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"LeMay, Matthew"
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Parasites of the hermit crab Pagurus hirsutiusculus; distribution, prevalence, and thermal ecology
Parasites are common throughout the biosphere and can play significant ecological roles. However, most parasites are understudied, particularly with regards to how their prevalence and impacts vary with environmental conditions. As a result, there remains an incomplete understanding of how both parasites and their hosts may be impacted by climate change. We conducted field surveys to better understand the parasite distributions of the intertidal hermit crab Pagurus hirsutiusculus in British Columbia . We found three genera of externally visible parasites ( Eremitione giardi, Peltogasterella sp., and Peltogaster sp.), and one hyperparasite ( Liriopsis pygmaea ), which were present throughout the surveyed region. The prevalence of E. giardi was related to salinity while Peltogaster sp. was related to host size. At some locations, we observed a decline in prevalence in the parasite Peltogaster sp. following the 2021 Pacific Northwest heat wave event. In the lab, we compared the metabolic rate across a temperature range and survivorship post heat stress in individuals infected with Peltogaster sp. and uninfected individuals. We did not find a difference in metabolism based on infection status but found that uninfected individuals had significantly higher survivorship following heat stress. This study highlights the pervasiveness of parasitic interactions and demonstrates the need to study them in combination with environmental factors to better understand the effects of climate change on populations.
Journal Article
Transcriptome of the coralline alga Calliarthron tuberculosum (Corallinales, Rhodophyta) reveals convergent evolution of a partial lignin biosynthesis pathway
The discovery of lignins in the coralline red alga Calliarthron tuberculosum raised new questions about the deep evolution of lignin biosynthesis. Here we present the transcriptome of C . tuberculosum supported with newly generated genomic data to identify gene candidates from the monolignol biosynthetic pathway using a combination of sequence similarity-based methods. We identified candidates in the monolignol biosynthesis pathway for the genes 4CL, CCR, CAD, CCoAOMT, and CSE but did not identify candidates for PAL, CYP450 (F5H, C3H, C4H), HCT, and COMT. In gene tree analysis, we present evidence that these gene candidates evolved independently from their land plant counterparts, suggesting convergent evolution of a complex multistep lignin biosynthetic pathway in this red algal lineage. Additionally, we provide tools to extract metabolic pathways and genes from the newly generated transcriptomic and genomic datasets. Using these methods, we extracted genes related to sucrose metabolism and calcification. Ultimately, this transcriptome will provide a foundation for further genetic and experimental studies of calcifying red algae.
Journal Article
Integrating technologies provides insight into the subsurface foraging behaviour of a humpback whale (Megaptera novaeangliae) feeding on walleye pollock (Gadus chalcogrammus) in Juan de Fuca Strait, Canada
Subsurface foraging is an important proportion of the activity budget of rorqual whales, yet information on their behaviour underwater remains challenging to obtain. Rorquals are assumed to feed throughout the water column and to select prey as a function of depth, availability and density, but there remain limitations in the precise identification of targeted prey. Current data on rorqual foraging in western Canadian waters have thus been limited to observations of prey species amenable to surface feeding, such as euphausiids and Pacific herring ( Clupea pallasii ), with no information on deeper alternative prey sources. We measured the foraging behaviour of a humpback whale ( Megaptera novaeangliae ) in Juan de Fuca Strait, British Columbia, using three complimentary methods: whale-borne tag data, acoustic prey mapping, and fecal sub-sampling. Acoustically detected prey layers were near the seafloor and consistent with dense schools of walleye pollock ( Gadus chalcogrammus ) distributed above more diffuse aggregations of pollock. Analysis of a fecal sample from the tagged whale confirmed that it had been feeding on pollock. Integrating the dive profile with the prey data revealed that the whale’s foraging effort followed the general pattern of areal prey density, wherein the whale had a higher lunge-feeding rate at the highest prey abundance and stopped feeding when prey became limited. Our findings of a humpback whale feeding on seasonally energy-dense fish like walleye pollock, which are potentially abundant in British Columbia, suggests that pollock may be an important prey source for this rapidly growing whale population. This result is informative when assessing regional fishing activities for semi-pelagic species as well as the whales’ vulnerability to fishing gear entanglements and feeding disturbances during a narrow window of prey acquisition.
