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Damage to saplings by red deer (Cervus elaphus): effect of foliage height and structure
Forest Ecology and Management 181 (2003) 31–37
Damage to saplings by red deer (Cervus elaphus): effect of foliage height and structure P.C. Renauda,b,*, H. Verheyden-Tixiera, B. Dumontb a
INRA, HYFS, Institut de Recherches sur les Grands Mammife`res, BP 27, F31326 Castanet-Tolosan Cedex, France b INRA, ENA, Unite´ de Recherches sur les Herbivores, Theix, F63122 St-Gene`s-Champanelle, France Received 1 November 2001; received in revised form 1 June 2002; accepted 10 September 2002
Abstract Red deer cause heavy damage to forest production, hence the need to better understand what determines their dietary choices. Deer are selective herbivores. According to the optimal foraging theory (OFT), they should select foods that maximise their net rate of energy gain. For a given nutritional quality, we predict that plant architecture and height should affect deer feeding preferences through intake rate variations. In the first experiment, 12 tame red deer with shoulder height (SH) ranging from 82 to 105 cm were individually offered fresh bunches of Salix caprea at seven heights regularly spaced from 25 to 205 cm. Animals preferred bunches at 85 and 115 cm height (29 and 32% of feeding time). There was a positive relationship between average consumption height (CH) and animal shoulder height (CH ¼ 0:99 SH; r 2 ¼ 0:43; P < 0:05) but intake rate did not change with consumption height. In the second experiment, 10 fresh bunches of Quercus pedunculata were offered on three wooden structures, resembling a bushy topped (BT), a normal (N) and a five-shoot (FS) oak sapling. For each structure, average bunch height was set at preferred consumption height. Five tame hinds were observed during individual cafeteria trials (double- then triple-choice). Intake rate was slightly higher for FS than for the other structures (FS ¼ 23:7 g DM/min, N ¼ 22:3 g DM/min and BT ¼ 22:0 g DM/min). Preferences were expressed as the proportion of feeding time during the first min of test. In the double-choice trials, preference was higher for FS relative to BT (61%–39%), and for N relative to BT (62%–38%), but similar between FS and N (57%–43%). In the triple-choice trials, preference for FS (44%), N (24%) and BT (32%) differed from 33%– 33%–33%. In both trials, there was thus a slight preference for FS, i.e. for the structure where all bunches were widely spaced and at the hinds’ preferred height. Foliage height and, to a lesser extent, structure of saplings thus affect the feeding preferences of red deer. These results can contribute to improving management practices to limit deer damages to commercial plantations. # 2003 Elsevier Science B.V. All rights reserved. Keywords: Red deer; Browsing; Preference; Intake rate; Sapling height; Canopy structure
1. Introduction Red deer, as well as other cervid populations, are rapidly increasing causing damages to forestry and *
Corresponding author. Tel.: þ33-5-6128-5499; fax: þ33-5-6128-5500. E-mail address: [email protected] (P.C. Renaud).
agriculture in northern Europe and America (Putman and Moore, 1998; Thompson and Henderson, 1998). A better understanding of deer diet selection is needed to construct successful predictive models of plant use and impact, as well as to provide a basis for habitat and deer population management (see Hanley, 1997 for review). In particular, Hanley has pointed out that ‘‘our view of the forage resource must broaden beyond
0378-1127/$ – see front matter # 2003 Elsevier Science B.V. All rights reserved. doi:10.1016/S0378-1127(03)00126-9
32
P.C. Renaud et al. / Forest Ecology and Management 181 (2003) 31–37
the concepts of genus, species and plant parts. It must include variation in (. . .) physical characteristics such as plant architecture’’. Deer are selective herbivores for which food selection is determined not only by preferences associated with quality and taste, but also by the cost of obtaining food. This cost modifies food intake rate and, according to optimal foraging theory (OFT), animals will select foods that maximise their energetic efficiency, i.e. their nutrient intake rate (Stephens and Krebs, 1986). Structural properties of plants are likely to affect nutrient intake rate, notably bite size and biting rate, thus affecting herbivores’ food choice (Laca et al., 2001). In particular, browsers are faced with a wide range of plant morphological structures affecting bite size and biting rate, such as fibrousness, spines (Dunham, 1980; Cooper and Owen-Smith, 1986), leaf size (Dunham, 1980), stem length (Bergstro¨ m and Danell, 1987; Danell et al., 1991; Edenius, 1992), leaf and stem architecture (Shipley and Spalinger, 1992; Shipley et al., 1994) and stem spatial distribution (Shipley and Spalinger, 1995). As a consequence, Cooper and Owen-Smith (1986) showed that plant acceptability for kudus (Tragelaphus strepsiceros) is reduced by the combination of small leaves and spines, but whether or not food choice by cervids is also based upon plant structural properties is not well documented. Jiang and Hudson (1993) found that grazing red deer left a feeding station when their neck angle reached a critical level, suggesting that biokinetic factors could have a major influence on herbivores’ foraging efficiency and decisions. Other evidence of plant structural effects comes from experiments where environmental manipulations were used to modify morphology and chemical composition of Sitka spruce saplings (Picea sitchensis), within the purpose of evaluating the consequences for deer’s consumption (Iason et al., 1996; Hartley et al., 1997). Large trees with more lateral branches were more likely to be browsed by deer and suffered greater offtake than smaller or less bushy trees. Sapling morphology appeared to have a greater influence on choice by red deer than sapling chemical composition. In this paper, we present results from two experiments designed to assess the effect of leafy browse architecture on intake rate and preference by red deer. In the first trial, we determined if there was a preferred browsing height in relation to the animals’ size, and to what extent intake rate differed between foliage heights. We predict that deer should have a preferred
feeding height according to their body size, due to biokinetic factors related to browsing height. In a second trial, we tested the effect of three different sapling structures on red deer intake rate and preference. Feeding preferences were tested with 10 fresh tree bunches of similar weight offered on wooden built structures, to avoid any confounding effects. We predict that the structure with more lateral bunches will provide the greatest bite size and intake rate (Shipley and Spalinger, 1992; Iason et al., 1996) and thus will be preferred. These two trials enable us to examine the consequences of sapling height and structure on their sensitivity to damages by red deer in commercial plantations.
