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Acta Theriologica 50 (2): 241–252, 2005. PL ISSN 0001–7051

Facilitative and competitive interactions between sympatric cattle, red deer and wild boar in Dutch woodland pastures A. T. KUITERS, Geert W. T. A. GROOT BRUINDERINK and Dennis R. LAMMERTSMA

Kuiters A. T., Groot Bruinderink G. W. T. A. and Lammertsma D. R. 2005. Facilitative and competitive interactions between sympatric cattle, red deer and wild boar in Dutch woodland pastures. Acta Theriologica 50: 241–252. Use of cattle-grazed and ungrazed woodland pastures by red deer Cervus elaphus Linnaeus, 1758 and wild boar Sus scrofa Linnaeus, 1758 was investigated monthly by measuring dung-deposition rates. Cattle Bos taurus grazed pastures year-round, with peak intensities during the growing season (May–September). Red deer and wild boar grazed pastures primarily during autumn and winter (October–April) when cattle occupancy was at a minimum. The lower occupancy of cattle in pastures from November to April was interpreted as the result of competition with red deer. Mean sward height in this period fell below 6.5 cm. In autumn and winter a negative relationship was found for red deer and wild boar occupancy with sward height, which indicated that red deer and wild boar preferred swards previously grazed by cattle. At the start of the growing season, when cattle occupancy in the pastures increased, red deer switched their habitat preference and almost totally disappeared from pastures to use alternative feeding grounds. Interpretation of the results lead to the conclusion that facilitative and competitive interactions occurred between sympatric cattle and red deer in woodland pastures, and to some extent also between cattle and wild boar. Alterra Green World Research, Wageningen University and Research Centre, P.O. Box 47, NL-6700 AA Wageningen, The Netherlands, email: [email protected] Key words: cattle, Cervus elaphus, competition, facilitation, Sus scrofa, woodland pastures

Introduction The diversity of closely related species in natural assemblages of herbivores has been explained by resource partitioning (Gordon and Illius 1989, Du Toit 1990, Murray and Illius 1996). Resource partitioning is defined as the differential use by animals of the available resources such as food or space (Schoener 1986). It has presumably evolved as a consequence of past competition and has been described extensively for African herbivore assemblages (Jarman and Sinclair 1979, Prins and Olff 1998, Voeten and Prins 1999, Arsenault and Owen-Smith 2002). Competition may arise where one species reduces shared food resources below that which can be exploited efficiently by another species (Illius and Gordon 1987). Small differences in sward height of the order of 1–2 cm, may lead to large [241]

