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Pronghorn foraging economy and predator avoidance in a desert ecosystem: Implications for the convertion of large mammalian herbivores
Biological Conservation 25 (1983) 193-208
Pronghorn Foraging Economy and Predator Avoidance in a Desert Ecosystem: Implications for the Conservation of Large Mammalian Herbivores Joel Berger Smithsonian Research Associate, Granite Range Field Project, Gerlach, Nevada 89412, USA
Dennis Daneke,* Jim J o h n s o n t & Stephen H. Berwick* * HDR Sciences, 804 Anacapa St., Santa Barbara, California 93101, USA t Department of Wildlife and Fisheries Biology, University of California, Davis, California, USA
ABSTRACT Assumptions of optimal foraging theory were applied to the feeding ecology of pronghorn Antilocapra americana to address issues of immediate relevance to conservation biology in the Great Basin Desert of North America. The relationships between foraging efficiency and." (1) group size; (2) habitat; and (3) disturbance history were examined in two study sites. Individual foraging efficiency increased with group size to a point in both study sites, but animals in the disturbed area remained in larger groups despite foraging less profitably. The hypothesis that individuals in a disturbed environment remain together for enhanced protection from (human ?) predators was supported and interpreted in the light of proposed habitat alterations in vast portions of this unique desert ecosystem.
INTRODUCTION 'Since man is creating disturbances in most ecosystems now, it is imperative that we learn to predict their impact, and the likelihood that they will shift the system's equilibrium.' (Sinclair, 1979) 193
Biol. Conserv. 0006-3207/83/0025-0193/$03.00 England, 1983. Printed in Great Britain
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Progress in habitat preservation during the past decade has resulted from the application of basic biological thought (Soul6 & Wilcox, 1980; Frankel & Soul6, 1981), such as the theory of 'insular ecology' (MacArthur & Wilson, 1967; Terborgh, 1974, 1976; Diamond, 1975, 1976) to entire ecosystems. In this paper we apply two additional ecological concepts--optimal foraging theory and antipredator grouping behaviour--to the conservation of large mammalian herbivores. Specifically, these topics are integrated so that a broader understanding of the changes in the spatial and foraging ecology of a species confronted with local extirpation may be predicted. Recent studies of optimal foraging (Schoener, 1971; Pulliam, 1974, 1980; Pyke et al., 1977; Belovsky, 1978) have yielded empirical data on optimisation processes, social foraging, and vigilance (Berger, 1978; Hoogland, 1979; Bertram, 1980; Lipetz, 1980). Clearly, our knowledge of these related events has progressed sufficiently so that it may now be applied to problems in biological conservation. Assuming, as theory suggests (see above references), that animals maximise their reproductive fitness by compromising their foraging activities with predator surveillance, the extent to which behavioural responses mediate extrinsic disturbances and are governed by ecological factors should be detectable. If individuals or populations differ in foraging and anti-predator strategies and the parameters responsible are known, wise mitigation in areas of animal-human interactions is possible. In many areas of western North America massive construction projects associated with mining or military defence are planned or currently underway. The Great Basin Desert of Nevada and Utah is one such area. This topographically diverse region is inhabited by a comparatively rich mammalian fauna including pronghorn Antilocapra americana (O'Gara, 1978), the sole extant species of ungulate endemic to North America. These highly selective feeders live in gregarious societies and exploit low desert shrub and grassland communities. To assess the potential responses of pronghorn to increased human activity associated with construction projects we evaluated social and ecological variables influencing foraging mechanics and determined how the juxtaposition of such variables affected anti-predator responses. Specifically, we asked: (1) to what extent is foraging behaviour influenced by the dispersion of food items and group sizes ? (2) how is foraging economy related to prior and current disturbances? and (3) what are the implications of optimal foraging models to the conservation of large mammalian herbivores ?