2. Materials and methods 2.1. Animals Animals were used to regular handling and were kept together in grass plots with few available trees. To accustom them to browse trees, they were daily offered fresh branches for 1 week before measurements began. In the first experiment, we used six 1year-old hinds and six 1-year-old stags, with shoulder height (SH) ranging from 82 to 105 cm. In the second experiment, we used five 1-year-old hinds with similar shoulder heights. When not tested, animals were kept in an indoor pen and were fed in the evening. Each animal received daily 1 kg of a natural mountain pasture hay and 700 g of pellets. Food offered outside the tests supplied 90% of their energy requirements for maintenance (Brelerut et al., 1990). On days of experiments, each animal was individually tested once a day in the first experiment, and from one to three times a day in the second one. Observation order was randomised each day. 2.2. Experiment 1: effect of foliage height on its consumption by deer Individual animals were offered fresh bunches of Salix caprea, readily eaten in this season (May), in a cafeteria trial on 3 successive days. For each test, 28 bunches of similar weight were regularly arranged at seven heights, ranging from 25 to 205 cm above ground level, on four adjacent wooden frames (Fig. 1).
P.C. Renaud et al. / Forest Ecology and Management 181 (2003) 31–37
33
Fig. 1. Wooden frames used to test the effect of S. caprea foliage height on its consumption by red deer; 28 bunches (coloured in grey) of similar biomass were regularly arranged at seven heights from 25 to 205 cm above ground level.
We used a hand-held computer (Workabout–Psion PLC, London, UK) with an event recorder to record the time spent feeding on each bunch. Observation was stopped when more than 75% of available leaves from one height were consumed or when an animal stopped eating for more than 1.5 min. The foliage mass removed from each bunch was estimated by weighing every bunch before and after consumption. One uneaten control bunch was used to calculate weight losses due to evaporation during the trial. For each height, we then calculated the animal’s preference (in % of feeding time) and mean intake rate over a given test (in g dry matter (DM)/min). 2.3. Experiment 2: effect of sapling structure on its utilisation by deer Three sapling structures were built from wood, resembling a normal sapling (N), a five-shoot oak sapling (FS, coppice form) and a bushy topped sapling
(BT, multi-stem form without an apical dominance). The latter two structures are frequently observed in commercial plantations where herbivores cause damages. Small holes were pierced on these structures to fix 10 fresh bunches of oak (Quercus pedunculata), readily eaten by deer during this season (June). Ten bunches of similar mass were attached on each structure with their barycentre set at the animals’ preferred consumption height (CH) (i.e. at 90 cm from ground level for these five hinds, Fig. 2). Individual animals were first offered the three sapling structures alone for 3 days in order to record their intake rate on each structure (in g DM/min; 3 measurement days, n ¼ 9 per animal and per structure). Second, preferences between these structures were recorded in double-choice trials (6 days, n ¼ 4 per animal and per choice) then in triple-choice trials (6 days, n ¼ 6 per animal), the position of the structures in the enclosure being reversed in the successive test in order to eliminate any potential position effect (e.g. Chevallier-Redor et al., 2001).
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P.C. Renaud et al. / Forest Ecology and Management 181 (2003) 31–37
Fig. 2. The three sapling structures offered to red deer were a normal oak sapling (N), a bushy topped oak sapling (BT) and a five-shoot oak sapling (FS); 10 bunches of Q. pedunculata (circle) of similar biomass were fixed on each structure.
Observation was stopped when more than 75% of the leaves available from one structure were consumed or when animal stopped eating for more than 1.5 min. Using the same procedure as in experiment 1, we recorded the time spent feeding on each group of bunches from each structure and the foliage mass removed. We defined the preference for each structure as the proportion of feeding time spent browsing it.
compared using one-way ANOVA and Bonferroni comparisons. Finally, we used a w2-test to compare the actual preference measurements with a theoretical no-preference hypothesis, i.e. 50%–50% for paired trials and 33%–33%–33% for the triple ones.
