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Parasites and Social Insects P Schmid-Hempel Parasites and social insects P Schmid-Hempel To cite this version: P Schmid-Hempel. Parasites and social insects. Apidologie, Springer Verlag, 1995, 26 (3), pp.255-271. hal-00891263 HAL Id: hal-00891263 https://hal.archives-ouvertes.fr/hal-00891263 Submitted on 1 Jan 1995 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Review article Parasites and social insects P Schmid-Hempel ETH Zürich, Experimental Ecology, ETH-Zentrum, NW, CH-8092 Zürich, Switzerland (Received 23 December 1994; accepted 8 March 1995) Summary — A short review shows that social insects have many parasites on larvae and adults but few on eggs. Social organisation simultaneously affects parasite transmission within and between colonies. Overall, the biology of social insects may be favourable to an epidemic, but such a process may quickly die out in the host population. social insects / parasite / polyandry / social organisation / epidemiology INTRODUCTION the final host of the parasite (Moore, 1983). Such changes of host behaviour which increase the chances of transmission for Under natural conditions, organisms are the parasite seem not to be uncommon and exposed to a wide range of parasites that may have consequences for may threaten their survival and reproduc- larger-scale (see Dobson, 1988; tive success. Research over the past 2 population dynamics for discussion). decades has broadened our knowledge and demonstrated that the effects of parasitism Social insects as hosts are no different may often be quite subtle rather than obvi- from other organisms, but the investigation ous. For example, a number of studies have of their parasites has been largely neglected, documented subtle behavioural changes of with the exceptions of commercially impor- the infected hosts that often seem to favour tant species (eg, honey bees; Bailey and the parasite. Many species of acanto- Ball, 1991), pest species (eg, fire ants; Jou- cephalan parasites seem to rely on inducing venaz, 1983), and studies of social para- changes in host behaviour to facilitate trans- sitism and inquilines (mostly in ants and mission to the next host (Moore, 1984). An bees; eg, Lin, 1964; Fisher, 1988). For infected isopod which serves as an inter- example, similar observations on mediate host will become positively photo- behavioural changes have been made in tactic and stay in exposed areas more fre- the classic case of a parasite infecting a quently than their uninfected counterparts. social insect. The liver fluke (Dicrocoelium) As a consequence, the infected host is more infects wood ants as intermediate hosts. likely to be preyed upon by a bird which is The infected ant changes its behaviour so as to climb onto exposed parts of its habitat infection intensity often show a positive cor- (eg, grass tips), where the ant will normally relation with group size (Davies et al, 1991; stay until eaten by the final host of the fluke, Keymer and Read, 1991). Negative corre- a herbivorous mammal such as a sheep lations have been reported for some vector- (Hohorst and Graefe, 1961; Schneider and transmitted diseases (Poulin and Fitzgerald, Hohorst, 1971). 1989). A possible cause for this difference rate con- Parasites can have additional effects on may be related to the increased of hosts. Snails infected by the trematode tacts in large groups that facilitates the trans- Schistosoma (the causative agent of human fer of directly transmitted parasites, and, at bilharzia) change their life history by increas- the same time a dilution effect that reduces the rate of vector attacks ing fecundity early in life at the expense of per capita (’the later reproduction. Minchella and Loverde selfish herd’). Besides this, the spread of (1981) demonstrated that such altered an infection within a group is likely to pro- fecundity schedules benefit the host ceed more rapidly than the spread of the because parasitism leads to castration of infection between groups. Such sugges- tions have been made for human the snail at an older age. Parasites have smallpox in African households and also been implicated in the pattern of geo- (Becker Angulo, graphical distribution of species because 1981), a population that for many purposes is structured in similar to social insect parasites could act as weapons of compe- ways tition among their hosts (Price et al, 1986, populations. Furthermore, fitness effects of have been for animals 1988). In fact, some drastic cases of range parasitism reported reduction in birds and ungulates have been living in groups, eg, cliff swallows that have traced back to the action of parasites (Dob- high levels of ectoparasitism (Brown and son and Hudson, 1986). More recent work Brown, 1986). Such evidence strongly sug- has concentrated