Elsevier

Agriculture, Ecosystems & Environment

Volume 237, 16 January 2017, Pages 265-273
Agriculture, Ecosystems & Environment

Environmental risk factors for Ixodes ricinus ticks and their infestation on lambs in a changing ecosystem: Implications for tick control and the impact of woodland encroachment on tick-borne disease in livestock

https://doi.org/10.1016/j.agee.2016.12.041Get rights and content

Highlights

  • Tick counts on ground vegetation is a good proxy of tick burdens on sheep.

  • Tree cover on pastures relates to tick counts on sheep and on ground vegetation.

  • Woodland encroachment onto pastures may increase sheep tick-borne disease risk.

Abstract

Despite global deforestation some regions, such as Europe, are currently experiencing rapid reforestation. Some of this is unintended woodland encroachment onto farmland as a result of reduced livestock pasture management. Our aim was to determine the likely impacts of this on exposure to ticks and tick-borne disease risk for sheep in Norway, a country experiencing ecosystem changes through rapid woodland encroachment as well as increases in abundance and distribution of Ixodes ricinus ticks and tick-borne disease incidence. We conducted surveys of I. ricinus ticks on ground vegetation using cloth lure transects and counts of ticks biting lambs on spring pastures, where lambs are exposed to infection with Anaplasma phagocytophilum, the causative agent of tick-borne fever in livestock. Pastures had higher densities of I. ricinus ticks on the ground vegetation and more ticks biting lambs if there was more tree cover in or adjacent to pastures. Importantly, there was a close correlation between questing tick density on pastures and counts of ticks biting lambs on the same pasture, indicating that cloth lure transects are a good proxy of risk to livestock of tick exposure and tick-borne disease. These findings can inform policy on environmental tick control measures such as habitat management, choice of livestock grazing area and off-host application of tick control agents.

Introduction

Agriculture is the main driver of massive historical and current global deforestation, and this rate of conversion has been accelerating: the net loss of forests increased from 4.1 million hectares per year between 1990 and 2000 to 6.4 million hectares between 2000 and 2005 (FAO and JRC, 2012). However, in some regions of the world such as China and Europe, the opposite trend is occurring: Europe has experienced an increase in forested land cover of more than 600,000 km2 between 1993 and 2006 (IEEP, 2010). Some of this increase is encouraged through European Union subsidies that incentivise active reforestation in order to improve ecosystem services such as carbon sequestration, water quality and biodiversity. However, much of the expansion of woodland cover in Europe is also unintended. For example, 560,000 Ha (60%) of traditional agricultural Alpine meadows in Switzerland are threatened with natural reforestation or “woodland encroachment” due to a reduction in livestock grazing and hay harvesting (Baur, 2006). The same issue exists in Norway, where reduced agricultural pasture management is allowing the encroachment of woodlands onto agricultural land (Bryn and Hemsing, 2012). This is of increasing concern in terms of availability of grazing land for food production, social heritage and tourism (Vinge and Flø, 2015). Such woodland encroachment onto pastures may also have other consequences, such as the potential to increase the risk of tick-borne diseases to livestock and people, unless tick control measures are implemented (Halos et al., 2010, Gilbert, 2013 and Gilbert, 2016).

I. ricinus ticks are generalists, feeding on a wide range of terrestrial vertebrates. Each developmental stage feeds for a few days before dropping off the host to moult and develop or lay eggs in the ground; over 90% of the life cycle of I. ricinus is spent off the host (Needham and Teel, 1991). I. ricinus are the most important tick species in Europe in terms of vectoring tick-borne pathogens to humans (particularly Borrelia burgdorferi sensu lato, the causative agents of Lyme borreliosis, and the tick-borne encephalitis virus) and livestock (particularly Anaplasma, Rikettsia and Babesia species). I. ricinus ticks are increasing in abundance and distribution in several areas of Europe (Lindgren et al., 2000, Danielová et al., 2006, Materna et al., 2008), including Norway (Jore et al., 2011). Norway has also experienced an increase in reported incidence of tick-borne diseases such as TBE (Andreassen et al., 2012) and Lyme borreliosis (Hjetland et al., 2014) in humans and tick-borne fever (caused by Anaplasma phagocytophilum) which is the most widespread tick-borne infection in animals in Europe (Stuen, 2007). Sheep Ovis aries farming is extremely important to livelihoods and economies in rural areas in Norway (SSB, 2013) and one of the main challenges to sheep farmers in the grazing season is the economic loss from tick-borne fever (Stuen and Kjølleberg, 2000, Stuen et al., 2002, Stuen, 2003, Grøva et al., 2011, Grøva et al., 2013), since 55–80% of lambs can be exposed to infection (Stuen and Bergstrom, 2001, Grøva et al., 2011) and A. phagocytophilum-related mortality rates of over 30% have been observed (Stuen and Kjølleberg, 2000, Brodie et al., 1986). It is thus of increasing urgency to control exposure of livestock to ticks and tick-borne pathogens, and this requires an understanding or where and why tick exposure to livestock is greatest.

