Vol. 117: 59–75, 2015 DISEASES OF AQUATIC ORGANISMS Published November 17 doi: 10.3354/dao02932 Dis Aquat Org

Epidemiology of lobomycosis-like disease in bottlenose dolphins Tursiops spp. from South America and southern Africa

Marie-Françoise Van Bressem1,*, Paulo C. Simões-Lopes2, Fernando Félix3, Jeremy J. Kiszka4, Fabio G. Daura-Jorge2, Isabel C. Avila5, Eduardo R. Secchi6,7, Leonardo Flach8, Pedro F. Fruet6,7, Kate du Toit9, Paulo H. Ott10,11, Simon Elwen9, Amanda B. Di Giacomo11, Jeanne Wagner12, Aaron Banks13, Koen Van Waerebeek1

1Cetacean Conservation Medicine Group (CMED), Peruvian Centre for Cetacean Research (CEPEC), Museo de Delfines, Pucusana, Peru 2Laboratory of Aquatic Mammals, Department of Ecology and Zoology, Federal University of Santa Catarina, PO Box 5102, Florianópolis, SC 88040-970, Brazil 3Museo de Ballenas, Av. General Enríquez Gallo, entre calles 47 y 50, Salinas, Ecuador 4Department of Biological Sciences, Florida International University, 3000 NE 151st Street, North Miami, FL 33181, USA 5Department of Biometry and Environmental System Analysis, University of Freiburg, 79106 Freiburg, Germany 6Laboratório de Ecologia e Conservação da Megafauna Marinha − EcoMega, Instituto de Oceanografia, Universidade Federal do Rio Grande/FURG, Cx.P. 474 Rio Grande, RS 96203-900, Brazil 7Museu Oceanográfico ‘Prof. Eliézer de C. Rios’/FURG, Rua Heitor Perdigão 10, Rio Grande, RS 96200-970, Brazil 8Instituto Boto Cinza, Itacuruçá, Mangaratiba, RJ 23860-000, Brazil 9Mammal Research Institute, Department of Zoology and Entomology, University of Pretoria, Pretoria 0002, South Africa 10Universidade Estadual do Rio Grande do Sul (Uergs), Laboratório de Ecologia e Conservação de Organismos e Ambientes Aquáticos (ECOAqua), Rua Machado de Assis, 1456, Osório, RS 95520-000, Brazil 11Grupo de Estudos de Mamíferos Aquáticos do Rio Grande do Sul (GEMARS), Rua Machado de Assis, 1456, Osório, RS 95520-000, Brazil 12Laboratoire ECOMAR, Université de la Réunion, 15 avenue René Cassin, BP 7151, 97715 St Denis Cedex, la Réunion, France 13Centre for Dolphin Studies, PO Box 1856, Plettenberg Bay, South Africa

ABSTRACT: We report on the epidemiology of lobomycosis-like disease (LLD), a cutaneous disorder evoking lobomycosis, in 658 common bottlenose dolphins Tursiops truncatus from South America and 94 Indo-Pacific bottlenose dolphins T. aduncus from southern Africa. Photographs and stranding records of 387 inshore residents, 60 inshore non-residents and 305 specimens of undetermined ori- gin (inshore and offshore) were examined for the presence of LLD lesions from 2004 to 2015. Seven- teen residents, 3 non-residents and 1 inshore dolphin of unknown residence status were positive. LLD lesions appeared as single or multiple, light grey to whitish nodules and plaques that may ul- cerate and increase in size over time. Among resident dolphins, prevalence varied significantly among 4 communities, being low in Posorja (2.35%, n = 85), Ecuador, and high in Salinas, Ecuador (16.7%, n = 18), and Laguna, Brazil (14.3%, n = 42). LLD prevalence increased in 36 T. truncatus from Laguna from 5.6% in 2007−2009 to 13.9% in 2013−2014, albeit not significantly. The disease has persisted for years in dolphins from Mayotte, Laguna, Salinas, the Sanquianga National Park and Bahía Málaga (Colombia) but vanished from the Tramandaí Estuary and the Mampituba River (Brazil). The geographical range of LLD has expanded in Brazil, South Africa and Ecuador, in areas that have been regularly surveyed for 10 to 35 yr. Two of the 21 LLD-affected dolphins were found dead with extensive lesions in southern Brazil, and 2 others disappeared, and presumably died, in Ecuador. These observations stress the need for targeted epidemiological, histological and molecular studies of LLD in dolphins, especially in the Southern Hemisphere.

KEY WORDS: Delphinidae · Cutaneous diseases · Southern Hemisphere · loboi · Paracoccidioides spp.

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*Corresponding author: [email protected] © Inter-Research 2015 · www.int-res.com 60 Dis Aquat Org 117: 59–75, 2015

INTRODUCTION et al. 2011, Daura-Jorge & Simões-Lopes 2011, Bess- esen et al. 2014, Palmer & Peterson 2014). In South Lobomycosis in Delphinidae is a chronic fungal America, LLD occurs in Brazil, Venezuela, Colombia, skin infection characterized by greyish, whitish to Ecuador and Peru with variable prevalence levels slightly pink, verrucous lesions, often in pronounced (Table 1; Van Bressem et al. 2007, Bermúdez et al. relief, that may ulcerate and form plaques exceeding 2009, Daura-Jorge & Simões-Lopes 2011). This skin 30 cm in their broadest dimension (Caldwell et al. condition may pro gress over time and cover exten- 1975, Simões-Lopes et al. 1993, Reif et al. 2006, Van sive body areas, but it is not known to regress (Kiszka Bressem et al. 2007). The disease has been observed et al. 2009, Daura-Jorge & Simões-Lopes 2011, Bess- in common bottlenose dolphins Tursiops truncatus esen et al. 2014). LLD has been associated with the from the USA, Brazil and Europe, in Guiana dolphins death or disappearance of severely affected individ- Sotalia guianensis from Surinam and in an Indian uals, including calves (Simões-Lopes et al. 1993, Van Ocean humpback dolphin Sousa plumbea from Bressem et al. 2007, Moreno et al. 2008, Kiszka et al. South Africa (Table 1; Caldwell et al. 1975, Symmers 2009, Daura-Jorge & Simões-Lopes 2011). 1983, Cowan 1993, Simões-Lopes et al. 1993, Reif et Over the past 10 yr, we have observed new cases of al. 2006, Van Bressem et al. 2007, Rotstein et al. 2009, LLD in bottlenose dolphins from South America and Lane et al. 2014). Microscopically, lemon-shaped, southern Africa, sometimes in areas where the dis- budding -like organisms resembling Lacazia ease had never been seen before although they had loboi (Taborda et al. 1999) were detected in skin been surveyed for several years. As earlier recom- lesions sampled in T. truncatus (Caldwell et al. 1975, mendations urged close follow-up work on the dyna - Simões-Lopes et al. 1993, Paniz-Mondolfi et al. 2012, mics and spread of skin diseases worldwide (IWC Van Bressem et al. 2007) and a S. guianensis from the 2009), here we report on these cases as well as on the Americas (Symmers 1983), and in a S. plumbea from progression of the lesions in some individuals, and on South Africa (Lane et al. 2014; Table 1). However, the geographic expansion of the disease in Brazil, recent molecular characterization of the 43 kDa gly- Ecuador and southern Africa. coprotein coding gene and of ribosomal DNA from lesions sampled in T. truncatus from the USA and Cuba, and in Indo-Pacific bottlenose dolphins T. adun- MATERIALS AND METHODS cus from Japan, indicated that the yeast-like organ- ism infecting these dolphins is more closely related Study areas and surveys (94−97%) to Paracoccidioides brasiliensis than to L. loboi (Rotstein et al. 2009, Esperón et al. 2012, Ueda Photo-identification (PI) surveys, most of these et al. 2013). Paracoccidioides spp. and L. loboi are dedicated and spanning multiple years, were carried dimorphic fungi that belong to the order Onygenales, out in South Africa, Mayotte, Ecuador, Colombia and family Ajellomycetaceae (Herr et al. 2001, Theodoro Brazil between 2004 and 2015. Some surveys were et al. 2012). Paracoccidioides spp. are the agents of opportunistic and were implemented during whale- , a serious systemic disease watching activities, acoustic research or shark stud- that involves multiple organs in cluding the skin, in ies. Systematic beach combing to record and sample humans and terrestrial mammals from South Amer- stranded marine mammals was also carried out in ica (Bagagli et al. 2003, Ricci et al. 2004, Corredor et southern Brazil in 2004 to 2014. The areas studied al. 2005, Richini-Pereira et al. 2008, Bocca et al. included bays, lagoons, estuaries and coastal waters 2013). for which salinity, water quality and sea surface tem- Skin diseases highly reminiscent of lobomycosis peratures (SST) varied widely (Table 2). We provide but for which a histological diagnosis was not avail- mid-point coordinates for the marine parks, bays, able have been observed in several populations of lagoons and estuaries and the northern and southern T. truncatus, T. aduncus, S. guianensis and Austra - limits for the areas covered during beach surveys. lian snubfin dolphin Orcaella heinsohni worldwide and have been called lobomycosis-like disease or lacaziosis-like disease (LLD; based on the name of Mayotte the fungus L. loboi, which was initially believed to cause lobomycosis in dolphins, see Table 1; Van Located in the northern Mozambique Channel, Bressem et al. 2007, 2009a,b, Moreno et al. 2008, Mayotte (12° 50’ S, 45° 10’ E) is almost entirely sur- Bermúdez et al. 2009, Kiszka et al. 2009, Burdett Hart rounded by a 197 km long barrier reef. The inner Van Bressem et al.: Lobomycosis-like disease in bottlenose dolphins 61

