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Epidemiology of tattoo skin disease in cetaceans worldwide: a general health indicator for
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cetacean and their environment
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Marie-Françoise Van Bressem1, Koen Van Waerebeek1, Juan Antonio Raga2, Paul Jepson3, Padraig Duignan4, Rob
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Deaville3, Leonardo Flach5, Francisco Viddi6, John Baker7, Ana Paula Di Beneditto8, Mónica Echegaray9, Tilen
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Genov10, Julio Reyes9, Fernando Felix11, Raquel Gaspar12, Renata Ramos13, Vic Peddemors14 and Ursula Siebert15
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Cetacean Conservation Medicine Group (CMED), CEPEC, Museo de Delfines, Pucusana, Peru;
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Marine Zoology Unit, Cavanilles Institute of Biodiversity and Evolutionary Biology, University of Valencia, P.O.
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Box 22085, 46071 Valencia, Spain;
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Research Unit;
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National Disease Control Centre, Level 1E, Agriculture House, Dublin 2, Ireland;
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Projeto Boto Cinza - MBR - Um Grupo CAEMI, Rua Sta Terezinha, 531 – 90 Vila Muriqui, 23860-000 -
Veterinary Science Group, Institute of Zoology, Regent's Park, London NW1 4RY, England, UK Sea Mammal
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Mangaratiba-RJ, Brazil;
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John Baker
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Universidade Estadual do Norte Fluminense-CBB, Laboratório de Ciências Ambientais, Av. A. Lamego, 2000-
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Campo dos Goytacazes, RJ 28013-602, Brazil;
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Áreas Costeras y Recursos Marinos (ACOREMA), Av. San Martín 1471, Pisco, Peru; Morigenos- Marine Mammal Research and Conservation Society Jarska cesta 36/a 1000 Ljubljana, Slovenia; Fundación Ecuatoriana para el Estudio de Mamíferos Marinos (FEMM), PO Box 09-01-11905, Guayaquil,
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Ecuador;
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Everest, Av. Nossa Senhora dos Navegantes, 675/1201, Enseada do Suá, Vitória, ES, 29056-900, Brazil;
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Graduate School of the Environment, Macquarie University, Sydney, NSW 2109, Australia;
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Büsum, Germany.
Gatty Marine Laboratory, University of St. Andrews, St. Andrews, Fife KY16 8LB, Scotland, U.K;
Forschungs- und Technologiezentrum Westküste, Christian-Albrechts-Universität Kiel, Hafentöern D-25761
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ABSTRACT
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INTRODUCTION
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In cetaceans tattoo skin disease (TSD) is characterised by very typical, irregular, grey, black or yellowish, stippled
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lesions (Figure 1) that may occur on any part of the body but show a preferential corporal distribution depending on
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the species (Van Bressem & Van Waerebeek, 1996). With some practice, tattoos are easily distinguished visually
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from other types of integument blemishes and scars. The disease has been observed in several species of free-
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ranging odontocetes from the North Atlantic and East Pacific Oceans and in the Mediterranean Sea, as well as in
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captive bottlenose dolphins (Tursiops truncatus) (see Van Bressem et al. 1999). It was also recently reported in a
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bowhead whale (Balaena mysticetus) though no pictures of the lesions were provided (Bracht et al. 2006). TSD is
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caused by poxviruses (Flom & Houk 1979, Geraci et al. 1979, Van Bressem et al. 1993, 2006) that belong to a new
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genus of Chordopoxvirinae, but have a common, most immediate ancestor with terrestrial poxviruses of the genus
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Orthopoxvirus (Bracht et al. 2006, Pearce et al. submitted). These viruses are thought to induce humoral immunity
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that protects neonates and young calves from the disease (Smith et al. 1983, Van Bressem & Van Waerebeek 1996,
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Van Bressem et al. 2006). Individual tattoo lesions may persist for months an even years and recurrence may occur
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(Van Bressem et al. 2003). They eventually heal and convert into light gray marks (G-marks) that may or may not
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have a darker outline and a darker center (Van Bressem et al. 2003).
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Though clinical and epizootiological data do not indicate that poxvirus infection induces a high mortality rate when
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enzootic (Van Bressem & Van Waerebeek 1996, Van Bressem et al. 2003), it may kill neonates and calves without
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protective immunity and thus affects host population dynamics. TSD may also have contributed to the decline of
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bottlenose dolphins from the Sado Estuary, Portugal, through affecting juvenile survival (Van Bressem et al. 2003).
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Besides, the presence of very large tattoo lesions and their persistence (over 3 years) in adult bottlenose dolphins
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may indicate immune deficiencies related to environmental contaminants (Van Bressem et al. 2003). In search of
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the potential for anthropogenic factors to influence the prevalence of tattoo disease, we started in 1995 a worldwide
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survey on the epidemiology and ecology of TSD. Here we present the results of this study.
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MATERIAL AND METHODS
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The presence of TSD was examined in 1,285 live, free-ranging and dead small cetaceans originating from the South
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Pacific, the Southwest and North Atlantic as well as from the North, Baltic, Mediterranean and Tasmanian Seas
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(Table 1). We include in this paper previously published data on the epidemiology of TSD in Peruvian small
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cetaceans and bottlenose dolphins (Tursiops truncatus) from the Sado Estuary, Portugal (Van Bressem & Van
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Waerebeek 1996, Van Bressem et al. 2003).
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Freshly dead specimens The majority of dead cetaceans had died in nets or stranded in the period 1984-2007
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(Table 1). Thus, condition varied from alive to early decomposed (but with mostly intact skin). The whole body
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surface was examined for the presence of tattoos. Several specimens were frozen before examination. Sexual
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maturity was determined directly from an examination of gonads and lactation or was inferred from standard body
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length and known life history parameters for these populations (Collet & Saint Girons 1984, Van Waerebeek 1992,
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Calzada 1995, Lockyer 1995, Reyes & Van Waerebeek 1995, Padraig: please add reference). When sexual maturity
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status could not be determined directly, it was inferred from the standard body length. Van Waerebeek (1992)
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estimated that 50% of Peruvian dusky dolphins L. obscurus in both sexes attain sexual maturity at 175 cm. Female
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and male Burmeister’s porpoises P. spinipinnis reach sexual maturity on average at 155cm and 160cm, respectively
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(Reyes & Van Waerebeek 1995). Female and male Mediterranean striped (Stenella coeruleoalba) dolphins larger
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than 187 cm and 190 cm, respectively, are considered sexually mature, more than 11 years old (Calzada 1995). The
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age of some animals was determined by standard techniques (Perrin & Myrick 1980; Hohn et al. 1989).
