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This Article Is the Copyright Property of the Entomological Society Of This article is the copyright property of the Entomological Society of America and may not be used for any commercial or other private purpose without specific written permission of the Entomological Society of America. COMMUNITY AND ECOSYSTEM ECOLOGY Sex-Biased Phoretic Mite Load on Two Seaweed Flies: Coelopa frigida and Coelopa pilipes 1 ANDRE S. GILBURN, KATIE M. STEWART, AND DOMINIC A. EDWARD School of Biological and Environmental Sciences, University of Stirling, Scotland FK12 5PD, United Kingdom Environ. Entomol. 38(6): 1608Ð1612 (2009) ABSTRACT Two hypotheses explain male-biased parasitism. Physiological costs of male sexually selected characteristics can reduce immunocompetence. Alternatively, ecological differences could generate male-biased parasitism. One method of comparing the importance of the two theories is to investigate patterns of phoresy, which are only likely to be generated by ecological rather than immunological differences between the sexes. Here we studied the pattern of phoresy of the mite, Thinoseius fucicola, on two species of seaweed ßy hosts, Coelopa frigida and Coelopa pilipes. We found a highly male-biased pattern of phoresy of T. fucicola on both species. These are the Þrst reported instances of sex-biased phoresy in a solely phoretic parasite. We also show the Þrst two cases of size-biased phoresy. We suggest that ecological factors, particularly, male mate searching, generated male biased patterns of phoresy. We highlight the potential importance of studies of phoresy in determining the relative roles of the immunocompetence and ecological theories in generating male-biased parasitism. We suggest that more studies of patterns of phoresy are carried out to allow detailed comparisons with patterns of parasitism. KEY WORDS sex-biased parasitism, coelopidae Sex biases in parasitism have been reported in a wide vertebrate data showed no evidence of a consistent range of vertebrate taxa including mammals (Poulin bias in the sex of the host (Sheridan et al. 2000). Since 1996, Schalk and Forbes 1997, Moore and Wilson the publication of this review, a few other studies have 2002), birds (McCurdy et al. 1998), Þsh (Reimchem been conducted. One showed a male bias in infections and Nosil 2001), and amphibians (Tinsley 1989). Two of two dragonßy species by the same mite (Lajeunesse main hypotheses have been proposed to explain why et al. 2004), whereas others showed female biased males should be more infected (Folstad et al. 1989, infections of a beetle (Seeman and Nahrung 2004) and Zuk and McKean 1996). Physiological differences, a damselßy (Robb and Forbes 2006). Although inver- such as reduced immunocompetence in males as a tebrates lack sex-speciÞc steroid hormones such as result of higher costs of producing sexually selected testosterone, physiological differences between the traits, can generate higher levels of infection in males sexes as a result of variation in the costs of reproduc- (Folstad et al. 1989, Folstad and Karter 1992, Kurtz and tion could still generate male-biased parasitism. Sexual Sauer 1999). Testosterone has been found to have an selection is just as likely to act more strongly on male immunosuppressive effect in males, reducing their invertebrates as male vertebrates generating higher ability to Þght off infections (McCurdy et al. 1998). costs of reproduction (Clutton-Brock and Parker 1992, Testosterone is thought to be particularly important in Owens and Thompson 1994). Unequal costs of repro- generating male-biased parasitism across vertebrate duction associated with the production of sexually taxa (Alexander and Stimson 1988, Folstad et al. 1989, selected ornaments can still affect levels of immunity Poulin 1996, Zuk and McKean 1996, McCurdy et al. in the absence of testosterone. For example, reduced 1998, Moore and Wilson 2002). Male-biased parasitism male immunities have been reported in a scorpion ßy in mammals is also associated with increased male- (Kurtz and Sauer 1999) and are believed to play a role biased sexual size dimorphism (Moore and Wilson in male biased parasitism in a copepod (Wedekind and 2002), although a similar pattern does not seem to be Jakobsen 1998). present in birds (McCurdy et al. 1998). Ecological differences can also generate male-bi- Far fewer studies have been carried out on inver- ased parasitism in both vertebrates and invertebrates. tebrate hosts. Some of these have shown a bias toward For example, behavioral differences might result in higher levels of infection in male hosts (Wedekind and males having higher exposure levels than females, as Jakobsen 1998). However, a meta-analysis of all in- seen in dragonßies (Lajeunesse et al. 2004). While searching for mates, males may encounter a higher 1 Corresponding author, e-mail: [email protected]. number of other individuals increasing the chances of 0046-225X/09/1608Ð1612$04.00/0 ᭧ 2009 Entomological Society of America December 2009 GILBURN ET AL.: SEX-BIASED PHORESY 1609 parasite transmission. Males can also pick up more Gilburn 2007), albeit to a lesser extent. The two spe- parasites