Showing papers in "The Biological Bulletin in 2022"

Impacts of Low Oxygen on Marine Life: Neglected, but a Crucial Priority for Research

Abstract: Global ocean O2 content has varied significantly across the eons, both shaping and being shaped by the evolutionary history of life on planet Earth. Indeed, past O2 fluctuations have been associated with major extinctions and the reorganization of marine biota. Moreover, its most recent iteration—now anthropogenically driven—represents one of the most prominent challenges for both marine ecosystems and human societies, with ocean deoxygenation being regarded as one of the main drivers of global biodiversity loss. Yet ocean deoxygenation has received far less attention than concurrent environmental variables of marine climate change, namely, ocean warming and acidification, particularly in the field of experimental marine ecology. Together with the lack of consistent criteria defining gradual and acute changes in O2 content, a general lack of multifactorial studies featuring all three drivers and their interactions prevents an adequate interpretation of the potential effects of extreme and gradual deoxygenation. We present a comprehensive overview of the interplay between O2 and marine life across space and time and discuss the current knowledge gaps and future steps for deoxygenation research. This work may also contribute to the ongoing call for an integrative perspective on the combined effects of these three drivers of change for marine organisms and ecosystems worldwide.

Too Hot to Eat: Wild and Lab-Bred Lymnaea stagnalis Differ in Feeding Response Following Repeated Heat Exposure

Abstract: Acute extreme heat events are increasing in frequency and intensity. Understanding their effects on ectothermic organisms’ homeostasis is both important and urgent. In this study we found that the exposure to an acute heat shock (30 °C for 1 hour) repeated for a seven-day period severely suppressed the feeding behavior of laboratory-inbred (W-strain) Lymnaea stagnalis, whereas the first-generation offspring of freshly collected wild (F1 D-strain) snails raised and maintained under similar laboratory conditions did not show any alterations. The W-strain snails might have inadvertently been selected against heat tolerance since they were first brought into the laboratory many (∼70) years ago. We also posit that the F1 D-strain snails do not perceive the heat shock as a sufficient stressor to alter their feeding response because their parental populations in wild environments have repeatedly experienced temperature fluctuations, thus becoming more tolerant and resilient to heat. The different responses exhibited by two strains of the same species highlight the importance of selecting the most appropriate strain for addressing questions about the impacts of global warming on organisms’ physiology and behavior.

Integrative Approaches to Understanding Organismal Responses to Aquatic Deoxygenation

Abstract: Oxygen bioavailability is declining in aquatic systems worldwide as a result of climate change and other anthropogenic stressors. For aquatic organisms, the consequences are poorly known but are likely to reflect both direct effects of declining oxygen bioavailability and interactions between oxygen and other stressors, including two—warming and acidification—that have received substantial attention in recent decades and that typically accompany oxygen changes. Drawing on the collected papers in this symposium volume (“An Oxygen Perspective on Climate Change”), we outline the causes and consequences of declining oxygen bioavailability. First, we discuss the scope of natural and predicted anthropogenic changes in aquatic oxygen levels. Although modern organisms are the result of long evolutionary histories during which they were exposed to natural oxygen regimes, anthropogenic change is now exposing them to more extreme conditions and novel combinations of low oxygen with other stressors. Second, we identify behavioral and physiological mechanisms that underlie the interactive effects of oxygen with other stressors, and we assess the range of potential organismal responses to oxygen limitation that occur across levels of biological organization and over multiple timescales. We argue that metabolism and energetics provide a powerful and unifying framework for understanding organism-oxygen interactions. Third, we conclude by outlining a set of approaches for maximizing the effectiveness of future work, including focusing on long-term experiments using biologically realistic variation in experimental factors and taking truly cross-disciplinary and integrative approaches to understanding and predicting future effects.

A Review of Asteroid Biology in the Context of Sea Star Wasting: Possible Causes and Consequences

Abstract: Sea star wasting—marked in a variety of sea star species as varying degrees of skin lesions followed by disintegration—recently caused one of the largest marine die-offs ever recorded on the west coast of North America, killing billions of sea stars. Despite the important ramifications this mortality had for coastal benthic ecosystems, such as increased abundance of prey, little is known about the causes of the disease or the mechanisms of its progression. Although there have been studies indicating a range of causal mechanisms, including viruses and environmental effects, the broad spatial and depth range of affected populations leaves many questions remaining about either infectious or non-infectious mechanisms. Wasting appears to start with degradation of mutable connective tissue in the body wall, leading to disintegration of the epidermis. Here, we briefly review basic sea star biology in the context of sea star wasting and present our current knowledge and hypotheses related to the symptoms, the microbiome, the viruses, and the associated environmental stressors. We also highlight throughout the article knowledge gaps and the data needed to better understand sea star wasting mechanistically, its causes, and potential management.

Reduced Oxygen Impairs Photobehavior in Marine Invertebrate Larvae

Abstract: Organisms in coastal waters experience naturally high oxygen variability and steep oxygen gradients with depth, in addition to ocean deoxygenation. They often undergo diel vertical migration involving a change in irradiance that initiates a visual behavior. Retinal function has been shown to be highly sensitive to oxygen loss; here we assess whether visual behavior (photobehavior) in paralarvae of the squid Doryteuthis opalescens and the octopus Octopus bimaculatus is affected by low oxygen conditions, using a novel behavioral paradigm. Larvae showed an irradiance-dependent, descending photobehavior after extinction of the light stimulus, measured through the change in vertical position of larvae in the chamber. The magnitude of photobehavior was decreased as oxygen was reduced, and the response was entirely gone at <6.4 kPa partial pressure of oxygen (<74.7 μmol kg−1 at 15.3 °C) in D. opalescens paralarvae. Oxygen also affected photobehavior in O. bimaculatus paralarvae. The mean vertical velocity of paralarvae was unaffected by exposure to reduced oxygen, indicating that oxygen deficits selectively affect vision prior to locomotion. These findings suggest that variable and declining oxygen conditions in coastal upwelling areas and elsewhere will impair photobehavior and likely affect the distribution, migration behavior, and survival of highly visual marine species.