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differences in bite volume, related to a difference in incisor breadth. Exclusion of the larger-sized ungulate species from short swards will be the result, as demonstrated both in modelling (Illius and Gordon 1987, Farnsworth et al. 2002) and field studies (Murray and Illius 2000). Alternatively, large herbivores may benefit smaller-sized grazers by facilitating access to food resources of a suitable height and quality (Bell 1970, McNaughton and Georgiadis 1986, Prins and Olff 1998). Grazing stimulates grass regrowth, thereby enhancing its nutritional quality (Gordon and Illius 1989, Van Soest 1994). Hence, co-existence of herbivores might be realised through differences in body size, leading to differential preferences for forage height and quality. Due to allometric relations of bite size and metabolic requirements to body size, small animals are able to subsist on shorter swards (Illius and Gordon 1987, 1992). When differences in body size are too small however, resource competition is expected to prevail over facilitative interactions (Prins and Olff 1998). When domestic stock is introduced into an area with indigenous wild herbivores, competition for available resources can occur during periods when forage is in limited supply, especially when the herbivore species have a more or less similar body size and feeding regime (Voeten and Prins 1999). Negative effects of cattle on indigenous herbivore species due to competition for food resources have frequently been reported (Kie et al. 1991, Fritz et al. 1996, Stewart et al. 2002, Jenks and Leslie 2003). There is however also evidence that cattle may improve forage quality for wild herbivores. Gordon (1989) and Gordon and Illius (1989) investigated the vegetation community use by red deer Cervus elaphus Linnaeus, 1758, cattle Bos taurus, goats Capra hircus and ponies Equus caballus on the Isle of Rum. The ungulates showed a high degree of resource overlap during summer when food was abundant. During winter when the availability of food resources was low, extensive resource partitioning was found between herbivore species. Red deer was found to feed preferentially on swards previously grazed by cattle (Gordon and Illius 1989). This was also observed in alpine pastures during summer (Mattiello et al. 2002). Sheep grazing was found to improve sward quality in autumn and winter for white-tailed deer and wapiti in Oregon (Rhodes and Sharrow 1990). Hobbs et al. (1996) investigated the implications of winter grazing by elk Cervus elaphus canadensis on cattle grazing during spring and early summer in sagebrush grasslands (Colorado). They found evidence that interactions between elk and cattle represented a composite of facilitative and competitive effects. When forage production was low and cattle density was high, competition was much stronger than facilitation. Facilitation is defined as a form of beneficial interaction between herbivores, whereby food material is made more available to one species by the activities of another (Sinclair and Norton-Griffiths 1982, Latham 1999). Facilitation has been observed in open grasslands, mostly in African savannah (Sinclair and Norton-Griffiths 1982), but also in temperate grasslands (Gordon 1989, Gordon and Illius 1988, 1989). Putman (1996) reported on a high degree of resource overlap between sympatric red deer, roe deer Capreolus capreolus, fallow deer Dama dama, sika deer Cervus nippon, ponies and

Ungulate interactions

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cattle in the New Forest (UK) over the summer period, when forage was abundant. During the winter period, when food was available in limited supply, resource partitioning was observed with different species exploiting relatively exclusive sets of resources. Competitive and facilitative interactions between ungulates in temperate ecosystems are frequently discussed (see Putman 1996 and Latham 1999 for reviews of literature) and included in modelling studies (Illius and Gordon 1987, Illius and Gordon 1992, Focardi et al. 1996, Farnsworth et al. 2002). Field studies quantifying resource partitioning and competitive or facilitative interactions in temperate grasslands are rare however, partly as a result of practical problems with manipulating herbivore densities. This paper describes the selection of cattle-grazed and ungrazed woodland pastures as feeding site by red deer and wild boar Sus scrofa Linnaeus, 1758 in Veluwezoom National Park, the Netherlands. The objective was to determine if either competitive or facilitative interactions between free-ranging cattle and both wild herbivore species prevailed, depending of season. Study area The study was carried out in Veluwezoom National Park (4900 ha; 52°30’N, 6°26’E). Mean annual precipitation is 790 mm and mean annual temperature amounts to 9.4°C, with a minimum of 2.5°C in January and a maximum in July of 16.4°C. Soil types are predominantly humus-podzols and brown-podzols, developed on a fluvioglacial Pleistocene loamy sand. The site supports a mosaic of coniferous stands, dominated by Scots pine Pinus sylvestris and mixed deciduous stands with oak Quercus robur, Q. petraea and beech Fagus sylvatica as most common tree species. One third is covered by dry to moist heathland Calluna vulgaris, Erica tetralix, with locally large surfaces of graminoid species like wavy hair-grass Deschampsia flexuosa and purple moor-grass Molinia caerulea. At different locations pastures occur, surrounded by forest stands. These originate from agricultural practices in the recent or further past. They are managed as game meadows and have a relatively productive grass sward. Vegetation is dominated by common couch Elytrigia repens, broom Bromus hordeaceus, meadowgrass Poa trivialis and P. annua and white clover Trifolium repens. Some pastures are occasionally mowed or ploughed and re-seeded. In 1982 a small group of free-ranging Scottish Highland cattle Bos taurus was introduced in the Veluwe National Park and added to the extant assemblage of wild herbivore species of red deer, roe deer and wild boar. Free-ranging cattle were used to maintain a half-open landscape (Van Wieren 1995, Kuiters et al. 1996). Initially, the cattle-grazed part of the National Park encompassed 170 hectares, but over the years has been extended to a total of 3800 ha in 2000. Concurrently the 2 number of animals increased from 17 to 200. Mean red deer density amounted to 2–3 head per km , 2 whilst wild boar density was estimated at ca 2 head per km . Although wild boar is an omnivore species, in the study area they fed predominantly on plant material. Especially in mast-poor years they were largely dependent of grasses along foot tracks and pastures (Groot Bruinderink et al. 1997).

