Accounting for unobserved population dynamics and aging error in close-kin mark-recapture assessments.

Obtaining robust estimates of population abundance is a central challenge hindering the conservation and management of many threatened and exploited species. Close-kin mark-recapture (CKMR) is a genetics-based approach that has strong potential to improve the monitoring of data-limited species by enabling estimates of abundance, survival, and other parameters for populations that are challenging to assess. However, CKMR models have received limited sensitivity testing under realistic population dynamics and sampling scenarios, impeding the application of the method in population monitoring programs and stock assessments. Here, we use individual-based simulation to examine how unmodeled population dynamics and aging uncertainty affect the accuracy and precision of CKMR parameter estimates under different sampling strategies. We then present adapted models that correct the biases that arise from model misspecification. Our results demonstrate that a simple base-case CKMR model produces robust estimates of population abundance with stable populations that breed annually; however, if a population trend or non-annual breeding dynamics are present, or if year-specific estimates of abundance are desired, a more complex CKMR model must be constructed. In addition, we show that CKMR can generate reliable abundance estimates for adults from a variety of sampling strategies, including juvenile-focused sampling where adults are never directly observed (and aging error is minimal). Finally, we apply a CKMR model that has been adapted for population growth and intermittent breeding to two decades of genetic data from juvenile lemon sharks (Negaprion brevirostris) in Bimini, Bahamas, to demonstrate how application of CKMR to samples drawn solely from juveniles can contribute to monitoring efforts for highly mobile populations. Overall, this study expands our understanding of the biological factors and sampling decisions that cause bias in CKMR models, identifies key areas for future inquiry, and provides recommendations that can aid biologists in planning and implementing an effective CKMR study, particularly for long-lived data-limited species.

Lateral line ablation by ototoxic compounds results in distinct rheotaxis profiles in larval zebrafish.

The zebrafish lateral line is an established model for hair cell organ damage, yet few studies link mechanistic disruptions to changes in biologically relevant behavior. We used larval zebrafish to determine how damage via ototoxic compounds impact rheotaxis. Larvae were treated with CuSO4 or neomycin to disrupt lateral line function then exposed to water flow stimuli. Their swimming behavior was recorded on video then DeepLabCut and SimBA software were used to track movements and classify rheotaxis behavior, respectively. Lateral line-disrupted fish performed rheotaxis, but they swam greater distances, for shorter durations, and with greater angular variance than controls. Furthermore, spectral decomposition analyses confirmed that lesioned fish exhibited ototoxic compound-specific behavioral profiles with distinct changes in the magnitude, frequency, and cross-correlation between fluctuations in linear and angular movements. Our observations demonstrate that lateral line input is needed for fish to hold their station in flow efficiently and reveals that commonly used lesion methods have unique effects on rheotaxis behavior.

Putting the Pacific marine heatwave into perspective: The response of larval fish off southern California to unprecedented warming in 2014-2016 relative to the previous 65 years.

The 2014-2016 Northeast Pacific marine heatwave (MHW) induced the warmest 3-year period on record in the California Current Ecosystem. We tested whether larval fish assemblage structure, phenology, and diversity dynamics were comparable to past warming events from 1951 to 2013. First, we hypothesized, based on past observations of biological effect of warming, that mesopelagic species with southern distributions relative to southern California and Pacific sardine Sardinops sagax (a coastal pelagic species) would increase during the MHW while northern mesopelagics and northern anchovy Engraulis mordax (coastal pelagic) abundances would decline. Similar to past warming, southern mesopelagics increased and northern mesopelagics decreased. Unexpectedly, however, a common southern mesopelagic, Mexican lampfish Triphoturus mexicanus, was approximately three times more abundant than the previous annual high. Furthermore, whereas sardine abundance did not increase, larval anchovy abundance rose to near-record highs in summer 2016. Second, we hypothesized that fishes would spawn earlier during the MHW. Fishes did not spawn in an earlier season within a year, but five of six southern mesopelagic taxa spawned earlier than typical within winter and spring. Third, we predicted that species richness would increase moderately due to an influx of southern and exodus of northern species. Richness, however, was very high in all seasons and the highest ever during the summer as multiple species with primarily southern distributions were recorded spawning for the first time in southern California. The richness of northern species was also unexpectedly high during the MHW. Northern species likely persisted in the study area because in addition to the warm water, pockets of cold water were consistently present. If, as predicted, conditions similar to the MHW become more common as oceans warm, this unique and largely unexpected combination of fishes may reflect future biological conditions.

