The use of cattle Bos taurus for restoring and maintaining holarctic landscapes: Conclusions from a long‐term study (1946–2017) in northern England

Abstract Cattle Bos taurus can perform valuable ecological functions in the maintenance of high nature value (HNV) pastoral systems. They have also attracted attention as potentially filling the ecological niches of megaherbivores, notably the extinct aurochs Bos primigenius, in rewilding initiatives. Native cattle breeds are recognized under the 1992 Rio Convention as components of biodiversity. They are used in HNV settings, but their conservation as breeds has rarely been an important consideration for their management in these contexts. The Chillingham herd has been kept under minimal management in Chillingham Park (northern England) for several centuries. Chillingham Park is not a rewilding scenario, but the long‐term study of the cattle can be informative for the design of rewilding schemes that involve cattle as megaherbivores. The pastures of the park are species‐rich seminatural grasslands. To 2004, pasture management was influenced by the need to provide herbage for a flock of sheep that was under separate ownership, as well as for the cattle. Surveys of the vegetation conducted in 1979 and 2006–2008 showed a decline of plant species richness (species per 100 m2 quadrat) from 33.8 in 1979 to 22.6 in 2006–2008. This was acceptable as the conservation priority has always been the cattle herd. With removal of the sheep from 2004, it became possible to include recovery of plant diversity as a management goal. In 2017, the cattle numbered 111 (64 in 1979). Plant species richness in 2017 had increased to 26.3 species per quadrat. It has therefore been possible at Chillingham both to conserve the cattle herd and to improve plant diversity. While providing basic information of relevance to the management of cattle in free‐ranging situations, this study also suggests a general principle, that the management of pastoral landscapes by native breeds of cattle, can deliver multiple conservation benefits.


| INTRODUC TI ON
Cattle Bos taurus are of acknowledged value in the management of high nature value (HNV) pastoral landscapes and are being used in many European countries, to restore floral and faunal diversity in anthropogenic landscapes (Redecker, Finck, Härdtle, Riecken, & Schröder, 2002). As individual native breeds, they are acknowledged under the Convention on Biodiversity as components of global biodiversity (FAO, 2012) and their conservation is an obligation of signatories to the Convention. For example, in the UK Biodiversity Framework, the conservation of 88 native breeds of livestock (including Chillingham and 24 other cattle breeds) is monitored under the Biodiversity Indicators system (JNCC, 2018).
In addition to the economic value of the breeds as genetic resources, they also have intrinsic or existence values as meriting conservation in their own right independent of potential for economic utilization. The Chillingham herd is an extreme example of this intrinsic value, having been supported for several centuries under the guardianship originally of the Earls of Tankerville and, since 1939, of the Chillingham Wild Cattle Association (CWCA), as a purely charitable activity.
Although known as Wild Cattle, they are descended from husbanded stock, and, while receiving minimal management intervention (culling on the basis of individual welfare, but no castration), the herd is confined in an area of 134 ha and there is winter hay feeding. This cannot be seen as a rewilding operation of any form, but in the absence of truly feral and accessible herds anywhere in the world, it can provide basic biological information of potential use for rewilding scenarios notably those where restoration of food webs is envisaged ("trophic rewilding": Genes, Svenning, Pires, & Fernandez, 2019;Svenning et al., 2016). Pettorelli et al. (2018) mention (their Table 3) seven sets of specific targets for rewilding initiatives, four explicitly involving the reintroduction of megaherbivores.
Our long-term ecological study on the historic Chillingham cattle has been conducted in a single locality; it is observational and not experimental, and the cattle have many unique features (which is a major reason why they have been conserved). Nonetheless, it is possible to draw conclusions which are relevant to policy and practice elsewhere, while aspiring to meet the definition (Baumgärtner, Becker, Frank, Müller, & Quaas, 2008) of an ecological case study as "the descriptive, explorative, and prospective study of a concrete real-world situation, including its practical context and determining factors, for the purpose of generating and testing hypotheses".
The broader context of this study is the issue of multifunctional conservation, with particular reference to the place of livestock biodiversity in socio-ecological systems. We believe this is the first long-term study of such a situation.
The present paper commences with a description of the study area and of the herd, followed by details of its population dynamics.
We then summarize the vegetation surveys we made in 1979, 2006-2008, and 2017. Changes in vegetation over the 38-year period are discussed in parallel with changes in the population dynamics of the cattle since 1946. Finally, we consider implications of this case study for the conservation of pastoral landscapes.

