Perspective: Something Old, Something New? Review of Wasting and Other Mortality in Asteroidea (Echinodermata)

Introduction

Marine disease events can have profound influences on ecosystem structure, causing shifts in species dominance, biodiversity, and function. Sea stars (Echinodermata: Asteroidea) are ecologically significant constituents of benthic communities worldwide, where some species can exert significant influence on the population structure and composition of sympatric organisms (Paine, 1966; Menge and Sanford, 2013). Asteroid diseases have been reported for over a century (Mead, 1898; Christensen, 1970; Menge, 1979; Dungan et al., 1982; Jangoux, 1987; Eckert et al., 1999; Bates et al., 2009).

The term “sea star wasting disease (SSWD)”, first used to describe a common suite of clinical signs that affected Asteroidea in Southern California asteroids in the early 1980s (Dungan et al., 1982) and late 1990s (Eckert et al., 1999), has more recently been used to describe the mass mortality of asteroids on the Pacific coast of North America beginning in 2013 (Hewson et al., 2014) and in the North Atlantic Ocean beginning in 2012 (Bucci et al., 2017). The sea star wasting outbreak [also referred to as “Asteroid Idiopathic Wasting Syndrome” (Hewson et al., 2018)] widely reported from 2013 to present is amongst the most geographically extensive marine mass mortality events ever observed (Hewson et al., 2014), leading to catastrophic declines in some species of sea stars in affected areas (Montecino-Latorre et al., 2016; Schultz et al., 2016) and increased abundance of prey urchins (Schultz et al., 2016). Whereas mass-mortalities of asteroids in the northeast Pacific Ocean prior to 2013 represented mostly endemic events with local impacts on ecosystem structure, wasting since 2013 is currently described as an epidemic and is hypothesized to result in continental-scale changes in coastal habitats (Harvell et al., 2019).

Generally, asteroid wasting is described as a progression of clinical signs whereby lesions appear on their surface tissues, followed by tissue decay around lesions, limb autotomy and death. Wasting can be rapid, leading to animal mortality in a few days (Miner et al., 2018). In the Northeast Pacific, apparently asymptomatic individuals that were collected and transported to the laboratory and housed in flow-through sea tables (i.e., ambient seawater conditions) showed very rapid (within hours) disintegration (Eisenlord et al., 2016; Kohl et al., 2016). Signs of wasting are similar to those produced by environmental stressors (e.g., desiccation) or physical injury, hence wasting occurrence is only recorded when large numbers of individuals in a population display extensive wasting signs (Miner et al., 2018) during systematic surveys of wasting (Eisenlord et al., 2016; Menge et al., 2016; Schultz et al., 2016). As with many invertebrate diseases, sea star wasting is not pathognomic (i.e., no defining disease signs) since echinoderms possess a limited repertoire of abnormal gross characteristics.

The purpose of this perspective is to summarize reported asteroid disorders recorded before 2013, and report two geographically disparate wasting events in 2015. It will also review physical injury and mortality due to predation and abnormalities induced by abiotic causes. Here we show that grossly apparent disease signs reported in the current Northeast Pacific sea star wasting outbreak share similarity with those caused by non-pathogenic factors, and are also similar to reported asteroid mass mortalities since at least 1898.