2.4. Statistical analyses
In the first trial, deer consumed bunches between heights of 25 and 175 cm. Preferred bunches were at 85 and 115 cm (29 and 32% of total feeding time). The effect of foliage height on its consumption by deer followed a unimodal distribution of bunch height (Fig. 3). Mean preferred consumption height ranged from 68 to 110 cm and was linearly related to the animals’shoulder height (CH ¼ 0:99 SH; r 2 ¼ 0:43; P < 0:05; n ¼ 12); the slope was not significantly different from one. Intake rate on Salix bunches (average 12.22 g DM/min) did not differ between bunch heights (F4;57 ¼ 0:47), but we observed significant differences between individuals (F11;57 ¼ 6:53; P < 0:0001). Individual intake rates ranged from 5.6 to 19.1 g DM/min. The interaction between bunch height and individual animals was not significant (F42;57 ¼ 0:58).
In the first experiment, the effect of animal size on its preferred consumption height was assessed by linear regression between average consumption height (% feeding time from the 3 measurement days) and animal shoulder height (cm). We tested whether the slope was different from one using the REG procedure of SAS (option TEST, SAS, 1989). We then used a two-way ANOVA with a full factorial model to analyse the effects of bunch height and individual animal on the intake rate of Salix bunches. We used a similar model in the second experiment to assess the effects of sapling structure and individual animal on the intake rate of Quercus bunches. A Duncan test was used to detect differences between structures. Intake rates on each structure offered alone, in pairs or trios were
3. Results
P.C. Renaud et al. / Forest Ecology and Management 181 (2003) 31–37
Fig. 3. Mean consumption of 12 red deer (% of feeding time) in relation to the foliage height (n ¼ 36).
In the second experiment, red deer hinds browsed the five-shoot structure faster (intake rate: 23.7 g DM/ min) than the other two structures (N: 22.3 g DM/min; BT: 22.0 g DM/min; F2;17 ¼ 4:868; P ¼ 0:013). Intake rates obtained in single-choice trials did not significantly differ from double- or triple-choice trials (P > 0:05). When the whole test was considered, no preference was observed for any of the structures in either the double- or the triple-choice trials. In the double-choice trials, preference was similar between FS and BT (53%–47%, not different from 50%–50%; w2 ¼ 0:36; d:f: ¼ 1; NS), between N and BT (46%– 54%; w2 ¼ 0:64; NS), and between FS and N (52%– 48%; w2 ¼ 0:16; NS). In the triple-choice trials, preference for FS (34%), N (33%) and BT (33%) did not differ from 33%–33%–33% (w2 ¼ 0:02; d:f: ¼ 2; NS). As this could be because animals usually switch to another structure before 75% of the first one is consumed, we repeated the same analysis on the choices recorded during the first min of the trial. Here, in the double-choice trials, preference was higher for FS relative to BT (61%–39%, different from 50%– 50%; w2 ¼ 4:84; d:f: ¼ 1; P < 0:05) and for N relative to BT (62%–38%;w2 ¼ 5:76; P < 0:05), but similar between FS and N (57%–43%; w2 ¼ 1:96; NS). In the triple-choice trials, preference for FS (44%), N (24%) and BT (32%) differed from 33%–33%–33% (w2 ¼ 6:09; d:f: ¼ 2; P < 0:05).
4. Discussion In the first experiment we showed that red deer prefer to browse at the level of their shoulder height,
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and this despite the fact that the animals’ intake rate remained constant between foliage heights. Roe deer also have a preferred browsing height of around 75 cm (Duncan et al., 1998), near their mean shoulder height (63–74 cm; Whitehead, 1993). Gill (1992) suggested that deer usually browse at an intermediate level between ground and full reach. Saint-Andrieux et al. (1999) found that browsing pressure by red deer is more intense between 90 and 130 cm height. The positive relationship between average consumption height and individuals’ shoulder height, observed in experiment 1, indicates that the effect of animal size on preferred browsing height should also occur within species, between individuals of different size. As this cannot be explained by differences in intake rates, the preference for foliage at shoulder height could be related to a postural benefit leading to lower postural cost at this level compared to a browsing position with head and neck raised or lowered. This suggests not only that biokinetic factors influence foraging decisions, as was assumed by Jiang and Hudson (1993), but also that they are sufficient to induce preferences even without intake rate maximisation. This relation between preferences and plant height could also be used in a management perspective to construct damage indicators. Through a regular survey of browsing signs on height classes of selected plants within or surrounding the commercial strands, this indicator could clearly show any increasing browsing pressure before damages on less preferred but commercially used saplings becomes too excessive. Webster et al. (2001) have proposed a similar approach using the mean height of three preferred herbaceous species to quantify the level of damage on the overall ground layer vegetation. It allowed them to successfully evaluate impact of white-tailed deer (Odocoileus virginianus) on forest plant communities before lasting damages occurred. In the second experiment, we observed a slight but regular preference for FS, i.e. for the structure where all bunches (laterals and apical) were widely spaced at hinds’ preferred height. We expected this preference for the structure allowing the greater intake rate. Intake rate on FS bunches was however only 7% higher than on the two others structures. An optimal behaviour would be to choose the FS structure first and then, to quickly switch to another structure as intake rates became similar, so as to eat a mix of every structure during the rest of the trial.