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Free-ranging dolphins Detection of tattoos in free-ranging bottlenose dolphins from Slovaquia, Portugal and Peru,
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estuarine dolphins (Sotalia guianensis) from Brazil and Chilean dolphins (Cephalorhynchus eutropia) from the
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northern Patagonia was done by examining photographic records taken during small-boat surveys (Reyes et al.
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2002, Van Bressem et al. 2003, Flach 2006, Viddi et al. 2005). Considering that in these animals generally only
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upper body parts were visible, the reported prevalence levels should be considered minimum values. Dolphins were
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individually identified from natural marks (WĂźrsig & Jefferson 1990). Maturity (calf, juvenile, adult) was estimated
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from relative body size and behavioural clues (Wells et al. 1980, Shane 1990; others).
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Tattoos. Tattoo lesions were identified on the basis of their typical appearance, i.e. irregular, dark gray, black or
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yellowish marks with a stippled pattern (Figure 1). The topography of these marks as well as their size (small,
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medium, large and very large) relative to the body of the dolphins were registered. The number of lesions per body
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area was noted and their minimum density (MD; minimum number of lesions per animal) was recorded as low (1 to
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5 lesions), medium (6 to 10) or high (>10). Light gray, irregular marks surrounded by a black line were considered
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regressing tattoos (Figure 2). Light gray, rounded irregular marks without a dark outline were regarded as healed
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lesions (Figure 3). In this study we included only animals that were examined by the authors to avoid biases related
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to investigators. First author examined pictures of tattoo lesions in most of the cases to confirm their identity. Only
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true tattoos (including regressing ones but not healed tattoos) were considered for the statistical analysis.
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Sexual, ontogenetic and health variation in TSD prevalence
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As harbour porpoises from the North Sea are considered a population distinct from porpoises in NW Scottish, Irish
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and western British waters and the Celtic shelf (Donovan & Bjørge 1995), we divided porpoises from the United
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Kingdom in two samples: the North Sea and NE Atlantic. The latter includes the English Channel, the Irish and
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Celtic Seas. D. delphis from the waters of the United Kingdom are thought to belong to one population (Murphy et
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al. 2006). We further split the porpoises and common dolphin samples into individuals that died a traumatic death
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(fisheries, T. truncatus attack) and those that died in poor health (i.e. starvation, high parasite burden, bacterial and
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fungal infections). For all species, with sample sizes permitting, we examined whether TSD prevalence varied with
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sex and sexual maturity as a proxy for age. We divided species and populations into three age classes: (1) MIM: a
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class including neonates and young calves likely protected by maternal immunity in populations where the virus is
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endemic, (2) juveniles: older calves and subadults, specimens likely not protected any more by passive immunity
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and susceptible to TSD and (3) adults, sexually mature animals that may have active immunity against the virus.
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Very little is known of the duration of passive immunity against TSD or any other viruses in cetaceans. Results of a
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previous study (Van Bressem and Van Waerebeek, 1996) suggested that Peruvian L. obscurus and P. spinipinnis till
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145 cm and 140 cm, respectively, were protected by maternal immunity. Tattoo-like lesions were first seen in 9 and
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14 months old calf T. truncatus from the Sado estuary, Portugal (Van Bressem et al. 2003). These observations,
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age-growth data and unpublished observations by the authors suggest that passive immunity in these species last at
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least till the six or nine first months of life. This is congruent with data on maternal immunity to lumpy skin disease
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virus (a capripoxvirus) in large artiodactyls (Weiss 1968), phylogenetically related to cetaceans (Gatesy et al. 1999,
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Milinkovitch et al. 1998). Thus, we include in the first group, small cetaceans considered less than less than 6-9
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months old: harbour porpoises smaller than 105.5 cm, striped dolphins smaller than 120 cm, Hector´s dolphins less
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than *** (Padraig please complete), South American D. delphis smaller than (Fernando please complete), L.
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obscurus less than 140 cm and P. spinipinnis smaller than 130 cm.
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Interspecific and habitat variation in TSD prevalence
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We examined inter-specific variation in MIM, juvenile and mature age categories in species with a sufficiently
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large sample size in six ocean provinces: Peruvian small cetaceans, harbour porpoises and common dolphins from
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European waters (north Sea and NE Atlantic), Hector’s dolphins (Cephalorhynchus hectori), Mediterranean striped
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dolphins, bottlenose dolphins from the Sado Estuary (Portugal) and short-beaked common dolphins from the coast
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of Ecuador. We further examined variation in prevalence between adults of different species occupying an explicit
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inshore, offshore-neritic and offshore-oceanic habitat. Finally, we compared the characteristics of the disease
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(minimal density of lesions, size and topography) in the inshore, neritic and offshore groups. Prevalence refers to
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the number of positive specimens in samples and sub-samples at the time of examination, without distinction
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between old and new cases (Thrusfield, 1986). Significance of differences in prevalence (≤ 0.05) was verified with
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chi-square contingency tests or 2-tailed Fisher’s exact tests (Swinscow, 1981).
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RESULTS
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Distribution. We detected TSD in Delphinidae, Phocoenidae and Ziphiidae from the South and Northeast Pacific,
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Southwest and North Atlantic as well as from the North, Tasmanian and Mediterranean Seas (Table 1). When
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present in a population, prevalence of TSD varied from 1.4% to 62.3%, according to the species, populations and
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ocean provinces (Table 1). The highest prevalence levels were recorded in P. spinipinnis and D. capensis from Peru
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(Table 1). We consider that TSD is endemic in all species and populations where prevalence is above 5% and where
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the disease was observed for several years (Table 1).
