Biological aspects of Cuvier’s beaked whale ( Ziphius cavirostris ) recorded in the Croatian part of the Adriatic Sea

The paper describes two stranded ziphiids from Croatia: a subadult female (length 430 cm, body mass 610 kg) that was stranded in 2001 and an adult male (length 510 cm, body mass ∼1,000 kg) that was stranded in 2002. Both were confirmed to be Cuvier’s

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  Eur J Wildl Res (2006) 52: 182  –  187DOI 10.1007/s10344-006-0032-8 ORIGINAL PAPER  Hrvoje Gomer č i ć  .Martina Ðuras Gomer č i ć  .Tomislav Gomer č i ć  .Hrvoje Luci ć  .Merel Dalebout .Ana Galov .Darinka  Š krti ć  .Snje ž ana  Ć urkovi ć  .Snje ž ana Vukovi ć  .Ðuro Huber Biological aspects of Cuvier ’ s beaked whale ( Ziphius cavirostris  )recorded in the Croatian part of the Adriatic Sea Received: 11 July 2005 / Accepted: 3 January 2006 / Published online: 22 February 2006 # Springer-Verlag 2006 Abstract  The paper describes two stranded ziphiids fromCroatia: a subadult female (length 430 cm, body mass610 kg) that was stranded in 2001 and an adult male (length510 cm, body mass  ∼ 1,000 kg) that was stranded in 2002.Both were confirmed to be Cuvier  ’ s beaked whales(  Ziphius cavirostris  Cuvier, 1823) from analysis of mito-chondrial DNA sequences and osteological features. Thereare no previous records of Cuvier  ’ s beaked whales from theCroatian part of the Adriatic. The external shape of thehead of the female specimen appears to be significantlydifferent from the heads of Cuvier  ’ s beaked whales fromother seas. The Croatian specimen exhibited embedded pieces of gravel in the gum tissue around the tip of thelower and upper jaws, which was observed for the first timein a Cuvier  ’ s beaked whale. The presence of the female inshallow coastal waters for several weeks and her boat- positive behaviour are apparently also first records of thiskind for the species. The female was found to have ingestedseveral plastic bags which likely caused her death. Theseare the northernmost findings of this species in the AdriaticSea. Keywords  DNA identification .External morphology .Osteometry .Behaviour  Introduction The family Ziphiidae is the most poorly known group of cetaceans (Rice 1998) and includes 21 species in six genera(Dalebout et al. 2003). Many ziphiid species are difficult to identify and differentiated from one another because thediagnostic morphological features are generally subtle andmay be present only in adult specimens (Heyning 1989;Mead 1989; Gomercic et al. 2002). An alternative and unambiguous method of accurately distinguishing amongspecies of the family Ziphiidae is provided by sequencing a portion of the mitochondrial (mt) DNA control region or cytochrome  b  and comparing it with the validated databaseof reference sequences that have been compiled for all 21 beaked whale species (Dalebout et al. 2003). Before the findings described here, only one specimen of  beaked whales was recorded from the Croatian part of theAdriatic Sea. At Cavtat, near Dubrovnik, an animal (length535 cm, body mass  ∼ 2,000 kg) identified as  Hyperoodonampullatus  was killed in 1939 (Hirtz 1940). It is to beregretted that nothing was retained of this specimen, andonly photographs and a general description are available.The only other ziphiids recorded from the MediterraneanSea are Cuvier  ’ s beaked whale and Blainville ’ s beakedwhale,  Mesoplodon densirostris  (Rice 1998). The former isseen as rare in this region (Kinzelbach 1985). This specieswas mentioned for the first time in the Croatian scientificliterature by Brusina (1889), who identified Cuvier  ’ s beaked whale as one of the species that inhabits or accidentally strays into the Mediterranean Sea but whichhad yet to be recorded from the Adriatic Sea. In 1986 and H. Gomer  č i ć  ( * ) . M. Ðuras Gomer  č i ć  .H. Luci ć  .D.  Š krti ć  .S.  Ć urkovi ć  .S. Vukovi ć Department of Anatomy, Histology and Embryology,Faculty of Veterinary Medicine, University of Zagreb,Heinzelova 55,10000 Zagreb, Croatiae-mail: T. Gomer  č i ć  .