S39.4: The significance of parasite loads in intertidal and freshwater invertebrates for their shorebird predators

¹Université de Montréal, Québec, Canada, e-mail mcneilr@ere.umontreal.ca; ²Universidad de Oriente, Cumaná, Sucre, Venezuela

Many invertebrate prey of shorebirds, both in freshwater and intertidal environments, are infested by helminth endoparasites (see Swennen 1969; Helluy 1983b; Curtis 1987; Jensen & Mouritsen 1992; Bick 1994; Mouritsen et al. 1997). Consequently, members of various shorebird species are often heavily infested with helminths (Cable et al. 1960; Loftin 1960; Threlfall 1963, 1968; Schmidt & Neiland 1968; Cabot 1969a, 1969b; Dronen & Badley 1979; Tallman et al. 1985; Goater & Bush 1988; Mariaux 1989; Ching 1990; McNeil et al. 1995, 1996).

Helminths (Platyhelminthes, Nematoda and Acanthocephala) typically parasitise vertebrates, although invertebrates, particularly arthropods and mollucs, act as intermediate hosts (see Smyth 1962). The Platyhelminthes that parasitise shorebirds are restricted to two groups: the Digenean Trematoda and the Cestoda. The Digenea (flukes) are found in strong and persistent association with aquatic habitats. They have complex life-cycles, typically with a molluscan primary host in which multiplication occurs, an intermediate transport host, and a vertebrate final host (Erasmus 1972). The Cestoda (tapeworms), in the adult stage, parasite the intestines of vertebrates; they also have complex life cycles with two or more hosts (Erasmus 1972). Many NEMATODA (roundworms) are free-living in soil and water but many others have intermediate stages in arthropods or are parasites in the tissues and fluids of plants and animals (Storer & Usinger 1957). The larvae of the ACANTHOCEPHALA (spiny-headed worms) occur in arthropods, but the adults parasitize the intestines of vertebrates (Storer & Usinger 1957).

According to Bush et al. (1990), the species richness of the helminth parasite community is, on average, lower in terrestrial hosts than in aquatic ones. The mean number of helminth species reported from different classes of aquatic hosts within vertebrates increases from fishes through herptiles to birds, declining slightly in mammals. Because migratory birds, in contrast to resident forms, are exposed to more than a single environment and its parasites, we should expect migratory species to have more severe infections, to allocate relatively more resources to anti-parasite defence, and to invest more in immune defence than closely related resident species (Møller & Erritzøe 1999).

In the case of most helminths, and particularly the Digeneans, the life-cycle (Fig. 1) involves larval transmission between two intermediate host-species. The two hosts, usually from different trophic levels, are used in an obligatory sequence by the parasite in order to reach the target host, where they mature and reproduce (see Dobson 1988, Combes 1991). Parasites have adopted a variety of evolutionary strategies and mechanisms that increase the chances of encounters between the infective stages of the parasites and the hosts. Transmission enhancement strategies are common in the methods used by helminths for reaching definitive hosts within different groups of vertebrate animals (e.g. see Holmes & Bethel 1972; Helluy 1983a, 1983b; Dobson 1988; Hurd 1990; Moore 1984; Milinski 1990; Moore & Gotelli 1990; Combes 1980, 1991). They appear to be examples of convergent evolution, since the same strategies have evolved in three groups of helminths (Cestoda, Trematoda and Acanthocephala) using Chaetognatha, Mollusca, Crustacea and Insecta as intermediate hosts to reach fishes, birds or mammals as final definitive hosts (see Helluy 1983a).

This review provides examples of the various transmission enhancement strategies adopted by helminths that use invertebrates of intertidal environments as intermediate hosts, and shorebirds as final definitive hosts, and attempts to elucidate the consequences for shorebird survival, migration capacity, and reproductive success.

