Parasite-related modification of mating behaviour and refuge use in the aquatic isopod Caecidotea intermedius: neurological correlates

in Behaviour
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The acanthocephalan Acanthocephalus dirus is a trophically transmitted parasite that infects freshwater isopods as intermediate hosts and fish as definitive hosts. Using a laboratory-based experiment, we examined if parasite infection was associated with changes in mating behaviour, refuge use and neurochemical levels of infected isopods (Caecidotea intermedius). Infected isopods were less likely to engage in mating behaviour and more likely to be located in the open than uninfected isopods. Infected isopods also contained lower levels of serotonin (5-HT) and dopamine (DA) and had a greater mass of neural tissue (CNS) than uninfected isopods. We propose that the parasite-related changes in mating behaviour and refuge use may be modulated by the serotonergic and dopaminergic systems. We also suggest that the parasites could potentially be modulating these behavioural changes by exploiting the neural-immune system of the hosts through their neuroinflammatory responses.



AdamoS.A. (2012). The strings of the puppet master: how parasites change host behavior. — In: Host manipulation by parasites ( HughesD.P.BrodeurJ.ThomasF., eds). Oxford University Press, Oxford, p.  36-51.

AdamoS.A. (2013). Parasites: evolution’s neurobiologists. — J. Exp. Biol. 216: 3-10.

AdamoS.A.ShoemakerK.L. (2000). Effects of parasitism on the octopamine content of the central nervous system of Manduca sexta: a possible mechanism underlying host behavioural change. — Can. J. Zool. 78: 1580-1587.

AmatoJ.F.R.AmatoS.B.AraujoP.B.QuadrosA.F. (2003). First report of pigmentation dystrophy in terrestrial isopods, Atlantoscia floridiana (van Name) (Isopoda, Oniscidae), induced by larval acanthocephalans. — Rev. Bras. Zool. 20: 711-716.

BeneshD.P.ValtonenE.T.SeppäläO. (2008). Multidimensionality and intra-individual variation in host manipulation by an acanthocephalan. — Parasitology 135: 617-626.

BierbowerS.M.SparkesT.C. (2007). Parasite-related pairing success in an intermediate host, Caecidotea intermedius (Isopoda): effects of male behavior and reproductive physiology. — J. Parasitol. 93: 445-449.

BollacheL.GambadeG.CézillyF. (2001). The effects of two acanthocephalan parasites, Pomphorhynchus laevis and Polymorphus minutus, on pairing success in male Gammarus pulex (Crustacea: Amphipoda). — Behav. Ecol. Sociobiol. 49: 296-303.

BratteyJ. (1983). The effects of larval Acanthocephalus lucii on the pigmentation, reproduction, and susceptibility to predation of the isopod Asellus aquaticus. — J. Parasitol. 69: 1172-1173.

CampJ.W.HuizingaH.W. (1979). Altered color, behavior and predation susceptibility of the isopod Asellus intermedius infected with Acanthocephalus dirus. — J. Parasitol. 65: 667-669.

CézillyF.Perrot-MinnotM.-J. (2005). Studying adaptive changes in the behaviour of infected hosts: a long and winding road. — Behav. Proc. 68: 223-228.

CézillyF.Perrot-MinnotM.-J. (2010). Interpreting multidimensionality in parasite-induced phenotypic alterations: panselectionism versus parsimony. — Oikos 119: 1224-1229.

CézillyF.FavratA.Perrot-MinnotM.-J. (2013). Multidimensionality in parasite-induced phenotypic alterations: ultimate versus proximate aspects. — J. Exp. Biol. 216: 27-35.

DasariS.VieleK.TurnerA.C.CooperR.L. (2007). Influence of PCPA and MDMA (ecstasy) on physiology, development and behavior in Drosophila melanogaster. — Eur. J. Neurosci. 26: 424-438.

DezfuliB.S.RossettiE.FanoE.A. (1994). Occurrence of larval Acanthocephalus anguillae (Acanthocephala) in the Asellus aquaticus (Crustacea, Isopoda) from the River Brenta. — Biol. Zool. 61: 77-81.

ForbesM.R.L. (1993). Parasitism and host reproductive effort. — Oikos 67: 444-450.

GulerY.FordA.T. (2010). Anti-depressants make amphipods see the light. — Aquat. Toxicol. 99: 397-404.

HallM.E.HofferB.J.GerhardtG.A. (1989). Rapid and sensitive determination of catecholamines in small tissue samples by high performance liquid chromatography coupled with dual-electrode coulometric electrochemical detection. — LC-GC 7: 258-265.

HechtelL.J.JohnsonC.L.JulianoS.A. (1993). Modification of antipredator behavior of Caecidotea intermedius by its parasite Acanthocephalus dirus. — Ecology 74: 710-713.

HelluyS. (2013). Parasite-induced alterations of sensorimotor pathways in gammarids: collateral damage of neuroinflammation?J. Exp. Biol. 216: 67-77.

