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

AbstractSea 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.

High-Altitude Pulmonary Edema in Ohio at an Elevation of 339 Meters.

BACKGROUND: HAPE (High-Altitude Pulmonary Edema) is a life-threatening form of high-altitude illness caused by noncardiogenic pulmonary edema. It has been most commonly reported in individuals who live at lower elevations and travel to elevations above 2500 m, typically in those who do so without any acclimatization. It can also occur in residents of high altitudes who descend to lower altitudes and then return to their native altitude without acclimatization. HAPE is more common in individuals with a history of prior HAPE, very rapid rates of ascent, upper respiratory illness, extreme exertion and cold environmental temperatures, Down's Syndrome, obesity and congenital pulmonary anomalies. CASE PRESENTATION: Our case discusses a patient presenting to an emergency department in Ohio with severe respiratory distress, hypoxia and a radiograph that showed pulmonary edema without cardiomegaly. Additional history revealed the patient had recently returned from Breckenridge, Colorado (an elevation of approximately 2926 m). The diagnosis of HAPE was recognized and he was appropriately treated. He was educated and will not be returning to high altitude without acclimatization in the future. CONCLUSION: Upon literature review, there has never been a prior documented case of a patient in Ohio with HAPE. Providers must consider altitude illness when evaluating travelers from high altitude destinations, even when traveling to a very low altitude like Ohio, as symptoms may be unresolved by descent alone. This case emphasizes the importance of obtaining relevant historical data including a travel history. It also emphasizes the importance of avoiding early closure of the diagnostic process by only considering common conditions. Finally, the case emphasizes the potential danger of anchoring bias to previously encountered conditions.

Large-scale impacts of sea star wasting disease (SSWD) on intertidal sea stars and implications for recovery.

Disease outbreaks can have substantial impacts on wild populations, but the often patchy or anecdotal evidence of these impacts impedes our ability to understand outbreak dynamics. Recently however, a severe disease outbreak occurred in a group of very well-studied organisms-sea stars along the west coast of North America. We analyzed nearly two decades of data from a coordinated monitoring effort at 88 sites ranging from southern British Columbia to San Diego, California along with 2 sites near Sitka, Alaska to better understand the effects of sea star wasting disease (SSWD) on the keystone intertidal predator, Pisaster ochraceus. Quantitative surveys revealed unprecedented declines of P. ochraceus in 2014 and 2015 across nearly the entire geographic range of the species. The intensity of the impact of SSWD was not uniform across the affected area, with proportionally greater population declines in the southern regions relative to the north. The degree of population decline was unrelated to pre-outbreak P. ochraceus density, although these factors have been linked in other well-documented disease events. While elevated seawater temperatures were not broadly linked to the initial emergence of SSWD, anomalously high seawater temperatures in 2014 and 2015 might have exacerbated the disease's impact. Both before and after the onset of the SSWD outbreak, we documented higher recruitment of P. ochraceus in the north than in the south, and while some juveniles are surviving (as evidenced by transition of recruitment pulses to larger size classes), post-SSWD survivorship is lower than during pre-SSWD periods. In hindsight, our data suggest that the SSWD event defied prediction based on two factors found to be important in other marine disease events, sea water temperature and population density, and illustrate the importance of surveillance of natural populations as one element of an integrated approach to marine disease ecology. Low levels of SSWD-symptomatic sea stars are still present throughout the impacted range, thus the outlook for population recovery is uncertain.

Decreased Temperature Facilitates Short-Term Sea Star Wasting Disease Survival in the Keystone Intertidal Sea Star Pisaster ochraceus.

An extensive 2013 mass mortality event along the West Coast of North America due to Sea Star Wasting Disease (SSWD) has affected at least 20 species of sea stars. Among environmental factors potentially contributing to the timing of the current outbreak, increased coastal water temperatures are hypothesized to have contributed to previous and current outbreaks of SSWD. With a laboratory experiment, we tested whether cooler temperatures, similar to average winter temperatures, compared to average summer temperatures could slow the progression of morbidity or prevent SSWD mortality entirely in Pisaster ochraceus. Sea stars housed in cooler water progressed through SSWD states more slowly than sea stars housed at summer temperatures. However, the cooler temperature did not prevent SSWD mortality, and all stars died of the disease. Our data are consistent with experimental studies and field observations during previous and current outbreaks, and support the hypothesis that changes in coastal water temperatures have influenced one of the largest disease related mass mortality events in our oceans.

Densovirus associated with sea-star wasting disease and mass mortality.

