Ectoparasitic effects on host survival and reproduction: the Drosophila-Macrocheles association

Ecology, July, 1996 by Michal Polak

Introduction

Parasites are ubiquitous in natural communities (Price 1980). By impairing host survival and reproduction, many parasitic species can affect disparate levels of biological organization. These levels range from the genetic and demographic structure of local host populations (Anderson and Crombie 1985, Crump and Pounds 1985, Hamilton et al. 1990) to the composition of entire ecological communities (Minchella and Scott 1991).

During the course of infection, parasites assimilate host nutrients that would otherwise remain available to the host. But parasites may also impair host feeding and assimilation efficiency (Holmes and Zohar 1990). As a consequence, many cases of parasitism lead to disturbed host physiological functions (Thompson 1983), physical emaciation, and elevated mortality (Holmes and Zohar 1990). Parasites may also utilize nutrients otherwise destined for host egg production (Hurd 1990, 1993), or indirectly cause diversion of nutrients from oogenesis by altering fat body metabolism and/or perturbing neuroendocrine control mechanisms (Holmes and Zohar 1990). Parasite-mediated fecundity depletion has been demonstrated in Argentine stem weevils, Listronotus bonariensis (Malone 1987), pyralid moths, Sceliodes cordalis (Mercer and Wigley 1987), and western fence lizards, Sceloporus occidentalis (Schall 1983) infected with protozoans, and in Drosophila putrida (Jaenike 1992) and Tribolium confusum (Keymer 1980) infected with nematodes and cestodes, respectively.

A growing body of the parasitological literature focuses on mechanisms by which microparasites (bacteria, viruses, protozoa, and fungi) reduce host fitness, primarily because of their role in regulating natural populations of many animals, including humans (Park 1948, Anderson and May 1981, May 1983, Ewald 1994). Baculovirus infections, for example, have been implicated in major oscillations in abundance of some temperate forest Lepidoptera (May 1983). Macroparasites, in contrast, which include parasitic helminths and arthropods, are not typically implicated in dramatic oscillations in host abundance. Nevertheless, their effects on host fitness can be pronounced, and some species can reduce host numbers and rates of exponential increase (Lanciani 1975, May and Anderson 1979, Keymer 1981, Kaya and Gaugler 1993). However, relative to parasitic helminths, less is known about how and to what extent parasitic arthropods, such as mites, can influence host fitness and population dynamics.

The present paper examines effects of infestation by mites Macrocheles subbadius (Berlese) (Macrochelidae: Mesostigmata) on multiple fitness components in Drosophila nigrospiracula Patterson and Wheeler (Drosophilidae: Diptera). Macrochelid mites have previously been believed to associate only phoretically with flies, i.e., to assume an entirely passive role while attached to their "host" (see Study organisms). Attachment is viewed merely as a means of facilitating mite dispersal to fresher substrates better suited for feeding and reproduction. In the present study, however, I demonstrate that M. subbadius is actually ectoparasitic, and examine dose-dependent effects of mites on the period prior to onset of oviposition, lifetime productivity, and survivorship of adult flies. I also address the potential of mites to affect fly populations in nature by drawing upon the results of a previous study by Polak and Markow (1995). This study demonstrated that the distribution of mites can be strongly aggregated in natural host populations, and that the degree of aggregation is positively correlated with a highly variable ecological parameter, age of the cactus necrosis.

Study organisms

Macrocheles mites occur worldwide. They feed and oviposit in a wide spectrum of substrates ranging from rotting plant tissue and moist soil to animal dung. In these materials, they primarily consume bacteriophagic nematodes (Rodriguez et al. 1962) and small arthropods, including the first and second instar larvae of flies (Pereira and de Castro 1945). Axtel (1963a, b) has suggested that by consuming the immature stages of flies, M. muscaedomesticae exerts a controlling effect on some house fly (Musca domestica) populations in nature. Nothing is known, however, about the capacity of these mites to reduce fly numbers in nature by feeding directly on adult hosts.

Macrochelid mites have been recovered from the body surface of adult flies, as well as from coprophagous scarab beetles and even from some rodents (reviewed by Krantz 1983). M. subbadius has been recovered from the house fly and the stable fly (Stomoxys calcitrans) (Axtell 1964), D. mettleri (M. Polak, unpublished data), D. mojavensis (T. A. Markow, personal communication), D. pachea (S. Pitnick, personal communication), and the cactus fly Odontoloxozus longicornis (Neriidae) (M. Polak, unpublished data). Female M. subbadius, in both adult and deutonymph stages of development, attach to adult Drosophila nigrospiracula (M. Polak, unpublished data). This fruit fly is endemic to the Sonoran desert of North America (Heed 1978). Courtship and mating occur on the outer skin of necrotic saguaro cacti, Carnegiea gigantea, and larvae develop within the decaying tissue (Markow 1988). Approximately 95% of attached mites occur on the ventral surface of the fly abdomen near the junction with the thorax. Mites occasionally cling to the dorsal surface of the abdomen, as well as to the neck and face of flies (Polak 1993). Under laboratory conditions, mites can remain attached for the entire life of the host. In nature, mean duration of infestation is unknown. Wade and Rodriguez (1961) speculated that M. muscaedomesticae can ". . . suck the body fluid . . ." of adult house flies, but they failed to substantiate their claim. In fact, Kinn (1966) found evidence to the contrary: M. muscaedomesticae failed to take up Nile Blue stain that had been injected into adult hosts of these mites.