Content uploaded by Marie-Francoise Van Bressem
Author content
All content in this area was uploaded by Marie-Francoise Van Bressem on Jul 11, 2019
Content may be subject to copyright.
DISEASES OF AQUATIC ORGANISMS
Dis Aquat Org
Vol. 117: 59–75, 2015
doi: 10.3354/dao02932 Published November 17
© Inter-Research 2015 · www.int-res.com*Corresponding author: mfb.cmed@gmail.com
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 · Lacazia loboi ·
Paracoccidioides spp.
Resale or republication not permitted without written consent of the publisher
Dis Aquat Org 117: 59–75, 2015
INTRODUCTION
Lobomycosis in Delphinidae is a chronic fungal
skin infection characterized by greyish, whitish to
slightly pink, verrucous lesions, often in pronounced
relief, that may ulcerate and form plaques exceeding
30 cm in their broadest dimension (Caldwell et al.
1975, Simões-Lopes et al. 1993, Reif et al. 2006, Van
Bressem et al. 2007). The disease has been observed
in common bottlenose dolphins Tursiops truncatus
from the USA, Brazil and Europe, in Guiana dolphins
Sotalia guianensis from Surinam and in an Indian
Ocean humpback dolphin Sousa plumbea from
South Africa (Table 1; Caldwell et al. 1975, Symmers
1983, Cowan 1993, Simões-Lopes et al. 1993, Reif et
al. 2006, Van Bressem et al. 2007, Rotstein et al. 2009,
Lane et al. 2014). Microscopically, lemon-shaped,
budding yeast-like organisms resembling Lacazia
loboi (Taborda et al. 1999) were detected in skin
lesions sampled in T. truncatus (Caldwell et al. 1975,
Simões-Lopes et al. 1993, Paniz-Mondolfi et al. 2012,
Van Bressem et al. 2007) and a S. guianensis from the
Americas (Symmers 1983), and in a S. plumbea from
South Africa (Lane et al. 2014; Table 1). However,
recent molecular characterization of the 43 kDa gly-
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-
cus from Japan, indicated that the yeast-like organ-
ism infecting these dolphins is more closely related
(94−97%) to Paracoccidioides brasiliensis than to L.
loboi (Rotstein et al. 2009, Esperón et al. 2012, Ueda
et al. 2013). Paracoccidioides spp. and L. loboi are
dimorphic fungi that belong to the order Onygenales,
family Ajellomycetaceae (Herr et al. 2001, Theodoro
et al. 2012). Paracoccidioides spp. are the agents of
paracoccidioidomycosis, a serious systemic disease
that involves multiple organs in cluding the skin, in
humans and terrestrial mammals from South Amer-
ica (Bagagli et al. 2003, Ricci et al. 2004, Corredor et
al. 2005, Richini-Pereira et al. 2008, Bocca et al.
2013).
Skin diseases highly reminiscent of lobomycosis
but for which a histological diagnosis was not avail-
able have been observed in several populations of
T. truncatus,T. aduncus, S. guianensis and Austra -
lian snubfin dolphin Orcaella heinsohni worldwide
and have been called lobomycosis-like disease or
lacaziosis-like disease (LLD; based on the name of
the fungus L. loboi, which was initially believed to
cause lobomycosis in dolphins, see Table 1; Van
Bressem et al. 2007, 2009a,b, Moreno et al. 2008,
Bermúdez et al. 2009, Kiszka et al. 2009, Burdett Hart
et al. 2011, Daura-Jorge & Simões-Lopes 2011, Bess-
esen et al. 2014, Palmer & Peterson 2014). In South
America, LLD occurs in Brazil, Venezuela, Colombia,
Ecuador and Peru with variable prevalence levels
(Table 1; Van Bressem et al. 2007, Bermúdez et al.
2009, Daura-Jorge & Simões-Lopes 2011). This skin
condition may pro gress over time and cover exten-
sive body areas, but it is not known to regress (Kiszka
et al. 2009, Daura-Jorge & Simões-Lopes 2011, Bess-
esen et al. 2014). LLD has been associated with the
death or disappearance of severely affected individ-
uals, including calves (Simões-Lopes et al. 1993, Van
Bressem et al. 2007, Moreno et al. 2008, Kiszka et al.
2009, Daura-Jorge & Simões-Lopes 2011).
Over the past 10 yr, we have observed new cases of
LLD in bottlenose dolphins from South America and
southern Africa, sometimes in areas where the dis-
ease had never been seen before although they had
been surveyed for several years. As earlier recom-
mendations urged close follow-up work on the dyna -
mics and spread of skin diseases worldwide (IWC
2009), here we report on these cases as well as on the
progression of the lesions in some individuals, and on
the geographic expansion of the disease in Brazil,
Ecuador and southern Africa.
MATERIALS AND METHODS
Study areas and surveys
Photo-identification (PI) surveys, most of these
dedicated and spanning multiple years, were carried
out in South Africa, Mayotte, Ecuador, Colombia and
Brazil between 2004 and 2015. Some surveys were
opportunistic and were implemented during whale-
watching activities, acoustic research or shark stud-
ies. Systematic beach combing to record and sample
stranded marine mammals was also carried out in
southern Brazil in 2004 to 2014. The areas studied
included bays, lagoons, estuaries and coastal waters
for which salinity, water quality and sea surface tem-
peratures (SST) varied widely (Table 2). We provide
mid-point coordinates for the marine parks, bays,
lagoons and estuaries and the northern and southern
limits for the areas covered during beach surveys.
Mayotte
Located in the northern Mozambique Channel,
Mayotte (12° 50’ S, 45° 10’ E) is almost entirely sur-
rounded by a 197 km long barrier reef. The inner
60
Van Bressem et al.: Lobomycosis-like disease in bottlenose dolphins
lagoon ranks as one of the largest in the world
(1100 km2, Quod et al. 2000) and is home to a resi-
dent population of Tursiops aduncus estimated at
82 ± 19 individuals (Kiszka et al. 2012, Pusineri et al.
2014). The human population has been growing
quickly in Mayotte during the last 30 yr, and urban-
ization as well as agriculture have been increasing
steadily together with the release of untreated fresh-
water run-off in the lagoon. Contamination by im -
munosuppressive polychlorinated biphenyls has in -
creased in hooded oysters Saccostrea cucullata in the
period 1997 to 2007 (Thomassin et al. 2008). From
July to October 2014, small-boat based surveys were
conducted in the lagoon with sea conditions not
exceeding Beaufort 3. Photographs were taken with
a digital 35 mm camera equipped with a 100−300 mm
lens (Kiszka et al. 2009, 2012). Data were collected
during 35 survey days, resulting in 29 encounters
with T. aduncus. A total of 250 photographs allowed
us to identify 16 new individuals and to recapture 19
dolphins identified during studies carried out from
2004 to 2009 (Kiszka et al. 2012, Pusineri et al. 2014).
South Africa
Located in the Western Cape Province, Plettenberg
Bay (34° 02’ S, 23° 22’ E) is separated from the Indian
Ocean by the Robberg Peninsula. It receives freshwa-
ters from the Keurbooms and Piesangs Rivers, consid-
ered of good quality with only some human-related
disturbance (Department of Water Affairs, South Africa:
www.dwa.gov.za/iwqs/ rhp/state_ of_ rivers .html). The
T. aduncus sub-population inhabiting Plettenberg
Bay was estimated to number be tween 1099 and 9492
individuals (95% CI, Phillips 2006). It is part of a
larger population of over 16 000 individuals that
ranges along the South African coastline (Reisinger &
Karczmarski 2010). Data were available for 203 days
in the period 2007 to 2010 from a variety of sources,
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
pers. comm). Some 165 images of 59 dolphins were of
sufficient quality to identify skin diseases on the body
areas visible when surfacing.
Ecuador
Posorja (02° 42’ S, 80° 15’ W), a small village in
Guayas Province at the Guayas River delta, is home
to a resident T. truncatus community estimated at
about 100 individuals, of which 85 have been photo-
identified (F. Félix unpublished data). Its fluviatile in-
fluenced coastal waters are contaminated by waste -
water from fish-processing industries, shrimp farms
and from Guayaquil, Ecuador’s largest city. In addi-
tion, run-off waters containing pesticides and other
agrochemicals used in banana and rice plantations in
the lower basin of the Guayas River are discharged
by several rivers into the inner estuary (CPPS 2014).
Thirty-three dedicated PI surveys on 8−10 m boats
were conducted in Posorja in 2005 to 2014 using digi-
tal cameras (6−18 megapixels) with 70−300 and
100−400 mm zooms. In total, 4270 images of regular
to good quality were analysed for this study.
Located in the south-eastern part of the inner
estuary of the Gulf of Guayaquil, Bajo Alto (03° 03’ S,
79° 53’ W) was surveyed on 14 April 2013. Among a
large group of T. truncatus, 42 individuals were iden-
tified. These dolphins belong to another community
separate from the one residing in the inner estuary
affected by LLD in 1990−1991 (Félix 1997, Van
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
traffic and a more extensive use of fishing nets.
