Mammalia 76 (2012): 21–29 © 2012 by Walter de Gruyter • Berlin • Boston. DOI 10.1515/MAMM.2011.100

Status of cetaceans in through analysis of stranding data from 1937 to 2009

Sami Karaa 1,2, *, Mohamed Nejmeddine Bradai2 , Balaenoptera borealis (Lesson, 1828), although mentioned, Imed Jribi1 , Hedia Attia El Hili 2 and remains doubtful (Heldt 1949 ). Abderrahmen Bouain1 Threats affecting the Mediterranean cetaceans may be rela- tively reduced in the waters adjacent to Tunisia, given there 1 Faculty of Sciences , Biology Department, is less pressure from human activities (e.g., population den- University, Sfax , Tunisia sity, pollution deriving from industrial and agricultural activi- 2 National Institute of Sea Sciences and Technologies , P.O. ties, etc.). Conversely, the interactions between cetaceans and Box 1035, 3018 Sfax , Tunisia, e-mail: [email protected] fi sheries in Tunisia are frequent and pose threats to the local * Corresponding author cetacean populations. These interactions fall into two catego- ries: operational interactions between coastal dolphins and fi sheries, and bycatch. Purse seine and trammel nets were the Abstract types of fi shing gear most vulnerable to dolphin depredation (Bradai 1991 , Ben Naceur et al. 2004 ). A survey of cetaceans stranded along the Tunisian coastline At present, the cetaceans are a diffi cult species to protect in (2004 – 2009) and a review of the literature allowed us to Tunisia as there is a lack of adequate knowledge of their popu- record a total number of 132 stranding events from 1937 to lation distribution, size, discreteness, trends and the dynamics 2009. They included two species of balaenopteridae, one spe- of these mammals. This is mostly due to the fact that many cies of physeteridae and fi ve species of delphinidae. The com- years of study are needed to determine how humans and natu- mon bottlenose dolphin Tursiops truncatus (Montagu, 1821) ral processes are affecting their population. Moreover, man- and the fi n whale Balaenoptera physalus (Linnaeus, 1758) agement policies are lacking in many fi sheries therefore there were the main stranded species in 83 and 21 stranding cases, is a lack of reporting as regards to cetacean bycatch. respectively, representing 78.78 % of all records. Stranding The protection of cetaceans is currently ensured through events occurred all the year round, with the highest frequency the enactment of the law no. 94–13 of 31 July 1994 and the in spring (21.68% ) and summer (50.60% ) for the common decree of the Minister of Agriculture, Tunisia of 28 September bottlenose dolphin and in winter for the fi n whale (50 % ). The 1995 regulating the exercise of fi shing activities. These reg- common bottlenose dolphin was more vulnerable to human ulations forbid the capture in the territorial waters of monk and fi sheries interaction while the fi n whale was more prone seals, of all cetaceans and marine turtles, as well as their trade to be trapped in shallow waters. and detention. Within the framework of the implementation of the UNEP/ Keywords: Balaenoptera physalus; stranding; Tunisian MAP Action Plan for the Conservation of Cetaceans in the coastline; Tursiops truncatus. and following the ratifi cation of relevant international conventions, ACCOBAMS in particular, Tunisia started a number of actions related to cetacean conservation, Introduction such as the founding of the National Stranding Network of cetaceans and marine turtles in 2004. Strategically located in the center of the Mediterranean Sea, The act of coming on to land, alive or dead, intentional or Tunisia lies in the middle of the passageway connecting the accidental, of cetaceans, sirenians and pinnipeds, is known western and the eastern basins, resulting in a high dynamism as a stranding (Jefferson et al. 1993 ). Stranding is probably of the surrounding water masses which leads to elevated the result of a sequence of events rather than a simple cause- marine productivity (Papaconstantinou and Farrugio 2000 , effect relationship (Cordes 1982 ). Several reasons explain Vera and Andrew 2002 ) (Figure 1 ). This productivity com- this phenomenon; the natural factors, such as bacterial and bined with the oceanographic and geographical conditions microbial infections (Stroud and Roff, 1979 , Lipscomb et in this area (narrow continental shelf with deep water in the al. 1994 ), predation (Nores and Perez 1988 ), navigational north and shallow plateau in the south-east) leads to a rich error (Dhermain et al. 2002 ), oceanographic or climatic diversity of cetacean fauna. Therefore, all cetacean species events (Bradshaw et al. 2006 ), are usually listed among the known to be resident in the Mediterranean have been recorded most probable causes. Anthropogenic causes, such as entan- off the Tunisian coastline (Notarbartolo di Sciara 2002 ), glements or injuries caused by ship or boat collision (Laist except Cuvier’ s beaked whale Ziphius cavirostris Cuvier et al. 2001 , Berggren et al. 2002 ), water pollution (Jarman et al. 1823 which has not been reported yet (Ktari -Chakroun 1980 , 1996 , Minh et al. 1999 ), noise of navy sonar (Filadelfo Bradai and Ghorbel 1998, 1999 ). The presence of sei whale, et al. 2009 ) and direct kill (Bearzi 2002 , Notarbartolo di 22 S. Karaa et al.: Status of cetaceans in Tunisia through analysis of stranding data from 1937 to 2009

8 9 10 11 12 13 14

39 39

38 38

37 37

36 36

35 35

34 34

33 33 0 50 100 km

891011 12 13 14

Figure 1 Geographic area covered by the Tunisian stranding network.

