ANNALES Ser. hist. nat. • 11 • 2001 1 (23)
original scientific paper	UDC 574.5:591.5(262)
received: 13.6.2001
FIRST CONFIRMED RECORD OF ANGULAR ROUGHSHARK OXYNOTUS CENTRINA (LINNAEUS, 1 758} PREDATION ON SHARK EGG CASE OF SMALL-SPOTTED CATSHARK SCYLIORHINUS CANICULA (LINNAEUS, 1758) IN MEDITERRANEAN WATERS
Joan 8ARRULL & Isabel MATE Lab. Vertebráis Secció Ictiología, Museo Zoología, C 08080 Barcelona, Aptai correus 59!? E-mail: jbamjli@pie.xtsc.es
ABSTRACT
The stomach content examination oí two male angular roughs hark individuals Oxynotus centrina captured in Barcelona's coastal waters on November 2000 and January 2001 revealed the presence of yolk sacks and embryos from the small-spotted catshark Scyliorhinus canícula. Up lo date, this is the first confirmed record of small-spotted catshark egg prédation in the Mediterranean waters
Key words: Oxynotus centrina, Scyliorhinus canícula, prédation, shark egg case, embryos, Mediterranean Sea
PRIMA SEGNALAZiONE CONFERMATA D! PREDAZIONE D! PESCE PORCO OXYNOTUS CENTRINA (LINNAEUS, 1758) SU CAPSULE OVARICHE DI CATTUCCI MINORI SCYLIORHINUS CANICULA (LINNAEUS, 1758) IN ACQUE MEDITERRANEE
SI NT ES I
L'esame del contenuto stomacale di due maschi di pesce porco Oxynotus centrina (Linnaeus, 1758) catt.urati davanti al litorale di Barcellona nel novembre 2000 e ne! gennaio 2001, ha rilevato la presenta di sacchi vitellini ed embrioni appartenenti alia specie dei gattucci minori Scyliorhinus canícula (Linnaeus, 1758). Per quanto è noto> si tratta della prima segnalazione confermala di predazione su capsule ovariche di gattucci minori in acque mediterra-
Parole chiave: Oxynotus centrina, Scyliorhinus canícula, predazione, capsula o va rica, embrioni, Mare Mediterráneo
ANNALES Ser. hist. nat. 11 - 2001 1 (23)
loar BARRULl S, Isabel MATE: fiRSr CONFIkMED RECORD OF ANGULAR ROUGHSHARK OXYNOTUS CEMRINA iUNNAtVS. I7SÍM ...,23-2f
INTRODUCTION
Records of prédation on elasmobranch eggs are relatively rare (Cox & Koob, 1993}. in this report we discuss the first confirmed record of elasmobranch prédation on embryos of an oviparous shark in Mediterranean waters.
MATERIAL AND METHODS
Two angular roughshark Oxynotus centrina (Linnaeus, 1758) male individuals (Figs. 1, 2) were caught in Catalonia's continental slope waters on November 10th 2000 and January 2nd 2001 by the fishing vessel "Maireta II" based in the port of Barcelona (Spain). The specimens were caught using a trawler net at a depth of 192 m in the fishing ground know as "La Serola", at a geographical position of 41°12' N, 2°28' E (Fig 3). The specimens were identified according to Compagno (1984a). They were deposited at the Ichthyological Collection of the Zoology Museum of Barcelona, with catalogue numbers MZB-2000-1035 and MZB-2001-0006. The roughshark were examined for parasites. Stomachs were dissected and the contents identified. The reproductive tracts of individuals were examined to determine maturity in agreement with Moreno & Hoyos (1982).