Ð. Huber Department of Biology, Faculty of Veterinary Medicine,University of Zagreb,Heinzelova 55,10000 Zagreb, CroatiaM. Dalebout School of Biological Sciences, University of Auckland,Private Bag 92019,Auckland 1000, New ZealandA. GalovDepartment of Animal Physiology, Faculty of Science,University of Zagreb,Rooseveltov trg 6,10000 Zagreb, Croatia  Present address: M. Dalebout Biology Department, Dalhousie University,Halifax, Nova Scotia, Canada  1992, the carcasses of two female Cuvier  ’ s beaked whaleswere found near Bari, on the southern part of Italy ’ sAdriatic coast (Centro Studi Cetacei 1987, 1995). In 2001 and 2002, two specimens of Cuvier  ’ s beaked whale werestranded at the Croatian Adriatic coast (Gomercic et al.2002; Gomer  č i ć  et al. 2003). The aim of this paper is to describe these two specimens.The description includes morphological data, observationof unusual behaviour in one of the two individuals, its parasites and the possible cause of its death. The morpho-logical findings are compared with literature data on other specimens of the species recorded in other parts of itsrange. Materials and methods The first specimen was observed alive for a period of 36 days (from 7 March to 11 April 2001) in a shallow bay(42°37 ′ 18" N, 18°12 ′ 24" E) near Srebreno, south of Dubrovnik, Croatia (Fig. 1). Around 8  A . M . on 12 April2001, the animal was found dead, floating on the surface of the sea. The second specimen was found dead on a beach inPupnatska luka (42°55 ′ 54" N, 17°25"; E), on the island of Kor  č ula, Croatia, on 7 February 2002 (Fig. 1). The carcasswas in advanced decomposition, and the tip of the upper  jaw was missing. Both carcasses were transported to theDepartment of Anatomy, Histology and Embryology,Faculty of Veterinary Medicine, University of Zagreb,Croatia. Necropsy and X-ray examination were performedon both specimens. Both skeletons are stored at the above-named institution. The presence of fused epiphyses of thevertebrae, humerus, radius and ulna was used as criterionfor physical maturity (Moore 1968). The sex of thespecimens was determined from morphological featuresfor the first animal and through molecular sexing using theSRY method of  Gilson et al. (1998) for the second. Tissue samples were collected from both animals and sent to theUniversity of Auckland, New Zealand for DNA extraction,mitochondrial DNA sequencing and analysis to determinespecies identity following standard methods (Dalebout et al. 2005). Twenty-two external measurements were taken for the first animal (after Perrin 1975), while only four of them for the second animal due to its advanced decompo-sition. Skull measurements were taken after Omura (1972)and postcranial skeletal measurements and meristics after Perrin (1975). The morphological data were compared withthose in the literature (Omura 1972; Heyning 1989). Ectoparasities and endoparasites were examined macro-scopically, and the species or genus identified according toHogans (1987) and Dailey and Brownell (1972), respec- tively. The behaviour of the first specimen was observedand documented (slide film and video) during 11-h totalobservation time from an inflatable boat (5.5 m long withan outboard engine) on 9 and 10 March. Weather conditions were good with no wind and the sea wascalm. The water was clear enough to watch the animal below the surface. For the rest of this period, its presencewas confirmed only by observation from land due to prohibition of sea traffic in the bay during the animal ’ s stay. Results Species identificationThe mtDNA control region sequences were amplifiedsuccessfully from both specimens. These  ‘ test  ’  sequences( ∼ 435 bp) were compared to the beaked whale referencedatabase (Dalebout et al. 2003). The two Croatian animals shared the same haplotype, which grouped strongly withreference sequences from Cuvier  ’ s beaked whale,  Ziphiuscavirostris  (bootstrap score, 100%), to the exclusion of sequences from all other beaked whale species in thedatabase. Based on these results, the specimens wereidentified as Cuvier  ’ s beaked whale .  