Sciara and Bearzi 2002 ) are also among the main causes of of Sea Sciences and Technology (INSTM), in the laboratory stranding. of marine biodiversity and biotechnology. Three groups of Strandings are a very valuable source of biological and sci- three to four persons have been set up to this effect, one based entifi c data. Not only do they contribute to a better explanation in the north (from the border with Algeria to K é libia), a sec- of the phenomenon itself, but they also provide further infor- ond group based in the center (from K é libia to La ) mation about the species involved in terms of health, distri- and a third in the south (from La Chebba to the border with bution, population dynamics, management and conservation Libya). Group members (researchers, veterinary doctors and actions (Berrow 2001 , Rodriguez-Fonseca and Cubero-Pardo students) can be reached at any moment by mobile phone. 2001 , Jefferson and Hung 2004 , Norman et al. 2004 ). For each stranding event, many data were registered, such On Tunisia ’ s coastline some cetacean stranding events have as dates, Global Positioning System coordinates or location, been reported (Heldt 1949 , Ktari-Chakroun 1980, Bradai and kind of coast (sandy, rocky), body measurements, sex and Ghorbel 1998 , 1999 , Bradai et al. 2002 ), but systematic cen- species identifi cation according to Di Natale (1987) . suses of stranded species have become available since 2004 Animals ’ conditions were reported as live animals, freshly through the National Stranding Network. dead, moderately decomposed (organs basically intact), This paper documents and analyzes, for the fi rst time, ceta- advanced decomposition (organs not recognizable) and mum- cean stranding records for the Tunisian coastline. It represents mifi ed/skeletal remains. Necropsy was performed on fresh a fi rst step towards systematic marine mammal ’ s research and moderately decomposed animals. Tissues were taken for aiming to assist in their conservation. histopathology, toxicological and genetic analyses; they were frozen at -20° C or preserved in ethanol and stored at INSTM; the presence and nature of parasites were noted. Materials and methods As regards to Odontoceti, two teeth or more were removed from the mid-lower left mandible for age determination. All Records of stranded cetaceans prior to 2004 were collected stranded cetaceans were examined for cause of death and/or through the available bibliography on the issue. The study of evidence of human interaction. Cetaceans might show indica- stranded cetaceans was strengthened in the beginning of 2004 tion of human interaction in a number of ways: fi shery related through the creation of the National Stranding Network. This mortality (e.g., net marks, attached gear), mutilation, and boat program was included in the activities of the National Institute collisions (blunt trauma and lacerations from the propeller). S. Karaa et al.: Status of cetaceans in Tunisia through analysis of stranding data from 1937 to 2009 23

Evidence of blunt trauma might consist of hemorrhage around Delphinidae was the most important family among the the point of impact. The lacerations from propellers were typi- stranding cases, both in terms of numbers and species diver- cally found on the dorsal surface of the dolphins. Information on sity, including 83 common bottlenose dolphin Tursiops trun- potential causes of death was also gathered with the necropsy. catus, eight Risso’ s dolphin Grampus griseus (G. Cuvier, To analyze spatial distribution of stranding, the χ 2 -test was 1812), three striped dolphins Stenella coeruleoalba (Meyen used to verify signifi cant stranding differences between the 1833), two short-beaked common dolphins Delphinus del- northern, central and southern coasts. phis (Linnaeus, 1758) and one long-fi nned pilot whale For temporal distribution, stranding events were catego- Globicephala melas (Traill, 1809). The Physeteridae family rized by months, seasons and years. The χ 2-test was also used was represented by nine sperm whales Physeter macroceph- to test differences in stranding frequencies between years, alus (Linnaeus, 1758) (Table 1 ). Concerning the balaenop- months and seasons. teridae, fi n whale Balaenoptera physalus was involved in 21 For length-classes analyses, we studied only species with stranding cases (Table 1 ); one individual corresponding to the large stranding sample size (> 20 stranding events were arbi- minke whale, Balaenoptera acutorostrata Lac é p è de, 1804, trarily chosen). In this context, only data concerning the fi n was recorded in (central Tunisia) in May 1975; the whale, Balaenoptera physalus and the common bottlenose head of this specimen was 40 cm in length and was conserved dolphin, Tursiops truncatus were analyzed. The common bot- in the Oceanographic Museum of Salammbo in the INSTM tlenose dolphin were classifi ed as either immature (≤ 2.8 m) (Bradai and Ghorbel 1998 ). or adult ( >2.8 m) following the criteria proposed by Pribanic et al. (2000) ; all individuals ≤ 1 m long were considered to be Temporal distribution neonates (Di Natale 1987 ). Length-classes of the fi n whale were identifi ed as adult (> 17.2 m) and immature ( ≤ 17.2 m) Since 2004, 93 strandings (70.45% ) have been recorded. The in accordance with data from the North Atlantic presented by increase of stranding reports would be a result of the improved Hain et al. (1992) . All individuals < 6 m long were considered effi ciency of the stranding network. to be neonates in accordance with data from the Ligurian Sea Stranding events occurred during the entire year, with sig- (Mediterranean) (Orsi Relini 2000 ). nifi cant differences between months (χ 2 = 27.07; p < 0.05), and seasons (χ 2 = 21.43; p < 0.05); the greatest number of reports occurred during June (n = 20, or 15.15 % ) and the least Results in November (n = 2, or 1.51 % ). Balaenoptera physalus was stranded mostly in winter (50% ) whereas Tursiops truncatus Stranded species was stranded mainly in the spring and summer (21.68% and 50.60 % , respectively). A total number of 132 stranding events were recorded on the Tunisian coasts from 1937 to 2009. They concerned Spatial distribution six species of Odontoceti (with three unknown dolphins) and two species of Mysticeti (with one unknown specimen) A highly signifi cant difference in the frequency of stranding (Table 1 ). No mass stranding has been registered. Of these was observed among the three zones (χ 2 for equal propor- records, 70.45% concern the period 2004– 2009, after the tion = 28.74; p < 0.05). Most stranding events were reported establishment of the stranding network. in the south (53.78% ; n= 132) whereas we reported 30.30%

Table 1 Occurrence of cetacean stranded in Tunisia from 1937 to 2009.