Hypoxia and High Temperature as Interacting Stressors: Will Plasticity Promote Resilience of Fishes in a Changing World?

Abstract: Determining the resilience of a species or population to climate change stressors is an important but difficult task because resilience can be affected both by genetically based variation and by various types of phenotypic plasticity. In addition, most of what is known about organismal responses is for single stressors in isolation, but environmental change involves multiple environmental factors acting in combination. Here, our goal is to summarize what is known about phenotypic plasticity in fishes in response to high temperature and low oxygen (hypoxia) in combination across multiple timescales, to ask how much resilience plasticity may provide in the face of climate change. There are relatively few studies investigating plasticity in response to these environmental stressors in combination; but the available data suggest that although fish have some capacity to adjust their phenotype and compensate for the negative effects of acute exposure to high temperature and hypoxia through acclimation or developmental plasticity, compensation is generally only partial. There is very little known about intergenerational and transgenerational effects, although studies on each stressor in isolation suggest that both positive and negative impacts may occur. Overall, the capacity for phenotypic plasticity in response to these two stressors is highly variable among species and extremely dependent on the specific context of the experiment, including the extent and timing of stressor exposure. This variability in the nature and extent of plasticity suggests that existing phenotypic plasticity is unlikely to adequately buffer fishes against the combined stressors of high temperature and hypoxia as our climate warms.

Molecular Characterization of the Cytochrome P450 Epoxidase (CYP15) in the Swimming Crab Portunus trituberculatus and Its Putative Roles in Methyl Farnesoate Metabolism

Abstract: CYP15, which encodes a microsomal cytochrome P450 enzyme, could be involved in juvenile hormone biosynthesis in insects. In this study, a full-length cDNA of CYP15 was cloned from the swimming crab Portunus trituberculatus. This PtCYP15 amino acid sequence contains six conserved domains, which is a typical feature of the cytochrome P450 family. Phylogenetic tree analysis results showed that PtCYP15 clusters in a single branch of crustacean species, suggesting that CYP15 may be more widely present in crustaceans. The PtCYP15 mRNA has a broad pattern of tissue expression in P. trituberculatus, including high levels of expression in the hepatopancreas of both sexes and in the ovary of female crabs. During ovarian development stages, PtCYP15 mRNA is highly expressed in stages I and II and less so in stages III and IV in the hepatopancreas and the ovary of the female crabs. These expression profiles are opposite those of methyl farnesoate in hemolymph, suggesting that PtCYP15 might be involved in methyl farnesoate metabolism. In vitro studies show that only methyl farnesoate upregulated vitellogenin expression in the hepatopancreas, suggesting that methyl farnesoate might be the equivalent of juvenile hormone III in crustaceans. Methyl farnesoate treatment increased levels of PtCYP15 in explants of the hepatopancreas and ovary, while juvenile hormone III treatment reduced levels of PtCYP15 mRNA in ovary explants, suggesting that PtCYP15 might be involved in degrading methyl farnesoate. Furthermore, PtCYP15 mRNA expression levels were inhibited by adding juvenile hormone III to ovary explants. These findings provide foundational information for future research on methyl farnesoate metabolism in crustaceans.

Breathless through Time: Oxygen and Animals across Earth’s History

Abstract: Oxygen levels in the atmosphere and ocean have changed dramatically over Earth history, with major impacts on marine life. Because the early part of Earth’s history lacked both atmospheric oxygen and animals, a persistent co-evolutionary narrative has developed linking oxygen change with changes in animal diversity. Although it was long believed that oxygen rose to essentially modern levels around the Cambrian period, a more muted increase is now believed likely. Thus, if oxygen increase facilitated the Cambrian explosion, it did so by crossing critical ecological thresholds at low O2. Atmospheric oxygen likely remained at low or moderate levels through the early Paleozoic era, and this likely contributed to high metazoan extinction rates until oxygen finally rose to modern levels in the later Paleozoic. After this point, ocean deoxygenation (and marine mass extinctions) is increasingly linked to large igneous province eruptions—massive volcanic carbon inputs to the Earth system that caused global warming, ocean acidification, and oxygen loss. Although the timescales of these ancient events limit their utility as exact analogs for modern anthropogenic global change, the clear message from the geologic record is that large and rapid CO2 injections into the Earth system consistently cause the same deadly trio of stressors that are observed today. The next frontier in understanding the impact of oxygen changes (or, more broadly, temperature-dependent hypoxia) in deep time requires approaches from ecophysiology that will help conservation biologists better calibrate the response of the biosphere at large taxonomic, spatial, and temporal scales.

Controversial Roles of Oxygen in Organismal Responses to Climate Warming

Abstract: Despite the global ecological importance of climate change, controversy surrounds how oxygen affects the fate of aquatic ectotherms under warming. Disagreements extend to the nature of oxygen bioavailability and whether oxygen usually limits growth under warming, explaining smaller adult size. These controversies affect two influential hypotheses: gill oxygen limitation and oxygen- and capacity-limited thermal tolerance. Here, we promote deeper integration of physiological and evolutionary mechanisms. We first clarify the nature of oxygen bioavailability in water, developing a new mass-transfer model that can be adapted to compare warming impacts on organisms with different respiratory systems and flow regimes. By distinguishing aerobic energy costs of moving oxygen from environment to tissues from costs of all other functions, we predict a decline in energy-dependent fitness during hypoxia despite approximately constant total metabolic rate before reaching critically low environmental oxygen. A new measure of oxygen bioavailability that keeps costs of generating water convection constant predicts a higher thermal sensitivity of oxygen uptake in an amphipod model than do previous oxygen supply indices. More importantly, by incorporating size- and temperature-dependent costs of generating water flow, we propose that oxygen limitation at different body sizes and temperatures can be modeled mechanistically. We then report little evidence for oxygen limitation of growth and adult size under benign warming. Yet occasional oxygen limitation, we argue, may, along with other selective pressures, help maintain adaptive plastic responses to warming. Finally, we discuss how to overcome flaws in a commonly used growth model that undermine predictions of warming impacts.

