AbstractEmerging infectious diseases can cause abrupt demographic changes in wildlife populations. The 2023 outbreak of highly pathogenic avian influenza caused widespread mortality in pinnipeds along the South American coast. We evaluated the population-level impact of the outbreak on South American sea lions (Otaria flavescens) and South American fur seals (Arctocephalus australis) in Patagonia, Argentina. Censuses conducted during the 2024 breeding season using aircraft and drones were compared with long-term pre-outbreak data (1973-2023) using two complementary approaches: raw census comparisons and colony trend projections. Raw census comparisons indicated proportional declines in counts of 17.07% in South American sea lions and 31.31% in South American fur seals between the most recent pre-outbreak censuses and the 2024 breeding season. Colony trend projections based on historical growth trajectories suggested outbreak-associated mortality of about 43.67% in South American sea lions and 15.01% in South American fur seals. Adult males exhibited the largest proportional declines in counts in both species. Pup production in 2024 was 54.17% lower than expected in South American sea lions and 45.01% lower in South American fur seals relative to projected values based on pre-outbreak colony trends. Differences in colony density, spatial distribution, and seasonal timing of breeding and haul-out likely contributed to the observed interspecific variability in mortality and reproductive output. The magnitude of adult losses and reduced pup production suggests that the outbreak may influence short- to medium-term population trajectories. Our results highlight the value of long-term census programs for detecting large-scale demographic impacts of emerging infectious diseases in recovering pinniped populations.
Edwardsia elegans Verrill, 1869 is the most commonly encountered and discussed species of Edwardsia from North America. Although it is familiar and commonly cited in field guides, its anatomy, cnidom, life history, and molecular resources have been only partially described. We provide a full account of E. elegans, along with an annotated transcriptome, and differentiate it from other species of Edwardsia from the western North Atlantic. We also describe the juvenile morphology and natural history of E. elegans, based on in situ observations in Maine and ex situ observations of captive specimens maintained in an aquarium. Edwardsia elegans is distinguished from all other edwardsiids from North America in having 16 tentacles arrayed in two cycles of eight, nemathybomes forming distinct aggregations in the middle of each mesenterial compartment, and a bulbous physa. Adults burrow using their physa and tend to aggregate into clusters in the field and the lab. Analysis of the transcriptome reveals differences in content of genes related to cellular stress with a broadly studied edwardsiid species, Nematostella vectensis. This updated account and the availability of reference sequence data for E. elegans will be useful for future research with this species and comparative work across edwardsiid anemones and the Cnidaria.
AbstractCoral bleaching, which occurs in response to breakdown of cnidarian-dinoflagellate symbiosis, is a major ecological issue that leads to destruction of the entire reef ecosystem. Therefore, understanding the mechanisms regulating symbiosis is of critical importance. One pathway implicated in both establishment and breakdown of cnidarian symbiosis is apoptosis, or programmed cell death. In vertebrates, this process is regulated by the Bcl-2 family, which contains both pro- and antiapoptotic proteins. In corals, Bcl-2 family gene expression is altered during thermal stress, but a role during symbiosis establishment remains unexplored. Additionally, variation in the Bcl-2 repertoire across cnidarians is not well understood. Therefore, we explored the evolution of the Bcl-2 family in cnidarians and their role in regulating apoptosis during symbiosis with homologous and heterologous dinoflagellates using the anemone Exaiptasia diaphana. This was done by correlating apoptosis levels measured by caspase-3 assays with Bcl-2 family gene expression data. The results indicated that each species has a unique repertoire of Bcl-2 proteins, likely as a result of multiple gene loss and duplication events. Functional work revealed that apoptosis was not initiated during recolonization with either homologous or heterologous symbionts, which corresponded to minimal differences in Bcl-2 family gene expression. Additionally, no gene expression changes were observed as a function of steady symbiotic state. Collectively, this work suggests that suppression of apoptosis is a common mechanism used by homologous and heterologous dinoflagellates to form long-term associations with a cnidarian host but members of the Bcl-2 family play a minimal role in this process.