Journal Article
Trophic control of cryptic coralline algal diversity
Understanding how trophic dynamics drive variation in biodiversity is essential for predicting the outcomes of trophic downgrading across the world’s ecosystems. However, assessing the biodiversity of morphologically cryptic lineages can be problematic, yet may be crucial to understanding ecological patterns. Shifts in keystone predation that favor increases in herbivore abundance tend to have negative consequences for the biodiversity of primary producers. However, in nearshore ecosystems, coralline algal cover increases when herbivory is intense, suggesting that corallines may uniquely benefit from trophic downgrading. Because many coralline algal species are morphologically cryptic and their diversity has been globally underestimated, increasing the resolution at which we distinguish species could dramatically alter our conclusions about the consequences of trophic dynamics for this group. In this study, we used DNA barcoding to compare the diversity and composition of cryptic coralline algal assemblages at sites that differ in urchin biomass and keystone predation by sea otters. We show that while coralline cover is greater in urchin-dominated sites (or “barrens”), which are subject to intense grazing, coralline assemblages in these urchin barrens are significantly less diverse than in kelp forests and are dominated by only 1 or 2 species. These findings clarify how food web structure relates to coralline community composition and reconcile patterns of total coralline cover with the widely documented pattern that keystone predation promotes biodiversity. Shifts in coralline diversity and distribution associated with transitions from kelp forests to urchin barrens could have ecosystem-level effects that would be missed by ignoring cryptic species’ identities.
Journal Article
Morphological complexity affects the diversity of marine microbiomes
Large eukaryotes support diverse communities of microbes on their surface—epibiota—that profoundly influence their biology. Alternate factors known to structure complex patterns of microbial diversity—host evolutionary history and ecology, environmental conditions and stochasticity—do not act independently and it is challenging to disentangle their relative effects. Here, we surveyed the epibiota from 38 sympatric seaweed species that span diverse clades and have convergent morphology, which strongly influences seaweed ecology. Host identity explains most of the variation in epibiont communities and deeper host phylogenetic relationships (e.g., genus level) explain a small but significant portion of epibiont community variation. Strikingly, epibiota community composition is significantly influenced by host morphology and epibiota richness increases with morphological complexity of the seaweed host. This effect is robust after controlling for phylogenetic non-independence and is strongest for crustose seaweeds. We experimentally validated the effect of host morphology by quantifying bacterial community assembly on latex sheets cut to resemble three seaweed morphologies. The patterns match those observed in our field survey. Thus, biodiversity increases with habitat complexity in host-associated microbial communities, mirroring patterns observed in animal communities. We suggest that host morphology and structural complexity are underexplored mechanisms structuring microbial communities.
Journal Article
Biodiversity of protists and nematodes in the wild nonhuman primate gut
Documenting the natural diversity of eukaryotic organisms in the nonhuman primate (NHP) gut is important for understanding the evolution of the mammalian gut microbiome, its role in digestion, health and disease, and the consequences of anthropogenic change on primate biology and conservation. Despite the ecological significance of gut-associated eukaryotes, little is known about the factors that influence their assembly and diversity in mammals. In this study, we used an 18S rRNA gene fragment metabarcoding approach to assess the eukaryotic assemblage of 62 individuals representing 16 NHP species. We find that cercopithecoids, and especially the cercopithecines, have substantially higher alpha diversity than other NHP groups. Gut-associated protists and nematodes are widespread among NHPs, consistent with their ancient association with NHP hosts. However, we do not find a consistent signal of phylosymbiosis or host-species specificity. Rather, gut eukaryotes are only weakly structured by primate phylogeny with minimal signal from diet, in contrast to previous reports of NHP gut bacteria. The results of this study indicate that gut-associated eukaryotes offer different information than gut-associated bacteria and add to our understanding of the structure of the gut microbiome.