lagoon ranks as one of the largest in the world about 100 individuals, of which 85 have been photo- (1100 km2, Quod et al. 2000) and is home to a resi- identified (F. Félix unpublished data). Its fluviatile in- dent population of Tursiops aduncus estimated at fluenced coastal waters are contaminated by waste- 82 ± 19 individuals (Kiszka et al. 2012, Pusineri et al. water from fish-processing industries, shrimp farms 2014). The human population has been growing and from Guayaquil, Ecuador’s largest city. In addi- quickly in Mayotte during the last 30 yr, and urban- tion, run-off waters containing pesticides and other ization as well as agriculture have been increasing agrochemicals used in banana and rice plantations in steadily together with the release of untreated fresh- the lower basin of the Guayas River are discharged water run-off in the lagoon. Contamination by im - by several rivers into the inner estuary (CPPS 2014). munosuppressive polychlorinated biphenyls has in - Thirty-three dedicated PI surveys on 8−10 m boats creased in hooded oysters Saccostrea cucullata in the were conducted in Posorja in 2005 to 2014 using digi- period 1997 to 2007 (Thomassin et al. 2008). From tal cameras (6−18 megapixels) with 70−300 and July to October 2014, small-boat based surveys were 100−400 mm zooms. In total, 4270 images of regular conducted in the lagoon with sea conditions not to good quality were analysed for this study. exceeding Beaufort 3. Photographs were taken with Located in the south-eastern part of the inner a digital 35 mm camera equipped with a 100−300 mm estuary of the Gulf of Guayaquil, Bajo Alto (03° 03’ S, lens (Kiszka et al. 2009, 2012). Data were collected 79° 53’ W) was surveyed on 14 April 2013. Among a during 35 survey days, resulting in 29 encounters large group of T. truncatus, 42 individuals were iden- with T. aduncus. A total of 250 photographs allowed tified. These dolphins belong to another community us to identify 16 new individuals and to recapture 19 separate from the one residing in the inner estuary dolphins identified during studies carried out from affected by LLD in 1990−1991 (Félix 1997, Van 2004 to 2009 (Kiszka et al. 2012, Pusineri et al. 2014). Bressem et al. 2007, F. Félix unpublished data). Al- though most habitat and environmental parameters are similar to those of Posorja, Bajo Alto sees less boat South Africa traffic and a more extensive use of fishing nets. Located at the northern edge of the Gulf of Guaya - Located in the Western Cape Province, Plettenberg quil, Salinas (02° 20’ S, 81° 00’ W) in Santa Elena Bay (34° 02’ S, 23° 22’ E) is separated from the Indian Province features a major yacht marina, a large arti- Ocean by the Robberg Peninsula. It receives freshwa- sanal fisheries port and a port for oil tankers, leading ters from the Keurbooms and Piesangs Rivers, consid- to heavy maritime traffic. It is also the main tourist ered of good quality with only some human-related site on the south-west coast of Ecuador. The adjacent disturbance (Department of Water Affairs, South Africa: coast boasts a string of densely populated seaside www.dwa.gov.za/iwqs/ rhp/state_ of_ rivers .html). The resorts and is affected by high levels of microbiologi- T. aduncus sub-population inhabiting Plettenberg cal and chemical pollution (Hurtado et al. 2012). A Bay was estimated to number be tween 1099 and 9492 small resident community of T. truncatus is frequently individuals (95% CI, Phillips 2006). It is part of a ob served close to the port of Salinas. Opportunistic larger population of over 16 000 individuals that surveys were carried out in 2006 to 2014 during ranges along the South African coastline (Reisinger & whale watching trips in the summer months (June to Karczmarski 2010). Data were available for 203 days October). A total of 502 images, from regular to good in the period 2007 to 2010 from a variety of sources, quality, were available for skin disease assessment. mainly collected off tour vessels by research interns with a smaller proportion (10 days) taken from dedi- cated T. aduncus focussed surveys in 2009 (T. Gridley Colombia pers. comm). Some 165 images of 59 dolphins were of sufficient quality to identify skin diseases on the body Declared a National Natural Park in 2010, Bahía areas visible when surfacing. Málaga (3° 56’ N, 77° 21’ W), Valle del Cauca, lies 36 km north of the port of Buenaventura in the Pacific Ocean. It is home to a likely resident T. truncatus Ecuador community (Rengifo et al. 1995) where 2 cases of LLD were observed in 2005 to 2006 (Van Bressem et al. Posorja (02° 42’ S, 80° 15’ W), a small village in 2007, Table 1). The bay is chemically contaminated Guayas Province at the Guayas River delta, is home by illegal logging, by heavy metals from the mining to a resident T. truncatus community estimated at industry in the Dagua and San Juan Rivers and by oil 62 Dis Aquat Org 117: 59–75, 2015 So- _list.htm) _code , Guiana dolphin country T. aduncus T. oneworld/ Moreno et al. (2008) caught at sea; S: stranded; Unkn.: unknown; sp. Ueda et al. (2013) sp. Esperón et al. (2012) worldwide. Spec.: specimens; FR: free-ranging; Nt: to- (H, MD) (H, MD) , Indo-Pacific bottlenose dolphin Paracoccidioides Paracoccidioides Orcaella heinsohni Tursiops truncatus Tursiops and Australian snubfin dolphin Sousa plumbea Gulf of Guayaquil, ECGolfo Dulce, CRBahía Málaga & surroundings, CO Callao, PE 1990−1991PNN Sanquianga & surroundings, CO FRGolfo Dulce, CR 1991−1992 2005−2006 441Unkn., JP FR 2010−2011 FRKagoshima, JP 1.6 56 FR 37Oak Hill, FL, US 2010−2011 2006 Unkn.Cedar Keys, FL, US 12.5Upper Keys, FL, US FR Unkn. 5.4St Augustine, FL, US FR LLD 38−68 Beach, FL, USVero 7.35−10.5 Unkn.Ft. Pierce, FL, US 2007 2013Sarasota, FL, US LLD Unkn. 1968 SRSurinam River Estuary, 1955 LLD FR & CA LLD Bressem et al. (2007) 1969 Van Fort Lauderdale, Unkn. FL, US 1970 S FL, USSarasota Bay, LLD Unkn. FR FR 1970Laguna Lagoon, BR 1971 Unkn. FR FL, US Bessesen et al. (2014) Sarasota Bay, early 1980s FR LLD Herrera et al. (2013) Unkn. Unkn. 1970Gulf of Mexico, TX, US Bressem et al. (2007) Van Unkn. Unkn.Santa Catarina, Baía Norte, 1970 BR C BC 50−60 Unkn. Unkn. BC 1980−1989 Bessesen et al. (2014) BR Estuary, Tramandaí 1993−2004 Unkn. FR Unkn. Unkn. No fungi detected Unkn. Unkn. FR 1990−1999Indian River Lagoon, FL, US Bressem et al. (2007) 1990 Van FR C Unkn. Unkn. 1992 Unkn.Unkn., CU et al. (2015) Tajima 25 FR 106 1999−2005 2000−2006 Unkn. LLD LLD 39 Lobomycosis (H, EM)Atlantic coast of Florida, US LLD S Lobomycosis (H) Unkn. Lobomycosis (H) 117 FR FR Unkn. LLD FR FL, USCharlotte Harbor, Caldwell et al. (1975) 4.7 2002−2008 Unkn. 5.1 Unkn. Bossart (1984) & Laarman (1973) de Vries 704 10 1.7 Lobomycosis (H) & LLD Lobomycosis (H) Caldwell et al. (1975) Caldwell et al. (1975) Unkn. FR Unkn. Burdett Hart et al. (2011) Caldwell et al. (1975) 2003 Caldwell et al. (1975) LLD 6.8 20.0 Migaki et al. (1971) 284 Lobomycosis (H) Lobomycosis (H) Lobomycosis (H) 2002 Lobomycosis (H) & LLD LLD FR 2.1 Bressem et al. (2007), Van Simões-Lopes et al. (1993) Burdett Lobomycosis (H) Hart et al. (2011) Cowan (1993) Caldwell et al. (1975) CA 591 Murdoch et al. (2008) Unkn. Bressem et al. (2007) Van 1.9 Unkn. LLD LLD Murdoch et al. (2010) Burdett Hart et al. (2011) , Indian Ocean humpback dolphin Ocean province and species LocationEast Pacific truncatus T. truncatus T. truncatus T. truncatus T. truncatus T. Sampling truncatus T. Spec. Pacific West aduncus T. Nt aduncus T. Atlantic West Prev. period truncatus T. truncatus T. truncatus T. truncatus T. Diagnosis truncatus T. truncatus T. truncatus T. Reference(s) S. guianensis truncatus T. truncatus T. (%) truncatus T. truncatus T. truncatus T. truncatus T. truncatus T. truncatus T. truncatus T. truncatus T. truncatus T. Table 1. Lobomycosis and lobomycosis-like disease (LLD) in common bottlenose dolphin Table talia guianensis tal number of dolphins; Prev.: prevalence;tal number of dolphins; Prev.: PNN: Parque Nacional Natural (National Park); CA: captive; BC: by-catch; C: H: histology; EM: electron microscopy; MD: molecular diagnosis; country abbreviations follow ISO Code 2 (www.nationsonline.org/ Van Bressem et al.: Lobomycosis-like disease in bottlenose dolphins 63