AbstractPlasticity in individual thermal physiology is dependent on a species' evolutionary history as well as local environments that influence acclimatization capacity. To test how physiology and acclimatization capacity vary with species and local thermal conditions, we investigated the thermal performance of two rocky shore snails in the genus Nerita. Thermal environments experienced by the snails and their physiological performances (using heart rate) were quantified for two tropical locations (Hong Kong and Singapore; two sites per species in each location) where one or both species were present. Nerita undata, which has a tropical evolutionary origin, was present in both locations, while Nerita yoldii, which has a more subtropical-temperate lineage, was present in Hong Kong but not Singapore. Thermal tolerance of N. undata increased with the maximum environmental temperature in Hong Kong but not Singapore, where sites were hotter and snails had higher but less variable thermal tolerances (~50 °C). Nerita yoldii inhabited hotter sites in Hong Kong than N. undata but, similar to N. undata in Singapore, showed limited plasticity to environmental temperatures. Such extended tolerances but limited plasticity reflect a trade-off that constrains acclimatization capacity, where extreme thermal stress may elicit high energy expenditure but restrict energy gain through feeding when the rock becomes hot and dry. The ability to exhibit physiological plasticity is therefore limited on thermally harsh rocky shores, supporting the hypothesis that tropical ectotherms live close to their thermal limits and are limited in their ability to acclimatize further to survive episodes of extreme thermal stress.
Ships, planes, and other vessels that come to rest on the seafloor introduce metals to the marine environment. Underwater cultural heritage (UCH) sites become important habitats for sessile invertebrates, but the materials they are made from can impact the composition of species living on them. We collected and analyzed images from three sites in Palau (two shipwrecks and one plane wreck from WWII) along with directly adjacent (1-5 m away) naturally occurring coral reefs. Community composition on UCH after similar to 80 years of submergence was significantly different from adjacent coral reefs, but summary metrics (i.e., richness, diversity, and evenness) were not. Differences in community composition were driven by which taxa-not how many-were present. Sponges were more common on UCH than coral reefs, reflecting their elevated metal tolerance and competitive dominance over corals. Coral taxa that dominated UCH habitats were characterized as "weedy" or "stress tolerant" in a previous study based on their life-history traits. However, stress-tolerant Porites corals were less common on UCH than coral reefs, potentially reflecting their sensitivity to bleaching in the presence of elevated iron. Coral juveniles on UCH were significantly different from adults on UCH and coral reefs, although their diversity was not sufficiently captured by our study. Overall, this study highlights differences in community composition between UCH habitats and adjacent natural reefs and raises questions for further investigation to understand the driving mechanisms.
The abilities of sabellariid annelids to regenerate missing anterior or posterior body regions are not well understood. We described regeneration ability in the sabellariid Phragmatopoma californica, carrying out amputations in three locations (the opercular region, the middle of the abdomen, and the posterior of the abdomen) and observing survivorship and regeneration in the resulting body fragments for 6 weeks. Both anterior and posterior regeneration were possible, with fragments missing the head and part of the opercular region regenerating missing anterior structures and fragments missing the posterior part of the abdomen and the cauda regenerating missing posterior structures. The posterior-most body region of sabellariids, the cauda, lacks parapodia and chaetae and is typically described as "apparently unsegmented," which raises questions about where new segments are added during growth. Using light and scanning electron microscopy, we show that caudae of P. californica contain serially repeated septa and lateral blood vessels, suggesting strongly that they are segmented, albeit cryptically. These results clarify previous ambiguity in the literature about the regeneration abilities of sabellariids, which will improve future reconstructions of the evolutionary history of regeneration ability in annelids and help focus new questions on how and where sabellariids add new segments to abdominal and caudal body regions.