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P.C. Renaud et al. / Forest Ecology and Management 181 (2003) 31–37
This would result in a slight preference for FS relative to the other structures, consistent with what has been observed during the first min. This choice thus followed OFT predictions. Although this difference in intake rate is statistically significant, it is also likely that it was too small to be perceived by animals. Indeed, in previous patch choice trials with sheep (Dumont et al., 1998) and goat (Illius et al., 1999), animals expressed highly variable preferences when the two alternatives were similar in energy or DM intake rates, whereas choices were systematically made in favour of the better alternative when they were of clearly different value, i.e. different by at least 50%. Similarly, here, deer probably did not discriminate between the offered alternatives on the basis of differences in intake rate. Animals rather selected structures on the basis of their architecture, e.g. preferring that structure with the lowest vertical dispersion of biomass around the preferred consumption height. As a consequence, apical buds of N and BT saplings were not attacked during the first min in 60 and 77% of double-choice trials and in 83 and 80% of the triple-choice ones. Thus, an animal moving across a commercial plantation should have a lower impact on buds of major importance for sapling growth as soon as these buds are higher than the deer’s preferred browsing height. 5. Conclusion Red deer have a preferred feeding height which is correlated with their shoulder height and which is independent of differences in intake rates between foliage heights. When offered the three sapling structures, red deer preferred the one where all bunches were widely spaced at their preferred height. Foliage height and, to a lesser extent, structure of saplings thus affect the feeding preferences of red deer. This knowledge can help in proposing management practices to limit their damages to commercial plantations, e.g. by indicating up to what height it is worthwhile protecting valuable saplings from deer browsing in order to avoid consumption of apical buds. Acknowledgements We greatly thank F. Anglard, B. Cargnelutti, N. Cebe, N. Chevallier-Redor and C. Mallet for their
excellent technical assistance and for their care of the animals. Ph. Ballon and D. Pe´ pin made useful comments on the experimental schedules. A.J.M. Hewison kindly revised the English version of the manuscript. We thank P. Duncan and another reviewer for useful comments on the manuscript. We are also grateful to the organising committee of the International Conference on Forest Dynamics and Ungulate Herbivory (Davos), which partly funded conference fees to present these results. We thank the INRA (HYFS and ENA department) for the thesis grant of P.C. Renaud.
References Bergstro¨ m, R., Danell, K., 1987. Effects of simulated winter browsing by moose on morphology and biomass of two birch species. J. Ecol. 75, 533–544. Brelerut, A., Pingard, A., The´ riez, M., 1990. Le cerf et son e´ levage—Alimentation, techniques et pathologie. Editions du point ve´ te´ rinaire, Maisons–Alfort, France. Chevallier-Redor, N., Verheyden-Tixier, H., Verdier, M., Dumont, B., 2001. Foraging behaviour of red deer Cervus elaphus as a function of the relative availability of two tree species. Anim. Res. 50, 57–65. Cooper, S.M., Owen-Smith, N., 1986. Effects of plant spinescence on large mammalian herbivore. Oecologia 68, 446–455. Danell, K., Edenius, L., Lunberg, P., 1991. Herbivory and tree stand composition: moose patch use in winter. Ecology 72, 1350– 1357. Dumont, B., Dutronc, A., Petit, M., 1998. How readily will sheep walk for a preferred forage? J. Anim. Sci. 76, 965– 971. Duncan, P., Tixier, H., Hoffman, R.R., Lechner-Doll, M., 1998. Feeding strategies and the physiology of digestion in roe deer. In: Andersen, R., Duncan, P., Linnell, J.D.C. (Eds.), The European Roe Deer: The Biology of Success. Scandinavian University Press, Oslo, pp. 91–116. Dunham, K.M., 1980. The feeding behaviour of a tame impala (Aepyceros melampus). Afr. J. Ecol. 18, 341–351. Edenius, L., 1992. Moose feeding in relation to position of food plants. Alces Suppl. 1, 132–138. Gill, R.M.A., 1992. A review of damage by mammals in north temperate forests. 1. Deer. Forestry 65, 145–169. Hanley, T.A., 1997. A nutritional view of understanding and complexity in the problem of diet selection by deer (Cervidae). Oikos 79, 209–218. Hartley, S.E., Iason, G.R., Duncan, A.J., Hitchcock, D., 1997. Feeding behaviour of Red Deer (Cervus elaphus) offered Sitka Spruce saplings (Picea sitchensis) grown under different light and nutrient regimes. Func. Ecol. 11, 348–357. Iason, G.R., Duncan, A.J., Hartley, S.E., Staines, B.W., 1996. Feeding behaviour of red deer (Cervus elaphus) on Sitka spruce
P.C. Renaud et al. / Forest Ecology and Management 181 (2003) 31–37 (Picea sitchensis): the role of carbon-nutrient balance. For. Ecol. Manage. 88, 121–129. Illius, A.W., Gordon, I.J., Elston, D.A., Milne, J.D., 1999. Diet selection in goats: a test of intake rate maximization. Ecology 80, 1008–1018. Jiang, Z., Hudson, R.J., 1993. Optimal grazing of wapiti (Cervus elaphus) on grassland: patch and feeding station departure rules. Evol. Ecol. 7, 488–498. Laca, E.A., Shipley, L.A., Reid, E.D., 2001. Structural anti-quality characteristics of range and pasture plants. J. Range Manage. 54, 413–419. Putman, R.J., Moore, N.P., 1998. Impact of deer in lowland Britain on agriculture, forestry and conservation habitats. Mamm. Rev. 28, 141–164. Saint-Andrieux, C., Wilmart, D., Bernard, S., 1999. Impacts du cerf et du chevreuil sur la re´ ge´ ne´ ration naturelle de sapin pectine´ . Le Bulletin Mensuel de l’Office National de la Chasse 247, 12–21. SAS, 1989. SAS/STAT User’s Guide (release 6.11). SAS Inst. Inc., Cary, NC.