Located at the northern edge of the Gulf of Guaya -
quil, Salinas (02° 20’ S, 81° 00’ W) in Santa Elena
Province features a major yacht marina, a large arti-
sanal fisheries port and a port for oil tankers, leading
to heavy maritime traffic. It is also the main tourist
site on the south-west coast of Ecuador. The adjacent
coast boasts a string of densely populated seaside
resorts and is affected by high levels of microbiologi-
cal and chemical pollution (Hurtado et al. 2012). A
small resident community of T. truncatus is frequently
ob served close to the port of Salinas. Opportunistic
surveys were carried out in 2006 to 2014 during
whale watching trips in the summer months (June to
October). A total of 502 images, from regular to good
quality, were available for skin disease assessment.
Colombia
Declared a National Natural Park in 2010, Bahía
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
community (Rengifo et al. 1995) where 2 cases of LLD
were observed in 2005 to 2006 (Van Bressem et al.
2007, Table 1). The bay is chemically contaminated
by illegal logging, by heavy metals from the mining
industry in the Dagua and San Juan Rivers and by oil
61
Dis Aquat Org 117: 59–75, 2015
62
Ocean province Location Sampling Spec. Nt Prev. Diagnosis Reference(s)
and species period (%)
East Pacific
T. truncatus Gulf of Guayaquil, EC 1990−1991 FR 441 1.6 LLD Van Bressem et al. (2007)
T. truncatus Golfo Dulce, CR 1991−1992 FR 56 12.5 LLD Bessesen et al. (2014)
T. truncatus Bahía Málaga & 2005−2006 FR 37 5.4 LLD Van Bressem et al. (2007)
surroundings, CO
T. truncatus Callao, PE 2006 FR Unkn. Unkn. LLD Van Bressem et al. (2007)
T. truncatus PNN Sanquianga & 2010−2011 FR Unkn. Unkn. LLD Herrera et al. (2013)
surroundings, CO
T. truncatus Golfo Dulce, CR 2010−2011 FR 38−68 7.35−10.5 LLD Bessesen et al. (2014)
West Pacific
T. aduncus Unkn., JP 2007 FR & CA Unkn. Unkn. Paracoccidioides sp. Ueda et al. (2013)
(H, MD)
T. aduncus Kagoshima, JP 2013 S Unkn. Unkn. No fungi detected Tajima et al. (2015)
West Atlantic
T. truncatus Oak Hill, FL, US 1955 FR Unkn. Unkn. LLD Caldwell et al. (1975)
T. truncatus Cedar Keys, FL, US 1968 FR Unkn. Unkn. LLD Caldwell et al. (1975)
T. truncatus Upper Keys, FL, US 1969 FR Unkn. Unkn. LLD Caldwell et al. (1975)
T. truncatus St Augustine, FL, US 1970 FR 50−60 Unkn. LLD Caldwell et al. (1975)
T. truncatus Vero Beach, FL, US 1970 C Unkn. Unkn. Lobomycosis (H, EM) Caldwell et al. (1975)
T. truncatus Ft. Pierce, FL, US 1970 FR 25 Unkn. LLD Caldwell et al. (1975)
T. truncatus Sarasota, FL, US 1970 C Unkn. Unkn. Lobomycosis (H) Migaki et al. (1971)
S. guianensis Surinam River Estuary, SR 1971 BC Unkn. Unkn. Lobomycosis (H) de Vries & Laarman (1973)
T. truncatus Fort Lauderdale, FL, US early 1980s BC Unkn. Unkn. Lobomycosis (H) Bossart (1984)
T. truncatus Sarasota Bay, FL, US 1980−1989 FR 106 4.7 Lobomycosis (H) & LLD Burdett Hart et al. (2011)
T. truncatus Laguna Lagoon, BR 1990 S Unkn. Unkn. Lobomycosis (H) Simões-Lopes et al. (1993)
T. truncatus Sarasota Bay, FL, US 1990−1999 FR 117 1.7 Lobomycosis (H) Burdett Hart et al. (2011)
T. truncatus Gulf of Mexico, TX, US 1992 FR Unkn. Unkn. Lobomycosis (H) Cowan (1993)
T. truncatus Santa Catarina, Baía Norte, BR 1993−2004 FR 39 5.1 LLD Van Bressem et al. (2007)
T. truncatus Tramandaí Estuary, BR 1999−2005 FR 10 20.0 Lobomycosis (H) & LLD Van Bressem et al. (2007),
Moreno et al. (2008)
T. truncatus Indian River Lagoon, FL, US 2000−2006 FR 704 6.8 Lobomycosis (H) Murdoch et al. (2008)
T. truncatus Unkn., CU 2002 CA Unkn. Unkn. Paracoccidioides sp. Esperón et al. (2012)
(H, MD)
T. truncatus Atlantic coast of Florida, US 2002−2008 FR 284 2.1 LLD Murdoch et al. (2010)
T. truncatus Charlotte Harbor, FL, US 2003 FR 591 1.9 LLD Burdett Hart et al. (2011)
Table 1. Lobomycosis and lobomycosis-like disease (LLD) in common bottlenose dolphin Tursiops truncatus, Indo-Pacific bottlenose dolphin T. aduncus, Guiana dolphin So-
talia guianensis, Indian Ocean humpback dolphin Sousa plumbea and Australian snubfin dolphin Orcaella heinsohni worldwide. Spec.: specimens; FR: free-ranging; Nt: to-
tal number of dolphins; Prev.: prevalence; PNN: Parque Nacional Natural (National Natural Park); CA: captive; BC: by-catch; C: caught at sea; S: stranded; Unkn.: unknown;
H: histology; EM: electron microscopy; MD: molecular diagnosis; country abbreviations follow ISO Code 2 (www.nationsonline.org/ oneworld/ country _code _list.htm)
Van Bressem et al.: Lobomycosis-like disease in bottlenose dolphins
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 km2along 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,
channels, open lagoons and intertidal sand plains,
mostly covered by dense mangrove forest (Díaz &
Acero 2003). The coastal waters adjacent to the park
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
(Table 1; Herrera et al. 2013). The rivers, especially
the Patía, are biologically and chemically contami-
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.
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,
53° 22’ W to 31° 21’ S, 51° 01’ W) in 2004 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
the Atlantic Ocean through a single 700 m wide arti-
63
Ocean province Location Sampling Spec. Nt Prev. Diagnosis Reference(s)
and species period (%)
T. truncatus Mampituba River, BR 2003−2004 FR Unkn. Unkn. LLD Van Bressem et al. (2007),
Moreno et al. (2008)
T. truncatus Indian River Lagoon, FL, US 2003−2004 FR 30 30.0 Lobomycosis (H) Reif et al. (2006)
T. truncatus Isla Margarita, VE 2004 S Unkn. Unkn. LLD Bermúdez et al. (2009)
T. truncatus Sarasota Bay, FL, US 2004 FR 156 5.8 Lobomycosis (H), LLD Burdett Hart et al. (2011)
T. truncatus North Carolina, US 2005 & 2008 S Unkn. Unkn. Paracoccidioides sp. Rotstein et al. (2009)
(H, MD)
S. guianensis Paranaguá Estuary, BR 2006−2007 FR 103 3.9 LLD Van Bressem et al. (2009a)
T. truncatus Laguna Lagoon, BR 2007−2009 FR 57 8.8 LLD Daura-Jorge & Simões-Lopes (2011)
T. truncatus Santa Catarina, Baía Sul, BR 2009 FR Unkn. Unkn. LLD Daura-Jorge & Simões-Lopes (2011)
East Atlantic
T. truncatus Bay of Biscay early 1970s BC Unkn. Unkn. Lobomycosis (H, EM) Symmers (1983)
Indian Ocean
T. aduncus Mayotte Lagoon, YT 2004−2008 FR 71 8.5 LLD Kiszka et al. (2009)
O. heinsohni Darwin Harbour, AU 2008−2010 FR Unkn. Unkn. LLD Palmer & Peterson (2014)
S. plumbea KwaZulu-Natal, ZA 2010−2012 BC 5 20 Lobomycosis (H) Lane et al. (2014)
Table 1 (continued)
Dis Aquat Org 117: 59–75, 2015
64
Ocean province Location Geographic Eco- Res. Spec. Sampling Nt N Prev. SST Salinity
and species coordinates type pattern period pos (%) (°C)
East Pacific
T. truncatus Posorja, EC 02° 42’ S, 80° 15’ W IN R FR 2005−2014 85 2 2.35 21.5−28 24−30
T. truncatus Bajo Alto, EC 03° 03’ S, 79° 53’ W IN R FR Apr 2013 42 0 0 21.5−28 24−30
T. truncatus Salinas, EC 02° 20’ S, 81° 00’ W IN R FR 2006−2014 18 3 16.7 22.8−27.4 33−35.1
T. truncatus Sanquianga coast, CO 02° 38’ N, 78° 15’ W IN R FR Jul 2013 Unkn 3 Unkn 25.5 33.5
T. truncatus Bahía Malaga, CO 03° 53’ N, 77° 22’ W IN R FR Aug−Sep 2008 Unkn 1 Unkn 25 30
West Atlantic
T. truncatus Patos Lagoon estuary 32° 06’ S, 52° 05’ W IN R FR 2005−2015 152 0 0 12−15 (winter) 0−35
(PLE), BR 23−26 (summer)
T. truncatus Coastal waters adjacent 32° 48’ S, 52° 28’ W IN R & NR FR 2005−2015 121 0 0 9 (winter) 27.7
to PLE, BR 27 (summer)
T. truncatus Shoreline adjacent 33° 44’ S, 53° 22’ W to IN & OFF R & NR S 2004−2014 130 1 0.77 9 (winter) 27.7
to PLE, BR 31° 21’ S, 51° 01’ W 27 (summer)
T. truncatus Tramandaí Estuary, BR 29° 57’ S, 50° 07’ W IN R FR 2009−2010 9 0 0 12 (winter) 1.8−37.2
29 (summer)
T. truncatus Mampituba River & adjacent 29° 19’ S, 49° 42’ W IN R & NR FR 2009−2013 28 0 0 14 (winter) 0−37
coastal waters, BR 26.5 (summer)
T. truncatus Shoreline adjacent to Lagoa 31° 21’ S, 51° 02’ W to IN & OFF R & NR S 2008−2014 16 0 0 12 (winter) 20−37