Material and methods Field study Six pastures were chosen as monitoring sites for occupancy by herbivores. All pastures were surrounded by forest stands. Three pastures were accessible to cattle, three others were situated in

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Table 1. Main characteristics of the pastures used in this study. Pastures

Code

Area (ha)

Steinhul Total Groenendaal

SH1 TT2 GD5

5 3 30

Cattlegrazing

Mowing/ Number of Length ploughing transects transects (m)

Ungrazed – – –

+ + –

4 4 8

61 56 150

– – –

4 4 8

95 77 150

Cattle-grazed VIP Noordhoek Groenendaal

VP3 NH4 GD6

3 2 30

+ + +

parts of the study site where cattle had no access or were fenced (Table 1). A fence, composed of five iron wires between 0.4 and 1.5 m, enclosed the cattle-grazed pastures. Red deer and wild boar could easily pass these fences as was confirmed by visual observations. Four pastures (SH1, TT2, VP3, NH4) had been used as game meadow for many years already. Two other pastures (GD5, GD6) were situated on a recently abandoned field (‘Groenendaal’), which was split into two equally-sized parts. This field had been fenced to exclude cattle, whereas deer and wild boar had free access. In May 1998, one month before the start of the monitoring, the fence of pasture GD6 was removed to allow cattle. In each pasture, four to eight transects were positioned and marked with wooden pickets. Dimensions were 40–150 m length and 2 m width. Sward height was recorded monthly along each transect, by measuring vegetation height every 10 m applying the drop disc-method using a circular polystyrene disc (Stewart et al. 2001) and averaging measurements along each transect. Occupancy by herbivores was estimated monthly from counts of faecal pellet groups containing more than 5 pellets (red deer, wild boar) and from counts of dung pats (cattle), using the plot-clearance method (Neff 1968, Rowland et al. 1984). After counting the number of pellet-groups deposited on each transect, all dung was trodden on to prevent double counting on subsequent visits. Observations were conducted from June 1998 to August 1999. Mean pellet-group or dung deposition rate was calculated, taking into account the surface sampled within each transect and the number of days between sampling dates. It was expressed as pellet groups or dung pats per ha per month (31 days). We had no information to what extent pellet- or dung-deposition rate differed between seasons as a function of seasonal variation in food intake and diet quality, and we assumed a constant rate of faecal output throughout the year. Data analyses Sward height data were log-transformed and data of pellet deposition rate were square root-transformed to reach homogeneity of variances. Differences in sward height and in occupancy of wild herbivores between cattle-grazed and ungrazed pastures were tested using a nested analysis of variance, with cattle and date as fixed model terms and pasture, and transects within pasture as random terms (GenStat package for Windows, version 6.1). Correlation between occupancy by different herbivore species were analysed using a Spearman rank correlation test. Relations between occupancy by herbivores and sward height were analysed by standard regression modelling, applying a log-log linear relationship (Sokal and Rohlf 1995). Relationships were expressed with the following regression equation: log (Öy) = a – b · (log x) where y is the occupancy of herbivore species i, measured as pellet group or dung pat deposition rate, and x is sward height in cm.