HelluyS.HolmesJ.C. (1990). Serotonin, ocotopamine, and the clinging behavior induced by the parasite Polymorphus paradoxus (Acanthocephala) in Gammarus lacustris (Crustacea). — Can. J. Zool. 68: 1214-1220.

HelluyS.ThomasF. (2010). Parasitic manipulation and neuroinflammation: evidence from the system Microphallus papillorobustus (Trematoda) — Gammarus (Crustacea). — Parasite Vectors 3: 38.

HughesD.P.BrodeurJ.ThomasF. (eds) (2012). Host manipulation by parasites. — Oxford University Press, Oxford.

KakizakiT.SaitoT.OhtakaA.NagasawaK. (2003). Effects of Acanthocephalus sp. (Acanthocephala: Echinorhynchidae) on the body size and reproduction of isopods (Asellus hilgendorfi). — Limnology 4: 43-46.

KaldonskiN.Perrot-MinnotM.-J.DodetR.MartinaudG.CézillyF. (2009). Carotenoid-based colour of acanthocephalan cystacanths plays no role in host manipulation. — Proc. Roy. Soc. Lond. B: Biol. Sci. 276: 169-176.

KennedyC.R. (2006). Ecology of the Acanthocephala. — Cambridge University Press, Cambridge.

KorkofigasE.ParkT.SparkesT.C. (2016). Acanthocephalan-related variation in the pattern of energy storage of a behaviorally and physiologically modified host: field data. — Parasitol. Res. 115: 339-345.

LaffertyK.D.ShawJ.C. (2013). Comparing mechanisms of host manipulation across host and parasite taxa. — J. Exp. Biol. 216: 56-66.

LagrueC.KaldonskiN.Perrot-MinnotM.-J.MotreuilS.BollacheL. (2007). Modification of hosts’ behavior by a parasite: field evidence for adaptive manipulation. — Ecology 88: 2839-2847.

LefèvreT.AdamoS.A.BironD.G.MisséD.HughesD.ThomasF. (2009). Invasion of the body snatchers: the diversity and evolution of manipulative strategies in host–parasite interactions. — Adv. Parasitol. 68: 45-83.

LyndonA.R. (1996). The role of acanthocephalan parasites in the predation of freshwater isopods by fish. — In: Aquatic predators and their prey ( GreenstreetS.P.R.TaskerM.L., eds). Blackwell Scientific Publishing, Oxford, p.  26-32.

MaynardB.J.DeMartiniL.WrightW.G. (1996). Gammarus lacustris harboring Polymorphus paradoxus show altered patterns of serotonin-like immunoreactivity. — J. Parasitol. 82: 663-666.

McCuskerR.H.KelleyK.W. (2013). Immune-neural connections: how the immune system’s response to infectious agents influences behavior. — J. Exp. Biol. 216: 84-98.

MooreJ. (1983). Responses of an avian predator and its isopod prey to an acanthocephalan parasite. — Ecology 64: 1000-1015.

MooreJ. (2002). Parasites and the behavior of animals. — Oxford University Press, Oxford.

MuzzallP.M.RabalaisF.C. (1975). 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.

OetingerD.F. (1987). Effects of Acanthocephalus dirus (Acanthocephala) on morphometrics and reproduction of Caecidotea intermedius (Crustacea: Isopoda). — T. Am. Microsc. Soc. 106: 240-248.

OetingerD.F.NickolB.B. (1981). Effects of acanthocephalans on pigmentation of freshwater isopods. — J. Parasitol. 67: 672-684.

OetingerD.F.NickolB.B. (1982). Developmental relationships between acanthocephalans and altered pigmentation in freshwater isopods. — J. Parasitol. 68: 463-469.

ØverliØ.PállM.BorgB.JoblingM.WinbergS. (2001). Effects of Schistocephalus solidus infection on brain monoaminergic activity in female three-spined sticklebacks Gasterosteus aculeatus. — Proc. Roy. Soc. Lond. B: Biol. Sci. 268: 1411-1415.

Perrot-MinnotM.-J.CézillyF. (2013). Investigating candidate neuromodulatory systems underlying parasitic manipulation: concepts, limitations and prospects. — J. Exp. Biol. 216: 134-141.

Perrot-MinnotJ.-P.MaddalenoM.BalourdetA.CézillyF. (2012). Host manipulation revisited: no evidence for a causal link between altered photophobia and increased trophic transmission of amphipods infected with acanthocephalans. — Funct. Ecol. 26: 1007-1014.

Perrot-MinnotM.-J.Sanchez-ThirionK.CézillyF. (2014). Multidimensionality in host manipulation mimicked by serotonin injection. — Proc. Roy. Soc. Lond. B: Biol. Sci. 281: 20141915.

