Phoresy revisited

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which the attached animal (termed the phoretic) ceases both feeding and ontogenesis, ..... Les Problèmes de l'Espèce dans le Règne Animal. III. Mémoires de la ...
Phoresy revisited

A.M. Camerik School of Animal, Plant and Environmental Sciences, University of the Witwatersrand, Wits, 2050, Johannesburg, South Africa. E-mail: [email protected]

Based on Farish & Axtell’s (1971) definition of phoresy and using Euzet & Combes (1980) terminology for the classification of host-parasite relationships, Athias-Binche (1994) proposed a classification of eco-physiological phoretic behaviour in mites. However, in the light of recent publications on mite-host relationships and of my own observations, Farish & Axtell’s (1971) definition of phoresy has to be revised and, consequently, Athias-Binche’s (1994) classification adapted. Key words: Phoresy, mite-host relationships, ecological and eco-physiological categories, evolution

esne’s (1896) definition of phoresy referred to a temporary, initially loose, interspecific association between certain free-living organisms – a transport vector (= host) and its passenger – which ended when the traveller disembarked as it arrived at a suitable location. The primary outcome of phoresy was dispersal. However, the author envisaged that this association over many generations could have evolved into a more permanent affiliation and finally became parasitic. In 1917, Deegener coined the word symphorium for phoretic associations. In this definition, he, like Lesne (1896), excluded parasitic and symbiotic relationships but did not include the temporary character of the phoretic association. He incorporated in his definition more permanent associations like barnacles on whales and sharks, anemones on crabs, and sessile protozoans on snails and insects. The issue became confused, when van Someren & McMahon (1950) and Noble & Noble (1964), according to Farish & Axtell (1971), began to use Lesne’s term phoresy in the sense in which Deegener defined symphorium. Farish & Axtell (1971) therefore proposed to re-introduce Lesne’s original understanding of phoresy and limit its use to strictly temporary associations. They defined phoresy as ‘a phenomenon in which one animal actively seeks out and attaches to the outer surface of another animal for a limited time during which the attached animal (termed the phoretic) ceases both feeding and ontogenesis, such attachment presumably resulting in dispersal from areas unsuited for further development, either of the individual or its progeny’. The physiological aspect of the phoretic relationship in this definition was indeed limited to a strictly temporary, non-parasitic association. However, already in 1931 Vitzthum, and later Lindquist (1983), noted how difficult it was to distinguish between phoresy, pseudo-, and real parasitism amongst free-living mites. The phoretic, according to

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Trends in Acarology [2009] M.W. Sabelis & J. Bruin (eds.)

Athias-Binche (1994), even when entering a quiescent stage during the journey, disturbs its host already by its sheer presence. Phoresy, according to this author, could therefore be considered to be a particular form of parasitism. This notion was further corroborated by the results of Houck & Cohen’s (1995) experiments with the astigmatic mite Hemisarcoptes cooremani Thomas and the coccinellid Chilocorus cacti (Coleoptera). This species-specific phoretic mite (phoretomorph or phoriont) rendered ambiguous the physiological aspect of a phoretic relationship being limited to a non-parasitic and non-symbiotic state. The phoretomorph lacked chelicerae, a mouth, and seemed to have a non-functional gut. However, during transport on the beetle the mite’s phoretomorph acquired at least tritiated water directly from its host’s haemolymph into its functional hindgut. Furthermore, the beetle’s haemolymph was a prerequisite for further development as hypopes not in contact with C. cacti died without completing their life cycle. Consequently the two attributes, feeding from its host and subsequently using the nourishment to promote its own development, belong to a parasitic way of life. Furthermore, the authors believed that the nymphal stage of some astigmatic lineages co-evolved with their common associates to such a degree that the mites developed an alternative deutonymphal stase, called the hypopus (hypopode or hypope). This stase could therefore be considered a link between free-living ancestors and a future strict parasitic way of life. Parasitism, they reasoned, comes to conclusion when the hypopes would moult into adults that continue to feed on their host. This pathway has not yet been completed in this species. It seemed, however, also possible that some free-living mites could develop into parasites without this kind of evolutionary pathway. In 1996 Polak described the unspecialised homeomorph of the mesostigmatic mite Macrocheles sub-

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A.M. Camerik badius (Berlese), phoretic on Drosophila nigrospiracula (Diptera). During transport the traveller pierced the fly’s integument and ingested its haemolymph. Moreover, the mite was not only phoretic on flies, but also attached to scarab beetles and rodents. M. subbadius, as GW Krantz stated (pers. comm.), ‘seems to have taken a shortcut to parasitism, without the expected evolutionary fanfare...’. Summarizing, restriction of the phoriont-phoront (traveler-host) association to the time during which transport takes place, limits the scope of the association. Nevertheless, even when this is restricted to the transport interval, phoresy excluding physiological connections is not guaranteed.

