the striped dolphin epizootic in the mediterranean sea

Royal Swedish Academy of Sciences

The Striped Dolphin Epizootic in the Mediterranean SeaAuthor(s): Alex Aguilar and J. Antonio RagaSource: Ambio, Vol. 22, No. 8 (Dec., 1993), pp. 524-528Published by: Springer on behalf of Royal Swedish Academy of SciencesStable URL: http://www.jstor.org/stable/4314142 .

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Article Alex Aguilar and J. Antonio Raga

The Striped Dolphin Epizootic in the Mediterranean Sea

From 1990 to 1992, an epizootic produced a massive die- off of striped dolphins in the Mediterranean Sea. The event started in mid-Spain but extended, through three apparently interconnected outbreaks, to finally coverthe whole western Mediterranean and the Tyrrhenian and Aegean Seas. Although more than 1000 carcasses of striped dolphins were collected during the event, the total toll remains unknown because of fragmentary coverage of rescue networks and because many carcasses never reached the shore. The primary cause of the episode was identified as an infection by a morbillivirus, the origin of which could not be ascertained. The dolphins affected were found to carry concentrations of pollutants higher than normal for the general population. This difference could not be explained by variation in nutritive condition or by sex or age composition. The dolphins that died at the beginning of the outbreak were in abnormally poor nutritional condition, and had increased prevalence of ectoparasites and epizoits. This suggested that these dolphins had recently undergone a period of restricted mobility, during which the ectoparasites had found attachment easier than under normal conditions. Abnormal weatherconditions, leading to depressed marine productivity, may have been the cause of some of these anomalies.

INTRODUCTION Beginning in July 1990 and extending through 1991 and 1992, an epizootic of complex origin and development produced a massive dolphin die-off in the Mediterranean Sea. The only species so far reported to have been affected by the epizootic is the striped dolphin, Stenella coeruleoalba (1), which is by far the most common cetacean in the Mediterranean Sea. In the western Mediterranean, strandings of this species represent about 60% of the total cetacean strandings (2) and, according to Marchessaux (3), the species is also very common in the eastern Mediterranean basin.

The striped dolphin, a cetacean (maximum body length of about 220 cm), inhabits offshore waters and is never found closer than about 10 miles from the coast. The population inhabiting Mediterranean waters is thought to be independent of that in the Atlantic Ocean, although some limited exchange of individuals is likely to occur through the Straits of Gibraltar (4). The dolphin is a social species and typically forms large schools of dozens of individuals. The diet of striped dolphins in the Mediterranean is based on a variety of cephalopod and fish species, many of which are exploited commercially (5).

DEVELOPMENT OF THE EPIZOOTIC The first dolphins affected by the epizootic were detected, moribund or dead, in the vicinity of Valencia (mid-Spain) at the beginning of July 1990. During the first weeks only isolated cases were

observed and the extent of the mortality was not detected until mid-August, when its virulence rose substantially. This delayed the launching of a network to collect diseased dolphins and made the information from the initial phases of the epizootic highly fragmentary.

The epizootic soon extended to other regions. In August, the first cases of affected dolphins were detected in Catalonia, the Balearic Islands and southeastern Spain and, by the end of Oc- tober, nearly 400 striped dolphin carcasses had been collected along the Spanish coasts (6). The highest mortality on the Span- ish coasts as a whole occurred during the period August to Oc- tober. Later, the frequency of dolphins being washed ashore decreased in the areas where the epizootic first occurred, but extended rapidly to the North, reaching the French coast at the end of September. In France, the peak of mortality was reached in October (7) and, approximately at the same time, affected dolphins began to appear in Italy (M. Podest'a, pers. comm.).

The epizootic extended more slowly southwards, but the coasts of southern Spain were affected from September to No- vember. However, it is difficult to determine the severity of the mortality in this area because of the long-standing conflict between small cetaceans and local fisheries, which produced a mortality that masked that originated by the epizootic. This can be clearly seen in the stranding reports from the area, in which at least 20% of the specimens examined presented characteristic signs, such as wounds produced by hooks or cuts in flippers or tail flukes, i.e. signs of having been freed from nets (6). At the end of 1990, some cases were also reported on the Atlantic side of the Straits of Gibraltar.

