Parasites and Host Behaviour I

Parasites & Host Behaviour I Dr Hazel Wright hzw@aber.ac.uk Edward Llwyd Building Why do we study behaviour in parasitology? What is Behaviour? Behaviour is defined as ‘the way in which individual organisms interact with other components of their environment. ‘Components of the environment’ include prey, competitors, predators, potential mates and parasites. Parasites and host Behaviour 1. Parasites exploit natural patterns of host behaviour to maximise transmission (e.g preferred prey) 2. Hosts use behavioural adaptations to defend against or reduce parasite infections (e.g. habitat selection) 3. Parasites manipulate the behaviour of hosts, which can have ecological consequences We will be discussing the first two points this morning 1. Parasites exploit natural patterns of host behaviour to maximise transmission The types of host behaviour that can be exploited by parasites is variable, but usually involves feeding / foraging. This is especially important for parasites with an indirect life-cycle Example 1: The Gasterosteus -Schistocephalus system Stickleback Free-swimming coracidium Copepod sp. Example 2: A tale of two fishes… Atlantic halibut Hippoglossus hippoglossus • Diurnal forager • Rests during night (sand) • Infected by: Entobdella hippoglossus Common sole Solea solea • Nocturnal forager • Rests during day (sand) • Infected by: Entobdella soleae Parasites are closely related, but cannot successfully infect the ‘wrong’ host Sole Halibut E. Hippoglossus hatching E. Soleae hatching Parasites lay sticky eggs that adhere to sand particles, near their potential hosts Eggs of E. hippoglossus and E. soleae exhibit opposite hatching periodicity, which match host activity patterns Example 3: The Guinea worm (Dracunculus medinensis ) Contaminated water consumed (poor areas) Copepod releases larvae into intestine Larvae migrate to connective tissue and develop into adults ‘little dragon’ Ulcer on limb Larvae released into water Adults migrate to limbs. Toxic substance breaks down skin. Combat infection by using medicinal plants (burning / itching) and scanning the water for infected copepods. • We have shown that host behaviour can influence parasite infections • Therefore…..variation in host behaviour patterns can create variation in parasite infection levels 2. Hosts can evolve behavioural resistance as a response to infection threat Behavioural resistance ‘the first line of defence’ Behavioural defence Prevention better than cure. Least energetically demanding defense Structural defence Skin and secretions. Mucous has anti-parasitic properties Skin of red sea cling fish takes seconds to produce enough mucous to entirely cover the fish. Crinotoxic fishes (sedentary) have epidermal toxins that protect against parasites Immunological defence Immune defense is important: BUT it is energetically expensive. Negative effects regarding growth, fat storage and reproduction Behavioural resistance the first line of defence • Avoiding infections – Food selection (cattle) – Nest use (great tits) – Mate choice (various) ● Reducing parasite loads Self grooming (chickens) Allogrooming (impala) Fumigation (starlings) Avoiding infections (1): Selective Foraging by cattle Michel (1955) sampled pasture for lungworm larvae Lungworm can be fatal to livestock via parasitic bronchitus. Passed to cattle through faeces. Foraged areas contained only 25% the density of infective larvae found in the random sample Density of Infective Larvae Random sample Currently grazed Recently grazed Cattle were grazing selectively on ‘clean’ pasture to reduce the chance of infection Avoiding infection (2): Nest box use by the great tit, Parus major Nests provide ideal accomodation for ectoparasites Re-build every year, or re-use nests? Fleas Bugs Flies Ticks Avoiding infection (2): Nest box use by the great tit, Parus major Three experimental studies carried out: 1. Clean nest box vs. old, parasite free nest No preference; both used equally 2. Parasite free nest vs. parasite infested nest Strong preference for parasite free nest 3. Parasite infested nest box vs. nothing Strong preference for nothing: birds did not use nest boxes Christe et al 1994 (Anim. Behav. 47, 895-898) Avoiding infection (3): Mate choice Sex is a highly risky, but necessary, behaviour Transmission of ectoparasites and microparasites Benefits of Parasite-Mediated Mate Choice 1. Reduced exposure to directly transmitted parasites 2. Reduced chance of passing parasites to offspring 3. Possibly selecting parasite resistance genes Is there any evidence of parasite mediated mate choice in nature? Avoiding infections 3: Mate choice – evidence for Parasitemediated sexual selection Species 2° sex trait Parasites reduce trait Females prefer ‘healthier’ males? Cricket Guppy Stickleback Pheasant Call rate No No Display rate Red colour Display Yes Yes Yes Yes Yes Yes Yes Yes Jungle Fowl Swallow Ornaments Tail length Yes Yes Where secondary sexual characters indicate health, parasite mediated sexual selection can occur Behavioural resistance the first line of defence • Avoiding infections – Food selection (cattle) – Nest use (great tits) – Mate choice (various) ● Reducing parasite loads Self grooming (chickens) Allogrooming (impala) Fumigation (starlings) Parasite reduction mechanisms 1:Self preening in chickens (Gallus gallus ) Number of feather lice recovered after 30d 10000 1000 100 data from Brown (1972) Poultry Science 51, 162-4 10 1 Control De-beaked Self preening is an effective anti-parasite behaviour Parasite reduction mechanisms 1: Self preening in chickens Body weight of hens (g) after 30d 900 800 700 600 500 400 300 200 100 0 data from Brown (1972) Poultry Science 51, 162-4 Control De-beaked Birds prevented from preening show poor growth Parasite reduction mechanisms 2: Reciprocal grooming in Macaroni penguins and impala Unpaired Macaroni penguins harbour 2-3x the number of ticks harboured by paired individuals Territorial male Impala do not perform reciprocal grooming They harbour 6x the number of ticks that females do Parasite reduction mechanisms 3: Nest fumigation by starlings (Sturnus vulgaris) Starlings (and other passerine birds) weave fresh green plant material into their nests Such plants contain biocidal substances Are birds using plant compounds as antiparasite ‘fumigants’? Evidence [Clark & Mason 1985, 1988 (Oecologia 67, 169-176; 77, 174-180)] 1. Preferred plants (fleabane and wild carrot) retard hatching of louse eggs, Non-preferred plants do not. 2. Removal of plant material from nests increased nest parasites 3. Species that re-use old nests are more likely to use anti-parasitic plants than those that re-build every year Summary Parasites exploit natural patterns of host behaviour for transmission Hosts have responded by adapting their behaviour to reduce the chance / intensity of infection Parasites and Host Behaviour II Dr Hazel Wright hzw@aber.ac.uk Edward Llwyd Building Parasite life cycles are enormously variable 2 main types Direct life cycles, e.g ectoparasitic lice Indirect life cycles (e.g cestodes, nematodes) How are parasites adapted to ‘navigate’ their life cycles? • Maximise transmission efficiency by: 1. Exploiting pre-existing host behaviour (this mornings lecture) 2. Manipulating host behaviour Why do parasites change host behaviour? The ‘mixed phenotype’ idea Parasite model ‘When infections cause changes in host behaviour…a parasite’s genes find phenotypic expression in the behaviour of the host’ ‘The Extended Phenotype’ Chapter 12 (‘Host phenotypes of parasite genes’) In other words………. The ‘mixed phenotype’ idea states that The behaviour of parasitised hosts is therefore a ‘mixed phenotype’, influenced by both host and parasite genomes. The ‘mixed phenotype’ Ecological events (such as finding food, or getting eaten) impact on the host and parasite simulatneously What happens to the host, also happens to the parasite Parasite phenotypes that alter the fate of the host to the benefit of the parasite should therefore be selected This can include behavioural manipulation Reasons for association of ‘odd’ host behaviour and infection Parasite adaptation that serves to maximise parasite fitness Host counter adaptations that serve to maximise host fitness Neutral side-effect of infection Behavioural effects of parasites What behaviours are changed? Recorded behaviour changes 1. Altered foraging - Time budgets / competitive ability / prey selection 2. Altered locomotion - Reduced performance / conspicuous locomotion 3. Altered sexual behaviour - Courtship / mate choice / parental care 4. Altered habitat selection - Horizontal / vertical / cover preferences 5. Altered Anti-predator behaviour - Susceptibility to encounter / detection / capture Altered Habitat Selection Dicrocoelium dendriticum, the lancet fluke Ant subeosophogeal ganglion .. Sheep Eggs released in faeces Ant Snail Ingested eggs form a sporocyst in the snail lung Cercariae (2nd stage larvae) secreted as slime balls on grass Altered Anti-predator behaviour: Toxoplasma gondii Cat (definitive host) Oocyte in faeces Soil Beetle / worm Rat Toxoplasma gondii • Infected rats are – less cautious of novel stimuli – more active = more easily seen – more likely to be caught in traps • Infected rats also show altered antipredator behaviour – In an enclosure experiment, uninfected rats avoided nesting areas that had been sprayed with cat urine / scent – BUT Toxoplasma infected rats readily approached areas laced with cat scent Mechanisms How do parasites change host behaviour? Direct and indirect manipulation Direct (e.g. secretion of a chemical) from Milinski (1990) Indirect (e.g. via alterations in nutrition) Indirect manipulation (an example) Physical presence / sensory disruption e.g. Fish infected with Diplostomum Diplostomum infections in fish Digenean trematodes Bird Snail Fish IH1: Snails IH2: Fish (larval stage – metacercariae) DH: Birds Invades the eyes or brain of many freshwater fish Infection is associated with behaviour changes Diplostomum in the eye • Infected dace – make a higher proportion of failed attacks on prey – spend more time foraging at the water surface – Spend less time hiding from predators Crowden & Broom (1980) Anim. Behav. 