do Peixe, Tramandaí & 29° 19’ S, 49° 42’ W 29 (summer)
Mampituba, BR
T. truncatus Laguna, BR 28° 30’ S, 48° 50’ W IN R FR 2013−2014 42 6 14.3 20 3.5−18
T. truncatus Shoreline adjacent to 28° 14’ S, 48° 39’ W & IN & OFF R & NR S 2012 9 0 0 14.4 (winter) 30.5−35.7
Laguna, BR 29° 19’ S, 49° 43’ W 24.4 (winter)
T. truncatus Baía Norte, BR 27° 30’ S, 48° 32’ W IN Unk. S Oct 2014 Unkn 1 Unkn 15 (winter) 25
29 (summer)
T. truncatus Sepetiba Bay, BR 22° 55’ S, 43° 53’ W IN NR FR 2005−2014 1 1 Unkn 22.6 29
Indian Ocean
T. aduncus Plettenberg Bay, ZA 34° 02’ S, 23° 22’ E IN NR FR 2007−2010 [59]a1 Unkn 17.1 35.3
T. aduncus Mayotte, YT 12° 50’ S, 45° 10’ E IN R FR Jul−Oct 2014 35 2 5.7 28.6 35
aOnly dolphins with skin lesions
Table 2. New cases of lobomycosis-like disease in common Tursiops truncatus and Indo-Pacific T. aduncus bottlenose dolphins from South America and southern Africa
in 2004 to 2015. Res: Residence; Spec.: specimens; FR: free-ranging; S: stranded; Nt: total number examined; Npos: number of positives; Prev.: prevalence; SST: sea sur-
face temperature; IN: inshore; OFF: offshore; R: resident; NR: non-resident
Van Bressem et al.: Lobomycosis-like disease in bottlenose dolphins
ficial inlet (Kjervfe 1986). The PLE and adjacent
areas are characterized by a high anthropogenic
influence, including boat traffic, fishing and contam-
ination with polycyclic aromatic hydrocarbons (Gar-
cia et al. 2010) and mercury (Mirlean et al. 2003). The
PLE hydrodynamics are mainly driven by wind and
freshwater input that result in flood regimes in the
channel area and play a key role in the control of
salinity (Pinotti et al. 2011).
Located in the north of Rio Grande do Sul, the Tra-
mandaí Lagoon (29° 57’ S, 50° 07’ W) covers an area
of about 13 km2with an average depth of 1.5 m
(Schwarzbold & Schäfer 1984). It receives fresh water
from the Rio Tramandaí and the Camarão Channel
and is connected to the Atlantic Ocean by a narrow
inlet bordering the municipalities of Imbé and Tra-
mandaí where a small community of T. truncatus
resides (Simões-Lopes & Fabian 1999, Zappes et al.
2011, Di Giacomo & Ott in press). LLD was detected
in 2 adults in the period 1999 to 2005 (Moreno et al.
2008). The estuary is contaminated with a high load
of faecal coliforms (Haase et al. 2003, FEPAM 2015),
hydrocarbons and heavy metals (Andrade et al. 2004,
Rocha 2013). During the present study, PI surveys
were carried out in the mouth of the Tramandaí estu-
ary in January 2009 to February 2010. About 2050
photographs were analysed, and 9 dolphins were
identified, including 3 calves (Di Giacomo & Ott in
press).
The Mampituba River drains a 1200 km2watershed
area, has a mean depth of around 4 m and is under a
microtidal regime (D’Aquino et al. 2011). The river
mouth (29° 19’ S, 49° 42’ W) straddles the border be -
tween the states of Rio Grande do Sul and Santa
Catarina. Its narrow inlet has been stabilized by jet-
ties to support a fishing harbour since 1970 (Lélis &
Calliari 2006). Along its course, the river receives
domestic sewage, agricultural drainage and munici-
pal wastewaters (Andrade et al. 2004). In 1995 to
2008, 6 common bottlenose dolphins had been photo-
identified in the river mouth, including 1 with LLD
(Moreno et al. 2008). New PI surveys were carried
out from April 2009 to April 2013 in the river mouth
and adjacent coastal waters, covering 20 km of the
coast. In total, 1480 images were examined and 22
adults were photo-identified. Most of the dolphins
were seen in the coastal area outside the estuary, and
only 2 entered the channel (Di Giacomo 2014,
GEMARS unpublished data), possibly because water
quality had deteriorated (Haase et al. 2003, FEPAM
2015). Systematic coastal beach surveys were con-
ducted in 2008 to 2014 to record stranding events
along a 260 km shoreline, ca. 80 km between the
estuaries of Mampituba and Tramandaí and a 180 km
area that extended southward to the Lagoa do Peixe
National Park (31° 21’ S, 51°02’ W).
Covering about 300 km2(28° 30’ S, 48° 50’ W), La -
guna is among the largest lagoon systems in southern
Brazil consisting of 3 smaller lagoons (Mirim, Imaruí
and Santo Antônio). Bordering the city of Laguna, the
lagoon is polluted by effluents from anthropogenic ac-
tivities including rice agriculture, shrimp farming and
coal mining (Daura-Jorge & Si mões-Lopes 2011). A
community of 52 to 57 resident common bottlenose
dolphins, studied since 1989, inhabits the Santo An-
tônio and Imaruí Lagoons (Simões-Lopes & Fabian
1999, Daura-Jorge et al. 2013). It is endemically af-
fected by LLD, with a pre valence of 9% for 57 dol-
phins in 2007 to 2009 (Daura-Jorge & Simões-Lopes
2011). During 2013 and 2014, boat surveys were con-
ducted weekly along pre-defined routes to collect
photo-identification data (Daura-Jorge et al. 2013).
About 12 000 photographs were taken during 76 sur-
veys and 42 resident dolphins were identified. In
2012, a coastal beach survey recorded stranding
events along 150 km of shoreline adjacent to Laguna
(28° 14’S, 48° 39’W and 29° 19’S, 49° 43’W).
Baía Norte (27° 30’ S, 48° 32’ W) and Baía Sul
(27° 43’ S, 48° 36’ W) are 2 coastal bays that separate
Santa Catarina Island from the mainland. Covering
ca. 250 km2, Baía Norte is greatly influenced by open
waters. Contiguous to a densely populated area
without adequate sanitation, the bay is exposed to
high levels of chemical and biological contaminants
(Souza et al. 2012). Non-systematic PI surveys in
2008 to 2011 suggest that a small inshore community
of at least 11 T. truncatus shows some degree of site
fidelity to Baía Norte and/or Baía Sul (F. Daura-Jorge
& P. Simões-Lopes unpubl. data). LLD was re por ted
in 2 T. truncatus from Baía Norte between 1993 and
2004 (Flores et al. 2005, Van Bressem et al. 2007) and
in 2 dolphins from Baía Sul in 2009 (Daura-Jorge &
Simões-Lopes 2011).
Located in southern Rio de Janeiro State (22° 55’ S,
43° 53’ W), Sepetiba Bay covers approximately 526 km2
and is connected to the Atlantic Ocean through the
western part of the bay. The eastern side features an
extensive mangrove forest and receives a high input
of fresh water from river drainage systems (Pessanha
& Araújo 2003, Flach et al. 2008). It is home to 4 large
ports and suffers from increasing organic and chemi-
cal contamination with more than 400 chemical, rub-
ber, printing and metal factories in the surrounding
area (Copeland et al. 2003, Molisani et al. 2004,
Ribeiro et al. 2013). A resident community of Sotalia
guianensis estimated at 1269 dolphins (95% CI =
65
Dis Aquat Org 117: 59–75, 2015
739−2196) inhabits the entrance of the bay and has
been the object of PI studies since 2005 (Flach et al.
2008). From 2005 to 2014, a total of 334 surveys were
conducted along pre-defined routes to collect S. guia-
nensis PI data (Flach 2015). T. truncatus were never
seen in the bay until September 2013 (Flach 2015).
Data collection and analysis
The large majority of the bottlenose dolphins exa -
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
of the offshore ecotype (Costa et al. 2015, Ott et al. in
press). Inshore dolphins were further classified as
resi dents (high sighting frequencies within and
between years, high site fidelity) or non-residents
(transients and semi-residents; Table 2). Individual
dol phins were identified through natural marks
(Würsig & Jefferson 1990). Maturity status (calf, juve-
nile, adult) was estimated from relative body size and
colouration, scars, behavioural clues and from the
verified duration of residence (Félix 1994, Di Gia-
como & Ott in press). Calves were defined as individ-
uals whose body length was one-third or less than
that of the larger dolphins in the area and which usu-
ally remained close to the same adult (Mann & Smuts
1999, Mann et al. 2000, Fruet et al. 2015a,b).
