Environmental associations of ticks and disease. Lucy Gilbert

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1 Environmental associations of ticks and disease Lucy Gilbert

Ticks in Europe 1. Ixodes arboricola 2. Ixodes caledonicus 3. Ixodes frontalis 4.

Ixodes acuminatus 9. Ixodes apronophorus 10. Ixodes canisuga 11.

Ixodes hexagonus 15. Ixodes ricinus 16. Dermacentor reticulatus 17.

Argas reflexus 21. Argas vespertilionis 22.

tick Puffin tick Cormorant tick Seabird tick Southern rodent tick Marsh tick Fox

2 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

3 Approx. distribution of Ixodes ricinus

Pathogens transmitted by Ixodid ticks : Viruses: Tick-Borne

Babesia spp cause babesiosis, red-water fever Bacteria: Rickettsiae

causes Q-fever Anaplasma and Ehrlichia sp e.g.

(HGA) and Tick-Borne Fever in sheep & cattle.

4 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

5 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

6 NYMPHS Nymphal tick abundance April May June July Aug Sept Oct

7 What are the environmental factors associated with ticks and tick-borne diseases? Climate Habitat, Hosts, e.g. wildlife & livestock

8 Using altitude to study the effect of climate on tick abundance X 9 hills

7 6 5 4 3 2 1 0 400 500 600 700 800 900 altitude

9 Tick abundance decreases dramatically at higher altitudes due to the colder climate nymphs per drag altitude (masl) increase of 3 o C Gilbert (2010) Oecologia 162:

10 Does risk of tick bites depend on the weather on the day? Experiment: 30 nymphs per tube 6 15 o C We counted the proportion of ticks that were questing at each temperature

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

Grasslands Semi-natural woodland Conifer plantation But

12 Which Habitats are worse for ticks? Tick surveys at 77 sites across Scotland Heather/bog Grasslands Semi-natural woodland Conifer plantation But high variation due to different regions, altitudes, climates, hosts. We need an experiment!

13 Effect of animal densities on tick abundance? Red deer Deer index (dung counts) 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

14 Deer exclosure experiment: fenced vs unfenced areas 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 Gilbert et al. (2012) Ecological Applications 22:

15 Tying the tick factors together: statistical analysis of 300+ site surveys HABITAT Broadleaved woodland Estimate (slope) = 3.2 SEASON (May/June) Estimate (slope) = 1.8 Coniferous woodland Estimate (slope) = 1.0 Heather moorland Estimate (slope) = 0.4 CLIMATE Frost days in September Estimate (slope) = -1.8 Deer density Estimate (slope) = 0.06 Mean annual temperature Estimate (slope) = 0.2

16 Lyme disease No longer notifiable

17 What is the prevalence of Borrelia in ticks in Scotland? Surveys of 25 woodlands Average prevalence = 5.6% Range = 1-14% What drives these differences in prevalence? Vegetation surveys, dung counts, GIS climate data. James et al. (2013) Parasitol. 140:

Which factors are associated with Borrelia

Estimate Upper CI Lower CI z-value p-value

051 Altitude -0.0002-0.0003-0.0001-2.954 0.

18 Which factors are associated with Borrelia in questing nymphs? B. burgdorferi s.l. Estimate Upper CI Lower CI z-value p-value Deciduous wood Altitude Julian day Relative humidity Ground vegetation height Red deer index Habitat/hosts climate season weather Habitat/hosts hosts James et al. (2013) Parasitol. 140:

19 Average Borrelia prevalence in nymph ticks = 2.1% (range 0-12%) 25 woodlands Including 6 from the previous survey to examine temporal stability. This study found no effect of deer or forest type on Borrelia prevalence. Only an effect of climate (warmer = more Borrelia).

20 Why these differences between the 2 studies? The effect of deer may depend on deer density, and what other hosts are available Theoretical Mathematical Models predict that as deer densities increase, there will be a rise then a fall in Borrelia prevalence: Borrelia prevalence Ratio of incompetent : competent transmission hosts Few deer many deer 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!

21 A study on garden/woodland birds found that the most important birds for ticks and Borrelia = All ground foragers James et al. (2011) Ibis 153:

22 Ticks, Louping Ill virus and Mountain Hares Using mathematical models to predict when culling mountain hares might reduce LIV

23 1. With grouse and hares only. Gilbert et al. (2001) Journal of Animal Ecology 70: R 0 =1 X 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

24 2. Add deer to the system (very low density: 2 km -2 ). Gilbert et al. (2001) Journal of Animal Ecology 70: X X 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

Most estates also have deer: Serious management

control ticks and LIV in the majority of cases.

LIV are THE main problem limiting grouse numbers.

more important, then tick or LIV control measures are

25 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 Journal of Applied Ecology 47:

26 THANK YOU! Jim McLeod, Jennifer Aungier, Dave Riach Alan Bowman, Ken Forbes, Marianne James Roman Biek, Caroline Millins Rachel Norman, Ros Porter Joseph Tomkins

How does tick ecology determine risk?

How does tick ecology determine risk? Sarah Randolph Department of Zoology, University of Oxford, UK LDA, Leicester, July.00 Tick species found in the UK Small rodents Water voles Birds (hole nesting)