A sequence represent-ing this haplotype has been deposited in Genbank (Accession No. DQ068239). Fig. 1  Geographic locations of the two Cuvier  ’ s beaked whalefindings in Croatian waters.  F   represents the femalespecimen and  M   the male183  MorphologyThe first animal was a juvenile female with uniform dark grey  –   brown coloration on the back and light grey color-ation ventrally. The animal was 430 cm long, with a bodymass of 610 kg. The skin surface was smooth, without scars except for a round, depigmented patch 5 cm indiameter below the dorsal fin on the right side of the body.The melon was distinct and sloped gently down to the short  beak (Fig. 2c). The caudal edge of the tail flukes was flat,laterally curved and lacked a median notch (Fig. 2d). The blowhole was large and semi-lunar with the horns pointinganteriorly (Fig. 2a). The flippers were relatively small. Thedorsal fin was small, falcate and set far back on the body(Fig. 2 b). In the gum of the tip of upper jaw, several piecesof gravel or shell were embedded while others wereovergrown and covered by epithelium. Pieces of over-grown gravel or shell were also found in the gum at the tipof the lower jaw. The area of gum where this material (sizeup to 5 mm, Fig. 3a,b) was embedded was circular with adiameter of 5  –  6 cm.A round, fatty, soft organ, possibly homologous to thespermaceti organ (Heyning 1989), was found beneath the blubber of the melon in a prenarial basin. The organ wastransparent, light yellow and had a gelatinous consistencyat room temperature (mass 5.67 kg, volume 6  –  7 l).There was neither chyle in the mesenterial lymph vesselsnor any traces of food in the digestive organs. Thethickness of the blubber was 3 cm on the back andabdomen. The cause of death was probably the obstructionof the opening between the fundic and first pyloriccompartment of stomach by four plastic bags. Two of the bags (size of 40×15 and 30×25 cm, respectively) wereshopping bags made of soft plastic. The other two bags(size of 15.5×11 and 20×14 cm, respectively) were made of more solid plastic. The latter two bags were of a type inwhich sweets and snacks are sold in Croatia. One of these bags must have been ingested after 10 March 2001 becausethe product was not sold before this date. Thus, the animallikely ingested this bag during its stay in the bay near Srebreno.Ovaries were 4.5×2.0×1.0 (left) and 4.3×1.8×1.0 cm(right) in size, with a mass of 4.0 and 3.0 g, respectively(measured after formalin fixation), with no visible corporafrom previous ovulations. The surface of both ovaries wassmooth and macroscopically lobulated.The heavily decomposed carcass of the second animal(length 510 cm, body mass approximately 1,000 kg) possessed incomplete viscera and a damaged skeleton.Molecular sexing indicated that this specimen was a male.Its teeth had fallen out due to decomposition and weremissing; however, two large alveoli in the tip of the lower  jaw were present.The female possessed a single pair of unerupted teeth at the tip of the lower jaw, together with a large number of unerupted, small, vestigial teeth attached loosely in thegum of both the upper and lower jaw. The two largemandibular teeth were set in alveoli and covered with gum.They were cylindrical  –  conical in shape with sharp unworntips (Fig. 3a,c). Tooth lengths were 41 (left) and 42 (right) Fig. 2  Female Cuvier  ’ s beaked whale:  a  alive near research boat;  b  alive near the coast in Srebreno;  c  head of dead animal,  arrow points  at left throat groove;  d  dorsal view of tail flukes184  mm. Both teeth were almost completely covered withcement, except for the upper 7 mm of the tips which werecovered with enamel. Dentin was almost completelyabsent, and the pulp cavity was broad and unfilled. Thetooth wall at the root was only 0.5- to 0.8-mm thick. Thevestigial teeth in the gums