pollution (Torres et al. 2012, PNN Uramba Bahía Málaga 2014). Dedicated surveys were conducted daily from a 20 m high shore platform using 7 × 50 binoculars in August and September 2008. Effort time was 488 h of observation. Located in the Nariño department, bordering Ecuador, the Sanquianga National Park (02° 55’ N, 78° 30’ W) covers 8900 km2 along a 60 km coastal strip of Colombia’s Pacific Ocean (Naranjo et al. 2006). Comprising a large delta formed by the San- quianga, Patía, La Tola, Aguacatal and Tapaje Ri - vers, the park protects a complex system of estuaries, Moreno et al. (2008) channels, open lagoons and intertidal sand plains, mostly covered by dense mangrove forest (Díaz & Acero 2003). The coastal waters adjacent to the park sp. Rotstein et al. (2009) are home to a community of T. truncatus that is seen year-round and is likely resident. Two cases of LLD were observed in this community in 2010 to 2011

(H, MD) (Table 1; Herrera et al. 2013). The rivers, especially the Patía, are biologically and chemically contami-

Paracoccidioides nated by fertilizers used for coca plantations, by heavy metals from the mining industry, by the inade- quate management of solid waste from local people and by commercial logging (PNN Sanquianga 2013, Parra & Restrepo 2014). PI surveys (29 h) were con- ducted opportunistically from a fibreglass boat in the waters adjacent to the park from 1 to 6 July 2013. Thirteen images of regular quality were used for skin disease assessment. Table 1 (continued) Table