Ecological studies of marine invertebrates lacking external sexual dimorphism have often overlooked potential roles of sex and sex determination systems. Yet sex-dependent effects can influence ecological outcomes for many species, including keystone echinoderms like the sunflower sea star (Pycnopodia helianthoides), which can play important roles in maintaining marine biodiversity. Although DNA sequencing has previously been used to document genetic associations with sex in some echinoderms, there is currently little information on sex determination in sea stars lacking sexual dimorphism. Here, we used whole-genome resequencing of 16 female and 18 male P. helianthoides to test for genetic associations with sex and to identify candidate genes. Principal component analysis and outlier tests were used to identify sex-associated genome regions and single-nucleotide polymorphisms distinguishing males from females. We used the annotated P. helianthoides genome to associate gene models with candidate single-nucleotide polymorphisms. Sex-associated single-nucleotide polymorphisms, characterized by male homozygosity and female heterozygosity, were concentrated in distinct haplotypes; the majority (86%) were on just two chromosomes. Of the 76 outlier sex-specific single-nucleotide polymorphisms identified, 73 always discriminated female sea stars from males. These single-nucleotide polymorphisms are in or adjacent to genes involved in gonad formation, sex-specific gene expression, and sex determination processes. These results provide an important resource for identifying sex and enable study of the role that sex plays in the biology, ecology, and conservation of the sunflower sea star.
Polydorids (family Spionidae) are marine annelids that mostly bore into and occupy a variety of calcareous substrates, including mollusc shells and coralline algae. Here we evaluated the identity of polydorids inhabiting coralline algae encrustations of shells of Conus species (family Conidae) from French Polynesia through analyses of sequences of a region of the mitochondrial 16S gene. We observed polydorids in samples of 18 specimens of six Conus species from three locations in French Polynesia. We obtained sequences of 138 polydorid specimens, which represented seven distinct haplotypes. Although it is unclear whether the distinct sequences represent intraspecific variation, they are most similar to a GenBank sequence of Dipolydora armata. For 12 of the 14 Conus specimens for which multiple polydorid individuals were sequenced, we recovered identical haplotype sequences; two haplotype sequences were obtained from the other three Conus specimens, but one of the haplotypes predominated the samples. Moreover, no particular polydorid haplotype showed any obvious association with any of the Conus species. These results suggest that the polydorids inhabiting the encrustations on cone snails of French Polynesia are D. armata or represent close relatives of this species and that communities of polydorids on individual snails are genetically homogenous and possibly established from settlement of few larvae and asexual reproduction of recruits.
AbstractTemperature is a key environmental factor influencing animal behavior, including foraging, predator avoidance, and habitat use. Intertidal fishes already experience extreme thermal variability and may be especially vulnerable to further environmental change; therefore, understanding how their behavior responds to temperature fluctuations is essential. This study investigates how chronic exposure to two ecologically relevant temperatures (10 °C and 20 °C) shapes the behavior of the intertidal common triplefin, Forsterygion lapillum. We use a series of behavioral assays to assess activity, emergence, feeding, evasive responses, and aggression. During the 6-week acclimation period, fish in the 20 °C treatment consumed more food and spent less time hidden within refuges. Fish acclimated to 20 °C also exhibited greater overall activity, increased aggression, and a shorter latency to initiate movement. However, evasive responses to a simulated bird strike did not differ significantly between treatments. These findings demonstrate that warmer conditions can substantially alter the behavior of intertidal triplefins. While elevated activity and aggression may bolster foraging success and territorial defense, they also bring higher energetic demands and increased risk of predator exposure. These trade-offs may ultimately influence individual survival, reproductive success, and population-level outcomes. In the context of ongoing climate change, our findings underscore the need to understand species-specific behavioral responses to warming. Even subtle behavioral shifts could cascade through intertidal communities, affecting ecological stability.
Symbiotic associations between deep-sea invertebrates and chemoautotrophic bacteria vary widely in terms of symbiont type, localization, and host nutritional strategy, yet host-symbiont dynamics remain poorly understood in some taxa. Here we advance knowledge of host-symbiont interactions within the snail genus Alviniconcha, which are abundant members of hydrothermal vent communities in the Indian and West Pacific Oceans. Using electron microscopy, we use comparative analyses based on the ultrastructural characteristics of the host bacteriocytes and bacterial symbionts. Despite previous assumptions that all Alviniconcha host endosymbiotic bacteria, we find that A. boucheti hosts episymbiotic bacteria, which densely populate the microvilli of bacteriocytes and appear to be endocytosed. Alviniconcha may also use species-specific organizational and nutritional strategies within bacteriocytes, supporting differences in symbiont maintenance and digestion. Alviniconcha adamantis and A. hessleri hosted endosymbionts in individual vacuoles with little evidence of symbiont digestion, A. kojimai and A. strummeri housed their symbionts similarly but with comparatively more evidence of digestion, and A. marisindica and A. boucheti stored symbionts in large multibacterial vacuoles, with the highest apparent degree of digestion in A. boucheti. Host species also differed in the density and morphotype of symbionts present, with all species hosting one to three morphotypes of symbionts resembling thiotrophic bacteria. In addition, both A. adamantis and A. hessleri harbored symbionts resembling methanotrophic bacteria, which genetic studies (16S rRNA amplicon and genomic) to date have not detected. This study provides the first genus-wide comparison of host-symbiont interactions in Alviniconcha, revealing key cellular features and advancing understanding of the diverse associations between hosts and their bacterial symbionts.
