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Acanthocephalan-related variation in the pattern of energy storage of a behaviorally and physiologically modified host: field data

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Abstract

The acanthocephalan parasite Acanthocephalus dirus infects the freshwater isopod Caecidotea intermedius as an intermediate host before completing its life cycle in a fish. Transmission to the definitive host occurs after the parasite has reached the cystacanth stage, and development into this stage is associated with changes in several behavioral and physiological traits of the host. Given the potential importance of host energy availability to trait modification, we examined the relationship between cystacanth-stage infection and energy storage of adult isopods. Six samples of infected and uninfected male C. intermedius were collected from a population in March, April, and May during which time cystacanth-stage A. dirus dominate infections and modification of behavior and physiology occurs in nature. Biochemical assays revealed that infected male C. intermedius contained more glycogen and more lipid than uninfected males and that this difference was present throughout the sampling period, which represents the entire adult phase of the host’s life. Additional analysis revealed that infected and uninfected males differed in their pattern of allocation to each energy source and that host lipid levels were negatively correlated with parasite intensity. We propose that the typical pattern of allocation and storage of host energy appears to be disrupted by A. dirus infection and that the changes are more likely to favor the parasite than the host.

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References

  • Amat F, Gozalbo A, Navarro JC, Hontoria F, Varó I (1991) Some aspects of Artemia biology affected by cestode parasitism. Hydrobiologia 212:39–44

    Article  Google Scholar 

  • Baudoin M (1975) Host castration as a parasitic strategy. Evolution 29:335–352

    Article  Google Scholar 

  • Bierbower SM, Sparkes TC (2007) Parasite-related pairing success in an intermediate host, Caecidotea intermedius (Isopoda): effects of male behavior and reproductive physiology. J Parasitol 93:445–449

    Article  PubMed  Google Scholar 

  • Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583

    Article  CAS  PubMed  Google Scholar 

  • Caddigan SC, Barkauskas RT, Sparkes TC (2014) Intra-population variation in behavior modification by the acanthocephalan Acanthocephalus dirus: are differences mediated by host condition? Parasitol Res 113:4307–4311

    Article  PubMed  Google Scholar 

  • Camp JW, Huizinga HW (1979) Altered color, behavior and predation susceptibility of the isopod Asellus intermedius infected with Acanthocephalus dirus. J Parasitol 65:667–669

    Article  Google Scholar 

  • Camp JW, Huizinga HW (1980) Seasonal population interactions of Acanthocephalus dirus (Van Cleave 1931) in the creek chub, Semotilus atromaculatus, and isopod, Asellus intermedius. J Parasitol 66:299–304

    Article  Google Scholar 

  • Dianne L, Bollache L, Lagrue C, Franceschi N, Rigaud T (2012) Larval size in acanthocephalan parasites: influence of intraspecific competition and effects on intermediate host behavioural changes. Parasite Vectors 5:166

    Article  Google Scholar 

  • Fielding NJ, MacNeil C, Dick JTA, Elwood RW, Riddell GE, Dunn AM (2003) Effects of the acanthocephalan parasite Echinorhynchus truttae on the feeding ecology of Gammarus pulex (Crustacea: Amphipoda). J Zool (Lond) 261:321–325

    Article  Google Scholar 

  • Forbes MRL (1993) Parasitism and host reproductive effort. Oikos 67:444–450

    Article  Google Scholar 

  • Hargeby A, Johansson J, Ahnesjö J (2004) Habitat-specific pigmentation in a freshwater isopod: adaptive evolution over a small spatiotemporal scale. Evolution 58:81–94

    Article  PubMed  Google Scholar 

  • Hechtel LJ, Johnson CL, Juliano SA (1993) Modification of antipredator behavior of Caecidotea intermedius by its parasite Acanthocephalus dirus. Ecology 74:710–713

    Article  Google Scholar 

  • Hernandez AD, Sukhdeo MVK (2008) Parasite effects on isopod feeding rates can alter the host’s functional role in a natural stream ecosystem. Int J Parasitol 38:683–690