Brazil

In the period 2005 to 2015, weekly boat-based sur- veys were conducted in the Patos Lagoon estuary (PLE; 32° 06’ S, 52° 05’ W) and adjacent coastal areas (32° 48’ S, 52° 28’ W) to photo-identify T. truncatus, as described by Fruet et al. (2015a,b). Analysis of 80 514 photographs taken during 334 boat surveys resul - ted in the identification of 273 T. truncatus, of which 152 were residents of the PLE and surrounding areas (Fruet et al. 2011, 2015a) and 121 were inshore dolphins that included transient, temporary and partially resident dolphins (R. Genoves pers. comm). During regular beach surveys covering about 345 km (135 km north to 220 km south of PLE, 33° 44’ S, Mampituba River, BRMampituba River, Indian River Lagoon, FL, USIsla Margarita, VE 2003−2004 FL, USSarasota Bay, 2003−2004North Carolina, US FR FR BRParanaguá Estuary, Laguna Lagoon, BR Unkn. 30Santa Catarina, Baía Sul, BR 2004 2004 Unkn. 2005 & 2008 2006−2007 30.0Bay of Biscay S 2009 FR FR S 2007−2009Mayotte Lagoon, YT Unkn. AUDarwin Harbour, Lobomycosis (H) LLD Unkn. 156 FR 103 FRKwaZulu-Natal, ZA Unkn. Unkn. Reif et al. (2006) Unkn. 57 5.8 3.9 2004−200853° early 1970s Unkn. 2008−201022’ Bressem et al. (2007), Van FR BC Lobomycosis (H), LLD 2010−2012 8.8 W FR LLD Burdett Hart et al. (2011) Unkn.to BC 71 Unkn. LLD31° Unkn. LLD Unkn. 521’ 8.5 Lobomycosis (H, EM) LLDS, Bermúdez et al. (2009) Symmers (1983) 51° Bressem et al. (2009a) Van 20 Daura-Jorge & Simões-Lopes (2011) 01’ LLD W) Daura-Jorge & Simões-Lopes (2011) LLD Lobomycosis (H)in 2004 Palmer & Peterson (2014) Lane et al. (2014) Kiszka et al. (2009) to 2014, 130 T. truncatus were found stranded. Although they mostly included inshore dolphins (residents and non- residents), a small proportion (<5%) may have been offshore T. truncatus (EcoMega unpublished data). The PLE, which covers ca. 971 km2, is connected to T. truncatus T. truncatus T. truncatus T. truncatus T. S. guianensis truncatus T. truncatus T. East Atlantic truncatus T. Indian Ocean aduncus T. O. heinsohni S. plumbea Ocean province and species Location truncatus T. Sampling Spec. Nt Prev. period Diagnosisthe Atlantic Reference(s) Ocean (%) through a single 700 m wide arti- 64 Dis Aquat Org 117: 59–75, 2015 29 (summer) 29 (summer) 27 (summer) 27 (summer) 29 (summer) 24.4 (winter) 26.5 (summer) 23−26 (summer) sitives; Prev.: prevalence; SST: sea sur- prevalence;sitives; Prev.: SST: 1 Unkn 17.1 35.3 a bottlenose dolphins from South America and southern Africa T. aduncus T. and Indo-Pacific Tursiops truncatus Tursiops temperature; IN: inshore; OFF: offshore; R: resident; NR: non-resident Baía Norte, BR BRSepetiba Bay, ZAPlettenberg Bay, 27° 30’ S, 48° 32’ W 22° 55’ S, 43° 53’ W 34° 02’ S, 23° 22’ E IN IN IN Unk. NR S NR FR 2014 Oct FR 2005−2014 Unkn 2007−2010 1 1 [59] Unkn 1 15 (winter) Unkn 25 22.6 29 Mampituba, BR Laguna, BRShoreline adjacent to Laguna, BR 28° 14’ S, 48° 39’ W & IN & OFF R & NR 28° 30’ S, 48° 50’ W S 29° 19’ S, 49° 43’ W IN 2012 R 9 FR 0 2013−2014 0 42 14.4 (winter) 30.5−35.7 6 14.3 20 3.5−18 Shoreline adjacent to Lagoa 31° 21’ S, 51° 02’ W to & do Peixe, Tramandaí IN & OFF R & NR S 29° 19’ S, 49° 42’ W 2008−2014 16 0 0 12 (winter) 20−37 Mayotte, YT 12° 50’ S, 45° 10’ E IN R FR Jul−Oct 2014 35 2 5.7 28.6 35 Posorja, ECBajo Alto, ECSalinas, ECSanquianga coast, COBahía Malaga, COPatos Lagoon estuary 02° 38’ N, 78° 15’ W(PLE), BR 02° 42’ S, 80° 15’ W 03° 03’ S, 79° 53’ WCoastal waters adjacent 03° 53’ N, 77° 22’ W INto PLE, BR 02° 20’ S, 81° 00’ W 32° 06’ S, 52° 05’ W INShoreline adjacent IN 32° 48’ S, 52° 28’ Wto PLE, BR IN IN BR Estuary, Tramandaí R IN R IN RMampituba River & adjacent 33° 44’ S, 53° 22’ W to FR R IN & OFFcoastal waters, BR 29° 19’ S, 49° 42’ W 29° 57’ S, 50° 07’ W R FR R & NR R FR R & NR Jul 2013 FR FR 2005−2014 S FR IN Apr 2013 Aug−Sep 2008 IN FR Unkn 2005−2015 Unkn 31° 21’ S, 51° 01’ W 85 2006−2014 2004−2014 2005−2015 R & NR 42 3 1 121 130 FR Unkn 18 2 R Unkn 152 0 0 2.35 2009−2013 1 3 0 FR 25.5 0 0 0.77 25 16.7 28 21.5−28 2009−2010 0 9 (winter) 22.8−27.4 9 (winter) 0 33.5 21.5−28 24−30 12−15 (winter) 9 0−35 30 33−35.1 27.7 0 27.7 24−30 0 14 (winter) 0 0−37 12 (winter) 1.8−37.2 Only dolphins with skin lesions T. truncatus T. truncatus T. Indian Ocean aduncus T. T. truncatus T. truncatus T. T. truncatus T. T. aduncus T. T. truncatus T. truncatus T. truncatus T. truncatus T. Atlantic West truncatus T. truncatus T. truncatus T. truncatus T. truncatus T. Ocean province and species LocationEast Pacific truncatus T. Geographic Eco- coordinates Res. Spec. Sampling type Nt pattern N Prev. SST period Salinity pos (%)a (°C) Table 2. New cases of lobomycosis-like disease in common Table in 2004 to 2015. Res: Residence; Spec.: specimens; FR: free-ranging; S: stranded; Nt: total number examined; Npos: of po Van Bressem et al.: Lobomycosis-like disease in bottlenose dolphins 65