RESULTS AND DISCUSSION
The two angular roughshark O. centrina male individuals measured both 555 mm total length. In table 1 the main morphometric data of specimens are presented following Compagno (1984a). Both were immature, and
Fig. 1; Angular roughshark Oxynotus centrina caught on November 10th 2000 in coastal waters off Barcelona. (Photo: f. Barrull & I. Mate) SI. 1: Morski prašič Oxynotus centrina, ujet 10. novembra 2000 nedaleč od Barcelone. (Futo: j. Barrull & /. Mate)
no internal or external parasites were found. The examination of one of the angular roughshark's stomach content revealed only fragments of ten yolk sacks and one 34 mm (total length) embryo (Fig. 4). The embryo, which had an external yolk sack, was determined to belong to the small-spotted catshark Scyllorhinus canicula, which was in agreement with the illustrations and morphological descriptions provided in Compagno (1984b), Moreno (1995) and Van Grevelynghe et al. (1999). The stomach content of the second shark showed two embryos at a total length of 60 mm from Scyllorhinus canicula (Fig. 5). No egg capsules were found. The egg content might have been sucked up by the angular roughshark
Very little is known about the angular roughshark's diet. It is a solitary animai. However, two specimens are sometimes captured at the same time. Angular rough-shark inhabits mud and sand-bottoms at depths of about 50-725 m (Barrull ef a/., 1999) and it is thought that its diet consists of poiychaetes and small animals from marine bottom (Compagno., ¡984a; Barrull & Mate, 1996). Capapé (1975) points out that in Tunisian waters it feeds on crustaceans. Some species of carnivorous gastropods may drill into and feed on embryos, or developing its own young, in egg cases of some oviparous sharks (Mc Laughlin & O'Cower, 1971; Cox & Koob, 1993). Shark egg cases have been taken from stomachs of teleost (Long, 1996), marine mammals ¡Morejohn & Baltz, 1970; Jones, 1981; Condit & Le Boeuf, 1984; Antonelis et al., 1987; Sinclair, 1994) and at least one species of shark (Crover, 1972). The fact that this is the first confirmed record of elasmobranches prédation on shark eggs in Mediterranean waters provokes a special interest. Firstly because it reveals something new about
Fig. 2: Angular roughshark Oxynotus centrina caught on January 2nd 2001 in coastal waters off Barcelona. (Photo:). Barrull & I. Mate)
SI. 2: Morski prašič Oxynotus centrina, ujet 2. Januarja 2001 nedaleč od Barcelone. (Foto: J. Barrull & I. Mate)
ANNALES • Ser. hist. nat. 11 2001 • 1 (23)
¡oar. 8AKKULL 4 Isabel MAT£: FIRST CONFIRMED RECORD OF ANGULAR KOUGHSHARK OXYNOTUS CiNTKINA (UNNAEUS,17ÎSJ ,.., 23-28
Fig. 3: Localization of the specimens of Angular rough-shark Oxynotus centrina in the Barcelona littoral (NW Mediterranean).
SI. 3: Lokacija osebkov morskega prašiča Oxynotus centrina v barcelonskem obrežnem pasu (SZ Sredozemsko morje).
high fat and protein content, and their accessibility. It is also important to point out that small-spotted catsnarks and angular roughsharks have a similar bathymetrica! distribution in almost ail the continental slope and at different depths {Barruil et a!., 1999). So, this kind of interaction would not be surprising.
It would be worth finding out how this predation could affect the small-spotted catshark population. Angular roughsharks are considered an unusual and not a very prolific shark, due to their year-long reproductive period, with litters between 8 and 23 young (Capape et a!., 1999, 2000), while the small spotted cat shark is considered an abundant and very prolific species. Also with a year reproductive period (with seasonal fluctuations), can produce between 96-115 egg cases each year (Capape, 1977). Considering all these facts, we assume that angular roughshark's predation on the small-spotted catshark's eggs will not threaten its population, it would be necessary, however, to acquire more documentation to adequately analyse this phenomena.
The fact that this may be the first accurately documented instance of elasmobranch predation on embryos of an oviparous shark in Mediterranean waters, should warrant the special interest.
ACKNOWLEDGEMENTS
angular roughshark's diet, and secondly for the consequences that this predation may have on species whose eggs are eaten.
The records of shark egg cases in stomachs of marine animals are rare (Cox & Koob, 1993). The question is how often this predation occurs. Small-spotted catshark eggs can be an important nutritional source, due to their
We wish to thank Mr. David Albiol for his help in collecting sharks, and Dr. Domenech Lioris for his helpful comments on the manuscript. We also would like to thank Ingrid lienito for translating the article into English, and Tiziano Storai for translating the abstract into Italian.
Fig. 4: Fragments of yolk sacks and 34 mm small-spotted catshark embryo from the stomach content of the November specimen. {Photo:}. Barruil & L Mate) SI. 4: Delci rumenjakovih vrečk in 34 mm dolgega zarodka morske mačke iz želodca v novembru ujetega morskega prašiča. (Foto: J. Barruil & I. Mate)
Fig. 5: 60 mm small-spotted catshark embryos from the stomach content of the January specimen. (Photo: }. Barruil & I. Male)
SI. S: 60 mm dolgi zarodki morske mačke iz želodca v januarju ujetega morskega prašiča. (Foto:/. Barruil & L Mate)
25
ANNALES • Ser. hist. nat. -11 2001 1 (23)
Joan BARftULL & ;»bel MATE: FIRST CONFIRMED RECORD OF ANGULAR KO'JCHSMAKK OXYNOTVS CEN TRIM «JNNAEUS, 1758) .... 23-26
Tab. 1: Proportional dimensions of the two angular rougbsbarks caught off Barcelona. Tab. 1: Proporcionalne dimenzije dveh morskih prašičev, ujetih v obrežnih vodah Barcelone.
