Echinodermata) University of the Aegean, Greece Ian Hewson1*, Brooke Sullivan2†, Elliot W
Total Page：16
File Type：pdf, Size：1020Kb
fmars-06-00406 July 10, 2019 Time: 17:15 # 1 PERSPECTIVE published: 11 July 2019 doi: 10.3389/fmars.2019.00406 Perspective: Something Old, Something New? Review of Wasting and Other Mortality in Asteroidea Edited by: Stelios Katsanevakis, (Echinodermata) University of the Aegean, Greece Ian Hewson1*, Brooke Sullivan2†, Elliot W. Jackson1, Qiang Xu3†, Hao Long3†, Reviewed by: Chenggang Lin3, Eva Marie Quijano Cardé1†, Justin Seymour4, Nachshon Siboni4, Sarah Annalise 5 6 Gignoux-Wolfsohn, Matthew R. L. Jones and Mary A. Sewell Rutgers University, The State 1 Department of Microbiology, Cornell University, Ithaca, NY, United States, 2 Department of BioSciences, University University of New Jersey, of Melbourne, Melbourne, VIC, Australia, 3 Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China, 4 Climate United States Change Cluster, University of Technology Sydney, Ultimo, NSW, Australia, 5 School of Applied Sciences, Auckland University Colette J. Feehan, of Technology, Auckland, New Zealand, 6 School of Biological Sciences, University of Auckland, Auckland, New Zealand Montclair State University, United States *Correspondence: Asteroids (Echinodermata) experience mass mortality events that have the potential Ian Hewson to cause dramatic shifts in ecosystem structure. Asteroid wasting describes a suite [email protected] of body wall abnormalities that can ultimately result in animal mortality. Wasting in †Present address: Brooke Sullivan, Northeast Pacific asteroids has gained considerable recent scientific attention due to its Department of Landscape geographic extent, number of species affected, and effects on overall population density Architecture, University in some affected regions. However, asteroid wasting has been observed for over a of Washington, Seattle, WA, United States century in other regions and species. Asteroids are subject to physical injury and adverse Qiang Xu and Hao Long, environmental conditions, which may result in very similar external manifestations to State Key Laboratory of Marine Resource Utilization in South China wasting, making identification of causative processes sometimes problematic. Here Sea, Hainan University, Haikou, China we review asteroid health abnormalities reported in years prior to the 2013–present Eva Marie Quijano Cardé, Northeast Pacific wasting mass mortality, and report two additional geographically Capital Veterinary Specialists, Tallahassee, FL, United States disparate wasting events that occurred concomitantly with the recent wasting outbreak. Keywords: sea star wasting, disease, syndrome, asteroid, echinoderm Specialty section: This article was submitted to Marine Ecosystem Ecology, a section of the journal INTRODUCTION Frontiers in Marine Science Received: 11 April 2019 Marine disease events can have profound influences on ecosystem structure, causing shifts Accepted: 01 July 2019 in species dominance, biodiversity, and function. Sea stars (Echinodermata: Asteroidea) are Published: 11 July 2019 ecologically significant constituents of benthic communities worldwide, where some species can Citation: exert significant influence on the population structure and composition of sympatric organisms Hewson I, Sullivan B, (Paine, 1966; Menge and Sanford, 2013). Asteroid diseases have been reported for over a century Jackson EW, Xu Q, Long H, Lin C, (Mead, 1898; Christensen, 1970; Menge, 1979; Dungan et al., 1982; Jangoux, 1987; Eckert et al., Quijano Cardé EM, Seymour J, 1999; Bates et al., 2009). Siboni N, Jones MRL and Sewell MA The term “sea star wasting disease (SSWD)”, first used to describe a common suite of clinical (2019) Perspective: Something Old, signs that affected Asteroidea in Southern California asteroids in the early 1980s (Dungan et al., Something New? Review of Wasting and Other Mortality in Asteroidea 1982) and late 1990s (Eckert et al., 1999), has more recently been used to describe the mass mortality (Echinodermata). of asteroids on the Pacific coast of North America beginning in 2013 (Hewson et al., 2014) and in Front. Mar. Sci. 6:406. the North Atlantic Ocean beginning in 2012 (Bucci et al., 2017). The sea star wasting outbreak doi: 10.3389/fmars.2019.00406 [also referred to as “Asteroid Idiopathic Wasting Syndrome” (Hewson et al., 2018)] widely reported Frontiers in Marine Science| www.frontiersin.org 1 July 2019| Volume 6| Article 406 fmars-06-00406 July 10, 2019 Time: 17:15 # 2 Hewson et al. Asteroid Wasting Perspectives from 2013 to present is amongst the most geographically change prior to death, show lesions consistent with abrasion (in extensive marine mass mortality events ever observed (Hewson the case of current scouring), or may show signs of advanced et al., 2014), leading