Epidemiology of tattoo skin disease in cetaceans worldwide: a general health indicator for
cetacean and their environment
3 4 5 6 7 8 9
Marie-Françoise Van Bressem1, Koen Van Waerebeek1, Juan Antonio Raga2, Paul Jepson3, Padraig Duignan4, Rob
Deaville3, Leonardo Flach5, Francisco Viddi6, John Baker7, Ana Paula Di Beneditto8, Mónica Echegaray9, Tilen
Genov10, Julio Reyes9, Fernando Felix11, Raquel Gaspar12, Renata Ramos13, Vic Peddemors14 and Ursula Siebert15
12 13 14 15 16
Cetacean Conservation Medicine Group (CMED), CEPEC, Museo de Delfines, Pucusana, Peru;
Marine Zoology Unit, Cavanilles Institute of Biodiversity and Evolutionary Biology, University of Valencia, P.O.
Box 22085, 46071 Valencia, Spain;
National Disease Control Centre, Level 1E, Agriculture House, Dublin 2, Ireland;
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
Universidade Estadual do Norte Fluminense-CBB, Laboratório de Ciências Ambientais, Av. A. Lamego, 2000-
Campo dos Goytacazes, RJ 28013-602, Brazil;
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,
Everest, Av. Nossa Senhora dos Navegantes, 675/1201, Enseada do Suá, Vitória, ES, 29056-900, Brazil;
Graduate School of the Environment, Macquarie University, Sydney, NSW 2109, Australia;
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
38 39 40 41
In cetaceans tattoo skin disease (TSD) is characterised by very typical, irregular, grey, black or yellowish, stippled
lesions (Figure 1) that may occur on any part of the body but show a preferential corporal distribution depending on
the species (Van Bressem & Van Waerebeek, 1996). With some practice, tattoos are easily distinguished visually
from other types of integument blemishes and scars. The disease has been observed in several species of free-
ranging odontocetes from the North Atlantic and East Pacific Oceans and in the Mediterranean Sea, as well as in
captive bottlenose dolphins (Tursiops truncatus) (see Van Bressem et al. 1999). It was also recently reported in a
bowhead whale (Balaena mysticetus) though no pictures of the lesions were provided (Bracht et al. 2006). TSD is
caused by poxviruses (Flom & Houk 1979, Geraci et al. 1979, Van Bressem et al. 1993, 2006) that belong to a new
genus of Chordopoxvirinae, but have a common, most immediate ancestor with terrestrial poxviruses of the genus
Orthopoxvirus (Bracht et al. 2006, Pearce et al. submitted). These viruses are thought to induce humoral immunity
that protects neonates and young calves from the disease (Smith et al. 1983, Van Bressem & Van Waerebeek 1996,
Van Bressem et al. 2006). Individual tattoo lesions may persist for months an even years and recurrence may occur
(Van Bressem et al. 2003). They eventually heal and convert into light gray marks (G-marks) that may or may not
have a darker outline and a darker center (Van Bressem et al. 2003).
Though clinical and epizootiological data do not indicate that poxvirus infection induces a high mortality rate when
enzootic (Van Bressem & Van Waerebeek 1996, Van Bressem et al. 2003), it may kill neonates and calves without
protective immunity and thus affects host population dynamics. TSD may also have contributed to the decline of
bottlenose dolphins from the Sado Estuary, Portugal, through affecting juvenile survival (Van Bressem et al. 2003).
Besides, the presence of very large tattoo lesions and their persistence (over 3 years) in adult bottlenose dolphins
may indicate immune deficiencies related to environmental contaminants (Van Bressem et al. 2003). In search of
the potential for anthropogenic factors to influence the prevalence of tattoo disease, we started in 1995 a worldwide
survey on the epidemiology and ecology of TSD. Here we present the results of this study.
MATERIAL AND METHODS
The presence of TSD was examined in 1,285 live, free-ranging and dead small cetaceans originating from the South
Pacific, the Southwest and North Atlantic as well as from the North, Baltic, Mediterranean and Tasmanian Seas
(Table 1). We include in this paper previously published data on the epidemiology of TSD in Peruvian small
cetaceans and bottlenose dolphins (Tursiops truncatus) from the Sado Estuary, Portugal (Van Bressem & Van
Waerebeek 1996, Van Bressem et al. 2003).
