Sea star wasting syndrome reaches the high Antarctic: Two recent outbreaks in McMurdo Sound.

Sea star wasting syndrome (SSWS) can cause widespread mortality in starfish populations as well as long-lasting changes to benthic community structure and dynamics. SSWS symptoms have been documented in numerous species and locations around the world, but to date there is only one record of SSWS from the Antarctic and this outbreak was associated with volcanically-driven high temperature anomalies. Here we report outbreaks of SSWS-like symptoms that affected ~30% of individuals of Odontaster validus at two different sites in McMurdo Sound, Antarctica in 2019 and 2022. Unlike many SSWS events in other parts of the world, these outbreaks were not associated with anomalously warm temperatures. Instead, we suggest they may have been triggered by high nutrient input events on a local scale. Although the exact cause of these outbreaks is not known, these findings are of great concern because of the keystone role of O. validus and the slow recovery rate of Antarctic benthic ecosystems to environmental stressors.

Integrative Approaches to Understanding Organismal Responses to Aquatic Deoxygenation.

AbstractOxygen 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.

Phylogenomic Resolution of Sea Spider Diversification through Integration of Multiple Data Classes.

Despite significant advances in invertebrate phylogenomics over the past decade, the higher-level phylogeny of Pycnogonida (sea spiders) remains elusive. Due to the inaccessibility of some small-bodied lineages, few phylogenetic studies have sampled all sea spider families. Previous efforts based on a handful of genes have yielded unstable tree topologies. Here, we inferred the relationships of 89 sea spider species using targeted capture of the mitochondrial genome, 56 conserved exons, 101 ultraconserved elements, and 3 nuclear ribosomal genes. We inferred molecular divergence times by integrating morphological data for fossil species to calibrate 15 nodes in the arthropod tree of life. This integration of data classes resolved the basal topology of sea spiders with high support. The enigmatic family Austrodecidae was resolved as the sister group to the remaining Pycnogonida and the small-bodied family Rhynchothoracidae as the sister group of the robust-bodied family Pycnogonidae. Molecular divergence time estimation recovered a basal divergence of crown group sea spiders in the Ordovician. Comparison of diversification dynamics with other marine invertebrate taxa that originated in the Paleozoic suggests that sea spiders and some crustacean groups exhibit resilience to mass extinction episodes, relative to mollusk and echinoderm lineages.

Body Size of Temperate Sea Spiders: No Evidence of Oxygen-Temperature Limitations.

AbstractOxygen limitation has been proposed as one of the key factors that limits body size at high temperatures (the oxygen-temperature hypothesis). Geographic patterns in body size are thought to be driven in part by the effects of temperature on oxygen supply and demand, particularly when the increased oxygen demand of tissues at higher temperatures outpaces the ability of large organisms to supply internal tissues with oxygen. We tested the effects of temperature on the rate of oxygen consumption of two temperate sea spider (Pycnogonida) species, Achelia chelata and Achelia gracilipes, across a range of body sizes. We measured oxygen consumption at 5 temperatures: 12, 16, 20, 24, and 28 °C. Oxygen consumption of both species increased significantly with temperature, but the effect did not depend on body size; thus, we found no evidence to support the oxygen-temperature hypothesis. While previous interspecific studies on Antarctic pycnogonids have found that larger-bodied animals have more porous cuticles, thus potentially offsetting their higher aerobic metabolic demand by increasing oxygen diffusivity, the pore area of the cuticle of the two temperate species did not change with body size. This suggests that the generally small size of warm-water sea spiders may be due to selective factors other than oxygen limitation.

Reconsidering the Oxygen-Temperature Hypothesis of Polar Gigantism: Successes, Failures, and Nuance.

