Selection and Use of Feeding Sites and Feeding Stations by Herbivores: a Review Christine Roguet, Bertrand Dumont, Sophie Prache

Selection and use of feeding sites and feeding stations by herbivores: A review Christine Roguet, Bertrand Dumont, Sophie Prache

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Christine Roguet, Bertrand Dumont, Sophie Prache. Selection and use of feeding sites and feeding stations by herbivores: A review. Annales de zootechnie, INRA/EDP Sciences, 1998, 47 (4), pp.225- 244. hal-00889728

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Selection and use of feeding sites and feeding stations by herbivores: A review

Christine Rogueta Bertrand Dumontb Sophie Pracheb

il Station de recherche sur la vache laitière, Inra, Saint-Gilles, 35590 L’Hermitage, France b Laboratoire adaptation des herbivores aux milieux, Inra, Clermont-FerrandfTheix, 63122 Saint-Genès-Champanelle, France

(Received 13 October 1997; accepted 20 May 1998)

Abstract - A better understanding of the animal x plant interaction is needed to develop management practices which will maintain a sufficiently rich and abundant vegetation in the pastures. Such practices would permit the animals to meet their nutritional requirements, and to ensure a sufficient production, while contributing to the maintenance of the environment. This review, drawn on a large number of experimental studies, takes stock of the factors influencing the selection and use of feeding sites and stations by herbivores. First, we present the theoretical framework in which the experimental observations are discussed. The general context of optimal foraging theory (OFT) and its predictions are described. Its ’applicability’, usefulness and validity to study the foraging behaviour of herbivores are then discussed. Second, we analyse how forage (quantity and quality, plant species, distribution), environment (topography, distance to water, predator risk) and some animal factors (cognitive abilities, social organisation) affect the choice and use of feeding sites and stations. In spite of some pro- blems of definitions (’patch’, ’prey’ for an herbivore?) and of the herbivores’ specific characteristics, the OFT has been successfully used to explain the foraging behaviour of herbivores. However, animals’ choices are rarely as absolute as predicted. Under natural conditions, animals not only respond to food resource, but are also constrained by some non-alimentary environmental factors and by the limits of their cognitive abilities (memory, discrimination). Other complementary approaches, such as ’hedonism’ and ’nutritional wisdom’, can partly influence animals’ choices and are also briefly discussed. (© Elsevier / Inra) grazing / herbivores / diet selection / optimal foraging theory / feeding site / feeding station

Résumé - Sélection et utilisation des sites et stations alimentaires par les herbivores : Une revue. À terme, mieux comprendre la relation animal - végétation est nécessaire pour développer des systèmes de gestion qui favorisent le maintien par le pâturage d’une ressource suffisamment riche et abondante. Dans ces conditions, l’animal peut couvrir ses besoins nutritionnels et assurer une pro- ductivité suffisante, tout en participant à l’entretien du milieu. Cette revue fait le point, à partir d’un grand nombre de travaux expérimentaux, sur les facteurs qui influencent la sélection et l’utilisation

* Correspondence and reprints Tel.: (33) 02 99 28 50 86; fax: (33) 02 99 28 51 O1; e-mail: [email protected] des sites et stations alimentaires par les herbivores. La première partie est consacrée au cadre théo- rique dans lequel sont discutées les observations expérimentales. Le contexte général de la théorie de l’alimentation optimale (TAO), et ses prédictions, sont décrits. L’« applicabilité », l’utilité et la vali- dité des modèles d’optimisation dans l’étude du comportement alimentaire des herbivores sont tout particulièrement considérées. Ensuite, est étudiée l’influence des différents facteurs, trophiques (quantité et qualité des ressources fourragères, distribution des espèces végétales), environnementaux (topographie, distance aux points d’eau, présence d’abris et risques de prédation) et animaux (capa- cités cognitives et organisation sociale) sur la sélection et l’utilisation des sites et des stations alimentaires par les herbivores. En dépit de quelques problèmes de définitions (patch, proie pour un herbivore ?) et des caractéristiques spécifiques des espèces animales étudiées, la TAO a pu être appli- quée, avec succès, à l’étude des stratégies alimentaires des herbivores. Cependant, les choix ne sont en général pas aussi absolus que ceux prédits par la théorie, En conditions naturelles, les animaux répon- dent non seulement à la ressource alimentaire, mais aussi à différentes contraintes externes (environnement non alimentaire) et internes (mémoire, discrimination, etc.). D’autres approches com- plémentaires, telles l’« hédonisme » et la « sagesse nutritionnelle », susceptibles d’influencer les choix des animaux, sont aussi brièvement analysées. (@ Elsevier / Inra) pâturage / herbivores / sélection / station alimentaire / site alimentaire / alimentation optimale