Pilecka-RapaczM. (1986). On the development of acanthocephalans of the genus Acanthocephalus Koelreuther, 1771, with special attention to their influence on intermediate host, Asellus aquaticus L.Acta Parasitol. Pol. 30: 233-250.

PoulinR. (2010). Parasite manipulation of host behavior: an update and frequently asked questions. — Adv. Stud. Behav. 41: 151-186.

PoulinR.BrodeurJ.MooreJ. (1994). Parasite manipulation of host behaviour: should hosts always lose?Oikos 70: 479-484.

PoulinR.NicholK.LathamA.D.M. (2003). Host sharing and host manipulation by larval helminths in shore crabs: cooperation or conflict?Int. J. Parasitol. 33: 425-433.

RauqueC.A.SemenasL. (2009). Effects of two acanthocephalan species on the reproduction of Hyalella patagonica (Amphipoda, Hyalellidae) in an Andean Patagonian Lake (Argentina). — J. Invert. Pathol. 100: 35-39.

RojasJ.M.OjedaF.P. (2005). Altered dopamine levels induced by the parasite Profilicollis antarcticus on its intermediate host, the crab Hemigrapsus crenulatus. — Biol. Res. 38: 259-266.

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

ShawJ.C.KorzanW.J.CarpenterR.E.KurisA.M.LaffertyK.D.SummersC.H.ØverliØ. (2009). Parasite manipulation of brain monoamines in California killifish (Fundulus parvipinnis) by the trematode Euhaplorchis californiensis. — Proc. Roy. Soc. Lond. B: Biol. Sci. 276: 1137-1146.

SparkesT.C.KeoghD.P.HaskinsK.E. (2000). Female resistance and male preference in a stream-dwelling isopod: effects of female molt characteristics. — Behav. Ecol. Sociobiol. 47: 145-155.

SparkesT.C.KeoghD.P.ParyR.A. (1996). Energetic costs of mate guarding behavior in male stream-dwelling isopods. — Oecologia 106: 166-171.

SparkesT.C.KeoghD.P.OrsburnT.H. (2002). Female resistance and mating outcomes in a stream-dwelling isopod: effects of male energy reserves and mating history. — Behaviour 139: 875-895.

SparkesT.C.WeilK.A.RenwickD.T.TalkingtonJ.A. (2006). Development-related effects of an acanthocephalan parasite on pairing success of its intermediate host. — Anim. Behav. 71: 439-448.

SparkesT.C.WrightV.M.RenwickD.T.WeilK.A.TalkingtonJ.A.MilhalyovM. (2004). Intra-specific host sharing in the manipulative parasite Acanthocephalus dirus: does conflict occur over host modification?Parasitology 129: 335-340.

StewartB.A.AtwoodH.L.RengerJ.J.WangJ.WuC.-F. (1994). Improved stability of Drosophila larval neuromuscular preparations in haemolymph-like physiological solutions. — J. Comp. Physiol. A 175: 179-191.

TainL.Perrot-MinnotM.-J.CézillyF. (2006). Altered host behaviour and brain serotonergic activity caused by acanthocephalans: evidence for specificity. — Proc. Roy. Soc. Lond. B: Biol. Sci. 273: 3039-3045.

TainL.Perrot-MinnotM.-J.CézillyF. (2007). Differential influence of Pomphorhynchus laevis (Acanthocephala) on brain serotonergic activity in two congeneric host species. — Biol. Lett. 3: 68-71.

ThomasF.AdamoS.MooreJ. (2005). Parasitic manipulation; where are we and where should we go?Behav. Proc. 68: 185-199.

ThomasF.PoulinR.BrodeurJ. (2010). Host manipulation by parasites: a multidimensional phenomenon. — Oikos 119: 1217-1223.

ThomasF.RigaudT.BrodeurJ. (2012). Evolutionary routes leading to host manipulation by parasites. — In: Host manipulation by parasites ( HughesD.P.BrodeurJ.ThomasF., eds). Oxford University Press, Oxford, p.  16-33.

ThomasF.UlitskyP.AugierR.DusticierN.SamuelD.StrambiC.BironD.G.CayreM. (2003). Biochemical and histological changes in the brain of the cricket Nemobius sylvestris infected by the manipulative parasite Paragordius tricuspidatus (Nematomorpha). — Int. J. Parasitol. 33: 435-443.

WardP.I. (1986). A comparative field study of the breeding behaviour of a stream and a pond population of Gammarus pulex (Amphipoda). — Oikos 46: 29-36.

ZhuY.C.YocomE.SifersJ.UraduH.CooperR.L. (2016). Modulatory effects on Drosophila larva hearts: room temperature, acute and chronic cold stress. — J. Comp. Physiol. B, DOI:10.1007/s00360-016-0997-x.

ZoharS.HolmesJ.C. (1998). Pairing success of male Gammarus lacustris infected by two acanthocephalans: a comparative study. — Behav. Ecol. 9: 206-211.


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