AbstractResearch suggests that tyramine and octopamine have complementary distributions and roles in invertebrates somewhat analogous to those of norepinephrine and epinephrine in vertebrates. Interestingly, these groups of neurotransmitters/hormones share similar biosynthetic pathways that include the apparently homologous enzymes tyramine-β hydroxylase (TBH) and dopamine-β hydroxylase (DBH), which convert tyramine to octopamine and dopamine to norepinephrine, respectively. In this paper we report sequence alignments and Western blots that support the homology of TBH and DBH, as well as validate the use of an antibody raised against a DBH target sequence for immunohistochemical analysis of octopaminergic neural elements in molluscs. Accordingly, we found that DBH and octopamine immunoreactivities did indeed colocalize in several, but not all, neurons in the buccal, cerebral, and pedal ganglia of the pond snail Lymnaea stagnalis. Additional, apparently off-target labeling was also observed that warrants future examination. It was noteworthy, however, that no colocalization was found between DBH and tyrosine hydroxylase immunoreactivities, thus providing no evidence for norepinephrine synthesis within the central nervous system of this mollusc. These results expand on previous descriptions of neuroanatomical examinations of L. stagnalis and reinforce the argument that DBH and TBH are homologous proteins, thus supporting DBH/TBH as a target to investigate octopaminergic localization and function in molluscs and, more broadly, among invertebrates.
AbstractThe long-spined sea urchin Centrostephanus rodgersii has space between the spines and the substratum, which creates a microhabitat for macroinvertebrates and some fishes. We sampled assemblages under sea urchins in self-excavated dwellings (boreholes) in macroalgal and urchin-grazed barrens habitats in rocky reefs in New South Wales, Australia, at sites spanning 400 km. A rich fauna of 80 nominal taxa was recorded, with 1-24 taxa and 1-963 individuals recorded under individual urchins. The fauna was dominated by gastropods (39 taxa), malacostracans (13 taxa), and chitons (8 taxa). Significant differences in associated fauna were observed between the two habitats at two of the four study locations and at one-third of all sites sampled. While the abundance of some groups differed significantly between the two habitats, taxonomic richness and total abundance of animals did not. Temporal variability in macroalgal habitat was noted in assemblages, as well as the abundance of several taxa, at the two sites that were sampled over three times. Our findings point to the importance of long-spined and bioeroding diadematid sea urchins as biogenic habitat to support biodiversity and the implications of their removal.
AbstractCephalopods, such as squids and cuttlefishes, play an integral role in food web dynamics as both prey and predator, whereby proficient turning is required for successful predator avoidance and prey capture. However, surprisingly little is known about the turning capabilities of most cephalopods. In this study, body movements and 3D flow fields around adult dwarf cuttlefish, Sepia bandensis, were recorded during a range of maneuvers to quantify turning performance. While significant variation in turning capabilities was observed, S. bandensis, on average, turned tightly (mean length-specific turning radius = 0.14±0.013 [SEM]; minimum length-specific turning radius = 0.013±0.002) but relatively slowly (average angular velocity = 45.85°±2.70° s-1; maximum angular velocity = 110.34°±7.09° s-1). Jet properties were not reliable predictors of turn performance, as S. bandensis relied primarily on short vortex ring jets (length-to-diameter ratio of jet vorticity = 2.47±0.18) of moderate velocity (average jet velocity ∼ 14 cm s-1; maximum jet velocity ∼ 22 cm s-1) irrespective of turn type. The orientation of the turn (arms-first vs. tail-first) did not have a significant effect on kinematic or hydrodynamic properties, and most turns were performed arms-first (72.6% of turns). Compared to other cephalopods, cuttlefish turned using shorter jets with similar velocity profiles. These results are consistent with the residence of S. bandensis in complex benthic habitats, where tight, controlled turns facilitated by short jet pulses and high turning proficiency in either orientation are needed.