1. INTRODUCTION Under harsh pasture conditions, intake and time per bite are the factors limiting the daily When grazing, an animal has both to intake of nutrients [53]. Through feeding search for and harvest its food. Its foragingg site selection, herbivores can increase their behaviour is affected by climatic, topogra- intake rate [21, 68]. However, when resources phic and predatory constraints. Forage cha- are very scattered or heterogeneous, pre- racteristics of habitats also influence the hension biting rate and intake rate can be spatial distribution of herbivores, their diet limited by the time to move between sites (intake, choice) and their impact on the envi- [127, 131 ]. ronment. A better understanding of the ani- More can be considered mal x vegetation interaction is needed to simply, grazing as the alternation of time’ develop management which will ’step-sets/moving practices between stations and of ’bite- maintain a rich and abundant feeding sufficiently time’ within stations vegetation in pastures. Such practices would sets/grazing feeding 134]. This breakdown makes permit the animals to meet their nutritional [52, 76, it possible to determine for each diet the relative and to ensure a sufficient pro- requirements contribution of station selection in duction, while contributing to the mainte- feeding the and of bite choice on the fee- nance of the environment. paddock ding station. In addition, some authors [10, The can be seen as the grazing process 63, 93, 125, 138] used this breakdown to result of a series of decisions taken the by define the idea of a ’feeding site’ for conti- animal at different levels spatio-temporal nuous resource situations. A ’feeding site’ is In the term, animals choose their [122]. long defined as ’a group of feeding locations loca- habitat and the time allocate to fora- they ted a short distance apart’. The distance bet- Within their habitat, select ’feed- ging. they ween feeding sites is then much longer. ing sites’ on which they choose and graze ’feeding stations’, i.e., the sward surface In this review, we analyse how trophic accessible to an animal without moving its (forage quantity and quality, plant species, forefeet [43]. Finally, they select bites within distribution), environmental (topography, a feeding station at the ’tussock’ level. distance to water, shelter, predator risk), and some animal (cognitive abilities, social orga- 2.2. Application to herbivores nisation) factors influence the choice and use of feeding sites and stations. Experi- OFT models were first developed on mental observations are discussed, particu- insects [ 14, 16, 51, 104], birds [15, 72, 74, larly in relation to optimal foraging theory 105, 126] and rodents [73]. These animals models. forage on ’preys’ of a high and relatively uniform nutritional value, concentrated in discrete ’patches’. The transfer of this theory to herbivore behaviour raises 2. THEORETICAL FRAMEWORK: foraging pro- blems of definitions is a or a OPTIMAL FORAGING THEORY (what ’patch’ ’prey’ for a herbivore?) and others related to the specific characteristics of herbivores 2.1. General context (digestion, cognitive abilities, social structure).). In the long term, a behaviour is said to The food resource herbivores exploit is be ’optimal’ when it enables the animal to generally continuous, making the definition maximise its contribution to the subsequent of a ’patch’ difficult. This is often conside- generation (’fitness’). This involves the red to be the major difficulty for testing opti- maximisation of survival and reproduction mal foraging predictions. A broad defini- probabilities. The optimal foraging theory tion of ’a patch’ is ’a surface which differs (OFT; [35, 75, 102, 107]) predicts the beha- from its surrounding with respect to its viour of animals when foraging. Conven- nature and its appearance’ [ 145]. According tional models maximise the net rate of to Pickett and White [95]: ’patch implies a energy gain. This currency, chosen a priori relative discrete spatial pattern, but does not largely on the basis of intuition, takes into establish any constraint on patch size, inter- account two major elements of the foraging nal homogeneity or discreteness’. In addi- activity: the energy in terms of benefit and tion, Forman and Godron [38] noted that: cost and the time [ 130]. Laca and Demment ’patches vary widely in size, shape, type, [70] considered this currency had the major heterogeneity and boundary characteristics’. limit that: ’it only took into account the Hence, patches have to be defined in relation nutritional and energetic consequences of to the animals and questions under study. feeding’. However, it seems very difficult Sih [124] defined ’patches’ as: &dquo;entities to construct a global optimisation model, which require search or pursuit time be- which would take into account all the com- tween periods of energy intake&dquo;. For herbi- promises an animal has to make between vores, this definition corresponds to food its different demands, while remaining func- resources that are reasonably long distances tional [88]. Mangel and Clark [79] develo- apart, i.e., to feeding sites or larger units of ped a class of unified behavioural models, selection. A feeding site can be small (a which included finding food, avoiding pre- single feeding station) or very broad (many dators and reproducing. They called it ’uni- stations). On continuous vegetation, and fied foraging theory’ because foraging is a especially on homogeneous ground covers, key behaviour for an animal, except during feeding sites are generally rare and large. hibernation and rut. But, the degree of rea- The animal grazes many feeding stations lism of their theory is severely constrained that are only short distances apart before it by its large computational demands [70]. starts (less frequently) a long walk towards Moreover, the aim of a model is not to per- a new feeding site. Conversely, the resources fectly imitate reality with thoroughly detai- can be distributed as very scattered indivi- led outputs, but to give general rules that dual feeding stations, either naturally (desert improve our understanding of behaviours. vegetation; [142] or artificially (mown or hand-constructed sward plates, trees in a cut time; c) patch resource availability does not paddock; [5, 10, 24, 68]. In this latter case, decrease during the time the animal spends feeding site identification is easier. in the patch; and d) ’fitness’ increases The nutritional value of herbivore food linearly with intake rate. resources is usually low and variable in time From these assumptions, the OFT predicts and space. Therefore, the time to harvest that an animal will spend all its time in the the nutrients that will make them meet their patch with the highest intake rate [73, 92]. can be a constraint. This requirements major However, is the time is limited the time allocated to other a) partly disproved by by limits in the discrimination capacities and activities, such as rumination, social resting, of herbivores. b) and c) seldom interactions, predator scanning, search for memory hold true in natural situations where vege- sexual partners, etc. In a changing environ- tation changes with time and animal ment, the animal also has to sample its on the resources to check their value and discover consumption patch progressively depletes it. At last, d) has never been confir- new foods. As herbivores eat long meals med for herbivores. If fitness is a non-linear during which they ingest numerous plant function of intake rate, or if it also species, it is difficult for them to sort out depends on a the choice the individual effects of each choice [26]. specific nutrient, optimal would be not to allocate all the time to a They express preferences between resources but rather to distribute it be- (plant species, plant parts with different fibre single patch, tween different sites and to allow time to contents), and make trade-offs between the quantity and quality of the food they ingest, sample the different alternatives [107]. both at the site and station levels (tall and 2.3.2. use mature sward vs. short and vegetative sward; Optimal patch [29]), and at the tussock level (stems vs. leaves; [96]). The classical model of optimal use of patchily distributed resources is the marginal value theorem An animal 2.3. Predictions (MVT; [17]). that seeks to maximise its intake rate will leave a patch when its marginal (i.e., ins- Pyke et al. [ 102] classified optimisation tantaneous) intake rate in that patch falls models into four groups, depending on whe- below the average intake rate in the habi- ther they predict, for an individual, (1 ) diet tat. The animal is assumed to have complete choice, (2) patch choice, (3) patch use, or of its environment and the pre- (4) movement. In this paper, we are inter- knowledge risk is assumed to be null. In addi- ested in the last three points. Other models datory tion, resource due to animal fora- such as the ideal free distribution (IFD; [39]) depletion decreases intake rate, and to a do not predict the distribution of the foraging moving new site is time and ging activity of an individual between the energy consuming. available resources, but how individuals in The MVT predicts: I) in an homoge- a population distribute themselves in the neous environment (a single patch type): i) habitat. the optimal grazing time per patch, from the intake curve on the patch and the moving 2.3.1. Optimal patch choice time between patches. Patch grazing time increases with patch value (figure la); ii) the Initial optimal patch choice models relationship between optimal grazing time involve the following assumptions [ 107]:] : per patch and moving time between patches. a) animal has complete knowledge of the Grazing time per patch increases with moving location and value of each patch; b) patch time between patches (figure Ib); 2) in an location and value remain constant over heterogeneous environment: patches are gra- 2.3.3. Optimal movement