Although exposure of livestock to ticks is often mitigated by acaricide (chemical pesticide) application to the host animal (George et al., 2004, George et al., 2008, Beugnet and Franc, 2012) there is now an increasing demand for alternative measures to reduce exposure of livestock to ticks such as habitat management, separation of livestock from tick-infested areas or the application of biological control agents to the pastures (Klingen and van Duijvendijk, 2016). In order to implement these alternative approaches we need to be able to identify which areas or habitats are likely to have the greatest tick abundance and, crucially, whether these areas or habitats are also associated with higher tick infestation on livestock. This latter point is essential to ascertain, because tick abundance in the environment does not necessarily correlate with tick burdens on livestock if the livestock avoid those areas or habitats. If this is the case, applying tick control measures to such areas is unlikely to alleviate exposure of livestock to tick-borne pathogens. However, once we have established which areas are associated with greatest tick burdens on both livestock and in the environment, tick control measures can be implemented in those areas.

Sheep in Norway commonly spend the winter at low altitudes in and around the shelter of the farm buildings. Lambing generally takes place indoors and when the lambs are 1–3 weeks old they are released, together with their mothers, onto fenced spring pastures close to the farm for 2–4 weeks. They are then let out for the summer onto unfenced “rangeland” areas, which generally have a mix of forested and open habitats and are usually at higher altitudes than the farm. Even though the sheep spend only 2–4 weeks on lowland fenced spring pastures, infection rates of lambs with A. phagocytophilum (the causative agent of tick-borne fever) during this time is reported to be very high

It is also the enclosed spring pastures where it will be most practical to implement tick control measures; once the sheep are free to roam on the higher altitude unfenced rangelands, controlling where they go or implementing tick control in the environment becomes much more difficult and costly (Klingen and van Duijvendijk, 2016). Therefore, this study focusses on fenced spring pastures, rather than high altitude unfenced range lands, in Norway.

The overarching objective of this study is to test the effect of woodland encroachment on the risk of exposure of livestock to Ixodes ricinus tick bites, with clear implications for risk of tick-borne diseases and economic consequences for agriculture. We therefore aim to identify the environmental risk factors, with a focus on tree cover, in spring pastures associated with (i) abundance of questing (i.e. host-seeking) I. ricinus on ground vegetation and (ii) I. ricinus tick burdens biting lambs. Importantly, we also test the relationship between the abundance of questing I. ricinus on the ground and tick burdens on lambs; this will also confirm whether surveys of questing ticks on ground vegetation can be used as a useful proxy of tick exposure to sheep for future studies.

Section snippets

Study sites

Surveys were conducted on fenced spring pastures in Møre and Romsdal county in mid-western Norway (62° 30′ N, 7° 10′ E), an area endemic with tick borne fever. A total of 25 spring pastures for grazing animals (predominantly sheep but also horses or cattle, see Table 1) were surveyed in the second half of May and the first half of June in 2011 and/or 2012; 14 pastures were surveyed in both years. All pastures were visited twice in each year surveyed, 1–3 weeks apart. All pastures were within an

Questing nymphs

The total number of nymphs counted over all flagging transects at all sites was 809 in 2011 and 648 in 2012, with an average of 1.1 (±0.35 SE, range 0–58) nymphs per 10m2. There were more questing nymphs if there was more canopy cover, less grass, lower ground vegetation, and fewer dung counted over the 10 m × 1 m transect. There were also more questing nymphs per transect if the whole pasture was characterised as having more tree cover or less grass cover. There were more questing nymphs with

Discussion

The main aim of this study was to assess the potential impact of woodland encroachment into pastures on tick bite risk (with implications for tick-borne diseases) for sheep in Norway, by examining the associations between tree cover on spring pastures on both questing ticks and lamb tick burdens.

We found that both questing nymph and questing adult tick abundances were positively associated with the proportion of tree canopy covering the 10 m × 1 m cloth lure transects and, conversely, negatively

Conclusions

We found that woodland encroachment into and surrounding lowland livestock pastures in Norway is associated with higher questing tick abundance in the ground vegetation and also, crucially, higher tick counts on lambs. While we did not measure tick-borne pathogens in the sheep or the ticks, there are clear implications for tick-borne disease risk given the high seroprevalence of A. phagocytophilum in sheep in many coastal regions of Norway, the general correlation between tick burdens and

Acknowledgements

We are indebted to the farmers for allowing access to their pastures and sheep, and to Peggy Haugnes, Anne deBoer, Marius Bless, Thomas Cull and Sean Webber for fieldwork assistance. This study was funded by the Norwegian Foundation for Research Levy on Agricultural Products (FFL) and the Agricultural Agreement Research Funds (JA), the Møre og Romsdal Council and County Governor in Møre og Romsdal through the project TICKLESS (project number 207737). L. Gilbert received addition support from

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