"Polar gigantism" describes a biogeographic pattern in which many ectotherms in polar seas are larger than their warmer-water relatives. Although many mechanisms have been proposed, one idea-the oxygen-temperature hypothesis-has received significant attention because it emerges from basic biophysical principles and is appealingly straightforward and testable. Low temperatures depress metabolic demand for oxygen more than supply of oxygen from the environment to the organism. This creates a greater ratio of oxygen supply to demand, releasing polar organisms from oxygen-based constraints on body size. Here we review evidence for and against the oxygen-temperature hypothesis. Some data suggest that larger-bodied taxa live closer to an oxygen limit, or that rising temperatures can challenge oxygen delivery systems; other data provide no evidence for interactions between body size, temperature, and oxygen sufficiency. We propose that these findings can be partially reconciled by recognizing that the oxygen-temperature hypothesis focuses primarily on passive movement of oxygen, implicitly ignoring other important processes including ventilation of respiratory surfaces or internal transport of oxygen by distribution systems. Thus, the hypothesis may apply most meaningfully to organisms with poorly developed physiological systems (eggs, embryos, egg masses, juveniles, or adults without mechanisms for ventilating internal or external surfaces). Finally, most tests of the oxygen-temperature hypothesis have involved short-term experiments. Many organisms can mount effective responses to physiological challenges over short time periods; however, the energetic cost of doing so may have impacts that appear only in the longer term. We therefore advocate a renewed focus on long-term studies of oxygen-temperature interactions.

Polar gigantism and the oxygen-temperature hypothesis: a test of upper thermal limits to body size in Antarctic pycnogonids.

The extreme and constant cold of the Southern Ocean has led to many unusual features of the Antarctic fauna. One of these, polar gigantism, is thought to have arisen from a combination of cold-driven low metabolic rates and high oxygen availability in the polar oceans (the 'oxygen-temperature hypothesis'). If the oxygen-temperature hypothesis indeed underlies polar gigantism, then polar giants may be particularly susceptible to warming temperatures. We tested the effects of temperature on performance using two genera of giant Antarctic sea spiders (Pycnogonida), Colossendeis and Ammothea, across a range of body sizes. We tested performance at four temperatures spanning ambient (-1.8°C) to 9°C. Individuals from both genera were highly sensitive to elevated temperature, but we found no evidence that large-bodied pycnogonids were more affected by elevated temperatures than small individuals; thus, these results do not support the predictions of the oxygen-temperature hypothesis. When we compared two species, Colossendeis megalonyx and Ammothea glacialis, C. megalonyx maintained performance at considerably higher temperatures. Analysis of the cuticle showed that as body size increases, porosity increases as well, especially in C. megalonyx, which may compensate for the increasing metabolic demand and longer diffusion distances of larger animals by facilitating diffusive oxygen supply.

Cuticular gas exchange by Antarctic sea spiders.

Many marine organisms and life stages lack specialized respiratory structures, like gills, and rely instead on cutaneous respiration, which they facilitate by having thin integuments. This respiratory mode may limit body size, especially if the integument also functions in support or locomotion. Pycnogonids, or sea spiders, are marine arthropods that lack gills and rely on cutaneous respiration but still grow to large sizes. Their cuticle contains pores, which may play a role in gas exchange. Here, we examined alternative paths of gas exchange in sea spiders: (1) oxygen diffuses across pores in the cuticle, a common mechanism in terrestrial eggshells, (2) oxygen diffuses directly across the cuticle, a common mechanism in small aquatic insects, or (3) oxygen diffuses across both pores and cuticle. We examined these possibilities by modeling diffusive oxygen fluxes across all pores in the body of sea spiders and asking whether those fluxes differed from measured metabolic rates. We estimated fluxes across pores using Fick's law parameterized with measurements of pore morphology and oxygen gradients. Modeled oxygen fluxes through pores closely matched oxygen consumption across a range of body sizes, which means the pores facilitate oxygen diffusion. Furthermore, pore volume scaled hypermetrically with body size, which helps larger species facilitate greater diffusive oxygen fluxes across their cuticle. This likely presents a functional trade-off between gas exchange and structural support, in which the cuticle must be thick enough to prevent buckling due to external forces but porous enough to allow sufficient gas exchange.

Upper limits to body size imposed by respiratory-structural trade-offs in Antarctic pycnogonids.