Freshly dead specimens The majority of dead cetaceans had died in nets or stranded in the period 1984-2007
(Table 1). Thus, condition varied from alive to early decomposed (but with mostly intact skin). The whole body
surface was examined for the presence of tattoos. Several specimens were frozen before examination. Sexual
maturity was determined directly from an examination of gonads and lactation or was inferred from standard body
length and known life history parameters for these populations (Collet & Saint Girons 1984, Van Waerebeek 1992,
Calzada 1995, Lockyer 1995, Reyes & Van Waerebeek 1995, Padraig: please add reference). When sexual maturity
status could not be determined directly, it was inferred from the standard body length. Van Waerebeek (1992)
estimated that 50% of Peruvian dusky dolphins L. obscurus in both sexes attain sexual maturity at 175 cm. Female
and male Burmeisterâ€™s porpoises P. spinipinnis reach sexual maturity on average at 155cm and 160cm, respectively
(Reyes & Van Waerebeek 1995). Female and male Mediterranean striped (Stenella coeruleoalba) dolphins larger
than 187 cm and 190 cm, respectively, are considered sexually mature, more than 11 years old (Calzada 1995). The
age of some animals was determined by standard techniques (Perrin & Myrick 1980; Hohn et al. 1989).
Free-ranging dolphins Detection of tattoos in free-ranging bottlenose dolphins from Slovaquia, Portugal and Peru,
estuarine dolphins (Sotalia guianensis) from Brazil and Chilean dolphins (Cephalorhynchus eutropia) from the
northern Patagonia was done by examining photographic records taken during small-boat surveys (Reyes et al.
2002, Van Bressem et al. 2003, Flach 2006, Viddi et al. 2005). Considering that in these animals generally only
upper body parts were visible, the reported prevalence levels should be considered minimum values. Dolphins were
individually identified from natural marks (WĂźrsig & Jefferson 1990). Maturity (calf, juvenile, adult) was estimated
from relative body size and behavioural clues (Wells et al. 1980, Shane 1990; others).
Tattoos. Tattoo lesions were identified on the basis of their typical appearance, i.e. irregular, dark gray, black or
yellowish marks with a stippled pattern (Figure 1). The topography of these marks as well as their size (small,
medium, large and very large) relative to the body of the dolphins were registered. The number of lesions per body
area was noted and their minimum density (MD; minimum number of lesions per animal) was recorded as low (1 to
5 lesions), medium (6 to 10) or high (>10). Light gray, irregular marks surrounded by a black line were considered
regressing tattoos (Figure 2). Light gray, rounded irregular marks without a dark outline were regarded as healed
lesions (Figure 3). In this study we included only animals that were examined by the authors to avoid biases related
to investigators. First author examined pictures of tattoo lesions in most of the cases to confirm their identity. Only
true tattoos (including regressing ones but not healed tattoos) were considered for the statistical analysis.
Sexual, ontogenetic and health variation in TSD prevalence
As harbour porpoises from the North Sea are considered a population distinct from porpoises in NW Scottish, Irish
and western British waters and the Celtic shelf (Donovan & BjĂ¸rge 1995), we divided porpoises from the United
Kingdom in two samples: the North Sea and NE Atlantic. The latter includes the English Channel, the Irish and
Celtic Seas. D. delphis from the waters of the United Kingdom are thought to belong to one population (Murphy et
al. 2006). We further split the porpoises and common dolphin samples into individuals that died a traumatic death
(fisheries, T. truncatus attack) and those that died in poor health (i.e. starvation, high parasite burden, bacterial and
fungal infections). For all species, with sample sizes permitting, we examined whether TSD prevalence varied with
sex and sexual maturity as a proxy for age. We divided species and populations into three age classes: (1) MIM: a
class including neonates and young calves likely protected by maternal immunity in populations where the virus is
endemic, (2) juveniles: older calves and subadults, specimens likely not protected any more by passive immunity
and susceptible to TSD and (3) adults, sexually mature animals that may have active immunity against the virus.
Very little is known of the duration of passive immunity against TSD or any other viruses in cetaceans. Results of a
previous study (Van Bressem and Van Waerebeek, 1996) suggested that Peruvian L. obscurus and P. spinipinnis till
145 cm and 140 cm, respectively, were protected by maternal immunity. Tattoo-like lesions were first seen in 9 and
14 months old calf T. truncatus from the Sado estuary, Portugal (Van Bressem et al. 2003). These observations,
age-growth data and unpublished observations by the authors suggest that passive immunity in these species last at
least till the six or nine first months of life. This is congruent with data on maternal immunity to lumpy skin disease
virus (a capripoxvirus) in large artiodactyls (Weiss 1968), phylogenetically related to cetaceans (Gatesy et al. 1999,
Milinkovitch et al. 1998). Thus, we include in the first group, small cetaceans considered less than less than 6-9
months old: harbour porpoises smaller than 105.5 cm, striped dolphins smaller than 120 cm, Hector´s dolphins less
than *** (Padraig please complete), South American D. delphis smaller than (Fernando please complete), L.
obscurus less than 140 cm and P. spinipinnis smaller than 130 cm.