There are many examples of helminths producing pathological conditions in their intermediate hosts (see Williams 1967; Beck & Beverley-Burton 1968; Smyth & Heath 1970; Holmes & Bethel 1972). The behaviour of a sick host could benefit the parasites (Robb & Reid 1996). Indeed, diseased or weak animals are more vulnerable than healthy ones and a sluggish intermediate host may have difficulty in escaping a predator (Holmes & Bethel 1972; Moore & Gotelli 1990). Transmission to the definitive host may thus be favoured by a strategy by which parasites decrease the stamina of the prey or affect its ability to respond to the predator (Holmes & Bethel 1972). For example, Moore (1984) found that all spiny-headed worms altered intermediate host behaviour in a way that increased their vulnerability to predators.

Reduced vision in fish hosts infested with Diplostomum species

One possible example affecting shorebirds in freshwater habitats is that of some digenean Diplostomum species whose cercariae leave the snails (first intermediate hosts), penetrate suitable fish hosts and migrate to the eye where they develop into metacercariae in the crystalline lens (see Erasmus 1972; Crowden & Broom 1980). The presence of these metacercariae may interfere with vision of fish which depend on it for food detection, thus reducing their feeding efficiency (which needs to be compensated by increasing the time spent feeding) and making them more susceptible to predation by birds which act as definitive hosts (Erasmus 1972; Crowden & Broom 1980; Milinski 1990). Many shorebird species, particularly the Tringa species like the Greater Yellowlegs (T. melanoleuca), occur in freshwater habitats and frequently forage on small fish in shallow waters (see Sperry & Cottam 1944; Reeder 1951; Robert & McNeil 1989; Piersma et al. 1996). The genus Diplostomum is known to infest the alimentary canal of Tringa species (see McNeil et al. 1995, 1996).

In some cases, the infecting stage is released when host activity favours infestation (see Combes 1980). This favours transmission between intermediate hosts, or to the definitive ones. In other cases, infested prey and potential final definitive hosts are at their maximum numbers at the same time of the year.

Dogwhelks Thais lapillus and the trematode Parorchis acanthus

Dogwhelks Thais lapillus, molluscs that form part of the diet of Eurasian Oystercatchers Haematopus ostralegus, especially during the autumn and spring (Feare 1971), act in some regions as the first intermediate hosts for the trematode Parorchis acanthus, known in the adult stage to infest several shorebird species (Cable et al. 1960; Loftin 1960; Schmidt & Neiland 1968; Dronen & Badley 1979; Ching 1990; McNeil et al. 1995). Although in most cases predation by birds of the first intermediate host of a trematode does not allow the life cycle to continue, the cercariae may encyst on the shells of molluscs, including Thais, and be infective in this state (see Moore & Gotelli 1990). Infested dogwhelks experience higher predation rates by oystercatchers than uninfested ones, but do not appear to be selected for having slower reaction times in withdrawing into their shell after disturbance (Feare 1971). Dogwhelks are not normally an important prey for oystercatchers in winter as they aggregate in crevices, clefts and pools where they are safe from the birds. However, those infested with P. acanthus delay forming aggregations in the autumn; they are thus vulnerable to the birds for longer and are plentiful on open rocky shores at the time when large numbers of oystercatchers and other shorebirds, including non-immunised juveniles, are arriving from their breeding grounds (Feare 1971). This delay in forming winter aggregations may explain why infested molluscs experience higher predation than uninfested ones and is of survival value to the parasite.

Seasonal variation in the trematode prevalence of Corophium volutator

Another example is that of the parasites of the amphipod Corophium volutator, a prey of various shorebird species (Prater 1972; Goss-Custard et al. 1977; Goss-Custard 1979, 1983; Hicklin & Smith 1979; Peer et al. 1986; Durell & Kelly 1990; Mouritsen 1994) and which acts as second intermediate host for the trematodes Levinseniella brachysoma and Maritrema subdolum (Bick 1994). These parasites occur in less than 10% Corophium in the spring, but in almost 100% in late summer and autumn (Bick 1994; see also Mouritsen et al. 1997). Both parasite species are known to infest shorebirds which act as definitive hosts (Cable et al. 1960; Threlfall 1963; Cabot 1969a, 1969b; Ching 1990). This increase in the prevalence of both parasites in the autumn when large numbers of shorebirds, including non-immunised juveniles, are arriving from their breeding grounds may be of survival value for the parasites.