by simply traveling between females (See- cies occur on beaches on which deposits of seaweed, man and Nahrung 2004). Additionally differences in known as wrack beds, are washed up (Dobson 1974), the diet of the two sexes might also vary their exposure often occurring sympatrically. The presence of a to parasites (Reimchem and Nosil 2001). wrack bed can be unpredictable, with long periods of The relative importance of the physiological and absence of seaweed at many sites (Day and Gilburn ecological models of male-biased parasitism has been 1997). Seaweed ßies live and breed throughout the the subject of debate (Zuk and McKean 1996, Reim- year, responding not to seasons, but to the arrival of chem and Nosil 2001). In vertebrates, testosterone is fresh deposits of seaweed whether these appear at the generally believed to be the most important factor height of summer or middle of winter. Thinoseus fuci- (Folstad et al. 1989, Poulin 1996, Zuk and McKean cola parasitize talitrid ampihipods which also occur 1996, McCurdy et al. 1998, Moore and Wilson 2002). year-round within wrack beds. The mite occurs The fact that invertebrates lack testosterone and a phoretically on both C. frigida and C. pilipes, using consistent male bias in infection (Sheridan et al. 2000) them as a means of transport between wrack beds. adds support to the testosterone-driven immunocom- Both C. frigida and C. pilipes are sexually dimorphic, petence hypothesis as the main explanation of male- with males being more variable in size and possessing biased parasitism in vertebrates. However, some au- hairier legs in both species. Sexual selection favors thors (Zuk and McKean 1996, Reimchem and Nosil large male size in both species (Gilburn et al. 1992, 2001) have criticized the fact that most studies re- Crean et al. 2000) because large males are better at porting sex-biased parasitism did not attempt to iden- withstanding female resistance during premating tify any underlying ecological cause. Consequently, struggles (Crean et al. 2000). the importance of ecological variation between the The purpose of this study is to investigate the extent sexes is likely to have been underestimated. Ecological that ecological differences between the sexes deter- causes of sex-biased parasitism such as variation in diet mine sex-biased phoresy in coelopids. The Þrst aim of and sexual dimorphisms that have evolved through this study was determine whether a sex bias exists in natural (as opposed to sexual) selection could also the numbers of T. fucicola occurring on C. frigida and play a signiÞcant role in generating sex-biased para- C. pilipes. The second aim was to determine whether sitism (Reimchem and Nosil 2001). Furthermore, as- the body size of coelopids, a sexually selected char- sociations between level of parasitism and exaggera- acteristic, is associated with phoretic mite load. tion in a sexually selected trait could have an ecological explanation. Materials and Methods A recent study (Lajeunesse et al. 2004) suggested that phoretic associations between species might pro- Experimental Procedures. We determined the vide important insights into determining the cause of prevalence and intensity of infestation (sensu Bush et male-biased parasitism. Male biases in patterns of al. 1997) of T. fucicola present on C. frigida and C. phoresy on hosts should only occur through morpho- pilipes by collecting adult seaweed ßies from several logical and ecological differences between the sexes. natural populations. Flies were collected using an as- Reduced immunocompetence is not likely to play a pirator in temperatures too cold for them to ßy. Flies role in generating a sex bias in phoresy because host were collected from various sites in eastern Scotland Þtness should not be signiÞcantly affected. Thus, if the in October 2004, namely Crail (Roome Bay, grid immunocompetence theory is correct, fewer and reference NO619079), St Monans (NO526014), and weaker sex biases should be found in patterns of phor- Elie (NT497996) in the East Neuk of Fife and White- esy compared with patterns of parasitism. Lajeunesse sands (NT709774) and Barns Ness (NT720773) in et al. (2004) studied sex biases in patterns of parasitism East Lothian. We also sampled ßies from Boulmer by a water mite and phoresy by the miteÕs preinfective (NU266141) in Northumberland, in northeast En- larvae on two dragonßy hosts. They found a male bias gland in November 2004 and February 2005. Large in both parasitic mites and preinfective phoretic lar- numbers of C. frigida were only found at Crail; thus, vae, which they concluded must have occurred be- C. pilipes alone was studied in the collections from the cause of ecological differences between the sexes. other sites. Flies were transported back to Stirling and Here we investigated sex bias in the prevalence and their mite infestation level was determined under ϫ15 infestation of a mite, Thinoseius fucicola, occurring magniÞcation. We also determined their wing length phoretically on two species of seaweed ßy hosts using a graticule unit under the same level of magni- (Diptera: Coelopidae): Coelopa frigida and Coelopa Þcation.
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