Interspecific and habitat variation in TSD prevalence
We examined inter-specific variation in MIM, juvenile and mature age categories in species with a sufficiently
large sample size in six ocean provinces: Peruvian small cetaceans, harbour porpoises and common dolphins from
European waters (north Sea and NE Atlantic), Hector’s dolphins (Cephalorhynchus hectori), Mediterranean striped
dolphins, bottlenose dolphins from the Sado Estuary (Portugal) and short-beaked common dolphins from the coast
of Ecuador. We further examined variation in prevalence between adults of different species occupying an explicit
inshore, offshore-neritic and offshore-oceanic habitat. Finally, we compared the characteristics of the disease
(minimal density of lesions, size and topography) in the inshore, neritic and offshore groups. Prevalence refers to
the number of positive specimens in samples and sub-samples at the time of examination, without distinction
between old and new cases (Thrusfield, 1986). Significance of differences in prevalence (≤ 0.05) was verified with
chi-square contingency tests or 2-tailed Fisher’s exact tests (Swinscow, 1981).
139 140 141
Distribution. We detected TSD in Delphinidae, Phocoenidae and Ziphiidae from the South and Northeast Pacific,
Southwest and North Atlantic as well as from the North, Tasmanian and Mediterranean Seas (Table 1). When
present in a population, prevalence of TSD varied from 1.4% to 62.3%, according to the species, populations and
ocean provinces (Table 1). The highest prevalence levels were recorded in P. spinipinnis and D. capensis from Peru
(Table 1). We consider that TSD is endemic in all species and populations where prevalence is above 5% and where
the disease was observed for several years (Table 1).
Sexual, ontogenic and health variation. With the exception of Burmeister´s porpoises from Peru, prevalence did
not vary with sex in all species and populations for which a sufficient number of individuals were examined (Table
2). Thus, sexes were pooled for subsequent analyses. Among cetaceans hat had died a traumatic death (caught in
nets, shot, attacked by bottlenose dolphins) as well as free-ranging T. truncatus from the Sado estuary, prevalence
varied with the age class, being null in the MIM group with the exception of Mediterranean S. coeruleoalba,
peaking among sexually immature and then decreasing in adults (Table 3). Significance of this variation varied with
the species and populations sampled (Table 3). On the opposite, prevalence increased in adult common dolphins
and adult harbour porpoises from the UK that had died in poor health though this variation was not significant in
the porpoises (2-tailed Fisher’s, NE Atlantic: P= 0,142, North Sea: P= 1) and could not be tested in the common
dolphins (Table 3). In the NE Atlantic prevalence of TSD was higher in P. phocoena of the poor health category
that in those of the trauma category though significance of these results was borderline (χ2= 3,59, df=1, P= 0,058).
Prevalence of TSD in adult P. phocoena and D. delphis belonging to the trauma category was null while it varied
between 25-33.3% in the poor health category, a highly significative (χ2= 7,25, df=1, P= 0,007) difference. In P.
spinipinnis, prevalence remained high in adults and was significantly higher in adult and juvenile males than in
females from the corresponding age categories (Van Bressem & Van Waerebeek 1996). Besides, in this species a 5
high density of lesions was only seen in males (2-tailed Fisher’s, P= 0,06) and prevalence of this condition
increased in adults (44,4%, N= 18 versus 21,4%, N= 14) though not significantly (2-tailed Fisher’s, P= 0,32). In the
MIM group, TSD was only seen in a 100cm male calf Mediterranean S. coeruleoalba that had a medium density of
small lesions on the melon (Figure 2).
Inter-specific and habitat variation. When the age and health status categories were considered, TSD prevalence
was exactly the same in both P. phocoena populations (NE Atlantic and North Sea) from UK coastal waters (Table
4). Among immatures, TSD prevalence was significantly (χ2= 5,38, df=1, P= 0,02) higher in D. capensis than in L.
obscurus from Peruvian neritic waters. However, there was no significant prevalence variation among adults from
these species (χ2= 1,88, df=1, P= 0,17). Prevalence of TSD varied very significantly (χ2= 29,8, df= 2, P< 0,001)
between inshore, neritic and offshore species, being high in the first two categories and low in the offshore (Table
4). In inshore dolphins and porpoises, prevalence remained high in adults while it significantly decreased in adult
neritic (χ2= 21,91, df= 1, P< 0,001) and offshore (χ2=4,55, df= 1, P = 0,03) cetaceans. A similar pattern was
observed with the density of tattoo lesions. Prevalence of this condition was high in immature coastal, neritic and
offshore cetaceans. It then lowered significantly (χ2= 10,73, df=1, P= 0,001) in adult neritic dolphins but stayed
high in coastal odontocetes (Table 5). Coastal adults had a very significantly (χ2= 14,95, df= 1, P= 0,0001) higher
prevalence of high tattoo density than neritic adults. Besides, very large lesions (Figure 4) were only seen in coastal
(3) and neritic (1) adults (Table 5).
