detected in TMD, where six of the eight species exhibited a similar contribution. Similarities in δ15N between D. antillarum and T. ventricosus may hint towards a similar trophic level for these species, although T. ventricosus is widely accepted as an omnivore, while D. antillarum is considered a generalist herbivore. The lack of overlap among species in the two biotopes seems to indicate a resource partitioning strategy to avoid niche competition among co-occurring species. Rev. Biol. Trop. 64 (2): 837-848. Epub 2016 June 01.

High variability in stable isotope diet-tissue discrimination factors of two omnivorous freshwater fishes in controlled ex situ conditions.

Diet-tissue discrimination factors (Δ(13)C and Δ(15)N) are influenced by variables including the tissues being analysed and the taxon of the consumer and its prey. Whilst differences in Δ(13)C and Δ(15)N are apparent between herbivorous and piscivorous fishes, there is less known for omnivorous fishes that consume plant and animal material. Here, the omnivorous cyprinid fishes Barbus barbus and Squalius cephalus were held in tank aquaria and exposed to three diets that varied in their constituents (plant based to fishmeal based) and protein content (13% to 45%). After 100 days and isotopic replacement in fish tissues to 98%, samples of the food items, and dorsal muscle, fin tissue and scales were analysed for δ(13)C and δ(15)N. For both species and all diets, muscle was always enriched in δ(15)N and depleted in δ(13)C compared with fin tissue and scales. Across the different diets, Δ(13)C ranged between 2.0‰ and 5.6‰ and Δ(15)N ranged between 2.0‰ and 6.9‰. The diet based on plant material (20% protein) always resulted in the highest discrimination factors for each tissue, whilst the diet based on fishmeal (45% protein) consistently resulted in the lowest. The discrimination factors produced by non-fish diets were comparatively high compared with values in the literature, but were consistent with general patterns for some herbivorous fishes. These outputs suggest that the diet-tissue discrimination factors of omnivorous fishes will vary considerably between animal and plant prey, and these specific differences need consideration in predictions of their diet composition and trophic position.

Unravelling the role of allochthonous aquatic resources to food web structure in a tropical riparian forest.

The role of matter and energy flow across ecosystem boundaries for the subsidized consumer populations is well known. However, little is known on the effects of allochthonous subsidies on food web structure and trophic niche dimensions of consumers in the tropics. We excluded allochthonous aquatic insects from tropical streams using greenhouse-type exclosures to test the influence of aquatic allochthonous subsidies on the trophic structure and niche dimensions of terrestrial predators using stable isotope methods. In exclosure treatments, abundance and biomass of terrestrial predators, and biomass of phytophages decreased and increased, respectively. Vegetation-living predators were more responsive to allochthonous inputs than those living on the ground. Overall, lower availability of allochthonous inputs did not affect community-wide metrics and niche width of predators. However, the niche width of some spider families had very low overlap between treatments, and others had wider isotopic niches in the control than in the exclusion treatment. Most of the C and N in predators living in control stretches came from aquatic subsidies, and those predators living in the exclusion treatments switched their diets to terrestrial sources, showing a preference of predators for allochthonous subsidies. Our results suggest that allochthonous subsidies are also relevant to tropical fauna living upon vegetation. Moreover, allochthonous resources may amplify the niche dimension of certain predators or considerably change the trophic niche of others. Our study highlights the importance of including modern isotopic tools in elucidating the role of allochthonous resources on the patterns of trophic structure and niche dimensions of consumers from donor ecosystems.