Species North Center South Total Male Female Undetermined Death Alive sex stranding stranding

Mysticeti 23 Balaenopteridae Balaenoptera physalus 2 1 1 8 2 1 4 0 1 7 1 6 5 Balaenoptera acutorostrata 0 1 0 1 0 0 1 1 0 U n k n o w n M y s t i c e t i 0 0 1 1 0 0 1 1 0 Odontoceti 109 Delphinidae Tursiops truncatus 1 7 1 7 4 9 8 3 2 0 1 2 5 1 8 0 3 Stenella coeruleoalba 2 0 1 3 1 1 1 3 0 Delphinus delphis 1 1 0 2 0 0 2 1 1 Grampus griseus 5 0 3 8 3 2 3 6 2 Globicephala melas 1 0 0 1 0 0 1 1 0 Physeteridae Physeter macrocephalus 9 0 0 9 3 1 5 8 1 U n k n o w n d o l p h i n s 1 1 1 3 0 0 3 3 0 Total 38 21 73 132 31 16 85 120 12 24 S. Karaa et al.: Status of cetaceans in Tunisia through analysis of stranding data from 1937 to 2009

(n = 132) and 15.9 % (n= 132) of stranding events in the north respectively), 44 immature individuals and 26 adults of about and in the center, respectively. Conversely, we recorded the 10– 12 years old according to gender (Sergeant et al. 1973 , most important biodiversity in the northern area whereas Connor et al. 1992 , Pribanic et al. 2000 ). seven species were recorded among a total number of eight As for Balaenoptera physalus, 17 individuals had sizes known species in Tunisia (Table 1 ). Both Tursiops trunca- ranging between 7.87 m and 19.2 m and were categorized as tus and Balaenoptera physalus were stranded along the entire 13 immature and four adults of about 6– 8 years old according Tunisian coastline (Figures 2 and 3 ) with a maximum num- to Aguilar et al. (1988) and Lockyer (1972) . ber along the south-eastern coastline. Conversely, the other cetacean species were stranded mainly along the northern Condition of carcass and cause of death Tunisian coastline. The carcass condition was registered in 78.20% of all the Sex and length-classes cases. Of those for which the condition was documented, 9.02 % (n = 12) stranded alive ( Table 1 ) , but the majority were Sex was not determined for two thirds of the stranding speci- in distress and died rapidly. Only two Balaenoptera physalus mens due to the carcass decomposition or to the large ceta- were successfully saved. Dead animals were usually found cean position, such as the fi n whales. These animals were also decomposed (48.4% ) or mummifi ed (36.6 % ). Animals freshly mostly stranded in very shallow waters, making it diffi cult to dead were not common (15 % ). determine the sex. The cause of stranding was determined in 35.60 % of all For sexed specimens, males (32; 65.30 % ) dominated reports. Natural causes accounted for 11.36% of the event and females (17; 34.69% ). Males were in fact easier to identify human-related causes for 24.24 % . Human and fi shery interac- than females, especially in moderately decomposed males tions included boat collision, interaction with fi shing gears having penis distended and exposed. and mutilation. Boat collision involved three Tursiops trunca- Age-class was determined only for Tursiops truncatus and tus, two Physeter macrocephalus and two Grampus griseus . Balaenoptera physalus. Seventy-one T. truncatus had a size Injuries infl icted to these species were different in their loca- range comprised between 0.9 m and 3.16 m and were catego- tions and depth. Concerning the T. truncatus and G. griseus , rized as three neonates (two were recorded on the southern the lacerations from propellers were apparent and were found coast of Tunisia on the coast of Jerba and , on their dorsal surface; these injuries were generally slightly

Figure 2 Spatial distribution of stranded Tursiops truncatus Figure 3 Spatial distribution of stranded Balaenoptera physalus (1937 – 2009). (1937 – 2009). S. Karaa et al.: Status of cetaceans in Tunisia through analysis of stranding data from 1937 to 2009 25