Gregarious larval settlement, a phenomenon in which cues associated with conspecifics induce larval settlement, plays a role in the growth of existing aggregations of many aggregation-forming sessile marine invertebrates. The formation of new aggregations, however, requires larvae to settle in response to other cues. The mechanism underlying this variation in larval settlement responses is unknown for most species with gregarious settlement. In this study we first present evidence that larvae of the serpulid annelid Ficopomatus enigmaticus settle gregariously. In no-choice, still-water experiments, a much higher percentage of larvae settled after 24 h of exposure to conspecific tube than after exposure to mussel shell collected from the same habitat. We then tested the hypothesis that larvae of F. enigmaticus display a genetically determined dimorphism in settlement behavior like that of the serpulid Hydroides dianthus, with most larvae capable of settling only in response to a conspecific cue but a small percentage of larvae capable of settling only in response to a biofilm cue. If this hypothesis is correct, the sum of the percentages of larvae that settle in response to a conspecific cue and those that settle in response to a biofilm cue cannot exceed 100% (since each larva can accept only one of the two cue types throughout its competent period). Our data on F. enigmaticus are not consistent with this prediction, suggesting that individual larvae can respond to multiple types of settlement cues during their competent period. This has significant implications for how frequently larvae can form new aggregations, a topic of special importance for F. enigmaticus and H. dianthus, both of which are well-known invasive species in marine habitats around the globe.
AbstractNudibranchs of the genus Spurilla (Aeolidiidae) are currently represented worldwide by five species: S. braziliana, S. croisicensis, S. dupontae, S. neapolitana, and S. sargassicola. Two of these, S. neapolitana and S. braziliana, have been previously reported from the Argentine Sea. This study aimed to identify Spurilla specimens collected from intertidal zones at four sites in the San Matías Gulf. We conducted detailed morphological and anatomical examinations, including external traits (body coloration, rhinophores, and cerata) and internal structures (radula, jaws, nervous system, and reproductive system). These characteristics were compared with published descriptions of all five known species. To strengthen our findings, we incorporated a molecular approach based on mitochondrial gene sequences. The analysis revealed low genetic differentiation between populations from Argentina and Brazil, supporting the presence of a single, widespread species, S. braziliana, throughout the southwestern Atlantic. Genetic patterns also suggest that Brazil may represent the species' center of origin, with subsequent southward dispersal to Argentina and northward expansion toward Central America and the Caribbean. This revision confirms that S. braziliana is the only species of the genus present along the western coast of the San Matías Gulf, contributing to a clearer understanding of regional marine biodiversity and species distributions.
AbstractThe abrasive, high-impact environment of rocky intertidal zones produces important abiotic stressors that many calcifying organisms are armored against. The ochre sea star (Pisaster ochraceus), a slow-moving but ecologically important predator in the wave-swept rocky intertidal of the eastern North Pacific, is covered aborally with calcium carbonate ossicles that are modified into spines. These spines may act as armor, providing lightweight protection for Pisaster against impacts and abrasion from abiotic particles in the intertidal. We used digital image analysis and scanning electron microscopy to characterize variation in the aboral armor of Pisaster across a range of sizes and intertidal habitats that vary in the joint impacts of water motion and abrasion. We found that Pisaster from different habitats exhibited distinct relationships between size and investment in aboral armor (spine density and areal spine coverage). Aboral armor was significantly higher in Pisaster from wave-exposed shores on which joint impacts of water motion and abrasion were highest, especially in smaller-sized individuals. We also identified specific aboral spine morphotypes, the proportions of which varied according to habitat. Individuals from wave-swept rock benches and boulder fields had short, blunt, and convex spines, whereas individuals from protected embayments had a higher proportion of upright, tapered, or columnar spines. Our results suggest that increased density and areal coverage of wider, convex spines in Pisaster are adaptive for more vulnerable life stages and in more abrasive and high-impact habitats. Future work should determine whether habitat-associated variation in the armor of Pisaster reflects a functional trade-off with feeding ability and whether it is primarily genetic or phenotypically plastic.
