Papers 121 PARASITES AND DISEASES OF THE AUKS (ALCIDAE) OF THE WORLD AND THEIR ECOLOGY—A REVIEW SABIR BIN MUZAFFAR & IAN L. JONES Department of Biology, Memorial University of Newfoundland, St John’s, Newfoundland, A1B 3X9, Canada ([email protected]) Received 1 March 2004, accepted 1 June 2004 SUMMARY MUZAFFAR, S.B. & JONES, I.L. 2004. Parasites and diseases of the auks (Alcidae) of the world and their ecology—a review. Marine Ornithology 32: 121–146. We reviewed all the organisms that are known to parasitize auks (Aves: Alcidae). Of the 23 extant auk species, parasites have been described from 19 species; no published information was found on parasites of Xantus’s Murrelet Synthliboramphus hypoleucus,Craveri’s Murrelet S. craveri, the Japanese Murrelet S. wumizusume or the Long-billed Murrelet Brachyramphus perdix. Our survey identified 184 taxa parasitic or pathogenic on auks. Endoparasitic microorganisms included 21 viruses, 13 bacteria, 3 dinoflagellates, 6 protozoa and 3 fungi. Other endoparasitic organisms included 57 platyhelminth (34 digenean, 23 cestode), 9 acanthocephalan and 22 nematode taxa. Ectoparasites (all arthropods) included 2 pentastomid, 14 acari and 30 insect taxa. We reviewed published information on the effects that these parasites have on the biology of auks. Most studies did not investigate relationships between the ecology, the breeding condition or the physiologic state of the birds and the presence of parasites. Even though episodes of mass mortality of seabirds are periodically recorded, few of those episodes have been exclusively linked to parasitic infestations. Viral isolates from auks have been recorded from several breeding colonies, but their epizootiologic consequences are unknown. Bacterial isolates, of which the most noteworthy species is the Lyme disease–causing agent Borrelia burgdorferi (sensu lato), have been recorded in auks and their tick ectoparasite Ixodes uriae. A few life cycles of digeneans and cestodes recorded from auks have been determined. Growing evidence indicates prey switching by auk species alters their endoparasitic fauna. Ectoparasitic organisms often play a role in transmitting endoparasites and may affect the reproductive success of their hosts. Some links have been clearly established; many others are only implied and urgently need close attention. The role of parasitism in host population dynamics and as reservoirs is discussed in the context of seabird ecology as a whole. Key words: Charadriiformes, Alcidae, ectoparasite, endoparasite, disease INTRODUCTION rarely been studied in detail (Petermann et al. 1989, Debacker et al. 1997), and the influence of diseases on seabird populations remains Parasites play a very important part in the lives of their hosts unclear (Gauthier-Clerc et al. 2003). (Rothschild & Clay 1957, Dogiel 1964). Nevertheless, relative to the enormous diversity in the multitude of parasites that live in or The general lack of information on seabird parasites applies on wild birds (Loye & Zuk 1991, Fowler 1993, Clayton & Moore equally to the Alcidae (auks or alcids). Although behavior, ecology 1997), little information is available on the intricate life cycles of and physiology are well known (reviewed by Gaston & Jones those parasites. Information on parasitic acari, for example, is 1998), relatively few studies have documented the incidence of limited to conspicuous taxa that are readily captured and isolated parasites and their influence on their hosts (Eveleigh 1974, from their hosts. Less-evident parasitic organisms, whether internal Eveleigh & Threlfall 1976, Fitzpatrick & Threlfall 1977, Choe & or external, are usually overlooked, and their complex interactions Kim 1987, Hoberg 1996, Muzaffar 2000). and potential influence on host life cycles are largely unknown. Parasites may incur costs for their avian hosts and are often Individual seabirds in breeding colonies may expose one another to regarded as an important drawback to colonial breeding (Brown & a multitude of viruses and bacteria (e.g. Oprandy et al. 1988, Gylfe Brown 1986). et al. 1999). Many seabirds, including the auks, breed during summer in large colonies (Gaston & Jones 1998) that also serve as Nest ectoparasites may reduce breeding success in Cliff Swallows ideal habitats for ectoparasites (e.g. Eveleigh & Threlfall 1975, Hirundo pyrrhonota (Brown & Brown 1986, 1996). Ectoparasites Clifford 1979). Many parasitic species have become highly have been shown to cause nest desertion and chick mortality in a specialized in synchronizing their life cycles with their hosts’ range of seabirds (Feare 1976; King et al. 1977a, 1977b; Duffy breeding phenology (e.g. Eveleigh & Threlfall 1975, Clifford 1979, 1983, 1991). There is also clear evidence of the impact of Lvov 