Optimising movement implies walking a minimal distance between the selected patches. This problem (’travelling salesman problem’; [ 1 ]) is so difficult to solve ((n-1)!I alternatives for n patches) that an animal is unlikely to find the optimal solution. The most efficient suboptimal solution consists of walking to the nearest preferred patch (’nearest neighbour rule’; [104, 133]). Be- tween patches, an animal walks in a straight line to avoid repeated use of the same patches (’directionality’; [103, 106]). Within the patch, it increases its travel sinuosity (i.e., shows klinokinesis) and reduces its walking speed (i.e., shows orthokinesis) when a ’prey’ (rewarding feeding station) has been found in the hope that some others may be close by (’area-restricted searching’; [ 103]).

2.3.4. Animals’ optimal distribution in the habitat: ’habitat matching’

Ideal free distribution (IFD; [39]) predicts the optimal distribution of individuals among the different patches of their habitat. The different hypotheses are as follows: a) individuals seek to maximise their feeding efficiency (energy gain/cost); b) they have complete knowledge of their environment (’Ideal’); c) they undergo no constraint to choose their sites (’Free’); d) they have equal competitive abilities; e) intake per animal decreases when the number of animals in the patch increases; and f) distance between patches does not significantly affect animal distribution.

In this case, the IFD predicts that the proportion of animals in a patch will be equal to the proportion of resources in this patch. This relationship is also called ’habitat matching’. Once again, assumption (b) comes up zed up to the same marginal value of intake against the limits of animals’ spatial rate intake rate of the Ani- (average habitat). memory. Group living is contrary to (c). mals will a rich than a graze patch longer Moreover, contrary to (d), animals do com- poor one (figure I c). pete with each other and they do not have equal competitive abilities [56]. Finally, taller in 68% of the tests). However, they movement between patches (f) generally grazed the taller patch more intensely [59]. cannot be considered as insignificant. Similarly, Vivas and Saether [137] (moose), Moving costs and gregariousness may and Distel et al. [24] (cattle) showed that induce ’overmatching’ (overexploitation of these animals did not visit the rich patches in the rich patches), whereas difficulties in dis- the habitat more frequently, but that the gra- criminating patch value and limits in spa- zing intensity on each patch (grazing time, tial memory may lead to ’undermatching’ intake) was positively related to the patch (overexploitation of the poor patches) [64]. richness (figure 2). In these cases, use of the expression ’selective use’ rather than ‘selection’, would be more appropriate. 3. INFLUENCE OF FOOD Herbivores choose and use their feeding RESOURCES sites according to their nutritional value and their distribution in the habitat (distance, Currently, the expression ’selection of aggregation; figure 3). Patch nutritional site S’ is often used to indicate the result of value depends on its resource quantity (bio- two distinct phenomena: 1 ) the animal pre- mass), structure (height, density), quality fers to visit the site S (number of visits); (digestibility, nitrogen and secondary com- and/or 2) at each visit, it exploits the site pound content) and nature (plant species). more intensely (grazing time, bite number, The amount of contrast between different intake). For example, selection of tall sward patches defines their relative interest. Aggre- patches by ewes (between two possibilities: gation level modifies moving constraints 12 vs. 7 cm) did not result from a higher and influences the relative use of the diffe- number of visits as the animals visited both rent patches. At the feeding station level, plates in turn (after they had first grazed the factors affecting grazing decisions seem to be less clear. We will discuss the reasons Herbivores do not seem to be able to esti- for this, and present some hypotheses and mate intake rate a priori. To select their feed- conclusions. ing sites, they rely on intake rate cues such as sward height [21, 59, 68] and to a lesser extent density, a factor that is more diffi- 3.1. Influence of patch nutritional value cult to estimate visually [10]. Illius et al. [59] observed that intake rate differences 3.1.1. Herbivores choose sites between two sward plates explained only with the highest intake rate 18% of the intake distribution variance, whereas differences in sward height and clover In agreement with OFT predictions, ani- content explained 60%. Brightness also indi- mals generally select feeding sites that per- cates nitrogen rich patches [10]. Finally, mit them to have the highest intake rate. herbivores use information gained when When offered two plates with structurally grazing sites to reinforce the exploitation of different swards (height and density), sheep the more profitable sites [24, 59].]. usually prefer the sward they can eat faster Dietary preferences also influence patch [13, 59]. Intake rate depends on patch choice and partly explain diet selection. resource availability, but also on ease of However, these may be subordinate to the prehension. For herbivores, ease of prehen- instantaneous intake rate maximisation pro- sion may be related to sward structure (den- cess: offered a choice between five sity, height) and fibre characteristics (resis- goats sward species (in pairs on plates at the same tance to shearing; [57, 97]). sward height) selected a diet which tended to maximise their instantaneous intake rate rather than expressing a preference for some of the plant species [60]. Similarly, under natural grazing situations, cattle, horses, and deer, all selected a diet that mainly included plant species with the highest organic mat- ter intake rate (cattle 58%, horses 52%, deer 72%) [ 136]. The remaining proportion see- med to indicate that OM intake rate maximisation was not the only rule involved.

