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The effects of harvest on arable wood mice Apodemus sylvaticus
Biological Conservation 1993, 65, 279-283
THE EFFECTS OF HARVEST ON ARABLE WOOD MICE
Apodemus sylvaticus T. E. T e w * & D. W. M a c d o n a l d Wildlife Conservation Research Unit, Department of Zoology, Oxford University, South Parks Road, Oxford OXI 3PS, UK. (Received 5 May 1992; revised version received 16 July 1992; accepted 1 August 1992) agriculture (e.g. 'conservation headlands', input quotas), which aim to integrate agriculture and conservation, and hence increase species biodiversity or animal abundance (see Macdonald & Smith, 1991, for review). However, there may be little benefit in increasing a species' abundance throughout the summer months if it is later destroyed by the autumnal harvest. The effect of harvest upon arable wildlife is an important consideration in its management, but one that has largely been neglected. This paper quantifies the effects of modern harvesting techniques on arable-dwelling wood mice, testing the null hypothesis that the behaviour and survival of individuals are unaffected by harvest, and quantifying the effects of harvest at the population level. We also discuss the implications of the results for the management of this species and its predators on arable farmland.
Abstract
The effects of cereal harvesting on the ecology of wood mice Apodemus sylvaticus were investigated at three arable study sites in Oxfordshire from 1987 to 1991 using both radio-tracking and live-trapping methodologies. The process of harvesting itself had little direct effect on the mice, but the removal of the cover afforded by the crop greatly increased predation pressure on the mice. After harvest, mice either emigrated from the arable ecosystem or reduced activity. Nevertheless, over half (17 of 32) of the mice radio-collared before harvest were taken by predators in the first week following harvest. Together with emigration, this produced an 80% decrease in the population. Post-harvest activities such as stubble burning subsequently further increased mortality. The dramatic increase in prey availability may benefit predators of small mammals in the cereal ecosystem such as tawny owls Strix aluco and weasels Mustela nivalis.
METHODS
Keywords." Apodemus sylvatics, cereal harvesting, agriculture, predators, small mammals.
Two types of data were collected from arable wood mice populations at three study sites, all of which were within 5 km of Oxford, UK and sown with winter wheat or winter barley. Live-trapping data were collected at monthly intervals between November 1990 and December 1991 from one of the study sites where the arable fields bordered woodland. Radio-tracking data were collected over the course of four years between 1987 and 1991. Mice were trapped using aluminium Longworth livetraps. Animals were weighed, sexed and individually marked with numbered Michel clip (Rocket Ltd, London, UK) eartags before being released at site of capture. The trapping grid consisted of one trap at each point, with 24 m spacing between points; an area of 10 ha was covered using 180 traps. Traps were set for four consecutive nights each calendar month and were checked at 0000, 0800 and 1600 h GMT. Wood mice were the only species frequently caught; other species which were caught occasionally, such as bank voles Clethrionomys glareolus and common shrews Sorex araneus, were released without marking at site of capture. The radio-tags (SS1 transmitters: Biotrack, Wareham, U.K.) weighed 2 g and were fitted only to adult mice weighing > 20 g (Wolton & Trowbridge 1985; Pouliquen et al., 1990). Radio-collars were secured with nylon cable ties and fitted whilst the animal was under light anaesthesia using methoxyfluorane. The tagged animal was then retained for 5-10 min to recover full
INTRODUCTION The intensively farmed arable ecosystem covers nearly 70% of Europe and represents an important habitat for many species. The wood mouse Apodemus sylvaticus, a generalist small mammal with catholic dietary (Pelz 1989) and habitat (Wolton & Flowerdew, 1985) requirements, has been particularly successful at exploiting farmland and occurs in that habitat throughout the year (Green, 1979; Tew, 1989; Loman, 1991). However, arable farmland is neither a natural nor an undisturbed habitat and all wildlife inhabiting this ecosystem inevitably faces periods of disruption. The most marked, and traumatic, of these periods is harvest, when the crop is removed from the fields and the ground prepared for sowing. With recent political initiatives encouraging reduced cereal production and increasing environmental awareness, several schemes have been proposed, either taking land out of production (e.g. 'set-aside') or extensifying * To whom correspondence should be addressed at: Joint Nature Conservation Committee, Monkstone House, City Road, Peterborough PE1 1JY, UK. Biological Conservation 0006-3207/93/$06.00 © 1993 Elsevier Science Publishers Ltd, England. Printed in Great Britain 279
T. E. Tew, D. W. MacdonaM
280
locomotor activity and released at site of capture. Wherever possible, radio-collared mice were recaptured after a period of three weeks' radio-tracking and the collars removed. The instrumented mice could generally be located from 50 m, using a Mariner receiver (Model M57: Mariner Radar, Lowestoft, UK) and hand-held threeelement Yagi aerial. Mice were radio-tracked intensively on foot throughout the night with radio-fixes taken every 10 min from first to last activity. In addition, nest-sites were checked daily to confirm residency and animal survival. Away from the nest, radio-fixes were taken to an accuracy of + 2-5 m, facilitated by the fact that the mice quickly habituated to the tracker's presence (Tew, 1989) and could be approached to within 10 m. A 50 m grid was marked out across the study sites by fibre-glass canes marked with coloured reflective tape. If the radio-signal disappeared, an immediate and extensive search of the surrounding area largely eliminated emigration from the study site as a possible cause. Although emigration could never be definitively eliminated as a cause of disappearance it is unlikely that many mice evaded these large-scale searches. Often, direct field observation allowed the cause of the loss to be identified-normally predation was either seen or predators were observed close to the area where the mouse was last seen. Alternatively, mouse collars were found lodged in trees, beneath owl perches or within weasel nests. Data were entered onto an Apple Macintosh system and analysed using the ' W I L D T R A K ' software package (Todd, 1992). Statistical analyses follow Sokal and Rohlf (1981) and unless otherwise stated significance is assumed when p < 0.05. RESULTS Live-trapping
Monthly estimates of population size, recruitment and survival rates, calculated using Jolly-Seber capture-mark--recapture analyses, are shown in Figs 1 and 2. Actual numbers of animals captured ranged from six in March 1991 to 133 in July 1991. Harvest occurred shortly after the August trapping session. 30 09
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Jun Jul 1991
Aug
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Fig. 1. Monthly population size (O) and recruitment (0), cap culated by Jolly-Seber capture-mark-recapture analyses. Time of harvest is indicated by the solid vertical line.