Across metazoa, surfaces for respiratory gas exchange are diverse, and the size of those surfaces scales with body size. In vertebrates with lungs and gills, surface area and thickness of the respiratory barrier set upper limits to rates of metabolism. Conversely, some organisms and life stages rely on cutaneous respiration, where the respiratory surface (skin, cuticle, eggshell) serves two primary functions: gas exchange and structural support. The surface must be thin and porous enough to transport gases but strong enough to withstand external forces. Here, we measured the scaling of surface area and cuticle thickness in Antarctic pycnogonids, a group that relies on cutaneous respiration. Surface area and cuticle thickness scaled isometrically, which may reflect the dual roles of cuticle in gas exchange and structural support. Unlike in vertebrates, the combined scaling of these variables did not match the scaling of metabolism. To resolve this mismatch, larger pycnogonids maintain steeper oxygen gradients and higher effective diffusion coefficients of oxygen in the cuticle. Interactions among scaling components lead to hard upper limits in body size, which pycnogonids could evade only with some other evolutionary innovation in how they exchange gases.

Respiratory gut peristalsis by sea spiders.

The fundamental constraint shaping animal systems for internal gas transport is the slow pace of diffusion [1]. In response, most macroscopic animals have evolved systems for driving internal flows using muscular pumps or cilia. In arthropods, aside from terrestrial lineages that exchange gases via tracheal systems, most taxa have a dorsal heart that drives O2-carrying hemolymph through peripheral vessels and an open hemocoel [2], with O2 often bound to respiratory proteins. Here we show that pycnogonids (sea spiders), a basal group of marine arthropods [3], use a previously undescribed mechanism of internal O2 transport: flows of gut fluids and hemolymph driven by peristaltic contractions of a space-filling system of gut diverticula. This observation fundamentally expands the known range of gas-transport systems in extant arthropods.

No Effects and No Control of Epibionts in Two Species of Temperate Pycnogonids.

Essentially all surfaces of marine plants and animals host epibionts. These organisms may harm their hosts in a number of ways, including impeding gas exchange or increasing the costs of locomotion. Epibionts can also be beneficial. For example, they may camouflage their hosts, and photosynthetic epibionts can produce oxygen. In general, however, the costs of epibionts appear to outweigh their benefits. Many organisms, therefore, shed epibionts by grooming, molting, or preventing them from initially attaching, using surface waxes and cuticular structures. In this study, we examined how epibionts affect local oxygen supply to temperate species of pycnogonids (sea spiders). We also tested the effectiveness of different methods that pycnogonids may use to control epibionts (grooming, cuticle wettability, and cuticular waxes). In two temperate species: Achelia chelata and Achelia gracilipes, epibionts consisted primarily of algae and diatoms, formed layers approximately 0.25-mm thick, and they colonized at least 75% of available surface area. We used microelectrodes to measure oxygen levels in and under the layers of epibionts. In bright light, these organisms produced high levels of oxygen; in the dark, they had no negative effect on local oxygen supply. We tested mechanisms of control of epibionts by pycnogonids in three ways: disabling their ovigers to prevent grooming, extracting wax layers from the cuticle, and measuring the wettability of the cuticle; however, none of these experiments affected epibiont coverage. These findings indicate that in temperate environments, epibionts are not costly to pycnogonids and, in some circumstances, they may be beneficial.

Out-of-the tropics or trans-tropical dispersal? The origins of the disjunct distribution of the gooseneck barnacle Pollicipes elegans.

BACKGROUND: Studying species with disjunct distributions allows biogeographers to evaluate factors controlling species ranges, limits on gene flow, and allopatric speciation. Here, we use phylogeographic and population genetic studies of the barnacle Pollicipes elegans to discriminate between two primary hypotheses about the origin of disjunct distributions of extra-tropical populations: trans-tropical stepping-stone colonization versus an out-of-the tropics origin. RESULTS: Nucleotide diversity peaked in the centre of the species' range in samples from El Salvador and was lower in samples from higher latitudes at Mexico and Peru. Haplotypes from El Salvador samples also had a deeper coalescent, or an older time to a most recent common ancestor. A deep phylogeographical break exists between Mexico and all samples taken to the south (El Salvador and Peru). Isolation-with-migration analyses showed no significant gene flow between any of the three regions indicating that the difference in genetic differentiation among all three regions is explained primarily by differences in population separation times. Approximate Bayesian Computation model testing found strong support for an out-of-the tropics origin of extra-tropical populations in P. elegans. CONCLUSIONS: We found little evidence consistent with a stepping-stone history of trans-tropical colonization, but instead found strong evidence for a tropical origin model for the largely disjunct distribution of P. elegans. Sea surface temperature and habitat suitability are likely mechanisms driving decline of populations in tropical regions, causing the disjunct distribution.

