foraging for patchy resources. However, while it is sometimes reasonable
to assume that parasite behaviours within the host are similar to parasite
behaviours outside the host, this may not always be the case. Consider
that orientation responses play a critical part in all host-finding strategies
by free-living infective stages. For orientation to occur, there is an explicit
requirement for a gradient (usually chemical), and the forager must
recognize the signal and signal strength and respond appropriately to this
gradient (Fraenkel and Gunn, 1940). Orientation responses are assumed to
occur in parasites in the host, when, for example, they migrate to the brain
of their host or when parasitoid larvae home in on competitors.
The problem is that the chemical gradients required for parasite
orientation over long distances have never been demonstrated within
hosts. In coelomate organisms, turbulence from the circulation of blood
or lymph precludes the formation of gradients. In addition, gradient
formation requires an open-ended system or a sink, where the signal can
diffusead infinitum, but hosts are closed systems. Furthermore, in more
than half a century of studies on parasite migrations within their hosts,
orientation behaviour has never been observed, despite intensive effort by
numerous scientists working on dozens of different host–parasite models
(Arai, 1980; Kemp and Devine, 1982; Holmes and Price, 1985; Sukhdeo
and Mettrick, 1987; Sukhdeo, 1997).
Orientation behaviours have also never been demonstrated in ecto-
parasite migrations on their hosts. The monogeneanEntobdella soleae
initially attaches to the dorsal side of its fish host, the soleSolea solea,
then migrates over the surface of the fish to the head. Water currents
generated by gill movements or gradients in mucus quality were thought
to provide the cues for orientation during this migration (Kearn, 1984;
Whittingtonet al., 2000), but this could not be demonstrated (Kearn,
1998). In fact, even though these parasites recognize sole-specific cues to
attach to the fish, the worms do not show orientation responses to any
host product (Kearn, 1967, 1998). Similarly, in terrestrial environments,
chemical gradients on the surface of the host were thought to provide
orientation cues for ectoparasite migrations. For example, after ticks
attach to their host, they often migrate over the surface of the body to the
head, neck or perianal areas of the host (Hartet al., 1990; Hart, 1994).
Laboratory experiments demonstrate that ticks are capable of orientation
and that they recognize components of host breath, including carbon
dioxide, hydrogen sulphide (Steullet and Guerin, 1992a,b) and a variety
of phenols, alcohols and aldehydes (Yunkeret al., 1992). Nevertheless,
investigators have not been able to show that orientation responses
contribute in any way to the directed migrations of ticks on their hosts
(Hart, 1994). As with monogenean ectoparasites on the surface of the fish,
tactile cues related to the topography and structure of skin and fur may
provide more reliable signals for directional movement than orientation
to chemical gradients (Sukhdeo and Sukhdeo, 2002).
A profitable direction for future studies might be founded on the
concept that all organisms live in species-specific perceptual worlds. VonDiverse Perspectives on Parasite Behavioural Ecology 343