Another strategy employed by parasites is to act in such a way that the habitat occupied by the prey (intermediate host) overlaps that used by the predator (final definitive host) (see Holmes & Bethel 1972). There are many examples of helminth-infested prey in contrast to non-infested ones frequenting shallower waters near the shore, or swimming near the water surface where birds are feeding (see Holmes & Bethel 1972; Combes 1980; Helluy 1983a; Bartoli & Prévot 1986; Milinski 1990; Moore & Gotelli 1990). This implies movement to locations where potential hosts are more likely to occur (Combes 1980). Such behavioural changes make infested prey more vulnerable to predation by birds (Holmes & Bethel 1972). However, they may not always be a direct result of natural selection but, at least in part, may result from other aspects of the host-parasite association such as, for example, parasite-induced increased oxygen demand forcing the potential prey to move closer to water surfaces (see Milinski 1990; Moore & Gotelli 1990).

Estuarine snails Ilyanassa obsoleta and the trematode Gynaecotyla adunca

Estuarine snails Ilyanassa obsoleta bearing larvae of the trematode Gynaecotyla adunca behave differently to conspecifics lacking this parasite. Indeed, following high tides and especially at night, infested snails leave their non-infested conspecifics at lower tidal levels and crawl up onto beaches and sandbars where cercariae, upon release, encyst as metacercariae in semiterrestrial crustaceans such as sand hopper amphipods (e.g. Talorchestia longicornis and T. megalopthalmia) and fiddler crabs Uca sp. before developing to the adult final stage in shorebirds (Curtis 1987). These amphipods are common prey of a variety of plovers and sandpipers (Rankin 1940; Curtis 1987) and the Uca crabs are preyed upon by Charadrius and Numenius species and the Willet Catoptrophorus semipalmatus (see Strauch & Abele 1979; Thibault & McNeil 1994, 1995; McNeil & Rompré 1995). This trematode genus is known to parasitise shorebirds like the Ruddy Turnstone Arenaria interpres, the Wilson's Plover Charadrius wilsonia, the Sanderling Calidris alba, and the Willet (Hunter 1952; Loftin 1960). The altered behaviour of the snails can be considered as unusual because it favours host-to-host transmission by cercariae rather than enhanced predation on prey infested by metacercariae, the commonly recognised consequence of parasitic modification of host behaviour (see Curtis 1987). The process by which trematodes modify the behaviour of infested snails increases the parasite’s prevalence in the prey of the shorebirds and in the areas where the latter forage, and is therefore beneficial to the parasites.

Location of Macoma balthica infested with Parvatrema affinis

In some parts of their geographical ranges, various shorebird species regularly prey on the mollusc Macoma balthica (Swennen 1969; Prater 1972; Goss-Custard et al. 1977; Pienkowski 1982; Goss-Custard 1983; Hulscher 1982; Worrall 1984; Durell & Kelly 1990; Michaud & Ferron 1990; Lim & Green 1991; Zwarts & Blomert 1992; Mouritsen 1994). Larger Macoma are more heavily infested with the trematode Parvatrema affinis than are smaller ones (i.e. they contain more sporocysts) and are almost all confined to the higher parts of the intertidal zone where most shorebirds forage (Hulscher 1973, 1982; Swennen & Ching 1974; Lim & Green 1991). This distribution may increase the chances of the parasite reaching the adult stage in the final hosts, and can be considered as beneficial to the trematodes. The final stage of P. affinis has been found in various waterbirds, including the European Oystercatcher (Loos-Frank 1971; cited by Swennen & Ching 1974).

Induced changes in host appearance by increasing conspicuousness may in some cases increase the likelihood of intentional ingestion by the definitive hosts (see Holmes & Bethel 1972, Hurd 1990). Such changes may result from counter-mimetism in some animals (Combes 1980) but in others may be a consequence of parasite-induced changes in behaviour (including hyperactivity and disorientation), making them more vulnerable to predators (Holmes & Bethel 1972, Moore & Gotelli 1990).

