Distinct evolutionary lineages of Schistocephalus parasites infecting co-occurring sculpin and stickleback fishes in Alaska.

Sculpins (coastrange and slimy) and sticklebacks (ninespine and threespine) are widely distributed fishes cohabiting 2 south-central Alaskan lakes (Aleknagik and Iliamna), and all these species are parasitized by cryptic diphyllobothriidean cestodes in the genus Schistocephalus. The goal of this investigation was to test for host-specific parasitic relationships between sculpins and sticklebacks based upon morphological traits (segment counts) and sequence variation across the NADH1 gene. A total of 446 plerocercoids was examined. Large, significant differences in mean segment counts were found between cestodes in sculpin (mean = 112; standard deviation [s.d.] = 15) and stickleback (mean = 86; s.d. = 9) hosts within and between lakes. Nucleotide sequence divergence between parasites from sculpin and stickleback hosts was 20.5%, and Bayesian phylogenetic analysis recovered 2 well-supported clades of cestodes reflecting intermediate host family (i.e. sculpin, Cottidae vs stickleback, Gasterosteidae). Our findings point to the presence of a distinct lineage of cryptic Schistocephalus in sculpins from Aleknagik and Iliamna lakes that warrants further investigation to determine appropriate evolutionary and taxonomic recognition.

Linking vertical movements of large pelagic predators with distribution patterns of biomass in the open ocean.

Many predator species make regular excursions from near-surface waters to the twilight (200 to 1,000 m) and midnight (1,000 to 3,000 m) zones of the deep pelagic ocean. While the occurrence of significant vertical movements into the deep ocean has evolved independently across taxonomic groups, the functional role(s) and ecological significance of these movements remain poorly understood. Here, we integrate results from satellite tagging efforts with model predictions of deep prey layers in the North Atlantic Ocean to determine whether prey distributions are correlated with vertical habitat use across 12 species of predators. Using 3D movement data for 344 individuals who traversed nearly 1.5 million km of pelagic ocean in [Formula: see text]42,000 d, we found that nearly every tagged predator frequented the twilight zone and many made regular trips to the midnight zone. Using a predictive model, we found clear alignment of predator depth use with the expected location of deep pelagic prey for at least half of the predator species. We compared high-resolution predator data with shipboard acoustics and selected representative matches that highlight the opportunities and challenges in the analysis and synthesis of these data. While not all observed behavior was consistent with estimated prey availability at depth, our results suggest that deep pelagic biomass likely has high ecological value for a suite of commercially important predators in the open ocean. Careful consideration of the disruption to ecosystem services provided by pelagic food webs is needed before the potential costs and benefits of proceeding with extractive activities in the deep ocean can be evaluated.

A shallow scattering layer structures the energy seascape of an open ocean predator.

Large predators frequent the open ocean where subsurface light drives visually based trophic interactions. However, we lack knowledge on how predators achieve energy balance in the unproductive open ocean where prey biomass is minimal in well-lit surface waters but high in dim midwaters in the form of scattering layers. We use an interdisciplinary approach to assess how the bioenergetics of scattering layer forays by a model predator vary across biomes. We show that the mean metabolic cost rate of daytime deep foraging dives to scattering layers decreases as much as 26% from coastal to pelagic biomes. The more favorable energetics offshore are enabled by the addition of a shallow scattering layer that, if not present, would otherwise necessitate costlier dives to deeper layers. The unprecedented importance of this shallow scattering layer challenges assumptions that the globally ubiquitous primary deep scattering layer constitutes the only mesopelagic resource regularly targeted by apex predators.

Widespread habitat loss and redistribution of marine top predators in a changing ocean.

The Northwest Atlantic Ocean and Gulf of Mexico are among the fastest warming ocean regions, a trend that is expected to continue through this century with far-reaching implications for marine ecosystems. We examine the distribution of 12 highly migratory top predator species using predictive models and project expected habitat changes using downscaled climate models. Our models predict widespread losses of suitable habitat for most species, concurrent with substantial northward displacement of core habitats >500 km. These changes include up to >70% loss of suitable habitat area for some commercially and ecologically important species. We also identify predicted hot spots of multi-species habitat loss focused offshore of the U.S. Southeast and Mid-Atlantic coasts. For several species, the predicted changes are already underway, which are likely to have substantial impacts on the efficacy of static regulatory frameworks used to manage highly migratory species. The ongoing and projected effects of climate change highlight the urgent need to adaptively and proactively manage dynamic marine ecosystems.