Abiotic Causes of Mass Mortality

Physical injury to asteroids may cause clinical signs similar to wasting and other health conditions (Figure 1). A treatise on abiotic health conditions in echinoderms, including asteroids, was prepared by Lawrence (1996). Abiotic factors that cause health abnormalities in asteroids include burial (obrution; Schaefer and Craig, 1972), dislodgement by storms and currents (Sieling, 1960; Tiffany, 1978; McClintock, 2013) leading to mass strandings [Sheehan and Cousens, 2017; see Supplementary Table 1 for stranding events in the popular press recorded in the last decade (2008–2018)], temperature excursions (Crisp, 1964; Moyse and Nelson-Smith, 1964; Staehli et al., 2008), desiccation during emersion (Hodgkin, 1959), salinity variation (Smith, 1940), hypoxia (Osborne, 1979), and exposure to anthropogenic toxins (Smith, 1968). Abiotic conditions generally present as density-independent occurrences, and normally also include sympatrics. Individuals experiencing the effects of abiotic abnormalities typically show either no gross morphological change prior to death, show lesions consistent with abrasion (in the case of current scouring), or may show signs of advanced decay (which is unrelated to the cause of death) when found (McClintock, 2013). For example, Waldichuk (1990) reported a highly localized mass mortality of deep water asteroids in southern British Columbia, where hundreds of individuals were found “broken into pieces” and attributed the event to fishing by-catch. Similarly, a mass mortality of asteroids, mostly intact, occurred near the Powell River in British Columbia, which was accompanied by mortality of conspecifics and therefore likely due to adverse environmental condition or pollutants (Anon, 1990). Abiotic mass mortalities of asteroids is observed in the fossil record, where thousands of individuals in a single strata (i.e., occurring at the same geological time and within a former shallow sea) occurred in a single region (Gale and Villier, 2013).

Figure 1. Unidentified disorders in asteroids. (A,B) Labidiaster sp. From Antarctica showing wasting signs. The individual was the sole example demonstrating abnormalities amongst hundreds of individuals (Photo credit Shaylyn Potter). (C) Lesions on Stichaster australis from Muriwai, Auckland, New Zealand in June 2015. The individual was the sole example of affected stars amongst hundreds. Subsequent surveys in the area later in 2015 revealed no additional stars (Photo credit Richard Taylor). (D) Degraded madreporite in S. australis from Piha, Auckland, New Zealand (madreporite indicated by yellow arrow) (E,F) Lesions on Patiriella regularis from the North Island of New Zealand, in December 2017 and January 2018, respectively. The individuals were one of a small handful with lesions which may indicate physical injury.

While physical injuries may be caused by predation, they are subject to predation by relatively few animals, presumably due to feeding deterrents in their tissues. Specifically, asteroids possess a suite of saponins, which are not palatable by many predators (Hashimoto and Yasumoto, 1960; Lucas et al., 1979). Despite these defenses, sea stars can be subject to predation by sympatrics, fish, seabirds (notably gulls) (Suraci and Dill, 2011; Rogers and Elliott, 2013) and otters (Estes et al., 2003; Vicknair and Estes, 2012; reviewed in Robles, 2013 and Pearse et al., 2010). Specifically, there are examples of predation on sea stars by birds (Verbeek, 1977) and otters when food is limited (Larsen, 1984). It is worthwhile noting that the physical injuries (bites/pecks) from predation are similar to lesions seen in sea star wasting.

Wasting Syndromes

While the 2013–present asteroid wasting event has attracted considerable recent attention, wasting as a phenomenon affecting asteroids is not new, and similar wasting signs described in previous events (Mead, 1898; Christensen, 1970; Menge, 1979; Pratchett, 1999; Staehli et al., 2008) are highly similar to those observed today.

The earliest known account of asteroid wasting was in Asterias forbesi more than 120 years ago (Mead, 1898). In a report on fisheries by the Harvard Professor A.D. Mead addressing a wide suite of starfish biology, they noted “on certain lots of star-fish, dredged from different localities, what appears to be a disease, attacking the skin first and not infrequently eating its way through the body. This disease attacks both the common star and the purple star. Some of the star-fish in my cars at Kickemuit river were so seriously affected that some of the arms were entirely eaten through and the ends dropped off. Later some of them recovered”. The author suggested that this disease could be of service in mitigating starfish impacts on the shellfish fishery, since “There seems to be no doubt but that, with the development of the oyster beds, the star-fish has become more numerous along our New England coast”.

Christensen (1970) reported that Astropecten irregularis was subject to wasting by a fungal infection of the epidermis, however, no specific pathogen was identified. During feeding experiments, Christensen (1970) also reported that one individual had an “unknown skin disease” which caused mortality several months after it first showed signs of wasting – the animal “bursted with parts of at least 2 gonads piercing through the body wall”. It is unclear if wasting resulted in the eventual death of the animal.

