Parasites

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Parasites Host Behaviour I

• Dr Hazel Wright
• hzw_at_aber.ac.uk
• Edward Llwyd Building

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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.
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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
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1. Parasites exploit natural patterns of host
behaviour to maximise transmission
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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
Stickleback
Free-swimming coracidium
Copepod sp.
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Example 2 A tale of two fishes
Parasites are closely related, but cannot
successfully infect the wrong host
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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
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Example 3 The Guinea worm (Dracunculus
medinensis )
Larvae migrate to connective tissue and develop
into adults
Adults migrate to limbs. Toxic substance breaks
down skin.
Combat infection by using medicinal plants
(burning / itching) and scanning the water for
infected copepods.
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• We have shown that host behaviour can influence
  parasite infections

• Therefore..variation in host behaviour
  patterns can create variation in parasite
  infection levels

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2. Hosts can evolve behavioural resistance as a
response to infection threat
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Behavioural resistance the first line of 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
Immune defense is important BUT it is
energetically expensive.
Negative effects regarding growth, fat storage
and reproduction
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Behavioural resistancethe first line of defence

• Avoiding infections
• Food selection (cattle)
• Nest use (great tits)
• Mate choice (various)

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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.
Cattle were grazing selectively on clean
pasture to reduce the chance of infection
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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?
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Avoiding infection (2) Nest box use by the
great tit, Parus major
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
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Avoiding infection (3) Mate choice
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?
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Avoiding infections 3 Mate choice evidence for
Parasite-mediated sexual selection
No Yes Yes Yes Yes Yes
No Yes Yes Yes Yes Yes
Call rate Display rate Red colour Display Ornament
s Tail length
Cricket Guppy Stickleback Pheasant Jungle
Fowl Swallow
Where secondary sexual characters indicate
health, parasite mediated sexual selection can
occur
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Behavioural resistancethe first line of defence

• Avoiding infections
• Food selection (cattle)
• Nest use (great tits)
• Mate choice (various)

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Parasite reduction mechanisms 1Self preening in
chickens (Gallus gallus )
Self preening is an effective anti-parasite
behaviour
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Parasite reduction mechanisms 1 Self preening
in chickens
Birds prevented from preening show poor growth
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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
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Parasite reduction mechanisms 3 Nest fumigation
by starlings (Sturnus vulgaris)
Such plants contain biocidal substances
Are birds using plant compounds as antiparasite
fumigants?
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
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Summary

• Parasites exploit natural patterns of host
  behaviour for transmission

Hosts have responded by adapting their behaviour
to reduce the chance / intensity of infection
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Parasites andHost Behaviour II

• Dr Hazel Wright
• hzw_at_aber.ac.uk
• Edward Llwyd Building

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Parasite life cycles are enormously variable
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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
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• Why do parasites change host behaviour?

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The mixed phenotype idea
Parasite model
When infections cause changes in host
behavioura parasites genes find phenotypic
expression in the behaviour of the host
The Extended Phenotype Chapter 12 (Host
phenotypes of parasite genes)
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In other words.
The mixed phenotype idea states that
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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
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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
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Behavioural effects of parasites

• What behaviours are changed?

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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
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Ant subeosophogeal ganglion
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Altered Anti-predator behaviour Toxoplasma
gondii
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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

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Mechanisms

• How do parasites change host behaviour?

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Direct and indirect manipulation
Direct (e.g. secretion of a chemical)
Indirect (e.g. via alterations in nutrition)
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Physical presence / sensory disruption
Indirect manipulation (an example)

• e.g. Fish infected with Diplostomum

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Diplostomum infections in fish
Digenean trematodes
DH Birds
Invades the eyes or brain of many freshwater fish
Infection is associated with behaviour changes
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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
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Diplostomum in the eye
Infected trout
Suffer from parasitic cataract disease as a
result of heavy infections
Infected fish are less likely to be caught by
anglers in fly fisheries
Economic consequences?
Moody Gaten (1982) Hydrobiologia 88, 207-209
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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
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Anaesthetic effects
Direct manipulation (1)

• e.g. Cod infected with nematodes

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Anisakis nematodes in cod (Gadus morhua)
Anisakis nematodes require fish intermediate
hosts to be eaten by marine mammals
.
.
.
.
.
.
Waste products include alcohols and ketones
Have an anaesthetic effect on fish muscle and
impair swimming
Ackman Gjelstad (1975) Anal. Biochem. 67,
684-687
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Neuro-endocrine disruption
Direct manipulation (2)

• e.g. Gammarus infected with Polymorphus

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Gammarids infected with Polymorphus paradoxus
Acanthocephala (thorny headed worms)
Gammarus live in vegetation at edge of lakes and
streams
Transmitted to ducks when they feed on submerged
vegetation
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Gammarids infected with Polymorphus paradoxus
Uninfected Gammarus avoid light and dive when
disturbed
Uninfected control
Infected
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
Bethel Holmes 1973 (J. Parasitol. 59, 945-956)
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Gammarids infected with Polymorphus paradoxus
Behaviour of infected Gammarus replicated in
non-infected individuals after injection with
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
Helluy Holmes (1990) Can. J. Zool. 68, 1214-1220
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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?

IH Gammarus
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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?
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Consequences of altered behaviour

• Do behavioural changes have real ecological
  effects?

• Ecology
• the distribution and abundance of organisms
  within and between habitats

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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)
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Infected killifish exhibited altered behaviour
Infected fish performed many more conspicuous
behaviours
Include flashing, jerking and surfacing
Lafferty Morris 1996 (Ecology 77, 1390-1397)
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Lafferty Morriss enclosure experiment
ecological effects of altered behaviour
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)
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Birds selectively caught infected fish
Lafferty Morris 1996 (Ecology 77, 1390-1397)
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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?

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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 shouldnt
manipulate their hosts?
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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)