Mechanistic Temperature-Size Rule Explanation Should Reconcile Physiological and Mortality Responses to Temperature

Abstract: The temperature-size rule is one of the universal rules in ecology and states that ectotherms in warmer waters will grow faster as juveniles, mature at smaller sizes and younger ages, and reach smaller maximum body sizes. Many models have unsuccessfully attempted to reproduce temperature-size rule-consistent life histories by using two-term (anabolism and catabolism) Pütter-type growth models, such as the von Bertalanffy. Here, we present a physiologically structured individual growth model, which incorporates an energy budget and optimizes energy allocation to growth, reproduction, and reserves. Growth, maturation, and reproductive output emerge as a result of life-history optimization to specific physiological rates and mortality conditions. To assess which processes can lead to temperature-size rule-type life histories, we simulate 42 scenarios that differ in temperature and body size dependencies of intake, metabolism, and mortality rates. Results show that the temperature-size rule can emerge in two ways. The first way requires both intake and metabolism to increase with temperature, but the temperature-body size interaction of the two rates must lead to relatively faster intake increase in small individuals and relatively larger metabolism increase in large ones. The second way requires only higher temperature-driven natural mortality and faster intake rates in early life (no change in metabolic rates is needed). This selects for faster life histories with earlier maturation and increased reproductive output. Our model provides a novel mechanistic and evolutionary framework for identifying the conditions necessary for the temperature-size rule. It shows that the temperature-size rule is likely to reflect both physiological changes and life-history optimization and that use of von Bertalanffy-type models, which do not include reproduction processes, can hinder our ability to understand and predict ectotherm responses to climate change.

Experimental Evolution Shows Body Size Decrease in Response to Hypoxia, with a Complex Effect on Plastic Size Response to Temperature

Abstract: There is a scientific debate whether oxygen concentration may be a factor driving the pattern of size decrease at higher temperature. Central to this debate is the fact that oxygen availability relative to demand for living organisms decreases with increasing temperature. We examined whether rotifers Lecane inermis exposed to hypoxic conditions would evolve smaller sizes than rotifers exposed to normoxic conditions, using experimental evolution with the same fluctuating temperature but differentiated by three regimes of oxygen availability: normoxia, hypoxia throughout the whole thermal range, and hypoxia only at the highest temperature. Immediately after the six-month experiment (more than 90 generations), we tested the plasticity of size responses to temperature in three post-evolution groups, and we related these responses to fitness. The results show that normoxic rotifers had evolved significantly larger sizes than two hypoxic rotifer groups, which were similar in size. All three groups displayed similar plastic body size reductions in response to warming over the range of temperatures they were exposed to during the period of experimental evolution, but they showed different and complex responses at two temperatures below this range. Any type of plastic response to different temperatures resulted in a similar fitness pattern across post-evolution groups. We conclude that (i) these rotifers showed a genetic basis for the pattern of size decrease following evolution under both temperature-dependent and temperature-independent hypoxia; and (ii) plastic body size responds consistently to temperatures that are within the thermal range that the rotifers experienced during their evolutionary history, but responses become more noisy at novel temperatures, suggesting the importance of evolutionary responses to reliable environmental cues.

Interactive Effects of Increasing Temperature and Decreasing Oxygen on Coastal Copepods

Abstract: The copepods of coastal seas are experiencing warming water temperatures, which increase their oxygen demand. In addition, many coastal seas are also losing oxygen because of deoxygenation due to cultural eutrophication. Warming coastal seas have changed copepod species’ composition and biogeographic boundaries and, in many cases, resulted in copepod communities that have shifted in size distribution to smaller species. While increases in ambient water temperatures can explain some of these changes, deoxygenation has also been shown to result in reduced copepod growth rates, reduced size at adulthood, and altered species composition. In this review we focus on the interactive effects of temperature and dissolved oxygen on pelagic copepods, which dominate coastal zooplankton communities. The uniformity in ellipsoidal shape, the lack of external oxygen uptake organs, and the pathway of oxygen uptake through the copepod’s integument make calanoid copepods ideal candidates for testing the use of an allometric approach to predict copepod size with increasing water temperatures and decreasing oxygen in coastal seas. Considering oxygen and temperature as a combined and interactive driver in coastal ecosystems will provide a unifying approach for future predictions of coastal copepod communities and their impact on fisheries and biogeochemical cycles. Given the prospect of increased oxygen limitation of copepods in warming seas, increased knowledge of the physiological ecology of present-day copepods in coastal deoxygenated zones can provide insights into the copepod communities that will inhabit a future warmer ocean.