    Article  PubMed  Google Scholar 

  • Hurd H (2001) Host fecundity reduction: a strategy for damage limitation? Trends Parasitol 17:363–368

    Article  CAS  PubMed  Google Scholar 

  • Insausti TC, Casas J (2009) Turnover of pigment granules: cyclic catabolism and anabolism of ommochromes within epidermal cells. Tissue Cell 41:421–429

    Article  CAS  PubMed  Google Scholar 

  • Jokela J, Uotila L, Taskinen J (1993) Effect of the castrating trematode parasite Rhipidocotyle fennica on energy allocation of fresh-water clam Anodonta piscinalis. Func Ecol 7:332–338

    Article  Google Scholar 

  • Kaldonski N, Perrot-Minnot M-J, Dodet R, Martinaud G, Cézilly F (2009) Carotenoid-based colour of acanthocephalan cystacanths plays no role in host manipulation. Proc Roy Soc Lond B 276:169–176

    Article  Google Scholar 

  • Kennedy CR (2006) Ecology of the Acanthocephala. Cambridge University Press, New York

    Book  Google Scholar 

  • Korkofigas E (2007) Mechanisms underlying parasite-related suppression of mating behavior in the intermediate host Caecidotea intermedius (Isopoda): behavior and physiology. DePaul University, MS Thesis

    Google Scholar 

  • Labaude S, Cézilly F, Tercier X, Rigaud T (2015) Influence of host nutritional condition on post-infection traits in the association between the manipulative acanthocephalan Pomphorhynchus laevis and the amphipod Gammarus pulex. Parasite Vectors 8:403

    Article  Google Scholar 

  • Lefèvre T, Adamo SA, Biron DG, Missé D, Hughes D, Thomas F (2009) Invasion of the body snatchers: the diversity and evolution of manipulative strategies in host-parasite interactions. Adv Parasitol 68:45–83

    Article  PubMed  Google Scholar 

  • Lettini SE, Sukhdeo MVK (2010) The energetic cost of parasitism in isopods. Ecoscience 17:1–8

    Article  Google Scholar 

  • Maure F, Brodeur J, Hughes D, Thomas F (2013) How much energy should manipulative parasites leave to their hosts to ensure altered behaviours? J Exp Biol 216:43–46

    Article  PubMed  Google Scholar 

  • McCahon CP, Brown AF, Pascoe D (1988) The effect of the acanthocephalan Pomphorhynchus laevis (Müller 1776) on the acute toxicity of cadmium to its intermediate host, the amphipod Gammarus pulex (L.). Arch Environ Con Tox 17:239–243

    Article  CAS  Google Scholar 

  • McCahon CP, Brown AF, Poulton MJ, Pascoe D (1989) Effects of acid, aluminium and lime additions on fish and invertebrates in a chronically acidic Welsh stream. Water Air Soil Poll 45:345–359

    Article  CAS  Google Scholar 

  • McCahon CP, Poulton MJ, Thomas PC, Xu Q, Pascoe D, Turner C (1991) Lethal and sub-lethal toxicity of field simulated farm waste episodes to several freshwater invertebrate species. Water Res 25:661–671

    Article  CAS  Google Scholar 

  • Médoc V, Piscart C, Maazouzi C, Simon L, Beisel J-N (2011) Parasite-induced changes in the diet of a freshwater amphipod: field and laboratory evidence. Parasitology 138:537–546

    Article  PubMed  Google Scholar 

  • Minchella DJ (1985) Host life-history variation in response to parasitism. Parasitology 90:205–216

    Article  Google Scholar 

  • Moore J (2002) Parasites and the behavior of animals. Oxford University Press, Oxford

    Google Scholar 

  • Muzzall PM, Rabalais FC (1975a) Studies on Acanthocephalus jacksoni Bullock, 1962 (Acanthocephala: Echinorhynchidae). I. Seasonal periodicity and new host records. Proc Helminthol Soc Wash 42:31–34