Building use-inspired species distribution models: Using multiple data types to examine and improve model performance.

Species distribution models (SDMs) are becoming an important tool for marine conservation and management. Yet while there is an increasing diversity and volume of marine biodiversity data for training SDMs, little practical guidance is available on how to leverage distinct data types to build robust models. We explored the effect of different data types on the fit, performance and predictive ability of SDMs by comparing models trained with four data types for a heavily exploited pelagic fish, the blue shark (Prionace glauca), in the Northwest Atlantic: two fishery dependent (conventional mark-recapture tags, fisheries observer records) and two fishery independent (satellite-linked electronic tags, pop-up archival tags). We found that all four data types can result in robust models, but differences among spatial predictions highlighted the need to consider ecological realism in model selection and interpretation regardless of data type. Differences among models were primarily attributed to biases in how each data type, and the associated representation of absences, sampled the environment and summarized the resulting species distributions. Outputs from model ensembles and a model trained on all pooled data both proved effective for combining inferences across data types and provided more ecologically realistic predictions than individual models. Our results provide valuable guidance for practitioners developing SDMs. With increasing access to diverse data sources, future work should further develop truly integrative modeling approaches that can explicitly leverage the strengths of individual data types while statistically accounting for limitations, such as sampling biases.

An enigmatic pelagic fish with internalized red muscle: A future regional endotherm or forever an ectotherm?

Ectothermy and endothermy in extant fishes are defined by distinct integrated suites of characters. Although only ⁓0.1% of fishes are known to have endothermic capacity, recent discoveries suggest that there may still be uncommon pelagic fish species with yet to be discovered endothermic traits. Among the most rarely encountered marine fishes, the louvar Luvarus imperialis is a remarkable example of adaptive evolution as the only extant pelagic species in the order Acanthuriformes (including surgeonfishes, tangs, unicornfishes and Moorish idol). Magnetic resonance imaging and gross necropsy did not yield evidence of cranial or visceral endothermy but revealed a central-posterior distribution of myotomal red muscle that is a mixture of the character states typifying ectotherms (lateral-posterior) and red muscle endotherms (central-anterior). Dissection of a specimen confirmed, and an osteological proxy supported, that L. imperialis has not evolved the vascular rete that is vital to retaining heat in the red muscle. The combination of presumably relying on caudal propulsion while exhibiting internal red muscle without associated retia is unique to L. imperialis among all extant fishes, raising the macroevolutionary question of whether this species - in geologic timescales - will remain an ectotherm or evolve red muscle endothermy.

Anticyclonic eddies aggregate pelagic predators in a subtropical gyre.

Ocean eddies are coherent, rotating features that can modulate pelagic ecosystems across many trophic levels. These mesoscale features, which are ubiquitous at mid-latitudes1, may increase productivity of nutrient-poor regions2,3, accumulate prey4 and modulate habitat conditions in the water column5. However, in nutrient-poor subtropical gyres-the largest marine biome-the role of eddies in modulating behaviour throughout the pelagic predator community remains unknown despite predictions for these gyres to expand6 and pelagic predators to become increasingly important for food security7. Using a large-scale fishery dataset in the North Pacific Subtropical Gyre, we show a pervasive pattern of increased pelagic predator catch inside anticyclonic eddies relative to cyclones and non-eddy areas. Our results indicate that increased mesopelagic prey abundance in anticyclone cores4,8 may be attracting diverse predators, forming ecological hotspots where these predators aggregate and exhibit increased abundance. In this energetically quiescent gyre, we expect that isolated mesoscale features (and the habitat conditions in them) exhibit primacy over peripheral submesoscale dynamics in structuring the foraging opportunities of pelagic predators. Our finding that eddies influence coupling of epi- to mesopelagic communities corroborates the growing evidence that deep scattering layer organisms are vital prey for a suite of commercially important predator species9 and, thus, provide valuable ecosystem services.

The Functional and Ecological Significance of Deep Diving by Large Marine Predators.

Many large marine predators make excursions from surface waters to the deep ocean below 200 m. Moreover, the ability to access meso- and bathypelagic habitats has evolved independently across marine mammals, reptiles, birds, teleost fishes, and elasmobranchs. Theoretical and empirical evidence suggests a number of plausible functional hypotheses for deep-diving behavior. Developing ways to test among these hypotheses will, however, require new ways to quantify animal behavior and biophysical oceanographic processes at coherent spatiotemporal scales. Current knowledge gaps include quantifying ecological links between surface waters and mesopelagic habitats and the value of ecosystem services provided by biomass in the ocean twilight zone. Growing pressure for ocean twilight zone fisheries creates an urgent need to understand the importance of the deep pelagic ocean to large marine predators.