of both upper andlower jaws (24in the upper left, 26 in the upper right, 33 in the lower left,and 31 in the lower right) were up to 13 mm long and up to2 mm in diameter (Fig. 3).The epiphyses of the last nine vertebrae (39th  –  48th) of the female were unfused, as were the epiphyses of humerus, radius and ulna, indicating that the specimenwas a juvenile. In contrast, in the male, the epiphyses of all46 vertebrae and epiphyses of humerus, radius and ulnawere completely fused, indicating that this was an adult animal. The female had five and the male six fused cervicalvertebrae.The structure of the synvertex cranii was identical in both animals, with a characteristic extremely high vertexand enlarged nasals which protruded anteriorly to overhangthe external bony nares (Fig. 4c,d). Condylobasal lengthwas 730 (female) and 840 mm (male). The greatest widthof skull across the postorbital processes of the frontals was390 mm (female). In the male, this measure could not betaken because of postmortem damage of the skull in thisregion.Both specimens possessed ten pairs of ribs. The eighthand ninth left and right ribs had developed only thetuberculum costae, which was joined with vertebraltransverse process.ParasitesThe female had 38 openings in its skin on the left body sideand 12 on the right side, through which parasitic copepods  Pennella balaenoptera  protruded to a length of approxi-mately 10 cm. The cephalothorax of each copepod sat inside a suppurating abscess with a diameter of 3  –  4 cm that  penetrated deep in the blubber but did not reach the fasciaeor muscles. The parasites could easily be pulled out of theabscesses. In the urinary ducts of the kidneys of the sameanimal, nematode conglomerates were found, probably Crassicauda  sp. (possibly  Crassicauda crassicauda ).These parasites (length 20  –  30 cm) were not attached tothe duct wall and could easily be removed. Fig. 3  Female Cuvier  ’ s beakedwhale:  a  X-rays of lower jawwith small pieces of gravelaround the tip;  b  X-rays of upper jaw with big stones on tip; c  X-rays of gum, upper right ( GD ), upper left ( GL ), lower left (  DL ) and lower right (  DD ),with apical mandibular andvestigial teeth;  d  some of thevestigial teeth Fig. 4  Skulls of Cuvier  ’ s beaked whale:  a  juvenilefemale;  b  adult male;  c  synver-tex of female;  d  synvertexof male185  Behaviour The female was seen daily over a period of 36 days in ashallow bay near the shore where the sea is only 2- to 3-mdeep (Fig. 2a,b). Water depth in the greater part of the bayis 30  –  50 m. It is, at least, a further 20 km from the shore before depth increases to 200  –  250 m, and with at least 30  –  50 km distance before a water depth of 1,000 m is reached.We estimated that the animal surfaced every 10  –  20 min,while swimming and diving slowly (with an estimatedspeed of 2  –  5 km/h). We never observed raising of the tailflukes. The individual approached within 10 m of the shoreat times and as close as 2 m from the research boat (Fig. 2a). At times, it would not be seen for a period of 1  –  3 h but would always return several times each day to thesame bay near Srebreno. Discussion Species identity of female could not be determined withconfidence based on its external morphology and behav-iour. Due to advanced decomposition, the identity of themale specimen could also not be determined with certaintyfrom external appearance. Analysis of mtDNA sequencestogether with skull osteological features, however, con-firmed that both specimens represented Cuvier  ’ s beakedwhales. These are the northernmost records of this speciesin the Adriatic Sea.The morphological differences observed between bothCroatian animals and Cuvier  ’ s beaked whales from other  partsoftheworldsuggestthattheremaybemoregeographicvariation in some of these features than previously realised.Contrary to Nishiwaki (1972), Zemskij (1980), Watson (1981)andJeffersonetal.