ficial inlet (Kjervfe 1986). The PLE and adjacent estuaries of Mampituba and Tramandaí and a 180 km areas are characterized by a high anthropogenic area that extended southward to the Lagoa do Peixe influence, including boat traffic, fishing and contam- National Park (31° 21’ S, 51° 02’ W). ination with polycyclic aromatic hydrocarbons (Gar- Covering about 300 km2 (28° 30’ S, 48° 50’ W), La- cia et al. 2010) and mercury (Mirlean et al. 2003). The guna is among the largest lagoon systems in southern PLE hydrodynamics are mainly driven by wind and Brazil consisting of 3 smaller lagoons (Mirim, Imaruí freshwater input that result in flood regimes in the and Santo Antônio). Bordering the city of Laguna, the channel area and play a key role in the control of lagoon is polluted by effluents from anthropogenic ac- salinity (Pinotti et al. 2011). tivities including rice agriculture, shrimp farming and Located in the north of Rio Grande do Sul, the Tra- coal mining (Daura-Jorge & Simões-Lopes 2011). A mandaí Lagoon (29° 57’ S, 50° 07’ W) covers an area community of 52 to 57 resident common bottlenose of about 13 km2 with an average depth of 1.5 m dolphins, studied since 1989, inhabits the Santo An- (Schwarzbold & Schäfer 1984). It receives fresh water tônio and Imaruí Lagoons (Simões-Lopes & Fabian from the Rio Tramandaí and the Camarão Channel 1999, Daura-Jorge et al. 2013). It is endemically af- and is connected to the Atlantic Ocean by a narrow fected by LLD, with a prevalence of 9% for 57 dol- inlet bordering the municipalities of Imbé and Tra- phins in 2007 to 2009 (Daura-Jorge & Simões-Lopes mandaí where a small community of T. truncatus 2011). During 2013 and 2014, boat surveys were con- resides (Simões-Lopes & Fabian 1999, Zappes et al. ducted weekly along pre-defined routes to collect 2011, Di Giacomo & Ott in press). LLD was detected photo-identification data (Daura-Jorge et al. 2013). in 2 adults in the period 1999 to 2005 (Moreno et al. About 12 000 photographs were taken during 76 sur- 2008). The estuary is contaminated with a high load veys and 42 resident dolphins were identified. In of faecal coliforms (Haase et al. 2003, FEPAM 2015), 2012, a coastal beach survey recorded stranding hydrocarbons and heavy metals (Andrade et al. 2004, events along 150 km of shoreline adjacent to Laguna Rocha 2013). During the present study, PI surveys (28° 14’ S, 48° 39’ W and 29° 19’ S, 49° 43’ W). were carried out in the mouth of the Tramandaí estu- Baía Norte (27° 30’ S, 48° 32’ W) and Baía Sul ary in January 2009 to February 2010. About 2050 (27° 43’ S, 48° 36’ W) are 2 coastal bays that separate photographs were analysed, and 9 dolphins were Santa Catarina Island from the mainland. Covering identified, including 3 calves (Di Giacomo & Ott in ca. 250 km2, Baía Norte is greatly influenced by open press). waters. Contiguous to a densely populated area The Mampituba River drains a 1200 km2 watershed without adequate sanitation, the bay is exposed to area, has a mean depth of around 4 m and is under a high levels of chemical and biological contaminants microtidal regime (D’Aquino et al. 2011). The river (Souza et al. 2012). Non-systematic PI surveys in mouth (29° 19’ S, 49° 42’ W) straddles the border be- 2008 to 2011 suggest that a small inshore community tween the states of Rio Grande do Sul and Santa of at least 11 T. truncatus shows some degree of site Catarina. Its narrow inlet has been stabilized by jet- fidelity to Baía Norte and/or Baía Sul (F. Daura-Jorge ties to support a fishing harbour since 1970 (Lélis & & P. Simões-Lopes unpubl. data). LLD was re por ted Calliari 2006). Along its course, the river receives in 2 T. truncatus from Baía Norte between 1993 and domestic sewage, agricultural drainage and munici- 2004 (Flores et al. 2005, Van Bressem et al. 2007) and pal wastewaters (Andrade et al. 2004). In 1995 to in 2 dolphins from Baía Sul in 2009 (Daura-Jorge & 2008, 6 common bottlenose dolphins had been photo- Simões-Lopes 2011). identified in the river mouth, including 1 with LLD Located in southern Rio de Janeiro State (22° 55’ S, (Moreno et al. 2008). New PI surveys were carried 43° 53’ W), Sepetiba Bay covers approximately 526 km2 out from April 2009 to April 2013 in the river mouth and is connected to the Atlantic Ocean through the and adjacent coastal waters, covering 20 km of the western part of the bay. The eastern side features an coast. In total, 1480 images were examined and 22 extensive mangrove forest and receives a high input adults were photo-identified. Most of the dolphins of fresh water from river drainage systems (Pessanha were seen in the coastal area outside the estuary, and & Araújo 2003, Flach et al. 2008). It is home to 4 large only 2 entered the channel (Di Giacomo 2014, ports and suffers from increasing organic and chemi- GEMARS unpublished data), possibly because water cal contamination with more than 400 chemical, rub- quality had deteriorated (Haase et al. 2003, FEPAM ber, printing and metal factories in the surrounding 2015). Systematic coastal beach surveys were con- area (Copeland et al. 2003, Molisani et al. 2004, ducted in 2008 to 2014 to record stranding events Ribeiro et al. 2013). A resident community of Sotalia along a 260 km shoreline, ca. 80 km between the guianensis estimated at 1269 dolphins (95% CI = 66 Dis Aquat Org 117: 59–75, 2015

739−2196) inhabits the entrance of the bay and has body exposed at surfacing could be examined. We been the object of PI studies since 2005 (Flach et al. only compared communities where dolphins were 2008). From 2005 to 2014, a total of 334 surveys were photo-identified and where LLD was present, which conducted along pre-defined routes to collect S. guia- limited our analysis to 4 resident communities nensis PI data (Flach 2015). T. truncatus were never (Posorja, Salinas, Laguna and Mayotte). Prevalence seen in the bay until September 2013 (Flach 2015). variation between study areas was assessed with a Kruskal-Wallis test. Temporal variation in prevalence in Laguna between 2007−2009 and 2014 was exam- Data collection and analysis ined with McNemar’s test using exact binomial prob- ability calculations (www.vassarstats.net/propcorr. The large majority of the bottlenose dolphins exa - html). All significance levels were set at α = 0.05. mined during this study belong to the inshore eco- type (Table 2). However, an unknown percentage of the dolphins stranded in southern Brazil were likely RESULTS of the offshore ecotype (Costa et al. 2015, Ott et al. in press). Inshore dolphins were further classified as The presence of LLD was examined in 658 Tursiops resi dents (high sighting frequencies within and truncatus from South America and 94 T. aduncus from between years, high site fidelity) or non-residents southern Africa (Table 2). Photographs and stranding (transients and semi-residents; Table 2). Individual records of 387 inshore residents, 60 inshore non- dol phins were identified through natural marks residents and 305 specimens of undetermined origin (Würsig & Jefferson 1990). Maturity status (calf, juve- (resident or non-resident inshore or offshore dol- nile, adult) was estimated from relative body size and phins) were examined for the presence of LLD lesions colouration, scars, behavioural clues and from the (Table 2). LLD cases were detected in 17 residents (2, verified duration of residence (Félix 1994, Di Gia- Mayotte; 5, Ecuador; 4, Colombia; 6, Brazil), in 3 non- como & Ott in press). Calves were defined as individ- residents (1, South Africa; 2, Brazil) and in 1 inshore T. uals whose body length was one-third or less than truncatus of unknown residence status in Brazil that of the larger dolphins in the area and which usu- (Fig. 1). The disease had persisted in minimum 3, and ally remained close to the same adult (Mann & Smuts perhaps 4, of these dolphins since previous studies 1999, Mann et al. 2000, Fruet et al. 2015a,b). (Van Bressem et al. 2007, Kiszka et al. 2009, Daura- Holders of PI catalogues of T. truncatus and Jorge & Simões-Lopes 2011). Thus, the number of true T. aduncus searched for the presence of skin lesions new cases amounts to 17 or 18 bottlenose dolphins. evoking LLD, i.e. multiple firm, light grey or whitish to slightly pink nodules, often raised, forming plaques and ulcerating, which may spread to the entire body Mayotte (Van Bressem et al. 2007, 2009a, Kiszka et al. 2009, Daura-Jorge & Simões-Lopes 2011). Images of sus- From July to October 2014, small-boat surveys pected positive dolphins were extracted and further allowed us to photographically recapture 19 known examined by M.F.V.B. and K.V.W. The relative size individuals and to identify an additional 16 T. adun- of the lesions was expressed as a percentage (P) = cus. While negative from 2005 to 2008, an adult had