Microbiome and Metabolome Contributions to Coral Health and Disease

Abstract: Coral populations are declining worldwide as a result of increased environmental stressors, including disease. Coral health is greatly dependent on complex interactions between the host animal and its associated microbial symbionts. While relatively understudied, there is growing evidence that the coral microbiome contributes to the health and resilience of corals in a variety of ways, similar to more well-studied systems, such as the human microbiome. Many of these interactions are dependent upon the production and exchange of natural products, including antibacterial compounds, quorum-sensing molecules, internal signaling molecules, nutrients, and so on. While advances in sequencing, culturing, and metabolomic techniques have aided in moving forward the understanding of coral microbiome interactions, current sequence and metabolite databases are lacking, hindering detailed descriptions of the microbes and metabolites involved. This review focuses on the roles of coral microbiomes in health and disease processes of coral hosts, with special attention to the coral metabolome. We discuss what is currently known about the relationship between the coral microbiome and disease, of beneficial microbial products or services, and how the manipulation of the coral microbiome may chemically benefit the coral host against disease. Understanding coral microbiome-metabolome interactions is critical to assisting management, conservation, and restoration strategies.

Ecological Review of the Ciona Species Complex

Abstract: The set of four closely related solitary ascidians Ciona spp. were once considered a single cosmopolitan species, Ciona intestinalis, but are now recognized as genetically and morphologically distinct species. The possibility of ecological differences between the species was not widely considered in studies preceding the schism of Ciona spp. Consequently, there may be an over-generalization of the ecology of Ciona spp., with potential implications for the broad range of studies targeting these species, encompassing the evolution, development, genomics, and invasion biology of Ciona spp. We completed a comprehensive review of the ecology of Ciona spp. to establish the similarities and differences between the widely distributed Ciona robusta and C. intestinalis (and what little is known of the two other species, Ciona sp. C and Ciona sp. D). When necessary, we used study locations and the species’ geographic ranges to infer the species in each study in the review. As expected, ecological similarities are the norm between the two species, spanning both abiotic and biotic interactions. However, there are also important differences that have potential implications for other aspects of the biology of Ciona spp. For example, differences in temperature and salinity tolerances likely correspond with the disparities in the geographic distribution of the species. Asymmetries in topics studied in each species diminish our ability to fully compare several aspects of the ecology of Ciona spp. and are priority areas for future research. We anticipate that our clarification of common and unique aspects of each species’ ecology will help to provide context for future research in many aspects of the biology of Ciona spp.

Immune Defense in Hypoxic Waters: Impacts of CO2 Acidification

Abstract: Periodic episodes of low oxygen (hypoxia) and elevated CO2 (hypercapnia) accompanied by low pH occur naturally in estuarine environments. Under the influence of climate change, the geographic range and intensity of hypoxia and hypercapnic hypoxia are predicted to increase, potentially jeopardizing the survival of economically and ecologically important organisms that use estuaries as habitat and nursery grounds. In this review we synthesize data from published studies that evaluate the impact of hypoxia and hypercapnic hypoxia on the ability of crustaceans and bivalve molluscs to defend themselves against potential microbial pathogens. Available data indicate that hypoxia generally has suppressive effects on host immunity against bacterial pathogens as measured by in vitro and in vivo assays. Few studies have documented the effects of hypercapnic hypoxia on crustaceans or bivalve immune defense, with a range of outcomes suggesting that added CO2 might have additive, negative, or no interactions with the effects of hypoxia alone. This synthesis points to the need for more partial pressure of O2 × low pH factorial design experiments and recommends the development of new host∶pathogen challenge models incorporating natural transmission of a wide range of viruses, bacteria, and parasites, along with novel in vivo tracking systems that better quantify how pathogens interact with their hosts in real time under laboratory and field conditions.

Structure-Function Relationships of Oxygen Transport Proteins in Marine Invertebrates Enduring Higher Temperatures and Deoxygenation

Abstract: Predictions for climate change—to lesser and greater extents—reveal a common scenario in which marine waters are characterized by a deadly trio of stressors: higher temperatures, lower oxygen levels, and acidification. Ectothermic taxa that inhabit coastal waters, such as shellfish, are vulnerable to rapid and prolonged environmental disturbances, such as heatwaves, pollution-induced eutrophication, and dysoxia. Oxygen transport capacity of the hemolymph (blood equivalent) is considered the proximal driver of thermotolerance and respiration in many invertebrates. Moreover, maintaining homeostasis under environmental duress is inextricably linked to the activities of the hemolymph-based oxygen transport or binding proteins. Several protein groups fulfill this role in marine invertebrates: copper-based extracellular hemocyanins, iron-based intracellular hemoglobins and hemerythrins, and giant extracellular hemoglobins. In this brief text, we revisit the distribution and multifunctional properties of oxygen transport proteins, notably hemocyanins, in the context of climate change, and the consequent physiological reprogramming of marine invertebrates.

Factors Modulating the Female Reproductive Performance of the Fiddler Crab <i>Leptuca uruguayensis</i> with Short Reproductive Season

Abstract: AbstractThis study aimed to evaluate the factors modulating the female reproductive performance of the fiddler crab Leptuca uruguayensis (Nobili, 1901) during the short reproductive season of a temperate population. We proposed two modulating factors: the age of females (young and old) and the periods of the reproductive season (beginning, middle, and end); we then evaluated the fecundity, reproductive output, egg volume, and biochemical composition of eggs. The fecundity of L. uruguayensis was affected by the size of females, a variable related to their age. Although young females showed lower fecundity, the reproductive output was not affected by the age or by the periods of the reproductive season, suggesting a constant reproductive effort, proportional to female size. The egg volume decreased, and carotenoid content increased at the end of the season for both female ages, probably as a consequence of variations in food availability and changes in the breeding strategies during the season. However, the content of protein and lipids in the egg clutches decreased at the end of the season only in old females spawning for the second time in the season. The main differences in the reproductive parameters were recorded between the beginning and the end of the reproductive season, probably because in these periods females exclusively use one of the breeding strategies. Finally, we determined that both factors, that is, female age and the periods of the short reproductive season, can modulate the reproductive performance of L. uruguayensis in temperate estuaries.