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Results Herbivores occupancy in the pastures

Mean pellet group deposition rates of the herbivore are presented in Table 2. Highest deposition rates were found for cattle and lowest for wild boar. Variation among pastures within the same group, ungrazed or cattle-grazed, was rather high. Herbivores occupancy in the pastures showed a clear seasonal pattern (Fig. 1). Dung deposition rate for cattle was significantly different among months (Nested ANOVA: F = 3.33, df = 13,143, p < 0.001). Highest pellet deposition rates were found during the growing season (May–October) and lowest during the autumn and winter period (November–April; Fig. 1). Occupancy by red deer in the pastures showed an opposite pattern compared to cattle (Fig. 1). Relatively high pellet deposition rates were found during autumn and winter (October–April), whereas it was very low during the summer months (May–August). The differences among seasons were significantly different (F = 15.19, df = 13, 286, p < 0.001). The opposite pattern in cattle and red deer’s occupancy was striking. This was reflected by a negative correlation between cattle and red deer occupancy (Spearman correlation: rS = –0.54, t = –0.21, df = 12, p = 0.047; Fig. 2). Although the mean level of red deer pellet deposition rate on cattle-grazed and ungrazed pastures was not significantly different over the year (F = 0.03, df = 1,4, p = 0.873), it peaked a few months earlier in the cattle-grazed pastures. This was reflected by a significant interaction term ‘cattle-grazing x season’ (F = 2.54, df = 13,286, p = 0.003). Apparently, when red deer entered the pastures in autumn, they preferred the pastures previously grazed by cattle and used the ungrazed pastures especially during the later winter period. Pellet group deposition rates by wild boar were significantly higher in cattle-grazed pastures (F = 23.30, df = 1,4, p = 0.008; Fig. 1), although the mean level was relatively low year-round. In the cattle-grazed pastures there was no Table 2. Monthly mean level (± SD) of dung-pat and pellet-group deposition rates in the ungrazed and cattle-grazed pastures from June 1998 to August 1999. Pastures

Cattle

Red deer

Wild boar

Ungrazed SH1 TT2 GD5 Mean

171 ± 193 120 ± 173 24 ± 18 105 ± 121

14 ± 20 8 ± 17 6 ± 11 9 ± 13

Cattle-grazed VP3 NH4 GD6

685 ± 344 279 ± 108 202 ± 134

220 ± 282 38 ± 36 62 ± 61

60 ± 175 32 ± 49 32 ± 30

Mean

388 ± 141

107 ± 119

42 ± 66

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Dung deposition rate (pats/ha/month)

1000

Cattle

800 600 400 200

Red deer

600

cattle-grazed ungrazed

400 200 0

Wild boar

400


2 Aug 1999

30 Aug 1999

28 Jun 1999

31 May 1999

28 Apr 1999

6 Apr 1999

1 Mar 1999

21 Jan 1999

30 Oct 1998

6 Oct 1998

31 Aug 1998

30 Jul 1998

0

30 Nov 1998

200

29 Jun 1998

Pellet deposition rate (groups/ha/month)

0

Fig. 1. Seasonal variation in dung-deposition rate (number of pats or faecal pellet groups per ha per month) of cattle, red deer and wild boar on the cattle-grazed and ungrazed pastures (means with 95% confidence limits).

significant correlation between occupancy by cattle and wild boar (rS = –0.31, t = –1.13, df =12, p = 0.281). Neither was there a significant correlation with occupancy by wild boar and red deer (rS = 0.20, t = 0.69, df =12, p = 0.503). Relationship between herbivores occupancy and sward height

Sward height significantly differed between the cattle-grazed and ungrazed pastures (F = 8.71, df = 1,4, p < 0.05; Fig. 3). Mean difference in sward height between cattle-grazed and ungrazed pastures amounted to 8 cm, with the highest difference found at the end of June (12–22 cm) and lowest begin in March (2 cm).

Pasture occupancy by red deer (pellet number/ha/month)


Fig. 2. Correlation between red deer and cattle occupancy in the pastures over the whole observation period. Occupancy data are presented as the square root-transformed values of dung-pat and pellet-group deposition rates.