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Sexual, ontogenic and health variation. With the exception of Burmeister´s porpoises from Peru, prevalence did
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not vary with sex in all species and populations for which a sufficient number of individuals were examined (Table
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2). Thus, sexes were pooled for subsequent analyses. Among cetaceans hat had died a traumatic death (caught in
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nets, shot, attacked by bottlenose dolphins) as well as free-ranging T. truncatus from the Sado estuary, prevalence
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varied with the age class, being null in the MIM group with the exception of Mediterranean S. coeruleoalba,
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peaking among sexually immature and then decreasing in adults (Table 3). Significance of this variation varied with
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the species and populations sampled (Table 3). On the opposite, prevalence increased in adult common dolphins
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and adult harbour porpoises from the UK that had died in poor health though this variation was not significant in
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the porpoises (2-tailed Fisher’s, NE Atlantic: P= 0,142, North Sea: P= 1) and could not be tested in the common
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dolphins (Table 3). In the NE Atlantic prevalence of TSD was higher in P. phocoena of the poor health category
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that in those of the trauma category though significance of these results was borderline (χ2= 3,59, df=1, P= 0,058).
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Prevalence of TSD in adult P. phocoena and D. delphis belonging to the trauma category was null while it varied
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between 25-33.3% in the poor health category, a highly significative (χ2= 7,25, df=1, P= 0,007) difference. In P.
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spinipinnis, prevalence remained high in adults and was significantly higher in adult and juvenile males than in
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females from the corresponding age categories (Van Bressem & Van Waerebeek 1996). Besides, in this species a 5
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high density of lesions was only seen in males (2-tailed Fisher’s, P= 0,06) and prevalence of this condition
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increased in adults (44,4%, N= 18 versus 21,4%, N= 14) though not significantly (2-tailed Fisher’s, P= 0,32). In the
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MIM group, TSD was only seen in a 100cm male calf Mediterranean S. coeruleoalba that had a medium density of
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small lesions on the melon (Figure 2).
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Inter-specific and habitat variation. When the age and health status categories were considered, TSD prevalence
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was exactly the same in both P. phocoena populations (NE Atlantic and North Sea) from UK coastal waters (Table
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4). Among immatures, TSD prevalence was significantly (χ2= 5,38, df=1, P= 0,02) higher in D. capensis than in L.
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obscurus from Peruvian neritic waters. However, there was no significant prevalence variation among adults from
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these species (χ2= 1,88, df=1, P= 0,17). Prevalence of TSD varied very significantly (χ2= 29,8, df= 2, P< 0,001)
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between inshore, neritic and offshore species, being high in the first two categories and low in the offshore (Table
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4). In inshore dolphins and porpoises, prevalence remained high in adults while it significantly decreased in adult
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neritic (χ2= 21,91, df= 1, P< 0,001) and offshore (χ2=4,55, df= 1, P = 0,03) cetaceans. A similar pattern was
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observed with the density of tattoo lesions. Prevalence of this condition was high in immature coastal, neritic and
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offshore cetaceans. It then lowered significantly (χ2= 10,73, df=1, P= 0,001) in adult neritic dolphins but stayed
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high in coastal odontocetes (Table 5). Coastal adults had a very significantly (χ2= 14,95, df= 1, P= 0,0001) higher
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prevalence of high tattoo density than neritic adults. Besides, very large lesions (Figure 4) were only seen in coastal
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(3) and neritic (1) adults (Table 5).
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DISCUSSION
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During this study we examined the presence and prevalence of TSD in several cetacean species and populations
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worldwide (Table 1). The disease was observed in 11 (check) species from the Atlantic and Pacific Oceans as well
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as from the North, Mediterranean and Tasmanian seas. Prevalence was likely more accurately determined in by-
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caught specimens as the whole body could be examined and there was no health bias as in stranded specimen. The
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higher prevalence levels (34.7%-62.3%) were observed in dolphins and porpoises caught off Peru in 1993-1994,
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followed by free-ranging T. truncatus (20%) that inhabited the Sado estuary (Portugal) in 1994-1997. The visual
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diagnostic of tattoo skin disease and subsequent poxvirus infection was confirmed by electron microscopy and/or
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polymerase chain reaction in harbour porpoises and a striped dolphin from the UK (Pearce et al. submitted) and
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Peruvian small cetaceans (Van Bressem et al. 1993, Van Bressem & Van Waerebek 1996).
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With the exception of P. spinpinnis (Van Bressem & Van Waerebeek, 1996), there was no significant sexual
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variation in TSD prevalence within the species and populations studied. Neonates and young calves were very
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rarely infected, presumably because protected by maternal immunity. Again with the exception of P. spinipinnis
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prevalence of the disease was lower in mature than in immature specimens in all species and populations that
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suffered a traumatic death. Though significance of this variation varied, this likely reflects that in these populations,
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the virus infects calves no longer protected by maternal immunity, provokes TSD and is then progressively cleared
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in adults as described in Peruvian Delphinidae (Van Bressem & Van Waerebeek 1996). A different epidemiological
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pattern of TSD (i.e. higher prevalence levels of TSD in adults than in immature) was observed in P. phocoena and
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D. delphis that died in poor health along the coast of the United Kingdom. Prevalence of TSD in poor health
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porpoises from the NE Atlantic was also almost significantly higher than in the trauma group congruent with
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observations from the UK co-authors over a period of (10?, Paul and Rob do you agree?) years and those from
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Geraci et al. (1979) who reported that in captive dolphins the development of TSD was linked to general health.
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Significantly, none of the adult P. phocoena and D. delphis from the trauma group had tattoos while at least a
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quarter of those from the poor health group were affected. These findings suggest that adult small cetaceans that
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stranded in poor health in the UK had a depressed immune system and could not adequately fight infections. High
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exposure to polychlorinated biphenyls (PCBs) was previously shown to increase the risk of mortality from
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infectious diseases in P. phocoena from the UK (Jepson et al. 2005, Hall et al. 2006).
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To examine the significance of habitat variations we compared TSD prevalence levels as well as prevalence of high
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tattoo density in coastal, neritic and offshore cetaceans, split into mature and immature (excluding MIM) groups.