Uncovering the Effects of Symbiosis and Temperature on Coral Calcification

Abstract: We tested the impact of temperature and symbiont state on calcification in corals, using the facultatively symbiotic coral Astrangia poculata as a model system. Symbiotic and aposymbiotic colonies of A. poculata were reared in 15, 20, and 27 °C conditions. We used scanning electron microscopy to quantify how these physiological and environmental conditions impact skeletal structure. Buoyant weight data over time revealed that temperature significantly affects calcification rates. Scanning electron microscopy of A. poculata skeletons showed that aposymbiotic colonies appear to have a lower density of calcium carbonate in actively growing septal spines. We describe a novel approach to analyze the roughness and texture of scanning electron microscopy images. Quantitative analysis of the roughness of septal spines revealed that aposymbiotic colonies have a rougher surface than symbiotic colonies in tropical conditions (27 °C). This trend reversed at 15 °C, a temperature at which the symbionts of A. poculata may exhibit parasitic properties. Analysis of surface texture patterns showed that temperature impacts the spatial variance of crystals on the spine surface. Few published studies have examined the skeleton of A. poculata by using scanning electron microscopy. Our approach provides a way to study detailed changes in skeletal microstructure in response to environmental parameters and can serve as a proxy for more expensive and time-consuming analyses. Utilizing a facultatively symbiotic coral that is native to both temperate and tropical regions provides new insights into the impact of both symbiosis and temperature on calcification in corals.

Multigenerational Life-History Responses to pH in Distinct Populations of the Copepod Tigriopus californicus

Abstract: Intertidal zones are highly dynamic and harsh habitats: organisms that persist there must face many stressors, including drastic changes in seawater pH, which can be strongly influenced by biological processes. Coastal ecosystems are heterogeneous in space and time, and populations can be exposed to distinct selective pressures and evolve different capacities for acclimation to changes in pH. Tigriopus californicus is a harpacticoid copepod found in high-shore rock pools on the west coast of North America. It is a model system for studying population dynamics in diverse environments, but little is known about its responses to changes in seawater pH. I quantified the effects of pH on the survivorship, fecundity, and development of four T. californicus populations from San Juan Island, Washington, across three generations. For all populations and generations, copepod cultures had lower survivorship and delayed development under extended exposure to higher pH treatments (pH 7.5 and pH 8.0), whereas cultures maintained in lower pH (7.0) displayed stable population growth over time. Reciprocal transplants between treatments demonstrated that these pH effects were reversible. Life histories were distinct between populations, and there were differences in the magnitudes of pH effects on development and culture growth that persisted through multiple generations. These results suggest that T. californicus might not have the generalist physiology that might be expected of an intertidal species, and it could be adapted to lower average pH conditions than those that occur in adjacent open waters.

Opsins in the Cephalic and Extracephalic Photoreceptors in the Marine Gastropod Onchidium verruculatum

Abstract: The marine gastropod Onchidium verruculatum has a pair of ocular photoreceptors, the stalk eyes, on the tip of its stalk near the head, as well as several extracephalic photosensory organs. The retinas of the stalk eye consist of two morphologically distinct visual cells, namely, the type I cells equipped with well-developed microvilli and the type II cells with less developed microvilli. The extracephalic photosensors comprise the dorsal eye, dermal photoreceptor, and brain photosensitive neurons. The characteristics of these cephalic and extracephalic photosensory organs have been studied from morphological and electrophysiological perspectives. However, little is known about the visual pigment molecules responsible for light detection in these organs. In the present study, we searched for opsin molecules that are expressed in the neural tissues of Onchidium and identified six putative signaling-competent opsin species, including Xenopsin1, Xenopsin2, Gq-coupled rhodopsin1, Gq-coupled rhodopsin2, Opsin-5B, and Gq-coupled rhodopsin-like. Immunohistochemical staining of four of the six opsins revealed that Xenopsin1, Gq-coupled rhodopsin1, and Gq-coupled rhodopsin2 are expressed in the rhabdomere of the stalk eye and in the dermal photoreceptor. Xenopsin2 was expressed in the type II photoreceptors of the stalk eye and in the ciliary photoreceptors of the dorsal eye. These immunohistochemical data were consistent with the results of the expression analysis, revealed by quantitative reverse transcription polymerase chain reaction. This study clarified the identities of opsins expressed in the extracephalic photosensory organs of Onchidium and the distinct molecular compositions among the photoreceptors.

Growth and Cyclin-E Expression in the Stony Coral Species Orbicella faveolata Post-Microfragmentation

Abstract: Coral growth is critical to reef health, resilience under rapidly changing environmental conditions, and restoration efforts. Although fragmenting coral has been occurring for many years in an effort to restore reefs, recently it was discovered that microfragmenting, the process of cutting one piece of coral into many small pieces (about three to five polyps), induces exponential growth. Our study investigates the process by which microfragments of nine different genotypes from the stony coral species Orbicella faveolata grow and exhibit Cyclin-E expression. Microfragments were examined by using a high-powered dissecting microscope with a camera to document the precise areas of tissue exhibiting exponential growth. We found that new polyp formation occurs only on the microfragment edges and that edge polyp growth rates varied between different genotypes. We then extracted tissue from both the edge and the center of five genotypes for genetic analysis. We chose to analyze Cyclin-E expression because it is involved with stimulating mitotic division and is a conserved signaling pathway that is known to exist in Drosophila, mammals, and Cnidaria. Two primers for Cyclin-E were utilized to examine the level of expression for center and edge tissue. We found that Cyclin-E is expressed differentially between O. faveolata polyps, with a tendency for increased expression of the Cyclin-E in edge versus center tissue in each of five genotypes, although this result was not significant. Despite consistently higher levels of Cyclin-E expression within an organism’s edge tissue, genotypes varied significantly in the degree of increased expression. This variation positively correlated with growth rate, suggesting the potential for molecular selection in aid of more rapid reef restoration. Future work will focus on deciphering the specific growth pathways involved in microfragmented coral growth and analyzing expression patterns in injured tissues.

