Lucy Gilbert

Environmental associations of ticks and disease

Ticks in Europe

1. Ixodes arboricola 2. Ixodes caledonicus 3. Ixodes frontalis 4. Ixodes lividus 5. Ixodes rothschildi 6. Ixodes unicavatus 7. Ixodes uriae 8. Ixodes acuminatus 9. Ixodes apronophorus 10. Ixodes canisuga 11. Ixodes ventalloi 12. Ixodes trianguliceps 13. Ixodes vespertilionis 14. Ixodes hexagonus 15. Ixodes ricinus 16. Dermacentor reticulatus 17. Rhipicephalus sanguineus 18. Hyalomma marginatum 19. Haemaphysalis punctata 20. Argas reflexus 21. Argas vespertilionis 22. Ornithodoros maritimus

Tree hole tick Northern bird tick Passerine tick Sand martin tick Puffin tick Cormorant tick Seabird tick Southern rodent tick Marsh tick Fox tick Rabbit tick Shrew tick Long-legged bat tick Hedgehog tick Sheep tick Ornate cow tick Brown dog tick Two-host tick Coastal red tick Pigeon tick Blyborough tick Marine argasid

Approx. distribution of Ixodes ricinus

Pathogens transmitted by Ixodid ticks : Viruses: Tick-Borne Encephalitis Virus complex, including

Louping ill virus Protozoa: Babesia spp cause babesiosis, red-water fever Bacteria: Rickettsiae causing spotted fever rickettsiosis, tick typhus Coxiella burnetii causes Q-fever Anaplasma and Ehrlichia sp e.g. Anaplasma phagocytophilum causes Human Granulocytotropic Anaplasmosis (HGA) and Tick-Borne Fever in sheep & cattle. Neoehrlichia mikurensis Bartonella - cat scratch fever Francisella tularensis causing tularaemia Borrelia burgdorferi s.l. complex - Lyme

borreliosis

Life cycle of I. ricinus & Borrelia

Most Borrelia infections in humans are from Nymphs. Larvae are uninfected.

Nymphs become infected when they are larvae feeding on rodents & birds

More larvae and nymphs feeding on rodents/birds increase transmission potential

Deer do not transmit Borrelia, but are main hosts for adult ticks, so create large larval tick populations

April May July Aug Sept Oct June

Nym

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tic

k ab

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NYMPHS

• Climate

• Habitat,

• Hosts, e.g. wildlife & livestock

What are the environmental factors associated with ticks and tick-borne diseases?

Using altitude to study the effect of climate on tick abundance

X 9 hills

altitude (masl)400 500 600 700 800 900

nym

phs p

er d

rag

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1

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3

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Tick abundance decreases dramatically at higher altitudes – due to the colder

climate

increase of 3oC Gilbert (2010) Oecologia 162: 217-225

Does risk of tick bites depend on the weather on the day?

We counted the proportion of ticks that were questing at each temperature

Experiment: 30 nymphs per tube 6 – 15oC

Ticks are more active at warmer temperatures – so risk is higher on warm days Note also that Scottish ticks are cold-adapted!

Which Habitats are worse for ticks?

Heather/bog Grasslands Semi-natural woodland

Conifer plantation

Tick surveys at 77 sites across Scotland

But high variation due to different regions, altitudes, climates, hosts. We need an experiment!

Effect of animal densities on tick abundance?

Variance due to different habitats and regions – need to test the effect of deer experimentally

- Test deer vs no deer in same habitat, same place, same time…

Deer index (dung counts)

Red deer

Moorland deer farm Small plots

V high deer density

Moorland estate Small plots

“normal” deer density

Commercial Forestry

An effective way to control ticks can be through deer management

Deer exclosure experiment: fenced vs unfenced areas

Gilbert et al. (2012) Ecological Applications 22: 658–667

SEASON (May/June) Estimate (slope) = 1.8

Deer density Estimate (slope) = 0.06

Broadleaved woodland Estimate (slope) = 3.2

Coniferous woodland Estimate (slope) = 1.0

Heather moorland Estimate (slope) = 0.4

HABITAT

Mean annual temperature Estimate (slope) = 0.2

Frost days in September Estimate (slope) = -1.8

CLIMATE

Tying the tick factors together: statistical analysis of 300+ site surveys

Lyme disease

No longer notifiable

http://www.documents.hps.scot.nhs.uk/giz/10-year-tables/lyme.pdf

What is the prevalence of Borrelia in ticks in Scotland?

What drives these differences in prevalence?

Vegetation surveys,

dung counts, GIS climate data.

Surveys of 25 woodlands

Average prevalence = 5.6% Range = 1-14%

James et al. (2013) Parasitol. 140: 237-246

B. burgdorferi s.l. Estimate Upper CI Lower CI z-value p-value

Deciduous wood 0.0341 -0.0007 0.0873 1.952 0.051

Altitude -0.0002 -0.0003 -0.0001 -2.954 0.003

Julian day 0.0007 0.0003 0.0012 3.112 0.002

Relative humidity -0.0012 -0.0021 -0.0002 -2.393 0.017

Ground vegetation height -0.0010 -0.0019 -0.0001 -2.173 0.03

Red deer index 0.0861 0.0054 0.2385 2.211 0.027

Which factors are associated with Borrelia in questing nymphs?

James et al. (2013) Parasitol. 140: 237-246

climate season weather Habitat/hosts hosts Habitat/hosts

25 woodlands

Including 6 from the previous survey to examine temporal

stability.

Average Borrelia prevalence in nymph ticks = 2.1% (range 0-12%)

This study found no effect of deer or forest type on Borrelia prevalence. Only an effect of climate (warmer = more Borrelia).

Theoretical Mathematical Models predict that as deer densities increase, there will be a rise then a fall in Borrelia prevalence:

Ratio of incompetent : competent transmission hosts

Few deer many deer

Borr

elia

pre

vale

nce

So far no research has investigated this properly. We need surveys covering the full range of deer densities.

I aim to do this and welcome your help to identify sites!

Why these differences between the 2 studies?

The effect of deer may depend on deer density, and what other hosts are available

A study on garden/woodland birds found that the most important birds for ticks and Borrelia =

James et al. (2011) Ibis 153: 293–302

All ground foragers

Ticks, Louping Ill virus and Mountain Hares

Using mathematical models to predict when culling mountain hares might reduce LIV

R0=1

1. With grouse and hares only.

The model predicts that, in the absence of other hosts such as deer, culling hares could potentially reduce LIV if the estate is “above the line”

Gilbert et al. (2001) Journal of Animal Ecology 70: 1053-1061.

X

2. Add deer to the system (very low density: 2 km-2).

In the presence of deer, even culling hares right down to zero will not work Because deer maintain the tick population while grouse transmit the virus

Gilbert et al. (2001) Journal of Animal Ecology 70: 1053-1061.

X

X

Most estates also have deer:

Serious management implication: culling mountain hares is unlikely to control ticks and LIV in the majority of cases.

It is also crucial to first establish whether ticks and LIV are THE main problem limiting grouse numbers.

If other reasons (weather/habitat/predators/worms) are more

important, then tick or LIV control measures are less likely to help.

Harrison et al. 2010. Journal of Applied Ecology 47: 926-930 .

THANK YOU!

Alan Bowman, Ken Forbes, Marianne James

Roman Biek, Caroline Millins

Rachel Norman, Ros Porter

Joseph Tomkins

Jim McLeod, Jennifer Aungier, Dave Riach