Menge (1979) reported a wasting event in Asterias spp. in the Gulf of Maine, which bears similarities to the 2013–2016 Northeast Pacific wasting event. He reported that animals experienced necrotic areas on their epidermis, which progressed to erosions through their body walls. Wasting first appeared in late autumn 1972 and was followed by disappearance of most large Asterias, causing a shift in the size range of individuals to smaller animals (and juveniles) in subsequent surveys.

Dungan et al. (1982) reported extensive wasting in the predatory sun star Heliaster kubiniji, in the Gulf of California during 1977 and 1978. Reported wasting signs included the appearance of white lesions on the aboral surface of affected individuals, which rapidly enlarged to encompass the whole animal and resulted in limb autotomy. The wasting onset corresponded with a period of higher-than-15 year average water temperatures and led to the functional extirpation of the species in the region (Dungan et al., 1982). Populations of H. kubiniji have not recovered as of 2008 (Sagarin et al., 2008).

A wasting-like disease was reported by Prestedge (1998) in the asterinid Patiriella vivipara in Tasmania. The condition – known as “brown spot” disease elicited small brown areas on the aboral and sometimes oral epidermis. The disease appeared to have a high prevalence in both natural and aquarium-housed individuals, and was present year-round over 8 years. The author indicated that brown spot may persist for months, clear up in some individuals, and in severe cases cause skin necrosis which over several weeks resulted in animal mortality (Prestedge, 1998).

Staehli et al. (2008) reported the presence of wasting in the sand star Astropecten johnstoni in Sardinian waters. Wasting manifested with the appearance of white lesions and loss of turgor, followed by swelling on one side, eversion of stomach through the mouth and erosions in body wall tissues, the spread of lesions over the entire body wall and finally animal death and disintegration within 48 h of appearance of first lesions. The authors found that enhanced temperature (+8–13^∘C above ambient) significantly accelerated the progress of wasting signs, and also observed the presence of several genera of bacteria, for which there are known pathogenic representatives (e.g., Vibrio spp.), in skin swabs of affected tissues.

Wasting was also reported by Pratchett (1999), where a single Acanthaster planci “was found with numerous lesions of the dermal tissue, collapsed spines, and a completely debilitated water-vascular system”. An experiment where affected tissues were placed into aquaria with healthy individuals resulted in identical wasting signs (epidermal lesions and collapsed spines) in 3 of 6 challenged individuals, resulting in mortality 6–9 days after challenge. Further investigation of wasting in A. planci revealed that wasting with the same signs could be induced by injection with thiosulfate-citrate-bile-sucrose (TCBS) (Rivera-Posada et al., 2011a; Rivera-Posada et al., 2012). TCBS media is used to selectively culture Vibrio spp. and other Proteobacteria (Lotz et al., 1983). Wasting was associated with dysbiosis and presence of bacterial genera with pathogenic representatives, notably Vibrio spp. (Rivera-Posada et al., 2011b,c). Interestingly, similar wasting, attributed to an unidentified sporozoan parasite, were observed in 1984 and 1986 in Suva, Fiji, which led to the extirpation of cohorts (Zann et al., 1990).

Bates et al. (2009) observed wasting in Pisaster ochraceus in Barkley Sound, Vancouver, British Columbia in 2008. Affected stars demonstrated the appearance of small white lesions (especially in inter-radial tissue), edema of epidermal tissues (a “mushroom”-like swelling) which spread to the whole individual, followed by spread of lesions across the body and ultimately animal death. There was a higher prevalence of wasting in field populations in presumably cooler waters of June than in August. Interestingly, wasting was also more prevalent in protected waters, which typically experience stronger diel temperature shifts than exposed shores.

An epidermal disease was reported in the circum-Antarctic asteroid Odontaster validus near the volcanic Deception Island (South Shetland Islands, near Antarctica) from 2012 to 2013 and again in 2016 (Núñez-Pons et al., 2018). The disease presented as focal epidermal dispigmentation, anorexia, and limb autotomy, affecting ∼10% of the population. The disease concurred with unprecedented geothermal anomalies (increased water temperature and seismic events). The authors found no evidence of disease transmission from affected to healthy individuals. Histopathological investigation revealed ulceration (edema), epidermal necrosis, and infiltration by hemocytes, accompanied by cleft formation between outer epidermis and ossicle-rich body wall tissues. Analyses of microbial communities on lesion fronts revealed decreased bacterial richness relative to unaffected tissues, and communities were different between lesions and healthy tissues. Fungal communities, however, were not different between lesions and clinically normal tissues. No etiological agent could be identified from analysis of the disease (Núñez-Pons et al., 2018).