Monogamy in the Burrowing Shrimp Axianassa australis Rodrigues & Shimizu, 1992 (Decapoda, Gebiidea, Axianassidae)

Abstract: Our knowledge of the mating systems in burrowing shrimps (infraorders Axiidea and Gebiidea) is still rather limited. Here we describe the burrow use pattern, sex ratio, and sexual dimorphism of the burrowing shrimp Axianassa australis to test for monogamy, considering that monogamous species live in heterosexual pairs and exhibit a low degree of sexual dimorphism. To this end, a total of 226 individuals of A. australis were collected from the northeast region of Brazil. Our results showed that A. australis inhabited its burrows mainly as pairs, most of which were male-female pairs. In agreement with the expectations, specimens of A. australis were found dwelling as heterosexual pairs more frequently than expected by chance alone. The presence of ovigerous females was associated with the burrow occupation; that is, brooding females were more frequently observed in male-female combinations than solitarily. Also supporting theoretical considerations, we did not observe sexual dimorphism in body size between males and females of the population and the different categories of the burrow occupation. Conversely, sexual dimorphism in cheliped size was evident in the population, with larger chelipeds in males than in females. This observation agrees with that reported for most burrowing shrimps in which male-male competition is the main evolutionary force of sexual selection. The observations above favor the hypothesis that A. australis is primarily monogamous, with a small fraction of the males moderately promiscuous.

Is It in the Stars? Exploring the Relationships between Species’ Traits and Sea Star Wasting Disease

Abstract: An explanation for variation in impacts of sea star wasting disease across asteroid species remains elusive. Although various traits have been suggested to play a potential role in sea star wasting susceptibility, currently we lack a thorough comparison that explores how life-history and natural history traits shape responses to mass mortality across diverse asteroid taxa. To explore how asteroid traits may relate to sea star wasting, using available data and recognizing the potential for biological correlations to be driven by phylogeny, we generated a supertree, tested traits for phylogenetic association, and evaluated associations between traits and sea star wasting impact. Our analyses show no evidence for a phylogenetic association with sea star wasting impact, but there does appear to be phylogenetic association for a subset of asteroid life-history traits, including diet, substrate, and reproductive season. We found no relationship between sea star wasting and developmental mode, diet, pelagic larval duration, or substrate but did find a relationship with minimum depth, reproductive season, and rugosity (or surface complexity). Species with the greatest sea star wasting impacts tend to have shallower minimum depth distributions, they tend to have their median reproductive period 1.5 months earlier, and they tend to have higher rugosities relative to species less affected by sea star wasting. Fully understanding sea star wasting remains challenging, in part because dramatic gaps still exist in our understanding of the basic biology and phylogeny of asteroids. Future studies would benefit from a more robust phylogenetic understanding of sea stars, as well as leveraging intra- and interspecific comparative transcriptomics and genomics to elucidate the molecular pathways responding to sea star wasting.

Population and Reproductive Dynamics of Zebra Mussels (Dreissena polymorpha) in Warm, Low-Latitude North American Waters

Abstract: Zebra mussels (Dreissena polymorpha), first reported in Texas during 2009, have infested 28 Texas reservoirs over 11 years. This species has not previously invaded water bodies as warm as those in Texas, where temperatures approach or exceed its previously accepted incipient upper thermal limit of 30 °C, raising the question of how such temperatures impact its population dynamics. Over 3–5 years, monthly collections of mussels, sampling for planktonic mussel veligers, juvenile settlement data, and water quality parameters, were undertaken at Texas lakes Texoma, Ray Roberts, and Belton to estimate mussel shell length growth rates, life spans, reproductive periods, and settlement patterns. Biannual spawning periods occurred at water temperatures of 18 to 28 °C, resulting in distinct spring and fall juvenile settlement cohorts. Growth rates were rapid, with both cohorts attaining mean maximum shell lengths of 20–25 mm within 8–15 months of settlement, compared to European and northeastern US populations that attained similar sizes after 2–4 years. Shortened life spans were demarcated by adult mussel die-offs during summer months of elevated water temperature the year after initial settlement, leading to short-term cyclical fluctuations in population densities. Large-scale mussel die-offs were caused by flooding and hypoxia events. Elevated temperatures appeared to facilitate mussel invasiveness by increasing spawning frequency and elevating growth rates, thus reducing time to maturity and allowing population recovery within 1–2 years after environmentally induced severe population declines.