U-shaped crawling tracks of Macoma balthica

The classical example quoted in many review papers is that dealing with M. balthica. This small bivalve, regularly preyed upon by shorebirds (see above), is known to make U-shaped crawling tracks during ebb tide on the sediment surface at higher levels of the intertidal zones at various sites along the Dutch coast and in the Wadden Sea, as well as in Hudson Bay (Swennen 1969; Hulscher 1982; Lim & Green 1991). This track-making behaviour has been linked by Swennen (1969), Swennen & Ching (1974), and Hulscher (1973, 1982) with high infestation with P. affinis. Indeed, Swennen (1969) and Hulscher (1973) reported that 100% of the clams that made these crawling tracks were infested with this trematode. Macoma serves as intermediate host, and shorebirds as final definitive hosts, of this parasite. On intertidal sand flats of Hudson Bay, Lim & Green (1991) found that not all crawling specimens were parasitized but that crawling clams were more heavily infested than buried ones. The crawling behaviour can be considered as making clams more conspicuous and thus as a parasite-induced behavioural change promoting the parasites' transmission to the shorebirds that act as final hosts (Swennen 1969; Hulscher 1973, 1982). However, this interpretation was seriously questioned by Mouritsen (1997). Indeed, he found that both crawling and buried Macoma were present on the intertidal flats of the White Sea in Russia, but that all appeared entirely free of trematodes or other types of macroparasites. It is possible that the high parasite prevalence usually observed among crawlers elsewhere is a consequence, rather than the cause, of the behaviour. Crawling specimens could represent a group of retarded animals that, in order to accelerate growth and gonad development, optimise deposit-feeding at the expense of anti-predator behaviour, and therefore move frequently to encounter unexploited food resources (Mouritsen 1997). Thus altered behaviour which incidentally favours parasite transmission efficiency is not always a direct result of natural selection but may sometimes be a side-effect of some of the host requirements such as satisfying its energy demands. Nevertheless, in regions like the Wadden Sea where crawlers dominate among infested individuals, the conspicuous behaviour of M. balthica may indeed favour the transmission of P. affinis to shorebirds and other waterbirds that feed on this clam species.

Increased surface activity of Corophium volutator infested with Maritrema subdolum

As mentioned above, the amphipod C. volutator is also an important prey for many shorebirds species. Mouritsen & Jensen (1997) have shown that, apparently due to parasite-induced anaemia, Corophium individuals infested with metacercariae of M. subdolum have increased activity at the surface of tidal flats. A great variety of shorebird species are commonly infested with M. subdolum and other species of Maritrema (Hadley & Castle 1940; Loftin 1960; Cabot 1969a, 1969b; Dronen & Badley 1969; Ching 1974, 1990; Deblock & Canaris 1992; McNeil et al.1995). According to Mouritsen & Jensen (1997), this parasite-induced behavioural change may facilitate transmission of infective stages of M. subdolum to shorebird hosts.

Surface activity of Venerupis aurea infested with Gymnophallus fossarum

The clam Venerupis aurea normally spends its post-larval life buried in the sand sediment. When heavily infested with the metacercariae of Gymnophallus fossarum, V. aurea often reverses its position in the sand, uncovering its ventral side, thus becoming more conspicuous and attractive to the European Oystercatcher. This behavioural change induced by the parasite facilitates the transmission of its infective stage to the oystercatcher in the intestine of which it develops into the adult final stage (Bartoli (1976).

Hyperactivity of Gammarus amphipods infested by the trematode Microphallus papillorobustus

After emerging from snails Hydrobia, the cercariae of the trematode Microphallus papillorobustus penetrate Gammarus amphipods which form part of the diet of various shorebird species (see Rebeck 1964; Bengtson & Svensson 1968; Helluy 1983b; Michaud & Ferron 1990; Holt & Warrington 1996). Helluy (1983a, 1983b) has shown that adult and juvenile G. insensibilis, and juvenile G. aequicauda, infested by the metacercariae, behave abnormally: they exhibit positive phototaxis and negative geotaxis, and thus move to the water surface. In addition, infested G. insensibilis, mechanically triggered by the movements of foraging shorebirds and other waterbirds, aggregate and become hyperactive at the air-water interface, while non-infested individuals remain motionless or swim to the bottom. Such parasite-induced aggregation and hyperactivity make infested amphipods more conspicuous and more vulnerable to shorebird predation and are of survival value to the parasites. Microphallus papillorobustus is known to infest various shorebird species (see Rebeck 1964).