to catastrophic declines in some species decay (which is unrelated to the cause of death) when found of sea stars in affected areas (Montecino-Latorre et al., 2016; (McClintock, 2013). For example, Waldichuk(1990) reported Schultz et al., 2016) and increased abundance of prey urchins a highly localized mass mortality of deep water asteroids in (Schultz et al., 2016). Whereas mass-mortalities of asteroids in southern British Columbia, where hundreds of individuals were the northeast Pacific Ocean prior to 2013 represented mostly found “broken into pieces” and attributed the event to fishing endemic events with local impacts on ecosystem structure, by-catch. Similarly, a mass mortality of asteroids, mostly intact, wasting since 2013 is currently described as an epidemic and occurred near the Powell River in British Columbia, which was is hypothesized to result in continental-scale changes in coastal accompanied by mortality of conspecifics and therefore likely due habitats (Harvell et al., 2019). to adverse environmental condition or pollutants (Anon, 1990). Generally, asteroid wasting is described as a progression of Abiotic mass mortalities of asteroids is observed in the fossil clinical signs whereby lesions appear on their surface tissues, record, where thousands of individuals in a single strata (i.e., followed by tissue decay around lesions, limb autotomy and occurring at the same geological time and within a former shallow death. Wasting can be rapid, leading to animal mortality in a sea) occurred in a single region (Gale and Villier, 2013). few days (Miner et al., 2018). In the Northeast Pacific, apparently While physical injuries may be caused by predation, they asymptomatic individuals that were collected and transported are subject to predation by relatively few animals, presumably to the laboratory and housed in flow-through sea tables (i.e., due to feeding deterrents in their tissues. Specifically, asteroids ambient seawater conditions) showed very rapid (within hours) possess a suite of saponins, which are not palatable by many disintegration (Eisenlord et al., 2016; Kohl et al., 2016). Signs predators (Hashimoto and Yasumoto, 1960; Lucas et al., 1979). of wasting are similar to those produced by environmental Despite these defenses, sea stars can be subject to predation by stressors (e.g., desiccation) or physical injury, hence wasting sympatrics, fish, seabirds (notably gulls) (Suraci and Dill, 2011; occurrence is only recorded when large numbers of individuals Rogers and Elliott, 2013) and otters (Estes et al., 2003; Vicknair in a population display extensive wasting signs (Miner et al., and Estes, 2012; reviewed in Robles, 2013 and Pearse et al., 2010). 2018) during systematic surveys of wasting (Eisenlord et al., 2016; Specifically, there are examples of predation on sea stars by birds Menge et al., 2016; Schultz et al., 2016). As with many invertebrate (Verbeek, 1977) and otters when food is limited (Larsen, 1984). It diseases, sea star wasting is not pathognomic (i.e., no defining is worthwhile noting that the physical injuries (bites/pecks) from disease signs) since echinoderms possess a limited repertoire of predation are similar to lesions seen in sea star wasting. abnormal gross characteristics. The purpose of this perspective is to summarize reported Wasting Syndromes asteroid disorders recorded before 2013, and report two While the 2013–present asteroid wasting event has attracted geographically disparate wasting events in 2015. It will also review considerable recent attention, wasting as a phenomenon affecting physical injury and mortality due to predation and abnormalities asteroids is not new, and similar wasting signs described in induced by abiotic causes. Here we show that grossly apparent previous events (Mead, 1898; Christensen, 1970; Menge, 1979; disease signs reported in the current Northeast Pacific sea star Pratchett, 1999; Staehli et al., 2008) are highly similar to wasting outbreak share similarity with those caused by non- those observed today. pathogenic factors, and are also similar to reported asteroid mass The earliest known account of asteroid wasting was in Asterias mortalities since at least 1898. forbesi more than 120 years ago (Mead, 1898). In a report on fisheries by the Harvard Professor A.D. Mead addressing a wide Abiotic Causes of Mass Mortality suite of starfish biology, they noted “on certain lots of star-fish, Physical injury to asteroids may cause clinical signs similar to dredged from different localities, what appears to be a disease, wasting and other health conditions (Figure 1). A treatise on attacking the skin first and not infrequently eating its way through abiotic health conditions in echinoderms, including asteroids, the body. This disease attacks both the common star and the purple was prepared by Lawrence(1996).