247

20

15 r S = -0.54 p = 0.047

10

5

0 10

15

20

30

Pasture occupancy by cattle (dung pat number/ha/month)

45


40

Sward height (cm)

25

35 30 25 20 15 10 5 30 Aug 1999

2 Aug 1999

28 Jun 1999

31 May 1999

28 Apr 1999

6 Apr 1999

1 Mar 1999

21 Jan 1999

30 Nov 1998

30 Oct 1998

6 Oct 1998

31 Aug 1998

30 Jul 1998

29 Jun 1998

3 Jun 1998

0

Fig. 3. Seasonal variation in sward height of the cattle-grazed and ungrazed pastures (means with 95% confidence limits).

Table 3. Mean sward height in cm (± SD) of the ungrazed and cattle-grazed pastures from June 1998 to August 1999. Ungrazed pastures

Sward height

Cattle-grazed pastures

Sward height

SH1 TT2 GD5

13.4 ± 9.94 13.5 ± 9.19 22.2 ± 8.54

VP3 NH4 GD6

4.5 ± 1.69 6.0 ± 1.96 14.8 ± 8.44

Mean

16.4 ± 8.14

Mean

8.5 ± 3.67


Cattle dung pat deposition rate log (number/ha/month)

248

10000

1000

100

10 1

10

100

log Sward height (cm) Fig. 4. Relationship between cattle dung deposition rate and sward height of the pastures over the whole monitoring period. The fitted model was: 10log [√(dung deposition rate)] = 2.944 – 0.595 (10log [sward height]).

Sward height of the recently abandoned GD5- and GD6-pastures was higher compared to the other pastures (Table 3). We fitted a linear function using Pasture occupancy by cattle showed a negative relationship with sward height. 2 log-transformed data, although the scatter around the fitted line was large (R = 0.193, df = 42, p < 0.01; Fig. 4). Minimum values for cattle occupancy during autumn and winter (November 1998 – April 1999) coincided with a mean sward height below 6.5 cm.

Pellet group deposition rate log (number/ha/month)

10000 red deer wild boar 1000

100

10

1

1

10

100

log Sward height (cm) Fig. 5. Relationship between red deer and wild boar pellet-group deposition rate in the pastures and sward height over the winter period (October 1998 to April 1999). The fitted models were: red deer: log [pellet-group deposition rate] = 3.645 – 1.800 (log [sward height]); wild boar: log [pellet-group deposition rate] = 2.258 – 1.075 (log [sward height]).


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Red deer used the pastures mainly during autumn and winter (October 1998 – April 1999), and used preferentially the shortest swards, reflected by a significantly negative relationship between pellet-group deposition rate and sward height (R2 = 0.754, df = 28, p < 0.001; Fig. 5). A similar, although slightly weaker, 2 negative relationship was found for wild boar occupancy and sward height (R = 0.324, df =18, p < 0.001). Discussion The observed seasonal patterns in dung and faecal pellet group densities were interpreted as differences in occupancy of the ungulates, although there may be some inaccuracy in this assumption. There are indications that defecation rate of ungulates varies with season (Mitchell and McCowan 1984). However, seasonal variation in defecation rates for ungulates in our temperate zone is assumed to be less than 15% (Mitchell et al. 1985), with lower faecal output during winter. Observations of dung deposition rates revealed that the woodland pastures in the study area were grazed by all ungulate species with seasonally dependent intensities. Whereas cattle used the pastures year-round, with maximum intensities during the growing season (May–September), red deer and wild boar occupancy was highest during autumn–winter (October–April). It suggests that resource partitioning occurred to some extent between the ungulate species. This was supported by diet analyses carried out earlier in this area (Groot Bruinderink and Hazebroek 1995, Groot Bruinderink et al. 1997). Cattle diet in summer was composed for ca 60% of graminoids. In autumn and winter this decreased to less than 40%, with other food resources being more important, such as browse of shrubs and deciduous trees. Red deer diet was composed for 45% of graminoids, with lowest levels during summer (20%). Spring and summer diet of red deer was largely composed of young twigs of bilberry Vaccinium myrtillus, heather Calluna vulgaris and of shrub and deciduous trees, like rowan Sorbus aucuparia, pedunculate and sessile oak. In autumn and winter graminoids in red deer diet raised to ca 50%. Also winter diet of wild boar contained a large proportion of grass (40–60%), especially during winters when mast-availability was low (Groot Bruinderink et al. 1997). The decrease in occupancy by cattle in the pastures started in November and lasted until the end of April. Although some hay was provided for the cattle for several weeks in late winter (February-mid April) when food supply was at a minimum, this could not explain the decrease in cattle occupancy in the pastures starting in November. Dung deposition rate decreased by 50% from October to November and this is too much to be only the result of a seasonal reduction in faecal output. Therefore, it is more likely that competition occurred to some extent between cattle and red deer. The decrease in occupancy by cattle coincided with a decrease in mean sward height below 6.5 cm. Both herbivore species partly select for differential heights of grass swards. Red deer are able to graze down grass swards to a height below that which can be tolerated by cattle (Gordon and Illius

