Drivers of population-level effects of parasite virulence

Life-history meets meta-analysis

Maggie J. Watson Charles Sturt University, Australia

A central goal of population ecology is to identify factors controlling population dynamics.

Population Size• Intrinsic Death Rate• Parasites• Predators• Disease

Population Size• Intrinsic Birth Rate• Food Supply

Parasites—the focus of MANY experimental studies

Do parasites affect individuals?

Parasites—the focus of MANY experimental studies

Do parasites regulate populations?

Population regulation by parasites has been identified in Red Grouse Lagopus lagopus scoticus

Hudson et al. 1998

Svalbard Reindeer Rangifer tarandus platyrhnchus

Albon et al. 2002

and Soay Sheep Ovis aries

Gulland 1992

...but, they are all managed populations

Thus, the question still remains—are parasites significant drivers of population-level effects and what host life-history traits drive

observed parasite virulence?

• Identify a common measure of EFFECT SIZE resulting in a weighted average

• Estimate, with great power, the TRUE EFFECT SIZE

A meta-analysis of 38 experimental studies (31 avian, 6 mammalian, 1 fish) of the costs of parasites to population-level measures of natural, free-ranging hosts revealed an overall effect size,

d =0.49

% breeding succ., # young produced, survival, clutch size, hatching succ.

d =0.49

This is HUGE!

But, a very small pool…

• 1 Perciformes• 2 Galliformes• 1 Columbiformes• 1 Ciconiiformes• 1 Pelicaniformes• 2 Charadriiformes• 1 Apodiformes• 23 Passeriformes• 2 Lagomorpha• 3 Rodentia• 1 Artiodactyla

But, a very small pool…

• 1 Perciformes• 2 Galliformes• 1 Columbiformes• 1 Ciconiiformes• 1 Pelicaniformes• 2 Charadriiformes• 1 Apodiformes• 23 Passeriformes• 2 Lagomorpha• 3 Rodentia• 1 Artiodactyla

Not

eve

ryth

ing

is a

pas

serin

e…

So where to now?

What host traits influence parasite

virulence?

Some predictions…

Expect greater effects in:

• Cavity nesters• Colonial species• Tropical species• Species with high

mortality rates

Møller et al. 2009 A meta-analysis of parasite virulence in nestling birds. Biol. Rev. 84: 567-588

Nidelet et al. 2009. Effects of shortened host life span on the evolution of parasite life history and virulence in a microbial host-parasite system. BMC Evolutionary Biology 9:65.

…cavity nesters?

-2

-1

0

1

2

3

4

Effec

t Siz

e

Open Nest Cavity Nest

Z*=-0.34p-value=0.97

…coloniality?

-2

-1

0

1

2

3

4

Effec

t siz

e

Not Colonial Highly Colonial

Z*=0.36p-value=0.72

…latitude?

0 15 30 45 60 75 90

-2

-1

0

1

2

3

4

Effec

t Siz

e (d

)

Z*=-1.30p-value=0.19

0 5 10 15 20 25 30 35 40 45 50-2

-1

0

1

2

3

4

Lifespan (years)

Effec

t siz

e

…host lifespan (maximum)?

Z*=-1.44p-value=0.15

0 5 10 15 20 25 30-2

-1

0

1

2

3

4

Lifespan (Years)

Effec

t Siz

e…host lifespan (average)?

Z*=-1.93p-value=0.05

0 5 10 15 20 25 30

-2

-1

0

1

2

3

4

Lifespan (Years)

Effec

t Siz

e of

Par

asite

s

…which species?

Some results…

Found greater effects in:

• Cavity nesters • Colonial species • Tropical species • Species with lower

average lifespans

Conclusions

• Yes, parasites do have population level effects, but are they biologically relevant to all species?

• What life-history attributes determine virulence?

• Future areas of inquiry—lifespan of host organism, ideally study (truly) long-lived organisms and species other than tits and swallows and martins!

An aside about data reporting…

• Means• SD or SE• Sample sizes• …and make sure

there are comparable categories to other studies

Now for a parasite removal experiment!

…and lots of pretty pictures!

Host species• Crested Tern (Thalasseus

bergii cristata , Stephens 1826)

• Colonial• Abundant (IUCN Least

Concern)• Ubiquitous (Africa to

Australia)• Naturally heavily

parasitised • And VERY long lived…

Parasite Species• Lice

– Austromenopon atrofulvum

– Quadraceps sellatus – Saemundssonia

laticaudata – …and maybe more!

• Ticks– Ornithodoros capensis– Ixodes kohlsi

Methods• Morphometric changes

– Bill + Head– Mass– Sex specific growth

• Haematological changes– Haematocrit

• Immunological changes– Total WBC counts– Heterophil/Eosinophil Ratio

• Survival• Metabolic (?) changes

– Ptilochronology– Fluctuating Asymmetry

Medication experiment:Sample size: 388; 178 recapturedIvomec vs. Control

Pthilochronology: growth bars

1 2 3

ResultsMedication reduced

parasite numbers (p=0.00051)

High vs. Low Parasites Weight gain p=0.23 Bill + Head p=0.51

Males vs. Females Weight gain p=0.35 Bill + Head p=0.39

Haematocrit NS

Results: Immunological (Total WBC Counts)

0 50 100 1500

5

10

15

20

25

30

R² = 0.378605881014183

Total WBC Count

Num

ber o

f Par

asite

s

Results: Immunological (H/E Ratio)

0 5 10 150

5

10

15

20

25

R² = 0.197254487275589

Heterophil:Eosinophil Ratio

Num

ber o

f Par

asite

s

2008-9 poor food supplies 2009-10 good food supplies

Results: Ptilochronology

0 5 10 15 20 250

2

4

6

R² = 0.02770795174516010 5 10 15 200

2

4

6

R² = 0.43324472117248

Number of Parasites (Rank Order)

Gro

wth

bar

s (m

m)

Results: Fluctuating Asymmetry

low parasites high parasites0.00

0.10

0.20

0.30

0.40

0.50

0.60

0.70

0.80

0.90

Asym

met

ry B

etw

een

Tail

Feat

hers

(mm

)

P=0.03

N=24

N=26

What do the non-significant results mean?

• Morphometric changes obfuscated by food supply

• Haematocrit and age• Ptilochronology and

food supply• Ptilochronology and

“quality”• Long-lived species and

survival

What do the significant results mean?

• The benefits of parasites• Immunological “costs”• Metabolic “costs” and

effects on long-term “quality

Conclusions • In highly evolved natural systems, parasites may not affect hosts except during extreme stochastic events.

• Long-lived species are not as affected by their parasites as short-lived species.

Acknowledgements

Trusty fieldworkers: Dave, Douglas, Jack and Charlie Watson, Andrew, and the other Maggie

The notoriously unphotographable advisor: Shane Raidal

Funded by ILWS CSU Scholarship and Holsworth Foundation Grants