Influence of host nutritional condition on post-infection traits in the association between the manipulative acanthocephalan Pomphorhynchus laevis and the amphipod Gammarus pulex

Particle and Fibre Toxicology

Thierry Rigaud¹  Xavier Tercier¹  Frank Cézilly¹  Sophie Labaude¹ 

[1] Université de Bourgogne Franche-Comté, UMR CNRS 6282 Biogéosciences, Dijon, France

关键词: Pomphorhynchus laevis;    Parasite manipulation;    Gammarus pulex;    Food resources;    Energetic constraints;    Deprivation;   

Others  :  1222133
DOI  :  10.1186/s13071-015-1017-9

 received in 2015-06-09, accepted in 2015-07-21,  发布年份 2015

【 摘 要 】

Background

Several parasites with complex life-cycles induce phenotypic alterations in their intermediate hosts. According to the host manipulation hypothesis, such phenotypic alterations are supposed to increase the fitness of the parasite at the expense of that of its intermediate hosts through increasing the probability of transmission to next hosts. Although the phenomenon has received a large attention, the proximate factors modulating the occurrence and intensity of host manipulation remain poorly known. It has however, been suggested that the amount of energy reserves in the intermediate host might be a key parameter, although its precise influence on the intensity of manipulation remains unclear. Dietary depletion in the host may also lead to compromise with other parasite traits, such as probability of establishing or growth or virulence.

Methods

Here, we address the question through performing experimental infections of the freshwater amphipod Gammarus pulex with two different populations of the acanthocephalan fish parasite Pomphorhynchus laevis, and manipulation of host nutritional condition. Following exposure, gammarids were given either a “standard” diet (consisting of elm leaves and chironomid larvae) or a “deprived” food treatment (deprived in proteins), and infection parameters were recorded. Once parasites reached the stage at which they become infective to their definitive host, refuge use (a behavioural trait presumably implied in trophic transmission) was assessed, and metabolic rate was measured.

Results

Infected gammarids exposed to the deprived food treatment showed a lower metabolic rate, indicative of a lower body condition, compared to those exposed to the standard food treatment. Parasite size was smaller, and, depending on the population of origin of the parasites, intensity of infection was lower or mortality was higher in deprived hosts. However, food treatment had no effect on either the timing or intensity of behavioural modifications.

Conclusions

Overall, while our results suggest that acanthocephalan parasites develop better in hosts in good condition, no evidence was found for an influence of host nutritional condition on host manipulation by parasites.

【 授权许可】

   
2015 Labaude et al.

【 图 表 】

Fig. 1.

Fig. 2.

Fig. 3.

Fig. 4.

Fig. 5.