Improving metabarcoding taxonomic assignment: A case study of fishes in a large marine ecosystem.

DNA metabarcoding is an important tool for molecular ecology. However, its effectiveness hinges on the quality of reference sequence databases and classification parameters employed. Here we evaluate the performance of MiFish 12S taxonomic assignments using a case study of California Current Large Marine Ecosystem fishes to determine best practices for metabarcoding. Specifically, we use a taxonomy cross-validation by identity framework to compare classification performance between a global database comprised of all available sequences and a curated database that only includes sequences of fishes from the California Current Large Marine Ecosystem. We demonstrate that the regional database provides higher assignment accuracy than the comprehensive global database. We also document a tradeoff between accuracy and misclassification across a range of taxonomic cutoff scores, highlighting the importance of parameter selection for taxonomic classification. Furthermore, we compared assignment accuracy with and without the inclusion of additionally generated reference sequences. To this end, we sequenced tissue from 597 species using the MiFish 12S primers, adding 252 species to GenBank's existing 550 California Current Large Marine Ecosystem fish sequences. We then compared species and reads identified from seawater environmental DNA samples using global databases with and without our generated references, and the regional database. The addition of new references allowed for the identification of 16 additional native taxa representing 17.0% of total reads from eDNA samples, including species with vast ecological and economic value. Together these results demonstrate the importance of comprehensive and curated reference databases for effective metabarcoding and the need for locus-specific validation efforts.

An inconvenient tooth: Evaluating female choice in multiple paternity using an evolutionarily and ecologically important vertebrate clade.

Understanding mating systems is a pillar of behavioural ecology, placing the complex interactions between females and males into a reproductive context. The field of multiple paternity, the phenomenon whereby many sires contribute to an individual litter, has traditionally viewed females as passive players in a male-male competitive framework. With the emergence of feminist perspectives in ecological fields, novel alternative mechanisms and evolutionary theories across invertebrate and vertebrate taxa recognize females are active stakeholders in the reproductive process. Despite their evolutionary significance, ecological diversity and myriad reproductive modes, elasmobranch (sharks, skates and rays) research lags behind other fields regarding complex biological processes, such as multiple paternity which is often ascribed to convenience polyandry. Here, we layout hypotheses and resynthesize multiple paternity literature from a female and life history perspective to highlight how alternative mechanisms influence the predominance of multiple paternity across elasmobranchs. We draw upon parallels in other invertebrate and vertebrate taxa to demonstrate how female elasmobranchs can influence multiple paternity outcomes that benefit their reproductive success. Our article challenges dogma that has resulted from years of dismissing the female perspective as important and provides a framework for future advancement using more holistic approaches to studying mating systems.

The skin microbiome of elasmobranchs follows phylosymbiosis, but in teleost fishes, the microbiomes converge.

BACKGROUND: The vertebrate clade diverged into Chondrichthyes (sharks, rays, and chimeras) and Osteichthyes fishes (bony fishes) approximately 420 mya, with each group accumulating vast anatomical and physiological differences, including skin properties. The skin of Chondrichthyes fishes is covered in dermal denticles, whereas Osteichthyes fishes are covered in scales and are mucous rich. The divergence time among these two fish groups is hypothesized to result in predictable variation among symbionts. Here, using shotgun metagenomics, we test if patterns of diversity in the skin surface microbiome across the two fish clades match predictions made by phylosymbiosis theory. We hypothesize (1) the skin microbiome will be host and clade-specific, (2) evolutionary difference in elasmobranch and teleost will correspond with a concomitant increase in host-microbiome dissimilarity, and (3) the skin structure of the two groups will affect the taxonomic and functional composition of the microbiomes. RESULTS: We show that the taxonomic and functional composition of the microbiomes is host-specific. Teleost fish had lower average microbiome within clade similarity compared to among clade comparison, but their composition is not different among clade in a null based model. Elasmobranch's average similarity within clade was not different than across clade and not different in a null based model of comparison. In the comparison of host distance with microbiome distance, we found that the taxonomic composition of the microbiome was related to host distance for the elasmobranchs, but not the teleost fishes. In comparison, the gene function composition was not related to the host-organism distance for elasmobranchs but was negatively correlated with host distance for teleost fishes. CONCLUSION: Our results show the patterns of phylosymbiosis are not consistent across both fish clades, with the elasmobranchs showing phylosymbiosis, while the teleost fish are not. The discrepancy may be linked to alternative processes underpinning microbiome assemblage, including possible historical host-microbiome evolution of the elasmobranchs and convergent evolution in the teleost which filter specific microbial groups. Our comparison of the microbiomes among fishes represents an investigation into the microbial relationships of the oldest divergence of extant vertebrate hosts and reveals that microbial relationships are not consistent across evolutionary timescales. Video abstract.

