Intra-population variation in behavior modification by the acanthocephalan Acanthocephalus dirus: are differences mediated by host condition?

Abstract

The acanthocephalan parasite Acanthocephalus dirus infects the freshwater isopod Caecidotea intermedius as an intermediate host before completing its life cycle in a fish. Male C. intermedius infected by A. dirus parasites are less likely to engage in mating behavior than uninfected males but there is a significant intra-population variation in the occurrence of this behavioral change. Previous studies on uninfected isopods have shown that glycogen content is a predictor of male mating behavior and we examined whether the intra-population variation in the mating behavior of infected male C. intermedius could be explained by this relationship. A field-based behavioral experiment was used to quantify intra-population variation in male mating behavior, which showed that 50% of infected males were responsive to females and 50% were not responsive. Biochemical analysis of responsive and non-responsive males revealed that glycogen content was a predictor of the mating behavior for uninfected males but was not a predictor of mating behavior for infected males. For infected males, parasite intensity was a predictor of mating behavior. Males that contained more A. dirus parasites were less likely to undergo modification of mating behavior. We propose that the intra-population variation in the mating behavior of infected C. intermedius identified in nature was not mediated by host condition.

Multidimensionality of Modification in an Isopod-Acanthocephalan System

“…Similar patterns between parasite intensity and multidimensionality have also been described in the European isopod A. aquaticus infected by the acanthocephalan A. lucii . However, it should be noted that that mean intensity was lower in the current study (1.4) than in the previous studies (2.5) in which an intensity-related effect was identified (Caddigan et al, 2014(Caddigan et al, , 2017. Thus, it is possible that intensity-related effects are present but occur at higher intensities than were examined here.…”

“…If competitive interactions among parasites influence the patterns of development, growth, and energy allocation, and if manipulation is costly, then parasites may benefit by adopting strategies that balance the conflicting demands associated with their own growth, and development with those that are associated with host manipulation (e.g., Poulin, 1994a;Parker et al, 2003;Thomas et al, 2005Thomas et al, , 2011Michaud et al, 2006;Ball et al, 2008;Franceschi et al, 2010;Maure et al, 2013). Consistent with this type of mechanism, infection of an aquatic isopod by an acanthocephalan parasite is associated with decreases in both parasite energy content, and modification of host behavior (mating) at higher intensities of infection (Caddigan et al, 2014(Caddigan et al, , 2017. Thus, by examining the relationship between parasite intensity and multidimensional modification, insights can be gained into both manipulation strategies, and constraints that may be imposed on these strategies by competition.…”

“…A change in the strategy of manipulation may be expected if host manipulation is energetically costly and if the competitive interactions influence the amount of resources each parasite has available to allocate to manipulation (Dianne et al, 2012;Caddigan et al, 2014Caddigan et al, , 2017. Previous research on the population studied here has shown that mating behavior is suppressed in infected male C. intermedius relative to uninfected males and that this suppression is less likely to occur at higher parasite intensities, i.e., when intraspecific competition is more intense (Caddigan et al, 2014). In this relationship, intraspecific competition does not appear to influence parasite size (Caddigan et al, 2017; Table 5 this study) but does influence parasite energy content (Caddigan et al, 2017).…”

“…Numerous studies have shown that host sharing can impact parasite development, growth, body size, and energy content, and that each of these factors has the potential to influence trait modification (Read and Phifer, 1959;Roberts, 2000;Dezfuli et al, 2001;Sparkes et al, 2004Sparkes et al, , 2006Benesh and Valtonen, 2007a;Franceschi et al, 2008Franceschi et al, , 2010Benesh et al, 2009a;Dianne et al, 2010Dianne et al, , 2012Caddigan et al, 2014Caddigan et al, , 2017. If competitive interactions among parasites influence the patterns of development, growth, and energy allocation, and if manipulation is costly, then parasites may benefit by adopting strategies that balance the conflicting demands associated with their own growth, and development with those that are associated with host manipulation (e.g., Poulin, 1994a;Parker et al, 2003;Thomas et al, 2005Thomas et al, , 2011Michaud et al, 2006;Ball et al, 2008;Franceschi et al, 2010;Maure et al, 2013).…”

“…F female only (for cases where members of both sexes were examined). 1 Seidenberg (1973), 2 Camp and Huizinga (1979), 3 Camp and Huizinga (1980), 4 Oetinger and Nickol (1981), 5 Oetinger and Nickol (1982a), 6 Oetinger and Nickol (1982b), 7 Oetinger (1987), 8 Hechtel et al (1993), 9 Sparkes et al (2004), 10 Sparkes et al (2006), 11 Bierbower and Sparkes (2007), 12 Korkofigas (2007), 13 Caddigan et al (2014), 14 Kopp et al, 2016, 15 Korkofigas et al (2016), 16 Caddigan et al (2017), 17 Muzzall and Rabalais (1975a), 18 Muzzall and Rabalais (1975b), 19 Muzzall and Rabalais (1975c), 20 Hernandez and Sukhdeo (2008), 21 Lettini and Sukhdeo (2010), 22 Brattey (1983), 23 Pilecka-Rapacz (1986), 24 Lyndon (1996), 25 Benesh and Valtonen (2007b), 26 Hasu et al (2007), 27 Benesh et al...…”