1980, Hoberg 1996, Gylfe et al. 1999, McCoy & Tirard ectoparasites on seabird reproductive success and population 2002). However, most auk species spend the greater part of the year dynamics (Boulinier & Danchin 1996, Gauthier–Clerc et al. 1998, dispersed at open sea where transmission and survival of parasites Bergström et al. 1999, Boulinier et al. 2001, Mangin et al. 2003). represents a major challenge. Nevertheless, foraging behavior and Outbreaks of disease likely related to parasitic infestations have diet facilitate the transmission of a variety of endoparasites through Marine Ornithology 32: 121–146 (2004) 122 Muzaffar & Jones: Parasites and diseases of the auks marine invertebrate and vertebrate species, although those The existence of active foci of viruses in the low Arctic latitudes is parasites, too, are better transmitted during the breeding season governed by adaptations of the viruses and the tick vectors to because of the abundance of marine littoral intermediate hosts environmental extremes (Lvov 1980). Murres in the low Arctic, for (Hoberg 1996). instance, may have tick prevalences of 10%–45%, increasing to as high as 100% in chicks (Lvov et al. 1979, Lvov 1980). With The objectives of our study were infestations of as many as 1000 ticks per bird, a means exists for • to present a review of the diversity of diseases and parasites of build-up and active exchange of viruses in the host population. alcids as reported in the literature, and Viruses, along with their tick hosts, overwinter within the rocks or • to highlight key studies documenting the ecology of the substrate of the auk colony site at depths of up to 40 cm, where host–parasite interactions and their relationship to the marine temperatures are adequate for their continued survival. Viruses environment. have been known to remain active in ticks for more than two years (Lvov et al. 1979). Viremic birds may also represent a source of TAXONOMY infection to a colony during the breeding season, but evidence to suggest that the viruses may overwinter in their seabird hosts is The literature exhibits some taxonomic uncertainty, particularly for lacking (Lvov et al. 1979, Lvov 1980). the helminth fauna of alcids. Our account is based on a search of the literature for the period 1899–2003 (including review papers), Bacterial infections and it clumps organisms into easily recognizable taxonomic A wide range of bacterial infections occur in free-ranging birds. groups. However, given that systematics and taxonomy vary among Such infections are regarded as important causes of morbidity and the groups, the taxonomic groupings are not consistent. Bacteria, mortality (Davis et al. 1971, Steele & Galton 1971). for example, form a Kingdom, whereas the Eucestoda represents a Class. We attempt to identify genera and species wherever possible. Escherichia coli is generally part of the natural intestinal flora of We also attempt to classify organisms in tables, and we provide birds, and it may cause disease in conjunction with other infections notes explaining taxonomic ambiguity wherever necessary. (e.g. Morishita et al. 1999). Infections with E. coli were recorded in 14% of the murres (Uria spp.) collected in a German study PARASITES AND DISEASES OF THE AUKS (Petermann et al. 1989). Viruses Pasteurella multocida, the causative agent of the contagious avian Ticks of the family Argasidae and Ixodidae are widely distributed cholera may occur as both a chronic and an acute infection in free- and are often associated with auks (Clifford 1979). The life cycles ranging birds, often leading to death (Friend & Franson 1999). It of seabird ticks tend to be closely attuned to seabird breeding has also been recorded from murres (Petermann et al. 1989). seasons [e.g. McCoy & Tirard 2002 (see the later discussion of ectoparasites]). Generally, Ixodes uriae (Ixodidae) serve as the An earlier study, also in Germany, prompted by an outbreak of primary vectors in more northern latitudes; Ornithodoros spp. Salmonella paratyphi B infections in humans, revealed heavily (Argasidae) play the same role in more temperate southern contaminated seawater in seabird feeding areas (Steineger & Hahn locations (Clifford 1979, Lvov 1980). 1953). Subsequently, isolates of the bacterium from droppings of Razorbill Alca torda, Common Murre U. aalge and gull (Larus I. uriae have been collected from seabird colonies in Russia (Lvov spp.) were reported, suggesting that foraging areas may be et al. 1979, Lvov 1980) and from the west and east coasts of North important in the spread of bacterial infections. America (Yunker 1975, Main et al. 1973, Oprandy et al. 1988). Viral isolation techniques from argasid and ixodid (mostly I. uriae) A long-term study on beached Common Murres on the Belgian ticks