1.2
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0.8" .=
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Fig. 2. Monthly survival rates, calculated using Jolly-Seber captur~mark recapture analysis (C)) and indices of radiocollar survival (Q). Time of harvest is indicated by the solid vertical line. Radio-tracking
--
survival
It is problematical to ascribe radio-tag failure definitively to predation since collars may be shed, or may stop due to battery failure, without the animal being killed. Radio-collars were occasionally shed by the animals, usually in the nest, and, in these instances the transmitters were often chewed by their previous owners and ceased to function. Usually, this sequence of events occurred within 3 days of collar attachment. The electronic (i.e. battery) lifespan of the radiotransmitters was determined by daily monitoring of the signal from a sample of transmitters that had been removed from animals and were kept in the laboratory. Although laboratory conditions are more constant than those in the field, this does give an indication of battery lifespan. The mean lifespan of the collars was 37.8 days and was very consistent (SD = 18, n = 23, range 35~41); the probability of a battery failing before 30 days was less than 0.001. For further analyses, therefore, any collar which failed after five days but within 30 days of its attachment was deemed to be due to causes that arose from neither faulty attachment nor battery failure, i.e. predation of the animal causing signal cessation or emigration of the animal from the study site. Indices of collar survival from 73 mice, radio-collared between February and November 1991, are shown in Fig. 2, alongside the estimates of population survival derived from live-trapping data. The indices are calculated as the proportion of radio-collared mice known to have survived for more than one month following collar attachment. The data describing the known fate of 33 mice radiotracked over the harvest period are summarised in Table 1. Radio-tracking
-- movements
The radio-tracking data were also analysed for differences in movements between the periods before and after harvest. Movement parameters were only calculated from data sets that spanned a complete night,
281
Effects o f harvest on wood mice Table 1. The fate of 33 radio-collared mice at harvest
Study site & year
Wytham 1987 Sescut, 1988 St Frides, 1990 Wytham, 1991 Totals
Sample size
Killed by combine harvester
Survived combine harvester
7 11 4 11
1
6
3
3
1
1
0 0 0
11 4 11
7 2 5
4 2 6
1 ---
2 --
33
1
32
17
15
2
3
from first to last activity. As many of the mice died soon after harvest there were fewer data from after harvest, which led to an unbalanced data set. To counter this, analyses were conducted only on equal numbers of nights from both before and after harvest. Twelve mice were radio-tracked both before and after harvest and there were significant decreases in the distance moved each night, the mean rate of movement and the percentage of time spent moving (Wilcoxon signed-rank test, Ho no difference in movements before and after harvest - - Table 2). Home-range size estimation is sensitive to the number of fixes taken and for this species three complete nights of radio-locations taken at 10min intervals are required for accurate estimates (Tew, 1989). Consequently, home-range size was only calculated for those animals where there were three or more nights' data from both before and after harvest. Homerange sizes were calculated using the restricted polygon technique (Wolton, 1985), which gives smaller, and more accurate, estimates of home-range size for this species than the minimum convex polygon method (Tew, 1989). There was no significant difference between home-range sizes before and after harvest (Wilcoxon signed-rank test, Ho: no difference in homerange sizes before and after harvest - - Table 2), although this may have been due to small sample sizes. Only six of the twelve mice satisfied the criteria for analysis, but five of these showed a decrease in homerange size. Following harvest, eight mice were radio-tracked during straw baling and none was killed in the process. Of five animals tracked during stubble burning in 1987 and 1988 two (40%) were killed, both of which had burrows directly below the lines of straw left by the Table 2. Home-range and movement parameter date from both before and after harvest and the results of a Wilcoxon signedrank test examining differences between the two
Movement parameter Pre-harvest Post-harvest (mean + s.d) (mean+ s.d)
n, Z, p
Total nightly distance 927 _+433 568 + 274 12, -2.75, 0.006 moved (m) Mean rate 1.71 +0.68 1.12+0.54 12, 2.63,0.009 movement(m rain I) Percentage of time 82.67 + 6.58 71.58+ 13-77 12, -2.63, 0.008 spent moving Home-range size (ha) 076 + 0.89 0.49+ 0.52 6, 1.41, 0.16
Disappeared within 1 week of harvest
Survived > 1 week after harvest
Killed by stubble burning
Survived Stubble burning