deep caused by essentially small motorized vessels. In regards is close to the coastline (Notarbartolo di Sciera et al. 1993 , to P. macrocephalus , the injuries were deeper and involved Bearzi et al. 2010 ); thus, data of its strandings suggest that both the dorsal and the ventral part of the body. These injuries adults of this species approach the Tunisian waters probably may have been caused by commercial ships or tankers. during the period of the increased population of their favor- Entanglement in fi shing gear seems to be the main cause ite prey: the cephalopods (winter and spring) (Jabeur et al. of strandings of Tursiops truncatus in the studied samples. 2000 ). Among 83 stranded animals, 30% (n =25) were by-caught in The stranding of Physeter macrocephalus occurs all the fi shing gear: one individual found torn into several pieces, year round only along the northern coastline. These stranding two adult males showing an asphyxia by net, two adult dol- events can be explained by the fact that this region is adjacent phins (one male and one female) showing net marks, three to P. macrocephalus habitat (continental slope in front of deep dolphins with their tails attached to a rope and 17 dolphins waters) where mesopelagic cephalopods are most abundant with an amputated tailfi n including fi ve adults (> 2.8 m in (Mullin et al. 2004 , Waring et al. 2005 ); whereas this kind length) and 12 juveniles. of habitat does not exist in the east and in the south. Whales have a size range between 6 m and 13 m. Following the age/ size proposed by (Drouot et al. 2004 ) and in the cases where Discussion specimens were measured, four immature (three males and one female), two sexually mature females (8.3– 9.2 m long) This study reports for the fi rst time organized data regarding and one sexually mature male (11– 12 m long and over) were stranding events occurring along the entire Tunisian coastline. categorized. These results could not be possible without the ratifi cation of The striped dolphin, the common dolphins and the long- relevant international conventions, driven by governmental fi nned pilot whale represent the least stranded Odontoceti authorities, and the establishment of the National Stranding along the Tunisian coastline. We note here the presence of cysts Network in 2004. of metacestodes Phyllobothrium delphini (Bosc, 1802) and The stranding analysis shows that the northern zone is Monorygma grimaldi (Moniez, 1889) in the abdominal cavity characterized by a high specifi c diversity of cetaceans. Few and muscles of two Stenella coeruleoalba stranded in observations both in number and in specifi c diversity were in 2006 and 2009, respectively (Attia El Hili et al. 2010 ). These reported in the central area. However, south-eastern Tunisia parasites were also reported in the striped dolphins stranded is the main region of stranding reports. along the Italian (Cerioni and Mariniello 1996 ) and French The most signifi cant stranded species were Tursiops coastline (Dhermain et al. 2005 ). Furthermore, another study truncatus and Balaenoptera physalus ; these species were described the occurrence of Monorygma spp . in the abdominal observed mainly in the south (Gulf of Gabes). Deep-water Delphinus delphis S. coeru- species as Delphinus delphis , Grampus griseus and Stenella cavity, blubber and muscles of , coeruleoalba were stranded mainly in the north. Only sperm leoalba , and Tursiops truncatus (Gibson et al. 1998 ). whales and one specimen corresponding to a long-fi nned pilot The most important stranded species, the bottlenose dol- whale were reported exclusively in northern Tunisia. phin Tursiops truncatus , occurred all the year round but During the surveys carried out in Tunisian waters, respec- mainly in summer. This costal species was abundant in the tively in May 2003 and May 2005, only Odontoceti species Gulf of Gabes, particularly around the Island of Jerba which were identifi ed: Tursiops truncatus was present both near the could offer more favorable conditions (large continental shelf shore and offshore along all the coasts, but Delphinus delphis , and shallow waters) either for food or for reproduction as Grampus griseus and Stenella coeruleoalba were observed in newly-born species were stranded there. the northern area in depths ranging from 200 to 1000 m (Ben The present results were in agreement with the bathymet- Naceur et al. 2004 , 2005 ). ric preference established by other authors who described Tursiops truncatus in coastal waters of all continents, over Specifi c characteristics of strandings shallow offshore banks, and around most oceanic islands (Rice 1998 ), as well as with the food mode distribution of The stranding of the Risso’ s dolphin and the sperm whale T. truncatus described in Western Mediterranean Sea, which represent the main Odontoceti stranded after the bottlenose is primarily composed of benthic species of the continental dolphin with eight and nine cases, respectively. shelf (Blanco et al. 2001 ). The Risso’ s dolpins were stranded mainly in late winter The high number of sightings (Ben Naceur et al. 2004 , and spring both in the north (fi ve strandings) and in the south 2005 ) and strandings of Tursiops truncatus in comparison of Tunisia (three strandings). Specimens have a size range with other species suggests that this species is abundant in the between 2.47 m and 3.41 m corresponding to seven mature North African shores of the Mediterranean (see also Reeves and one immature individual recorded according to the age/ and Notarbartolo di Sciara, 2006 ). size proposed by Di Natale (1987) . Five specimens were As regards to baleen whales, the stranding of one common sexed (three males and two females). minke whale in the center of Tunisia and 21 fi n whales in dif- Data on the distribution of the Risso ’ s dolphins in the ferent areas of the Tunisian coastline confi rms the scarcity of Mediterranean are very scarce but sightings seem to indi- the fi rst Mysticeti and the occasional presence of the second cate that this species prefers the slope, mostly when the latter Mysticeti around the Tunisian waters. 26 S. Karaa et al.: Status of cetaceans in Tunisia through analysis of stranding data from 1937 to 2009

