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Sea Urchin Diadema Africanum Mass Mortality in the Subtropical Eastern Atlantic: Role of Waterborne Bacteria in a Warming Ocean

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Sea Urchin Diadema Africanum Mass Mortality in the Subtropical Eastern Atlantic: Role of Waterborne Bacteria in a Warming Ocean Vol. 506: 1–14, 2014 MARINE ECOLOGY PROGRESS SERIES Published June 23 doi: 10.3354/meps10829 Mar Ecol Prog Ser FREEREE FEATURE ARTICLE ACCESSCCESS Sea urchin Diadema africanum mass mortality in the subtropical eastern Atlantic: role of waterborne bacteria in a warming ocean S. Clemente1,*, J. Lorenzo-Morales2, J. C. Mendoza1, C. López1, C. Sangil3, F. Alves4, M. Kaufmann4,5,6, J. C. Hernández1 1Biodiversidad, Ecología Marina y Conservación, Departamento de Biología Animal (Ciencias Marinas), Facultad de Biología, Universidad de La Laguna, Avda. Astrofísico Francisco Sánchez s/n, 38206 La Laguna, Tenerife, Canary Islands, Spain 2University Institute of Tropical Diseases and Public Health of the Canary Islands, Universidad de La Laguna, Avda. Astrofísico Francisco Sánchez s/n, 38203 La Laguna, Tenerife, Canary Islands, Spain 3Botánica Marina, Departamento de Biología Vegetal, Universidad de La Laguna, 38071 La Laguna, Tenerife, Canary Islands, Spain 4CIIMAR-Madeira (Interdisciplinary Centre of Marine and Environmental Research of Madeira), Edifício Madeira Tecnopolo, Caminho da Penteada, 9020-105 Funchal, Madeira, Portugal 5University of Madeira, Centre of Life Sciences, Marine Biology Station of Funchal, 9000-107 Funchal, Madeira, Portugal 6CIIMAR/CIMAR (Interdisciplinary Centre of Marine and Environmental Research), University of Porto, Rua dos Bragas 289, 4050-123 Porto, Portugal ABSTRACT: A widespread mass mortality event of the sea urchin Diadema africanum was detected in the subtropical eastern Atlantic, extending from Madeira to the Canary Islands, covering a straight- line distance of >400 km. This is the first disease- related die-off of a diadematid documented in the eastern Atlantic Ocean. Diseased individuals showed deterioration of the epidermis and water-vascular system, resulting in epidermal necrosis and release of spines. Despite some spatial heterogeneity in disease incidence at the study sites, there was a 65% overall reduction in urchin abundance after the mortality event compared to numbers pre-mortality. However, the reduction in urchin numbers did not compromise the species’ reproductive success; the settlement peak following the mortality event was of a similar magnitude to that in prior years. Bacterial Diadema africanum displaying symptoms of disease and isolation and culture techniques, and subsequent accumulations of dead individuals recorded during the mor- laboratory in fection experiments, strongly suggested tality event in the Canary Islands. that Vibrio alginolyticus was involved in the disease. Image: Julián Rodríguez Medina We hypo thesize that the mass mortality event devel- oped due to anomalously high seawater tempera- tures recorded in the 2 studied archipelagos and that warmer temperatures enabled infection of D. africa - num by waterborne pathogenic bacteria. Fluctua- tions in urchin populations are key in de termining KEY WORDS: Echinoids · Diadematid · Disease · the structure and functioning of benthic ecosystems: Widespread die-off · Vibrio · Infection experiments · under the current seawater warming scenario, dis- Canary Islands · Madeira ease may result in more frequent phase shifts, aiding Resale or republication not permitted without the persistence of macroalgae. written consent of the publisher *Corresponding author: [email protected] © Inter-Research 2014 · www.int-res.com 2 Mar Ecol Prog Ser 506: 1–14, 2014 INTRODUCTION region then led to a decrease in coral cover (Lessios 1988, Levitan 1988, Edmunds & Carpenter 2001). In recent decades, mass mortality events resulting Similarly, in recent decades the sea urchin Strongylo- from disease have been widely described in the centrotus droebachiensis has suffered recurrent marine environment (e.g. Goreau et al. 1998, Hoegh- amoeba-induced mass mortalities off the North Guldberg 1999, Porter et al. 2001) and the preva- Atlantic coast of Nova Scotia. In this location, the lence or severity of these disease outbreaks in marine mortality events were associated with increases in organisms appears to be increasing (Epstein 1996, SST and an increase in the incidence of tropical Harvell et al. 1999, Hayes et al. 2001, Lafferty et al. storms (Scheibling & Hennigar 1997, Scheibling et al. 2004). The increase in disease frequency has been 2010, Feehan et al. 2012). Increased frequencies of linked with a variety of factors that influence the diseased sea urchins have also reported in temperate introduction and propagation of pathogens. Many of regions during blooms of tropical dinoflagellates of the identified causes are climate related, such as the genus Ostreopsis (Shears & Ross 