Populations of at least 20 asteroid species on the Northeast Pacific Coast have recently experienced an extensive outbreak of sea-star (asteroid) wasting disease (SSWD). The disease leads to behavioral changes, lesions, loss of turgor, limb autotomy, and death characterized by rapid degradation ("melting"). Here, we present evidence from experimental challenge studies and field observations that link the mass mortalities to a densovirus (Parvoviridae). Virus-sized material (i.e., <0.2 µm) from symptomatic tissues that was inoculated into asymptomatic asteroids consistently resulted in SSWD signs whereas animals receiving heat-killed (i.e., control) virus-sized inoculum remained asymptomatic. Viral metagenomic investigations revealed the sea star-associated densovirus (SSaDV) as the most likely candidate virus associated with tissues from symptomatic asteroids. Quantification of SSaDV during transmission trials indicated that progression of SSWD paralleled increased SSaDV load. In field surveys, SSaDV loads were more abundant in symptomatic than in asymptomatic asteroids. SSaDV could be detected in plankton, sediments and in nonasteroid echinoderms, providing a possible mechanism for viral spread. SSaDV was detected in museum specimens of asteroids from 1942, suggesting that it has been present on the North American Pacific Coast for at least 72 y. SSaDV is therefore the most promising candidate disease agent responsible for asteroid mass mortality.

Preference alters consumptive effects of predators: top-down effects of a native crab on a system of native and introduced prey.

Top-down effects of predators in systems depend on the rate at which predators consume prey, and on predator preferences among available prey. In invaded communities, these parameters might be difficult to predict because ecological relationships are typically evolutionarily novel. We examined feeding rates and preferences of a crab native to the Pacific Northwest, Cancer productus, among four prey items: two invasive species of oyster drill (the marine whelks Urosalpinx cinerea and Ocenebra inornata) and two species of oyster (Crassostrea gigas and Ostrea lurida) that are also consumed by U. cinerea and O. inornata. This system is also characterized by intraguild predation because crabs are predators of drills and compete with them for prey (oysters). When only the oysters were offered, crabs did not express a preference and consumed approximately 9 juvenile oysters crab(-1) day(-1). We then tested whether crabs preferred adult drills of either U. cinerea or O. inornata, or juvenile oysters (C. gigas). While crabs consumed drills and oysters at approximately the same rate when only one type of prey was offered, they expressed a strong preference for juvenile oysters over drills when they were allowed to choose among the three prey items. This preference for oysters might negate the positive indirect effects that crabs have on oysters by crabs consuming drills (trophic cascade) because crabs have a large negative direct effect on oysters when crabs, oysters, and drills co-occur.

Behavioral plasticity in an invaded system: non-native whelks recognize risk from native crabs.

Inducible defenses have the potential to affect both invasion success and the structure of invaded communities. However, little is known about the cues used for risk-recognition that influence the expression of inducible defenses in invasive prey, because they involve a novel threat. In laboratory experiments, we investigated behavioral defenses induced by a native crab on two invasive oyster drills (marine whelks Urosalpinx cinerea and Ocinebrina inornata). Both drills hid more often and reduced their feeding rates when they detected predators consuming conspecific prey. Examination of the responses of U. cinerea to specific cue sources (predator kairomones, conspecific alarm cues) indicated that this species had the strongest responses to cues from injured conspecifics, but that it did recognize the novel crab predator. Our observation of native predator (per se) recognition by an invasive marine prey is novel. In addition, we observed that neither species of drill reduced their defensive behavior to reflect predation risk shared by a group of prey. The lack of density dependence in risk-assessment could cause populations of invasive prey to transmit both quantitatively and qualitatively different community effects over the course of an invasion as abundance changes. Together, these findings demonstrate several ways that the risk-assessment strategies could be important in establishment and post-establishment dynamics of invasive prey.

Should I stay or should I go: predator- and conspecific-induced hatching in a marine snail.

Predator-induced hatching plasticity has been demonstrated in many species of amphibians. However, animals from other clades (e.g., marine species of molluscs and annelids) also place their embryos in capsules or gelatinous masses and might also exhibit hatching plasticity to predators. To date there is no evidence of predator-induced hatching plasticity from any marine species or a major clade of bilateria animals, the Lophotrochozoa. We studied predator-induced hatching plasticity of Nucella lamellosa, a carnivorous marine snail that deposits embryos in capsules. We used two experiments to investigate the effects of two types of predator, crabs and isopods, on developing embryos. In the first experiment, we quantified proportion of hatched embryos from capsules through time exposed to water-borne chemicals of crabs and isopods. Crabs delayed time-to-hatching, and the effects of predators were additive. In the second experiment, we quantified proportion of hatched embryos from capsules through time, developmental stage, and size of embryos in capsules exposed to water-borne chemicals of crabs and conspecifics. With this experiment, we wanted to answer: (1) whether a delay in hatching corresponded to embryos developing slower, and (2) whether the general products of metabolic waste from organisms can delay hatching. We unexpectedly observed that adult conspecific snails accelerated hatching but not developmental rate-the few past studies on the effects of conspecifics have all demonstrated that conspecifics delay time-to-hatching and rate of development. The results were also inconsistent with metabolic waste in general causing a delay in hatching, although the effect of conspecifics does weaken this inference. This study demonstrates that predators delay time-to-hatching in a marine mollusc, and suggests that predator-induced hatching plasticity is widespread among animals and likely evolved multiple times within the bilateria. In addition, conspecifics accelerated time-to-hatching in a marine mollusc, which suggests that conspecifics, like predators, might commonly influence when embryos hatch.