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Shipley, L.A., Spalinger, D.E., 1992. Mechanics of browsing in dense food patches: effects of plant and animal morphology on intake rate. Can. J. Zool. 70, 1743–1752. Shipley, L.A., Spalinger, D.E., 1995. Influence of size and density of browse patches on intake rates and foraging decisions of young moose and white-tailed deer. Oecologia 104, 112–121. Shipley, L.A., Gross, J.E., Spalinger, D.E., Hobbs, N.T., Wunder, B.A., 1994. The scaling of intake rate in mammalian herbivores. Am. Nat. 143, 1055–1082. Stephens, D.W., Krebs, J.R., 1986. Foraging Theory. Princeton University Press, Princeton, NJ. Thompson, M.J., Henderson, R.E., 1998. Elk habituation as a credibility challenge for wildlife professionals. Wildl. Soc. Bull. 26, 477–483. Webster, C.R., Jenkins, M.A., Parker, G.R., 2001. A field test of herbaceous plant indicators of deer browsing intensity in mesic hardwood forests of Indiana, USA. Nat. Areas J. 21, 149–158. Whitehead, G.K., 1993. The Whitehead Encyclopedia of Deer. Swan-Hill Press, Shrewsburg, England.
Damage to saplings by red deer (Cervus elaphus): effect of foliage height and structure P.C. Renauda,b,*, H. Verheyden-Tixiera, B. Dumontb a
INRA, HYFS, Institut de Recherches sur les Grands Mammife`res, BP 27, F31326 Castanet-Tolosan Cedex, France b INRA, ENA, Unite´ de Recherches sur les Herbivores, Theix, F63122 St-Gene`s-Champanelle, France Received 1 November 2001; received in revised form 1 June 2002; accepted 10 September 2002
Abstract Red deer cause heavy damage to forest production, hence the need to better understand what determines their dietary choices. Deer are selective herbivores. According to the optimal foraging theory (OFT), they should select foods that maximise their net rate of energy gain. For a given nutritional quality, we predict that plant architecture and height should affect deer feeding preferences through intake rate variations. In the first experiment, 12 tame red deer with shoulder height (SH) ranging from 82 to 105 cm were individually offered fresh bunches of Salix caprea at seven heights regularly spaced from 25 to 205 cm. Animals preferred bunches at 85 and 115 cm height (29 and 32% of feeding time). There was a positive relationship between average consumption height (CH) and animal shoulder height (CH ¼ 0:99 SH; r 2 ¼ 0:43; P < 0:05) but intake rate did not change with consumption height. In the second experiment, 10 fresh bunches of Quercus pedunculata were offered on three wooden structures, resembling a bushy topped (BT), a normal (N) and a five-shoot (FS) oak sapling. For each structure, average bunch height was set at preferred consumption height. Five tame hinds were observed during individual cafeteria trials (double- then triple-choice). Intake rate was slightly higher for FS than for the other structures (FS ¼ 23:7 g DM/min, N ¼ 22:3 g DM/min and BT ¼ 22:0 g DM/min). Preferences were expressed as the proportion of feeding time during the first min of test. In the double-choice trials, preference was higher for FS relative to BT (61%–39%), and for N relative to BT (62%–38%), but similar between FS and N (57%–43%). In the triple-choice trials, preference for FS (44%), N (24%) and BT (32%) differed from 33%– 33%–33%. In both trials, there was thus a slight preference for FS, i.e. for the structure where all bunches were widely spaced and at the hinds’ preferred height. Foliage height and, to a lesser extent, structure of saplings thus affect the feeding preferences of red deer. These results can contribute to improving management practices to limit deer damages to commercial plantations. # 2003 Elsevier Science B.V. All rights reserved. Keywords: Red deer; Browsing; Preference; Intake rate; Sapling height; Canopy structure
1. Introduction Red deer, as well as other cervid populations, are rapidly increasing causing damages to forestry and *
Corresponding author. Tel.: þ33-5-6128-5499; fax: þ33-5-6128-5500. E-mail address: [email protected] (P.C. Renaud).