Compound Extreme Events Induce Rapid Mortality in a Tropical Sea Urchin

Abstract: The frequency, magnitude, and duration of marine heatwaves and deoxygenation events are increasing globally. Recent research suggests that their co-occurrence is more common than previously thought and that their combination can have rapid, dire biological impacts. We used the sea urchin Echinometra lucunter to determine whether mortality occurs faster when deoxygenation events are combined with extreme heating (compound events), compared to deoxygenation events alone. We also tested whether prior exposure to local heatwave conditions accentuates the impacts of compound events. Animals were first exposed for five days to either ambient temperature (28 °C) or a warmer temperature that met the minimum criteria for a local heatwave (30.5 °C). Animals were then exposed to hypoxia, defined as oxygen levels 35% below their average critical oxygen limit, combined with ambient or extreme field temperatures (28 °C, 32 °C). Subsets of animals were removed from the hypoxic treatments every 3 hours for 24 hours to determine how long they could survive. Prior exposure to heatwave conditions did not help or hinder survival under hypoxic conditions, and animals exposed to hypoxia under ambient temperatures experienced little mortality. However, when hypoxia was coupled with extreme temperatures (32 °C), 55% of the animals died within 24 hours. On the reefs at our Panama study site, we found that extreme hypoxic conditions only ever occurred during marine heatwave events, with four compound events occurring in 2018. These results show that short durations (∼1 day) of compound events can be catastrophic and that increases in their duration will severely threaten sea urchin populations. La frecuencia, magnitud y duración de las olas de calor marinas y los eventos de desoxigenación están aumentando a nivel mundial. Investigaciones recientes sugieren que su coocurrencia es más común de lo que se pensaba anteriormente y que su combinación puede tener impactos biológicos rápidos y nefastos. Usamos el erizo de mar Echinometra lucunter para determinar si la mortalidad de estos ocurre más rápido cuando los eventos de desoxigenación se combinan con un calentamiento extremo (eventos compuestos), en comparación con los eventos de desoxigenación solos. También probamos si la exposición previa a las condiciones locales de olas de calor acentúa los impactos de los eventos compuestos. Primero se expusieron a los animales durante cinco días a temperatura ambiente (28 °C) o una temperatura más cálida que cumpliera con los criterios mínimos para una ola de calor local (30.5 °C). Luego, los animales se expusieron a hipoxia, definida como niveles de oxígeno un 35% por debajo de su límite de oxígeno crítico promedio, combinado con temperaturas ambientales o de campo extremas (28 °C, 32 °C). Se retiraron los subconjuntos de animales de los tratamientos hipóxicos cada 3 horas durante 24 horas para determinar los tiempos de supervivencia. La exposición previa a condiciones de olas de calor no ayudó ni obstaculizó la supervivencia en condiciones hipóxicas, y los animales expuestos a hipoxia en temperatura ambiente experimentaron poca mortalidad. Sin embargo, cuando la hipoxia se combinó con temperaturas extremas (32 °C), el 55% de los animales murió en 24 horas. Las condiciones compuestas en nuestro sitio de estudio en Panamá fueron poco frecuentes y cortas (3 horas). Pero cuando ocurrieron, fueron durante olas de calor marinas, con un total de cuatro eventos compuestos observados en los arrecifes locales durante las olas de calor en 2018. Estos resultados muestran que las duraciones cortas (∼1 día) de eventos compuestos pueden ser catastróficas y aumentar debido al calentamiento, en su duración amenazarán severamente las poblaciones de erizos de mar.

Scope for Developmental Plasticity of Feeding Larvae of a Holothuroid, Contrasted with Other Echinoderm Larvae

Abstract: Feeding larvae of echinoderms appear to differ in scope for adaptive developmental plasticity in response to food. Extension of the ciliary band on narrow arms supported by skeletal rods, as in echinoid and ophiuroid larvae, may enable a greater increase in maximum clearance rate per cell added, conferring greater advantages from developing longer ciliary bands when food is scarce. Formation of the juvenile mouth and water vascular system at a new site, as in echinoid and asteroid larvae, permits extensive growth of the juvenile rudiment during larval feeding, with advantages from earlier or more growth of the rudiment when food is abundant. In contrast, plasticity in storage of nutrients is unrelated to the form of the ciliary band or the site of formation of the juvenile’s mouth. Feeding larvae (auriculariae) of holothuroids lack arms supported by skeletal rods and formation of the mouth at a new site but as a unique feature store nutrients in hyaline spheres. In this study, more food for auriculariae of Apostichopus californicus resulted in juveniles (pentactulae) with longer and wider bodies and larger hyaline spheres, but effects of food supply on the size of most body parts of auriculariae were small. Auriculariae with more food developed relatively larger stomachs and larger posterior hyaline spheres, indications of greater nutrient storage. Auriculariae with less food developed relatively wider mouths and differed in some exterior dimensions, which might enhance the capture of food. Plasticity is limited in rudiment development and perhaps in structures for feeding, but plasticity in nutrient storage can provide advantageous compromises between duration of growth as a feeding larva and the condition of juveniles formed at metamorphosis.

Genetic Evidence Supports Species Delimitation of Luidia in the Northern Gulf of Mexico

Abstract: Accurate species delimitation is crucial to understanding biodiversity. In the northern Gulf of Mexico, recent genetic evidence has suggested that the tricolor Luidia lawrencei is not a species distinct from the gray Luidia clathrata. We collected Luidia specimens from Apalachee Bay, Florida, and morphologically identified 11 as L. clathrata and 16 as L. lawrencei. We sequenced 1074 bp of the cytochrome c oxidase subunit I (COI) and found ~14% divergence between L. clathrata and L. lawrencei, suggesting two distinct species (within-species divergence was <1%). Two specimens were phenotypically L. lawrencei (i.e., tricolor morph) but mitochondrially were L. clathrata. Our findings lend support to maintaining L. clathrata and L. lawrencei as distinct species. However, the species boundary between these two taxa may be porous, and ongoing hybridization may occur when the two species are found in sympatry. Future work with nuclear markers is warranted to determine the frequency of hybridization and the extent of introgression. Clarifying the genetic relationship between these species will provide a baseline for assessing ongoing changes in connectivity of these two highly abundant sea stars in the rapidly warming northern Gulf of Mexico.