28, 287-294 Diplostomum in the eye Infected trout Suffer from ‘parasitic cataract disease’ as a result of heavy infections This means that lenses become clouded as a result of the invasion of large numbers of parasites Infected fish are less likely to be caught by anglers in fly fisheries Economic consequences? Moody & Gaten (1982) Hydrobiologia 88, 207-209 Diplostomum in the brain • Shoals formed by infected minnows… – are less compact – swim closer to the surface …than those formed by uninfected fish Radabaugh (1980) J. Fish Biol. 16, 621-628 Direct manipulation (1) Anaesthetic effects e.g. Cod infected with nematodes Anisakis nematodes in cod (Gadus morhua) Anisakis nematodes require fish intermediate hosts to be eaten by marine mammals Encyst in the musculature of the body wall Waste products include alcohols and ketones Have an anaesthetic effect on fish muscle and impair swimming .. .. . Human herring cod Ackman & Gjelstad (1975) Anal. Biochem. 67, 684-687 Direct manipulation (2) Neuro-endocrine disruption e.g. Gammarus infected with Polymorphus Gammarids infected with Polymorphus paradoxus Acanthocephala (thorny headed worms) Gammarus Duck IH: Gammarus DH: Dabbling ducks Gammarus live in vegetation at edge of lakes and streams Transmitted to ducks when they feed on submerged vegetation Gammarids infected with Polymorphus paradoxus Uninfected Gammarus avoid light and dive when disturbed Gammarus infected with P. paradoxus do not dive, and do not avoid light Instead they skim around the surface and cling to plants when disturbed 100 80 60 40 20 0 % time in light Skimming (%) Clinging (%) Uninfected control Infected Bethel & Holmes 1973 (J. Parasitol. 59, 945-956) Gammarids infected with Polymorphus paradoxus Behaviour of infected Gammarus replicated in non-infected individuals after injection with serotonin Uninfected control Infected Uninfected + Serotonin Parasites located near ganglion Ganglion = cluster of nerve cells. Nerves run from ganglia in passage to or from the brain to specific sites in the body Parasites may control host behaviour by modifying hosts natural levels of neurotransmitter 100 80 60 40 20 0 % time in light Skimming Clinging (%) (%) Serotonin = parasite effects Helluy & Holmes (1990) Can. J. Zool. 68, 1214-1220 Gammarids infected with Polymorphus paradoxus • Serotonin – neurotransmitter, release controlled by complex pathway. Affects emotion, behaviour and thought. Lack of seratonin is thought to cause depression in humans • • Production of serotonin modulated by – Prozac™ – Chocolate – Red wine – LSD Clinging is only normally exhibited as part of mating behaviour – Are parasites manipulating Gammarus behaviour by influencing host ‘sex drive’? • Mechanisms of manipulation: summary • Parasites employ a wide range of mechanisms, from the simple (site selection, e.g. the eye) to the complex (neurochemical modulation) to alter the behaviour of hosts But, does parasite manipulation of hosts have real ecological effects? Consequences of altered behaviour Do behavioural changes have real ecological effects? Ecology – the distribution and abundance of organisms within and between habitats Ecological effects: A study of ‘Parasite Increased Trophic Transmission (PITT)’ Lafferty & Morris examined the behaviour of parasitised and non-parasitised killifish Parasite: Euhaplorchis californiensis (Trematode) Large numbers of cercariae encyst in the brain case of host fish = behaviour change…. Lafferty & Morris 1996 (Ecology 77, 1390-1397) Infected killifish exhibited altered behaviour Infected Conspicuous behaviours in 30min Uninfected 30 25 20 15 Infected fish performed many more ‘conspicuous’ behaviours 10 5 0 0 500 1000 1500 2000 2500 Include ‘flashing’, jerking and ‘surfacing’ Number of parasites Lafferty & Morris 1996 (Ecology 77, 1390-1397) Lafferty & Morris’s enclosure experiment: ecological effects of altered behaviour Open to allow bird predation Closed to stop bird predation Enclosures were stocked with equal proportions of uninfected and infected fish Herons, kingfishers and egrets were seen to hunt in the open enclosures Examined proportion of infected and non-infected fish at the end of the study in each type of enclosure (20d) Birds selectively caught infected fish 1 Proportion eaten by birds 0.9 0.8 0.7 0.6 0.5 0.4 0.3 0.2 0.1 0 Uninfected <1400 cysts >1400 cysts Parasite intensity Lafferty & Morris 1996 (Ecology 77, 1390-1397) Summary of Lafferty and Morris, 1996 • No difference in the mortality of infected and non-infected fish in the covered enclosure • In the open enclosure, infected fish were 40x more likely to be taken by birds! • Suggests that parasites have an enormous effect on the ecology of ecosystems • What would happen if the parasites did not exist? Just for thought…… We have shown that parasites rely on host behaviour for trophic transmission But in the ‘real ecological world’ many non-target predators will consume infected hosts. This diminishes the adaptiveness of behavioural manipulation! e.g. The new zealand cockle and the trematode, Curtuteria australis (Mouritsen & Poulin, 2003, International Journal Parasitology) When do you think parasites should or shouldn’t manipulate their hosts? Recommended reading Moore, J (2002) Parasites and the Behavior of Animals. Zimmer, C (2001) Parasite Rex. Barnard, CJ & Behnke, JM (1990) Parasitism & Host Behaviour Dawkins, R (1982) The Extended Phenotype (Ch.12)