Balaenoptera physalus was stranded mainly in the last physalus were more likely to be trapped in the shallow waters decade (recorded events varied from 0.4 stranding/year associated with large tidal range. The stranding of two live between 1990 and 1999 to 0.9 stranding/year between 2000 B. physalus (9.6 m and 12 m long) in Sfax and Mahdia in and 2009); this stranding rate confi rms the presence of this 2001 and 2002, respectively, in channels during low tide whale in Tunisian waters all the year round and the better (almost 1 m-deep) showed that the topography along the east- monitoring of the stranding network. ern Tunisian coastline could constitute an environmental trap Most data showed that Balaenoptera physalus strand- for these whales. A trapping of a fi n whale was also recorded ings occurred mainly in the Gulf of Gabes during the win- in the northern Mediterranean Sea where a young fi n whale ter months. This seasonal dispatching could be a result of calf was stranded in 1 m-deep water off the mouth of the Great possible cyclic migration of some Mediterranean fi n whales Rhone in the Camargue on 17 October 1996. This whale was between the western and eastern basins. The decrease in fi n strapped and pulled off to the sea, thanks to major logistical whale density occurring in the north-western Mediterranean means (Dhermain et al. 2002 ). from early autumn to the outset of spring (Viale 1985 ) also In general, data on Tunisian stranded cetacean suggest suggests a seasonal migration of this whale. that fi shery activities did not impact on large cetaceans. According to Aissi et al. (2008) , Balaenoptera physalus Conversely, many accidental captures of large cetaceans follow an aggregation-dispersion-aggregation scheme in the could be cited: (1) two minke whale were reported dying in Mediterranean Sea, they: (1) aggregate in summer in the a purse seine in Sidi Daoud (northern Tunisia) in May 1976 north-western Mediterranean Sea, one of the main productive and in drift nets in (Southern Tunisia) in October 1995 areas to meet their feeding requirements; (2) migrate through with a total length of 4.5 m and 5 m, respectively (Bradai and the Strait of Messina during autumn and early winter to reach Ghorbel 1998 ); (2) a humpback whale (8.5 m long) captured the eastern basin where whales are clustered until spring; and in a “ mernine ” driftnet (now prohibited) (Bradai and Bouain (3) aggregate, for some individuals, around Lampedusa Island 1994 ); and (3) one fi n whale (9.88 m long) was also caught in in winter and until the beginning of spring. gillnet in the region of Sfax in August 2008. The identifi cation of the Lampedusa Island as a winter feed- Actually, mortality in fi shing operation is the most com- ing ground of Balaenoptera physalus in the Mediterranean mon source of anthropogenic mortality of small cetacean Sea (Canese et al. 2006 ) could support the numerous stranded (Read and Murray 2000 , Friedlaender et al. 2001 ). It was cases of this whale in the south of Tunisia during this migra- often claimed that dolphin stole fi sh from the net, scared the tion. The abundance of zooplankton (Drira et al. 2010 ) and fi sh away, or damaged the catch and fi shing gear. In Tunisia, small pelagic Clupeidae and Engraulidae (Anonymous 2006 ) the current interactions include essentially gill nets and purse could be also favorable to the fi n whale feedings. Furthermore, seines fi sheries. Fishermen generally cut the tail fl uke of the the presence of large numbers of two species of ecto-parasites entangled dolphin while trying to release the animal, in order attached to the several whales stranded on the coast of the to avoid a greater damage to their fi shing gear. However, Kerkennah Islands support the hypothesis of the aggregation within the context of fi sh stock collapse in Tunisian waters of some fi n whales near this area. These parasites are the barna- (Ben Mariem et al. 1996 , Ghorbel et al. 1997 ), Tursiops trun- cle of the superfamily Coronuloidea Xenobalanus globicipitis catus was considered as a direct competitor with traditional (Steenstrup, 1851), sampled on the caudal fi n, and the copepod fi sheries. This may result in various actions, such as keeping of the family of Pennellidae Pennella spp Oken, 1816 sampled the animals away from the nets by the intentional killings or from various parts of the host body. These ecto-parasites were the use of acoustic deterrents. This behavior was also reported also reported from other cetaceans as the striped dolphins in many areas in the Mediterranean Sea (Silvani et al. 1992 , (Stenella coeruleoalba) from the Spanish coast (Aznar et al. Brotons et al. 2008 ). 1994 ) and the minke whale (Balaenoptera acutorostrata) from During the current study, the interaction between Tursiops the Northwestern Pacifi c Ocean (Uchida and Araki 2000 ). truncatus and fi sheries concerns many juveniles. Those indi- A length-frequency distribution of 17 Balaenoptera physa- viduals are vulnerable to entrapment because of their lack of lus showed that specimen sized between 7.87 m and 19.2 m. experience and the tendency to play and spend a lot of time The mean length of the sample was 14.18 m (S.E. = 3.28). scouting (Mann et al. 1995 , Fertl and Leatherwood 1997 ). This value was comparable to the mean length (13.8 m; Conversely, according to Bearzi (2002) , there are very little S.E. = 0.52) of the same species stranded in the Mediterranean scientifi c data on this subject, and for most Mediterranean Sea (Notarbartolo di Sciara et al. 2003 ). countries only anecdotal reports exist. The number of registered stranded Tursiops truncatus Causes of strandings showing a positive human interaction should be taken as a minimum because some interactions do not leave any physi- The cause of stranding could not be determined for 58% of cal evidence. In fact, it was a rare occurrence to have gear cases due to their decomposed state which prevented us from attached to the carcass; therefore, the determination of human performing necropsy, or due to our inability to manipulate interaction was usually made by observing external marks the animals fl oating near the shore. Generally, the causes of of mutilation, boat collision or lines imprinted by the fi sh- stranding differ according to the species: small cetaceans as ing gear. Other undetermined causes must also be taken into Tursiops truncatus were more vulnerable to the human and account. These causes may include, above all, illnesses and fi shery interaction, while big cetaceans as Balaenoptera environmental degradation. S. Karaa et al.: Status of cetaceans in Tunisia through analysis of stranding data from 1937 to 2009 27