Relationships among egg size, composition, and energy: a comparative study of geminate sea urchins.

Egg size is one of the fundamental parameters in the life histories of marine organisms. However, few studies have examined the relationships among egg size, composition, and energetic content in a phylogenetically controlled context. We investigated the associations among egg size, composition, and energy using a comparative system, geminate species formed by the closure of the Central American Seaway. We examined western Atlantic (WA) and eastern Pacific (EP) species in three echinoid genera, Echinometra, Eucidaris, and Diadema. In the genus with the largest difference in egg size between geminates (Echinometra), the eggs of WA species were larger, lipid rich and protein poor compared to the smaller eggs of their EP geminate. In addition, the larger WA eggs had significantly greater total egg energy and summed biochemical constituents yet significantly lower egg energy density (energy-per-unit-volume). However, the genera with smaller (Eucidaris) or no (Diadema) differences in egg size were not significantly different in summed biochemical constituents, total egg energy, or energy density. Theoretical models generally assume a strong tradeoff between egg size and fecundity that limits energetic investment and constrains life history evolution. We show that even among closely-related taxa, large eggs cannot be assumed to be scaled-up small eggs either in terms of energy or composition. Although our data comes exclusively from echinoid echinoderms, this pattern may be generalizable to other marine invertebrate taxa. Because egg composition and egg size do not necessarily evolve in lockstep, selective factors such as sperm limitation could act on egg volume without necessarily affecting maternal or larval energetics.

Why might they be giants? Towards an understanding of polar gigantism.

Beginning with the earliest expeditions to the poles, over 100 years ago, scientists have compiled an impressive list of polar taxa whose body sizes are unusually large. This phenomenon has become known as 'polar gigantism'. In the intervening years, biologists have proposed a multitude of hypotheses to explain polar gigantism. These hypotheses run the gamut from invoking release from physical and physiological constraints, to systematic changes in developmental trajectories, to community-level outcomes of broader ecological and evolutionary processes. Here we review polar gigantism and emphasize two main problems. The first is to determine the true strength and generality of this pattern: how prevalent is polar gigantism across taxonomic units? Despite many published descriptions of polar giants, we still have a poor grasp of whether these species are unusual outliers or represent more systematic shifts in distributions of body size. Indeed, current data indicate that some groups show gigantism at the poles whereas others show nanism. The second problem is to identify underlying mechanisms or processes that could drive taxa, or even just allow them, to evolve especially large body size. The contenders are diverse and no clear winner has yet emerged. Distinguishing among the contenders will require better sampling of taxa in both temperate and polar waters and sustained efforts by comparative physiologists and evolutionary ecologists in a strongly comparative framework.

Estradiol's beneficial effect on murine muscle function is independent of muscle activity.

Estradiol (E2) deficiency decreases muscle strength and wheel running in female mice. It is not known if the muscle weakness results directly from the loss of E2 or indirectly from mice becoming relatively inactive with presumably diminished muscle activity. The first aim of this study was to determine if cage activities of ovariectomized mice with and without E2 treatment differ. Ovariectomized mice were 19-46% less active than E2-replaced mice in terms of ambulation, jumping, and time spent being active (P ≤ 0.033). After E2-deficient mice were found to have low cage activities, the second aim was to determine if E2 is beneficial to muscle contractility, independent of physical activities by the mouse or its hindlimb muscles. Adult, female mice were ovariectomized or sham-operated and randomized to receive E2 or placebo and then subjected to conditions that should maintain physical and muscle activity at a constant low level. After 2 wk of hindlimb suspension or unilateral tibial nerve transection, muscle contractile function was assessed. Soleus muscles of hindlimb-suspended ovariectomized mice generated 31% lower normalized (relative to muscle contractile protein content) maximal isometric force than suspended mice with intact ovaries (P ≤ 0.049). Irrespective of whether the soleus muscle was innervated, muscles from ovariectomized mice generated ∼20% lower absolute and normalized maximal isometric forces, as well as power, than E2-replaced mice (P ≤ 0.004). In conclusion, E2 affects muscle force generation, even when muscle activity is equalized.