AbstractDefining the metabolic cost of specific biochemical processes is key to understanding strategies of energy (ATP) allocation. In this study, we determined the energy cost of RNA synthesis and the allocation of the ATP pool to this biosynthetic process. Rates of oxygen consumption, RNA synthesis, and protein synthesis were measured in early-stage embryos (single cell layer, 18-h-old blastula stage) of the sea urchin (Strongylocentrotus purpuratus) that have high rates of RNA synthesis. The inhibitory effects of actinomycin D on these processes were measured to calculate the energy cost of RNA synthesis. Across 15 different cohorts of embryos studied, the average rate of RNA synthesis was 0.19 ± 0.031 (SEM) ng RNA embryo-1 h-1. In the presence of actinomycin D, the rate of RNA synthesis decreased by 59%, and respiration decreased by 26%. As expected, actinomycin D also inhibited protein synthesis (by 28%) but had no effect on rates of uridine and alanine transport. This analysis revealed that the energy cost of RNA synthesis is 2.01 ± 0.24 (SEM) μJ (ng RNA synthesis)-1-a value that is notably similar to the known cost of protein synthesis in this species of 2.40 ± 0.21 μJ (ng protein synthesis)-1. In embryos, the rate of RNA synthesis was lower than that of protein synthesis, resulting in the former requiring only 11% of the total available ATP pool, compared to 67% for the latter. The significance of these findings is presented in the context of understanding the constraints and trade-offs of ATP allocation during development.
Bioluminescence is a common feature of the fishes inhabiting the dimly lit waters of the deep sea and is thought to play roles in prey attraction, predator avoidance, communication, and counterillumination. Stomiiformes, the most abundant and speciose order of deep-sea fishes, have a stunning variety of bioluminescent organs and tissues. While some of these structures have been well described, others are poorly characterized and rarely discussed in literature. Here we synthesize data in the literature on the four types of photophores found among stomiiforms (complex serial, complex minute, simple pigmented, and simple unpigmented photophores) and assess the size, density, and distribution of the little-known complex minute photophores, in particular, in 31 species in 25 stomiiform genera. The predicted orientation of light emitted from complex serial and minute photophores in 14 species in the stomiid subfamily Stomiinae was inferred from the placement of the lens (through which light is transmitted). Complex minute photophores were found, in addition to complex serial photophores, in all stomiines examined (and in one gonostomatid) and were notably smaller and occurred in higher densities than the complex serial photophores. The predicted ventral orientation of the light emitted by the complex serial photophores in all species presumably functions in counterillumination. However, the predicted direction of transmission of light produced by complex minute photophores appears to vary within and among species, suggesting multiple functions (e.g., camouflage and/or communication), warranting further studies of photophores in these intriguing and ecologically critical fishes.
AbstractThe high Arctic is defined by an annual light regime ranging from 24-h light (Midnight Sun) to 24-h dark (Polar Night). Light acts as an important cue for marine zooplankton, influencing their orientation and vertical migration, prey detection and predator avoidance, and population dynamics and reproductive strategies. The spectrum and intensity of underwater light differ between Midnight Sun and Polar Night, and these differences are relevant to zooplankton visual processes. Here, we determine behavioral responses of the Arctic copepod Metridia longa, measured as swimming activity in a novel laboratory apparatus, to spectral- and irradiance-controlled light stimuli during times of Midnight Sun and Polar Night. Metridia longa maintains a consistent blue-green spectral response, from 400 to 550 nm, during both times of year. However, peak spectral response shifted between seasons, with Midnight Sun individuals showing increased activity at 501 nm compared to 473-490 nm during Polar Night. Additionally, Polar Night M. longa showed heightened irradiance sensitivity by an order of magnitude as compared to Midnight Sun individuals. Their irradiance response was also consistent across varying temperatures. We show that spectral and irradiance responses in M. longa are seasonally adapted and temperature compensated, suggesting that this copepod maintains a consistent light-mediated predator avoidance capacity, despite predicted seasonal light and temperature shifts in the high Arctic.