In general, the quality of food resources varies inversely with the quantity. For example, a mature sward is tall but of low nutritional value, whereas a vegetative sward is short but of high nutritional value. Hence herbivores have to make a compromise between intake rate over the short term and food processing rate over the longer term [86, 139, 147, 148]. Wilmshurst et al. [ 148] offered wapitis regrowths of 2, 4, 6, 8 and 100 weeks that each covered 20% of a paddock area. Wapitis preferentially used (30% of grazing time) the patches with medium biomass and quality (4-week regrowth) rather than the 2-week patches (better quality but low availability; 2% of grazing time) or the 6, 8 and 10-week patches (higher availabi- 3.1.2. Herbivores express matching lity but lower quality; 26%, 24%, and 18% patterns in their choices of grazing time). Wallis de Vries and Dale- boudt [1391 observed that cattle selected Herbivores’ choices are indeed generally mature feeding sites only when the exclusive not as absolute as predicted by the OFT. use of short vegetative patches did not allow Herbivores often match the time they spend them to fulfil their daily requirements in a in an area with the resources found there. restricted time. Similarly, sheep and cattle An animal can graze the different alterna- progressively switched to less preferred food tives in proportion to their relative value resources (reproductive sward strip at pas- (’strict matching’). It can also overexploit ture or bad hay indoors) when their prefer- the rich patches (’overmatching’) or, on the red forage (vegetative sward strip at pasture contrary, underexploit them (’undermat- Predictive of or good hay indoors) became less accessible ching’) [71, 122]. equations [28, 29]. population distribution in the habitat can be adapted to predict the distribution of an indi- Selection of the most profitable patches is vidual’s foraging behaviour between its food even more apparent when there is a high resources (table n. of contrast between degree patches [ 139]. Behaviours related to ’matching’ have For example, when foraging on 16 patches been frequently observed in various herbi- in line 1.2 (sward plates) presented every m, vore species: moose [92, 137], wapiti [71, with a mean sward of 10 cattle height cm, 148], sheep [59, 60] and cattle [24]. In gene- chose the tallest ones when dif- only height ral, these behaviours are explained by the ference was large, 15 vs. 5 cm (figure 4). need for a regular sampling to update the Conversely, they partly switched to the less values of the different patches in a complex profitable patches when contrast was redu- and changing environment, i.e., an adapta- ced ( 12.5 vs. 7.5 cm) thereby decreasing tion over the middle rather than the short selection profit [68], while increasing dis- term [126], or more simply as an imprecise crimination difficulty [ 139]. discrimination of patch value [60, 147, 148]. Matching was also related to the ’recognition times observed (To, s) by Laca et al. [68] time’ necessary for the animal to assess a were close to the quantitative prediction patch value when entering it [107]. Fur- (Tp, s) of the MVT, in particular for long thermore, it could simply result from the grazing times (To = 7.7 (± 3.61) + 0.9 (± 0.09) decrease in the value of the high quality Tp, r2 = 0.89). The compensation for the patches when exploited that leads animals to increased distance between patches by an switch progressively to initially less profi- increase in intake per patch may be more table ones [50]. Finally, when the high qua- than complete [21 ]. In practice, for the same lity patches are scatterly distributed, ani- biomass per hectare, a heterogeneous food mals can take advantage of poor quality distribution seems to be more profitable in patches while walking to a richer patch. terms of intake per selective animal than a more homogeneous distribution. On continuous rules 3.2. Effect of the spatial distribution preferred vegetation, of movement are of little as the of the feeding sites in the habitat importance encounter rate with the food resource is not 3.2.1. Movement constraints a limiting factor [127, 142]. When these resources are abundant, high intake rates allow animals to allocate more time to In order to maximise its intake a rate, search for preferred feeding sites. Animals herbivore has to make a trade-off between can also masticate large bites while walkingg ’to stay in a patch whose food availability is long distances. Nevertheless, animals tend to and ’to move to a richer decreasing’ patch’, limit the distances travelled. When foraging i.e., between intake rate depression due to on hand-constructed patches of alfalfa plants food depletion on the patch, and intake rate set in a very short pasture, bighorn sheep reduction due to moving time [69]. typically moved from one plant to the nea- When the moving time between sites rest one (75% of the moves), or to one of increases, this compromise results in a more the three nearest (90% of the moves; [48]).). intense site exploitation [L0, 21, 68, 114, The ’nearest neighbour rule’ seems to apply 123] (see figure 4), as predicted by intake when the animal can see the available rate maximisation models [17]. The grazing patches and when they are of equal value. When sites are more distant, some models in the 12-site treatment. Strong patch aggre- assume that the animal uses its memory to gation in the habitat and the subsequent move directly to the preferred patches [133]. overgrazing of these aggregated resources The animal may also choose to move at ran- has a double disadvantage: 1 ) for the ani- dom until it encounters an interesting site mal a strong reduction in the availability of [113]. its