Conclusion Bearzi, G., R.R. Reeves, E. Remonatoa, N. Pierantonioa and S. Airoldi. 2010. Risso’ s dolphin Grampus griseus in the The most important species in Tunisian waters were Tursiops Mediterranean Sea. Mamm. Biol. 76: 385 – 400. truncatus , as the only common species either in stranding or Ben Mariem, S., H. Gharbi and N.S. Ezzedin. 1996. Red mul- in occurrence at sea and Balaenoptera physalus which strands let Mullus surmuletus in Tunisia: assessment of stocks and mainly in the southern area where it is frequently observed fi sheries management. FAO Fisheries Reports, 533(suppl): 269 – 284. at sea. Ben Naceur, L., A. Gannier, M.N. Bradai, V. Drouot, S. Bourreau, The oceanographic characteristics of the Gulf of Gabes N. Khalfallah, R. M’ rabet and M. Bdioui. 2004. Recensement could contribute to the increase in the number of strandings. In du grand dauphin Tursiops truncatus dans les eaux Tunisiennes. fact, in such a low-depth area, cetaceans are more frequently Bull. Inst. Nat. Sci. Tech. Mer de Salammb ô . 31: 75 – 81. trapped and come in contact with the coastal fi shing activity Ben Naceur, L., A. Gannier, M.N. Bradai, I. Jribi, H. Ali, which is important. The weak slope of the continental shelf in M. Makhloufi and S. Karaa. 2005. Compagne d ’ observation des this region can provoke displacements of cetaceans (by igno- c é tac é s dans les eaux tunisiennes: la Galite 2005. Acte de la qua- rance of the littoral) and consequently lead to their stranding. torzi è me conf é rence internationale pour la protection des mam- Moreover, the monitoring of stranding is more regular in this mif è res marins en M é diterran é e occidentale. pp. 16. area than in any other parts of the Tunisian coast where some Berggren, P., P.R. Wade, J. Carlstr ö m and A.J. Read. 2002. Potential sites are not accessible or are characterized by the absence of limits to anthropogenic mortality for harbour porpoises in the coastal communities. Baltic region. Biol. Cons. 103: 313 – 322. Berrow, S. 2001. Biological diversity of cetaceans (whales, dol- It is important to note here that this work presents the fi rst phins and porpoises). In: (J.D. Nunn, ed.) Marine biodiver- step for the study of cetaceans in Tunisia. Other biological sity in Ireland and adjacent waters. Ulster Museum Belfast, and ecological studies (toxicology, genetic, interaction with pp. 115 – 120. fi sheries and monitoring at sea) are still in progress in order to Blanco, C., O. Salomon and J.A. Raga. 2001. Diet of bottlenose enrich our knowledge about the status of cetaceans in Tunisian dolphin ( Tursiops truncatus) in the western Mediterranean Sea. waters and thus better contribute to their conservation. J. Mar. Biol. Ass. U.K. 81: 1053 – 1058. Bradai, M.N. 1991. Nouvelles mentions de Delphinidae. Rev. Inst. Nat. Agronom. . 6: 169 – 172. Acknowledgments Bradai, M.N. and A. Bouain. 1994. La mer: resources et problè mes. Association de la protection de l’ environnement de Sfax Tunisie. The authors wish to thank all people working within the framework (eds.), p. 155. of the National Stranding Network and volunteers contributing to Bradai, M.N. and M. Ghorbel. 1998. Les c é tac é s dans la r é gion du the notifi cation, recovery, transportation and sample’ s collection of golfe de Gabes. Premiè res mentions de deux Balaenopteridae: stranded cetaceans. Anonymous reviewers and the editor made valu- Megaptera noveangliae et Balaenoptera acutorostrata . Bull. able comments, allowing me to improve the text; the English gram- Inst. Nat. Sci. Tech. Mer de Salammb ô . 4: 9 – 11. mar was improved by Mr. Jamil Jaoua. I thank them all. Bradai, M.N. and M. Ghorbel. 1999. Les c é tac é s dans les eaux tunisiennes nouvelles mentions d’ esp è ces rares en M é diterran é e. Acte de la huiti è me conf é rence internationale References pour la protection des mammif è res marins en M é diterran é e occidentale 8: 51– 53. Aguilar, A., M. Olmos and C.H. Lockyer. 1988. Sexual maturity in Bradai, M.N., A. Elouaer, A. Elabed and K. Maatoug. 2002. fi n whales ( Balaenoptera physalus) caught off Spain. Rep. Int. Sauvetage de deux rorquals communs Balaenoptera physalus Whal. Commn. 38: 317 – 322. é chou é s vivants sur les cô tes tunisiennes. Acte de la onziè me Aissi, M., A. Celona, G. Comparetto, R. Mangano, M. Wurtz and conf é rence internationale pour la protection des mammif è res A. Moulin. 2008. Large-scale seasonal distribution of fi n whales marins en M é diterran é e occidentale 11: 52 – 53. ( Balaenoptera physalus) in the Central Mediterranean Sea. J. Bradshaw, C.J., A.K. Evans and M.A. Hindell. 2006. Mass cetacean Mar. Biol. Ass. U.K. 88: 1253 – 1261. strandings – a plea for empiricism. Cons. Biol. 20: 584 – 586. Anonymous. 2006. Coastal environment and estimating stocks of Brotons, J.M., A. Grau and L. Randell. 2008. Estimating the sardines, anchovies and tuna. Internal Report of the National impact of interactions between bottlenose dolphins and artisa- Institute of Science and Technology of the sea, Tunisia. pp. 244. nal fi sheries around the Balearic Islands. Mar. Mamm. Sci. 24: Attia El Hili, H., B. Cozzi, C. Ben Salah, M. Podestà , W. Ayari, 112 – 127. N. Ben Amor and R. Mraouna. 2010. A survey of cetaceans Canese, S., A. Cardinali, C.M. Fortuna, M. Giusti, G. Lauriano, stranded along the northern coast of Tunisia: recent fi nd- E. Salvati and S. Greco. 2006. The fi rst identifi ed winter feed- ings (2005 – 2008) and a short review of the literature. J. Clin. ing ground of fi n whales (Balaenoptera physalus ) in the Rheumatol. 26: 982– 985. Mediterranean Sea. J. Mar. Biol. Ass. U.K. 86: 903 – 907. Aznar, F.J., J.A. Balbuena and J.A. Raga. 1994. Are epizoites bio- Cerioni, S. and L. Mariniello. 1996. Metazoi parassiti di Stenella logical indicators of a western Mediterranean striped dolphin coeruleoalba (Cetacea: Delphinidae) spiaggiata lungo le coste die-off ? Dis. Aquat. Org. 18: 159 – 163. laziali dal 1985 al 1991. Parassitologia 38: 505 – 510. Bearzi, G. 2002. Interactions between cetaceans and fi sheries in Connor, R.C., R.A. Smolker and A.F. Richards. 1992. Two levels the Mediterranean Sea. In: (G. Nortarbartolo di Sciara, ed.) of alliance formation among male bottlenose dolphins ( Tursiops Cetaceans of the Mediterranean and Black Seas: state of knowl- sp ). Proc. Natl. Acad. Sci. USA. 89: 987 – 990. edge and conservation strategies. A report to the ACCOBAMS Cordes, D.O. 1982. The causes of whale strandings. New. Zeal. Vet. Secretariat. Section 9. Monaco. pp. 20. J. 30: 21 – 24. 28 S. Karaa et al.: Status of cetaceans in Tunisia through analysis of stranding data from 1937 to 2009