Journal Article
Integrating technologies provides insight into the subsurface foraging behaviour of a humpback whale
Subsurface foraging is an important proportion of the activity budget of rorqual whales, yet information on their behaviour underwater remains challenging to obtain. Rorquals are assumed to feed throughout the water column and to select prey as a function of depth, availability and density, but there remain limitations in the precise identification of targeted prey. Current data on rorqual foraging in western Canadian waters have thus been limited to observations of prey species amenable to surface feeding, such as euphausiids and Pacific herring (Clupea pallasii), with no information on deeper alternative prey sources. We measured the foraging behaviour of a humpback whale (Megaptera novaeangliae) in Juan de Fuca Strait, British Columbia, using three complimentary methods: whale-borne tag data, acoustic prey mapping, and fecal sub-sampling. Acoustically detected prey layers were near the seafloor and consistent with dense schools of walleye pollock (Gadus chalcogrammus) distributed above more diffuse aggregations of pollock. Analysis of a fecal sample from the tagged whale confirmed that it had been feeding on pollock. Integrating the dive profile with the prey data revealed that the whale's foraging effort followed the general pattern of areal prey density, wherein the whale had a higher lunge-feeding rate at the highest prey abundance and stopped feeding when prey became limited. Our findings of a humpback whale feeding on seasonally energy-dense fish like walleye pollock, which are potentially abundant in British Columbia, suggests that pollock may be an important prey source for this rapidly growing whale population. This result is informative when assessing regional fishing activities for semi-pelagic species as well as the whales' vulnerability to fishing gear entanglements and feeding disturbances during a narrow window of prey acquisition.
Journal Article
Effect of environmental DNA sampling resolution in detecting nearshore fish biodiversity compared to capture surveys
Sampling and sequencing marine environmental DNA (eDNA) provides a tool that can increase our ability to monitor biodiversity, but movement and mixing of eDNA after release from organisms before collection could affect our inference of species distributions. To assess how conditions at differing spatial scales influence the inferred species richness and compositional turnover, we conducted a paired eDNA metabarcoding and capture (beach seining) survey of fishes on the coast of British Columbia. We found more taxa were typically detected using eDNA compared to beach seining. eDNA identified more taxa with alternative habitat preferences, and this richness difference was greater in areas of high seawater movement, suggesting eDNA has a larger spatial grain influenced by water motion. By contrast, we found that eDNA consistently missed low biomass species present in seining surveys. Spatial turnover of communities surveyed using beach seining differed from that of the eDNA and was better explained by factors that vary at small (10–1000s meters) spatial scales. Specifically, vegetation cover and shoreline exposure explained most species turnover from seining, while eDNA turnover was not explained by those factors and showed a distance decay pattern (a change from 10% to 25% similarity from 2 km to 10 km of distance), suggesting unmeasured environmental variation at larger scales drives its turnover. Our findings indicate that the eDNA sample grain is larger than that of capture surveys. Whereas seining can detect differences in fish distributions at scales of 10s–100s of meters, eDNA can best summarize fish biodiversity at larger scales possibly more relevant to regional biodiversity assessments.
Journal Article
Fine‐scale diversity of prey detected in humpback whale feces
Predator diets are largely influenced by prey availability and abundance. Yet, in heterogenous marine environments, identifying the prey species consumed by diving mammals remains a fundamental challenge. For rorqual whales, the energetic constraints of prey engulfment require that the whales seek areas of high prey abundance and execute discrete lunge feeding events on patches of high‐density prey. Prey occurrences in feces should therefore provide meaningful insight into the dominant taxa in food patches selected by the animal. We investigated the prey consumed by humpback whales in three regions in southern British Columbia (BC), Canada, using opportunistic fecal sampling, microscopy, and DNA metabarcoding of 14 fecal samples. Fish including Pacific herring (Clupea pallasii), hake (Merluccius productus), and eulachon (Thaleichthys pacificus) were the most common fish species potentially targeted by humpback whales in two regions. The krill Euphausia pacifica was the most prevalent invertebrate DNA detected in all three regions, while sergestid and mysid shrimp may also be important. High DNA read abundances from walleye pollock (Gadus chalcogrammus) and sablefish (Anoplopoma fimbria) were also recovered in one sample each, suggesting that juveniles of these semi‐pelagic species may occasionally be targeted. In general, we observed heavily digested fecal material that drove substantial dissimilarities in taxonomic resolution between polymerase chain reaction‐based and morphological analyses of the feces. Pacific herring and walleye pollock were the only prey species confirmed by both methods. Our results highlight that molecular and visual analyses of fecal samples provide a complementary approach to diet analysis, with each method providing unique insight into prey diversity. We investigated the prey consumed by humpback whales in three heterogenous regions in southern British Columbia, Canada, using opportunistic faecal sampling, microscopy, and DNA metabarcoding of 14 faecal samples. Fish including Pacific herring (Clupea pallasii), hake (Merluccius productus), and eulachon (Thaleichthys pacificus) were the most common fish species potentially targeted by humpback whales in two regions. The krill Euphausia pacifica was the most prevalent invertebrate DNA detected in all three regions, while sergestid and mysid shrimp may also be important.
Journal Article