preferred species; and 2) for the plant a to survive when In heterogeneous pastures, patch choice difficulty heavily grazed can considerably increase distance travel- [31 ]. led [131]. Animals usually compensate for moving time constraint by walking faster 3.3. station choice and use [3, 30, 94, 112, 123, 127]. They can also Feeding partly switch to less preferred patches [28, within feeding sites 42]. For example, ewes increased the time Factors decisions and spent eating a poor quality hay available ad affecting foraging assessment of costs and benefits are to libitum when the distance to walk for a good likely hay offered in limited quantities increased apply at every level, from habitat to bite selection the finer the [30]. In fact, preference for a good hay was [67]. However, scale, the smaller the associated costs and bene- the same when 2 Q g of good hay rewarded and the harder are to a 46 m walk as when Q g of good hay rewar- fits, they probably ded a 23 m walk. The decision to move was assess by the animal. Indeed, ’there is evidence from not related to the absolute value of a patch operant conditioning experi- but rather to its procurement cost, i.e., the ment that the marginal value of many be- ratio of reward to distance. When model- haviour declines with increasing rate of behaviour’ Within a the bene- ling the foraging behaviour of moose, Roese [129]. patch, fit of a which et al. [113] successfully used a similar move- selecting given feeding station, ment rule: animals assessed the profitabi- would necessitate to gain sufficient infor- is small in lity of each tree based on edible biomass mation, relatively comparison and distance to the plant. with a more random search [140], particularly as the short travels between stations 3.2.2. Effect of site distribution type make it possible to quickly correct a selec- (random, uniform, aggregated) tion ’error’. The high number of stations within a site, their small size, the small differences in their resources that the Clarke et al. [ 18] studied how sheep and imply animal would have to make a considerable deer used a preferred Agrostis/fescue sward effort to discriminate their relative distributed either as 1 large, 4 medium or profits. it is for him to 12 small sites within a moorland pasture. Furthermore, impossible remember the location of so For each distribution, the sward represen- precise many alternatives in the habitat. ted 20% of pasture area. Sward distribution did not affect the choice of deer but influen- Arditi and Dacorogna [2, 3], and later ced that of sheep. The more the grass was Focardi et al. [36] proposed the existence dispersed, the more the ewes grazed the hea- of a critical biomass (threshold) per station, ther: 9, 25 and 43% of foraging time for the that could be used to distinguish selected 1, 4 and 12 grass-site treatments. This switch from refused stations. An animal foraging on to heather was attributed to an increase in a continuous food resource would graze a border zone. Sheep also encountered more station along its foraging path if the bio- frequently heather when moving between mass available at this point is above this grass patches. Due to the faster resource threshold, and would go on walking if it is depletion of the small compared to the large below. The acceptance threshold would be grass sites, these moves were more frequent influenced by recent experience (encounter with a high/low quality station raises/lowers 3.4. Conclusion this threshold), and by the satiation level of the animal [122]. Most studies show that herbivores’ responses to the dietary constraints of their The use of intake rate in the decision to environment are in agreement with the qua- abandon a feeding station [17] is made dif- litative predictions of intake rate maximi- ficult by two cumulative phenomena: 1 ) as sation models. For instance, grazing time the distances between stations are often very per site increases with site value and/or dis- short, the residual effect of the grazing rate tance between sites. However, animals’ at the previous station may affect the intake choices are rarely as absolute as predicted by rate estimation at the subsequent station; OFT models. In general, animals express and 2) this residual effect is even stronger partial preferences. when the feeding station residence time and Quantitatively, most of the few experi- intake during a visit are small, and may pre- ments [5, 10, 15, 24, 110] showed large dif- vent the animal from experiencing an intake ferences between observations and OFT pre- rate depression [59]. Senft et al. [122] sug- dictions. Three reasons are usually proposed: gested that, within a site, diet selection was 1) The precise determination of the patch an ’instantaneous maximisation’ process that and station values in terms of intake rate would dictate sequential acceptance of the and of the gain curves is particularly difficult more palatable food items encountered at even under controlled conditions [60]. But, each station, probably until palatability drop- the shape of these gain curves has a very ped below a certain level. The animal would strong effect on the optimal grazing time stop grazing on a station when most of the [5, 24]. green forage had been fully consumed [ 131]. 