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Prevalence of TSD varied very significantly between inshore, neritic and offshore species, being high in the first
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two categories and low in the offshore. Besides, prevalence of TSD did not vary significantly between adults and
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immature in the inshore while it decreased significantly in the adult neritic and offshore specimens. Among adults,
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prevalence of a high tattoo density was significantly higher in the inshore than in neritic cetaceans and prevalence
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of this condition remained high in coastal adult cetaceans. These results strongly suggest than the immune response
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of coastal cetaceans and their subsequent ability to clear the virus and limit its dissemination is compromised.
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Environmental contaminants including PCBs, dibenzo-p-dioxins (PCDDs), dibenzofurans (PCDFs) and related
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compounds have been repeatedly shown to affect the efficiency of the immune response in marine mammals and
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represent a factor facilitating infectious diseases (De Swart et al., 1996, Ross et al. 1996, De Guise et al. 1998, Hall
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2002, Ross 2002, Jepson et al. 2005, Hall et al. 2006). Adults, and especially males, accumulate these lipophilic
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contaminants and thus may be more susceptible to infectious diseases (Aguilar et al. 1999, Ross et al. 1996). This is
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congruent with our observations in P. spininpinnis where prevalence of TSD was significantly higher in males than
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in females and where only males had a high tattoo density. Agricultural, mining and industrial activities in South
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America are thought to have released vast amounts of contaminants into the marine environment (Borrell & Aguilar
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1999). Sewage of various origins is still discharged, mostly untreated, in the coastal waters of Peru
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(PNUMA/CONAM 2006, Van Waerebeek, Van Bressem, Reyes and Echegaray, own observations). High levels of
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contaminants have been regularly reported in P. phocoena from the North Atlantic (Aguilar & Borrell 1995, Smyth
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et al. 2000, Aguilar et al. 2002) and recent studies have indicated that an increased exposure to polychlorinated
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biphenyls (PCBs) is associated with a higher risk of infectious diseases in this species (Jepson et al. 1999, 2005,
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Hall et al. 2006). The Sado estuary suffers from eutrophication and pollution from mining, industrial and
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agricultural activities as well as from domestic sewage (Harzen 1995, Ferreira et al. 1989, Bruxelas et al. 1992) and
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high levels of PCB and heavy metal contamination have been registered in these waters (Caeiro et al. 2005).
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Padraig: could you please write a line on the contamination of the waters where C. hectori live? Thank you.
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The very high TSD prevalence levels (over 30%) seen in immature Peruvian small cetaceans and Hectorâ&#x20AC;&#x2122;s dolphins
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may be related to the stress caused by incidental and direct captures. Acute capture-related stress may result in
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widespread damage to the circulatory system and kidneys (Cowan & Curry 2002) and in alteration of the immune
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response through increase of the cortisol level and modification of the cytokine pattern (Fonfara et al. 2007).
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Chronic stress associated with high levels of fishery mortality and concomitant repeated disruption of the herd
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structure may lead to structural changes in the adrenals that may result in the secretion of more stress hormones, as
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described in T. truncatus (Clark et al. 2006). These in turn may depress the immune system, increase the
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susceptibility to infectious diseases and diminish the individual potential to clear the infection, as described in other
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mammals (Biondi & Zannino 1997, Marsland et al. 2002).
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Results of the present study strongly suggest that the epidemiological pattern of TSD may be an indicator of a
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degrading and stressful aquatic environment. A high prevalence of TSD in adult cetacean populations as well as the
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presence of large lesions may be indicative of serious health threats. Further research should include correlation
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between the presence, density and size of tattoo lesions with data on blubber concentration of PCB congeners in
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each specimen as well as on the morphology of the adrenal glands and cytokine pattern. Coastal cetaceans suffering
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capture-related stress and living in a contaminated environemnent as is the case of Peruvian P. spinipinnis very
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likely have serious problems to develop an adequate immune response against infectious agents.
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ACKNOWLEDGMENTS (co-authors, please any person or institute you wish to acknowledge. Thank you)
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We kindly thank Celia Agusti and Patricia Gozalbes for their help in processing the data collected in Mediterranean
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cetaceans, Dr RJ Monies for providing the picture of a giant tattoo in P. phocoena from the UK, Dr Sequeira for the
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picture of an infected D. delphis from Portugal, Dr Crespo for the pictures of tattoo lesions in C. commersonnii, Dr
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Jorgensen for allowing us to examine the P. phocoena collected by his institute and Dr Pearce for the PCR data.
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This study was supported by the Cetacean Society International, the Whale and Dolphin Conservation Society, the
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‘Fundação para a Ciência e Tecnologia’ from the Portuguese Ministry of Science and Technology, the ‘Reserva
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Natural do Estuário do Sado’, the ‘Conselleria de Medio Ambiente de la Generalitat Valenciana’, the ‘Ministerio de
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Medio Ambiente’, Spain and the Federal Ministry for Education and Research, Germany. CEPEC field research
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was supported by several grants from the Gesellschaft zum Schutz der Meeressäugetiere, Leopold III Fund for
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Nature Research and Conservation, IFAW, IUCN Cetacean Specialist Group and the Chicago Zoological Society.
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REFERENCES
269
Aguilar A, Borrell A (1994) Abnormally high polychlorinated biphenyl levels in striped dolphins (Stenella
270
coeruleoalba) affected by the 1990-1992 Mediterranean epizootic. Sc Total Environ 154: 237-247.
271
Aguilar A, Borrell A (1995) Pollution and harbour porpoises in the Eastern North Atlantic: a review. In Bjørge A,
272 273 274 275 276 277 278 279 280 281 282 283 284
Donovan GP (Eds) The Biology of Phocoenids. Rep Intl Whal Commn (special issue 16): 231-242. Aguilar A, Borrell A, Pastor T (1999) Biological factors affecting variability of persistent pollutant levels in cetaceans. J Cetacean Res Manag (Special Issue 1): 83-116. Aguilar A, Borrell A, Reijnders PJH (2002) Geographical and temporal variation in levels of organochlorine contaminants in marine mammals. Mar Envir Res 53: 425-452. Biondi M, Zannino LG (1997) Psychological stress, neuroimmunomodulation, and susceptibility to infectious diseases in animals and man: a review. Psychother Psychom 66: 3-26. Borrell A, Aguilar A (1999) A review of organochlorine and metal pollutants in marine mammals from Central and South America. J Cetacean Res Manag (Special Issue 1): 195-207. Bracht AJ, Brudek RL, Ewing RY, Manire CA, Burek KA, Rosa C, Beckmen KB, Maruniak JE, Romero CH (2006) Genetic identification of novel poxviruses of cetaceans and pinnipeds. Arch Virol 151:423-438 Bruxelas A, Cabeçadas L, Rosado C (1992) Recursos Marinhos e Poluição no estuário do Sado. In: Estudos de biologia e conservação da natureza. Instituto da Conservação da Natureza, nber 6, 20pp.