		MZB-2000-1035	MZB-2001 -0006
		Sex (M)	Sex (M)
total length (mm)	TL	555	555
precauda! length	PRC	79.8	80.2
pre-first dorsal length	PD1	19.4	19.1
pre-second dorsal length	PD2	58.4	57.9
first dorsal length	D1L	25.2	22,9
second dorsal length	D2L	14.8	14.9
first dorsal base	DIB	20.9	18.9
second dorsal base	D2B	11.7	10.4
first dorsal inner margin	Dll	43	4.0
second dorsal inner margin	D2I	3.1	4.5
first dorsal height	D1H	12.1	12,6
second dorsal height	D2H	10.3	10.6
first spine length	SI	11.0	13.1
second spine length	S2	8.8	7.4
dorsal caudal margin	C DM	20.7	20.4
preventral caudal margin	CPV	12.1	11.3
terminal caudal lobe	CTL	6.5	6-7
prepectoral length	PP1	18.6	18.5
pectoral anterior margin	P1A	15.5	16.0
pectoral posterior margin	PIP	14.4	14.0
pectoral base	P1B	5.8	4.9
pectoral inner margin	P1I	2,5	4.5
prepelvic length	PP2	62.2	60.9
pelvic length	P2L	10.1	10.8
pelvic anterior margin	P2A	6.7	6.1
clasper outer length	CLO	1.1	1.3
clasper inner length	Cti	5.9	6.1
mouth width	MOW	4.6	4.2
preoral length	POR	4.0	5.4
nostril width	MOW	2.2	3.4
internarial space	INW	1.1	2.5
prenarial length	PRN	2.0	3.6
prespiracular length	PSP	9.4	9.9
preorbitaf length	POB	4.3	7.7
eye length	EYL	4.3	.3.8
eye height	EYH	2.1	2.0
intergill length	INC	4.0	5.1
first gill slit height	GS1	1.3	1.7
fifth gill slit height	CS5	1.5	1.5
ANNALES • Ser. hist. nat. -11 2001 • 1 (23)
lo,™ BARRLflL & Isabel MATE: FÍRST CONFIRMAD RECORD OF ANGULAR ROUCHSHARK OXYNOTUS CONTRINA'Xi NNAEUS 1758».... 24-2»-
PRVI POTRJENI PRIMER OPLENJENEGA JAJČNEGA OVOJA MORSKE MAČKE SCYLIORHINUS CANICULA V TREBUHU MORSKEGA PRAŠIČA OXYNOTUS CENTRINA
(LINNAEUS, 1 758) V SREDOZEMSKEM MORJU
Joan BARRULL & Isabel MATE Lah. Vertebra» Secció Ictiología, Museo Zoología, F-08060 Barcelona. Aptat correus 593 E-mail: jharruli® pie.xtec.es
POVZETEK
Podatki o plenjenju jajčec morskih psov in skatov so razmeroma redki. Nekatere vrste mesojedih polžev lahko vrtajo v zarodke (in se hranijo z njimi) ali vzrejajo zarod v kapsulah oviparnih morskih psov. jajčni ovoji sami pa so bili najdeni v želodcih pravih kostnic, morskih sesalcev in v najmanj eni vrsti živorodnega morskega psa. V tem prispevku avtorja razpravljata o bržkone prvem potrjenem primeru plenjenja zarodkov oviparnega morskega psa v vodah Sredozemskega morja. Dne 10. novembra 2000 in 2. januarja 2001 sta bila z vlečno mrežo ribiške ladje "Maireta I!" (z matičnim pristaniščem v Barceloni) ujela dva 5S0 mm dolga samca morskega prašiča Oxynotus centrina (Linnaeus, 1758) v vodah celinskega pobočja nedaleč od katalonskega obrežja. Ujeta sta bila v globini 192 metrov na ribiški lokaciji, znani kot "La Serola", in sicer 41 2' N, 2°28' E. Oba samca sla bila izročena Zoološkemu muzeju v Barceloni in označena s kataloškima številkama MZB-2000-1035 in MZB-2001 -0006. Pregled želodca enega od morskih prašičev je razkril delce desetih rumenjakovih vrečk in enega zarodka v skupni dolžini 34 mm. Na osnovi primerjav z ilustracijami in morfološkimi opisi Compagna (¡984a), Morena (1995) in Van Grevelvngheja et al. (1999) je bilo ugotovljeno, da je zarodek, z zunanjo rumenjakovo vrečko, pripadal morski mački Scyüorhinus canícula (Linnaeus, 1758). V želodcu drugega morskega prašiča pa sta bila odkrita dva zarodka morske mačke Scyüorhinus canícula v skupni dolžini 60 mm. jajčnih ovojev ni bilo, in prav mogoče je, da je morski prašič jajčno vsebino izsesai
Ta primer bo bržkone pritegnil še nadaljnje zanimanje strokovnjakov, saj je prvi natančno dokumentirani zapis o morskih psih (Elasmobranchii) z uplenjenimi zarodki oviparnega morskega psa v vodah Sredozemskega morja.