2) The OFT is based on strong assump- It would be interesting to determine if the tions that are not realistic for herbivores feeding station departure ’rule’ is an absolute (e.g., a complete knowledge of the envi- threshold (residual biomass or sward height) ronment). Moreover, the time scale on which or a relative one, i.e., an almost constant this theory applies has yet to be defined. proportion of available biomass [65, 137], Wallis de Vries and Daleboudt [139] sug- sward height or green leaf mass. Whatever gested that herbivores maximised energy the rules used by an animal, the thresholds intake not on an instantaneous scale but are reached later on rich stations than on rather on a daily basis. It may, therefore, be to model poor stations: hence grazing time per sta- impossible validate optimisation short duration tests. How- tion (and intake) increases with resource predictions using availability in the feeding station [34, 89, ever, the longer the time scale, the more dif- 111, 112, 115, 118, 123]. ficult to predict the quantity and quality of resources. Hence, it is also unlikely that Jiang and Hudson [63] showed that nei- decisions about patch choice are taken on a scale than a few ther a given bite number, nor a given grazing longer days [141].]. time, nor the prehension biting rate decrease 3) Animal decisions about patch choice (below the mean value for the season) were and use are not only influenced by food fac- used as feeding station departure rules by tors, but also by their non-alimentary envi- wapiti. The unique indication was the neck ronment and their own characteristics. This angle, almost constant when the animal left is what we will discuss in the next sections. a station, which for the authors suggested The usefulness of the OFT is yet not dis- the important role played by biokinetic fac- credited for the study of herbivore foraging tors in this decision. Intake rate was not tes- behaviour [59, 70, 136, 147]. Rather its pre- ted as option in their study. dictions should be considered as references against which to compare the behaviour of and horses avoid slopes above 30 and 50%, animals in various situations. Differences respectively [41]. Topography also offers between the observed and predicted values shelter against bad weather and predators will generate new assumptions which can [117]: lactating bighorn ewes prefer the then be integrated into the models and, by habitats that cannot be reached by predators ’iteration’, improve our understanding of [I I], and the goral, an Himalayan goat, rea- foraging rules [93]. dily chooses steep slopes above 30 degrees [82]. The degree of habitat openness dic- tates the presence or absence of some animal 4. INFLUENCE OF THE NON- species: gregarious ungulates avoid wood- ALIMENTARY ENVIRONMENT lands [98] where flock movements and visual contacts are more difficult [62]. The microclimate influences selection and Patch value is related to forage quantity patch and quality, i.e., the ’site forage value’, but movements [121]. Antelopes prefer areas sheltered from strong winds and warmed also to abiotic factors such as predator risks, the sun because winds distance to water, shelter, micro-climate and by [ 116] strong may limit topography that determine the ’perceived movements [9]. (global) site value’ [8]. Predator risks limit intake rate maximi- 5. INFLUENCE OF ANIMAL sation via: 1) a time/energy cost of vigi- CHARACTERISTICS lance, which can be important: 2 to 95% of foraging time for ungulates [ 134]; and 2) a Herbivores are influenced by some cha- loss in accuracy when discriminating be- racteristics and state variables in their fora- tween different sites, as an animal’s ability to ging decisions. These have been reviewed in deal simultaneously with several pieces of numerous papers [26, 27]: 1) body-size [45, information is limited [25]. The trade-off 62]; 2) abilities related to body-size: diges- between intake rate maximisation and pre- tion, selection and walk [20, 22, 44, 45, 54, dator risk minimisation has been widely stu- 58, 91]; 3) dietary preferences [27, 84, 94]; died in other species than herbivores (for 4) feeding motivation and physiological reviews see [77, 83]). It has been shown that state [29, 31, 47, 85]. Patch selection also a risky patch had to contain between 8 [66] implies that the animal is able to discrimi- (rodents) and 25 [87] (ants) times more food nate the relative value of patches. An animal than a safe patch to be considered of equal has also to remember the location of the pre- value. For a ruminant, the optimal strategy ferred patches in order to return to them. may consist in selecting sward covers that We will now focus on these cognitive abi- allow the highest intake rate even if their lities and on social behaviour, because these quality is poor. The animal can then watch factors have been less thoroughly reviewed for predators when ruminating [86]. Preda- [70]. tor risks also modify patch use. Ibex exploited patches with a high predator risk less intensely than safe patches: they consumed 25 5.1. Cognitive abilities vs. 45% of food resources, respectively [65]. Water location strongly influences feed- Cognitive abilities include perception, ing site choice, under both dry [146] and discrimination, learning and memory capa- temperate conditions [49, 61 ]. Topography city that enable an animal to adapt to its environment. imposes a physical barrier to movement [117]. Slopes increase the time and energy Laca et al. [68] observed that cattle fora- required to walk a given distance. Cattle ging on heterogeneous sward covers were able to distinguish feeding stations that dif- ferred food patches and to sample the fered from their surroundings by less than various alternatives. Edwards et al. [32] sho- 5 cm in height. Illius et al. [59] showed that wed that sheep were able to learn and to patch selection by sheep foraging on two remember the location of four full bowls sward plates was affected by clover content within 32 bowls in a 30 x 45 m2 paddock. In differences (tested factor), but also by sward addition, sheep learned the bowl locations height differences shorter than 2.7 cm. Yet, more quickly when these were associated