【 参考文献 】

• [1]Poulin R, Thomas F. Phenotypic variability induced by parasites: extent and evolutionary implications. Parasitol Today. 1999; 15:28-32.
• [2]Moore J. Parasites and host behaviour. Trends Ecol Evol. 2002; 17:585-6.
• [3]Thomas F, Adamo SA, Moore J. Parasitic manipulation: where are we and where should we go? Behav Processes. 2005; 68:185-99.
• [4]Kaldonski N, Perrot-Minnot M-J, Dodet R, Martinaud G, Cézilly F. Carotenoid-based colour of acanthocephalan cystacanths plays no role in host manipulation. Proc R Soc B Biol Sci. 2009; 276:169-76.
• [5]Perrot-Minnot M-J, Maddaleno M, Balourdet A, Cézilly F. Host manipulation revisited : no evidence for a causal link between altered photophobia and increased trophic transmission of amphipods infected with acanthocephalans. Funct Ecol. 2012; 26:1007-14.
• [6]Ponton F, Biron DG, Joly C, Helluy S, Duneau D, Thomas F. Ecology of parasitically modified populations: a case study from a gammarid-trematode system. Mar Ecol Prog Ser. 2005; 299:205-15.
• [7]Sato T, Watanabe K, Kanaiwa M, Niizuma Y, Harada Y, Lafferty KD. Nematomorph parasites drive energy flow through a riparian ecosystem. Ecology. 2011; 92:201-7.
• [8]Koella JC, Sørensen FL, Anderson RA. The malaria parasite, Plasmodium falciparum, increases the frequency of multiple feeding of its mosquito vector, Anopheles gambiae. Proc R Soc B Biol Sci. 1998; 265:763-8.
• [9]Klein SL. Parasite manipulation of host behavior: mechanisms, ecology, and future directions. Behav Processes. 2005; 68:219-21.
• [10]Cézilly F, Thomas F, Médoc V, Perrot-Minnot M-J. Host-manipulation by parasites with complex life cycles: adaptive or not? Trends Parasitol. 2010; 26:311-7.
• [11]Poulin R. Parasite manipulation of host behavior: an update and frequently asked questions. Adv Study Behav. 2010; 41:151-86.
• [12]Thomas F, Brown SP, Sukhdeo MVK, Renaud F. Understanding parasite strategies: a state-dependent approach? Trends Parasitol. 2002; 18:387-90.
• [13]Benesh DP, Valtonen ET. Effects of Acanthocephalus lucii (Acanthocephala) on intermediate host survival and growth: implications for exploitation strategies. J Parasitol. 2007; 93:735-41.
• [14]Poulin R. Information about transmission opportunities triggers a life-history switch in a parasite. Evolution. 2003; 57:2899-903.
• [15]Thomas F, Brodeur J, Maure F, Franceschi N, Blanchet S, Rigaud T. Intraspecific variability in host manipulation by parasites. Infect Genet Evol. 2011; 11:262-9.
• [16]Maure F, Brodeur J, Hughes DP, Thomas F. How much energy should manipulative parasites leave to their hosts to ensure altered behaviours? J Exp Biol. 2013; 216(Pt 1):43-6.
• [17]Lettini SE, Sukhdeo MVK. The energetic cost of parasitism in isopods. Ecoscience. 2010; 17:1-8.
• [18]Shik JZ, Kaspari M, Yanoviak SP. Preliminary assessment of metabolic costs of the nematode Myrmeconema neotropicum on its host, the tropical ant Cephalotes atratus. J Parasitol. 2011; 97:958-9.
• [19]Dianne L, Bollache L, Lagrue C, Franceschi N, Rigaud T. Larval size in acanthocephalan parasites: influence of intraspecific competition and effects on intermediate host behavioural changes. Parasit Vectors. 2012; 5:166. BioMed Central Full Text
• [20]Franceschi N, Bollache L, Cornet S, Bauer A, Motreuil S, Rigaud T. Co-variation between the intensity of behavioural manipulation and parasite development time in an acanthocephalan–amphipod system. J Evol Biol. 2010; 23:2143-50.
• [21]Maure F, Brodeur J, Ponlet N, Doyon J, Firlej A, Elguero E et al.. The cost of a bodyguard. Biol Lett. 2011; 7:843-6.
• [22]Plaistow SJ, Troussard J-P, Cézilly F. The effect of the acanthocephalan parasite Pomphorhynchus laevis on the lipid and glycogen content of its intermediate host Gammarus pulex. Int J Parasitol. 2001; 31:346-51.
• [23]Caddigan SC, Barkauskas RT, Sparkes TC. Intra-population variation in behavior modification by the acanthocephalan Acanthocephalus dirus: are differences mediated by host condition? Parasitol Res. 2014; 113:4307-11.
