Walk or ride? Phoretic behaviour of amblyceran and ischnoceran lice

Highlights

• Phoresy should be a universal behaviour amongst immobile symbionts.

• We investigated the relationship between immobility and phoretic ability.

• We conducted experiments using a rock pigeon-fly-louse model system.

• Highly mobile species displayed less phoretic behaviour than immobile species.

• The most phoretic species was one of the most immobile species.

Abstract

Phoresy is a behaviour where one organism hitches a ride on another more mobile organism. This is a common dispersal mechanism amongst relatively immobile species that specialise on patchy resources. Parasites specialise on patchily distributed resources: their hosts. Although host individuals are isolated in space and time, parasites must transmit between hosts or they will die with their hosts. Lice are permanent obligate ectoparasites that complete their entire life cycle on their host. They typically transmit when hosts come into direct contact; however, lice are also capable of transmitting phoretically. Yet, phoresy is rare amongst some groups of lice. Fundamental morphological differences have traditionally been used to explain the phoretic differences amongst different suborders of lice; however, these hypotheses do not fully explain observed patterns. We propose that a more fundamental natural history trait may better explain variation in phoresy. Species able to disperse under their own power should be less likely to engage in phoresy than more immobile species. Here we experimentally tested the relationship between independent louse mobility and phoresy using a system with four species of lice (Phthiraptera: Ischnocera and Amblycera) that all parasitize a single host species, the Rock Pigeon (Columba livia). We quantified the relative ability of all four species of lice to move independently off the host, and we quantified their ability to attach to, and remain attached to, hippoboscid flies (Pseudolynchia canariensis). Our results show that the most mobile louse species is the least phoretic, and the most phoretic species is quite immobile off the host. Our findings were consistent with the hypothesis that phoretic dispersal should be rare amongst species of lice that are capable of independent dispersal; however other factors such as interspecific competition may also play a role.

Introduction

Organisms often specialise on resources that are patchily distributed in space and time (MacAurthur and Pianka, 1966). Although patches can be resource-rich, dispersing amongst these spatially isolated and ephemeral patches can be difficult. This is particularly true of free-living and parasitic organisms that are relatively immobile such as wingless insects, mites and worms. Some organisms have solved this dispersal problem by being phoretic. Phoresy is a behaviour where a relatively immobile organism disperses by hitching a ride on another more mobile organism (Farish and Axtell, 1971, Houck and OConnor, 1991).

Phoresy has evolved in several phyla and is relatively common amongst nematodes, mites, lice, beetles and pseudoscorpions, some of which are obligate parasites or mutualists of vertebrate hosts (Treat, 1956, Keirans, 1975a, Roubik and Wheeler, 1982, Houck and OConnor, 1991, Zeh and Zeh, 1992, Athias-Binche and Morand, 1993). Hosts are patchily distributed because each host individual is, in essence, an island of exploitable resources (Kuris et al., 1980). Moreover, hosts are temporally patchy because all hosts eventually die. Thus, dispersal amongst host individuals (also referred to as transmission) is critical for the persistence of parasite and mutualist lineages.

Lice (Phthiraptera) are permanent, obligate ectoparasites of birds and mammals. Lice most commonly transmit between hosts when individuals come into direct, physical contact, such as contact between mates and contact between parents and offspring (Rothschild and Clay, 1952, Johnson and Clayton, 2003b; Clayton et al., 2016). However, lice also engage in phoretic transmission. In most cases, lice hitch rides on hippoboscid flies, which are blood-feeding parasites of birds and mammals (Keirans, 1975a, Durden, 1990). Rarely, lice also hitch rides on other insects such as fleas, dragonflies, bees and butterflies (Worth and Patterson, 1960, Keirans, 1975b, Durden, 1990, Kirk-Spriggs and Mey, 2014).

There are three major suborders of lice: Anoplura, Amblycera and Ischnocera (Price et al., 2003). Although there are records of phoretic lice from all three suborders (Table 1), phoresy appears to be exceptionally rare amongst amblyceran lice (Table 2). To date, there is only one documented case of phoresy amongst over 1300 species of amblyceran lice (Hopkins, 1946), whereas at least 33 of the more than 3000 spp. of the suborder Ischnocera are known to engage in phoresy (Table 2). Some species of ischnoceran lice even engage in phoresy quite regularly. Studies by Markov, 1938, Edwards, 1952, Corbet, 1956, Bennett, 1961, and Baum (1968) report that 20–43.5% of hippoboscid flies in their field studies carried ischnoceran lice. Moreover, flies frequently carry more than one louse; for example, Peters (1935) found a fly with 31 lice attached.

Keirans (1975a) noted that lice attached to flies with their mandibles, and he hypothesised that the differences in the frequency of phoresy amongst lice is determined by the ability or inability of lice to grab onto flies with their mouthparts. Lice of the suborder Ischnocera have dorso-ventrally aligned, mandibulate mouthparts that are used to bite or scrape the host’s integument (Johnson and Clayton, 2003b). Species of the suborder Ischnocera, which use their mandibles to cling tightly to the hair or feathers of their host, also use their mandibles to grasp setae on the body of hippoboscid flies (Keirans, 1975a). In contrast, lice of the suborder Amblycera have chewing mouthparts that are essentially modified to suck blood and lice of the suborder Anoplura have piercing, sucking mouthparts for sucking blood (Johnson and Clayton, 2003b).