combine. Post-mortem examination suggested that these mice were asphyxiated, rather than burnt, by the stubble fire. DISCUSSION There have been few studies of small mammals in the arable habitat (Kikkawa, 1964; Bergstedt, 1966; Pollard & Relton, 1970; Eldridge, 1971; Green, 1979, Loman, 1991) and none of these have specifically addressed the effects of harvest, although Loman (1991) noted that farming activity in autumn may have had detrimental effects on the wood mouse population, attributing these effects to the reduction in food availability and destruction of burrow entrances. Recent work has also investigated the traumatic effects of pesticide application on arable small mammal populations (Tarrant et al., 1990; Johnson et al., 1991; Tew, 1992). Arable populations of wood mice may be split into two types. Those close to woodland are joined by immigrating conspecifics in the spring (e.g. Kikkawa, 1964; Bergstedt, 1966; Corke, 1974) whereas those far from woodland are not (e.g. Pollard & Relton, 1970; Green, 1979). This study site falls into the former category: between February and May, as the growing crop in the fields started to provide cover, there was a steady immigration of adults into the population from arable hedgerows and the neighbouring woodland (Fig. 1). These immigrants join the overwintered residents to set up the summer breeding system of female defence polygyny (Tew, 1989) and form the breeding population. Young of the year started to enter the population in May, and there was a burst of juvenile recruits in June, July and August. These were joined in July and August by a large influx of (newly) adult animals, probably the first cohort of animals born in the wood which were then emigrating from that habitat. Harvest of the cereal crop occurred between the August and September trapping sessions. Fig. 1 illustrates the dramatic crashes, in both recruitment and population density, immediately following harvest. Because emigration can not be definitively excluded as a causal process, hereafter we shall refer to the 'persistence' of the arable population rather than its 'survival'. Although the estimation of persistence distributions for radio-tagged animals has recently been the subject of some elegant analyses (Pollock et al., 1989, White &
282
T. E. Tew, D. W. MacdonaM
Garrott, 1990), allowing for both the staggered entry of radio-tagged animals and transmitter failure or emigration, they assume that the censoring mechanism is random. In this study, where predators stop the radio-signal whilst killing the animal, such assumptions are unjustified. Furthermore, the precision of such analyses is poor unless the number of animals tagged at any one time is greater than 20. In this study, the number of tagged animals rarely exceeded 10 at any one time and so simpler survival analyses were employed. Nevertheless, the indices calculated for collar survival accurately reflected the overall persistence of the population (Fig. 2), indicating both that the estimates were accurate and that the radio-tagged animals were a representative sample of the population. Figure 2 illustrates the dramatic decrease in persistence of the wood mouse population after harvest. The crash in arable population levels at harvest is due to two effects. First, animals may emigrate from the harvested fields. Live-trapping in the neighbouring wood two weeks after harvest captured 13 mice that were previously resident in the arable fields (none of these were radio-collared animals, supporting the view that our methods of detecting emigration amongst the radio-collared sample were adequate). Secondly, many of the mice in the arable fields are taken by predators immediately following harvest. The mechanical actions of harvest have little direct effect upon the mice and only 1 out of 33 (3%) was killed by the combine harvester (Table 1). However, 17 of 32 (53%) of the radio-collared mice disappeared within one week of harvest and, in nine of these 17 instances, predation by either weasels Mustela nivalis or tawny owls Strix aluco was either directly observed or inferred. In the latter cases, the circumstantial evidence, consisting of chewed collars in weasel nests or bloodied collars lodged in trees, was conclusive. In addition, direct field observation of predators suggests that they react to the changes in the arable habitat at harvest. In particular, tawny owls changed their hunting behaviour at harvest. Prior to harvest, they rarely hunt farmland. When they do, they concentrate particularly on the grassy banks bordering hedgerows since the crop prevents them from stooping on prey. Immediately following harvest, however, the owls fly low over the fields and stoop onto prey both in the stubble and directly into the straw lines left by the combine (Tew unpublished data). In response to the change in their habitat the mice are less active above ground, moving slower, less frequently and travelling shorter distances. There was a decrease in home-range size after harvest, although this was not significant, probably due to the small sample sizes. It seems likely that this reduction in activity is in direct response to the increase in predation pressure caused both by their increased vulnerability to predation and the increase in predator activity. Several weeks after harvest the straw is baled and the stubble is either ploughed into the soil or burned. Baling had no effect on the mice but stubble burning killed 40% of the remainder, although sample sizes were small.