The information about the epizootic available from northern Africa is very fragmentary, but it is known that many striped dolphins were washed ashore on the beaches of Morocco from September to November. Apparently, the coasts of Algeria were only slightly affected by the epizootic, although it is likely that the small number of stranding reports in that area is more a consequence of the lack of a monitoring network than of a lower severity of the epizootic in the region.

When temperatures decreased in November, the number of dolphins affected by the epizootic and being washed ashore throughout the region diminished strikingly, although diseased animals continued to appear sporadically along the coastline throughout the winter of 1990/91.

Between June and September 1991, the epizootic broke out again, this time in southern Italy. As with the first outbreak, this also rapidly extended through the southern Adriatic coast and the Ionian Sea, and to a lesser extent to the Sicilian Channel and the southern Tyrrhenian Sea (8). The western fringe of the Greek Archipelago was also affected (9), but the information available from that area is extremely fragmentary and the time period during which the epizootic affected the area cannot be established with precision. In spring 1992, a third outburst was initi- ated in the central region of the Greek islands and apparently extended to the East and Northeast. Again, the information about

524 AMIBIO VOL. 22 NO. 8, DEC. 1993



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The striped dolphin (Stenella coeruleoalba) was the only species affected by the epizootic. About one third of the specimens were alive when they reached the shore but all died a few hours later. Photo: A. Aguilar.

the timing and mortality involved in this third phase is extremely scarce.

Although the 1991 and 1992 outbreaks were very poorly monitored compared with that of 1990, the toll was also quite high and the causative agents were apparently identical (10), and for this reason these outbreaks have been considered to be a continuation of the 1990 one. Figure 1 shows the areas known to be affected during each outbreak.

From specimens collected in Spain it would seem that the animals most affected by the die-off were those between 11 and 20-years old (11). However, the mortality rate of neonates and calves was also high, apparently not as a direct result of the disease, but because of the death of the lactating females on which they were dependent. This mortality was substantially increased by the fact that the most severe phases of both outbreaks coincided with calving and the beginning of the lactation period (12).

EXTENT OF THE MORTALITY During the epizootic, especially in the early phases, many dolphins reaching the coast were still alive. Although attempts were made to revive these animals, all efforts failed and they inevitably died.

Table 1 details the number of carcasses of striped dolphins collected along the coasts of Spain, France and Italy during the 1990 and 1991 outbreaks. The minimum total was 1107 dead dolphins, but the true number of casualties produced by the

epizootic in the Mediterranean population of striped dolphins is impossible to determine and the figures represent only a small fraction of the actual toll. There are at least two reasons for this.

First, flights carried out by coastguard helicopters in Spanish waters, cruises made in Spanish and French waters by boats from cooperating institutions (6), and reports provided by fishing boats and yachts cruising offshore waters throughout the affected areas during the epizootic, revealed that only a small proportion of the dead dolphins finally reached the shore and were included in the statistics (6, 13). This can be explained by the normal distribution of the striped dolphins, with the highest population densities being located in open, very distant waters (14). For this reason, it is difficult to give even an order of magnitude for the number of striped dolphin casualties off the Mediterranean coasts of Europe, although mortality can be estimated at several thousand individuals.

Second, the network for reporting stranded dolphins worked only fairly efficiently in Spain, France and Italy. The information available from the northern coast of Africa and the coasts of Greece is highly fragmentary and does not reflect the scale that the die-off reached in these areas. For example, about 30 dolphins were reported to have been washed ashore in Ceuta and Melilla, two small Spanish enclaves situated on the coast of Morocco which encompass less than 20 km of coastline, but the number of striped dolphins stranded along the nearly 400 km of adjacent Moroccan coastline is still unknown.

Figure 1. Areas affected by the different epizootic outbreaks.

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Unfortunately, there are no reliable data on the number of striped dolphins in the western Mediterranean basin before the outbreak of the epizootic. Consequently, even if the true number of deaths the event produced was known, it would still not be possible to establish the impact it had on the total population.

Surveys in the field carried out by the Greenpeace ship Sirius and coastguard helicopters used by the Spanish Institute for the Conservation of Nature (ICONA) during the most severe phase of the first outbreak in Spanish and French waters, suggest that the size of striped dolphin schools decreased to about one third of the normal level for the area. Thus, before the epizootic started, 70% of the dolphin schools were composed fromI to 20 individuals, and large aggregations (more than 50 individuals) were not unusual. However, at the peak of the 1990 mortality, 70% of the schools observed contained only 1 to 5 dolphins and large schools were practically nonexistent (6, 13).