Despite these extreme morphological differences, anopluran lice are as phoretic as ischnocerans (Table 2). Instead of using mouthparts, anopluran lice cling to flies with their tarsal claws (Mitzmain, 1912, Allingham, 1987, Durden, 1990). Recent phoretic records indicate that some ischnocerans also attach to flies using their legs and claws (Harbison et al., 2009). The single published record of phoresy of an amblyceran louse noted that the louse was attached by its mouthparts to one of the fly’s legs (Hopkins, 1946). In addition, we recently examined hippoboscid flies (Pseudolynchia canariensis) leaving captive Rock Pigeons (Columba livia) and found amblyceran lice (Hohorstiella lata) attached to several flies (Fig. 1). These lice appeared to be attached using their tarsal claws; these lice may also be attached with their mouthparts but scanning electron microscope images of this point of attachment were inconclusive (Fig. 1).

Regardless of the precise way in which lice attach to flies, it is clear that lice from all three suborders can be phoretic. Given that all lice face similar transmission barriers, why is phoresy so rare amongst some groups of lice? We suggest that a fundamental life-history difference is responsible for these phoretic differences.

Dispersal is risky. However, phoresy may be an especially risky dispersal strategy given that lice typically disperse by moving from one host to another during periods of direct, physical contact between two host individuals (Clayton et al., 2016). Off the vertebrate host, lice can only live a few days (Johnson and Clayton, 2003b). Lice that are not transported to a compatible host during this short time-frame will die. Lice that fall off or are groomed off the fly will also die without reaching a new host. Furthermore, hippoboscid flies are not as host-specific as lice. Flies may transport lice to a novel host species where the lice cannot survive or reproduce. The benefits of phoresy may outweigh the costs of phoretic dispersal for highly immobile species, but species that can move independently between host individuals may not need to engage in such risky behaviour. For example, agile amblyceran lice will crawl away from dead or distressed hosts in search of a new host (Keirans, 1975a, Johnson and Clayton, 2003a, Clayton et al., 2016). It is not clear what cues most lice use to locate new host individuals, but the few studies that have been done indicate that chemosensory and tactile mechanisms are likely involved (Wigglesworth, 1941, Clayton et al., 2016). Regardless of the types of cues used, the probability of crawling to a new host may be high, especially amongst gregarious or colonial host species that roost or nest in close proximity. In contrast, ischnoceran lice are so specialised for life on hair or feathers that they typically remain on the host, even if it is dead (Keirans, 1975a). For these lice, the benefits of phoresy may outweigh the costs.

Here, we investigated the relationship between independent mobility and phoresy amongst four species of lice that are ecological “replicates” in many respects (Johnson and Clayton, 2003b, Johnson et al., 2005). We compared two ischnoceran species: Columbicola columbae and Campanulotes compar; and two amblyceran species: H. lata and Menacanthus stramineus (Fig. 2). All four of these species are permanent obligate parasites that are found on Rock Pigeons (C. livia; Brown, 1971, Dranzoa et al., 1999, Price et al., 2003, Musa et al., 2011). Rock Pigeons are also parasitized by a hippoboscid fly (P. canariensis). These flies feed on blood and crawl throughout the bird’s plumage (Harbison, C.W., 2008. Ecology and Evolution of Transmission in Feather-Feeding Lice (Phthiraptera: Ischnocera). Ph.D. Thesis, University of Utah, USA). Flies are found most commonly on the abdomen of the bird (Harbison et al., 2008), a region of the body where all four lice species occur. Thus, all four species have had opportunities to engage in phoresy over macroevolutionary time.

Another aspect of this host–parasite system that makes it especially suitable for testing the relative role of phoretic dispersal versus independent dispersal is that Rock Pigeons nest in flocks. Rock Pigeon nests are often very close together; neighbouring nests are frequently 0.1–1.0 m apart (Johnston and Janiga, 1995). Thus, all four species of lice have had opportunities to disperse to new host individuals by crawling to neighbouring hosts over macroevolutionary time.

Despite these ecological similarities, these four species of lice have very different phoretic records. Columbicola columbae has been observed on hippoboscid flies on several occasions (Table 1), and has been shown to be phoretic in experiments (Harbison et al., 2009). The other ischnoceran louse, Ca. compar, has not been observed on flies and did not engage in phoresy in experimental settings (Harbison et al., 2009, Harbison and Clayton, 2011). Of the two amblyceran species in this study, neither species has been observed phoretically dispersing. However, one closely related species (Hohorstiella gigantea, a parasite of Stock Doves, Columba oenas) was found on a hippoboscid fly and is the only known case of phoresy from the suborder Amblycera (Hopkins, 1946, Table 1).

Here, we investigate the relationship between the ability of these four species of lice to move independently off the surface of the host relative to their phoretic ability. Specifically, we quantify how far each species can crawl off the surface of the host in a specified amount of time. We also conduct three assays to determine the relative abilities of these four species of lice to (i) attach to hippoboscid flies; (ii) remain attached to hippoboscid flies while the flies groom, and (iii) remain attached to hippoboscid flies during flight.