2009, and refer- ocean warming and the incidence of storms (Scheib- ences therein); however, the mechanisms involved ling & Hennigar 1997, Harvell et al. 2002, Scheibling largely remain unknown. et al. 2010, Feehan et al. 2012, Hendler 2013). An - Benthic communities in the eastern Atlantic Archi- thropogenic pressures may also influence the out- pelagos, including Madeira and the Canary Islands, break of disease, with factors including pollution, similar to other temperate and subtropical regions, harvesting, the introduction of foreign species, or the are often characterized by 1 of 2 alternative commu- modification of coastal habitats (Harvell et al. 1999, nity states: productive macroalgal beds or barren Lafferty et al. 2004, Hendler 2013, Ebert 2013). Ele- grounds dominated by sea urchins and encrusting vated sea-surface temperatures (SST) are commonly coralline algae (Hernández et al. 2008a). The sea associated with reports of marine disease and mass urchin Diadema africanum (Rodríguez et al. 2013) is mortalities (Epstein 1996, Harvell et al. 1999). How- widely distributed throughout these archipelagos ever, establishing cause−effect relationships is ex - and facilitates the transition from macroalgal beds to tremely complicated given the number of different urchin-grazed barren grounds due to its intense interacting factors that could be involved (Harvell et grazing activity (Alves et al. 2001, Hernández et al. al. 1999). Different pathogens may also display dif- 2008b). To the best of our knowledge, no mortality ferent re sponses to environmental change (Lafferty events of D. africanum had been recorded prior to et al. 2004), with contrasting outcomes for disease this study in the eastern Atlantic Ocean, and high development. abundances of the species have persisted for decades Episodes of extensive mortality resulting from dis- in the archipelagos (e.g. Madeira, Alves et al. 2001; ease have been observed in a wide array of marine the Canarian Archipelago, Hernández et al. 2008b). taxa (Lafferty et al. 2004, Ward & Lafferty 2004), Only 1 episode of disease causing mass mortality is many of them driving community state shifts (Harvell known for echinoids in this region; it specifically et al. 1999). The effects are most significant when affected intertidal populations of the species Para- mortality affects species playing key roles in the eco- centrotus lividus and was related to high SST cou- system, such as key producers, key herbivores, pled with extremely low tides (Girard et al. 2012). or keystone predators. Modifications to community For the first time we report here on a mortality event structure and the food web take place when the of the sea urchin Diadema africanum in subtropical population of a key species is depleted as a direct eastern Atlantic Ocean waters. In October 2009 popu- consequence of disease progress (Lessios 1988, lations of the sea urchin began to die off around the Scheibling et al. 2013). Many echinoid species can be southeast coastline of Madeira Island; by the end of described as key herbivores, controlling algal March 2010 the mortality event had reached some production and diversity and hence community state. spots of the Canary Islands (Gran Canaria Island, F. One of the most notable examples of a sea urchin Tuya, Universidad de Las Palmas de Gran Canaria, mass mortality episode was that of Diadema antil- pers. comm.), and by April 2010 it had spread to many larum in the Caribbean (western Atlantic) in the areas throughout the archipelagos (Fig. 1). 1980s caused by an unidentified pathogen (Lessios Disease is an important natural mechanism known 1988, 1995). After the abundances of D. antillarum to cause mass mortalities of key herbivore sea ur - were widely decimated in the Caribbean, extensive chins (Feehan et al. 2012). The comprehensive study proliferation of macroalgae occurred. The subsequent of this phenomenon aids our understanding of mech- dominance of macroalgal stands throughout the anisms that mediate transitions between alternate Clemente et al.: Mass mortality of Diadema africanum 3 Madeira 34º Madeira Island N Reis Magos Oct. 09 32º ATLANTIC OCEAN La Palma Canary Islands 30º Los Cancajos Apr. 10 La Bombilla El Pozo Puerto Naos El Fraile Tenerife 28º Fuencaliente Boca Cangrejo Teno Mar. 10 Punta Prieta El Porís N Abades 10 0 10 20 km La Caleta de Adeje 18ºW 16º 14º Fig. 1. Study sites around Madeira and the Canary Islands (La Palma and Tenerife). Spread of the mortality event is shown by grey arrows labelled with the timing of observed mortality (month and year) ecosystem states. We specifically aimed to assess the mental Prediction/National Centre for Atmospheric ecological effects of the reported D. africanum die-off Research (NCEP/NCAR) reanalysis data for each throughout the eastern Atlantic archipelagos, and to region (Kalnay et al. 1996). provide insight into the cau sative agents of this event. To measure
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