However, these results cannot be taken as an indication that the striped dolphin population was reduced to a third of its original abundance. The number of observations made during the epizootic were limited and, more importantly, most of them were restricted to the area around the Balearic Islands, north- eastern Spain and the Gulf of Lions, the region that apparently suffered the greatest mortality. For this reason the demographic changes observed in that area cannot be extrapolated to the whole range of the striped dolphin in the Mediterranean and, therefore, it is impossible to ascertain the percentage of the population that was lost because of the epizootic.

In August 1991, almost one year after the first, most virulent outburst of the epizootic, the mean size of the striped dolphin schools in the western Mediterranean was again very similar to that reported before the onset of the event (14). However, given the short time period since the die-off, this apparent return to normality can probably be explained, not by a recovery of the population, but by a regrouping of the survivors into a smaller number of schools of pre-epizootic size. This plasticity in social structure makes it difficult to evaluate the actual impact of the epizootic on the total population as well as its response to a reduction in abundance. The striped dolphin population in the western Mediterranean that survived the 1990 outbreak has, however, recently been estimated at about 225 000 individuals (14).

CAUSES OF THE EPIZOOTIC AND ASSOCIATED FACTORS Epizootics in cetaceans were unknown until 1987, when massive mortality of bottlenose dolphins (Tursiops truncatus) occurred off the Atlantic coasts of the United States. Since then, at least four major mortalities of small odontocetes (15-18) and one of mysticetes (19) are known to have occurred, all of them in regions heavily affected by human activities. The causative agents of these events in marine mammals have often remained unidentified, although interaction of infectious diseases and environmental alterations, such as abnormally warm weather and heavy pollution, have been suggested (20-22).

In the Mediterranean epizootic, the proximate cause of the dolphins' mortality was identified as an infection produced by a morbillivirus similar to that producing distemper in carnivores (23, 24). Before the Mediterranean outbreak, morbillivirus infections had been reported to be responsible for at least two main marine mammal epizootics, one causing the death of about 17 000 northern European harbor seals (Phoca vitulina) in 1987 and 1988 (25-27), and another affecting Baikal seals (Phoca sibirica) in 1988 (28). It has been suggested that the northern European infection originated in the harp seal population inhabiting the northern fringe of the North Atlantic and the Barents Sea, i.e. populations that have been exposed to morbillivirus since at least 1985 apparently with low morbidity (29, 30). In

cetaceans, morbillivirus had only been isolated in the past from tissues of harbor porpoises (Phocoena phocoena) stranded in the Irish Sea (31), but had not previously been identified as a significant cause of mortality.

In the Mediterranean striped dolphins, the morbillivirus infection produced bronchiolo-interstitial pneumonia, nonsup- purative meningoencephalitis, lymphoid depletion and necrosis of lymphocytes in spleen and lymph nodes, and formation of multinucleate syncytia in the cortex of lymph nodes (32-34). These lesions were all similar to those caused by morbillivirus in seals and porpoises (35, 36), and in the dolphins led to partial collapse of lungs, subsequent respiratory insufficiency, and fre- quent nervous and locomotory disorders.

The origin of the morbillivirus responsible for the Mediteffa- nean striped dolphin epizootic has not been ascertained. Recent studies on the antigenic properties of this virus (10, 33) suggest that it was very similar, if not identical, to that isolated from common porpoises from the Irish Sea, but distinct from the one that caused the 1987 harbor seal epizootic. However, if the Mediterranean event originated from that population of common porpoises it is unclear how the virus reached the western Medi- terranean striped dolphins without affecting the dense population of the same species which inhabits the Atlantic waters off the Iberian Peninsula and the Alboran Sea. Nor is it known whether the Mediterranean population of striped dolphin had been exposed to morbillivirus in the past. Unfortunately, no blood samples from individuals of this population sampled before the event are available to check for viral antibodies.

On the other hand, the striped dolphins affected by the 1990 epizootic in the western Mediterranean showed a number of physiological and health-related alterations that could not be adequately explained by the action of the morbillivirus, and it has been suggested that these indicate the contribution of nonin- fectious agents to the development of the epizootic.