Limits to diffusive O2 transport: flow, form, and function in nudibranch egg masses from temperate and polar regions.

BACKGROUND: Many aquatic animals enclose embryos in gelatinous masses, and these embryos rely on diffusion to supply oxygen. Mass structure plays an important role in limiting or facilitating O2 supply, but external factors such as temperature and photosynthesis can play important roles as well. Other external factors are less well understood. METHODOLOGY/PRINCIPAL FINDINGS: We first explored the effects of water flow on O2 levels inside nudibranch embryo masses and compared the effects of flow on masses from temperate and polar regions. Water flow (still vs. vigorously bubbled) had a strong effect on central O2 levels in all masses; in still water, masses were considerably more hypoxic than in bubbled water. This effect was stronger in temperate than in polar masses, likely due to the increased metabolic demand and O2 consumption of temperate masses. Second, we made what are to our knowledge the first measurements of O2 in invertebrate masses in the field. Consistent with laboratory experiments, O2 in Antarctic masses was high in masses in situ, suggesting that boundary-layer effects do not substantially limit O2 supply to polar embryos in the field. CONCLUSIONS/SIGNIFICANCE: All else being equal, boundary layers are more likely to depress O2 in masses in temperate or tropical regions; thus, selection on parents to choose high-flow sites for mass deposition is likely greater in warm water. Because of the large number of variables affecting diffusive O2 supply to embryos in their natural environment, field observations are necessary to test hypotheses generated from laboratory experiments and mathematical modeling.

Egg size as a life history character of marine invertebrates: Is it all it's cracked up to be?

Egg size is one of the most important aspects of the life history of free-spawning marine organisms, and it is correlated with larval developmental mode and many other life-history characters. Egg size is simple to measure and data are available for a wide range of taxa, but we have a limited understanding of how large and small eggs differ in composition; size is not always the best measure of the characters under selection. Large eggs are generally considered to reflect increased maternal investment, but egg size alone can be a poor predictor of energetic content within and among taxa. We review techniques that have been used to measure the energetic content and biochemical makeup of invertebrate eggs and point out the strengths and difficulties associated with each. We also suggest a number of comparative and descriptive approaches to biochemical constituent analysis that would strengthen our understanding of how natural selection shapes oogenic strategies. Finally, we highlight recent empirical research on the intrinsic factors that drive intraspecific variation in egg size. We also highlight the relative paucity of these data in the literature and provide some suggestions for future research directions.

Oxygen hypothesis of polar gigantism not supported by performance of Antarctic pycnogonids in hypoxia.

Compared to temperate and tropical relatives, some high-latitude marine species are large-bodied, a phenomenon known as polar gigantism. A leading hypothesis on the physiological basis of gigantism posits that, in polar water, high oxygen availability coupled to low metabolic rates relieves constraints on oxygen transport and allows the evolution of large body size. Here, we test the oxygen hypothesis using Antarctic pycnogonids, which have been evolving in very cold conditions (-1.8-0 degrees C) for several million years and contain spectacular examples of gigantism. Pycnogonids from 12 species, spanning three orders of magnitude in body mass, were collected from McMurdo Sound, Antarctica. Individual sea spiders were forced into activity and their performance was measured at different experimental levels of dissolved oxygen (DO). The oxygen hypothesis predicts that, all else being equal, large pycnogonids should perform disproportionately poorly in hypoxia, an outcome that would appear as a statistically significant interaction between body size and oxygen level. In fact, although we found large effects of DO on performance, and substantial interspecific variability in oxygen sensitivity, there was no evidence for sizexDO interactions. These data do not support the oxygen hypothesis of Antarctic pycnogonid gigantism and suggest that explanations must be sought in other ecological or evolutionary processes.