Dhermain, F., L. Soulier and J.M. Bompar. 2002. Natural mortal- Lipscomb, T.P., F.Y. Schulman, D. Moffatt and S. Kennedy. 1994. ity factors affecting cetaceans in the Mediterranean Sea. In: (G. Morbilliviral disease in Atlantic dolphins ( Tursiops truncatus ) Notarbartolo di Sciara, ed.) Cetaceans of the Mediterranean and from the 1987 – 1988 epizootic. J. Wildl. Dis. 30: 567 – 571. Black Seas: state of knowledge and conservation strategies. pp. Lockyer, C. 1972. The age at sexual maturity of the southern fi n 1 – 14. whale (Balaenoptera physalus) using annual layer counts in the Dhermain, F., et le r é seau Echouage M é diterran é en, 2005. ear plug. J. Cons. Int. Explor. Mer. 34: 276 – 294. Recensement des é chouages de c é tac é s (Cetacea Brisson, Mann, J., R.A. Smolker and B.B. Smuts. 1995. Responses to calf 1762 ) sur les c ô tes fran ç aises de M é diterran é e. Ann é e 2003. entanglement in free-ranging bottlenose dolphins. Mar. Mamm. Rapport interm é diaire pour le Minist è re de l ’ Ecologie et du Sci. 11: 100 – 106. D é veloppement Durable, GECEM, p. 56. Minh, T.B., M. Watanabe, H. Nacata, S. Tanabe and T.A. Jefferson. Di Natale, A. 1987. Mammif è res Baleines, dauphins, marsouins et 1999. Contamination by persistent organochlorines in small phoques. In: (M.L. Bauchot and M. Schneider, eds.) Fiches FAO cetaceans from Hong Kong coastal waters. Mar. Poll. Bull. 39: d ’ identifi cation des espè ces pour le besoin de la pê che, Rome. 383 – 392. pp. 1439 – 1472. Mullin, K.D., W. Hoggard and L.J. Hansen. 2004. Abundance and Drira, Z., M. Belhassen, H. Ayadi, A. Hamza, R. Zarrad, A. Boua ï n seasonal occurrence of cetaceans in outer continental shelf and L. Aleya. 2010. Copepod community structure related to and slope waters of the north-central and northwestern Gulf of environmental factors from a summer cruise in the Gulf of Gabes Mexico. Gulf of Mexico Sci. 2004: 62 – 73. (Tunisia, eastern Mediterranean Sea). J. Mar. Biol. Ass. U.K. 90: Nores, C. and C. Perez. 1988. Multiple strandings of Stenella coeru- 145 – 157. leoalba and Globicephala macrorhynchus on the coast of Spain. Drouot, V., A. Gannier and J.C. Goold. 2004. Summer social dis- Eur. Res. Cet. 2: 25 – 26. tribution of sperm whales (Physeter macrocephalus ) in the Norman, S.A., C.E. Bowlby, M.S. Brancato, J. Calambokidis, D. Mediterranean Sea. J. Mar. Biol. Ass. U.K. 84: 675 – 680. Duffi eld, P.J. Gearin, T.A. Gornall, M.E. Gosho, B. Hanson, S.J. Fertl, D. and S. Leatherwood. 1997. Cetacean interactions with trawls: Jefries, B. Lagerquist, D.M. Lambourn, B. Mate, B. Norberg, a preliminary review. J. Northw. Atl. Fish. Sci. 22: 219 – 248. R.W. Osborne, J.A. Rash, S. Riemer and J. Scording. 2004. Filadelfo, R., J. Mintz, E. Michlovich, A. D ’ Amico, P.L. Tyack and Cetacean strandings in Oregon and Washington between 1930 D.R. Ketten. 2009. Correlating military sonar use with beaked and 2002. J. Cetacean Res. Manage. 6: 87 – 99. whale mass stranding: what do the historical data show ? Aqua. Notarbartolo di Sciara, G. 2002. Cetacean species occurring in the Mamm. 35: 435 – 444. Mediterranean and Black Seas. In: (G. Notarbartolo di Sciara, ed.) Friedlaender, A.S., W.A. McLellan and D.A. Pabst. 2001. Cetaceans of the Mediterranean and Black Seas: state of knowl- Characterising an interaction between coastal bottlenose dolphins edge and conservation strategies. A report to the ACCOBAMS ( Tursiops truncatus ) and the spot gillnet fi shery in southeastern Secretariat. Monaco, Section 3, p. 17. North Carolina, USA. J. Cetacean Res. Manage. 3: 293 – 303. Notarbartolo di Sciara, G. and G. Bearzi. 2002. Cetacean direct killing Ghorbel, M., O. Jarboui, and A. Bouain. 1997. É valuation du stock and live capture in the Mediterranean Sea. In: (G. Notarbartolo de pageot ( Pagellus erythrinus, Sparidae) dans le golfe de Gabes di Sciara, ed.) Cetaceans of the Mediterranean and Black Seas: (Tunisie) par analyse de pseudo-cohorte. Cybium 21: 55 – 65. state of knowledge and conservation strategies. A report to the Gibson, D.I., E.A. Harris, R.A. Bray, P.D. Jepson, T. Kuiken, J.R. ACCOBAMS Secretariat, Monaco, Section 5, p. 4. Baker and V.R. Simpson. 1998. A survey of the helminth para- Notarbartolo di Sciera, G., M.C. Venturino, M. Zanardelli, F.J. sites of cetaceans stranded on the coast of England and Wales Borsani and B. Cavalloni. 1993. Cetaceans in the central during the period 1990± 1994. J. Zool. 244: 563 – 574. Mediterranean Sea: distribution and sighting frequencies. Boll. Hain, J.H.W., M.J. Ratnaswamy, R.D. Kenney and H.E. Winn. 1992. Zool. 60: 131 – 138. The fi n whale, Balaenoptera physalus , in waters of the north- Notarbartolo di Sciara, G., M. Zanardelli, M. Jahoda, S. Panigada eastern United States continental shelf. Rep. Int. Whal. Commn. and S. Airoldi. 2003. The fi n whale Balaenoptera physalus 42: 653 – 669. (L. 1758) in the Mediterranean Sea. Mamm. Rev. 33: 105 – 150. Heldt, H. 1949. Incursions de baleinoptè res sur les cô tes tunisiennes. Orsi Relini, L. 2000. The cetacean sanctuary in the Ligurian Sea: a Ann. Biol. 6: 80. further reason. Biol. Mar. Medit. 7: 117 – 127. Jabeur, C., B. Gobert and H. Missaoui. 2000. Typologie de la fl ottille Papaconstantinou, C. and H. Farrugio. 2000. Fisheries in the de pê che cô ti è re dans le golfe de Gabè s (Tunisie). Aquat. Living. Mediterranean. Med. Mar. Sci. 1: 5 – 18. Resour. 13: 421 – 428. Pribanic, S., D. Miokovic and D. Kovaic. 2000. Preliminary growth Jarman, W.M., R.T. Nostran, D.C.G. Muir, B. Rosenberg, M. Simon rate and body lengths of the bottlenose dolphins Tursiops trun- and R.W. Baird. 1996. Levels of organochlorine compounds, catus (Montagu, 19821) from the Adriatic Sea. Nat. Croat. 9: including PCDDS and PCDFS, in the blubber of cetaceans from 179 – 188. the west coast of North America. Mar. Poll. Bull. 32: 426 – 436. Read, A.J. and K.T. Murray. 2000. Gross evidence of human-induced Jefferson, T.A. and S.K. Hung. 2004. A review of the Indo-Pacifi c mortality in small cetaceans. NOAA Technical Memorandum . humpback dolphin Sousa chinensis in Chinese waters. Aquat. NMFS-OPR-15. p. 21. Mamm. 30: 149 – 158. Reeves, R. and G. Notarbartolo di Sciara (compilers and editors). Jefferson, T.A., S. Leatherwood and M.A. Webber. 1993. Marine 2006. The status and distribution of cetaceans in the Black Sea mammals of the world: FAO species identifi cation guide. FAO/ and Mediterranean Sea. International Union for Conservation of UNEP, Rome. pp. 320. Nature center for Mediterranean Cooperation, Malaga, Spain. pp. Ktari-Chakroun, F. 1980. Les c é tac é s des c ô tes tunisiennes. Bull. 137. Inst. Nat. Sci. Tech. Mer de Salammb ô . 7: 139 – 149. Rice, D.W. 1998. Marine mammals of the world. Systematics and Laist, D.W., A.R. Knowlton, J.G. Mead, A.S. Collet and M. Podesta. distribution. Soc. Mar. Mamm. Spec. Publ. 4: 1 – 231. 2001. Collision between ships and whales. Mar. Mamm. Sci. 17: Rodriguez-Fonseca, J. and P. Cubero-Pardo. 2001. Cetacean strand- 35 – 75. ing in Costa Rica (1966 – 1999). Rev. Biol. Trop. 49: 667 – 672. S. Karaa et al.: Status of cetaceans in Tunisia through analysis of stranding data from 1937 to 2009 29

