Findings of elasmobranch eggs in the stomachs of sperm whales and by luckboy


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									J. Mar. Biol. Ass. U.K. (2003), 83, 1351^1353 Printed in the United Kingdom

Findings of elasmobranch eggs in the stomachs of sperm whales and other marine organisms
P.H.F. Bor*P and M.B. SantosO
*Lepelaarsoord 6, 2317 XK Leiden, The Netherlands. ODepartment of Zoology, University of Aberdeen, Tillydrone Avenue, Aberdeen, Scotland, AB24 2TZ. PCorresponding author, e-mail:

The ¢rst records of thorny skate eggs in stomachs of sperm whales are described. Predation on elasmobranch eggs, especially by marine mammals, is reviewed.

The tough, leathery shell of elasmobranch eggs would seem to provide a good protection against predators. However, elasmobranch eggs are preyed on by a variety of marine animals (see Appendix 1). Several species of gastropods make holes in the egg-shell to be able to consume the contents (e.g. Ansell, 1961; Cox & Koob, 1991; Smith & Gri⁄ths, 1997; Bor, 2002). There is one record of a sea urchin, Strongylocentrotus droebachiensis (Mˇller, 1776), preying on skate eggs (Cox & Koob, 1991). Complete elasmobranch eggs have been found in the stomach contents of several species of bony ¢sh (e.g. Jensen, 1914; Long, 1996), elasmobranchs (e.g. Jensen, 1914; Varoujean, 1972), northern elephant seal, Mirounga angustirostris (Gill, 1866) (e.g. Morejohn & Baltz, 1971; Jones, 1981; Sinclair, 1994; Antonelis et al., 1998), northern sea lion, Eumetopias jubatus (Schreber, 1776) (Bonnot, 1928) and sperm whale, Physeter macrocephalus L., 1758 (Cox & Koob, 1993; Santos et al., 1999). There are records of only two non-marine mammal species eating elasmobranch eggs. Chacma baboons, Papio ursinus (Kerr, 1792) have been ¢lmed while eating shark eggs (see Appendix 1). Winkler (1882) refers to humans eating elasmobranch eggs, citing Wood (‘an English writer’), who wrote that English ¢shermen boiled skate eggs and ate them. It is uncertain if this last record is trustworthy, since according to Winkler, Wood himself expressed some doubts about the story! Findings of elasmobranch eggs in sperm whale stomachs are scarce. Cox & Koob (1993) mention two eggs of Raja rhina Jordan & Gilbert, 1880, found in the stomach of a sperm whale landed at the whaling station, Field’s Landing, California (USA) on 11 April 1951. A sperm whale stranded at Cod¢sh Park (Massachusetts, USA) on 29 December 1997 was also reported as containing ‘skate egg sacs’ (see Appendix 1). More recently, Santos et al. (1999) published descriptions of the stomach contents of sperm whales stranded in the north-east Atlantic. Skate eggs were found twice, both in sperm whales stranded on the Scottish coast. One egg was recorded in a sperm whale stranded on 23 March 1995 at Nairn (Highland, OS grid reference, NH 796586), the other in one of six sperm whales stranded on 28 January 1996 at Cruden Bay (Grampian, OS grid reference, MK 084345). Santos et al. (1999) did not identify the skate eggs to species. Renewed study of these eggs
Journal of the Marine Biological Association of the United Kingdom (2003)

revealed that they both belong to the thorny skate, Amblyraja radiata (Donovan, 1808). Although this is not the ¢rst time that skate eggs have been found in stomachs of sperm whales, they are, however, the ¢rst records for eggs of A. radiata. There are two possible explanations for the way in which the skate eggs got into the sperm whale stomachs: (1) skate eggs are laid at the sea-bottom, from where the sperm whales could have picked them up (actively, by feeding on them, or accidentally, when pursuing other prey); (2) the sperm whales could have ingested the eggs with a gravid female skate (the eggs may have been laid by the female under stress conditions while being eaten or the eggs may survive longer than £esh in the sperm whale stomach). It seems very unlikely that sperm whales actively prey on A. radiata eggs with a length of a few centimetres (4.3 and 4.1cm respectively, without horns). It is possible that the sperm whales picked up the eggs when pursuing larger prey near the sea-bottom. However, the most plausible explanation is that the sperm whales took the eggs with a gravid female skate. Cox & Koob (1993) found two almost identical Raja rhina eggs in a sperm whale stomach and suggested that they had been ingested with a single female skate. The A. radiata eggs found in the two sperm whales di¡er somewhat in colour and one had fresh yolk inside while the other contained only traces of yolk. Skates usually produce two eggs at the same time. In these two cases the twin-eggs were not found, maybe because not all the stomach contents could be studied (see Santos et al., 1999). Since elasmobranchs lack bone or otoliths, hard remains of these ¢sh are rarely found in stomach contents or faeces of their marine mammal predators. Dermal scutes of skates however, have been recorded in seal faeces in the UK (e.g. Pierce et al., 1990).
We would like to thank Steve Spina, Connie Merigo (both New England Aquarium), Marianne Stanton (Inquirer and Mirror) and Andy Horton for their contributions to this article. Also we would like to thank Trish Cairns-Bristol (BBC) and Arjan Hoogesteger for help with locating the ‘baboon eating shark eggs’ movie. Martien van Oijen (curator of ¢shes, National Museum of Natural History, Leiden) and Graham Pierce are warmly thanked for improving earlier versions of this manuscript. The ¢rst author would like to express his gratitude to the