Ključne besede: Oxynotus centrina, Scyliorhinus canícula, predatorstvo, jajčni ovoj, zarodki, Sredozemsko morje
REFERENCES
Antonelis, G. A., M. S. Lowry, D. P. De Master & C. H. Fiscus (1987): Assessing northern elephant seal feeding by stomach lavage. Marine Mammal Science, 3, 308322.
Barrull, J. & I. Mate (1996): Els (aurons dels Pai'sos Catalans. Barcelona, Pôrtie, 183 pp. Barrull, J., I. Mate & M. Bueno (1999): Observaciones de tiburones (Chondrichthyes Euselachii) en aguas de Cataluña (Mediterráneo NO), con algunos aspectos generales de su ecología. Scientia gerundensis, 24, 127151.
Capapé, C. (1975): Observations sur le régime alimentarle de 29 Sélaciens pieurotrémes des côtes tunisiennes. Arch. Inst. Pasteur Tunis, 52(4), 395-414. Capapé, C. (1977): Contribution à la biologie des Scyliorhinidae des côtes tunisiennes. (. Scyliorhinus canícula (Linné, 1758): répartition géographique et bathymétrique, sexualité, reproduction, fécondité. Bull Off. Natn Pêch. Tunisie, 2(1-2), 109-140.
Capapé, C., A. A. Seek & J. P. Quignard (1999): Observations on the reproductive biology of the angular rough shark, Oxynotus centnna (Oxynotidae). Cybium, 23(3), 259-271.
Capapé, C, }. A. Tomasini & J. P. Quignard (2000): Les
Elasmobranches Pleurotrémes de la Côte du Languedoc (France Méridionale): Observations biologiques et démographiques. Vie et Milieu, 50(2), 123-133. Compagno, L. ). V (1984a): F AO species catalogue. Vol. 4. Sharks of the world. An annotated and illustrated catalogue of shark species known to date. Pari 1. Hex-anchiformes to Lamniformes. FAO Fish. Synop., 125(4), 1-249.
Compagno, L. J. V (1984b): FAO species catalogue. Vol. 4. Sharks of the world. An annotated and illustrated catalogue of shark species known to date. Part 2. Car-charhiniformes. FAO Fish. Synop., 125(4), 251-655. Cox, D. L. & T. J. Koob (1993): Prédation on elasmo-branch eggs. Environmental Biology of Fishes, 38, 117125.
27
ANNALES • Ser. hist. nat. 11 • 2001 I (23)
Joan BARRULl & Isabel MATE; flRST CONflftMÍO RECORD OF ANGULAR ROUCHSHARK ÜXYNOWS CMTRINA (LINNAEUS, 1758}..., 23-28
Condit, R. & B. |. Le Boeuf (1984): Feeding habits and feeding grounds of the northern elephant seal. Journal of Mammalogy, 65, 281-290.
Grover, C. A. (1972): Prédation on egg-cases of the swell shark, CephaloscyMum ventriosum. Copeia, 1972, 871-872.
Jones, R. E. (1981): Food habits of smaller marine mammals from northern California. Proceedings of the California Academy of Sciences, 42, 409-433. Long, D. J. (1996): First confirmed record of teleost prédation on a shark egg case. California Fish and Game, 82(2), ¡03-104.
Mc Laughlin, R. H. & A. K. O'Gower (1971): Life history and underwater studies of a heterodont shark. Ecological monographs, 41, 271-289.
Morejohn, G. V. & D. M. Bait* (1970): Contents of the stomach of an elephant seal, journal of Mammalogy, 51, 173-174.
Moreno, J. A. (1995): Guía de los tiburones de aguas ibéricas, Atlántico Nororiental y Mediterráneo. Pirámide, Madrid, 310 pp.
Moreno, J. A. & A. Hoyos (1982): La reproducción de los tiburones. Quercus, 7, 28-30. Sinclair, E. H. (1994): Prey of juvenile northern elephant seals (Mirounga angustirostris) in the Southern California Bight. Marine Mammals Science, 10, 230-239. Van Grevelynghe, G., A. Diringer & B. Séret (1999): Tous les requins du monde. Ed. Delachaux et Niestié, Lausanne, 336 pp.
28