agriculture in northern Europe and America (Putman and Moore, 1998; Thompson and Henderson, 1998). A better understanding of deer diet selection is needed to construct successful predictive models of plant use and impact, as well as to provide a basis for habitat and deer population management (see Hanley, 1997 for review). In particular, Hanley has pointed out that ‘‘our view of the forage resource must broaden beyond
0378-1127/$ – see front matter # 2003 Elsevier Science B.V. All rights reserved. doi:10.1016/S0378-1127(03)00126-9
32
P.C. Renaud et al. / Forest Ecology and Management 181 (2003) 31–37
the concepts of genus, species and plant parts. It must include variation in (. . .) physical characteristics such as plant architecture’’. Deer are selective herbivores for which food selection is determined not only by preferences associated with quality and taste, but also by the cost of obtaining food. This cost modifies food intake rate and, according to optimal foraging theory (OFT), animals will select foods that maximise their energetic efficiency, i.e. their nutrient intake rate (Stephens and Krebs, 1986). Structural properties of plants are likely to affect nutrient intake rate, notably bite size and biting rate, thus affecting herbivores’ food choice (Laca et al., 2001). In particular, browsers are faced with a wide range of plant morphological structures affecting bite size and biting rate, such as fibrousness, spines (Dunham, 1980; Cooper and Owen-Smith, 1986), leaf size (Dunham, 1980), stem length (Bergstro¨ m and Danell, 1987; Danell et al., 1991; Edenius, 1992), leaf and stem architecture (Shipley and Spalinger, 1992; Shipley et al., 1994) and stem spatial distribution (Shipley and Spalinger, 1995). As a consequence, Cooper and Owen-Smith (1986) showed that plant acceptability for kudus (Tragelaphus strepsiceros) is reduced by the combination of small leaves and spines, but whether or not food choice by cervids is also based upon plant structural properties is not well documented. Jiang and Hudson (1993) found that grazing red deer left a feeding station when their neck angle reached a critical level, suggesting that biokinetic factors could have a major influence on herbivores’ foraging efficiency and decisions. Other evidence of plant structural effects comes from experiments where environmental manipulations were used to modify morphology and chemical composition of Sitka spruce saplings (Picea sitchensis), within the purpose of evaluating the consequences for deer’s consumption (Iason et al., 1996; Hartley et al., 1997). Large trees with more lateral branches were more likely to be browsed by deer and suffered greater offtake than smaller or less bushy trees. Sapling morphology appeared to have a greater influence on choice by red deer than sapling chemical composition. In this paper, we present results from two experiments designed to assess the effect of leafy browse architecture on intake rate and preference by red deer. In the first trial, we determined if there was a preferred browsing height in relation to the animals’ size, and to what extent intake rate differed between foliage heights. We predict that deer should have a preferred
feeding height according to their body size, due to biokinetic factors related to browsing height. In a second trial, we tested the effect of three different sapling structures on red deer intake rate and preference. Feeding preferences were tested with 10 fresh tree bunches of similar weight offered on wooden built structures, to avoid any confounding effects. We predict that the structure with more lateral bunches will provide the greatest bite size and intake rate (Shipley and Spalinger, 1992; Iason et al., 1996) and thus will be preferred. These two trials enable us to examine the consequences of sapling height and structure on their sensitivity to damages by red deer in commercial plantations.
2. Materials and methods 2.1. Animals Animals were used to regular handling and were kept together in grass plots with few available trees. To accustom them to browse trees, they were daily offered fresh branches for 1 week before measurements began. In the first experiment, we used six 1year-old hinds and six 1-year-old stags, with shoulder height (SH) ranging from 82 to 105 cm. In the second experiment, we used five 1-year-old hinds with similar shoulder heights. When not tested, animals were kept in an indoor pen and were fed in the evening. Each animal received daily 1 kg of a natural mountain pasture hay and 700 g of pellets. Food offered outside the tests supplied 90% of their energy requirements for maintenance (Brelerut et al., 1990). On days of experiments, each animal was individually tested once a day in the first experiment, and from one to three times a day in the second one. Observation order was randomised each day. 2.2. Experiment 1: effect of foliage height on its consumption by deer Individual animals were offered fresh bunches of Salix caprea, readily eaten in this season (May), in a cafeteria trial on 3 successive days. For each test, 28 bunches of similar weight were regularly arranged at seven heights, ranging from 25 to 205 cm above ground level, on four adjacent wooden frames (Fig. 1).