Organic contaminants as an ecological tool to explore niche partitioning: a case study using three pelagic shark species.

Chemical contaminant profiles are linked to an animal's niche, providing a potential tool by which to assess resource partitioning in pelagic species. As proof of concept, we examined contaminant signatures in three species of sharks (Isurus oxyrinchus, Prionace glauca, and Alopias vulpinus) known to overlap in both space and time. Since these sharks comprise a predatory guild within the Southern California Bight (SCB), we predicted that species may partition spatial and dietary resources to limit the extent of competitive exclusion. Indeed, species were distinguishable by both total contaminant loads and their contaminant fingerprint, as random forest analysis found that species could be correctly classified 96% of the time. Our results demonstrate the utility of chemical analyses for ecological studies, and how contaminant tracers can be used in combination with traditional methods to elucidate how species may undergo niche partitioning to reduce competition for overlapping resources within predatory guilds.

Species-Specific Characteristics Influence Contaminant Accumulation Trajectories and Signatures Across Ontogeny in Three Pelagic Shark Species.

Factors influencing organic contaminant accumulation in sharks, especially across ontogeny, are not well-known. Contaminant concentrations were measured in three species of sharks (Blue, Shortfin Mako, and Common Thresher) across a range of size classes (neonatal to adult) that vary in their ecological and physiological characteristics. Empirical data was compared to a theoretical framework that predicted the shape of lifetime accumulation curves. We found that a one-size-fits-all accumulation model was not appropriate as species-specific characteristics had a significant effect on contaminant accumulation trajectories. Maternal offloading likely has an important effect on determining neonatal shark contaminant starting points, and trophic ecology and physiology may interact to affect the shape of species' contaminant accumulation curves. Makos were found to have the highest accumulation potential and Blues the lowest, with Threshers being intermediate in accumulation potential. Changes in species' ecology and/or physiology were also reflected in contaminant signature changes over ontogeny. If contaminant concentrations are to be used as a proxy for risk, species-specific characteristics need to be taken into account when estimating contaminant exposure and its potential negative effects on shark health and human consumption safety.

An Introduction to Modelling Abundance and Life History Parameters in Shark Populations.

Elasmobranchs play critically important ecological roles throughout the world's oceans, yet in many cases, their slow life histories and interactions with fisheries makes them particularly susceptible to exploitation. Management for these species requires robust scientific input, and mathematical models are the backbone of science-based management. In this chapter, we provide an introductory overview of the use of mathematical models to estimate shark abundance. First, we discuss life history models that are used to understand the basic biology of elasmobranchs. Second, we cover population dynamics models, which are used to make inferences regarding population trend, size, and risk of extinction. Finally, we provide examples of applied models used to assess the status of elasmobranchs in the Northeast Pacific Ocean to guide management for these species. This chapter is not a comprehensive review of quantitative methods, but rather introduces various mathematical tools in fisheries management, with a focus on shark management in the Northeast Pacific Ocean.

The skin microbiome of the common thresher shark (Alopias vulpinus) has low taxonomic and gene function ß-diversity.

The health of sharks, like all organisms, is linked to their microbiome. At the skin interface, sharks have dermal denticles that protrude above the mucus, which may affect the types of microbes that occur here. We characterized the microbiome from the skin of the common thresher shark (Alopias vulpinus) to investigate the structure and composition of the skin microbiome. On average 618 812 (80.9% ± S.D. 0.44%) reads per metagenomic library contained open reading frames; of those, between 7.6% and 12.8% matched known protein sequences. Genera distinguishing the A. vulpinus microbiome from the water column included, Pseudoalteromonas (12.8% ± 4.7 of sequences), Erythrobacter (5. 3% ± 0.5) and Idiomarina (4.2% ± 1.2) and distinguishing gene pathways included, cobalt, zinc and cadmium resistance (2.2% ± 0.1); iron acquisition (1.2% ± 0.1) and ton/tol transport (1.3% ± 0.08). Taxonomic community overlap (100 - dissimilarity index) was greater in the skin microbiome (77.6), relative to the water column microbiome (70.6) and a reference host-associated microbiome (algae: 71.5). We conclude the A. vulpinus skin microbiome is influenced by filtering processes, including biochemical and biophysical components of the shark skin and result in a structured microbiome.