Holders of PI catalogues of T. truncatus and
T. aduncus searched for the presence of skin lesions
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
(Van Bressem et al. 2007, 2009a, Kiszka et al. 2009,
Daura-Jorge & Simões-Lopes 2011). Images of sus-
pected positive dolphins were extracted and further
examined by M.F.V.B. and K.V.W. The relative size
of the lesions was expressed as a percentage (P) =
Alesion/Adorsal × 100, where Alesion is the area of the le-
sion and Adorsal is the 1-sided area of the dorsal fin
(DFA; Daura-Jorge & Simões-Lopes 2011). Relative
size of lesions (% of DFA) was estimated from images
magnified on-screen and assigned to 1 of 4 cate go -
ries: small (<10%), medium (10−20%), large (20−
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-
lated as the ratio of affected individuals to the
number of PI dolphins in a community or to the total
number of stranded dolphins examined during the
study period. In free-ranging dolphins, prevalence
levels were minimal as, generally, only the upper
body exposed at surfacing could be examined. We
only compared communities where dolphins were
photo-identified and where LLD was present, which
limited our analysis to 4 resident communities
(Posorja, Salinas, Laguna and Mayotte). Prevalence
variation between study areas was assessed with a
Kruskal-Wallis test. Temporal variation in prevalence
in Laguna between 2007−2009 and 2014 was exam-
ined with McNemar’s test using exact binomial prob-
ability calculations (www.vassarstats.net/ propcorr.
html). All significance levels were set at α = 0.05.
RESULTS
The presence of LLD was examined in 658 Tursiops
truncatus from South America and 94 T. aduncus from
southern Africa (Table 2). Photographs and stranding
records of 387 inshore residents, 60 inshore non-
residents and 305 specimens of undetermined origin
(resident or non-resident inshore or offshore dol-
phins) were examined for the presence of LLD lesions
(Table 2). LLD cases were detected in 17 residents (2,
Mayotte; 5, Ecuador; 4, Colombia; 6, Bra zil), in 3 non-
residents (1, South Africa; 2, Brazil) and in 1 inshore T.
truncatus of unknown residence status in Brazil
(Fig. 1). The disease had persisted in minimum 3, and
perhaps 4, of these dolphins since previous studies
(Van Bressem et al. 2007, Kiszka et al. 2009, Daura-
Jorge & Simões-Lopes 2011). Thus, the number of true
new cases amounts to 17 or 18 bottlenose dolphins.
Mayotte
From July to October 2014, small-boat surveys
allowed us to photographically recapture 19 known
individuals and to identify an additional 16 T. adun-
cus. While negative from 2005 to 2008, an adult had
developed small and medium LLD lesions on its dor-
sum and tailstock by October 2014 (Fig. 2A,B). In
individual MY08, chronic LLD lesions on the dorsum
and tailstock had clearly progressed, covering 1% of
the visible body surface in 2006 (Kiszka et al. 2009) to
approximately 20% in 2014.
South Africa
One case of LLD was observed in a T. aduncus in
Plettenberg Bay (Fig. 2C) on 11 November 2008. The
dolphin had several small to medium-sized nodules,
some confluent and ulcerated, on the dorsum, right
66
Van Bressem et al.: Lobomycosis-like disease in bottlenose dolphins
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.
Twenty-one T. truncatus groups (4–8 ind. per group)
were observed in Salinas between 2006 and 2014. Of
the 18 PI dolphins, 3 (16.7%) showed small to large
LLD lesions on the DF, dorsum, flanks and tailstock
during that period. In dolphin S4, a whitish lesion
located at the base of the dorsal fin (right side) in -
creased markedly from 8.5% DFA in September 2006
to 28.5% DFA in April 2010 (Figs. 3C−E & 4). A lesion
located on the left side of the dorsal fin progressed
from 25% DFA in 2006 to 50% DFA in 2009 (Fig. 4).
It did not visibly grow in 2010 to 2011 (Fig. 4).
Colombia
An adult T. truncatus with LLD lesions was sighted
in Bahía Málaga on 9 August 2008 (Table 2). The dol-
phin was part of a group of 9 individuals. However,
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
Fig. 2. Lobomycosis-like disease (LLD) in Indo-Pacific bot-
tlenose dolphins Tursiops aduncus from the Indian Ocean.
(A) Absence of LLD in a dolphin from Mayotte in 2005; (B)
small and medium-sized LLD lesions on the dorsum of the
same dolphin in October 2014; (C) several small to medium-
sized LLD lesions on the back and right flank of a T. aduncus
from Plettenberg Bay, South Africa, in November 2008
Dis Aquat Org 117: 59–75, 2015
as it was not photo-identified, it is unknown whether
it corresponded to 1 of the 2 affected individuals
reported in 2005 and 2006 (Van Bressem et al. 2007)
or whether it represented a new case.
Small to medium LLD lesions were seen in 2
T. trun catus 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 (Eco Mega 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
origin found washed ashore during beach surveys
along the seashores adjacent to the PLE in 2004 to
2014, 1 dolphin (0.77%) had LLD (Table 2). The 26 yr
old male stranded dead at Cassino Beach (32° 48’ S,
52° 28’ W), 80 km south of the PLE on 18 January
2009, had numerous, small to very large, light grey,
verrucous LLD lesions that affected approximately
30% of its body surface (Fig. 5A). Supported by PI
data, its mtDNA control region haplotype matched
the most common haplotype found in the Southwest-
ern Atlantic inshore ecotype (Fruet et al. 2014). The
dolphin did not belong to the communities residing in
the PLE and adjacent coastal waters and was likely a
transient.
LLD was not observed in any of the T. truncatus
(6 adults and 3 calves) that were repeatedly photo -
graphed in the Tramandaí estuary from January 2009
to February 2010. Of the 6 adults, 4 (I6, I7, I9, I11)
were known since 1992, 1 (I14) since 2004, and 1
(I15) was first sighted in 2009. Therefore, all adults
but 1 had occupied the estuary during a period when
LLD occurred there (1999−2005).
During surveys carried out from April 2009 to April
2013, LLD was not detected in T. truncatus (22 adults
and 6 calves) photographed in the Mampituba River
mouth and adjacent inshore waters. Of the 22 adults,
only 1 was known to have used the estuary in 2004 at
a time when LLD occurred there (2003−2004). None
of the 16 T. truncatus stranded along the coastline
68
Fig. 3. Lobomycosis-like disease (LLD) in common bottle-
nose dolphins Tursiops truncatus from the Southeast Pacific.
Progression of LLD in dolphin P58 in (A) April 2011 and (B)
February 2013 from Posorja, Ecuador; and in individual S4
from the Salinas community (Ecuador) in (C) 2006, (D) 2008
and (E) 2010. (F) LLD lesions on the dorsum and flank of a
dolphin nearshore in Sanquianga National Park, Colombia,
3 July 2013
2005
Lesion progression (% cover)
2006 2007 2008 2009 2010 2011 2012 2013 2014
0
10
20
30
40
50
60
Fig. 4. Progression of some lobomycosis-like disease lesions
in bottlenose dolphins Tursiops truncatus S4 (blue = left side
of dorsal fin, red = right side of dorsal fin) and P58 (yellow)
from Ecuador
Van Bressem et al.: Lobomycosis-like disease in bottlenose dolphins
between Mampituba estuary and the Lagoa do Peixe
National Park in 2008 to 2014 had LLD (GEMARS
unpubl. data).
Santa Catarina State
Two of the 4 adult T. truncatus (L07, L20) of Laguna
confir med with LLD in 2007 to 2009 were still
affected in 2013 to 2014. The other 2 positive individ-
uals (L17, L19) had disappeared (Daura-Jorge &
Simões-Lopes 2011, unpubl. data). Four other adult
dolphins (L04, L34, L38, NI) had developed the dis-
ease. On 15 January 2014, L34, which had been pho-
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
seen again on 18 April 2014 with no notable changes
in LLD lesion size and corporal distribution. On both
occasions, it presented an unusual behaviour, namely
continuously leaping out of the water and landing on
its right side, during the entire observation period
(40 min). Conceivably pruritus may be a symptom of
LLD, commonly seen in cutaneous mycoses (Fran -
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
lesions. LLD prevalence in adults was 14.3% (N = 42)
in 2013 to 2014. In 36 adults examined during both
periods, the prevalence of LLD was higher in 2013 to
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.).
Rio de Janeiro State
On 9 September 2013, an adult-sized T. truncatus
was photographed with extensive, nodular, ulcerated
LLD lesions on its posterior flanks and tailstock
(Fig. 5D) in a mangrove area at the centre of Sepetiba
Bay. Several nodules were associated with tooth -
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
disappeared. At no point was it seen close to Sotalia
guianensis groups. It was thought not to belong to
the inshore T. truncatus community inhabiting wa -
ters around Rio de Janeiro (Lodi et al. 2014) but may
represent a transient inshore individual. Although
the resident community of S. guianensis is affected
by various skin diseases (Van Bressem et al. 2007,
2015), LLD lesions have never been seen in these
dolphins (L. Flach pers. obs.).