P.C. Renaud et al. / Forest Ecology and Management 181 (2003) 31–37
33
Fig. 1. Wooden frames used to test the effect of S. caprea foliage height on its consumption by red deer; 28 bunches (coloured in grey) of similar biomass were regularly arranged at seven heights from 25 to 205 cm above ground level.
We used a hand-held computer (Workabout–Psion PLC, London, UK) with an event recorder to record the time spent feeding on each bunch. Observation was stopped when more than 75% of available leaves from one height were consumed or when an animal stopped eating for more than 1.5 min. The foliage mass removed from each bunch was estimated by weighing every bunch before and after consumption. One uneaten control bunch was used to calculate weight losses due to evaporation during the trial. For each height, we then calculated the animal’s preference (in % of feeding time) and mean intake rate over a given test (in g dry matter (DM)/min). 2.3. Experiment 2: effect of sapling structure on its utilisation by deer Three sapling structures were built from wood, resembling a normal sapling (N), a five-shoot oak sapling (FS, coppice form) and a bushy topped sapling
(BT, multi-stem form without an apical dominance). The latter two structures are frequently observed in commercial plantations where herbivores cause damages. Small holes were pierced on these structures to fix 10 fresh bunches of oak (Quercus pedunculata), readily eaten by deer during this season (June). Ten bunches of similar mass were attached on each structure with their barycentre set at the animals’ preferred consumption height (CH) (i.e. at 90 cm from ground level for these five hinds, Fig. 2). Individual animals were first offered the three sapling structures alone for 3 days in order to record their intake rate on each structure (in g DM/min; 3 measurement days, n ¼ 9 per animal and per structure). Second, preferences between these structures were recorded in double-choice trials (6 days, n ¼ 4 per animal and per choice) then in triple-choice trials (6 days, n ¼ 6 per animal), the position of the structures in the enclosure being reversed in the successive test in order to eliminate any potential position effect (e.g. Chevallier-Redor et al., 2001).
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Fig. 2. The three sapling structures offered to red deer were a normal oak sapling (N), a bushy topped oak sapling (BT) and a five-shoot oak sapling (FS); 10 bunches of Q. pedunculata (circle) of similar biomass were fixed on each structure.
Observation was stopped when more than 75% of the leaves available from one structure were consumed or when animal stopped eating for more than 1.5 min. Using the same procedure as in experiment 1, we recorded the time spent feeding on each group of bunches from each structure and the foliage mass removed. We defined the preference for each structure as the proportion of feeding time spent browsing it.
compared using one-way ANOVA and Bonferroni comparisons. Finally, we used a w2-test to compare the actual preference measurements with a theoretical no-preference hypothesis, i.e. 50%–50% for paired trials and 33%–33%–33% for the triple ones.
2.4. Statistical analyses
In the first trial, deer consumed bunches between heights of 25 and 175 cm. Preferred bunches were at 85 and 115 cm (29 and 32% of total feeding time). The effect of foliage height on its consumption by deer followed a unimodal distribution of bunch height (Fig. 3). Mean preferred consumption height ranged from 68 to 110 cm and was linearly related to the animals’shoulder height (CH ¼ 0:99 SH; r 2 ¼ 0:43; P < 0:05; n ¼ 12); the slope was not significantly different from one. Intake rate on Salix bunches (average 12.22 g DM/min) did not differ between bunch heights (F4;57 ¼ 0:47), but we observed significant differences between individuals (F11;57 ¼ 6:53; P < 0:0001). Individual intake rates ranged from 5.6 to 19.1 g DM/min. The interaction between bunch height and individual animals was not significant (F42;57 ¼ 0:58).
In the first experiment, the effect of animal size on its preferred consumption height was assessed by linear regression between average consumption height (% feeding time from the 3 measurement days) and animal shoulder height (cm). We tested whether the slope was different from one using the REG procedure of SAS (option TEST, SAS, 1989). We then used a two-way ANOVA with a full factorial model to analyse the effects of bunch height and individual animal on the intake rate of Salix bunches. We used a similar model in the second experiment to assess the effects of sapling structure and individual animal on the intake rate of Quercus bunches. A Duncan test was used to detect differences between structures. Intake rates on each structure offered alone, in pairs or trios were
3. Results
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Fig. 3. Mean consumption of 12 red deer (% of feeding time) in relation to the foliage height (n ¼ 36).