8
285
Caeiro S, Costa MH, Ramos TB, Fernandes F, Silveira N, Coimbra A, Medeiros G, Painho M (2005) Assessing
286
heavy metal contamination in Sado Estuary sediment: An index analysis approach. Ecol Indicators 5: 151–
287
169
288 289 290 291 292 293
Calzada N (1995) Biología del delfín listado (Stenella coeruleoalba) del Mediterraneo occidental. Ph.D. Thesis, University of Barcelona, Spain, 161 pp. Clark LS, Cowan DF, Pfeiffer DC (2006) Morphological changes in the Atlantic bottlenose dolphin (Tursiops truncatus) adrenal gland associated with chronic stress. J Comp Pathol 135(4): 208-16. Collet A, Saint Girons H (1984) Preliminary study of the male reproductive cycle in common dolphins, Delphinus delphis, in the Eastern North Atlantic. Rep Int Whal Commn (Special Issue) 6: 355-360.
294
Cowan D, Curry B (2002) Histopathological assessment of dolphins necropsied onboard vessels in the eastern
295
tropical pacific tuna fishery, Southwest Science, Center National Marine Service, NOAA 8604 La Jolla
296
Shores, Drive La Jolla, CA 92037.
297 298
De Guise S, Martineau D, Beland P, Fournier M (1998) Effects of in vitro exposure of beluga whale leukocytes to selected organochlorines. J Toxicol Environ Health A 55:479–493.
299
De Swart RL, Ross PS, Vos JG, Osterhaus ADME (1996) Impaired immunity in harbour seals (Phoca vitulina)
300
exposed to bioaccumulated environmental contaminants: review of a long-term feeding study. Environ
301
Health Perspect 104(suppl4):823–828.
302 303 304 305
Donovan GP, Bjørge A (1995) Harbour porpoises in the North Atlantic: edited extract from the report of the IWC Scientific Committee, Dublin 1995 Rep Int Whal Commn (Special Issue 16) 4-25. Ferreira A, Castro OG, Vale C (1989) Factores reguladores das variações de PCB e DDT no estuário superior do Sado. International symposium on integrated approaches to water pollution problems.
306
Flach L (2006) Photo-Identification study reveals human threats towards estuarine dolphins in Southeast Brazil. in:
307
S. Siciliano, M. Borobia, N.B. Barros, Marques, F. Trujillo, P.A.C Flores (Eds) Workshop on Research
308
and Conservation of the Genus Sotalia, Armação dos Búzios, Rio de Janeiro, Brazil, 19-23 June 2006.
309 310 311 312 313 314
Flom JO, Houk EJ (1979) Morphologic evidence of poxvirus in "tattoo" lesions from captive bottlenosed dolphins. J Wildl Dis 15:593-596. Fonfara S, Siebert U, Prange A, Colijn F. (2007) The impact of stress on cytokine and haptoglobin mRNA expression in blood samples from harbour porpoises (Phocoena phocoena). J Mar Ass UK 87: 305-311 Gatesy J, Milinkovitch MC, Waddelld V, Stanhope M (1999) Stability of cladistic relationships between Cetacea and higher level Artiodactyl taxa. Syst Biol 48: 6-20.
315
Geraci JR, Hicks BD, St Aubin DJ (1979) Dolphin pox: a skin disease of cetaceans. Can J Comp Med 43: 399-404
316
Jepson PD, Bennett PM, Allchin CR, Law RJ, Kuiken T, Baker JR, Rogan E, Kirkwood JK (1999) Investigating
317
potential associations between chronic exposure to polychlorinated biphenyls and infectious disease
318
mortality in harbour porpoises from England and Wales. Sci Total Environ 243/244: 339-348.
319
Jepson PD, Bennett PM, Deaville R, Allchin CR, Baker JR, Law RJ (2005) Relationships between polychlorinated
320
biphenyls and health status in harbor porpoises (Phocoena phocoena) stranded in the United Kingdom.
321
Environ Toxicol Chem 24:238–348.
322 323
Hall A (2002) Organohalogenated contaminants in marine mammals. In: Marine Mammals Biology and Conservation (Ed. PJ.G.H. Evans and A.J. Raga), Kluwer Academic/Plenum Publishers, New York, 626p
9
324
Hall A, Hugunin K, Deaville R, Law RJ, Allchin CR, Jepson P. (2006) The risk of infection from polychlorinated
325
biphenyl exposure in the harbor porpoise (Phocoena phocoena): a case-control approach. Environ Health
326
Perspect 114: 1:60.
327 328 329 330 331 332 333 334
Harzen S (1995) Behaviour and social ecology of the bottlenose dolphin (Tursiops truncatus) (Montagu, 1821), in the Sado estuary, Portugal. PhD thesis, University of Bielefeld, Germany Hohn A, Scott MD, Wells RS, Sweeney JC, Irvine AB (1989) Growth layers in teeth from known age, free-ranging bottlenose dolphins. Mar Mamm Sci 5: 315-342. Lockyer C (1995) Investigation of aspects of the life history of the harbour porpoise, Phocoena phocoena, in British waters. Rep Int Whal Commn (Special Issue 16): 189-197 Marsland AL, Bachen EA, Cohen S, Rabin B, Manuck SB (2002) Stress, immune reactivity and susceptibility to infectious disease. Physiol Behav 77: 711-6
335
Milinkovitch MC, Bérubé M, Palsbøll PJ (1998) Cetaceans are highly specialized Artiodactyls. Pages 113-131 in
336
THEWISSEN, J.G. (Ed) The Emergence of Whales: Evolutionary Patterns in the Origin of Cetacea.