Variation in LLD prevalence among study areas
Among the inshore/estuarine dolphins, prevalence
varied significantly (Kruskal-Wallis test, χ2 = 8.65,
df = 3, p = 0.0343) among 4 communities with the
highest prevalence level observed in Salinas (mean ±
SD: 0.17 ± 0.38), followed by Laguna (0.14 ± 0.35),
Mayotte (0.06 ± 0.24) and Posorja (0.02 ± 0.15; Fig. 6)
DISCUSSION
This paper provides an update on the epidemiol-
ogy and geographical distribution of LLD in bottle-
69
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-
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
9 September 2013
Dis Aquat Org 117: 59–75, 2015
nose dolphins from South America and southern
Africa in 2004 to 2015. Beach combing and examina-
tion of photographs taken during dedicated and
opportunistic PI surveys resulted in the identification
of 21 cases of LLD in Mayotte, South Africa, Brazil,
Ecuador and Colombia (Fig. 1). Macroscopic charac-
teristics of LLD varied between individuals, possibly
reflecting disease progression and individual immuno-
logic response, ranging from small to very large,
whitish to dark grey, isolated or confluent nodules to
plaque-like verrucous lesions that were often ulcer-
ated (Figs. 2, 3 & 5). This agrees with observations in
other Delphinidae populations around the world
(Rotstein et al. 2009, Van Bressem et al. 2009a,b,
Murdoch et al. 2010, Esperón et al. 2012). However, it
is possible that different aetiological agents cause
skin diseases resembling lobomycosis in dolphins
(Tajima et al. 2015), and further research is neces-
sary. In the Southern Hemisphere, only 3 histological
studies have demonstrated the presence of a fungus
resembling Lacazia loboi in skin lesions sampled in 2
Tursiops truncatus from Laguna (Simões-Lopes et al.
1993) and the Tramandaí Estuary (Moreno et al.
2008) and a third in a Sousa plumbea from South
Africa (Lane et al. 2014). Molecular analysis of the
pathogenic agents causing LLD in dolphins from
South America and southern Africa will be necessary
to firmly establish their taxonomic identity, specifi-
cally their relationship to known species of the genus
Paracoccidioides and its sister taxon L. loboi.
LLD progression could be assessed in 3 dolphins
that were repeatedly sighted in Salinas, Posorja and
Mayotte (Figs. 3 & 4). Although only limited data
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
also because new individuals became infected. How-
ever, our data also show that LLD may vanish from
very small T. truncatus communities after the death
or disappearance of affected individuals and absence
of new infections. Five of 6 adults from the Traman-
daí Estuary and 1 from Mampituba River did not con-
tract LLD although they were photo-identified in
1999 to 2005 when the disease occurred in these
communities (Van Bressem et al. 2007, Moreno et al.
2008). LLD persistence has been observed in T. trun-
catus in the Indian River Lagoon and Sarasota Bay,
Florida, and in Golfo Dulce, Costa Rica (Murdoch et al.
2008, Burdett Hart et al. 2011, Bessesen et al. 2014).
Of the 21 LLD-infected bottlenose dolphins, 17
were inshore residents inhabiting spatially re stricted
areas that were biologically and chemically contami-
nated (see ‘Materials and methods’) and were con-
stantly exposed to multiple anthropogenic stressors,
including fisheries. Such factors may depress the
immune system and affect skin integrity (Fair &
Becker 2000, Romano et al. 2004, Reif et al. 2009,
Martin et al. 2010). Immune compromise was sug-
gested to increase lobomycosis infection risk in T.
truncatus in the Indian River Lagoon (Reif et al. 2009,
Murdoch et al. 2010). A similar situation may occur in
resident bottlenose dolphins from South America and
Mayotte. Further studies are needed to investigate
this hypothesis.
Prevalence varied significantly between resident
dolphin communities, being low in Posorja (2.35%)
and high in Laguna (14.3%) and Salinas (16.7%,
Fig. 6). Similarly, LLD prevalence levels in other dol-
phin communities worldwide varied widely (Table 1).
Although differences in sample size and methodo -
logy may explain some of this variation, environmen-
tal and individual factors likely also play an impor-
70
Fig. 6. Variation in lobomycosis-like disease (LLD) preva-
lence between bottlenose dolphins from South America and
southern Africa
Van Bressem et al.: Lobomycosis-like disease in bottlenose dolphins
tant role. Burdett Hart et al. (2011) suggested that
differences in freshwater input could influence the
development and persistence of lobomycosis be -
tween T. truncatus communities of west and east
coast estuaries in Florida. Although several of the
areas studied here (Laguna, the mangrove area of
Sepetiba Bay, Posorja, Sanquianga National Park
and Bahía Malaga) received important riverine
freshwater input, this was not the case for Salinas
where the highest LLD prevalence was observed.
Wilson et al. (1999) reported that bottlenose dolphin
communities from areas of low water temperature
and low salinity exhibited higher lesion prevalence.
In the present study, high LLD prevalence levels
were found in areas of medium (Laguna) and high
(Mayotte and Salinas) salinity, and both in warm
(28.5°C, Mayotte) and temperate waters (20°C, La -
guna; Table 2). Thus, the role of these factors in the
ecology of the disease remains unclear. Low genetic
variability could contribute to high LLD prevalence
levels in some small communities by altering the im -
mune response (Frank 2002, Sommer 2005). Re cent
studies showed that among south-western Atlantic T.
truncatus, the lowest genetic variability was found in
the Laguna community where inbreeding is likely to
occur, and in a chronically LLD-infected dolphin from
the Tramandaí Estuary that died in 2005 (Moreno et
al. 2008, Fruet et al. 2014, Costa et al. 2015). In
humans, there is mounting evidence that a genetic
component may predispose individuals to superficial
fungal infections through alterations of the innate
and adaptive immune system (Gupta et al. 2014).
LLD seems to have expanded geographically in at
least 3 countries where PI surveys and/or beach
combing were regularly carried out. In Brazil, LLD
was previously determined to be distributed between
the Paranaguá Estuary (25° 22’ S, 48° 25’ W) and the
Tramandaí Estuary in Sotalia guianensis and T. trun-
catus (Simões-Lopes et al. 1993, Van Bressem et al.
2007, 2009a, Moreno et al. 2008, Siciliano et al. 2008,
Daura-Jorge & Simões-Lopes 2011). New LLD re -
cords in T. truncatus from Sepetiba Bay and Cassino
Beach, areas that have been extensively surveyed
since the late 1970s (Cassino) and 2005 (Sepetiba),
expand the known distribution of the disease 520 km
to the north (22° 55’ S, 43° 53’ W) and ca. 390 km to
the south (32° 48’ S, 52° 28’ W). The Sepetiba and
Cassino individuals were transient inshore dolphins,
suggesting that these communities may play a role
in the geographic expansion of LLD. Interestingly,
in South America, the first T. truncatus reported
with lobomycosis in 1990 was a transient specimen
(Si mões-Lopes et al. 1993, Simões-Lopes & Fabian
1999). In Ecuador, LLD was recently (2011−2013)
observed in 2 T. truncatus from a community in
Posorja of around 100 individuals that was regularly
monitored since 2005. LLD was initially described
from the inner estuary of the Gulf of Guayaquil
(02° 52’ S, 80° 01’ W) with a prevalence of 1.6% for
441 dolphins in 1990 to 1991 (Van Bressem et al.
2007). The Posorja record expands the known geo-
graphical range of the disease to include the outer
estuary, some 40 km to the west. In South Africa,
although images of regular quality were available
since 2006 and opportunistic surveys were carried
out since 1999, LLD was detected only in 1 T. adun-
cus in November 2008. A case of lobomycosis was
documented in 1 of 5 S. plumbea by-caught along the
coast of KwaZulu-Natal (about 1000 km east of Plet-
tenberg Bay) in 2010 to 2011 but not in 35 T. aduncus
accidentally captured in the same region during the
same period (Lane et al. 2014).
In Laguna, LLD prevalence in 36 adult dolphins
more than doubled (albeit without statistical signifi-
cance) between 2007 and 2009 (5.6%) and 2014
(13.9%). This apparent increase may either reflect
natural fluctuations, or may indicate that the disease
is spreading in this small, declining community, rais-
ing concern for its long-term survival. Although
bottle nose dolphins may live with LLD for years,
severely affected individuals have died or disap-
peared in the Americas and southern Africa, includ-
ing 2 adult Laguna residents sighted in 2007 to 2009
but not in 2014 (Moreno et al. 2008, Bermúdez et al.
2009, Kiszka et al. 2009, Daura-Jorge & Simões-
Lopes 2011). Among the 21 dolphins observed with
LLD during this study, 2 were found dead with exten-
sive skin lesions in Brazil and 2 others disappeared
and presumably died in Ecuador, a presumed 19%
mortality rate. The persistence, high prevalence lev-
els and unknown case fatality rates of LLD in some
small, and sometimes endangered, communities of T.
truncatus and T. aduncus are a cause for concern.
These data stress the need for intensified, targeted
epidemiological, histological and molecular studies
of this disease in Delphinidae in the Southern Hemi-
sphere.