About the Cover

Abstract: Next article FreeAbout the CoverPDFPDF PLUSFull Text Add to favoritesDownload CitationTrack CitationsPermissionsReprints Share onFacebookTwitterLinked InRedditEmailQR Code SectionsMoreA defining feature of echinoderms is their five-fold symmetry, which arises during the metamorphosis of a bilaterally symmetrical larva. During echinoderm metamorphosis, the coelomic cavities undergo an elaborate transformation from early mesodermal pouches to a complex system of tubes and rings that make up the numerous internal components of the animal. In this issue (pp. 283–298), H. C. Sweet and several undergraduate research students (G. Azriel, N. Jaff, J. Moser, T. A. Riola, C. Ideman, M. Barton, J. Nelson, and M. M. Lenhart) demonstrate the origin of the coelomic structures and their morphogenesis in the vitellaria larva of the brittle star Ophioplocus esmarki. Many of the structures first form when the archenteron becomes subdivided into an unpaired axocoel, hydrocoel, somatocoel, and stomach rudiment. The right somatocoel and part of the left somatocoel originate as bilateral invaginations of the larval ectoderm. This supports the findings of others that ectodermal invagination of the somatocoels is an unusual feature of brittle star development. Confocal microscopy and 3D modeling were used to document the later morphogenesis of the coelomic cavities as they form juvenile structures with five-fold symmetry.The cover image demonstrates the complex structure of the vitellaria larva. The image shows the color-coded coelomic cavities superimposed with an image of the skeleton and an outline of body of the vitellaria larva. At this stage, the outer ectoderm has ciliary bands on raised ridges that are used for swimming (grayscale outline), but most of the internal structures are patterned in five-fold symmetry with the axial complex near the anterior end (top). Coelomic structures include the water vascular system derived from the hydrocoel (yellow), hypogastric coelom derived from the left somatocoel (purple), genital coelom (peach) derived from the left somatocoel, epigastric coelom derived from the right somatocoel (magenta), pericardial coelom (green), axial coelom (orange), and pore canal (red). The juvenile skeletal plates form adjacent to the coelomic structures and the overlying ectoderm. The image was generated with confocal microscopy, polarized light imaging, and image colorizing and processing in GIMP and Fiji.Credits: Photo, Hyla C. Sweet; cover design, Olivia Kinker. Next article DetailsFiguresReferencesCited by The Biological Bulletin Volume 243, Number 3December 2022 Published in association with the Marine Biological Laboratory Article DOIhttps://doi.org/10.1086/724434 © 2022 The University of Chicago. All rights reserved.PDF download Crossref reports no articles citing this article.

About the Cover

Abstract: Next article FreeAbout the CoverPDFPDF PLUSFull Text Add to favoritesDownload CitationTrack CitationsPermissionsReprints Share onFacebookTwitterLinkedInRedditEmailPrint SectionsMoreThe cover image depicts the color plate for Crepidula from Sowerby’s Thesaurus Conchyliorum, volume 5 of Genera of Shells. Commonly referred to as slipper shell snails, members of this group are protandrous sequential hermaphrodites, starting sexual maturity as males and transitioning to females later in life.In this issue (pages 238–249) N. L. Kleinas and J. M. Carroll explore whether the timing of sex change in Crepidula fornicata is impacted by the presence of a biotic stressor, the boring sponge Cliona celata. Previous research demonstrates that the boring sponge can affect growth and condition of several mollusc species, including gastropods, likely due to the energetic costs of repairing damaged shell. Using both field surveys and an in situ experiment, the authors demonstrate variability in the response of C. fornicata to the boring sponge, but no biologically relevant differences in sex change between sponge-infested and uninfested individuals. Therefore, the reproductive strategy of C. fornicata appears robust to this biotic stressor.And on pages 222–237, M. Castelin, R. Collin, R. Harbo, E. Spence, K. Aschenbrenner, W. Merilees, S. R. Gilmore, C. Abbott, and D. J. Eernisse test the historical hypothesis that Crepidula adunca and Crepidula norrisiarum, both abundant in the northeastern Pacific, are two allopatric species that live on different hosts and differ in body size. They show that the taxonomy of C. adunca and C. norrisiarum has been confused, especially in the northern part of the range where all small-bodied animals were previously identified as C. adunca. Their observations lay groundwork for a new hypothesis that shell morphology and body size are not species-specific traits but reflect regional differences in habitat, host use, and host availability.Credits: G. B. Sowerby, Thesaurus Conchyliorum, Monographs in Genera of Shells, 1840–1887, public domain via Wikimedia Commons. Cover design: Olivia Kinker, University of Chicago Press. Next article DetailsFiguresReferencesCited by The Biological Bulletin Volume 242, Number 3June 2022 Published in association with the Marine Biological Laboratory Article DOIhttps://doi.org/10.1086/721608 Views: 384Total views on this site © 2022 The University of Chicago. All rights reserved.PDF download Crossref reports no articles citing this article.

The Influence of Natural Barriers on the Amphidromous Shrimp Potimirim brasiliana (Caridea, Atyidae) from Two Rivers in Southeastern Brazil

Abstract: The migratory behavior of freshwater shrimps may be affected by natural barriers in limnetic environments. This study evaluated the river areas separated by natural barriers, such as waterfalls, which affect the amphidromous shrimps’ (Potimirim brasiliana) population features and reproductive aspects. Results indicate that in the Félix and Prumirim Rivers from southeastern Brazil shrimps show few differences in sampling areas, and these differences may not be causally related to the waterfalls. This is demonstrated by the absence of a pattern in the size and sex ratio in each area and the absence of a significant difference in most reproductive aspects. The presence of juveniles and reproductive individuals in all sampling areas strongly indicates a constant migration along them in both rivers, indicating that all individuals evaluated correspond to one single patchy population structure for each river. This migration conducted by P. brasiliana, such as its crawling behavior, demonstrated that it would be important to maintain the minimum number of individuals flowing between the different river sampling areas in this shrimp group. Thus, based on a helpful model observed in P. brasiliana, the results help us understand how natural barriers may affect the populations of amphidromous shrimp and how the migration behavior up- and downstream can help sustain the population. This premise can help future construction decisions and impacts of unnatural barriers, such as dams.