Both mice that were killed by stubble burning had burrows directly below the straw lines, where the stubble fire burnt most fiercely. All three survivors had burrows between the straw lines. Post-mortem examination suggested that the mice had been asphyxiated by the stubble fire, and it is likely that as the fire passed overhead it drew the air out of the burrow system. Since the burrows of arable wood mice tend to be simple, with a single entrance, there is no opportunity for escape. In woodland habitats, wood mice populations show a characteristic decrease over the winter and spring as adult animals fulfill their life expectancy and die off (Flowerdew, 1985). Whilst the mortality of the arable wood mouse population at harvest is dramatic, many of the animals killed at this time of year are nearing their natural life expectancy, and it may be that the predation corresponds to a 'doomed surplus' (Errington, 1963). It is unlikely that a specialist small mammal predator such as the weasel can regulate wood mouse numbers, although more facultative predators such as the tawny owl may do so (Erlinge et al., 1983). In any case, harvesting of the cereal presents a great increase in food availability for the predators of the arable ecosystem, and its timing may be beneficial to summer-born predators dispersing from their natal ranges. Such juveniles are often considered to be the age class under most stress. In summary, the harvest of the cereal crop has little direct effect on the resident wood mice but the removal of cover greatly increases the predation pressure upon them. The mice react by either leaving the habitat altogether, emigrating into neighbouring woodland, or by decreasing foraging activity. Nevertheless, approximately half the population falls to predators immediately following harvest. The baling of the straw and ploughing has no effect upon the mice, although stubble burning further increases post-harvest mortality. Despite high mortality, there appear to be sufficient remaining animals to overwinter in the agricultural habitat and sustain the following year's mouse population. ACKNOWLEDGEMENTS We thank S. J. Adams, E. D. Brown, J. Rae, I. A. Todd and numerous field assistants for their technical support. The original version of this paper was much improved by the comments of Dr. R. E. Kenward and an anonymous referee, to whom we are very grateful. The work was supported by the Joint Agricultural and Environmental Programme (JAEP/NERC) and The Environmental Research Fund (TERF). REFERENCES Bergstedt, B. (1966). Home ranges and movementsof the rodent species Clethrionomys glareolus (Schreber), Apodemus flavicollis (Melchior) and Apodemus sylvaticus (Linn~) in southem Sweden. Oikos, 17, ! 50-7. Corke, D. (1974). The comparative ecology of the two British species of the genus Apodemus (Rodentia, Muridae). Unpublished PhD thesis, University of London.
Effects of harvest on wood mice Eldridge, M. J. (1971). Some observations on the dispersion of small mammals in hedgerows. J. of Zool., Lond., 165, 530-4. Erlinge, S. et al. (1983). Predation as a regulating factor on small rodent populations in southern Sweden. Oikos, 40, 36-52. Errington, P. L. (1963). Muskrat populations. Iowa State University Press, Ames. Flowerdew, J. R. (1985). The population dynamics of wood mice and yellow-necked mice. Symp. of ZooL Soc. of Lond., 55, 315-38). Green, R. (1979). The ecology of wood mice Apodemus sylvaticus on arable farmland. J. Zool., Lond., 188, 357-77. Johnson, I. P., Flowerdew, J. R. & Hare, R. (1991). Effects of broadcasting and of drilling methiocarb molluscicide pellets on field populations of wood mice, Apodemus sylvaticus. Bull. of Environ. Contam. & ToxicoL, 46, 84-91. Kikkawa, J. (1964). Movement, activity and distribution of the small rodents Clethrionomys glareolus and Apodemus sylvaticus in woodland. J. Anim. Ecol., 33, 259-99. Loman, J. (1991). The small mammal fauna in an agricultural landscape in southern Sweden, with special reference to the wood mouse Apodemus sylvaticus. Mammalia., 55, 91-6. Macdonald, D. W. & Smith, H. N. (1991). New perspectives on agro-ecology: between theory and practice in the agricultural ecosystem. In The ecology of temperate cereal fields, ed. L. G. Firbank, N. Carter, J. F. Darbyshire, & G. R. Potts. Blackwell Scientific Publications, Oxford, pp. 413-48. Pelz, H-J. (1989). Ecological aspects of damage to sugar beet seeds by Apodemus sylvaticus. In Mammals as pests, ed. R. J. Putman. Chapman & Hall, London, pp.34-48. Pollard, E. & Relton, J. (1970). Hedges, V. A study of small mammals in hedges and cultivated fields. J. of Appl. Ecol., 7, 549-57.
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Pollock, K. H. Winterstein, S. R., Bunck, C. M. & Curtis, P. D. (1989). Survival analysis in telemetry studies: the staggered entry design. J. Wild. Manage., 53, 7-15. Pouliquen, O., Leishman, M. & Redhead, T. D. (1990). Effects of radio-collars on wild mice, Mus domesticus. Can. J. Zoology., 68, 1607-9. Sokal, R. R. & Rohlf, F. J. (1981). Biometry, 2nd edn W. H. Freeman, New York. Tarrant, K. A., Johnson, I. P., Flowerdew, J. R. & GreigSmith, P. W. (1990). Effects of pesticide applications on small mammals in arable fields, and the recovery of their populations. In Proceedings of the 1990 Brighton Crop Protection Conference -- Pests & Diseases, pp. 173-82. Tew, T. E. (1989). The behaviourial ecology of the wood mouse in the cereal field ecosystem. DPhil thesis, University of Oxford. Tew, T. E., Macdonald, D. W. & Rands, M. R. W. (1992). Herbicide application affects microhabitat use by arable wood mice Apodemus sylvaticus. J. of Appl. Ecol., 29, 352-9. Todd, I. A. (1992). WildTrak - - Home-range analyses for the Macintosh system. Department of Zoology, University of Oxford, 89 pp. White, G. C. & Garrott, R. A. (1990). Analysis of wildlife radio-tracking data. Academic Press, California. Wolton, R. J. (1985). The ranging and nesting behaviour of wood mice, Apodemus sylvaticus (Rodentia; Muridae), as revealed by radio-tracking. J. of Zool., London., 2116, 203-22). Wolton, R. J. & Flowerdew, J. R. (1985). Spatial distribution and movements of wood mice, yellow-necked mice and bank voles. Symp. of Zool. Soc. Lond., 55, 249-75. Wolton, R. J. & Trowbridge, B. J. (1985). The effects of radio-collars on wood mice, Apodemus sylvaticus. J. of Zool., London., 206, 222-4.