Does lipid-correction introduce biases into isotopic mixing models? Implications for diet reconstruction studies.

Carbon isotopes are commonly used in trophic ecology to estimate consumer diet composition. This estimation is complicated by the fact that lipids exhibit a more depleted carbon signature (δ13C) than other macromolecules, and are often found at different concentrations among individual organisms. Some researchers argue that lipids bias diet reconstructions using stable isotopes and should be accounted for prior to analysis in food web mixing models, whereas others contend that removing lipids may result in erroneous interpretations of the trophic interactions under study. To highlight this disagreement on best practices for applying δ13C in food web studies, we sampled the recent literature to determine the frequency and method of lipid-correction. We then quantified the potential magnitude and source of bias in mixing model results from a theoretical example and case study of diet reconstruction. The literature was split nearly evenly as to whether lipid-correction was applied to δ13C data in mixing model estimates of diet composition. Comparative mixing model scenarios demonstrated that lipid-correction can substantially alter the estimated diet composition and interpretation of consumer foraging habits. Given the lack of consensus on whether or not to lipid-correct prey and/or consumers, and the associated variation in mixing model results, we call for the establishment of a unified framework that will guide diet reconstruction in stable isotope ecology. Uncertainty in the prevalence of direct routing versus de novo synthesis of lipids across ecosystems, taxa, and trophic levels must be resolved to better guide treatment of lipids in isotope studies using carbon.

Retention of a chromosomal inversion from an anadromous ancestor provides the genetic basis for alternative freshwater ecotypes in rainbow trout.

Migratory behaviour patterns in animals are controlled by a complex genetic architecture. Rainbow trout (Oncorhynchus mykiss) is a salmonid fish that spawns in streams but exhibits three primary life history pathways: stream-resident (fluvial), lake-migrant (adfluvial) and ocean-migrant (anadromous). Previous studies examining fluvial and anadromous O. mykiss have identified several genes associated with life history divergence including the presence of an inversion complex within chromosome 5 (Omy05) that appears to maintain a suite of linked genes controlling migratory behaviour. However, adfluvial trout are migratory without being anadromous, and the genetic basis for this life history has not been investigated from evolutionary perspectives. We sampled wild, native nonanadromous rainbow trout occupying connected stream and lake habitats in a southwest Alaskan watershed to determine whether these fish exhibit genetic divergence between fluvial and adfluvial ecotypes, and whether that divergence parallels that documented in fluvial and anadromous O. mykiss. Data from restriction site-associated DNA (RAD) sequencing revealed an association between frequencies of both the Omy05 inversion complex and other single nucleotide polymorphisms (SNPs) with habitat type (stream or lake), supporting the genetic divergence of fluvial and adfluvial individuals in sympatry. The presence of a genetic basis for migration into lakes, analogous to that documented for anadromy, indicates that the adfluvial ecotype must be recognized separately from the fluvial form of O. mykiss even though neither is anadromous. These results highlight the genetic architecture underlying migration and the importance of chromosomal inversions in promoting and sustaining intraspecific diversity.

Potential Biological Control of Schistosomiasis by Fishes in the Lower Senegal River Basin.

More than 200 million people in sub-Saharan Africa are infected with schistosome parasites. Transmission of schistosomiasis occurs when people come into contact with larval schistosomes emitted from freshwater snails in the aquatic environment. Thus, controlling snails through augmenting or restoring their natural enemies, such as native predators and competitors, could offer sustainable control for this human disease. Fishes may reduce schistosomiasis transmission directly, by preying on snails or parasites, or indirectly, by competing with snails for food or by reducing availability of macrophyte habitat (i.e., aquatic plants) where snails feed and reproduce. To identify fishes that might serve as native biological control agents for schistosomiasis in the lower Senegal River basin-one of the highest transmission areas for human schistosomiasis globally-we surveyed the freshwater fish that inhabit shallow, nearshore habitats and conducted multivariate analyses with quantitative diet data for each of the fish species encountered. Ten of the 16 fish species we encountered exhibited diets that may result in direct (predation) and/or indirect (food competition and habitat removal) control of snails. Fish abundance was low, suggesting limited effects on schistosomiasis transmission by the contemporary fish community in the lower Senegal River basin in the wild. Here, we highlight some native species-such as tilapia, West African lungfish, and freshwater prawns-that could be aquacultured for local-scale biological control of schistosomiasis transmission.