250


1988, Gordon 1989). Cattle, foraging with a sweep of the tongue, have a less deep bite horizon than red deer that can bite swards to a height of 2 cm. Illius and Gordon (1987) developed a model based on the allometry of metabolic requirements and bite size, which shows that smaller-sized herbivores are able to subsist on shorter swards than larger-sized animals. It explains why red deer and wild boar were able to exploit the grassland sward of woodland pastures during autumn and winter, whereas cattle foraged to a large extent on other vegetation types during this period. That the larger-sized herbivore species had to move first as a consequence of sward height reduction, once the vegetation has stopped growing, was also observed for cattle on the Isle of Rum (Illius and Gordon 1987). Probably available forage biomass at the pastures became too low to meet the intake requirements. It is likely that competitive displacement by red deer occurred. Sward height and herbage mass are cues in the allocation of residence time of cattle (Wallis de Vries and Daleboudt 1994, Distel et al. 1995). Competitive displacement has also been found for other ungulate assemblages, like for topi Damaliscus lunatus and wildebeest Connochaetes murinus in East African savannah (Murray and Illius 2000). Models on optimal foraging predict that a herbivore uses a foraging site only if the biomass exceeds a certain threshold level. It does not consume all available food, but moves away when food density reaches the threshold level (Focardi et al. 1996). Red deer occupancy in the pastures was low during the growing season. It sharply declined at the end of April, both in the cattle-grazed and ungrazed pastures (Fig. 1). Apparently, red deer switched to food resources of higher quality or abundance that become available in early spring (Groot Bruinderink and Hazebroek 1995). Red deer foraging habits are highly variable amongst seasons (Gebert and Verheyden-Tixier 2001). Results also indicated that cattle-grazing facilitated red deer and wild boar foraging at the pastures. Although faecal pellet groups of wild boar were found in relatively low densities, its occupancy during autumn and winter (October–April) was significantly higher on the cattle-grazed pastures. The significant negative relationship between autumn and winter occupancy of red deer and wild boar with sward height (Fig. 5) suggests this was related to a better sward quality of the cattle-grazed pastures. Moreover, the peak in red deer occupancy was at the cattle-grazed pastures a few months earlier compared to the ungrazed pastures. Apparently, red deer and wild boar preferred grass swards that were previously grazed by cattle. Grazing stimulates grass regrowth, thereby enhancing the nutritional quality. Digestible energy content and crude protein content of grasses have been reported to be negatively correlated with sward height (Mattson 1980, Van Soest 1994). Results indicated that grazing of free-ranging cattle had a positive impact on autumn and winter forage quality, thereby facilitating both red deer and wild boar. It suggests that introduction of cattle might have been beneficial for both wild ungulate species. This is confirming the outcome of multi-species models (Farnsworth et al. 2002).


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Acknowledgements: We thank the people employed by Vereniging Natuurmonumenten and a number of volunteers who assisted in the field work. Bert van der Werf is acknowledged for statistical advices and Liesbeth van der Sluijs for her support in improving the English text. We received grants from the Ministry of Agriculture, Nature and Food Quality and from Vereniging Natuurmonumenten.

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