THE EFFECTS OF HARVEST ON ARABLE WOOD MICE
Apodemus sylvaticus T. E. T e w * & D. W. M a c d o n a l d Wildlife Conservation Research Unit, Department of Zoology, Oxford University, South Parks Road, Oxford OXI 3PS, UK. (Received 5 May 1992; revised version received 16 July 1992; accepted 1 August 1992) agriculture (e.g. 'conservation headlands', input quotas), which aim to integrate agriculture and conservation, and hence increase species biodiversity or animal abundance (see Macdonald & Smith, 1991, for review). However, there may be little benefit in increasing a species' abundance throughout the summer months if it is later destroyed by the autumnal harvest. The effect of harvest upon arable wildlife is an important consideration in its management, but one that has largely been neglected. This paper quantifies the effects of modern harvesting techniques on arable-dwelling wood mice, testing the null hypothesis that the behaviour and survival of individuals are unaffected by harvest, and quantifying the effects of harvest at the population level. We also discuss the implications of the results for the management of this species and its predators on arable farmland.
Abstract
The effects of cereal harvesting on the ecology of wood mice Apodemus sylvaticus were investigated at three arable study sites in Oxfordshire from 1987 to 1991 using both radio-tracking and live-trapping methodologies. The process of harvesting itself had little direct effect on the mice, but the removal of the cover afforded by the crop greatly increased predation pressure on the mice. After harvest, mice either emigrated from the arable ecosystem or reduced activity. Nevertheless, over half (17 of 32) of the mice radio-collared before harvest were taken by predators in the first week following harvest. Together with emigration, this produced an 80% decrease in the population. Post-harvest activities such as stubble burning subsequently further increased mortality. The dramatic increase in prey availability may benefit predators of small mammals in the cereal ecosystem such as tawny owls Strix aluco and weasels Mustela nivalis.
METHODS
Keywords." Apodemus sylvatics, cereal harvesting, agriculture, predators, small mammals.
Two types of data were collected from arable wood mice populations at three study sites, all of which were within 5 km of Oxford, UK and sown with winter wheat or winter barley. Live-trapping data were collected at monthly intervals between November 1990 and December 1991 from one of the study sites where the arable fields bordered woodland. Radio-tracking data were collected over the course of four years between 1987 and 1991. Mice were trapped using aluminium Longworth livetraps. Animals were weighed, sexed and individually marked with numbered Michel clip (Rocket Ltd, London, UK) eartags before being released at site of capture. The trapping grid consisted of one trap at each point, with 24 m spacing between points; an area of 10 ha was covered using 180 traps. Traps were set for four consecutive nights each calendar month and were checked at 0000, 0800 and 1600 h GMT. Wood mice were the only species frequently caught; other species which were caught occasionally, such as bank voles Clethrionomys glareolus and common shrews Sorex araneus, were released without marking at site of capture. The radio-tags (SS1 transmitters: Biotrack, Wareham, U.K.) weighed 2 g and were fitted only to adult mice weighing > 20 g (Wolton & Trowbridge 1985; Pouliquen et al., 1990). Radio-collars were secured with nylon cable ties and fitted whilst the animal was under light anaesthesia using methoxyfluorane. The tagged animal was then retained for 5-10 min to recover full
INTRODUCTION The intensively farmed arable ecosystem covers nearly 70% of Europe and represents an important habitat for many species. The wood mouse Apodemus sylvaticus, a generalist small mammal with catholic dietary (Pelz 1989) and habitat (Wolton & Flowerdew, 1985) requirements, has been particularly successful at exploiting farmland and occurs in that habitat throughout the year (Green, 1979; Tew, 1989; Loman, 1991). However, arable farmland is neither a natural nor an undisturbed habitat and all wildlife inhabiting this ecosystem inevitably faces periods of disruption. The most marked, and traumatic, of these periods is harvest, when the crop is removed from the fields and the ground prepared for sowing. With recent political initiatives encouraging reduced cereal production and increasing environmental awareness, several schemes have been proposed, either taking land out of production (e.g. 'set-aside') or extensifying * To whom correspondence should be addressed at: Joint Nature Conservation Committee, Monkstone House, City Road, Peterborough PE1 1JY, UK. Biological Conservation 0006-3207/93/$06.00 © 1993 Elsevier Science Publishers Ltd, England. Printed in Great Britain 279
T. E. Tew, D. W. MacdonaM
280
locomotor activity and released at site of capture. Wherever possible, radio-collared mice were recaptured after a period of three weeks' radio-tracking and the collars removed. The instrumented mice could generally be located from 50 m, using a Mariner receiver (Model M57: Mariner Radar, Lowestoft, UK) and hand-held threeelement Yagi aerial. Mice were radio-tracked intensively on foot throughout the night with radio-fixes taken every 10 min from first to last activity. In addition, nest-sites were checked daily to confirm residency and animal survival. Away from the nest, radio-fixes were taken to an accuracy of + 2-5 m, facilitated by the fact that the mice quickly habituated to the tracker's presence (Tew, 1989) and could be approached to within 10 m. A 50 m grid was marked out across the study sites by fibre-glass canes marked with coloured reflective tape. If the radio-signal disappeared, an immediate and extensive search of the surrounding area largely eliminated emigration from the study site as a possible cause. Although emigration could never be definitively eliminated as a cause of disappearance it is unlikely that many mice evaded these large-scale searches. Often, direct field observation allowed the cause of the loss to be identified-normally predation was either seen or predators were observed close to the area where the mouse was last seen. Alternatively, mouse collars were found lodged in trees, beneath owl perches or within weasel nests. Data were entered onto an Apple Macintosh system and analysed using the ' W I L D T R A K ' software package (Todd, 1992). Statistical analyses follow Sokal and Rohlf (1981) and unless otherwise stated significance is assumed when p < 0.05. RESULTS Live-trapping