(1993),thetailflukesofourfemale specimen had a flat, laterally curved caudal edge without amedian notch (Fig. 2d). This observation is, however, inagreement with both Leatherwood and Revees (1983) andHeyning (1989) who stated that Cuvier  ’ s beaked whale hasno distinct notch between the tail flukes. In three [distances:(1) between tip of upper jaw to centre of eye, (2) between tipofupperjawtoblowholealongmidlineand(3)betweentipof upper jaw to anterior insertion of flipper] of 16 externalmeasurements, the female differs significantly (i.e. by morethan one standard deviation) from the majority (95%) of females measured byHeyning (1989).The external shape of the head of the female (Fig. 2c) appears to be significantlydifferent from the heads of other Cuvier  ’ s beaked whales(Heyning1989),althoughtherestofthebodyproportionsaresimilar.Mead (1984) reported an ovary mass of 5.2 g for aneonate Cuvier  ’ s beaked whale. In the Croatian female, theovaries had a mass of only 3 and 4 g, respectively. It islikely that ovaries of our juvenile animal were smaller thanthe ovaries in the neonate (Mead 1984) due to the atresia of  large numbers of primary oocytes between birth and puberty.Heyning (1989) examined a female Cuvier  ’ s beakedwhale of 470-cm length and 1,300-kg body mass. Thisdiffers markedly from the Croatian female, which wasslightly shorter (430 cm) but weighed only 610 kg. Theabsence of food in the digestive system, the presence of  plastic bags blocking the first of the stomach openings andthe overall poor physical condition indicated that thisanimal was starving. Comparisons with the presumablyhealthy female of similar size examined by Heyning (1989)suggest that our female animal had lost (or failed to gain)almost half its normal body mass.Our observations of embedded pieces of gravel aroundthe tip of the lower and upper jaws of the female animal arehighly unusual. It is difficult to explain how this could haveoccurred except as a result of the animal repeatedly strikingits beak against such gravel on the seafloor over anextended period of time, sufficient for some of thesewounds to heal and the embedded gravel become over-grown with gum tissue. Ziphiids feed primarily on deep-water squid (Heyning and Mead 1996). They are not known to be bottom feeders, although North Atlantic bottlenose whales would take small numbers of benthicechinoderms andwere observed to come to the surface withmud from the seafloor on their beaks (Benjaminsen andChristensen 1979). Necropsies of this species have not,however, revealed the presence of embedded gravel in their  jaws.The discovery that the female specimen most likely diedas a direct result of ingesting plastic bags is of particular concern. Marine debris is a growing threat for cetaceansworldwide (e.g. Laist  1997). A sick or starving animal may be more likely to take up foreign material than a healthyone (Kastelein and Lavaleije 1992). That at least two of thefour plastic bags found in the stomach of the female animalappeared to have been ingested during the time it spent inthe shallow coastal waters could be taken as support for thehypothesis that the animal was starving.Off the coast of Japan, Cuvier  ’ s beaked whale is most commonly found in waters over 1,000-m deep (Nishiwakiand Oguro 1972). In the Mediterranean, four pairs of Cuvier  ’ s beaked whales were sighted in the CentralTyrrhenian Sea, where water depth is 1,200  –  1,800 m(Marini et al. 1992). Our observation of an individual of  this species in shallow coastal waters (30  –  50 m deep) over 30  –  50 km away from areas with a water depth of >1,000 mis, therefore, highly unusual.Unlike most other ziphiids, North Atlantic bottlenosewhales will often approach slow-moving or stationaryvessels (Gray 1882). In contrast, Cuvier  ’ s beaked whaleoften avoid vessels (Heyning 1989). The boat-positive behaviour exhibited by the female animal was, therefore,also unusual .  Our observation of Cuvier  ’ s beaked whale inshallow coastal waters for several weeks and its boat- 186
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