The impacts of climate change in coastal marine systems.

Anthropogenically induced global climate change has profound implications for marine ecosystems and the economic and social systems that depend upon them. The relationship between temperature and individual performance is reasonably well understood, and much climate-related research has focused on potential shifts in distribution and abundance driven directly by temperature. However, recent work has revealed that both abiotic changes and biological responses in the ocean will be substantially more complex. For example, changes in ocean chemistry may be more important than changes in temperature for the performance and survival of many organisms. Ocean circulation, which drives larval transport, will also change, with important consequences for population dynamics. Furthermore, climatic impacts on one or a few 'leverage species' may result in sweeping community-level changes. Finally, synergistic effects between climate and other anthropogenic variables, particularly fishing pressure, will likely exacerbate climate-induced changes. Efforts to manage and conserve living marine systems in the face of climate change will require improvements to the existing predictive framework. Key directions for future research include identifying key demographic transitions that influence population dynamics, predicting changes in the community-level impacts of ecologically dominant species, incorporating populations' ability to evolve (adapt), and understanding the scales over which climate will change and living systems will respond.

Size correction: comparing morphological traits among populations and environments.

Morphological relationships change with overall body size and body size often varies among populations. Therefore, quantitative analyses of individual traits from organisms in different populations or environments (e.g., in studies of phenotypic plasticity) often adjust for differences in body size to isolate changes in allometry. Most studies of among population variation in morphology either (1) use analysis of covariance (ANCOVA) with a univariate measure of body size as the covariate, or (2) compare residuals from ordinary least squares regression of each trait against body size or the first principal component of the pooled data (shearing). However, both approaches are problematic. ANCOVA depends on assumptions (small variance in the covariate) that are frequently violated in this context. Residuals analysis assumes that scaling relationships within groups are equal, but this assumption is rarely tested. Furthermore, scaling relationships obtained from pooled data typically mischaracterize within-group scaling relationships. We discuss potential biases imposed by the application of ANCOVA and residuals analysis for quantifying morphological differences, and elaborate and demonstrate a more effective alternative: common principal components analysis combined with Burnaby's back-projection method.

Legacies in life histories.

Complex life-histories are common in nature, have many important biological consequences, and are an important focal area for integrative biology. For organisms with complex life-histories, a legacy is something handed down from an ancestor or previous stage, and can be genetic, nutritional/provisional, experiential, as well as the result of random chance and natural variation in the environment. As we learn more about complex life-histories, it becomes clear that legacies are inexorably linked in the short- and long-term through ecology and evolution. Understanding the consequences and drivers of life-history patterns can therefore only be understood by considering all types of legacies and integrating legacies across the entire life cycle. Larry McEdward was a leader in the field of ecological physiology, and evolutionary ecology of marine invertebrate larvae with complex life-histories. Through his scientific work and publications, devotion to students, colleagues, family, and friends, Larry has left a lasting legacy that will impact the future development of the field of larval ecology and complex life-histories.

Estimation and interpretation of egg provisioning in marine invertebrates.

Per-offspring maternal investment is an integral part of life-history theory. To understand the evolution of per-offspring maternal investment in marine invertebrates, a number of mathematical models have been developed. These models examine how selection affects the proportion of maternally derived egg energy used to produce a newly metamorphosed juvenile (s) and make predictions about the distribution of s in nature. However, there are very few published values of s and therefore it is difficult to evaluate how well these models match nature. We present several equations to empirically estimate values of s for any group of marine invertebrate, and use data from echinoderms to compare the different equations. The calculations that directly estimate s require information on the amount of egg energy, juvenile energy, and energy metabolized during development. Currently, there are few data available for directly estimating s, and thus generating distributions of s derived from direct estimates is not possible. Furthermore, the direct estimations of s are informative for planktotrophy but not for lecithotrophy. We have developed an equation that can be used to directly estimate s for lecithotrophs. The calculations to indirectly estimate s only require egg energy or egg size for the species in question and the value of s and egg energy or size for a reference species. This reference species replaces the need to measure juvenile energy and energy metabolized during larval development. Because egg energy or size is currently available for many species, the indirect estimates will be useful for generating distributions of s, and will allow comparisons with models. Although these indirect methods are good for generating distributions of s, they do not provide reliable estimates of s for any particular species. Estimating values of s to compare models is a critical gap in our current evaluations of marine invertebrate life-history models.

Ecological consequences of phenotypic plasticity.

Phenotypic plasticity is widespread in nature, and often involves ecologically relevant behavioral, physiological, morphological and life-historical traits. As a result, plasticity alters numerous interactions between organisms and their abiotic and biotic environments. Although much work on plasticity has focused on its patterns of expression and evolution, researchers are increasingly interested in understanding how plasticity can affect ecological patterns and processes at various levels. Here, we highlight an expanding body of work that examines how plasticity can affect all levels of ecological organization through effects on demographic parameters, direct and indirect species interactions, such as competition, predation, and coexistence, and ultimately carbon and nutrient cycles.