Association between Microphallus papillorobustus and Maritrema subdolum

Helluy (1983b) has shown that M. subdolum frequently infests Gammarus species together with M. papillorobustus. Indeed, the cysts of M. subdolum are present in larger numbers in those Gammarus exhibiting Microphallus-altered behaviour than in normal ones. Shorebirds are commonly infested with M. subdolum and other species of Maritrema (see above). As a consequence, all metacercariae of M. subdolum that are infesting Gammarus species in the presence of metacercariae of M. papillorobustus have increased chances of infesting shorebird species (Helluy 1983b).

Parasites might increase their chances of attaining final hosts by increasing the size of intermediate hosts or by selecting the larger ones, which are more attractive to predators. For many shorebirds, larger prey are more profitable than smaller ones and are preferred (see Goss-Custard 1979; Schneider 1981; Zwarts & Drent 1981; Sutherland 1982; Pienkowski 1983; Sutherland & Ens 1987). It has often been reported that parasites enhance the growth of molluscan hosts, leading to 'gigantism', and frequently also to lost fecundity of hosts (see Lim & Green 1991). However, evidence for such parasite-induced gigantism is equivocal in many cases (see Sousa 1983a; Hurd 1990; Mouritsen & Jensen 1994) and will not be discussed here. Cases of enhanced growth have been reported for snails (Cerithidea californica, Hydrobia ulvae, Ilyanassa obsoleta) caused by echinostomatide (Himasthla sp., Echinoparyphium sp.), notocotylide (Catatropis sp.), microphallide (Maritrema, Microphallus) and philopthalmide (Parorchis) trematodes (Sousa 1983a; Mouritsen & Jensen 1994; Curtis 1995). All these trematode species are known to infest shorebird species (Threlfall 1963; Schmidt & Neiland 1968; Cabot 1969a; Dronen & Badley 1979; Tallman et al. 1985; Ching 1990). However, their larval stages, after leaving the snail, need to develop in a second intermediate host before infesting shorebirds (see Sousa 1993b). As a consequence, there is little chance that the 'gigantism' induced in snails by these parasite species affects their prevalence in shorebird species.

However, there are cases in which the tendency for heavier infestations to occur in larger sizes of prey may result in increased parasite prevalence in shorebirds. For example, the larger M. balthica are more heavily infested by P. affinis than smaller ones (see above). In spite of the fact that European Oystercatchers sometimes reject infested Macoma (Hulscher, 1973, 1982), the less experienced juveniles of these and other shorebird species that feed on Macoma may be inclined to select the larger individuals, and thus may increase their risks of being infested with P. affinis. Another example concerns C. volutator. According to Bick (1994), larger C. volutator are more severely infested with L. brachysoma and M. subdolum than smaller ones. Both species are known to infest shorebirds (see above) and larger Corophium are preferred to small ones by many shorebird species (see Goss-Custard 1979; Peer et al. 1986).

The larger size and increased conspicuousness of infested Hydrobia ulvae

The snails H. ulvae are common prey of various shorebird species (see Prater 1972; Goss-Custard et al. 1977; Pienkowski 1992; Worrall 1984; Durell & Kelly 1990; Mouritsen 1994). According to Huxham et al. (1995), the snails larger than 6.1 mm are more heavily infested with the metacercariae of digenean trematodes than the smaller ones, and the snails with metacercarial infestation are more active on the sediment surface than uninfested snails and snails with cercarial infestation. In this way, the parasites benefit both from an increased availability of the snails to the final hosts and the phenomenon of 'gigantism', since the shorebirds probably select the largest snails (see above).