Wilmhurst et al. [148] and Illius et al. [60] with a proximal cue [32, 33]. the limita- explained partial preferences by We can two of tions in the animal’s discrimination distinguish types memory: ability. ’reference least 20 for et al. constructed a habitat memory’(at days Spencer [ 128] which enables animals to selection model that took into account the ungulates), remember a location and value for a differences between animals’ abilities to dis- patch and least criminate values. showed that long period, ’working memory’ (at patches’ They 8 h for in which are stored the animals which were sensitive to differences ungulates) that were [6-8]. between patch values concentrated in the patches recently depleted may be ’selective’, in that the poor more Memory profitable patches. patches would be forgotten less rapidly than An animal’s experiences in the young the rich ones because large herbivores are sensitive to the conse- age (learning with its mother) and over the particularly negative course of its life (acquisition of feeding quences of their choices [6, 46, 55]. In a habits) influence its foraging behaviour. risk-limiting strategy, they would try to Four weeks after weaning, lambs preferred maximise the possibility of avoiding a net plant species they had consumed with their loss [109]. Some patch choice models inte- of locations mothers before or during weaning [ 108]. grate the memory patch [8, 37, Dietary imprinting is particularly strong 117]. during the transformation of the young rumi- Animals’ limits in collecting, analysing nant’s digestive tract [23, 99]. Young ani- and processing information [ 109] force them mals can habits that influence acquire dietary to use simple ’rules-of-thumb’ to help them their behaviour for a foraging long period. to select and abandon their feeding sites For even after 4 in example, years common, (e.g., choose the nearest, greenest and tallest goats foraging on a tropical savannah selec- patch). Indeed, the potential relative increase ted a diet that was still influenced their by in feeding efficiency with a more complete environment after original [ 12]. Conversely, information would not make up for the 3-4 weeks, the of lambs for a preference time/energy required to process it [48, 140]. plant species they used to graze was not any Milinski [81 ] even showed that feeding effi- than that of lambs higher inexperienced ciency could be reduced by an information on the same In this foraging pasture [90]. overload and by the weariness and poten- case, the feeding habits of the test group had tial mistakes that could result from it. probably not become an integral part of their foraging behaviour for a sufficiently long time. 5.2. Influence of social organisation The use of spatial memory for returning to preferred food patches has been demons- The influence of social factors on indi- trated in many species: squirrels [73], tits vidual’s choice increases when the study [19], deer [42], cattle [6, 7], sheep [32]. It scale widens (from tussock to habitat). At increases an animal’s efficiency when the ’tussock’ level, bite characteristics (geo- exploiting habitat resources [42], by decrea- metry, weight, quality) are only slightly sing the time necessary to search for pre- affected by the presence of congeners. Young red deer have yet a lower prehen- ferred patches. Conversely, in newly consti- sion biting rate when they forage near a tuted groups, animals would move away to dominant animal, whereas it remains unchan- reach preferred feeding sites. The result of ged near a subordinate [ 132]. Group attrac- the conflict between social and feeding moti- tion and movements influence the distances vations not only depends on the strength of travelled by individual animals [93] and also relations between individuals in the group, feeding station choice and use. An animal but also on their knowledge of the environ- may graze a station longer if the surroun- ment. In a new environment, lambs are ding ones are not free [ 10], or it may be dri- strongly influenced by congeners’ location ven out of a station by a dominant animal. to choose their feeding sites. In a familiar There may be conflicting demands between environment, they will more readily express staying in the group and moving away to their preferences [120]. reach a preferred site. Scott et al. [ 119] enables animals to mini- observed that in groups of animals reared Group foraging mise risks and to take since their social attrac- predator [40, 62] together young age, of in tion was stronger than the attraction for pre- advantage congeners’ past experience locating sites and determining their value [78, 135, 149]. Gregariousness also has a cost in terms of exploitative and interference competition, aggressiveness, judgement mistakes by the ’leader’. Wallis de Vries [141] modelled the effect of group size on the number of patches visited and distance travelled per day and per cow in a 100-site environment. When group size increased, patch resource depletion was faster. Conse- quently, the animals moved more frequently and had to walk a longer distance to meet their nutritional requirements (figure 5a). Above a given number of individuals in the group, depletion of available resources per individual strongly hindered weight gain during the 100-day simulation (figure 5b). Fritz and de Garine-Wichatitsky [40] showed that antelopes selected their patches (bushes) according to the biomass of the accessible leaves but also to the number of animals in their group. They anticipated the consequences of feeding competition by selecting patches whose value was propor- tional to group size. Hence, group size is a factor to consider for understanding how an individual perceives patch value.