337
Plenum, New York.
338 339 340 341 342 343
Murphy S, Herman JS, Pierce GJ, Rogan E, Kitchener AC (2006) Taxonomic status and geographical cranial variation of common dolphins (Delphinus) in the eastern north Atlantic. Mar Mamm Sci 22: 573-599 Pearce G, Blacklaws BA, Gajda AM, Jepson P, Deaville R, Van Bressem M-F (submitted) Molecular identification of poxviruses in tattoo skin lesions. Perrin WF, Myrick Jr AC (eds). 1980. Age determination of toothed whales and sirenians. Rep Int Whal Commn (Special Issue 3): 97-133.
344
PNUMA/CONAM (2006) Informe sobre el Estado del Medio Ambiente. GEO Bahía Paracas-Pisco. Lima, 164 pp.
345
Reyes JC, Van Waerebeek K (1995) Aspects of the biology of Burmeister's porpoise from Peru. Rep Int Whal
346
Commn (Special Issue 16): 349-364.
347
Reyes JC, Echegaray M, De Paz N (2002) Distribución, comportamiento y conservación de cetáceos en el área
348
Pisco Paracas. Pages 136-144 in: J. Mendo and M. Wolff (Eds). Memorias I Jornada Científica Reserva
349
Nacional de Paracas. Universidad Nacional Agraria, Lima.
350 351 352 353 354 355 356 357
Ross PS (2002) The role of immunotoxic environmental contaminants in facilitating the emergence of infectious diseases in marine mammals. HERA 8: 277-292. Ross PS, De Swart RL, Van Loveren H, Osterhaus ADME, Vos JG (1996) The immunotoxicity of environmental contaminants to marine wildlife: a review. Ann Rev Fish Dis 6: 151-165. Shane S H (1990) Behavior and ecology of the bottlenose dolphin at Sanibel Island, Florida. Pages 245-265 in: S. Leatherwood and R.R. Reeves (Eds.) The Bottlenose Dolphin. Academic Press, San Diego, CA. Smith AW, Skilling DE, Ridgway SH, Fenner CA (1983) Regression of cetacean tattoo lesions concurrent with conversion of precipitin antibody against a poxvirus. JAVMA 183: 1219-1222.
358
Smyth M, Berrow S, Nixon E, Rogan E (2000) Polychlorinated biphenyls and organochlorines in by-caught
359
harbour porpoises Phocoena phocoena and common dolphins Delphinus delphis from Irish coastal waters.
360
Biol Environm: Proc Royal Irish Acad 100B: 85-96.
361
Swinscow TDV (1981) Statistics at square one. 7th edition. British Medical Association, London.
362
Thrusfield M (Ed) (1986) Veterinary epidemiology. Butterworths & Co, London, pp 280.
10
363 364 365 366 367 368 369 370
Van Bressem M-F, Van Waerebeek K (1996) Epidemiology of poxvirus in small cetaceans from the Eastern South Pacific. Mar Mam Sci 12: 371-382 Van Bressem M-F, Van Waerebeek K, Raga JA (1999) A review of virus infections of cetaceans and the potential impact of morbilliviruses, poxviruses and papillomaviruses on host population dynamics. DAO 38: 53-65 Van Bressem M-F, Gaspar R, Aznar J (2003) Epidemiology of tattoo skin disease in bottlenose dolphins (Tursiops truncatus) from the Sado estuary, Portugal. Dis Aquat Org 56: 171-179. Van Bressem M-F, Van Waerebeek K, Bennett M (2006) Orthopoxvirus neutralising antibodies in small cetaceans from the Southeast Pacific. LAJAM 5(1): 49-54.
371
Van Bressem M-F, Van Waerebeek K, Reyes J-C, Dekegel D, Pastoret P-P (1993) Evidence of poxvirus in dusky
372
dolphin (Lagenorhynchus obscurus) and Burmeister's porpoise (Phocoena spinipinnis) from coastal Peru.
373
J Wildl Dis 29: 109-113.
374 375
Van Waerebeek K (1992) Population identity and general biology of the dusky dolphin Lagenorhynchus obscurus (Gray, 1828) in the Southeast Pacific. PhD Thesis, University of Amsterdam, 160 pp.
376
Viddi FA, Van Bressem M-F, Bello M, Lescrauwaet AK (2005) First records of skin lesions in coastal dolphins off
377
southern Chile. 16th Biennial Conference on the Biology of Marine Mammals, San Diego, California, 12-
378
16 December 2005.
379
Weiss KE (1968) Lumpy skin disease virus. Virol Monogr 3: 111–130.
380
Wells RS, Irvine AB, Scott MD (1980) The social ecology of inshore odontocetes. Pages 263-317 in Herman, LM
381 382 383 384 385
(Ed). Cetacean behavior: Mechanisms and Functions. John Wiley and Sons, New York, USA. Wilson B, Hammond PS, Thompson PM (1999) Estimating size and assessing trends in a coastal bottlenose dolphin population. Ecol. Applications 9: 288-300 Würsig B, Jefferson TA (1990) Methods of photo-identification for small cetaceans. Rep Int Whal Commn (Special Issue 12): 42–43.
386 387 388
11
FIGURES
Figure 1. Typical tattoo lesions on the head of a juvenile female harbour porpoise (Phocoena phocoena) from the North Sea.
Figure 2. Regressing tattoos on the back of an adult estuarine dolphin (Sotalia guianensis) from Sepetiba Bay, Brazil
Figure 3. Remain of a tattoo on the dorsal fin of an adult estuarine dolphin (Sotalia guianensis) from Sepetiba Bay, Brazil
Figure 4. Giant tattoo on the flank and back of an adult female harbour porpoise (Phocoena phocoena) from the Northeast Atlantic (Picture courtesy of Dr RJ Monies).