Alesion/Adorsal × 100, where Alesion is the area of the le- developed small and medium LLD lesions on its dor- sion and Adorsal is the 1-sided area of the dorsal fin sum and tailstock by October 2014 (Fig. 2A,B). In (DFA; Daura-Jorge & Simões-Lopes 2011). Relative individual MY08, chronic LLD lesions on the dorsum size of lesions (% of DFA) was estimated from images and tailstock had clearly progressed, covering 1% of magnified on-screen and assigned to 1 of 4 catego - the visible body surface in 2006 (Kiszka et al. 2009) to ries: small (<10%), medium (10−20%), large (20− approximately 20% in 2014. 50%) and very large (>50%). Time series allowed an evaluation of relative progress in 2 T. truncatus from Posorja and Salinas. Prevalence of LLD was calcu- South Africa lated as the ratio of affected individuals to the number of PI dolphins in a community or to the total One case of LLD was observed in a T. aduncus in number of stranded dolphins examined during the Plettenberg Bay (Fig. 2C) on 11 November 2008. The study period. In free-ranging dolphins, prevalence dolphin had several small to medium-sized nodules, levels were minimal as, generally, only the upper some confluent and ulcerated, on the dorsum, right Van Bressem et al.: Lobomycosis-like disease in bottlenose dolphins 67

Fig. 1. Locations in South America and Africa where lobomy cosis-like disease was observed in bottlenose dol- phins Tursiops truncatus and T. aduncus

flank (Fig. 2C) and tailstock. LLD was not recognized on any good quality photographs of 58 other individ- uals identified between 2007 and 2010 and specifi- cally examined for skin disease (du Toit 2011).

Ecuador

Two (P58 and P59) of 85 (2.35%) T. truncatus photo-identified since 2005 in Posorja were observed with LLD in April 2011 (Fig. 3A,B). They were seen swimming together on 3 occasions in 2011 but were no longer encountered in 2014. In both individuals, the skin was affected on both sides of the dorsal fin (DF). In P58, small LLD nodules present at the base of the right side of the DF in April 2011 had grown and coalesced to form a larger lesion by February 2013 (Fig. 3A,B), i.e. an increase from 14.5 to 24.4% of DFA (Fig. 4). LLD was not detected in 42 T. truncatus pho- tographed in April 2013 in Bajo Alto. Fig. 2. Lobomycosis-like disease (LLD) in Indo-Pacific bot- Twenty-one T. truncatus groups (4–8 ind. per group) tlenose dolphins Tursiops aduncus from the Indian Ocean. (A) Absence of LLD in a dolphin from Mayotte in 2005; (B) were observed in Salinas between 2006 and 2014. Of small and medium-sized LLD lesions on the dorsum of the the 18 PI dolphins, 3 (16.7%) showed small to large same dolphin in October 2014; (C) several small to medium- LLD lesions on the DF, dorsum, flanks and tailstock sized LLD lesions on the back and right flank of a T. aduncus during that period. In dolphin S4, a whitish lesion from Plettenberg Bay, South Africa, in November 2008 located at the base of the dorsal fin (right side) in - creased markedly from 8.5% DFA in September 2006 Colombia to 28.5% DFA in April 2010 (Figs. 3C−E & 4). A lesion located on the left side of the dorsal fin progressed An adult T. truncatus with LLD lesions was sighted from 25% DFA in 2006 to 50% DFA in 2009 (Fig. 4). in Bahía Málaga on 9 August 2008 (Table 2). The dol- It did not visibly grow in 2010 to 2011 (Fig. 4). phin was part of a group of 9 individuals. However, 68 Dis Aquat Org 117: 59–75, 2015

Small to medium LLD lesions were seen in 2 T. truncatus among a group of 50 passing off ‘Playa Mulatos’ in Pacific waters adjacent to the Sanqui - anga National Park on 3 July 2013 (Fig. 3C, Table 2). On 6 July 2013, another T. truncatus with possible LLD lesions was observed among 20 dolphins feed- ing at the mouth of the Amarales River, close to the village of Amarales, in the park. These dolphins were different from the 3 individuals with LLD docu- mented in 2010 to 2011 by Herrera et al. (2013).

Brazil

Rio Grande do Sul State

LLD was not detected in 152 PLE T. truncatus from the Patos Lagoon estuary during 10 yr (2005−2015) of systematic PI studies and more than 20 yr of non- systematic PI studies (EcoMega unpubl. data; Table 2). It was also not detected in 121 resident and non- resident inshore T. truncatus inhabiting coastal waters adjacent to the PLE and photo-identified during the same period. Among the 130 T. truncatus of mixed Fig. 3. Lobomycosis-like disease (LLD) in common bottle- origin found washed ashore during beach surveys nose dolphins Tursiops truncatus from the Southeast Pacific. along the seashores adjacent to the PLE in 2004 to Progression of LLD in dolphin P58 in (A) April 2011 and (B) 2014, 1 dolphin (0.77%) had LLD (Table 2). The 26 yr February 2013 from Posorja, Ecuador; and in individual S4 old male stranded dead at Cassino Beach (32° 48’ S, from the Salinas community (Ecuador) in (C) 2006, (D) 2008 and (E) 2010. (F) LLD lesions on the dorsum and flank of a 52° 28’ W), 80 km south of the PLE on 18 January dolphin nearshore in Sanquianga National Park, Colombia, 2009, had numerous, small to very large, light grey, 3 July 2013 verrucous LLD lesions that affected approximately 30% of its body surface (Fig. 5A). Supported by PI 60 data, its mtDNA control region haplotype matched the most common haplotype found in the Southwest- 50 ern Atlantic inshore ecotype (Fruet et al. 2014). The 40 dolphin did not belong to the communities residing in the PLE and adjacent coastal waters and was likely a 30 transient. LLD was not observed in any of the T. truncatus 20 (6 adults and 3 calves) that were repeatedly photo - graphed in the Tramandaí estuary from January 2009 10 to February 2010. Of the 6 adults, 4 (I6, I7, I9, I11)

Lesion progression (% cover) 0 were known since 1992, 1 (I14) since 2004, and 1 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014 (I15) was first sighted in 2009. Therefore, all adults Fig. 4. Progression of some lobomycosis-like disease lesions but 1 had occupied the estuary during a period when in bottlenose dolphins Tursiops truncatus S4 (blue = left side LLD occurred there (1999−2005). of dorsal fin, red = right side of dorsal fin) and P58 (yellow) During surveys carried out from April 2009 to April from Ecuador 2013, LLD was not detected in T. truncatus (22 adults and 6 calves) photographed in the Mampituba River as it was not photo-identified, it is unknown whether mouth and adjacent inshore waters. Of the 22 adults, it corresponded to 1 of the 2 affected individuals only 1 was known to have used the estuary in 2004 at reported in 2005 and 2006 (Van Bressem et al. 2007) a time when LLD occurred there (2003−2004). None or whether it represented a new case. of the 16 T. truncatus stranded along the coastline Van Bressem et al.: Lobomycosis-like disease in bottlenose dolphins 69