    Google Scholar 

  • Muzzall PM, Rabalais FC (1975b) Studies on Acanthocephalus jacksoni Bullock, 1962 (Acanthocephala: Echinorhynchidae). II. An analysis of the host-parasite relationship of larval Acanthocephalus jacksoni in Lirceus lineatus (Say). Proc Helminthol Soc Wash 42:35–38

    Google Scholar 

  • Muzzall PM, Rabalais FC (1975c) Studies on Acanthocephalus jacksoni Bullock, 1962 (Acanthocephala: Echinorhynchidae). III. The altered behavior of Lirceus lineatus (Say) infected with cystacanths of Acanthocephalus jacksoni. Proc Helminthol Soc Wash 42:116–118

    Google Scholar 

  • Oetinger DF (1987) Effects of Acanthocephalus dirus (Acanthocephala) on morphometrics and reproduction of Caecidotea intermedius (Crustacea: Isopoda). Trans Am Microsc Soc 106:240–248

    Article  Google Scholar 

  • Oetinger DF, Nickol BB (1981) Effects of acanthocephalans on pigmentation of freshwater isopods. J Parasitol 67:672–684

    Article  Google Scholar 

  • Oetinger DF, Nickol BB (1982a) Spectrophotometric characterization of integumental pigments from uninfected and Acanthocephalus dirus-infected Asellus intermedius. J Parasitol 68:270–275

    Article  CAS  Google Scholar 

  • Oetinger DF, Nickol BB (1982b) Developmental relationships between acanthocephalans and altered pigmentation in freshwater isopods. J Parasitol 68:463–469

    Article  Google Scholar 

  • Plaistow SJ, Troussard J-P, Cézilly F (2001) The effect of the acanthocephalan parasite Pomphorhynchus laevis on the lipid and glycogen content of its intermediate host Gammarus pulex. Int J Parasitol 31:346–351

    Article  CAS  PubMed  Google Scholar 

  • Perrot-Minnot M-J, Maddaleno M, Balourdet A, Cézilly F (2012) Host manipulation revisited: no evidence for a causal link between altered photophobia and increased trophic transmission of amphipods infected with acanthocephalans. Func Ecol 26:1007–1014

    Article  Google Scholar 

  • Ponton F, Biron DG, Joly C, Helluy S, Duneau D, Thomas F (2005) Ecology of parasitically modified populations: a case study from a gammarid-trematode system. Mar Ecol Prog Ser 299:205–215

    Article  Google Scholar 

  • Poulin R (1994) The evolution of parasite manipulation of host behaviour: a theoretical analysis. Parasitology 109:S109–S118

    Article  PubMed  Google Scholar 

  • Poulin R (1995) “Adaptive” changes in the behaviour of parasitized animals: a critical review. Int J Parasitol 25:1371–1383

    Article  CAS  PubMed  Google Scholar 

  • Poulin R (2002) Parasite manipulation of host behaviour. In: Lewis EE, Campbell JF, Sukhdeo MVK (eds) The behavioural ecology of parasites. CABI Publishing, New York, pp 243–257

    Chapter  Google Scholar 

  • Poulin R (2010) Parasite manipulation of host behavior: an update and frequently asked questions. Adv Stud Behav 41:151–186

    Article  Google Scholar 

  • Poulin R, Brodeur J, Moore J (1994) Parasite manipulation of host behaviour: should hosts always lose? Oikos 70:479–484

    Article  Google Scholar 

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    Article  Google Scholar 

  • Sánchez MI, Thomas F, Perrot-Minnot M-J, Biron DG, Bertrand-Michel J, Missé D (2009) Neurological and physiological disorders in Artemia harboring manipulative cestodes. J Parasitol 95:20–24

    Article  PubMed  Google Scholar 

  • Sánchez MI, Rode NO, Flaven E, Redón S, Amat F, Vasileva GP, Lenormand T (2012) Differential susceptibility to parasites of invasive and native species of Artemia living in sympatry: consequences for the invasion of A. franciscana in the Mediterranean region. Biol Invasions 14:1819–1829