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C O N C E P T U A L M O D E L A N D CORROBORATIVE EVIDENCE It is necessary to develop a scenario depicting the most efficient methods of energy exploitation by individuals in any given environment. We concentrate here on large mammalian herbivores. An abundant literature indicates that movements and foraging aggregations are inextricably linked to food quality, dispersion, and productivity (Jarman, 1974; Owen-Smith, 1977, 1979; Geist, 1978), social organisation (Wilson, 1975; Crook et al., 1976; Berger, 1979a; Eisenberg, 1981), and predator pressures (Alexander, 1974). Consequently, we reasoned that behavioural measures of foraging animals reflect, in part, food quality and dispersion, a fact often documented (Jarman, 1974; Owen-Smith, 1979). Of central importance is the idea that animals maximise their energy intake and minimise its expenditure (Pyke et al., 1977). Given that other factors are equal, we assume: (1) animals ranging more widely than conspecifics do so because preferred food items are highly dispersed; (2) individuals switching from one p l a n t to the next more often than conspecifics do so because rates of energy decline to unprofitable levels ('the marginal value theorem' (Charnov, 1976)); (3) the number of paces taken during a standardised foraging bout indicates the relative distance between preferred food items simply because widely dispersed resources require more movement; and (4) the number of times a foraging animal moves to other food plants per unit time indicates relative food quality. Items (1) and (2) (above) introduce the ideas upon which this paper is based and (3) and (4) are the actual measures through which foraging is assessed. For example, consider two foraging pronghorn, A and B, feeding under ecological regimes differing only in the quality and dispersion of food items. A consumes morsels (designated as 'chew') from a single bush for 200 s, moves 5 paces (1 pace/s) without chewing, and immediately feeds on the next bush for 95 s. Thus, A fed for 295/300 s and interrupted non-mobile chewing only once to move to another plant. In contrast, B feeds for 5 s at a bush, moves to another food item that requires 45 paces (1 pace/s) and does not chew (hence no net gain in food accrued because mastication has not occurred), feeds at another bush for 5 s, moves an additional 45 paces again without chewing, and so forth until 300 s have elapsed. The chewing time per unit foraging period is greater in A than B because the former not only chewed longer but moved and interrupted chewing less frequently.
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With this example in mind, it is possible to identify and measure specific components of a foraging animal's time budget. The time allocated to securing energy (i.e. eating) and expending it (i.e. moving without chewing) provides a basis from which foraging effort can be assessed. Foraging effort is defined as the distance of walking movement associated with chewing or searching for food per unit time. It is indicated (Fig. 1) by
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the interplay of food quality (the independent variable) measured by the frequency of movements between food plants per unit time; and food dispersion (the dependent variable) measured by the mean number of paces per movement. According to this model, as foraging effort loci approach the origin in Fig. 1, food patch quality increases. These areas contain voluminous closely associated food items and the subsequent rate of energy expenditure is low because animals move relatively little. Conversely, animals expressing foraging effort further from the origin move more frequently and/or further per foraging bout. A multiplicative function of the two variables (xy) was avoided so that the effects of food quality and food dispersion could be separated.
METHODS Study sites Two study sites were established, each in Pine Valley, west central Utah (see Beale & Smith, 1970 for a more thorough description). The northern study site was located on the Desert Range Experiment Station, an area of about 130 km 2 of undisturbed habitat. We designated this the 'undisturbed' site (UND) because public access was restricted. The second study site was located about 20 km south in the same desert valley at the same altitude. This area was called the disturbed site (DIS) because public access was unrestricted and hunting, mining, and construction activities have occurred there, these latter two activities primarily during the past 6 years. We used the DIS as a representative example of an area where previously undisturbed animals were confronted with a new construction project. The densities of pronghorn and their natural predators were similar at both study sites. Animals were observed for about 800 h between July through October 1980. Definitions and rationale A 'foraging bout' was defined as a continuous 300-s period which commenced after pronghorn first ingested food. Time spent for allogrooming, elimination, and social interactions were subtracted from the
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300 s to restrict the analysis to only foraging and antipredator components. Foraging bouts included two general types of behaviour patterns, each concerning energy balance. Those relating directly to ingestion were designated 'energy enhancing activities' (EEAs) and included biting plants, masticating, ruminating, and searching for food. Searching occurred when an animal oriented its head toward the ground without chewing. The ratio of chew time per foraging bout measured mean 'foraging efficiency'. This measure is therefore a ratio based on time commitments to various activities and it does not imply caloric intake. The Foraging Effort Model (Fig. 1) is based solely on EEAs. Behaviours not directly associated with the pursuit of food were energy debits and called 'energy consuming activities' (ECAs). These included walking with the head in an upright position, scanning (i.e. standing with the head up), and alert postures (see Kitchen, 1974). 'Vigilance' was the time an animal spent with its head up per bout without chewing or walking. Anti-predator behaviours associated with flight were also quantified. 'Escape effort' (defined as the sum of the products of distance fled and speed) was determined. Distance fled was estimated visually by how far an animal moved when first disturbed until its next bite of food. Speed was estimated by using five gaits; (1)walk, (2) trot, (3) slow run or lope, (4) full run, and (5) maximum sprint. Piloerection of hair follicles on the rump and tendencies for pronghorn to clump together or remain dispersed were also recorded when 50 ~o or more of a group's members engaged in those behaviours. Data collection
The number of paces taken by focal animals and the times allocated to components of EEAs and ECAs were recorded for different sized groups. Observations from both study sites were based on at least 130 different animals and occurred just after sunrise or before dusk, periods when foraging activity was greatest. Data on males were excluded because part of the study occurred during the rut. Broad variability in foraging occurred since we sampled animals feeding under a wide range of ecological conditions. Our observations were indeed quite different from prior studies (cf Berger, 1978; Lipetz, 1980) of ungulate foraging ecology where sampling procedures were restricted to animals feeding in uniform habitats.