PHORESY REDEFINED I propose to redefine phoresy as a function of the evolutionary phoretomorph in the sense in which Lesne (1896) first defined it and propose to include a modified version of Athias-Binche’s (1994) eco-biological and eco-physiological phoretic categories. This leads to the following: Phoresy is a dynamic interspecific, temporary relationship whereby the phoretic (traveler, phoretomorph, phoriont) attaches to the host (carrier, phoront) for the duration of migration from one habitat to another, with the primary outcome being dispersal. The migration is facultative or obligatory; the physical associations could represent some stage along the evolutionary axis between euryxeny to steno- or oioxeny (= strict host-specificity), and their physiological relationships at any juncture between an allotrophic or predatory and parasitic or parasitoid life style. Phoresy includes at its origin an unspecialized phoretic homeomorph, but excludes at the other extreme those relationships in which the transition from phoriont to parasite is completed and its primary outcome, namely dispersal, no longer exists.

TYPES OF PHORESY Ecological phoretic relationships Athias-Binche (1994) described ecological types of phoretic associations as a function of the frequency with which migration occurs. Related to the increasing frequency of migration, the types are classified from occasional or accidental to facultative and obligate (Fig. 1). Phoresy is termed occasional or accidental when free-living edaphic, not strictly phoretic mites accidentally meet another animal and mount for ‘a ride’. Facultative phoresy is environmentally induced and encountered mainly in unpredictable, transient habitats, while obligate phoresy mostly occurs in predictable, seasonal or cyclical environments. Athias-Binche’s parameter ‘frequency of migrations’ has become ambiguous with Polak’s (1996) M. subbadius. As an opportunist, this mite presumably migrates frequently, at least more than once in its life. Such a frequent traveller would not fit in Athias-Binche’s first category. On the other hand, as a polyphagous predator, ‘taking a ride’ whenever a suitable host comes its way, it should be classified under this category. Athias-Binche (1994) reserved the term obligate phoresy for groups of mites inhabiting long-term habitats, like decaying logs. Migration in these populations is induced seasonally and determined by cyclical recurrent climatic factors. According to Knülle (1991), phoretomorph formation in

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these populations was anticipated through season-related cues like photoperiod or seasonal drought. Athias-Binche (1994) classified Pediculaster under the category facultative phoresy, since Gurney & Hussey (1967) and Cross & Kaliszewski (1988) were able to delay phoretomorph formation in Pediculaster by continuously transplanting the population to fresh fungus cultures. Knülle (1987), experimenting with Lepidoglyphus destructor (Schrank) (Glyciphagidae), explained that delaying phoretomorph formation was possible because the development of the phenotypically different heteromorph was genetically programmed, yet environmentally induced. In general, it may be presumed that in long-term as well as short-term temporary habitats, phoresy induced by fluctuations in the environment is a function of these changes and as such is obligate and not facultative. I therefore suggest that phoretic categories be expressed in terms related to fluctuations or changes in the environment rather than to frequency of migration. The advantage of this would be that, using Athias-Binche’s (1994) categories, the term obligate would encompass mite migration induced by a deteriorating habitat (Gurney & Hussey, 1967; Karg, 1967; Farish & Axtell, 1971; Cross & Kaliszewski, 1988), migration in response to factors inherent to the host (Krantz & Mellot, 1972; Schwarz & Müller, 1992; Schwarz et al., 1998), and environmental factors affecting host emigration and consequently mite migration (Zhang, 1998). Within this category one could introduce the parameter frequency of migration. In short-term temporary habitats, as in a dung pad or a water-filled tree-hole, each new generation moves on via a phoretomorph within a relatively short ‘migration window’. The frequency of migration in such a habitat is high, and directly linked to a deteriorating environment. In a decaying tree log or a savannah pan, a long-term temporary habitat, the comparatively low frequency of migration also occurs via a phoretomorph. In these habitats though, not every new generation travels. Phoretomorph formation is induced by environmental fluctuations, linked to seasonal factors, such as photoperiod, temperature, humidity. In both short-term and long-term habitats, phoretic migration is a regular and recurrent (cyclical) event. Migrations unrelated to environmental induction would be termed facultative. These would then be characterised by their unpredictability. In this classification system, host-specificity is excluded, as it is not a function of environmental fluctuations but of the degree of phoretic adaptations that have taken place in the course of the phoretic-phoront’s common evolution. The proposed modifications of Athias-Binche’s classification system are summarised in Figure 2.

ECOLOGICAL CATEGORIES OF PHORESY (Athias-Binche, 1994) Frequency of migrations

Infrequent/ Occasional

Facultative

Obligate

Edaphic, eurytopic, pioneers, polyphagous predators

transient, unpredictable (e.g., dung, rotting fruit)

transient, predictable, cyclical, seasonal (e.g., rotting wood)

No phoretic adaptations

phoretic adaptations, e.g., hypope, polymorph induced by changes in the environment

Accidentally, ‘taking a ride’

complex: environment × genetic interactions

Figure 1 Ecological categories of phoresy of mites (Acari) as a function of migration frequency (Athias-Binche, 1994).