Species Delphinus spp. Phocoena phocoena Phocoena phocoena Phocoena phocoena Pontoporia blainvillei Sotalia guianensis Stenella frontalis Tursiops aduncus Tursiops truncatus Cephalorhynchus commersonii Phocoena phocoena Phocoena phocoena Delphinus delphis Ziphius cavirostris
Ocean province Indian Ocean (South Africa) Baltic Sea (Germany) North Sea (Germany) west Greenland SW Atlantic (Brazil) SW Atlantic (Brazil, Northern Rio de Janeiro) SW Atlantic (Brazil) Indian Ocean (South Africa) Adriatic Sea (Slovenia) SW Atlantic (Argentine) Northwest Atlantic (Canada) NE Pacific Northeast Atlantic (Portugal) North Sea (UK)
Specimens
By-caught Stranded
offshore/neritic inshore/neritic inshore/neritic inshore/neritic inshore/estuarine inshore/neritic offshore/oceanic inshore/neritic inshore/neritic inshore/neritic inshore inshore offshore offshore
Tursiops truncatus Delphinus delphis
SE Pacific (Peru) SE Pacific (Ecuador)
Free-ranging By -caught
inshore/neritic offshore/pelagic
Sotalia guianensis Phocoena phocoena Stenella coeruleoalba Cephalorhynchus hectori maui Cephalorhynchus eutropia Delphinus delphis Tursiops truncatus Phocoena phocoena Cephalorhynchus hectori
SW Atlantic (Brazil, Sepetiba Bay) NE Atlantic (UK) Mediterranean (Spain) SW Pacific (New Zealand) SE Pacific (Chile) NE Atlantic and North Sea (UK) Mediterranean (Spain) North Sea (UK) SW Pacific (New Zealand)
Free-ranging Stranded and by-caught By -caught and stranded By -caught and stranded Free-ranging Stranded By -caught and stranded Stranded and by-caught By -caught and stranded
inshore/neritic inshore/neritic offshore/oceanic inshore/neritic inshore/neritic offshore/neritic probably inshore inshore/neritic inshore/neritic
Tursiops truncatus Stenella coeruleoalba Lagenorhynchus obscurus Tursiops truncatus Delphinus capensis Phocoena spinipinnis
NE Atlantic (Portugal) NE Atlantic and North Sea (UK) SE Pacific (Peru) SE Pacific (Peru) SE Pacific (Peru) SE Pacific (Peru)
Free-ranging Stranded By -caught By -caught By -caught By -caught
inshore/estuarine offshore offshore/neritic offshore/oceanic offshore/neritic inshore/neritic
By-caught Stranded and by-caught (1) shot By -caught and stranded By -caught and stranded By -caught and stranded Free-ranging Free-ranging By-caught
Habitat
Sampling period 2000 1991-1995 1991-1995 1995 1989-2005 1988-2004 1992-1999 2000 2005-2006 2005 1984 2007 1990 2006
Suspected related environmental factor
2004-2006 1992 2005-2006
Directed and incidental fisheries, pollution By-catch Fisheries, boat strike, pollution
2004-2006 2000-2006 1997-2006 2003-2004 2004-2006 2000-2006 2004-2006 1997-2006
By-catch and pollution Unknown By-catch Aquaculture By-catch and pollution Unknown By-catch and pollution By-catch
168 72 41 13 13 25 8 39 63
1994-1997 2004-2006 1993-1994 1993-1994 1993-1994 1993-1994
Pollution Unknown Directed and incidental fisheries Fisheries Directed and incidental fisheries Directed and incidental fisheries, pollution
35 4 196 12 54 77
25 8 12 14 104 91 8 21 80 1 1 1 1 1
Table 1. Characteristics of samples of 1,285 odontocetes examined for the prevalence of tattoo skin disease worldwide. Nex= number of animals examined, prev= prevalence. a
prevalence is likely higher,
b
considering only dolphins with confirmed tattoo lesions.
Nex
70 27
Prev 0% 0% 0% 0% 0% 0% 0% 0% 0% unknown unknown unknown unknown unknown a 1.42% 3.7% a 4.1 6.9% 7.3% 7.7% 7.7% 11.1% 12.5% 12.8% 17.5% b 20% 25% 34.7% 41.6% 61.1% 62.3%
Status absent absent absent absent absent absent absent absent absent unknown unknown unknown unknown unknown unknown unknown possibly endemic endemic unknown endemic endemic endemic endemic endemic endemic endemic unknown endemic endemic endemic endemic
Geographic area Species, ocean province, cause of death
Immature Male
Female
significance
Mature Male
Female
significance
Spain Stenella coeruleoalba , Mediterraneana, stranded
8.3% (N= 11)
11.1% (N=12)
Fisher´s, P= 1
0%
0%
NR
United Kingdom Phocoena phocoena , NE Atlantic, traumatic death Phocoena phocoena , NE Atlantic, poor health Delphinus delphis , NE Atlantic, by-catch and stranded
0% (N= 7) 7.7% (N= 13) 0% (N= 8)
0% (N= 8) 14.3% (N= 14) 33.3% (N= 3)
NR Fisher´s, P= 1 NR
0% (N= 2) 33.3% (N= 3) 16.7% (N= 6)
0% (N= 6) 20% (N= 5) 10% (N= 10)
NR NR NR
Fisher´s, P= 1
14.3% (N= 21)
8.3% (N= 12)
Fisher´s, P= 1
New Zealand Cephalorhynchus hectori hectori (South Island), by-catch and stranded
38.5% (N= 13) 28.6% (N= 7)
Table 2. Sexual variation in prevalence of tattoo skin disease. a the MIM and immature categories were grouped.