2014 (13.9%) than in 2007 to 2009 (5.6%), though not significantly so (McNemar’s test, χ2 = 1.42, df = 35, p = 0.23). During beach surveys carried out in 2012, 16 T. truncatus carcasses were recovered, including 7 from Laguna and 9 of mixed origin (Table 2). All were negative for LLD. On 21 October 2014, an inshore (confirmed from cranial morphology), sexually mature female T. trun- catus (UFSC-1420) of unknown residence pattern was found dead in Baía Norte, ca. 90 km north of Laguna. It had many elevated, small to very large verrucous lesions on the left flank, ventrum and tail- stock (Fig. 5C). Some lesions were ulcerated and necrotized. Samples were taken for histology and molecular studies (C. Sacristan & J. L. Catão Dias pers. comm.). Fig. 5. Lobomycosis-like disease cases in Tursiops truncatus in the Southwest Atlantic, Brazil: (A) mature male stranded dead in Rio Grande do Sul on 15 January 2009; (B) free- Rio de Janeiro State ranging adult in Laguna on 18 April 2014; (C) adult female stranded dead in Baía Norte, Santa Catarina, on 21 October 2014; and (D) free-ranging dolphin in Sepetiba Bay on On 9 September 2013, an adult-sized T. truncatus 9 September 2013 was photographed with extensive, nodular, ulcerated LLD lesions on its posterior flanks and tailstock between Mampituba estuary and the Lagoa do Peixe (Fig. 5D) in a mangrove area at the centre of Sepetiba National Park in 2008 to 2014 had LLD (GEMARS Bay. Several nodules were associated with tooth - unpubl. data). rakes. The solitary animal moved back and forth within a restricted area (about 0.02 km2) of shallow water less than 6 m deep, during 7 d, after which it Santa Catarina State disappeared. At no point was it seen close to Sotalia guianensis groups. It was thought not to belong to Two of the 4 adult T. truncatus (L07, L20) of Laguna the inshore T. truncatus community inhabiting wa - confir med with LLD in 2007 to 2009 were still ters around Rio de Janeiro (Lodi et al. 2014) but may affected in 2013 to 2014. The other 2 positive individ- represent a transient inshore individual. Although uals (L17, L19) had disappeared (Daura-Jorge & the resident community of S. guianensis is affected Simões-Lopes 2011, unpubl. data). Four other adult by various skin diseases (Van Bressem et al. 2007, dolphins (L04, L34, L38, NI) had developed the dis- 2015), LLD lesions have never been seen in these ease. On 15 January 2014, L34, which had been pho- dolphins (L. Flach pers. obs.). tographed regularly since 2010, was recognized with very large LLD lesions on the head, throat, dorsum, trunk and right flipper (Fig. 5B). The dolphin was Variation in LLD prevalence among study areas seen again on 18 April 2014 with no notable changes in LLD lesion size and corporal distribution. On both Among the inshore/estuarine dolphins, prevalence occasions, it presented an unusual behaviour, namely varied significantly (Kruskal-Wallis test, χ2 = 8.65, continuously leaping out of the water and landing on df = 3, p = 0.0343) among 4 communities with the its right side, during the entire observation period highest prevalence level observed in Salinas (mean ± (40 min). Conceivably pruritus may be a symptom of SD: 0.17 ± 0.38), followed by Laguna (0.14 ± 0.35), LLD, commonly seen in cutaneous mycoses (Fran - Mayotte (0.06 ± 0.24) and Posorja (0.02 ± 0.15; Fig. 6) cesconi et al. 2014), and could trigger such behav- iour. In the other 3 new cases, the disease was char- acterized by single, small to large, light grey, verrucous DISCUSSION lesions. LLD prevalence in adults was 14.3% (N = 42) in 2013 to 2014. In 36 adults examined during both This paper provides an update on the epidemiol- periods, the prevalence of LLD was higher in 2013 to ogy and geographical distribution of LLD in bottle- 70 Dis Aquat Org 117: 59–75, 2015

were available, it appears that progression rate var- ied between lesions in the same individual (S4) and between individuals, as observed in T. truncatus from Sarasota Bay, Florida (Burdett Hart et al. 2010). Very large lesions were observed in a T. aduncus from Mayotte that had been infected for at least 6 yr (2008−2014), in 2 free-ranging T. truncatus from Sepetiba Bay and Laguna and in 2 stranded dolphins from Baía Norte and Cassino Beach. Present and published data indicate that LLD has persisted for several years in the bottlenose dolphin communities of Mayotte (1999−2014), Laguna (1993−2014), Sali- nas (2006−2014), Sanquianga National Park (2010− 2013) and Bahía Málaga (2005−2008) (Van Bressem et al. 2007, Kiszka et al. 2009, Daura-Jorge & Simões- Lopes 2011, Herrera et al. 2013). The disease persists because the affected dolphins failed to clear it and Fig. 6. Variation in lobomycosis-like disease (LLD) preva- lence between bottlenose dolphins from South America and also because new individuals became infected. How- southern Africa ever, our data also show that LLD may vanish from very small T. truncatus communities after the death nose dolphins from South America and southern or disappearance of affected individuals and absence Africa in 2004 to 2015. Beach combing and examina- of new infections. Five of 6 adults from the Traman- tion of photographs taken during dedicated and daí Estuary and 1 from Mampituba River did not con- opportunistic PI surveys resulted in the identification tract LLD although they were photo-identified in of 21 cases of LLD in Mayotte, South Africa, Brazil, 1999 to 2005 when the disease occurred in these Ecuador and Colombia (Fig. 1). Macroscopic charac- communities (Van Bressem et al. 2007, Moreno et al. teristics of LLD varied between individuals, possibly 2008). LLD persistence has been observed in T. trun- reflecting disease progression and individual immuno- catus in the Indian River Lagoon and Sarasota Bay, logic response, ranging from small to very large, Florida, and in Golfo Dulce, Costa Rica (Murdoch et al. whitish to dark grey, isolated or confluent nodules to 2008, Burdett Hart et al. 2011, Bessesen et al. 2014). plaque-like verrucous lesions that were often ulcer- Of the 21 LLD-infected bottlenose dolphins, 17 ated (Figs. 2, 3 & 5). This agrees with observations in were inshore residents inhabiting spatially restricted other Delphinidae populations around the world areas that were biologically and chemically contami- (Rotstein et al. 2009, Van Bressem et al. 2009a,b, nated (see ‘Materials and methods’) and were con- Murdoch et al. 2010, Esperón et al. 2012). However, it stantly exposed to multiple anthropogenic stressors, is possible that different aetiological agents cause including fisheries. Such factors may depress the skin diseases resembling lobomycosis in dolphins immune system and affect skin integrity (Fair & (Tajima et al. 2015), and further research is neces- Becker 2000, Romano et al. 2004, Reif et al. 2009, sary. In the Southern Hemisphere, only 3 histological Martin et al. 2010). Immune compromise was sug- studies have demonstrated the presence of a fungus gested to increase lobomycosis infection risk in T. resembling Lacazia loboi in skin lesions sampled in 2 truncatus in the Indian River Lagoon (Reif et al. 2009, Tursiops truncatus from Laguna (Simões-Lopes et al. Murdoch et al. 2010). A similar situation may occur in 1993) and the Tramandaí Estuary (Moreno et al. resident bottlenose dolphins from South America and 2008) and a third in a Sousa plumbea from South Mayotte. Further studies are needed to investigate Africa (Lane et al. 2014). Molecular analysis of the this hypothesis. pathogenic agents causing LLD in dolphins from Prevalence varied significantly between resident South America and southern Africa will be necessary dolphin communities, being low in Posorja (2.35%) to firmly establish their taxonomic identity, specifi- and high in Laguna (14.3%) and Salinas (16.7%, cally their relationship to known species of the genus Fig. 6). Similarly, LLD prevalence levels in other dol- Paracoccidioides and its sister taxon L. loboi. phin communities worldwide varied widely (Table 1). LLD progression could be assessed in 3 dolphins Although differences in sample size and methodo - that were repeatedly sighted in Salinas, Posorja and logy may explain some of this variation, environmen- Mayotte (Figs. 3 & 4). Although only limited data tal and individual factors likely also play an impor- Van Bressem et al.: Lobomycosis-like disease in bottlenose dolphins 71