Asteroid wasting in the northeast Pacific (Bates et al., 2009; Hewson et al., 2014) and northwest Atlantic (Bucci et al., 2017) from 2013 onward manifested with similar wasting signs to those reported previously (Christensen, 1970; Menge, 1979; Dungan et al., 1982; Pratchett, 1999; Staehli et al., 2008). Affected individuals demonstrated various wasting signs, including loss of turgor, appearance of body wall lesions on their aboral surfaces, which enlarged to permit internal organs (i.e., gonads and pyloric caeca) to protrude, tissue loss and limb autotomy. A more subjective wasting sign, limb twisting and folding, was also reported (Hewson et al., 2014). The etiology of the northeast Pacific and northwest Atlantic wasting events remains poorly resolved (Miner et al., 2018). While the Sea Star Associated Densovirus (SSaDV) was the best candidate microorganism associated with wasting in one species of asteroid (Hewson et al., 2014), no candidate pathogenic microorganism has been identified for the remaining 19 species of sea star affected in the region (Hewson et al., 2018). Furthermore, while increased temperature (Eisenlord et al., 2016; Kohl et al., 2016), decreased temperature (Menge et al., 2016), and shifts in temperature and precipitation (Hewson et al., 2018) corresponded with SSWD at some locations, there remains no parsimonious explanation for wasting occurrence across the event’s geographically wide distribution.

Here we report the occurrence of two significant asteroid wasting events that occurred elsewhere in 2015 that have hitherto been undocumented. Beginning in April 2015 and continuing until at least September 2015, asteroid wasting was observed in the Yellow Sea, China. Wasting was first observed in the field in Dongjiakou Bay in April, followed by Haizhou Bay in May, and further North in Qingdao in subsequent months, affecting three species of asteriid sea stars, Asterias amurensis, Aphelasterias japonica, and Distolasterias nipon (Figures 2A–F). In Haizhou Bay, most surviving sea stars were small individuals with armlength shorter than 3 cm. A collection of >130 apparently healthy adult A. amurensis with well-developed gonads was performed from Rongcheng, Weihai, in June 2015 for use in experiments aimed to determine the etiology of field-observed wasting. After collection and maintenance in aquaria, 80% of collected individuals died within 7 days. Individuals demonstrated wasting-like signs consistent with wasting in the northeast Pacific, including limb twisting and autotomy, appearance of lesions and protrusion of internal organs, and finally death.

Figure 2. Wasting signs in four species of asteroid. (A) Asterias amurensis with sympatric Patria pectinifera from the Yellow Sea, April–June 2015; (B) Autotomized limb of A. amurensis; (C) A. amurensis recovered in the lab; (D) Distolasterias nipon; (E,F) Aphelasterias japonica showing arm lesions (denoted by black arrows); (G,H) Coscinasterias muricata inhabiting Port Phillip Bay, Australia, September–October 2015.