Acknowledgements. We thank 3 anonymous reviewers for
their constructive comments on the manuscript. We thank
Lina Correa for help with data collection in Bahía Málaga
and surroundings; and Johana Velasquez, Colombo Estu -
piñán, Paula Casas and Saturnino Montaño for their sup-
port. Rodrigo Genoves and Rafael Camargo are kindly
acknowledged for collecting the T. truncatus stranded south
of the Patos Lagoon Estuary. We thank researchers from
GEMARS and the support from CECLIMAR/UFRGS for col-
lecting the stranded common bottlenose dolphin from the
71
Dis Aquat Org 117: 59–75, 2015
northern coast of Rio Grande do Sul and Silvina Botta for age
determination of the dolphin from Cassino Beach, Brazil. We
thank J. Brack and R. Amboni for providing Figs. 2B and 5B,
respectively. A fellowship and financial support was granted
by the Conselho Nacional de Desenvolvimento Científico e
Tecnológico (CNPq) to E.R.S. (PQ 307846/2014-8) and P.H.O.
(Process 572180/2008-0), who contributed as members of
the Research Group ‘Ecologia e Conservação da Megafauna
Marinha − EcoMega/CNPq’ and ‘Ecologia e Conservação de
Organismos e Ambientes Aquáticos − ECOAqua/ CNPq’.
L.F. was sponsored by Petrobras through Petrobras Socio
Ambiental. We thank T. Gridley, V. Cockcroft and M. N.
Bester for assistance with the South African data access and
analysis, as well as the Centre for Dolphin Studies and Orca
Foundation. Data collection around Mayotte was supported
by ‘Collectivité Départementale de Mayotte, Ministère de
l’Environment, Agence des Aires Marines Protégées’ and
the ‘Fond National de la Recherche du Luxembourg’.
LITERATURE CITED
Andrade VM, Silva J, Silva FR, Heuser VD, Dias JF, Yoneama
ML, Freitas TRO (2004) Fish as bioindicators to assess the
effects of pollution in two southern Brazilian rivers using
the comet assay and micronucleus test. Environ Mol
Mutagen 44: 459−468
Bagagli E, Franco M, Bosco SDM, Hebeler-Barbosa F, Trinca
LA, Montenegro MR (2003) High frequency of Paracoc-
cidioides brasiliensis infection in armadillo (Dasypus no -
vemcinctus): an ecological study. Med Mycol 41: 217−223
Bermúdez L, Van Bressem MF, Reyes-Jaimes O, Sayegh AJ,
Paniz-Mondolfi AE (2009) Lobomycosis in man and
lobomycosis-like disease in bottlenose dolphin, Vene -
zuela. Emerg Infect Dis 15: 1301−1303
Bessesen BL, Oviedo L, Burdett Hart L, Herra-Miranda D
and others (2014) Lacaziosis-like disease among bottle-
nose dolphins Tursiops truncatus photographed in Golfo
Dulce, Costa Rica. Dis Aquat Org 107: 173−180
Bocca AL, Amaral AC, Teixeira MM, Sato PK, Shikanai-
Yasuda MA, Soares Felipe MS (2013) Paracoccidioido -
mycosis: eco-epidemiology, taxonomy and clinical and
therapeutic issues. Future Microbiol 8: 1177−1191
Bossart GD (1984) Suspected acquired immunodeficiency
in an Atlantic bottlenosed dolphin with chronic-active
hepatitis and lobomycosis. J Am Vet Med Assoc 185:
1413−1414
Burdett Hart L, Wells RS, Adams JD, Rotstein DS, Schwacke
LH (2010) Modeling lacaziosis lesion progression in com-
mon bottlenose dolphins Tursiops truncatus using long-
term photographic records. Dis Aquat Org 90: 105−112
Burdett Hart L, Rotstein DS, Wells RS, Bassos-Hull K,
Schwacke LH (2011) Lacaziosis and lacaziosis-like pre -
valence among wild, common bottlenose dolphins Tur-
siops truncatus from the west coast of Florida, USA. Dis
Aquat Org 95: 49−56
Caldwell DK, Caldwell MC, Woodard JC, Ajello L, Kaplan
W, McLure HM (1975) Lobomycosis as a disease of the
Atlantic bottle-nosed dolphin (Tursiops truncatus Mon-
tagu, 1821). Am J Trop Med Hyg 24: 105−114
Copeland G, Monteiro T, Couch S, Borthwick A (2003)
Water quality in Sepetiba Bay, Brazil. Mar Environ Res
55: 385−408
Corredor GG, Peralta LA, Castaño JH, Zuluaga JS and
others (2005) The naked-tailed armadillo Cabassous
centralis (Miller 1899): a new host to Paracoccidioides
brasiliensis. Molecular identification of the isolate. Med
Mycol 43: 275−280
Costa APB, Fruet P, Daura-Jorge FG, Simões-Lopes PC, Ott
PH, Valiati VH, Oliveira LR (2015) Bottlenose dolphin
communities from the southern Brazilian coast: Do they
exchange genes or are they just neighbours? Mar Freshw
Res (in press) http: //dx.doi.org/10.1071/MF14007
Cowan DF (1993) Lobo’s disease in a bottlenose dolphin
(Tursiops truncatus) from Matagorda Bay, Texas. J Wildl
Dis 29: 488−489
CPPS (Comisión permanente del Pacifico Sur) (2014) Estado
del Medio Ambiente Marino y Costero del Pacífico Sud-
este. Serie Estudios Regionales 4. CPPS, Guayaquil
D’Aquino CA, Neto JSA, Barreto GAM, Schettini CAF
(2011) Caracterização oceanográfica e do transporte de
sedimentos em suspensão no estuário do rio Mampituba,
SC. Rev Bras Geofís 29: 217−230
Daura-Jorge FG, Simões-Lopes PC (2011) Lobomycosis-like
disease in wild bottlenose dolphins Tursiops truncatus of
Laguna, southern Brazil: monitoring of a progressive
case. Dis Aquat Org 93: 163−170
Daura-Jorge F, Ingram S, Simões-Lopes PC (2013) Seasonal
abundance and adult survival of bottlenose dolphins
(Tursiops truncatus) in a community that cooperatively
forages with fishermen in southern Brazil. Mar Mamm
Sci 29: 293−311
de Vries GA, Laarman JJ (1973) A case of Lobo’s disease in
the dolphin Sotalia guianensis. Aquat Mamm 1: 26−33
Di Giacomo AB (2014) Padrão de ocorrência e uso de habitat
do golfinho-nariz-de-garrafa (Tursiops truncatus) no
estuário do rio Mampituba e regiões adjacentes, no sul
do Brasil. MSc thesis, Universidade Federal do Espírito
Santo, Aracruz
Di Giacomo AB, Ott PH (in press) Long-term site fidelity and
residency patterns of bottlenose dolphins (Tursiops trun-
catus) in the Tramandaí estuary, southern Brazil. Lat Am
J Aquat Mamm
Díaz JM, Acero A (2003) Marine biodiversity in Colombia:
achievements, status of knowledge, and challenges.
Gayana Zool 67: 261−274
du Toit K (2011) Prevalence of skin disease and ecto-
parasites in bottlenose dolphins around southern Africa.
BSc Honours thesis, University of Pretoria
Esperón F, García-Párraga D, Bellière EN, Sánchez-Vizcaíno
JM (2012) Molecular diagnosis of lobomycosis-like dis-
ease in a bottlenose dolphin in captivity. Med Mycol 50:
106−109
Fair PA, Becker PR (2000) Review of stress in marine mam-
mals. J Aquat Ecosyst Stress Recovery 7: 335−354
Félix F (1994) Ecology of the coastal bottlenose dolphin Tur-
siops truncatus in the Gulf of Guayaquil, Ecuador. Invest
Cetacea 25: 235–256
Félix F (1997) Organization and social structure of the bot-
tlenose dolphin Tursiops truncatus in the Gulf of Guaya -
quil, Ecuador. Aquat Mamm 23: 1−16
FEPAM (Fundação Estadual de Proteção Ambiental Hen-
rique Luiz Roessler) (2015) Monitoramento da quali-
dade da água da Região Hidrográfica das Bacias Lito -
râneas. Available at www.fepam.rs.gov.br/qualidade/
balneabilidade_historico.asp (accessed 20 Feb 2015)
Flach L (2015) Estimativa de parâmetros populacionais, área
de vida, mortalidade e impactos da atividade pesqueira
sobre a população de botos-cinza (Sotalia guianensis)
(Van Bénéden, 1864) (Cethartiodactyla, Delphinidae) na
72
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
Van Bressem et al.: Lobomycosis-like disease in bottlenose dolphins
Baía de Sepetiba (RJ). PhD thesis, Universidade do
Estado do Rio de Janeiro
Flach L, Flach PA, Chiarello AG (2008) Aspects of behav-
ioral ecology of Sotalia guianensis in Sepetiba Bay,
southeast Brazil. Mar Mamm Sci 24: 503−515
Flores PAC, Bazzalo M, Da Silva LZ, Wells RS (2005) Evidên-
cia de residência individual e ocorrência de lesões epidér-
micas em golfinhos Tursiops truncatus na Baía Norte, SC,
Brasil. In: Fagundes V, Costa LP, Leite LR, Mendes SL (eds)
Livro de Resumos, III Congresso Bra sileiro de Mastozo-
ologia, 12-16 October, 2005, Aracruz, Espirito Santo, p 87
Francesconi VA, Klein AP, Santos AP, Ramasawmy R,
Francesconi F (2014) Lobomycosis: epidemiology, clini-
cal presentation, and management options. Ther Clin
Risk Manag 10: 851−860
Frank SA (2002) Immunology and evolution of infectious
disease. Princeton University Press, Princeton, NJ
Fruet PF, Secchi ER, Di Tullio JC, Kinas PG (2011) Abun-
dance of bottlenose dolphins, Tursiops truncatus (Ceta -
cea: Delphinidae), inhabiting the Patos Lagoon estuary,
southern Brazil: implications for conservation. Zoologia
28: 23−30
Fruet PF, Secchi ER, Daura-Jorge F, Vermeulen E and others
(2014) Remarkably low genetic diversity and strong pop-
ulation structure in common bottlenose dolphins (Tur-
siops truncatus) from coastal waters of the Southwestern
Atlantic Ocean. Conserv Genet 15: 879−895
Fruet PF, Daura-Jorge F, Möller LM, Genoves RC, Secchi ER
(2015a) Abundance and demography of bottlenose dol-
phins inhabiting a sub-tropical estuary in the Southwest-
ern Atlantic Ocean. J Mammal 96: 332−343
Fruet PF, Genoves RC, Möller LM, Botta S, Secchi ER
(2015b) Using mark-recapture and stranding data to esti-
mate reproductive traits in female bottlenose dolphins
(Tursiops truncatus) of the Southwestern Atlantic Ocean.