tant role. Burdett Hart et al. (2011) suggested that 1999). In Ecuador, LLD was recently (2011−2013) differences in freshwater input could influence the observed in 2 T. truncatus from a community in development and persistence of lobomycosis be - Posorja of around 100 individuals that was regularly tween T. truncatus communities of west and east monitored since 2005. LLD was initially described coast estuaries in Florida. Although several of the from the inner estuary of the Gulf of Guayaquil areas studied here (Laguna, the mangrove area of (02° 52’ S, 80° 01’ W) with a prevalence of 1.6% for Sepetiba Bay, Posorja, Sanquianga National Park 441 dolphins in 1990 to 1991 (Van Bressem et al. and Bahía Malaga) received important riverine 2007). The Posorja record expands the known geo- freshwater input, this was not the case for Salinas graphical range of the disease to include the outer where the highest LLD prevalence was observed. estuary, some 40 km to the west. In South Africa, Wilson et al. (1999) reported that bottlenose dolphin although images of regular quality were available communities from areas of low water temperature since 2006 and opportunistic surveys were carried and low salinity exhibited higher lesion prevalence. out since 1999, LLD was detected only in 1 T. adun- In the present study, high LLD prevalence levels cus in November 2008. A case of lobomycosis was were found in areas of medium (Laguna) and high documented in 1 of 5 S. plumbea by-caught along the (Mayotte and Salinas) salinity, and both in warm coast of KwaZulu-Natal (about 1000 km east of Plet- (28.5°C, Mayotte) and temperate waters (20°C, La - tenberg Bay) in 2010 to 2011 but not in 35 T. aduncus guna; Table 2). Thus, the role of these factors in the accidentally captured in the same region during the ecology of the disease remains unclear. Low genetic same period (Lane et al. 2014). variability could contribute to high LLD prevalence In Laguna, LLD prevalence in 36 adult dolphins levels in some small communities by altering the im- more than doubled (albeit without statistical signifi- mune response (Frank 2002, Sommer 2005). Re cent cance) between 2007 and 2009 (5.6%) and 2014 studies showed that among south-western Atlantic T. (13.9%). This apparent increase may either reflect truncatus, the lowest genetic variability was found in natural fluctuations, or may indicate that the disease the Laguna community where inbreeding is likely to is spreading in this small, declining community, rais- occur, and in a chronically LLD-infected dolphin from ing concern for its long-term survival. Although the Tramandaí Estuary that died in 2005 (Moreno et bottle nose dolphins may live with LLD for years, al. 2008, Fruet et al. 2014, Costa et al. 2015). In severely affected individuals have died or disap- humans, there is mounting evidence that a genetic peared in the Americas and southern Africa, includ- component may predispose individuals to superficial ing 2 adult Laguna residents sighted in 2007 to 2009 fungal infections through alterations of the innate but not in 2014 (Moreno et al. 2008, Bermúdez et al. and adaptive immune system (Gupta et al. 2014). 2009, Kiszka et al. 2009, Daura-Jorge & Simões- LLD seems to have expanded geographically in at Lopes 2011). Among the 21 dolphins observed with least 3 countries where PI surveys and/or beach LLD during this study, 2 were found dead with exten- combing were regularly carried out. In Brazil, LLD sive skin lesions in Brazil and 2 others disappeared was previously determined to be distributed between and presumably died in Ecuador, a presumed 19% the Paranaguá Estuary (25° 22’ S, 48° 25’ W) and the mortality rate. The persistence, high prevalence lev- Tramandaí Estuary in Sotalia guianensis and T. trun- els and unknown case fatality rates of LLD in some catus (Simões-Lopes et al. 1993, Van Bressem et al. small, and sometimes endangered, communities of T. 2007, 2009a, Moreno et al. 2008, Siciliano et al. 2008, truncatus and T. aduncus are a cause for concern. Daura-Jorge & Simões-Lopes 2011). New LLD re - These data stress the need for intensified, targeted cords in T. truncatus from Sepetiba Bay and Cassino epidemiological, histological and molecular studies Beach, areas that have been extensively surveyed of this disease in Delphinidae in the Southern Hemi- since the late 1970s (Cassino) and 2005 (Sepetiba), sphere. expand the known distribution of the disease 520 km to the north (22° 55’ S, 43° 53’ W) and ca. 390 km to Acknowledgements. We thank 3 anonymous reviewers for the south (32° 48’ S, 52° 28’ W). The Sepetiba and their constructive comments on the manuscript. We thank Lina Correa for help with data collection in Bahía Málaga Cassino individuals were transient inshore dolphins, and surroundings; and Johana Velasquez, Colombo Estu - suggesting that these communities may play a role piñán, Paula Casas and Saturnino Montaño for their sup- in the geographic expansion of LLD. Interestingly, port. Rodrigo Genoves and Rafael Camargo are kindly in South America, the first T. truncatus reported acknowledged for collecting the T. truncatus stranded south of the Patos Lagoon Estuary. We thank researchers from with lobomycosis in 1990 was a transient specimen GEMARS and the support from CECLIMAR/UFRGS for col- (Simões-Lopes et al. 1993, Simões-Lopes & Fabian lecting the stranded common bottlenose dolphin from the 72 Dis Aquat Org 117: 59–75, 2015

northern coast of Rio Grande do Sul and Silvina Botta for age centralis (Miller 1899): a new host to Paracoccidioides determination of the dolphin from Cassino Beach, Brazil. We brasiliensis. Molecular identification of the isolate. Med thank J. Brack and R. Amboni for providing Figs. 2B and 5B, Mycol 43: 275−280 respectively. A fellowship and financial support was granted Costa APB, Fruet P, Daura-Jorge FG, Simões-Lopes PC, Ott by the Conselho Nacional de Desenvolvimento Científico e PH, Valiati VH, Oliveira LR (2015) Bottlenose dolphin Tecnológico (CNPq) to E.R.S. (PQ 307846/2014-8) and P.H.O. communities from the southern Brazilian coast: Do they (Process 572180/2008-0), who contributed as members of exchange genes or are they just neighbours? Mar Freshw the Research Group ‘Ecologia e Conservação da Megafauna Res (in press) http: //dx.doi.org/10.1071/MF14007 Marinha − EcoMega/CNPq’ and ‘Ecologia e Conservação de Cowan DF (1993) Lobo’s disease in a bottlenose dolphin Organismos e Ambientes Aquáticos − ECOAqua/ CNPq’. (Tursiops truncatus) from Matagorda Bay, Texas. J Wildl L.F. was sponsored by Petrobras through Petrobras Socio Dis 29:488−489 Ambiental. We thank T. Gridley, V. Cockcroft and M. N. CPPS (Comisión permanente del Pacifico Sur) (2014) Estado Bester for assistance with the South African data access and del Medio Ambiente Marino y Costero del Pacífico Sud- analysis, as well as the Centre for Dolphin Studies and Orca este. Serie Estudios Regionales 4. CPPS, Guayaquil Foundation. 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Editorial responsibility: Michael Moore, Submitted: March 23, 2015; Accepted: September 21, 2015 Woods Hole, Massachusetts, USA Proofs received from author(s): October 30, 2015