In the second experiment, red deer hinds browsed the five-shoot structure faster (intake rate: 23.7 g DM/ min) than the other two structures (N: 22.3 g DM/min; BT: 22.0 g DM/min; F2;17 ¼ 4:868; P ¼ 0:013). Intake rates obtained in single-choice trials did not significantly differ from double- or triple-choice trials (P > 0:05). When the whole test was considered, no preference was observed for any of the structures in either the double- or the triple-choice trials. In the double-choice trials, preference was similar between FS and BT (53%–47%, not different from 50%–50%; w2 ¼ 0:36; d:f: ¼ 1; NS), between N and BT (46%– 54%; w2 ¼ 0:64; NS), and between FS and N (52%– 48%; w2 ¼ 0:16; NS). In the triple-choice trials, preference for FS (34%), N (33%) and BT (33%) did not differ from 33%–33%–33% (w2 ¼ 0:02; d:f: ¼ 2; NS). As this could be because animals usually switch to another structure before 75% of the first one is consumed, we repeated the same analysis on the choices recorded during the first min of the trial. Here, in the double-choice trials, preference was higher for FS relative to BT (61%–39%, different from 50%– 50%; w2 ¼ 4:84; d:f: ¼ 1; P < 0:05) and for N relative to BT (62%–38%;w2 ¼ 5:76; P < 0:05), but similar between FS and N (57%–43%; w2 ¼ 1:96; NS). In the triple-choice trials, preference for FS (44%), N (24%) and BT (32%) differed from 33%–33%–33% (w2 ¼ 6:09; d:f: ¼ 2; P < 0:05).
4. Discussion In the first experiment we showed that red deer prefer to browse at the level of their shoulder height,
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and this despite the fact that the animals’ intake rate remained constant between foliage heights. Roe deer also have a preferred browsing height of around 75 cm (Duncan et al., 1998), near their mean shoulder height (63–74 cm; Whitehead, 1993). Gill (1992) suggested that deer usually browse at an intermediate level between ground and full reach. Saint-Andrieux et al. (1999) found that browsing pressure by red deer is more intense between 90 and 130 cm height. The positive relationship between average consumption height and individuals’ shoulder height, observed in experiment 1, indicates that the effect of animal size on preferred browsing height should also occur within species, between individuals of different size. As this cannot be explained by differences in intake rates, the preference for foliage at shoulder height could be related to a postural benefit leading to lower postural cost at this level compared to a browsing position with head and neck raised or lowered. This suggests not only that biokinetic factors influence foraging decisions, as was assumed by Jiang and Hudson (1993), but also that they are sufficient to induce preferences even without intake rate maximisation. This relation between preferences and plant height could also be used in a management perspective to construct damage indicators. Through a regular survey of browsing signs on height classes of selected plants within or surrounding the commercial strands, this indicator could clearly show any increasing browsing pressure before damages on less preferred but commercially used saplings becomes too excessive. Webster et al. (2001) have proposed a similar approach using the mean height of three preferred herbaceous species to quantify the level of damage on the overall ground layer vegetation. It allowed them to successfully evaluate impact of white-tailed deer (Odocoileus virginianus) on forest plant communities before lasting damages occurred. In the second experiment, we observed a slight but regular preference for FS, i.e. for the structure where all bunches (laterals and apical) were widely spaced at hinds’ preferred height. We expected this preference for the structure allowing the greater intake rate. Intake rate on FS bunches was however only 7% higher than on the two others structures. An optimal behaviour would be to choose the FS structure first and then, to quickly switch to another structure as intake rates became similar, so as to eat a mix of every structure during the rest of the trial.
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This would result in a slight preference for FS relative to the other structures, consistent with what has been observed during the first min. This choice thus followed OFT predictions. Although this difference in intake rate is statistically significant, it is also likely that it was too small to be perceived by animals. Indeed, in previous patch choice trials with sheep (Dumont et al., 1998) and goat (Illius et al., 1999), animals expressed highly variable preferences when the two alternatives were similar in energy or DM intake rates, whereas choices were systematically made in favour of the better alternative when they were of clearly different value, i.e. different by at least 50%. Similarly, here, deer probably did not discriminate between the offered alternatives on the basis of differences in intake rate. Animals rather selected structures on the basis of their architecture, e.g. preferring that structure with the lowest vertical dispersion of biomass around the preferred consumption height. As a consequence, apical buds of N and BT saplings were not attacked during the first min in 60 and 77% of double-choice trials and in 83 and 80% of the triple-choice ones. Thus, an animal moving across a commercial plantation should have a lower impact on buds of major importance for sapling growth as soon as these buds are higher than the deer’s preferred browsing height. 5. Conclusion Red deer have a preferred feeding height which is correlated with their shoulder height and which is independent of differences in intake rates between foliage heights. When offered the three sapling structures, red deer preferred the one where all bunches were widely spaced at their preferred height. Foliage height and, to a lesser extent, structure of saplings thus affect the feeding preferences of red deer. This knowledge can help in proposing management practices to limit their damages to commercial plantations, e.g. by indicating up to what height it is worthwhile protecting valuable saplings from deer browsing in order to avoid consumption of apical buds. Acknowledgements We greatly thank F. Anglard, B. Cargnelutti, N. Cebe, N. Chevallier-Redor and C. Mallet for their
excellent technical assistance and for their care of the animals. Ph. Ballon and D. Pe´ pin made useful comments on the experimental schedules. A.J.M. Hewison kindly revised the English version of the manuscript. We thank P. Duncan and another reviewer for useful comments on the manuscript. We are also grateful to the organising committee of the International Conference on Forest Dynamics and Ungulate Herbivory (Davos), which partly funded conference fees to present these results. We thank the INRA (HYFS and ENA department) for the thesis grant of P.C. Renaud.
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