Thus, the diseased dolphins examined in 1990 in the western Mediterranean were found to carry concentrations of organochlorine pollutants, in particular polychlorinated biphenyls (PCBs) that were between two and three times the levels com- monly found in the healthy population, according to free ranging individuals sampled with biopsy darts before (1987, 1988 and 1989) and after (1 99 1) the 1990 outbreak (37, 38). Thus, the median concentration of PCBs in dolphins considered to be healthy was 282 ppm lipid basis, while that in dolphins killed by the epizootic was 778 ppm lipid basis. The difference in organochlorine concentrations between the two sample groups was found to be highly significant according to a Kruskal-Wallis test (p < 0.00 1), and could not be explained by variation in the nutritive condition of the specimens analyzed, or by the sex or age composition of the sample (38).

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526 AMBIO VOL. 22 NO. 8, DEC. 1993



The total number of casualties produced by the epizootic could not be determined because many carcasses never reached the shore. Photo: A. Aguilar.

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Among other effects, PCBs are active depressors of the immune system of mammals (39-42) and increase the susceptibil- ity of the affected individual to infections. Because of this, it has been suggested that PCBs might have played a role in previous dolphin epizootics (43, 44).

PCBs are very abundant in the Mediterranean and it has long been recognized that the striped dolphin population inhabiting this sea has carried extremely high levels of these pollutants for, at least, the two last decades (45). The PCB levels detected in 1991 in apparently healthy dolphins-presumably survivors of the epizootic-were similar to those found in the three years previous to the event (38). Given the fact that these compounds appear to be fairly stable once they are incorporated in the body, the abnormally high levels detected in the dolphins that died during the epizootic cannot be explained by pollution occurring in 1990 but, rather, by an increased mortality among the dolphins with the highest PCB loads. The immunodepressor capacity of PCBs, which would make it difficult for the highly polluted individuals to overcome the morbillivirus infection, may explain this selective mortality (38).

Moreover, the nutritional state of the dolphins that died at the onset, and most virulent phase of the 1990 outbreak (the first 70 days), was unusually poor. It was estimated that the lipid reserves of these animals had been reduced to about 60% of the values considered normal for the species in that region and sea- son (46). This diminished nutritional state could not be explained by the viral infection, the development of which is usually quite rapid. Moreover, the dolphins that died in subsequent phases, with identical pathological conditions, showed similar, or indeed even slightly higher, condition indices as apparently healthy, free-ranging individuals, in previous years.

This finding coincided with the observation of an increased prevalence of ectoparasites and epizoits in the diseased striped dolphins, in comparison with individuals from the same species and region studied previously (47). These differences were especially noteworthy with regard to the appearance of the barna- cles Conchoderma virgatum and Lepas pectinata, and to the high frequency of occurrence of Xenobalanus globicipitis. This suggested that the dolphins had recently gone through a period of restricted mobility during which the attachment of these crustaceans had become easier than under normal conditions (48). Coincidentally, studies carried out in 1987, on bottlenose dolphins affected by an epizootic in the Atlantic coastal areas of

the US, also revealed an abnormally high occurrence of barna- cles (43).

Both the impoverished nutritional state and the high prevalence of ectoparasites and epizoits have been taken as indicative of the weakened state of the dolphins that died at the onset and during the most severe phase of the epizootic (6). The cause of this weakened condition has not been established, although it could be related to the occurrence of abnormally warm water temperatures in the western Mediterranean basin during the winter that preceded the epizootic. Increased water temperatures have been associated in the past with the development of some epizootics in seals (20), but a clear cause-effect relationship has not yet been established (49).

In the present case, the abnormal temperatures in the 1989/90 winter were apparently responsible for a depression of the peak of productivity that usually occurs each year in early spring in this region (M. Estrada, pers. comm.) and which is of key im- portance for the dynamics of the ecosystem (50). If this effect is confirmed, it would be reasonable to suppose that a decrease in productivity led to a reduction in available food and this, in turn, compromised their capacity to overcome the disease and contributed to increasing the final toll caused by the morbillivirus infection.

THE POTENTIAL THREAT TO OTHER SPECIES To date, no species of marine mammal other than the striped dolphin appears to have been affected by the Mediterranean epizootic. Coincidental mortality of other cetaceans was at previously recorded levels or could be explained by local fishing (6). However, since the start of the epizootic, 11 monk seals from the highly endangered population inhabiting the coasts of northern Morocco and Algeria are known to have died (51). In none of the cases was the actual cause of death established, and the recent examination of a monk seal from this population did not reveal morbillivirus antibodies in the blood or any indication of distemper disease (A. Osterhaus and L. Vedder, pers. comm.). Moreover, the antigenic characteristics of the morbillivirus isolated from striped dolphins suggest that monk seals may be less susceptible to infection by this agent than dolphins (10, 52), although the possibility that the disease could spread to this endangered marine mammal cannot be ruled out.