    Article  Google Scholar 

  • Seidenberg AJ (1973) Ecology of the acanthocephalan, Acanthocephalus dirus (Van Cleave, 1931), in its intermediate host, Asellus intermedius Forbes (Crustacea: Isopoda). J Parasitol 59:957–962

    Article  Google Scholar 

  • Sparkes TC, Keogh DP, Pary RA (1996) Energetic costs of mate guarding behavior in male stream-dwelling isopods. Oecologia 106:166–171

    Article  Google Scholar 

  • Sparkes TC, Wright VM, Renwick DT, Weil KA, Talkington JA, Milhalyov M (2004) Intra-specific host sharing in the manipulative parasite Acanthocephalus dirus: does conflict occur over host modification? Parasitology 129:335–340

    Article  CAS  PubMed  Google Scholar 

  • Sparkes TC, Weil KA, Renwick DT, Talkington JA (2006) Development-related effects of an acanthocephalan parasite on pairing success of its intermediate host. Anim Behav 71:439–448

    Article  Google Scholar 

  • Thomas F, Adamo S, Moore J (2005) Parasitic manipulation: where are we and where should we go? Behav Process 68:185–199

    Article  Google Scholar 

  • Thomas F, Brodeur J, Maure F, Franceschi N, Blanchet S, Rigaud T (2011) Intraspecific variability in host manipulation by parasites. Infect Genet Evol 11:262–269

    Article  PubMed  Google Scholar 

  • Thompson SN (1983) Biochemical and physiological effects of metazoan endoparasites on their host species. Comp Biochem Phys B 74:183–211

    CAS  Google Scholar 

  • Thompson SN (1990) Physiological alterations during parasitism and their effects on host behaviour. In: Barnard CJ, Behnke JM (eds) Parasitism and host behavior. Taylor & Francis, New York, pp 64–94

    Google Scholar 

  • Thompson SN (1993) Redirection of host metabolism and effects on parasite nutrition. In: Beckage NE, Thompson SN, Federici BA (eds) Parasites and pathogens of insects, vol. 1: parasites. Academic Press, New York, pp 125–144

    Chapter  Google Scholar 

  • Thompson SN, Binder BF (1984) Altered carbohydrate levels and gluconeogenic enzyme activity in Trichoplusia ni parasitized by the insect parasite, Hyposoter exiguae. J Parasitol 70:644–651

    Article  CAS  Google Scholar 

  • Thompson SN, Kavaliers M (1994) Physiological bases for parasite-induced alterations of host behaviour. Parasitology 109:S119–S138

    Article  PubMed  Google Scholar 

  • Van Handel E (1965) Microseparation of glycogen, sugars, and lipids. Anal Biochem 11:266–271

    Article  PubMed  Google Scholar 

  • Wahl G, Sparkes TC (2012) Egg dispersal in the acanthocephalan Acanthocephalus dirus: field data. J Parasitol 98:894–896

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

Funding was provided by DePaul University through the Paid Leave Program (University Research Council), a Competitive Research Grant (University Research Council), a Faculty Summer Research Grant (College of Science and Health), and the Department of Biological Sciences.

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Authors and Affiliations

  1. Department of Biological Sciences, DePaul University, 2325 North Clifton Avenue, Chicago, IL, 60614, USA

    Evan Korkofigas, Tracey Park & Timothy C. Sparkes

  2. Nanosphere Inc., 4088 Commercial Avenue, Northbrook, IL, 60062, USA

    Evan Korkofigas

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  1. Evan Korkofigas
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  2. Tracey Park
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  3. Timothy C. Sparkes
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Correspondence to Timothy C. Sparkes.

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Korkofigas, E., Park, T. & Sparkes, T.C. Acanthocephalan-related variation in the pattern of energy storage of a behaviorally and physiologically modified host: field data. Parasitol Res 115, 339–345 (2016). https://doi.org/10.1007/s00436-015-4753-z

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  • DOI: https://doi.org/10.1007/s00436-015-4753-z

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