Phoresy is a special kind of commensal relationship in which one organism (the phoretic or phoront) attaches to another (the host) for a limited time period to enhance dispersal of the pho-ront from the natal (or birth) habitat, resulting in colonization of a new and potentially better habitat. In addition to transport, the phoretic host may incidentally provide substrate, shelter, and even some indirect defense or protection for the phoront, but the strict definition of phoresy excludes any direct physiological benefit during transit. For example, the host does not provide the phoretic with food while in transit nor does it contribute to the ontogeny (development) of the phoretic during transit. If feeding does occur, the more appropriate term to describe this relationship would be parasitism. Although phoresy is not a form of parasitism, phoresy can eventually extend into a parasitic association (see below). Alternatively, if the host receives a benefit from its passenger the relationship is again not phoresy, but a form of mutualism. Thus, this discrete definition of phoresy separates phoresy from all other forms of symbiotic interactions.
The term phoresy is uniformly applied throughout the plant and animal kingdoms and does not exclusively apply to interactions of, or with, insects. Seeds that hitchhike on fur and pants are phoretic. The remora fish (Echeniedea: Remora remora) has a dorsal fin modified into a sucker that allows it to attach to the sides of larger fish and turtles, using them for phoretic transport. However, if the remora also snatches pulverized leftovers created during feeding by the host, this act violates the strict definition of phoresy. It soon becomes clear that it can be difficult to distinguish phoresy from other forms of symbiosis. Detailed aspects of behavior, natural history, and physiology are essential to a firm understanding of interspecific associations.
PHORESY AMONG INSECTS AND ARACHNIDS
Phoresy among arthropods has been recognized since at least the mid-1700s. It was formalized and defined by Lesne in 1896 as “those cases in which the transport host serves its passenger as a vehicle.” The etymology of the word unites the perspective of both the phoretic (phor (Gr.) = thief) and the host (phoras (Gr.) = bearing) within the interaction and has a counterpart to most forms of human transport: a “boat” in aquatic phoretic interactions, a “bus” in terrestrial settings, and an “aircraft” in aerial transport. Despite the medium being traversed, there are general principles that seem to be consistent among phoretic relationships, but these are not inclusive and exceptions occur: (1) the phoretic is usually much smaller than its host; (2) there are often several phoretic passengers on any individual host, and mass transit is not uncommon; (3) the phoretic does not have an effective means of independent dispersal (e.g., wings or oars), whereas the host usually is quite mobile; (4) phoresy has played a role in dispersal for a long time and evidence of phoretic relationships can be found in Baltic and Dominican amber from as far back as the early Tertiary (40 mya); (5) phoresy is a response to degradation of an ephemeral habitat (transient habitats available for relatively short periods of time, e.g., beach wrack, dung, etc.) or depletion of a limited resource; (6) phoretics dismount from the host when a suitable new habitat is encountered by the host, indicating that the phoretic has sensory recognition and interpretation of some element in that habitat; (7) usually only one member of a complex life cycle participates in the phoresy and the other members in the life cycle are not phoretic; in such cases, the phoretic may come from among any of the life stages (adult, nymph, or larva); (8) phoresy may be highly coevolved and stenoxenic when both the phoretic and the host are trophic specialists or very indiscriminant, in which case many “buses” may lead to alternate and appropriate habitats; (9) phoresy may be obligate (required) or facultative (occurring under some conditions); (10) phoretics may have little morphological adaptation specific to the attachment to the host (e.g., hold on with mouthparts or clasp with legs) and some have extensive modifications specific to attachment (e.g., extensive sucker plates or highly modified grasping legs); (11) enhanced by wind currents, phoresy is effective across impressive distances and there is even evidence of transoceanic voyages; (12) phoresy may be continual or seasonal, period, or cyclical; (13) the phoretic and the host may come from very different branches of the “tree of life,” as divergent as humans and plants, or from within related lineages (e.g., different insect orders); and (14) phoresy has originated independently several times within one lineage, in some instances (e.g., Meloidae or the blister beetles).