on the hypothesis that gests that we should be concerned about entire species communities may be affected parasitism in social insects, and that in fact by the presence of parasites (Dobson and social insects may be highly suitable study Crawley, 1994). Finally, parasites have also objects for investigating the interactions been assigned a prominent role for the evo- between parasitism and social organisation. lution of sexual selection and mate choice This paper discusses a somewhat arbitrary (Andersson, 1994), an area of interest which selection of issues on host-parasite inter- has grown explosively over the last years. actions in social insects. Parasites should be especially important for social this has species, although aspect PARASITES OF SOCIAL INSECTS often been neglected in discussions on the evolution of sociality. In social animals, par- asites can be contracted by many individ- Colonies of social insects should be a highly uals and subsequently may threaten many rewarding target for parasites, because they members of the social group. For this rea- offer both a locally high density of potential son, it has been suggested that character- hosts and, at the same time, an assemblage istics which at first sight seem quite dis- of hosts that (on a crude level) are geneti- parate, such as group aggression towards cally more similar to each other than the newcomers, territory maintenance, or group population average. In discussions of mod- size, may all have evolved to prevent novel ern epidemiology and evolutionary ecology infections from being introduced to the group it is usual to use the category of micropara- (Alexander, 1974; Freeland, 1976). Indeed, sites which refers to parasites whose the number of parasite species per host and dynamics can be described by referring to infected, uninfected (susceptible), or resis- whether this lack of egg parasites is real or tant hosts (’SIR models’, Anderson and May, reflects a lack of studies. Given the many 1981). Viruses, bacteria, and protozoa would taxa of parasitic wasps that specialise on all qualify for this category despite the many eggs of lepidoptera (Strand, 1986), this defi- differences in their biology. On the other ciency is remarkable and is possibly the hand, macroparasites are those parasites result of the widespread mode of brood care where the dynamics can be better described and the use of sheltered nest sites that may by looking at individual parasites and their make eggs difficult to utilise for most para- fate within hosts (’Sir model", Anderson and sitoids. Consequently, if present at all, the May, 1981). Helminths, such as trematodes most likely targets of egg parasites must be and nematodes, fall into this category. surface nesters, a nesting habit found in Finally, social insects are hosts to para- many wasps and some bees. sitoids and social I will not dis- parasites. Larval parasites, on the other hand, are cuss the case of subsocial which arthropods, quite common, but these often include infec- shed an extra on the of the may light origin tious parasites. This may reflect the fact that association between social insects and their infectious diseases can readily spread within parasites. a nest once infected. It is unclear, however, A brief survey of the literature will show why eggs are not attacked at the same time, that a wide variety of parasites of all cate- but essentially a similar absence of infec- gories are associated with social insects tious diseases of eggs is also true for non- (table I). As in other organisms, parasites social insects. Possibly, it is simply more can attack different life cycle stages of the difficult to penetrate the egg and its chorion. host (table II). In social insects, this would Another reason may be the fact that infec- include eggs, larvae, pupae and adults, and tions cannot be easily transmitted by the we may, for practical reasons, add the nest eggs since they are immobile and will not as such, for example, its supporting structure easily get in contact with new hosts, unless (eg, wax) or debris. In termites, which have the mode of brood care ensures transmis- a hemimetabolous development, different sion. In polydomous social insects eggs and nymphal stages could be the target of para- brood are often carried from one nest to the sites. Furthermore, parasites may infect a other and thus infections may easily spread particular stage, eg, the larva, but be trans- to different nests within the colony. mitted to the next host or a vector by A large number of parasites attack work- from the or adult. An another, eg, pupa ers. These include viruses, bacteria, fungi, example is the microsporidian Burenella protozoa, helminths, and parasitoids (table the fire ant dimorpha infecting Solenopsis.
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