During this study we examined the presence and prevalence of TSD in several cetacean species and populations
worldwide (Table 1). The disease was observed in 11 (check) species from the Atlantic and Pacific Oceans as well
as from the North, Mediterranean and Tasmanian seas. Prevalence was likely more accurately determined in by-
caught specimens as the whole body could be examined and there was no health bias as in stranded specimen. The
higher prevalence levels (34.7%-62.3%) were observed in dolphins and porpoises caught off Peru in 1993-1994,
followed by free-ranging T. truncatus (20%) that inhabited the Sado estuary (Portugal) in 1994-1997. The visual
diagnostic of tattoo skin disease and subsequent poxvirus infection was confirmed by electron microscopy and/or
polymerase chain reaction in harbour porpoises and a striped dolphin from the UK (Pearce et al. submitted) and
Peruvian small cetaceans (Van Bressem et al. 1993, Van Bressem & Van Waerebek 1996).
With the exception of P. spinpinnis (Van Bressem & Van Waerebeek, 1996), there was no significant sexual
variation in TSD prevalence within the species and populations studied. Neonates and young calves were very
rarely infected, presumably because protected by maternal immunity. Again with the exception of P. spinipinnis
prevalence of the disease was lower in mature than in immature specimens in all species and populations that
suffered a traumatic death. Though significance of this variation varied, this likely reflects that in these populations,
the virus infects calves no longer protected by maternal immunity, provokes TSD and is then progressively cleared
in adults as described in Peruvian Delphinidae (Van Bressem & Van Waerebeek 1996). A different epidemiological
pattern of TSD (i.e. higher prevalence levels of TSD in adults than in immature) was observed in P. phocoena and
D. delphis that died in poor health along the coast of the United Kingdom. Prevalence of TSD in poor health
porpoises from the NE Atlantic was also almost significantly higher than in the trauma group congruent with
observations from the UK co-authors over a period of (10?, Paul and Rob do you agree?) years and those from
Geraci et al. (1979) who reported that in captive dolphins the development of TSD was linked to general health.
Significantly, none of the adult P. phocoena and D. delphis from the trauma group had tattoos while at least a
quarter of those from the poor health group were affected. These findings suggest that adult small cetaceans that
stranded in poor health in the UK had a depressed immune system and could not adequately fight infections. High
exposure to polychlorinated biphenyls (PCBs) was previously shown to increase the risk of mortality from
infectious diseases in P. phocoena from the UK (Jepson et al. 2005, Hall et al. 2006).
To examine the significance of habitat variations we compared TSD prevalence levels as well as prevalence of high
tattoo density in coastal, neritic and offshore cetaceans, split into mature and immature (excluding MIM) groups.
Prevalence of TSD varied very significantly between inshore, neritic and offshore species, being high in the first
two categories and low in the offshore. Besides, prevalence of TSD did not vary significantly between adults and
immature in the inshore while it decreased significantly in the adult neritic and offshore specimens. Among adults,
prevalence of a high tattoo density was significantly higher in the inshore than in neritic cetaceans and prevalence
of this condition remained high in coastal adult cetaceans. These results strongly suggest than the immune response
of coastal cetaceans and their subsequent ability to clear the virus and limit its dissemination is compromised.