Monthly estimates of population size, recruitment and survival rates, calculated using Jolly-Seber capture-mark--recapture analyses, are shown in Figs 1 and 2. Actual numbers of animals captured ranged from six in March 1991 to 133 in July 1991. Harvest occurred shortly after the August trapping session. 30 09
.t:
2o E
z
I
Feb
Mar
|
Apr
I
May
I
I
Jun Jul 1991
Aug
I
I
Sop
Oct
Nov
Fig. 1. Monthly population size (O) and recruitment (0), cap culated by Jolly-Seber capture-mark-recapture analyses. Time of harvest is indicated by the solid vertical line.
1.2
1.0
0.8" .=
0.6 0.4' 0.2 0.0 Mar
I
i
Apr
May
i
i
Jun
Jul
•
Aug
Sop
i
Oct
i
Nov
Dec
1991
Fig. 2. Monthly survival rates, calculated using Jolly-Seber captur~mark recapture analysis (C)) and indices of radiocollar survival (Q). Time of harvest is indicated by the solid vertical line. Radio-tracking
--
survival
It is problematical to ascribe radio-tag failure definitively to predation since collars may be shed, or may stop due to battery failure, without the animal being killed. Radio-collars were occasionally shed by the animals, usually in the nest, and, in these instances the transmitters were often chewed by their previous owners and ceased to function. Usually, this sequence of events occurred within 3 days of collar attachment. The electronic (i.e. battery) lifespan of the radiotransmitters was determined by daily monitoring of the signal from a sample of transmitters that had been removed from animals and were kept in the laboratory. Although laboratory conditions are more constant than those in the field, this does give an indication of battery lifespan. The mean lifespan of the collars was 37.8 days and was very consistent (SD = 18, n = 23, range 35~41); the probability of a battery failing before 30 days was less than 0.001. For further analyses, therefore, any collar which failed after five days but within 30 days of its attachment was deemed to be due to causes that arose from neither faulty attachment nor battery failure, i.e. predation of the animal causing signal cessation or emigration of the animal from the study site. Indices of collar survival from 73 mice, radio-collared between February and November 1991, are shown in Fig. 2, alongside the estimates of population survival derived from live-trapping data. The indices are calculated as the proportion of radio-collared mice known to have survived for more than one month following collar attachment. The data describing the known fate of 33 mice radiotracked over the harvest period are summarised in Table 1. Radio-tracking
-- movements
The radio-tracking data were also analysed for differences in movements between the periods before and after harvest. Movement parameters were only calculated from data sets that spanned a complete night,
281
Effects o f harvest on wood mice Table 1. The fate of 33 radio-collared mice at harvest
Study site & year
Wytham 1987 Sescut, 1988 St Frides, 1990 Wytham, 1991 Totals
Sample size
Killed by combine harvester
Survived combine harvester
7 11 4 11
1
6
3
3
1
1
0 0 0
11 4 11
7 2 5
4 2 6
1 ---
2 --
33
1
32
17
15
2
3
from first to last activity. As many of the mice died soon after harvest there were fewer data from after harvest, which led to an unbalanced data set. To counter this, analyses were conducted only on equal numbers of nights from both before and after harvest. Twelve mice were radio-tracked both before and after harvest and there were significant decreases in the distance moved each night, the mean rate of movement and the percentage of time spent moving (Wilcoxon signed-rank test, Ho no difference in movements before and after harvest - - Table 2). Home-range size estimation is sensitive to the number of fixes taken and for this species three complete nights of radio-locations taken at 10min intervals are required for accurate estimates (Tew, 1989). Consequently, home-range size was only calculated for those animals where there were three or more nights' data from both before and after harvest. Homerange sizes were calculated using the restricted polygon technique (Wolton, 1985), which gives smaller, and more accurate, estimates of home-range size for this species than the minimum convex polygon method (Tew, 1989). There was no significant difference between home-range sizes before and after harvest (Wilcoxon signed-rank test, Ho: no difference in homerange sizes before and after harvest - - Table 2), although this may have been due to small sample sizes. Only six of the twelve mice satisfied the criteria for analysis, but five of these showed a decrease in homerange size. Following harvest, eight mice were radio-tracked during straw baling and none was killed in the process. Of five animals tracked during stubble burning in 1987 and 1988 two (40%) were killed, both of which had burrows directly below the lines of straw left by the Table 2. Home-range and movement parameter date from both before and after harvest and the results of a Wilcoxon signedrank test examining differences between the two
Movement parameter Pre-harvest Post-harvest (mean + s.d) (mean+ s.d)
n, Z, p
