Parasites and Animal Behaviour. Karen Loxton Department of Zoology

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1 Parasites and Animal Behaviour Karen Loxton Department of Zoology

2

3 Lecture Outline 1. Life Cycles of parasites 2. Behaviours that enhance transmission 3. Behaviours that reduce infection 4. Behaviours that minimise impact

4 Some Terminology Parasitism: symbiotic relationship between organisms of different species where one organism (parasite) benefits at the expense of the other (host) Definitive Host: host in which the parasite matures sexually and produces offspring. Intermediate Host: host where parasite undergoes development, but do not reach sexual maturity. Parasitoid - insect whose larvae live as parasites that eventually kill their hosts (typically other insects)

5 Some Terminology Pathology: causes and effects of a disease. Virulence: degree of pathology how much damage parasite causes.

6 1. Parasite Life Cycles

7 *Isopod = e.g. woodlouse

8 Outcomes of Infection Egg stage Transmission of eggs depends on host activity Cystacanth stage Transmission depends on ingestion of host (death)

9 Why should parasites evolve to manipulate host behaviour?

10 Outcomes of Infection Egg Stage Transmission depends on host activity Low virulence Starling suffers little harm R0 increased Cystacanth stage Transmission depends on ingestion of host High virulence As virulence increases, transmission increases R0 increased

11 2. Behaviours that Enhance Transmission

12 When is it Adaptive Manipulation? Sick animals behave differently Side effects/pathology simplest explanation may or may not benefit the parasite. Adaptive trait must confer fitness benefits to its bearer (increase R 0 ). Parasite fitness is higher in hosts with altered behaviour than hosts without

13 Polymorphus paradoxus- Trophic transmission

14 Infected Gammarus photophilic skimmed surface clung to floating debris Experiments - ducks consumed 4x as many infected Mechanism serotonin?

15 Sphaerularia bombi - Hitching a ride Direct lifecycle Infection of queen changes post hibernation behaviour Parasitised queens sterilised remain on the wing for much longer do not found nests

16 Glyptapanteles - Parasitoids and caterpillar body guards Female oviposit into caterpillars Caterpillars continue developing and feeding until parasitoid larvae pupate Host undergoes behavioural changes stops feeding and moving more head-swings upon disturbance

17

18 Effect of parasitism on host-predator interactions in the laboratory. Effect of removing the guarding host on field mortality of parasitoid pupae

19 Toxoplasma gondii The brain parasite Protozoan parasite Transmitted from rat to cat Cause attraction to cat odour in rats Behavioural changes in humans? Slower reaction times, six fold increased risk of traffic accidents in infected males Links to schizophrenia including hallucinations and reckless behaviour Approx. third of people infected worldwide

20 Lecture Outline 1. Behaviours that enhance transmission 2. Behaviours that reduce infection 3. Behaviours that minimise impact

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22 Adaptive behaviour in hosts? Adaptive behaviour may occur if Parasite is harmful Behaviour mitigates this harm (not always easy to prove) Avoidance behaviours have effect of removing susceptibles from host population Reduce R0 of parasite

23 Mate selection Selection on females to avoid mating with parasitised males Self-protection Good parent Coincidence Good genes Peacock s Tail an elaborate, costly trait

24 Parasite Resistance and Good Genes Hamilton Zuk Bright Male Hypothesis Male elaborations serve as a marker for health Experimental evidence body colouration as indicator of overall health Stickleback females prefer red coloured males parasitism decreases red colour

25 Moving away immediate response cattle/mosquitoes long-term response reindeer/warble fly nest-desertion great tits/ hen fleas

26 Changing habitats Observational data hippos & tabanid flies Experimental data sticklebacks and branchiuran parasites (fish lice)

27 Changing posture protective positions lying down e.g., deer/head flies sensitive areas birds reduce exposure of feather free areas

28 Ovipositing and Parasite infection level

29 Becoming social Trade-offs Selfish herd Dilution effect vs. increased attraction vs. increased transmission. Experimental evidence sticklebacks and crustacean ectoparasite

30 Patch choice faeces-evasion in horses Changing diet Item rejection oystercatchers rejected heavily infected clams isopods avoid eating starling faeces containing acanthocephalan eggs.

31 Fighting back Swatting, stamping, ear twitching, slapping Tool use in elephants Energetically expensive 24% daily energy budget in howler monkeys

32 Lecture Outline 1. Behaviours that enhance transmission 2. Behaviours that reduce infection 3. Behaviours that minimise impact

33 Grooming Self-, allo-, and cross-species Costs Decrease/increase risk? Dpylidium caninum

34 Behavioural fever and chills Host/parasite differential temperature resistance Fevers - kill parasite grasshoppers infected with parasitic fungus Chills - delay parasite development Bumblebee parasitised by conopid flies

35 Self-medication Geophagy clay, minerals Leaves trichomes and worm removal Nesting material repel ectoparasitic insects

36 Complex interactions - bumble bees and conopid flies

37 Conclusions >50% of all animal species are parasites most animals are parasitised all the time if transmission can be increased, parasites should alter host behaviour

38 Further Reading Clayton, D. H. (1991) The influence of parasites on host sexual selection. Parasitol. Today 7: Folstad, I., A. C. Nilssen, O. Halvorsen, and J. Andersen. (1991) Parasite avoidance: the cause of post-calving migrations in Rangifer? Can. J. Zool. 69: Grosman AH, et al. (2008) Parasitoid increases survival of its pupae by inducing hosts to fight predators. PLoSONE 3(6): e2276. doi: /journal.pone Lozano, G.A. (1998) Parasitic Stress and Self-Medication in Wild Animals. Advances in the Study of Behavior, Volume 27: Stress and Behavior (v. 27) Moore, J., (2002) Parasites and the Behavior of Animals. Oxford University Press, Oxford. Moore, J Altered behavioral-responses in intermediate hosts - an acanthocephalan parasite strategy. American Naturalist 123:

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