The larger size of some infested prey (see above), in addition to making them more attractive, can make them more profitable if larger size is induced by somatic growth. Indeed, larger size may sometimes mean more food. For example, the cercariae of trematodes such as Maritrema sp., Microphallus sp. and Himasthla sp. produce enhanced shell and somatic growth in H. ulvae, their first intermediate host (see Mouritsen & Jensen 1994), which is commonly preyed upon by various shorebird species (see Prater 1972; Goss-Custard et al. 1977; Pienkowski 1982; Durell & Kelly 1990). As a consequence, shorebirds might get some indirect advantage from the helminths that infest their invertebrate prey, for the risks of being infested by these helminth species are low, since the shorebirds are predating on the first and not the second intermediate hosts. In addition, Lafferty (1992) considers that, when the parasites are only slightly pathogenic and energetic costs of parasitism are moderate, final hosts also may actually benefit from eating parasite-modified prey.

The likelihood of helminth infestation is higher in juvenile birds (Borgsteede et al. 1988; Hoeve & Scott 1988; Goater 1989; McNeil et al. 1995, 1996). Helminths may normally be considered as having low pathogenicity and do not always exert a negative effect on the fitness of their hosts (see Reid 1991). However, by definition, parasites damage their hosts and have negative effects on them at least some of the time during their life-cycle (see Holmes & Zohar 1990) and any parasites that use the tissues or food of their hosts may very well have negative effects, but the extent of these greatly depends on the number of parasites (infestation intensity) (Cheng 1973; Reid 1991; Goater & Holmes 1997). Many of the negative effects of helminths on hosts are concentrated on juveniles (Goater & Holmes 1997). Pathogenic helminths depend upon the host for nourishment which may lead to nutrient deficiencies, produce toxic substances with local or general action detrimental to the host, damage the host's intestinal mucosa, cause intestinal obstruction, have irritative and inflammatory actions, produce enteritis and diarrhoea, sometimes undertake complex migrations through various organs of the host, produce anaemia and haemorrhage, pave the way for pathogenic microbes and viruses, sensitise the hosts to other diseases, and even result in death of hosts (Watson 1960; Dogiel 1964; Ulmer 1971; Cheng 1973). Many of these detrimental effects may apply to migratory birds, as recognised by Wehrmann (1909).

Various hypotheses have been proposed to explain oversummering (remaining on 'wintering' grounds during the boreal summer) in boreal-breeding shorebirds (see McNeil 1970; McNeil et al. 1994). Although most oversummering birds are approximately one year old, the age as such does not appear to be the causative factor (see McNeil et al. 1994). Indeed, some individuals of species known to oversummer do migrate to the breeding grounds and start breeding at the end of their first year of life (McNeil et al. 1994). In oversummering individuals, pre-migratory moult and fattening either do not take place, or are delayed (see McNeil 1970; McNeil et al. 1994). The relationship between digenean trematode infestation, absence of or delay in developing premigratory condition, and oversummering, first suggested by McNeil (1970), has been examined in Greater Yellowlegs oversummering in northeastern Venezuela (McNeil et al. 1995, 1996). Of the individuals collected, 57.6% were infested with one to four digenean species. Eleven genera were found (Table 1); specimens of Prosthogonimus ovatus and of Maritrema, Stictodora, Odhneria, and Diplostomum were present only in juveniles. The 26 adults collected in August, September and October shortly after their arrival on the 'wintering' ground had an average trematode infestation intensity (14.69) significantly higher than that (0.25) of the 8 juveniles collected in September, October and November. In contrast, the average parasite load of juveniles (68.69) collected in March, April, May and June tended to be higher than that of adults (7.00) collected during the same interval, but the difference was not significant at the 5% level. Infestation intensity in the air sacs was significantly higher in first-year birds than in adults. The prevalence of digenean infestation (in adult and juvenile birds pooled, due to the small size of the samples) increased steadily from November, shortly after the arrival of juveniles, to April-May. In fact, between mid-February and mid-March, when yellowlegs carried their highest premigratory fat loads, there was a significant inverse exponential relationship between fat loads and parasite loads (McNeil et al. 1995, 1996).