Total nightly distance 927 _+433 568 + 274 12, -2.75, 0.006 moved (m) Mean rate 1.71 +0.68 1.12+0.54 12, 2.63,0.009 movement(m rain I) Percentage of time 82.67 + 6.58 71.58+ 13-77 12, -2.63, 0.008 spent moving Home-range size (ha) 076 + 0.89 0.49+ 0.52 6, 1.41, 0.16
Disappeared within 1 week of harvest
Survived > 1 week after harvest
Killed by stubble burning
Survived Stubble burning
combine. Post-mortem examination suggested that these mice were asphyxiated, rather than burnt, by the stubble fire. DISCUSSION There have been few studies of small mammals in the arable habitat (Kikkawa, 1964; Bergstedt, 1966; Pollard & Relton, 1970; Eldridge, 1971; Green, 1979, Loman, 1991) and none of these have specifically addressed the effects of harvest, although Loman (1991) noted that farming activity in autumn may have had detrimental effects on the wood mouse population, attributing these effects to the reduction in food availability and destruction of burrow entrances. Recent work has also investigated the traumatic effects of pesticide application on arable small mammal populations (Tarrant et al., 1990; Johnson et al., 1991; Tew, 1992). Arable populations of wood mice may be split into two types. Those close to woodland are joined by immigrating conspecifics in the spring (e.g. Kikkawa, 1964; Bergstedt, 1966; Corke, 1974) whereas those far from woodland are not (e.g. Pollard & Relton, 1970; Green, 1979). This study site falls into the former category: between February and May, as the growing crop in the fields started to provide cover, there was a steady immigration of adults into the population from arable hedgerows and the neighbouring woodland (Fig. 1). These immigrants join the overwintered residents to set up the summer breeding system of female defence polygyny (Tew, 1989) and form the breeding population. Young of the year started to enter the population in May, and there was a burst of juvenile recruits in June, July and August. These were joined in July and August by a large influx of (newly) adult animals, probably the first cohort of animals born in the wood which were then emigrating from that habitat. Harvest of the cereal crop occurred between the August and September trapping sessions. Fig. 1 illustrates the dramatic crashes, in both recruitment and population density, immediately following harvest. Because emigration can not be definitively excluded as a causal process, hereafter we shall refer to the 'persistence' of the arable population rather than its 'survival'. Although the estimation of persistence distributions for radio-tagged animals has recently been the subject of some elegant analyses (Pollock et al., 1989, White &
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Garrott, 1990), allowing for both the staggered entry of radio-tagged animals and transmitter failure or emigration, they assume that the censoring mechanism is random. In this study, where predators stop the radio-signal whilst killing the animal, such assumptions are unjustified. Furthermore, the precision of such analyses is poor unless the number of animals tagged at any one time is greater than 20. In this study, the number of tagged animals rarely exceeded 10 at any one time and so simpler survival analyses were employed. Nevertheless, the indices calculated for collar survival accurately reflected the overall persistence of the population (Fig. 2), indicating both that the estimates were accurate and that the radio-tagged animals were a representative sample of the population. Figure 2 illustrates the dramatic decrease in persistence of the wood mouse population after harvest. The crash in arable population levels at harvest is due to two effects. First, animals may emigrate from the harvested fields. Live-trapping in the neighbouring wood two weeks after harvest captured 13 mice that were previously resident in the arable fields (none of these were radio-collared animals, supporting the view that our methods of detecting emigration amongst the radio-collared sample were adequate). Secondly, many of the mice in the arable fields are taken by predators immediately following harvest. The mechanical actions of harvest have little direct effect upon the mice and only 1 out of 33 (3%) was killed by the combine harvester (Table 1). However, 17 of 32 (53%) of the radio-collared mice disappeared within one week of harvest and, in nine of these 17 instances, predation by either weasels Mustela nivalis or tawny owls Strix aluco was either directly observed or inferred. In the latter cases, the circumstantial evidence, consisting of chewed collars in weasel nests or bloodied collars lodged in trees, was conclusive. In addition, direct field observation of predators suggests that they react to the changes in the arable habitat at harvest. In particular, tawny owls changed their hunting behaviour at harvest. Prior to harvest, they rarely hunt farmland. When they do, they concentrate particularly on the grassy banks bordering hedgerows since the crop prevents them from stooping on prey. Immediately following harvest, however, the owls fly low over the fields and stoop onto prey both in the stubble and directly into the straw lines left by the combine (Tew unpublished data). In response to the change in their habitat the mice are less active above ground, moving slower, less frequently and travelling shorter distances. There was a decrease in home-range size after harvest, although this was not significant, probably due to the small sample sizes. It seems likely that this reduction in activity is in direct response to the increase in predation pressure caused both by their increased vulnerability to predation and the increase in predator activity. Several weeks after harvest the straw is baled and the stubble is either ploughed into the soil or burned. Baling had no effect on the mice but stubble burning killed 40% of the remainder, although sample sizes were small.