• [24]Cézilly F, Favrat A, Perrot-Minnot M-J. Multidimensionality in parasite-induced phenotypic alterations: ultimate versus proximate aspects. J Exp Biol. 2013; 216(Pt 1):27-35.
• [25]Cézilly F, Grégoire A, Bertin A. Conflict between co-occuring manipulative parasites; an experimental study of the joint influence of two acanthocephalan parasites on the behaviour of Gammarus pulex. Parasitology. 2000; 120:625-30.
• [26]Durieux R, Rigaud T, Médoc V. Parasite-induced suppression of aggregation under predation risk in a freshwater amphipod. Sociality of infected amphipods. Behav Processes. 2012; 91:207-13.
• [27]Kaldonski N, Perrot-Minnot M-J, Cézilly F. Differential influence of two acanthocephalan parasites on the antipredator behaviour of their common intermediate host. Anim Behav. 2007; 74:1311-7.
• [28]Perrot-Minnot M-J, Kaldonski N, Cézilly F. Increased susceptibility to predation and altered anti-predator behaviour in an acanthocephalan-infected amphipod. Int J Parasitol. 2007; 37:645-51.
• [29]Dianne L, Perrot-Minnot M-J, Bauer A, Gaillard M, Léger E, Rigaud T et al.. Protection first then facilitation: a manipulative parasite modulates the vulnerability to predation of its intermediate host according to its own developmental stage. Evolution. 2011; 65:2692-8.
• [30]Perrot-Minnot M-J, Sanchez-Thirion K, Cézilly F. Multidimensionality in host manipulation mimicked by serotonin injection. Proc R Soc B Biol Sci. 2014; 281:20141915.
• [31]Franceschi N, Bauer A, Bollache L, Rigaud T. The effects of parasite age and intensity on variability in acanthocephalan-induced behavioural manipulation. Int J Parasitol. 2008; 38:1161-70.
• [32]Bauer A, Trouvé S, Grégoire A, Bollache L, Cézilly F. Differential influence of Pomphorhynchus laevis (Acanthocephala) on the behaviour of native and invader gammarid species. Int J Parasitol. 2000; 30:1453-7.
• [33]Bauer A, Haine ER, Perrot-Minnot M-J, Rigaud T. The acanthocephalan parasite Polymorphus minutus alters the geotactic and clinging behaviours of two sympatric amphipod hosts: the native Gammarus pulex and the invasive Gammarus roeseli. J Zool. 2005; 267:39-43.
• [34]Lagrue C, Wattier R, Galipaud M, Gauthey Z, Rullmann J-P, Dubreuil C et al.. Confrontation of cryptic diversity and mate discrimination within Gammarus pulex and Gammarus fossarum species complexes. Freshw Biol. 2014; 59:2555-70.
• [35]Franceschi N, Cornet S, Bollache L, Dechaume-Moncharmont F-X, Bauer A, Motreuil S et al.. Variation between populations and local adaptation in acanthocephalan-induced parasite manipulation. Evolution. 2010; 64:2417-30.
• [36]Kelly DW, Dick JTA, Montgomery WI. The functional role of Gammarus (Crustacea, Amphipoda): shredders, predators, or both? Hydrobiologia. 2002; 485:199-203.
• [37]Macneil C, Dick JTA, Elwood RW. The trophic ecology of freshwater Gammarus Spp. (crustacea:amphipoda): problems and perspectives concerning the functional feeding group concept. Biol Rev. 1997; 72:349-64.
• [38]Moss BR. Ecology of Freshwaters: A View for the Twenty-First Century, 4th Edition. Wiley-Blackwell; 2010
• [39]Rosi-marshall EJ, Wallace JB. Invertebrate food webs along a stream resource gradient. Freshw Biol. 2002; 47:129-41.
• [40]Eedy RI, Giberson DJ. Macroinvertebrate distribution in a reach of a north temperate eastern Canadian river: Relative importance of detritus, substrate and flow. Fundam Appl Limnol / Arch für Hydrobiol. 2007; 169:101-14.
• [41]Policar T, Stejskal V, Kristan J, Podhorec P, Svinger V, Blaha M. The effect of fish size and stocking density on the weaning success of pond-cultured pikeperch Sander lucioperca L. juveniles. Aquac Int. 2012; 21:869-82.
• [42]Dezfuli BS, Zanini N, Reggiani G, Rossi R. Echinogammarus stammen (Amphipoda) as an intermediate host for Pomphorhynchus laevis (Acanthocephala) parasite of fishes from the river Brenta. Bolletino di Zool. 1991; 58:267-71.
• [43]Dianne L, Perrot-Minnot M-J, Bauer A, Guvenatam A, Rigaud T. Parasite-induced alteration of plastic response to predation threat: increased refuge use but lower food intake in Gammarus pulex infected with the acanothocephalan Pomphorhynchus laevis. Int J Parasitol. 2014; 44:211-6.