P.H.F. Bor and M.B. Santos

Findings of elasmobranch eggs in the stomachs of sperm whales
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 con¢rmed record of teleost predation on a shark egg case. California Fish and Game, 82, 103^104. McEachran, J.D., Boesch, D.F. & Musick, J.A., 1976. Food division within two sympatric species-pairs of skates (Pisces: Rajidae). Marine Biology, 35, 301^317. McLaughlin, R.H. & O’Gower, A.K., 1971. Life history and underwater studies of a heterodont shark. Ecological Monographs, 41, 271^289. Morejohn, G.V & Baltz, D.M., 1970. Contents of the stomach of . an elephant seal. Journal of Mammology, 51, 173^174. Nichols, J.T., 1931. Egg capsule of Scyliorhinus retifer. Copeia, 1931, 38^39. Pierce, G.J., Boyle, P.R. & Thompson, P.M., 1990. Diet selection by seals. In T rophic relations in the marine environment. Proceedings of the 24th European Marine Biology Symposium (ed. M. Barnes & R.N. Gibson), pp. 222^238. Aberdeen: Aberdeen University Press. Santos, M.B. et al., 1999. Stomach contents of sperm whales Physeter macrocephalus stranded in the North Sea 1990^1996. Marine Ecology Progress Series, 183, 281^294. Sinclair, E.H., 1994. Prey of juvenile northern elephant seals (Mirounga angustirostris) in the Southern California Bight. Marine Mammal Science, 10, 230^239. Smith, C. & Gri⁄ths, C., 1997. Shark and skate egg-cases cast up on two South African beaches and their rates of hatching success, or causes of death. South AfricanJournal of Zoology, 32, 112^117. Varoujean, D.H., 1972. Systematics of the genus Echinorhinus Blainville, based on a study of the prickly shark Echinorhinus cookei Pietschmann. MSc thesis, Fresno State College, Fresno, California, USA. Winkler,T.C.,1882. Gids op het strand. Haarlem: De Erven Loosjes.
Submitted 3 September 2002. Accepted 28 September 2003.

sta¡ of the library of the National Museum of Natural History, Leiden, for the help in ¢nding ‘di⁄cult’ literature.

Ansell, A.D., 1961. Egg capsules of the dog¢sh (Scylliorhinus canicula, L.) bored by Natica (Gastropoda, Prosobranchia). Proceedings of the Malacological Society of London, 34, 248^249. Antonelis, G.A., Lowry, M.S., DeMaster, D.P. & Fiscus, C.H., 1987. Assessing northern elephant seal feeding by stomach lavage. Marine Mammal Science, 3, 308^322. Barrull, J. & Mate, I., 2001. First con¢rmed record of Angular Roughshark Oxynotus centrina (Linnaeus, 1758) predation on shark egg case of small-spotted catshark Scyliorhinus canicula (Linnaeus, 1758) in Mediterranean waters. Annales, Series Historia Naturalis, 11, 23^28. Bonnot, P., 1928. Report on the seals and sea lions of California. Fishery Bulletin, State of California Division of Fish and Game, 14, 1^61. Bor, P.H.F., 2002. Predatie door slakken op eieren van haaien en roggen. Spirula, 326, 44^46. Condit, R. & Le Boeuf, B.J., 1984. Feeding habits and feeding grounds of the northern elephant seal. Journal of Mammalogy, 65, 281^290. Cox, D.L. & Koob, T.J., 1991. Predation on eggs of the little skate (Raja erinacea) in the gulf of Maine. Bulletin of the Mount Desert Island Biological Laboratory, 30, 123^124. Cox, D.L. & Koob, T.J., 1993. Predation on elasmobranch eggs. Environmental Biology of Fishes, 38, 117^125. Cox, D.L., Walker, P. & Koob, T.J., 1999. Predation on eggs of the thorny skate. Transactions of the American Fisheries Society, 128, 380^384. Jensen, A.S., 1914. The selachians of Greenland. Mindeskrift Japetus Steenstrup FÖds, 2, 1^40.