Mar Biol 162: 661−673
Garcia MR, Mirlean N, Baisch PR, Caramão EB (2010)
Assessment of polycyclic aromatic hydrocarbon influx
and sediment contamination in an urbanized estuary.
Environ Monit Assess 168: 269−276
Gupta AK, Simpson FC, Brintnell WC (2014) Do genetic
mutations and genotypes contribute to onychomycosis?
Dermatology 228: 207−210
Haase J, Stringuini MH, Silva MLBC, Rodrigues MLK, Koch
SMV (2003) Qualidade das águas superficiais do litoral-
norte e médio do Rio Grande do Sul. In: 22º Congresso
Brasileiro de Engenharia Sanitária e Ambiental, 14–19
Sep, Join ville, Brazil. Available at www. fepam. rs. gov. br/
qualidade/arg/VI_049-QAS_LN_LM_RS.pdf
Herr RA, Tarcha EJ, Taborda PR, Taylor JW, Ajello L, Men-
doza L (2001) Phylogenetic analysis of Lacazia loboi
places this previously uncharacterized pathogen within
the dimorphic Onygenales. J Clin Microbiol 39: 309−314
Herrera JC, Van Bressem MF, Cantera-Kintz JR (2013) Pres-
encia de lobomycosis en delfines nariz de botella (Tur-
siops truncatus), en aguas cercanas al Parque Nacional
Natural Sanquianga. In: Campos NH, Dueñas P (eds)
Memorias del XV Seminario Na cional de Ciencias y Tec-
nologías del Mar, Cartagena, Colombia, p 149–150
Hurtado MD, Hurtado MG, Hurtado L (2012) Estado de la
contaminación marina en Ecuador. Consultancy report to
the Permanent Commission for the South Pacific (CPPS),
Guayaquil, Ecuador. http://cpps.dyndns.info/cpps-docs-
web/planaccion/docs2013/mar/xix_ag/025.%20INFORME
_FINAL_ECU_CONTAMINACIÓN_MARINA.pdf
IWC (International Whaling Commission) (2009) Report of
the Workshop on Cetacean Skin Diseases. J Cetacean
Res Manag 11: 503−516
Kiszka J, Van Bressem MF, Pusineri C (2009) Lobomycosis-
like disease and other skin conditions in Indo-Pacific
bottlenose dolphins Tursiops aduncus from the Indian
Ocean. Dis Aquat Org 84: 151−157
Kiszka J, Simon-Bouhet B, Gastebois C, Pusineri C, Ridoux
V (2012) Habitat partitioning and fine scale population
structure among insular bottlenose dolphins (Tursiops
aduncus) in a tropical lagoon. J Exp Mar Biol Ecol 416-
417:
176−184
Kjerfve B (1986) Comparative oceanography of coastal
lagoons. In: Wolfe DA (ed) Estuarine variability. Academic
Press, New York, NY, p 63–81.
Lane EP, de Wet M, Thompson P, Siebert U, Wohlsein P, Plön
S (2014) A systematic health assessment of Indian ocean
bottlenose (Tursiops aduncus) and Indo-Pacific hump-
back (Sousa plumbea) dolphins incidentally caught in
shark nets off the KwaZulu-Natal Coast, South Africa.
PLoS ONE 9: e107038
Lélis RJF, Calliari LJ (2006) Historical shoreline changes
near lagoonal and river stabilized inlets in Rio Grande do
Sul state, southern Brazil. J Coast Res Spec Issue 39:
301−305
Lodi L, Cantor M, Daura-Jorge F, Monteiro-Neto C (2014) A
missing piece from a bigger puzzle: declining occurrence
of a transient group of bottlenose dolphins off Southeast-
ern Brazil. Mar Ecol 35: 516−527
Mann J, Smuts B (1999) Behavioral development of wild bot-
tlenose dolphin newborns. Behaviour 136: 529−566
Mann J, Connor RC, Barre LM, Heithaus MR (2000) Female
reproductive success in bottlenose dolphins (Tursiops
sp.): life history, habitat, provisioning, and group-size
effects. Behav Ecol 11: 210−219
Martin LB, Hopkins WA, Mydlarz LD, Rohr JR (2010) The
effects of anthropogenic global changes on immune
functions and disease resistance. Ann NY Acad Sci 1195:
129−148
Migaki G, Valerio MG, Irvine B, Garner FM (1971) Lobo’s
disease in an Atlantic bottle-nosed dolphin. J Am Vet
Med Assoc 159: 578−582
Mirlean N, Andrus VE, Baisch P (2003) Mercury pollution
sources in sediments of Patos Lagoon Estuary, Southern
Brazil. Mar Pollut Bull 46: 331−334
Molisani MM, Marins RV, Machado W, Paraquetti HHM,
Bidone ED, Lacerda LD (2004) Environmental changes in
Sepetiba Bay, SE Brazil. Reg Environ Change 4: 17−27
Moreno IB, Ott PH, Tavares M, Oliveira LR and others (2008)
Mycotic dermatitis in common bottlenose dolphins (Tur-
siops truncatus) from southern Brazil, with a confirmed
record of lobomycosis disease. Paper SC/60/DW1 pre-
sented to the IWC Scientific Committee, Santiago, Chile,
May 2008
Murdoch ME, Reif JS, Mazzoil M, McCulloch SD, Fair PA,
Bossart GD (2008) Lobomycosis in bottlenose dolphins
(Tursiops truncatus) from the Indian River Lagoon, Flo -
rida: estimation of prevalence, temporal trends, and spa-
tial distribution. EcoHealth 5: 289−297
Murdoch ME, Mazzoil M, McCulloch S, Bechdel S, O’Corry-
Crowe G, Bossart GD, Reif JS (2010) Lacaziosis in bottle-
nose dolphins Tursiops truncatus along the coastal
Atlantic Ocean, Florida, USA. Dis Aquat Org 92: 69−73
Naranjo LG, Castillo LF, Johnston-González R, Hernández
C, Ruiz C, Estela F (2006) Waterbird monitoring and con-
73
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
Dis Aquat Org 117: 59–75, 2015
servation in protected areas of the Colombian Pacific. In:
Boere GC, Galbraith CA, Stroud DA (eds) Waterbirds
around the world. The Stationery Office, Edinburgh,
p 177−180
Ott PH, Barreto AS, Siciliano S, Laporta P and others (in
press) Report of the working group on taxonomy and
stock identity of bottlenose dolphins in the Southwestern
Atlantic Ocean. Lat Am J Aquat Mamm
Palmer C, Peterson A (2014) First report of a lacaziosis-like
disease (LLD) observed in the Australian snubfin dolphin
(Orcaella heinsohni) in Darwin Harbour, Northern Terri-
tory, Australia. North Territ Nat 25: 3−6
Paniz-Mondolfi A, Talhari C, Sander Hoffman L, Connor DL
and others (2012) Lobomycosis: an emerging disease in
humans and Delphinidae. Mycoses 55: 298−309
Parra AS, Restrepo Á (2014) El colapso ambiental en el río
Patía, Colombia: variaciones morfológicas y alteraciones
en los ecosistemas de manglar. Lat Am J Aquat Res 42:
40−60
Pessanha AL, Araújo FG (2003) Spatial, temporal and diel
variations of fish assemblages at two sandy beaches in
the Sepetiba Bay, Rio de Janeiro, Brazil. Estuar Coast
Shelf Sci 57: 817−828
Phillips GL (2006) Bottlenose dolphins (Tursiops aduncus) in
Plettenberg Bay, South Africa: population estimates and
temporal dynamics of groups. MSc thesis, Nelson Man-
dela Metropolitan University, Port Elizabeth
Pinotti RM, Colling L, Bemvenuti CE (2011) Temporal
dynamics of deep infralittoral macrobenthic fauna inside
a subtropical estuarine environment. Braz J Aquat Sci
Technol 15: 26−41
PNN (Parque Nacional Natural) Sanquianga (2013) Actual-
ización del Plan de Manejo del Parque Nacional Natural
Sanquianga Componente Diagnóstico. Ministerio de
ambiente y desarrollo sostenible parques nacionales,
Dirección Territorial Pacifico, Cali, Columbia
PNN Uramba Bahía Málaga (2014) Componente ordena -
miento para el Plan de Manejo Parque Nacional Natural
Uramba Bahía Málaga. Dirección Territorial Pacífico, Par-
ques Nacionales Naturales de Colombia, Bahía Málaga,
Buenaventura, Valle del Cauca— Pacífico Colombiano
Pusineri C, Barbraud C, Kiszka J, Caceres S, Mougnot J,
Daudin G, Ridoux V (2014) Capture-mark-recapture
modelling suggests an Endangered status for the May-
otte Island (eastern Africa) population of Indo-Pacific
bottlenose dolphins. Endang Species Res 23: 23−33
Quod JP, Naim O, Abdourazi F (2000) The Comoros archi-
pelago. In: Sheppard C (ed) Seas at the Millennium:
an environmental evaluation. Pergamon Press, Oxford,
p 243–252
Reif JS, Mazzoil MS, McCulloch SD, Varela RA, Goldstein
JD, Fair PA, Bossart GD (2006) Lobomycosis in Atlantic
bottlenose dolphins from the Indian River Lagoon,
Florida. J Am Vet Med Assoc 228: 104−108
Reif JS, Peden-Adams MM, Romano TA, Rice CD, Fair PA,
Bossart GD (2009) Immune dysfunction in Atlantic bot-
tlenose dolphins (Tursiops truncatus) with lobomycosis.