Phoresy revisited

Physiological phoretic relationships Athias-Binche (1994) applied Euzet & Combes’s (1980) terminology for parasitic to phoretic assemblages. The relationships between phoretic partners, termed phoretic specificity, could progress from loose, occasional, euryxenous, via ecoethological, to steno- and oioxenous. An assemblage was called ‘euryxenous’ when the phoriont potentially used a wide range of carriers, and ‘eco-ethological’ when the phoretic partners shared the same habitat and when the host’s activities were linked to the mite population’s survival. Athias-Binche (1994) explicitly excluded phylogenetic relationships from the eco-ethological category. As the host-phoretic relationships became increasingly more stringent and the phoretic exhibited preferences for a host family or genus, the assemblage was called stenoxenous. Oioxenous or monospecific was reserved for associations where the phoriont consistently chose a single host species, or a closely related species. The term specificity in parasitic relationships usually refers to a monospecific liaison between host and parasite. However, phoretic relationships are usually more dynamic and, depending on the availability of their preferred host, the phoretic could be found attached to alternative hosts (own observation). This usually occurred only towards the close of the migration window. I therefore suggest the use of the term host preference instead of host specificity. I also suggest the inclusion of phylogenetic relationships in the category ‘eco-ethological’. In a dung environment, which necessitates frequent recurrent migrations, the phoretic preference remains within the dung fauna. This preference is usually restricted to one or a few different insect orders. Because of this restriction a common evolutionary history between host and phoretic may be expected. This assumption is supported for heterostigmatic mites by Magowski (1995). He described an 85 million years old fossil ECOLOGICAL CATEGORIES OF PHORESY Fluctuations in the environment Facultative

Phoretic feeding relationships The feeding relationships between mites and their hosts could, according to Athias-Binche (1994), have evolved from a casual (allotrophic or predatory) via commensal and mutualistic to either parasitoid or parasitic type. According to Cross (1965), Vitzthum stated that mated but non-gravid females of Pigmephorus (sic) – now Pediculaster – mesembrinae (Canestrini) would ‘ride upon adult flies and drop off at the oviposition sites where they (would) attack developing larvae’ (1931) – however, this observation has never been confirmed since and doubted by several researchers (EE Lindquist and EA Cross, pers. comm.). If Vitzthum’s observation was correct, these larvae were developing immatures of other than those of the host species, and thus the host/phoretic relationship did not involve feeding of the host larvae and can be classified as eco-ethological and predatory. Were the larvae immatures of the host species, the association could be classified as eco-ethological and parasitoid. However, as Lindquist noted (pers. comm.), one has to question whether Vitzthum (1931) presumed or actually observed such a feeding relationship as, according to present day authors, P. mesembrinae is fungi- and not larvivorous (Gurney & Hussey, 1967; Kosir, 1975; Clift & Toffolon, 1981; own observations). That the feeding relationships are not always clear-cut and do not have to progress in parallel along various axes is illustrated by the previously discussed phoretic feeding relationships of H. cooremani and the beetle C. cacti presented by Houck & Cohen (1995) and of M. subbadius and its various hosts, described by Polak (1996). However, the proposed modifications and extensions in Athias Binche’s system may prove to be a useful tool to classify phoretic relationships.

Obligate

Migrations unrelated to environmental fluctuations transient, unpredictable environment, accidentally, ‘take a ride’

migrations environmentally induced, transient, predictable, cyclical environment, complex (environment x genetic constitution) frequent short term, each generation, e.g., dung, carrion, rotting fruit, temporary pools

edaphic, eurytopic, pioneers

no phoretic adaptations

infrequent long term, seasonal, e.g., rotting wood

phoretic adaptations

Figure 2 Ecological categories of phoresy of mites (Acari) as a function of environmental fluctuations. ECO-PHYSIOLOGICAL CATEGORIES OF PHORESY

Facultative

Obligate

Loose / occasional, no phyletic relationships no host preference

Predatory

assemblage in amber, in which a heterostigmatic mite, possibly a female pygmephoroid (its external morphology suggests an affinity to the taxonomically confused Pediculaster complex), was found associated with its caeculid (Diptera) host. The two evolutionary axes, ecological categories and the physiological phoretic relationships are synthesised in Figure 3.

linked assemblages phyletic relationships preference for host(s) in

1 order mainly

1 family >1 genus

1 species or closely related species

Eco-ethological

Stenoxenous

Oioxenous

Figure 3 Synthesis of the ecological and physiological categories of phoresy of mites (Acari).

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