6. CONCLUSION

Herbivore foraging behaviour can be divided into a series of decisions that direct animals to a habitat where they choose and exploit feeding sites, feeding stations and reaches an equilibrium, for example between bites. These decisions are influenced by a rich but risky patch and a poor but safe numerous factors including food characte- patch (or a rich but distant patch compared ristics, the abiotic environment and animal to a poor but close patch) [66]. In all cases, factors (table I!. The effect of non-alimen- feeding efficiency remains the primary goal of selection and use tary factors on habitat use depends on the patch [7 1 ]. type of animal (domestic/wild), its envi- Optimal foraging theory seems to be a ronment (temperate/tropical), and its social valid approach to study resource exploitation organisation (more or less gregarious). Ani- by herbivores. In controlled situations invol- mals have to make trade-offs, in particular ving simple choices, with a minimum of between intake and predator risks, between constraints, animals tend to exploit patches that enable them to maximise their intake quantity and quality, etc. As in a chemical equilibrium, the relative importance of the rate. different factors could be estimated by deter- Other determinants of foraging behaviour mining at which moment feeding activity can also be reported. Animals may not seek to optimise, but remain content with satis- [3] Arditi R., Dacorogna B., Optimal foraging on their minimal for survival arbitrary food distribution and the definition of fying requirement habitat patches, Am. Nat. 131 ( 1988) 837-846. and in when these reproduction, particular )4jJ Armstrong H.M., Predicting the effects of large needs are low [88]. ’Optimal’ or ‘satisfying’, herbivores on hill vegetation in the UK. The art animal choices are also certainly influen- and graph of modelling in applied biology, Asp. ced by the pleasant feelings eating produces Appl. Biol. 26 (1991) 217-220. [51] Astr6m M., Lundberg P., Danell K., Partial prey (gustative, olfactory, or tactile) [100]. Dif- consumption by browsers: trees as patches, J. ficult to quantify, hedonism (the search for Anim. Ecol. 59 ( 1990) 287-300. pleasant feelings) probably has a slighter t6] Bailey D.W., Rittenhouse L.R., Hart R.H., influence on patch selection (the animal may Richards R.W., Characteristics of spatial still remember the location of the most memory in cattle, Appl. Anim. Behav. Sci. 23 ’plea- ( 1989) 331-340. sant’ than on use grazing patches) patch t7l Bailey D.W., Rittenhouse L.R., Hart R.H., (selection of green leaves, of particular plant Swift D.M., Richards R.W., Association of rela- species, etc.). Herbivores also seem able, in tive food availabilities and locations by cattle, J. 42 480-482. a innate (euphagia, [100]) and/or learned Range Manag. (1989) of effects of food 181 Bailey D.W., Gross J.E., Laca E.A., Ritten- (learning post-ingestive house L.R., Coughenour M.B., Swift D.M., Sims item choices, [101]) manner, to determine P.L., Mechanisms that result in large herbivore the nutritional (sodium, phosphorus, pro- grazing distribution patterns, J. Range Manage teins, etc.) and toxic (tannins, cyanogens, 49 (1996) 387-397. etc.) characteristics of the !9![ Bao J., Giller P.S., Kett J. J., The effect of mik plants they ingest. level on behaviour of friesian In this selection could be production grazing case, patch partly cows under valuable pasture conditions, Irish J. attributed to the desire to ingest a balanced Agric. 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