Both mice that were killed by stubble burning had burrows directly below the straw lines, where the stubble fire burnt most fiercely. All three survivors had burrows between the straw lines. Post-mortem examination suggested that the mice had been asphyxiated by the stubble fire, and it is likely that as the fire passed overhead it drew the air out of the burrow system. Since the burrows of arable wood mice tend to be simple, with a single entrance, there is no opportunity for escape. In woodland habitats, wood mice populations show a characteristic decrease over the winter and spring as adult animals fulfill their life expectancy and die off (Flowerdew, 1985). Whilst the mortality of the arable wood mouse population at harvest is dramatic, many of the animals killed at this time of year are nearing their natural life expectancy, and it may be that the predation corresponds to a 'doomed surplus' (Errington, 1963). It is unlikely that a specialist small mammal predator such as the weasel can regulate wood mouse numbers, although more facultative predators such as the tawny owl may do so (Erlinge et al., 1983). In any case, harvesting of the cereal presents a great increase in food availability for the predators of the arable ecosystem, and its timing may be beneficial to summer-born predators dispersing from their natal ranges. Such juveniles are often considered to be the age class under most stress. In summary, the harvest of the cereal crop has little direct effect on the resident wood mice but the removal of cover greatly increases the predation pressure upon them. The mice react by either leaving the habitat altogether, emigrating into neighbouring woodland, or by decreasing foraging activity. Nevertheless, approximately half the population falls to predators immediately following harvest. The baling of the straw and ploughing has no effect upon the mice, although stubble burning further increases post-harvest mortality. Despite high mortality, there appear to be sufficient remaining animals to overwinter in the agricultural habitat and sustain the following year's mouse population. ACKNOWLEDGEMENTS We thank S. J. Adams, E. D. Brown, J. Rae, I. A. Todd and numerous field assistants for their technical support. The original version of this paper was much improved by the comments of Dr. R. E. Kenward and an anonymous referee, to whom we are very grateful. The work was supported by the Joint Agricultural and Environmental Programme (JAEP/NERC) and The Environmental Research Fund (TERF). REFERENCES Bergstedt, B. (1966). Home ranges and movementsof the rodent species Clethrionomys glareolus (Schreber), Apodemus flavicollis (Melchior) and Apodemus sylvaticus (Linn~) in southem Sweden. Oikos, 17, ! 50-7. Corke, D. (1974). The comparative ecology of the two British species of the genus Apodemus (Rodentia, Muridae). Unpublished PhD thesis, University of London.
Effects of harvest on wood mice Eldridge, M. J. (1971). Some observations on the dispersion of small mammals in hedgerows. J. of Zool., Lond., 165, 530-4. Erlinge, S. et al. (1983). Predation as a regulating factor on small rodent populations in southern Sweden. Oikos, 40, 36-52. Errington, P. L. (1963). Muskrat populations. Iowa State University Press, Ames. Flowerdew, J. R. (1985). The population dynamics of wood mice and yellow-necked mice. Symp. of ZooL Soc. of Lond., 55, 315-38). Green, R. (1979). The ecology of wood mice Apodemus sylvaticus on arable farmland. J. Zool., Lond., 188, 357-77. Johnson, I. P., Flowerdew, J. R. & Hare, R. (1991). Effects of broadcasting and of drilling methiocarb molluscicide pellets on field populations of wood mice, Apodemus sylvaticus. Bull. of Environ. Contam. & ToxicoL, 46, 84-91. Kikkawa, J. (1964). Movement, activity and distribution of the small rodents Clethrionomys glareolus and Apodemus sylvaticus in woodland. J. Anim. Ecol., 33, 259-99. Loman, J. (1991). The small mammal fauna in an agricultural landscape in southern Sweden, with special reference to the wood mouse Apodemus sylvaticus. Mammalia., 55, 91-6. Macdonald, D. W. & Smith, H. N. (1991). New perspectives on agro-ecology: between theory and practice in the agricultural ecosystem. In The ecology of temperate cereal fields, ed. L. G. Firbank, N. Carter, J. F. Darbyshire, & G. R. Potts. Blackwell Scientific Publications, Oxford, pp. 413-48. Pelz, H-J. (1989). Ecological aspects of damage to sugar beet seeds by Apodemus sylvaticus. In Mammals as pests, ed. R. J. Putman. Chapman & Hall, London, pp.34-48. Pollard, E. & Relton, J. (1970). Hedges, V. A study of small mammals in hedges and cultivated fields. J. of Appl. Ecol., 7, 549-57.
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