| CHILLING HAM PARK AND THE CHILLING HAM C AT TLE
Chillingham Park is in northern England (55°31′N, 2°54′W), between 98 and 235 m above sea level, at the boundary of an area of mixed moorland and enclosed farmland. It is one of the very few landscape parks in Britain where the tree and pasture components have both survived almost in their original state (Bunce & Hall, 2013;Hall, 2013).
In nearby farmland, most grass fields are lacking in plant species richness (R.G.H. Bunce, unpublished). The plant species richness of Chillingham Park is therefore of both regional and national interest.
The most remarkable feature of Chillingham Park is the herd of white, red-eared, horned cattle ( Figure 1) that have been isolated within the Park, possibly since before the first written record which is dated 1646. This breed is distinctive genetically (Orozco-terWengel et al., 2015;Williams et al., 2015) and intense inbreeding appears to have purged harmful recessive genes (Visscher, Smith, Hall, & Williams, 2001). However, males are subfertile with very poor semen quality (T.J. Fletcher, pers. comm.). While several British landscape parks are associated today with specific herds or breeds, the historic continuity of the Chillingham herd and its relative freedom from invasive management are unique. Indeed, worldwide, relatively few cattle live in a feral state, with unmanaged herd structure and sex ratio. In Europe, the Albères, Monchina, and Mostrenca of Spain, the Cachena (Portugal), and the Betizuak (Basque country) are described as semiferal (Porter, Alderson, Hall, & Sponenberg, 2016). In the Orkney archipelago off northern Scotland, the cattle of Swona have been feral since the 1970s (Hall & Moore, 1986).
All the above-mentioned breeds are associated with landscapes with which they share cultural significance. In situations such as HNV systems using breeds from other countries, or rewilding projects that use Heck cattle (a synthetic "re-creation" of the aurochs; Lorimer & Driessen, 2014), or a more recent development, the "tauros" (Pettorelli et al., 2018;Richmond, Sinding, & Gilbert, 2016), cultural significance is less evident, but may develop as time progresses.
Chillingham cattle have a special official status (Hall et al., 2005), being excluded from the food chain and not required to have ear tags or passports. By special permission, routine testing of the Chillingham herd for bovine tuberculosis is replaced by autopsy of at least one animal per year. Similar provisions apply elsewhere, for example, in the Netherlands a special status of "not kept" is possible (Vermeulen, 2015).
Chillingham cattle are not housed in winter and receive hay in response to appetite. They are relatively small-bodied (mature bull: 300-430 kg, cow approx. 280 kg); about half the body weight of the British beef breeds such as the Galloway cattle frequently used in extensive grazing systems. Practical local experience with beef cattle indicates that Chillingham Park could support a mixed-age herd of 120 animals, provided winter feed is given (C.J. Leyland, pers. comm.) and provided there are no sheep. As a result of intensification practices aimed to secure the herbage supply of the herd and the sheep flock, plant species richness was lost between 1979 and 2008 (Bunce & Hall, 2013). The opportunity now exists to improve the general floral and faunal biodiversity of the Cattle Park by promoting recovery of plant species richness.
Management policy is to keep the herd at just over 100 total.
Apart from a reserve herd in northeast Scotland, this is the only herd • 1980: Deaths of six lactating cows attributed to magnesium deficiency. A rotational programme of fertilization (magnesian limestone) commenced, finally discontinued in 2004 (Bunce & Hall, 2013). No lactating females have been lost for nutritional causes since that date; • 1981: Sheep husbandry was intensified with progressive shift to crossbred ewes (73 kg body weight), flock size 300 ewes; • 1983: Die-off of young and senescent animals, of 27 males and 41 females present in January, 19 males and 13 females (47%) died; Biomass of the Chillingham herd (223 kg/ha; Bunce & Hall, 2013) is high compared with other relatively unmanaged cattle. In the Netherlands reserve of Kennemerduinen (2069 ha, 79 cattle) where there is no winter feeding, biomass is 17 kg/ha (Cromsigt, Kemp, Rodriguez, & Kivit, 2018). On Swona (Hall & Moore, 1986), 113 ha are occupied by 15-20 totally unmanaged cattle which numbered 17 in January 2017 (C. Annal, personal communication), a biomass of 40-88 kg/ha. The sole winter forage supply is cast-up seaweed whose abundance varies from year to year. Generally, in Europe, in extensive husbandry with winter feeding, cattle biomass is very variable (100-500 kg/ha; Hall, 2018).
In principle, the continuance of the Chillingham herd could be achieved with a much smaller herd under a more intensive and invasive management regime but the issues of tradition, male subfertility and demographic stochasticity make this inadvisable.