Environmental contaminants including PCBs, dibenzo-p-dioxins (PCDDs), dibenzofurans (PCDFs) and related
compounds have been repeatedly shown to affect the efficiency of the immune response in marine mammals and
represent a factor facilitating infectious diseases (De Swart et al., 1996, Ross et al. 1996, De Guise et al. 1998, Hall
2002, Ross 2002, Jepson et al. 2005, Hall et al. 2006). Adults, and especially males, accumulate these lipophilic
contaminants and thus may be more susceptible to infectious diseases (Aguilar et al. 1999, Ross et al. 1996). This is
congruent with our observations in P. spininpinnis where prevalence of TSD was significantly higher in males than
in females and where only males had a high tattoo density. Agricultural, mining and industrial activities in South
America are thought to have released vast amounts of contaminants into the marine environment (Borrell & Aguilar
1999). Sewage of various origins is still discharged, mostly untreated, in the coastal waters of Peru
(PNUMA/CONAM 2006, Van Waerebeek, Van Bressem, Reyes and Echegaray, own observations). High levels of
contaminants have been regularly reported in P. phocoena from the North Atlantic (Aguilar & Borrell 1995, Smyth
et al. 2000, Aguilar et al. 2002) and recent studies have indicated that an increased exposure to polychlorinated
biphenyls (PCBs) is associated with a higher risk of infectious diseases in this species (Jepson et al. 1999, 2005,
Hall et al. 2006). The Sado estuary suffers from eutrophication and pollution from mining, industrial and
agricultural activities as well as from domestic sewage (Harzen 1995, Ferreira et al. 1989, Bruxelas et al. 1992) and
high levels of PCB and heavy metal contamination have been registered in these waters (Caeiro et al. 2005).
Padraig: could you please write a line on the contamination of the waters where C. hectori live? Thank you.
The very high TSD prevalence levels (over 30%) seen in immature Peruvian small cetaceans and Hectorâ€™s dolphins
may be related to the stress caused by incidental and direct captures. Acute capture-related stress may result in
widespread damage to the circulatory system and kidneys (Cowan & Curry 2002) and in alteration of the immune
response through increase of the cortisol level and modification of the cytokine pattern (Fonfara et al. 2007).
Chronic stress associated with high levels of fishery mortality and concomitant repeated disruption of the herd
structure may lead to structural changes in the adrenals that may result in the secretion of more stress hormones, as
described in T. truncatus (Clark et al. 2006). These in turn may depress the immune system, increase the
susceptibility to infectious diseases and diminish the individual potential to clear the infection, as described in other
mammals (Biondi & Zannino 1997, Marsland et al. 2002).
Results of the present study strongly suggest that the epidemiological pattern of TSD may be an indicator of a
degrading and stressful aquatic environment. A high prevalence of TSD in adult cetacean populations as well as the
presence of large lesions may be indicative of serious health threats. Further research should include correlation
between the presence, density and size of tattoo lesions with data on blubber concentration of PCB congeners in
each specimen as well as on the morphology of the adrenal glands and cytokine pattern. Coastal cetaceans suffering
capture-related stress and living in a contaminated environemnent as is the case of Peruvian P. spinipinnis very
likely have serious problems to develop an adequate immune response against infectious agents.
ACKNOWLEDGMENTS (co-authors, please any person or institute you wish to acknowledge. Thank you)
We kindly thank Celia Agusti and Patricia Gozalbes for their help in processing the data collected in Mediterranean
cetaceans, Dr RJ Monies for providing the picture of a giant tattoo in P. phocoena from the UK, Dr Sequeira for the
picture of an infected D. delphis from Portugal, Dr Crespo for the pictures of tattoo lesions in C. commersonnii, Dr
Jorgensen for allowing us to examine the P. phocoena collected by his institute and Dr Pearce for the PCR data.
This study was supported by the Cetacean Society International, the Whale and Dolphin Conservation Society, the
‘Fundação para a Ciência e Tecnologia’ from the Portuguese Ministry of Science and Technology, the ‘Reserva
Natural do Estuário do Sado’, the ‘Conselleria de Medio Ambiente de la Generalitat Valenciana’, the ‘Ministerio de
Medio Ambiente’, Spain and the Federal Ministry for Education and Research, Germany. CEPEC field research
was supported by several grants from the Gesellschaft zum Schutz der Meeressäugetiere, Leopold III Fund for
Nature Research and Conservation, IFAW, IUCN Cetacean Specialist Group and the Chicago Zoological Society.
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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)
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
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
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,
considering only dolphins with confirmed tattoo lesions.
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
Spain Stenella coeruleoalba , Mediterraneana, stranded
8.3% (N= 11)
Fisher´s, P= 1
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
Immature Nt Npos
Significance ontogenic variation
Spain, Mediterranean Stenella coeruleoalba, offshore, strandings
Fisher's excluding NEO, P= 0,43
United Kingdom, North East Atlantic Phocoena phocoena (NE Atlantic, inshore)-traumatic death
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
Fisher's, P= 0,013
New Zealand Cephalorhynchus hectori maui (North Island, inshore) Cephalorhynchus hectori hectori (South Island, inshore)
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
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
Immature Nt pos
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%
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
0 0 2
Minimal density of tattoos Immature
Topography of lesions All
Size of lesions Immature
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
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