• [44]Hervant F, Mathieu J, Barré H, Simon K, Pinon C. Comparative study on the behavioral, ventilatory, and respiratory responses of hypogean and epigean crustaceans to long-term starvation and subsequent feeding. Comp Biochem Physiol. 1997; 118A:1277-83.
• [45]Ansell AD. Changes in oxygen consumption, heart rate and ventilation accompanying starvation in the decapod crustacean Cancer pagurus. Netherlands J Sea Res. 1973; 7:455-75.
• [46]Dall W, Smith DM. Oxygen consumption and ammonia-N excretion in fed and starved tiger prawns, Penaeus esculentus Haswell. Aquaculture. 1986; 55:23-33.
• [47]Marsden ID, Newell RC, Ahsanullah M. The effect of starvation on the metabolism of the shore crab, Carcinus maenas. Comp Biochem Physiol Part A Physiol. 1973; 45:195-213.
• [48]Köster M, Krause C, Paffenhöfer G-A. Time-series measurements of oxygen consumption of copepod nauplii. Mar Ecol Prog Ser. 2008; 353:157-64.
• [49]Glazier DS. A unifying explanation for diverse metabolic scaling in animals and plants. Biol Rev Camb Philos Soc. 2010; 85:111-38.
• [50]Noguchi K, Gel YR, Brunner E, Konietschke F. nparLD : an R software package for the nonparametric analysis of longitudinal data in factorial experiments. J Stat Softw. 2012; 50:1-23.
• [51]Haye PA, Ojeda PF. Metabolic and behavioral alterations in the crab Hemigrapsus crenulatus (Milne-Edwards 1837) induced by its acanthocephalan parasite Profilicollis antarcticus (Zdzitowiecki 1985). J Exp Mar Bio Ecol. 1998; 228:73-82.
• [52]Rumpus AE, Kennedy CR. The effect of the acanthocephalan Pomphorhynchus laevis upon the respiration of its intermediate host, Gammarus pulex. Parasitology. 1974; 68:271-84.
• [53]Fielding NJ, MacNeil C, Dick JTA, Elwood RW, Riddell GE, Dunn AM. Effects of the acanthocephalan parasite Echinorhynchus truttae on the feeding ecology of Gammarus pulex (Crustacea: Amphipoda). J Zool. 2003; 261:321-5.
• [54]Habib MAB, Yusoff FM, Phang SM, Ang KJ, Mohamed S. Nutritional values of chironomid larvae grown in palm oil mill effluent and algal culture. Aquaculture. 1997; 158:95-105.
• [55]Czeczuga B. Some carotenoids in Chironomus annularius Meig. larvae (Diptera : Chironomidae). Hydrobiologia. 1970; 36:353-60.
• [56]Beckage NE, Riddiford LM. Growth and development of the endoparasitic wasp Apanteles congregatus: dependence on host nutritional status and parasite load. Physiol Entomol. 1983; 8:231-41.
• [57]Logan A, Ruiz-González MX, Brown MJF. The impact of host starvation on parasite development and population dynamics in an intestinal trypanosome parasite of bumble bees. Parasitology. 2005; 130:637-42.
• [58]Pulkkinen K, Ebert D. Host starvation decreases parasite load and mean host size in experimental populations. Ecology. 2004; 85:823-33.
• [59]Seppälä O, Liljeroos K, Karvonen A, Jokela J. Host condition as a constraint for parasite reproduction. Oikos. 2008; 117:749-53.
• [60]Brown SP, Renaud F, Guégan J, Thomas F. Evolution of trophic transmission in parasites: the need to reach a mating place? J Evol Biol. 2001; 14:815-20.
• [61]Steinauer ML, Nickol BB. Effect of cystacanth body size on adult success. J Parasitol. 2003; 89:251-4.
• [62]Poulin R, Wise M, Moore J. A comparative analysis of adult body size and its correlates in acanthocephalan parasites. Int J Parasitol. 2003; 33:799-805.
• [63]Fredensborg BL, Poulin R. Larval helminths in intermediate hosts: does competition early in life determine the fitness of adult parasites? Int J Parasitol. 2005; 35:1061-70.
• [64]Dezfuli BS, Giari L, Poulin R. Costs of intraspecific and interspecific host sharing in acanthocephalan cystacanths. Parasitology. 2001; 122:483-9.
• [65]Benesh DP, Seppälä O, Valtonen ET. Acanthocephalan size and sex affect the modification of intermediate host colouration. Parasitology. 2009; 136:847-54.
• [66]Poulin R. Variation in infection parameters among populations within parasite species: intrinsic properties versus local factors. Int J Parasitol. 2006; 36:877-85.