Med Mycol 47: 125−135
Reisinger RR, Karczmarski L (2010) Population size estimate
of Indo-Pacific bottlenose dolphins in the Algoa Bay
region, South Africa. Mar Mamm Sci 26: 86−97
Rengifo B, Capella J, Flórez González L (1995) Patterns of
occurrence of bottlenose dolphins in Bahía Málaga,
Colombian Pacific: preliminary observations. In: 11th
Biennial Conference on the Biology of Marine Mammals,
Orlando, FL. Society for Marine Mammalogy, Moss
Landing, CA, p 96
Ribeiro AP, Figueiredo AM, dos Santos JO, Dantas E and
others (2013) Combined SEM/AVS and attenuation of
concentration models for the assessment of bioavailabil-
ity and mobility of metals in sediments of Sepetiba Bay
(SE Brazil). Mar Pollut Bull 68: 55−63
Ricci G, Mota FT, Wakamatsu A, Serafim RC, Borra RC,
Franco M (2004) Canine paracoccidioidomycosis. Med
Mycol 42: 379−383
Richini-Pereira VB, Bosco SDMG, Griese J, Theodoro RC
and others (2008) Molecular detection of Paracoccid-
ioides brasiliensis in road-killed wild-animals. Med
Mycol 46: 35−40
Rocha CM (2013) Qualidade das águas na BH Rio Traman-
daí. In: Castro D, Mello RSP (eds) Atlas ambiental da
bacia hidrográfica do Rio Tramandaí. Edicions Via Sapi-
ens, Porto Alegre, p 149−155
Romano TA, Keogh MJ, Kelly C, Feng P and others (2004)
Anthropogenic sound and marine mammal health: meas-
ures of the nervous and immune systems before and after
intense sound exposure. Can J Fish Aquat Sci 61:
1124−1134
Rotstein DS, Burdett-Hart LG, McLellan W, Schwacke L and
others (2009) Lobomycosis in offshore bottlenose dol-
phins (Tursiops truncatus), North Carolina. Emerg Infect
Dis 15: 588−590
Schwarzbold A. Schäfer A (1984) Gênese e morfologia das
lagoascosteiras do Rio Grande do Sul, Brasil. Amazoni-
ana 9: 87−104
Siciliano S, Van Bressem MF, Moreno IB, Ott PH and others
(2008) Review of lobomycosis and lobomycosis-like disease
(LLD) in Cetacea from South America. Paper SC/ 60/ DW13
presented to the IWC Scientific Committee, Santiago,
Chile, May 2008. www. research gate .net/ publication/ 272
018662_Review_of_Lobomycosis_and_ Lobomycosis-like _
disease _%28LLD%29_in_Cetacea_ from_ South _ America
Simões-Lopes PC, Fabian ME (1999) Residence patterns and
site fidelity in bottlenose dolphins, Tursiops truncatus
(Montagu) (Cetacea, Delphinidae) off Southern Brazil.
Rev Bras Zool 16: 1017−1024
Simões-Lopes PC, Paula GS, Xavier FM, Scaramelo AC
(1993) First case of lobomycosis in a bottlenose dolphin
from southern Brazil. Mar Mamm Sci 9: 329−331
Sommer S (2005) The importance of immune gene variabil-
ity (MHC) in evolutionary ecology and conservation.
Front Zool 2: 16
Souza DSM, Ramos APD, Nunes FF, Moresco V and others
(2012) Evaluation of tropical water sources and mollusks
in southern Brazil using microbiological, biochemical and
chemical parameters. Ecotoxicol Environ Saf 76: 153−161
Symmers WS (1983) A possible case of Lobo’s disease
acquired in Europe from a bottlenosed-dolphin (Tursiops
truncatus). Bull Soc Pathol Exot Filiales 76: 777−784
Taborda PR, Taborda VA, McGinnins MR (1999) Lacazia
loboi gen. nov., comb. nov., the etiologic agent of lobo -
mycosis. J Clin Microbiol 37: 2031−2033
Tajima Y, Sasaki K, Kashiwagi N, Yamada TK (2015) A case
of stranded Indo-Pacific bottlenose dolphin (Tursiops
aduncus) with lobomycosis-like skin lesions in Kinko-
wan, Kagoshima, Japan. J Vet Med Sci 77: 989−992
Theodoro RC, Teixeira MDM, Felipe MS, Paduan KDS,
Ribolla PM, San-Blas G, Bagagli E (2012) Genus Para -
coccidioides: species recognition and biogeographic
aspects. PLoS ONE 7: e37694
74
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
Van Bressem et al.: Lobomycosis-like disease in bottlenose dolphins 75
Thomassin BA, Garcia F, Lagadec V, Sarrazin L and others
(2008) Mayotte: évaluation de la qualité des eaux
côtières du lagon à partir des polluants dosés dans les
huîtres médiolittorales (Octobre–Novembre 2007). Re -
port of GIS LagMay, Direction de l’Agriculture et de la
Forét de Mayotte, Momoudzou
Torres JI, Pinzón MP, Esquivia M, Parra A, Espitia E (2012)
La explotación ilícita de recursos minerales en Colombia:
Casos Valle del Cauca (Río Dagua)— Chocó (Río San
Juan), Efectos sociales y ambientales. Contraloría Dele-
gada, Sector Minas y Energía, Contraloría General de la
República, Bogotá
Ueda K, Sano A, Yamate J, Itano Nakagawa E and others
(2013) Two cases of lacaziosis in bottlenose dolphins (Tur-
siops truncatus) in Japan. Case Rep Vet Med 2013: 318548
Van Bressem MF, Van Waerebeek K, Reyes JC, Felix F and
others (2007) A preliminary overview of skin and skeletal
diseases and traumata in small cetaceans from South
American waters. Lat Am J Aquat Mamm 6: 7−42
Van Bressem MF, de Oliveira Santos MC, de Faria Oshima
JE (2009a) Skin diseases in Guiana dolphins (Sotalia
guianensis) from Paranagua estuary, Brazil: a possible
indicator of a compromised marine environment. Mar
Environ Res 67: 63−68
Van Bressem MF, Raga JA, Di Guardo G, Jepson PD and
others (2009b) Emerging infectious diseases in cetaceans
worldwide and the possible role of environmental stres-
sors. Dis Aquat Org 86: 143−157
Van Bressem MF, Flach L, Reyes JC, Echegaray M and
others (2015) Epidemiological characteristics of skin
disorders in cetaceans from South American waters. Lat
Am J Aquat Mamm 10: 20−32
Wilson B, Arnold H, Berazi G, Fortuna CM and others (1999)
Epidermal lesions in bottlenose dolphins: impacts of nat-
ural and anthropogenic factors. Proc R Soc Lond B Biol
Sci 266: 1077−1083
Würsig B, Jefferson RA (1990) Methods of photo-identifica-
tion for small cetaceans. Rep Int Whal Comm Spec Issue
12: 42−43
Zappes CA, Andriolo A, Simões-Lopes PC, Di Beneditto
APM (2011) ‘Human-dolphin (Tursiops truncatus —
Montagu, 1821) cooperative fishery’ and its influence on
cast net fishing activities in Barra de Imbé/Tramandaí,
Southern Brazil. Ocean Coast Manag 54: 427−432
Editorial responsibility: Michael Moore,
Woods Hole, Massachusetts, USA
Submitted: March 23, 2015; Accepted: September 21, 2015
Proofs received from author(s): October 30, 2015
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