| MONITORING ME THODS: PL ANTS
Vegetation studies commenced in 1978 to support behavioral ecology studies (Hall, 1988(Hall, ,1989). The first plant survey used the approach which was subsequently formalized as the Countryside Vegetation System (CVS; Bunce et al., 1999). This avoids the difficulties of repeatability associated with phytosociological approaches (Hearn et al., 2011). Agreement Document between Natural England and CWCA, as indicators of "semi-improved grassland" and "dry acid lowland grassland", were distinguished.
In 1979, the vegetation of Chillingham Park was found to be, mainly, infertile, relatively species-rich grassland of a type then still widespread in Britain (Hall & Bunce, 1984). The vegetation was resurveyed by Bunce and Hall (2013) in 2006(denoted here as 2008. Diversity was found to have declined, as would have been anticipated from the liming programme. Regular bracken cutting was undertaken from 2002 to improve the pasture resource in terms of productivity and of species richness. Some wet ground was drained in order to reduce incidence of liver fluke, and further tree regeneration and woodland enhancement were initiated.

| MONITORING ME THODS: C AT TLE
Herd records were available for the period 1945 to December 2017.
Except during limited periods animals were not individually identifiable but all known births and deaths, and sexes were recorded. Animals in at least their third year of life were defined as adults. ULM software (Legendre & Clobert, 1995) was used to calculate the asymptotic natural rate of population increase λ (S.J.G. Hall, unpublished). Adult survival rates over the whole study are compared between the sexes and the phases of the study in Table 1. Comparisons between the phases, and female fertility rates and calculated values for λ, are also given.

| Changes in species richness
The numbers of species of flowering plants, ferns, and mosses, per 100 m 2 quadrat were as follows (mean, with standard deviation When the 2017 quadrats were grouped into Aggregate Classes, mean species richness was, for AC IV, AC VI, and AC VII, respectively, 26, 21, and 31.

| Changes in indicator species
Of 23 indicators of semi-improved grassland and 38 of lowland dry acid grassland, 12 and 14, respectively, have been recorded in our study (of which ten and eight, respectively, in 2017). Of the 18 indicators noted in 2017, 13 showed an increase or no change in number of quadrats where they were found (Table 2). Of the ten indicators for which total cover abundance was assessed all except the herb, Cardamine pratensis showed a decline from 2008 to 2017 (Table 3).
Percentage reduction in bracken cover was not significantly correlated with absolute increase in number of species (n = 29 quadrats, r = 0.28; the only species to show a marked increase in cover abundance was the Competitor (Grime, Hodgson, & Hunt, 2007) species Cirsium arvense.

| Environmental changes
The MAVIS analysis showed that, at the level of Aggregate Classes,

| D ISCUSS I ON
In many respects the Chillingham cattle and their parkland habitat are unique, and while this is a reason to develop an evidence base to underpin their conservation, the results of such research need to be transferable. Long-term monitoring of the herd has already shown this by providing some important scientific insights. Comparison of birth and death data from the mid-19th century with those from the late 20th century (Hall & Hall, 1988) demonstrated continued viability, and the reproductive rate is now higher than when it was last studied intensively . This has implications for the genetic understanding of inbreeding (Visscher et al., 2001;Williams et al., 2015). Also, analysis of birth dates collected since 1946 yielded one of the very few mammalian examples of phenological effects of climate warming (Burthe, Butler, Searle, Hall, & Thackeray, 2011). If the distribution of birth dates over the year is expressed in relation to a fixed date, the median date of conception is seen to have advanced by one day per year over the period 1947-2008, from late September to late July. This phenological change is ascribed to climate warming, acting through advance of the herbage growing season.
We report two new sets of results, firstly, the recent changes in population dynamics of the herd (probably influenced by the greater abundance of herbage following the removal of sheep), and secondly, documentation of vegetation change whose causes, due to the lack of controlled experimentation, we cannot ascertain (including liming, sheep grazing, and eutrophication by nitrogen deposition).

| Population biology of free-living cattle
Our findings on population dynamics provide new characterization information on free-living cattle. This will help to remedy what Pettorelli et al. (2018) describe as "a perceived lack of empirical information [relevant to rewilding] … much could be achieved by adequately synthesizing existing information." Ours is the only longterm dataset on the population dynamics and behavioral ecology of relatively unmanaged cattle of natural sex ratio and age distribution. TA B L E 2 (Continued) TA B L E 2 Numbers of quadrats in which selected plant species occurred that showed changes or stasis in occurrence (numbers of quadrats in which recorded) over the period 1979-2017. In 1979  have been observed in only two years since 1947 and management policy is to avoid these as they could raise concerns for animal welfare, as has happened at Oostvaardersplassen (Gamborg, Gremmen, Christiansen, & Sandøe, 2010). There is no evidence of density dependence in mortality or birth rate (present study, and Hall & Hall, 1988).
Patterns of change in cattle numbers suggest that the liming programme and the resulting vegetation changes, which were evident in 2008 (Bunce & Hall, 2013) were of limited benefit to the cattle which showed a decline in numbers over the period. The sheep may have prevailed in competition for the available herbage, as predicted by Illius and Gordon (1987). The implication is of a conflict of interest between the cattle and the commercial sheep flock, which was only resolved by the purchase by CWCA of the grazing lease and the removal of the flock.