The location of parasites as well as their numbers (see above) explain to some extent their pathogenicity. Most parasites that infested Greater Yellowlegs were found in the intestine, air sacs and the body cavity. All helminths found in the air sacs, particularly Harrarium halli, belonged to the Cyclocoelidae. Cyclocoelids have severe effects on their hosts (McLaughlin 1977; Feizullaev 1985; Hoeve & Scott 1988). For example, Cyclocoelum mutabile penetrates the intestine and enters the body cavity, then penetrates the liver and, after a period of development, leaves the liver and becomes established in the air sacs of the avian host where it matures and causes in extremely severe damage (McLaughlin 1977).

It is therefore quite possible that, in addition to causing enteritis, anaemia and death of some individuals, helminths may also prevent or delay normal moult and pre-migratory fattening in some shorebirds on their wintering grounds, and hence be an important factor responsible for their oversummering (McNeil 1970; McNeil et al. 1994, 1995). Digestive disturbances resulting from intestinal helminth infestation are also expected to result in similar effects.

Birds may develop some degree of immunity to reinfestation with particular species of trematodes (see Macy 1973; Huffman & Roscoe 1986; Wallace & Pence 1986; Hoeve & Scott 1988). Partial immunity would explain, at least in part, (1) why juveniles Greater Yellowlegs tended to be more highly infested with digeneans at the time of or just before to the normal spring migration period, (2) why adults were also parasitised to some extent, and (3) why adults, which constitute the bulk of those 'scheduled' for migrating north, were less infested with trematodes in spite of the fact that the additional feeding associated with fat accumulation almost certainly exposed them to greater risk of parasitic infestation.

It seems likely that trematode infestation may be a significant factor responsible for oversummering in at least some shorebird species, although probably not in all species, and can interfere with their migration, and ultimately with their reproductive success. The likelihood of helminth infestation might be higher in those shorebird species breeding in boreal and low Arctic and wintering in freshwater and coastal lagoons and wetlands than in those breeding in the high Arctic regions and wintering in coastal marine environments. Indeed, high Arctic tundra and marine shores seem to be relatively parasite-free. Shorebirds breeding at rather low latitudes and/or being found in habitats other than coastal marine appear to have higher loads of parasites. According to Piersma (1997), the use of relatively parasite-poor high Arctic breeding habitats would go hand-in-hand with energetically costly longer migration distances, restriction to seashore environments in the non-breeding season, and low investment in general immunocompetence.

Trematodes may normally be considered as having low pathogenicity, except when habitat conditions are such that birds can acquire heavy worm burdens (Reid 1991). Some helminth species can become a problem when crowding or flocking of many individuals of the same host species occur (Dogiel 1964; Schmidt & Roberts 1985). Over the years, a great deal of pressure has been placed on tropical wetlands and coastal habitats, much of it at the expense of shorebirds (McNeil et al. 1985, 1990). Increased crowding in shorebirds on the wintering grounds may lead to their more rapid infestation by digenean helminths through a more rapid contamination of some of their invertebrate prey, the intermediate hosts, though no evidence is currently available to support this hypothesis. If the trend continues and shorebirds are forced into smaller and less suitable habitats, parasitism is likely to increase and the natural balance between hosts and parasites might become disturbed. The long term implication is that shorebird populations will decline as a result.

This study was financed by NSERC (Canada), Université de Montréal and Universidad de Oriente, Venezuela, through the collaboration agreement between both universities. We thank Peter R. Evans and Kim N. Mouritsen for useful suggestions for improving the manuscript.

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Table 1. Prevalence and mean intensity of digenean trematodes infesting Greater Yellowlegs in northeastern Venezuela (Taken from McNeil et al. 1995).

Fig. 1. Typical example for the life cycle of digenean microphallid trematodes such as Maritrema subdolum and Microphallus claviformis with intertidal invertebrates as first and secondary intermediate hosts, and shorebirds as final definitive ones (Adapted from Mouritsen et al. 1997).