AMBIO VOL. 22 NO. 8, DEC. 1993 527



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43. Brody, M. 1989. Explaining sea mammal deaths proves challenging. Am. Soc. Microbiol. News 56, 595-598.

44. Kuehl, D.W., Haebler, R. and Potter, C. 1991. Chemical residues in dolphins from the U.S. Atlantic coast including Atlantic bottlenose obtained during the 1987/88 mass mortality. Chemosphere 22, 1017-1084.

45. Alzieu, C. and Duguy, R. 1979. Organochlorine levels in cetaceans and pinnipeds from the French coasts. Oceanol. Acta 2, 107-120. (In French, summary in English).

46. Aguilar, A., Borrell, A., Calzada, N. and Grau, E. 1992. Body fat reserves in striped dolphins examined during the western Mediterranean die-off. In: Proceedings of the Mediterranean Striped Dolphin Mortality International Workshop, 1991, 4-5 Nov., Palma de Mallorca. Pastor, X. and Simmonds, M. (eds). Greenpeace Mediterranean Sea Project, p. 47-52.

47. Raga, J.A. and Carbonell, E. 1985. New data about parasites on Stenella coeruleoalba (Meyen, 1833) (Cetacea: Delphinidae) in the western Mediterranean. Invest. Cetacea 18, 207-213.

48. Raga, J.A., Aznar, J., Balbuena, J.A. and Fernandez, M. 1992. Parasites and epizoits in striped dolphins affected by an epizootic in the western Mediterranean. In: Proceedings of the Mediterranean Striped Dolphin Mortality International Workshop, 1991, 4-5 Nov., Palma de Mallorca. Pastor, X. and Simmonds, M. (eds). Greenpeace Mediterranean Sea Project, p. 39-46.

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51. Anonymous. 1992. Newsletter. Fondo para la Foca del Mediterraneo. Palma de Mal- lorca, 16 p. (In Spanish).

52. Osterhaus, A.D.M.E., Visser, I.K.G., Swart, R.L., van Bressem, M. F., van de Bildt, M.W.G., Orvell, C. and Raga, J.A. Morbillivirus threat to Mediterranean monk seals? Vet. Rec. (In press).

53. Raw mortality data from Spain were provided by the Autonomous Governments of Catalonia, Valencia, the Balearic Islands, Murcia and Andalusia and coordinated through Spain's Institute forthe Conservation of Nature. Greenpeace International, the Barcelona Zoo, the Asociaci6n Naturalista del Sudeste (ANSE), Marineland of Palma de Mallorca and Palafolls, and the dolphinarium of Vergel also contributed data on dolphin distribution and mortality. Recovery of carcasses and tissue sample collection for many of the studies discussed in the text were also carried out by some of the abovementioned institutions and were funded by specific grants from ICONA and the Autonomous Governments of Catalonia and Valencia. Many individuals contributed personally to the strandings network with their efforts and cooperation, and we would like to express our sincere gratitude to all of them. Compilation of data was made possible through funding from the CICYT (projects NAT90-1254-E/1255-E and NAT91-1 128-C04-01/02), and the U. S. Marine Mammal Commission.

54. First submitted 3 August 1992, accepted for publication 29 October 1992.

Alex Aguilar is a professor of animal biology at the University of Barcelona. He has been member of the Scientific Committee of the International Whaling Commission for many years and is currently the chairman of the European Cetacean Society. His research is mostly focused on the ecology and toxicology of marine mammals. His address: Department of Animal Biology, Faculty of Biology, University of Barcelona, 08071 Barcelona, Spain. J. Antonio Raga is professor of animal biology at the University of Valencia and he is engaged in research on parasitology of marine fauna, especially marine mammals, on which subject he has produced numerous contributions. His address: Department of Animal Biology, Faculty of Biological Sciences, University of Valencia, Dr. Moliner 50, Burjasot, 46100 Valencia, Spain.

528 AMBIO VOL. 22 NO. 8, DEC. 1993



the striped dolphin epizootic in the mediterranean sea

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