Journal of the Marine Biological Association of the United Kingdom (2003)

Findings of elasmobranch eggs in the stomachs of sperm whales Appendix 1. Summary of predators on chondrichthyan eggs.
Mollusca Natica alderi, N. catena, N. montagui, N. pusilla, N. sordida Buccinum undatum Burnupena papyracea, B. lagenaria

P.H.F. Bor and M.B. Santos 1353




Scyliorhinus canicula

Ansell (1961)

predator not established, all ¢ve Natica spp. as possible predators not Buccinum undulatum predation only established for Haploblepharus eggs in aquarium conditions

Cypraea spadicea Unknown gastropod Unknown gastropod Unknown gastropod

Leucoraja erinacea Haploblepharus pictus, H. edwardsii, H. fuscus, Poroderma pantherinum, P. africanum, Rostroraja alba, Raja miraletus, Raja cf. clavata (?Raja strealeni), Raja sp., Callorhinchus capensis Heterodontus francisci Heterodontus portusjacksoni

Cox & Koob (1991, 1993) Smith & Gri⁄ths (1997)

Unknown gastropod Echinodermata Strongylocentrotus droebachiensis Elasmobranchii Echinorhinus cookei Oxynotus centrina Somniosus microcephalus Unknown sharks Amblyraja radiata Actinopterygii ‘halibut (and other ¢shes)’ ‘sea bass’ Hexagrammos decagrammus Pimelometopon pulchrum

Cephaloscyllium ventriosum Raja eglanteria, Cephaloscyllium ventriosum, and several other species from museum samples (Bathyraja trachura, B. parmifera, Leucoraja erinacea, Raja diaphanes, Raja sp., Scyliorhinus boa, Scyliorhinus sp., Parmaturus xanurius, Apristurus brunneus, Apristurus sp., Cephaloscyllium ventriosum) Amblyraja radiata Cox et al. (1999)

Bor (2002) McLaughlin & O’Gower (1971) Grover (1972) Cox & Koob (1993)

‘a gastropod of the order Stenoglossa’

‘naticid and muricid gastropods’

Leucoraja erinacea

Cox & Koob (1991)

Apristurus brunneus Scyliorhinus canicula Amblyraja hyperborea Bathyraja spinicauda (?) Malacoraja senta

Varoujean (1972) Barrull & Mate (2001) Jensen (1914) Jensen (1914) McEachran et al. (1976)

as discussed in Long (1996) no egg-capsules found, only embryos also discussed in Clarck (1922)

Amblyraja radiata Scyliorhinus retifer (?) Apristurus brunneus Cephaloscyllium ventriosum, Heterodontus francisci

Jensen (1914) Nichols (1931) Long (1996) Grover (1972)

also discussed in Clarck (1922) also discussed in Long (1996) seen biting and puncturing eggs in an aquarium

Mammalia Mirounga angustirostris

Apristurus brunneus

Eumetopias jubatus Physeter macrocephalus

Cephaloscyllium ventriosum and an unidenti¢ed species Heterodontus francisci, Cephaloscyllium ventriosum, Raja binoculata, Raja sp. ‘greenish colored eggs of a skate or shark’ Raja rhina ‘skate egg’ ‘skate egg sacs’ ‘shark eggs’

Morejohn & Baltz (1970), Jones (1981), Condit & Le Boeuf (1984) Antonelis et al. (1987) Sinclair (1994) Bonnot (1928) Cox & Koob (1993) Santos et al. (1999)

Papio ursinus

Homo sapiens

‘skate eggs’

Winkler (1882)

also discussed in this article 021998/0219pg-8.html programmes/tv/wildafrica/ picpops/diary___jan___pop1.shtml English ¢shermen; according to ‘an English writer called Wood’, not sure if this is fact or ¢ction

Journal of the Marine Biological Association of the United Kingdom (2003)

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