Sergeant, D.E., D.K. Caldwell and M.C. Caldwell. 1973. Growth and Vera, N.A. and B. Andrew. 2002. ‘ Ocean triads’ in the Mediterranean maturity of bottlenose dolphin (Tursiops truncatus) from north- Sea: physical mechanisms potentially structuring reproductive east Florida. J. Fish. Res. Board Can. 30: 1009 – 1011. habitat suitability (with example application to European anchovy, Silvani, L., I. Raich, and A. Aguilar. 1992. Bottlenose dolphin, Engraulis encrasicolus). Fisheries Oceanogr. 11: 129– 142. Tursiops truncatus, interacting with fi sheries in the Balearic Viale, D. 1985. Cetaceans in the North-western Mediterranean: their Islands, Spain. Eur. Res. Cet. 6: 32 – 34. place in the ecosystem. Oceanogr. Mar. Biol. 23: 491 – 571. Stroud, B.K. and T.J. Roff. 1979. Causes of death in marine mammals Waring, G.T., E.C.E. Josephson, C.P. Fairfi eld and K. Maze-Foley. stranded along the Oregon coast. J. Wildlife Dis. 15: 91 – 97. 2005. U.S. Atlantic and Gulf of Mexico Marine Mammal Stock Uchida, A. and J. Araki. 2000. Ectoparasites and endoparasites Assessments 2005. NOAA Tech Memo NMFS-NE-194. pp. 318. in the minke whale (Balaenoptera acutorostrata) from the North-Western Pacifi c Ocean. J. Jpn. Vet. Med. Assoc. 53: Received March 17, 2011; accepted October 4, 2011; previously 85 – 88. published online January 19, 2012