A sea star wasting event was observed in Port Phillip Bay, Victoria, Australia from September–December 2015 (Figures 2G,H) concomitant with the wasting epidemic on the North American West Coast from 2013 to 2016. The Port Phillip Bay event occurred at the same time as the longest and most intense marine heat wave ever recorded in the region (Oliver et al., 2017). The first observations were made in individuals transferred from wild populations to the Victorian Marine Science Consortium (VMSC) in Queenscliff, Victoria in September 2015. Signs of wasting presented in two species transferred to the lab, including the invasive A. amurensis, and the native Coscinasterias muricata. Symptoms were much more pronounced in the C. muricata, which dominated the study site and were most frequently observed. The signs presented were typical of wasting elsewhere, including loss of turgor, swelling, lesion formation, tissue decay and limb autotomy, resulting eventually in animal mortality. In total 18 A. amurensis and 12 C. muricata died within 3 days of arriving at the research center. Upon first observation of wasting at the VMSC aquaria, field observations of asteroid health were performed by a snorkeler over the same 5 transects on two dates (4 October 2015 and 27 October 2015). A population decline of >75% (of n = 146 individuals on 4 October 2015) was estimated from the surveys, and asteroid rays and other detached parts were observed on adjacent beaches and washing up with the tides. These semi-quantitative and anecdotal observations suggest that the asteroid population in Queenscliff experienced a widespread die-off. Photographs and videos were taken both of captive and wild asteroids to document their health state using the wasting scale (0–4)¹. A total of 155 individuals were assessed for wasting category. This analysis indicated that there was no significant change (t-test, df = 128) in mean wasting category between 4 October 2015 and 27 October 2015, with most individuals having limb autotomy and body wall lesions (mean category = 3.0 ± 0.3 on 4 October and = 2.2 ± 0.1 on 27 October). Since there had been no accounts of large asteroid losses previously in Port Phillip Bay, there was little support or resources available to researchers for further investigation. In addition, the study site was destroyed (buried) during pier improvements in 2016 and the populations have not been observed since.

Priorities for Future Research

As of June 2019, the cause of most echinoderm health conditions remain unknown; however, there are several lines of evidence to suggest association with either putative pathogens or environmental stressors. The mass mortality of Diadema antillarum in the early 1980s was almost certainly transmissible, but few specimens of affected individuals were collected, and those that were collected were in an advanced state of degradation for histopathology (Peters, 1992). Hence, scientists may never learn the cause of that wasting event. Early wasting asteroids from southern California (H. kubiniji) and from the Mediterranean (Christensen, 1970) were likewise not preserved. Future efforts to elucidate the causes of asteroid wasting should ensure adequate long-term preservation and archiving of samples for future analyses that may not be possible with contemporary technologies. In veterinary medicine, case studies of infectious diseases are typically made to provide an up-to-date summary for field-practitioners and clinicians to help guide them toward best practices for diagnosis. No case study currently exists for wasting, which could be of great value to guide researchers and veterinarians toward a standardized approach for field-sampling, reporting and documentation. Wasting is currently an umbrella term to describe any and all signs of an affected sea star, which may not be appropriate since these signs are not pathognomic. The signs of wasting that have been categorized into progressive stages require greater detail and attention for each species. For instance, there might exist subtleties among lesions or signs that have important biological significance that would help distinguish between two or more diseases.

Conclusion

Asteroid wasting events exhibit similarity in clinical signs, which are most notably characterized by appearance of lesions which may enlarge over time to allow internal organs to protrude. These events can have significant impacts on the population density of their hosts (Menge, 1979; Dungan et al., 1982; Zann et al., 1990; Menge et al., 2016), and shift population structure from large individuals (presumably adults) to juveniles (Menge, 1979; Menge et al., 2016). However, distinguishing between wasting diseases is difficult since they demonstrate consistent suites of clinical signs but may represent different etiologies (Hewson et al., 2018). The apparent “emergence” of wasting disease in the Northeastern Pacific in 2013 is perhaps not a new phenomenon but a more geographically widespread, and within-population intensive, phenomenon that has been observed for over a century.

Data Availability

All datasets generated for this study are included in the manuscript and/or the Supplementary Files.

Author Contributions

All authors wrote the manuscript. QX, HL, CL, and BS performed field observations and laboratory analysis of wasting events in the China and Australia.

Funding

This work was supported by NSF grants OCE-1537111 and OCE-1737127 awarded to IH.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Acknowledgments

The authors thank J. Pearse for comments on an early draft of this manuscript. The authors gratefully acknowledge the assistance of Lucy Chapman, Jacob Sangren, Kalia Bistolas and Jason Button for their assistance with laboratory and field work. The authors also thank Shaylyn Potter and Richard Taylor for permission to use photographs of wasting and injured asteroids.

Supplementary Material

The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fmars.2019.00406/full#supplementary-material

Footnotes

1. ^ www.seastarwasting.org

References