Country and ocean province
MIM Nt
Npos
Prev
Immature Nt Npos
Prev
Mature Nt
Npos
Prev
Significance ontogenic variation
Spain, Mediterranean Stenella coeruleoalba, offshore, strandings
7
1
14.3%
16
1
6.3%
21
0
0%
Fisher's excluding NEO, P= 0,43
United Kingdom, North East Atlantic Phocoena phocoena (NE Atlantic, inshore)-traumatic death
4
0
0%
15
0
0%
8
0
0%
Phocoena phocoena (NE Atlantic, inshore)-poor health Phocoena phocoena (North Sea, inshore)-traumatic death Phocoena phocoena (North Sea, inshore)-poor health Delphinus delphis (NE Atlantic, offshore)-traumatic death Delphinus delphis (NE Atlantic, offshore)-poor health/strandings
7 1 6 1 1
0 0 0 0 0
0% 0% 0% 0% 0%
27 4 9 7 2
3 1 1 1 0
11.1% 25% 11.1% 14.3% 0%
8 5 12 10 6
2 0 3 0 2
25% 0% 25% 0% 33.3%
NR X2 = 2,27, df= 2, P= 0,32 NR NR Fisher's excluding NEO, P= 0,41 NR
Portugal, Sado estuary Tursiops truncatus (inshore), free-ranging
0
0
-
10
5
50%
25
2
8%
Fisher's, P= 0,013
New Zealand Cephalorhynchus hectori maui (North Island, inshore) Cephalorhynchus hectori hectori (South Island, inshore)
4 10
0 0
0% 0%
2 20
1 7
50% 35%
7 33
0 4
0% 12.1%
NR X2 = 7,03, df= 2, P= 0,03
Peru, Southeast Pacific Lagenorhynchus obscurus , neritic, bycatch Delphinus capensis , neritic, bycatch Tursiops truncatus , pelagic, bycatch Phocoena spinipinnis , coastal, females, bycatch Phocoena spinipinnis , coastal, males, bycatch
16 0 0 4 2
0 0 0 0 0
0% 0% 0%
69 44 6 9 22
35 32 5 5 18
50.7% 72.7% 83.3% 55.6% 81.8%
111 10 6 16 24
34 1 0 5 20
30.6% 10% 0% 31.3% 83.3%
X2 = 17, df= 2, P= 0,0002 Fisher's, P= 0,00042 NR Fisher's, P= 0,4 no difference in prevalence
Ecuador, Southeast Pacific Delphinus delphis , offshore, bycatch
13
0
0%
11
1
9.1%
3
0
0%
Table 3. Ontogenic, health and interspecific variation in prevalence of tattoo skin disease. Nt= total number of specimens, pos= number of positive cetaceans, prev= prevalence
Inshore Phocoena phocoena (NE Atlantic, UK)-all Phocoena phocoena (North Sea, UK)-all Phocoena spinipinnis (Peru) Cephalorhynchus hectori hectori (South Island, NZ) Tursiops truncatus (Portugal) Neritic Lagenorhynchus obscurus (Peru) Delphinus capensis (Peru) Offshore Stenella coeruleoalba (Mediterranean) Stenella coeruleoalba (UK) Delphinus delphis (UK)-all Delphinus delphis (Ecuador) Tursiops truncatus (Peru)
All but MIM Nt pos
Prev
Immature Nt pos
Prev
Mature Nt
60 31 71 53 35 250
5 5 48 11 7 76
8.3% 16.1% 67.6% 20.8% 20% 30,4%
44 14 31 20 10 119
3 2 23 7 5 40
6.8% 14.3% 74.2% 35% 50% 33.6%
16 17 40 33 25 131
2 3 25 4 2 36
12.5% 17.6% 62.5% 12.1% 25% 27.4%
180 54 234
69 33 102
38.3% 61.1% 43,6%
69 44 113
35 32 67
50.7% 72.7% 59.3%
111 10 121
34 1 35
30.6% 10% 28.9%
34 4 25 14 12 89
1 1 3 1 5 11
2.9% 25% 12% 7.1% 41.7% 12,3%
16 4 9 11 6 46
1 1 1 1 5 9
6,3% 25% 11,1% 9.1% 83.3% 19,6%
18
Table 4. Inter-specific and habitat variation in prevalence of tattoo skin disease. MIM= neonates and young calves, Nt= total number, pos, number of positive cetaceans, prev= prevalence.
16 3 6 43
pos
0 0 2
Prev
-
0 2
12.5% 4.7%
Minimal density of tattoos Immature
Mature
Topography of lesions All
Size of lesions Immature
Mature
Inshore Tursiops truncatus , Sado estuary, Portugal Phocoena phocoeana , NE Atlantic Phocoena phocoena , North Sea Cephalorhynchus hectori hectori , South Island Cephalorhynchus hectori maui , North Island Cephalorhynchus eutropia , Chile Phocoena spinipinnis , SE Pacific Sotalia guianensis , Sepetiba Bay, Brazil Total
N= 5, high (100%) N= 3, low (2) to high (1) N= 2, high
N=2, high (100%) N= 2, low (1) to high (1) N= 3, high
B, Fs, Ts, H H, Fs H, Fs, Ts, Belly, generalised
small to large small to large small to large
small to very large (1 of two positive) small to very large (1 case) small to large
ND N= 19, low (57.9%) to high (15.8%) ND N= 29, high (37.9%)
N=1, medium N= 23, low (43.5%) to high (34.8%) N= 7, low (71.4%) to medium (14.3%) N= 38, high (36,8%)
Back H, Fs, belly, back, flippers, Ts B, Dorsal, Head
ND small to large ND
medium small to very large small to large
Neritic Lagenorhynchus obscurus , Peru Delphinus capensis , Peru Total
N= 33, low (81,2%) to high (6,1%) N= 27, low (33.3%) to high (55.5%) N= 60, high (28.3%)
N= 47, low (85%) to high (4,3%) N=1, low N= 48, high (4.1%)
Fs, H, B, flippers, throat, Ts everywhere
small to large small to large
small to very large (1 case) unknown-likely small to medium
Offshore Stenella coeruleoalba , Mediterranean Stenella coeruleoalba, NE Atlantic Delphinus delphis , NE Atlantic Tursiops truncatus , Peru Total
N=1, medium (1) N= 1, high N= 1, high N= 4, low (2) to medium (2) N= 7, high (28,6%)
NOB NOB N= 2, low NOB
Head, body H, B Flanks and Rob and Paul, please complete H, Belly, sides, Flippers
small to large
NOB
small small to medium
small to large NOB
Table 5. Characteristics of TSD in different species and populations of small cetaceans worldwide. Abbreviations are: MD= minimal density; F(s)= flank(s), D= dorsal fin, B= back, H= head, Ts= tailstock, ND= no data, NOB= not observed