| Chillingham cattle and their botanical and cultural environments
The priority at Chillingham continues to be the maintenance of a   1998Carey et al. (2008. At Chillingham, AC IV is therefore comparatively species-rich, with more species in a smaller quadrat (25.7 species per 100 m 2 quadrat) and is therefore an important resource of this biodiverse habitat. Mitchell et al. (2017) found that in Scottish grasslands over the are likely to be long-lasting (Melts et al., 2018). For example, in arable land in Canada, the effect of a single application of lime on soil pH was still detectable 30 years later (Beckie & Ukrainetz, 1996).
Some changes in species cover and abundance suggest a decrease in fertility from 2008 to 2017; changes in quadrat from one vegetation class to another are consistent with this, but statistically significant effects are not present.

| Multifunctionality in conservation
The Chillingham study is the first published example of multiple conservation benefits coming from a plant-herbivore system operating in an acknowledged cultural and historic landscape. Chillingham Park exemplifies a medium productivity environment that would be best managed with a land-sharing, rather than land-sparing approach (Maskell et al., 2013), and is an expression of the linkage that is envisaged between agri-environment schemes and ecosystem services (Whittingham, 2011). In practical terms it highlights the relative ease of long-term monitoring and, together with earlier publications (for example, Hall, 1989;Hall & Hall, 1988) provides baseline data on the biology of nonhusbanded cattle, of potential value for rewilding projects. Management priority will continue to be assigned to the cattle, but the value of Chillingham Park as a species-rich example of a diminishing habitat type is now acknowledged. Breed choice for trophic rewilding will be more restricted, with a premium being on hardiness, but the persistence of the Swona herd (descendants of Shorthorn -Aberdeen Angus crossbreds) in apparently difficult conditions suggests the choice may be fairly wide.
Heck cattle or the "tauros" would be other choices, which could be controversial for reasons beyond the scope of this paper.
In Europe, cattle B. taurus are subject to national animal welfare and health laws which can, however, be adapted to accommodate freeliving herds (Hall et al., 2005;Vermeulen, 2015). There is much public interest in rewilding (Jorgensen, 2015) and considerable public sensitivities to the welfare of extensively kept cattle (van Klink & Kampf, 2008), which will need to be addressed early in project development.

| Livestock biodiversity in a broader context
A prediction of the present discussion that could be tested by modeling is that the overall monetized and nonmonetized conservation F I G U R E 4 Changes from 1979 to 2008 and 2008 to 2017 in Ellenberg scores and on the competitor/stress-tolerator/ruderal scales (see text). Kruskal-Wallis tests for heterogeneity of medians, for each trio of boxplots, were all significant (p < 0.01) except for that relating to "light". All post hoc comparisons between 1978 and 2008 boxplots gave significant results, while none of the 2008-2017 comparisons did so (details in text) benefits of the management of HNV systems can be enhanced by the use of traditional livestock breeds.
Livestock biodiversity has clear intrinsic value as cultural and social assets well as economic value as a genetic resource, while its cultural value can also yield economic benefit in the form of local food and other specialities. It is enfolded into human culture, which Jorgensen (2015) emphasizes would be at risk in conservation models which seek to remove the human element from environments.
There are many areas in Europe where society is not ready to accept what is seen as full rewilding of postproductive and abandoned landscapes, but where "nature-and-culture-friendly" land uses, based on the husbandry of traditional livestock breeds and the securing of floral and faunal biodiversity, could be acceptable.

CO N FLI C T O F I NTE R E S T
None declared.

AUTH O R CO NTR I B UTI O N S
Both authors conceived the ideas. SJGH collated and analyzed the population data recorded by the Chillingham Wild Cattle Association, of which he is Vice Chairman. RGHB coordinated the vegetation studies. SJGH and RGHB wrote the manuscript. Both authors contributed critically to the drafts and gave final approval for publication.

DATA ACCE SS I B I LIT Y
Data are in the Dryad Digital Repository https://doi.org/10.5061/ dryad.2gm8348.