Most insect orders have members that participate in phoresy; however, the Diptera and Coleoptera form some of the most extensive phoretic associations with vertebrates, other insects, and mites. They can participate in phoresy as phoronts, as well as phoretic hosts. An interesting example of an insect as a phoretic host is the case of a common phoretic nematode, Pelodera coarctata, and its dung beetle host, Aphodius. As a dung pat deteriorates and dries, a special resistant phoretic nematode larva is produced that attaches to visiting dung beetles. The phoretic nematodes remain in a dormant state on the beetles until the beetles arrive at a fresh dung pat. Then the nematodes emerge, become active, and begin a new population of free-living nematodes.
Pseudoscorpions (arachnids that looks like small scorpions) are notorious phoronts, found on an impressively large array of insect hosts: Diptera, Hymenoptera, Coleoptera, Odonata, Orthoptera, Heteroptera, Lepidoptera, Trichoptera, harvestmen (Opiliones), spiders, birds, and even small mammals. Pseudoscorpions attach by the chela, or venomous pedipalps, and hold on tightly enough to prevent being brushed off or blown off the host during transit. In one interesting phoretic interaction, a neriid fly that began as a phoretic host for a species of pseudoscorpion then becomes a postdispersal meal at the end of the journey: a case of turning the bus into a lunch wagon at the point of destination.
However, by far the most impressive radiation of phoretic associations occurs among the mites (Fig. 1). Intense selection pressure results in phoresy when organisms are of such extremely small size and they do not possess wings for dispersal. Small body size allows mites to exploit limited ephemeral resources that would be too small to be useful to larger organisms (e.g., a dead snail or nectar within a single flower). Because these resources are small, they degrade quickly and disappear rapidly. And, there may be large distances between them.
FIGURE 1 Example of a mite-beetle phoretic relationship. The mites on the head and body of the Nicrophorus beetle are likely Poecilochirus (Mesostigmata: Parasitidae), which feed on nema-todes in the beetles’ nest chamber.
To survive, mites must travel to a better resource. Thus, they spend their lives tracking transient habitats. Establishing phoretic relationships with other organisms traveling among the same kinds of habitats gives them more rapid and direct access to a potentially better future and enhances their chances of survival.
Dung beetles, for example, thrive on dung, but as the dung dries and turns to soil it is no longer useful to the dung beetles. As the beetles depart, mites using the dung patties climb on board and hitch a ride to the next site. The journey would be perilous if these soft-bodied mites had to depend on walking the distance to their next meal. As the phoretic association progresses, the mites becomes increasingly dependent on those organisms that provide the most direct route to the best habitats.
EVOLUTION OF PARASITISM FROM PHORESY
Phoresy may begin with unrelated organisms moving independently among shared habitats. A relationship between a phoretic and a potential host can be established when some of the members of the population incidentally and randomly climb on board and are then delivered fortuitously to a habitat suitable for population growth. If encounters are repeated and consistent, mites develop cues to the most productive of these associations. Successful relationships become even more specialized and eventually stenoxenic. In some instances, phoretic association can become an intermediate step that grades into parasitism when the phoretic finds a way to get a meal, as well as transport, from the host.
A well-documented case of a phoretic relationship becoming parasitic is that of the mite Hemisarcoptes and the coccinellid beetle Chilocorus. Both feed on diaspid scale insects and the association originated as a phoretic relationship. However, coccinellid beetles are reflex bleeders and Hemisarcoptes has become adapted to the reflexed alkaloid toxins in the hemolymph and now requires it to molt and complete its development. Because feeding and completion of ontogenesis are part of the contribution of the host, this relationship has graded into parasitism. Other related members of the same mite family (Hemisarcoptidae), which use other phoretic hosts, remain phoretic. This is good evidence that phoresy can be an end point and that it can also progress to other forms of symbiosis (e.g., parasitism). Phoresy thus benefits the individual, but it can also act to enhance the diversity and complexity of community interactions within and among habitats.