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Group sizes of foraging animals were lumped into categories to maintain sample size consistency. The position of an individual within a group was recorded as central or peripheral only when animals were clearly situated within such positions. Following the collection of foraging data, pronghorn were disturbed systematically on foot or by a moving vehicle. Our perturbations were standardised by: (1) walking toward the study animals from 400-800 m distant when pronghorn visibility was unobscured; and (2) driving slowly ( < 32 km h-1) along dirt roads beginning at distances 1.6 km or greater with visibility conditions as above. RESULTS Patch size and quality If the study sites differed in the distriiaution, size, or quality of food patches, then differences should be detectable in at least two parameters associated with social foraging: (1) group sizes, and (2) foraging effort. Although these parameters are not distinctly different, evidence concerning each are presented separately for the sake of clarity. The UND had both a significantly larger mean group size (X = 5.2, N = 199; p < 0.05; t Test) than the DIS 02, = 4-0, N = 258) and a greater proportion of larger groups (Fig. 2). This evidence suggests that the U N D was richer in food quality and/or had larger food patches than the DIS when only food resources were considered. Little is indicated pertaining to the mechanics of patch exploitation in groups of varying size from either site (see below). Differences in the quality (and indirectly size) of food patches should be reflected in foraging effort. This index was standardised between environments by holding EEA time constant and using absolute measures of distances (paces) and interruptions (frequency). If the U N D was indeed characterised by food patches of higher nutritional value than the DIS habitat and not simply by larger patches of equivalent food value, then individuals foraging in patches from the UND should expend less foraging effort. This appears not to be the case. The lack of significant differences in foraging effort between individuals in equal sized groups from each site suggests that patch quality did not differ between our two study sites. It therefore appears that larger groups in the U N D are explained by larger food patches than those located on the DIS.
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Furthermore, foraging effort increased with group size on the DIS (the differences between groups 1-2 and 5-7 were significant; p < 0-05; Fig. 1) whereas it was similar among all group sizes on the UND.
Foraging efficiency and predator surveillance Because animals in large groups tend to forage more efficiently than those in smaller groups (Berger, 1978), we hypothesised that pronghorn in the U N D would experience greater chew time/bout as mean group sizes were larger there. Overall, this prediction was supported. Average foraging efficiency per individual differed between study sites and approached statistical significance. In the U N D mean foraging efficiency per individual increased with group size and it attained the maximum for groups of 5-7 animals declining only slightly thereafter (Fig. 3). This slight decrease was attributed to peripheral animals which were significantly (p < 0.05) more vigilant than their centrally located conspecifics. In smaller groups this relationship was obscured possibly because of our inability in clearly assigning animals into a central versus peripheral dichotomy.
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The maximum foraging efficiency for DIS pronghorn occurred in groups of 3-4 animals and declined thereafter. When pronghorn in equal sized groups were compared between study sites, U N D animals in groups 5-7 or larger foraged significantly (p < 0.05) more efficiently than those from the DIS. With regard to vigilance, DIS pronghorn spent more time/bout scanning than did U N D animals (Fig. 3). Flight effort and perturbations No significant differences were noted in flight characteristics (see below) between large and small groups. Therefore, data were pooled and the
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responses of individuals from each study site compared. Those in the DIS expended approximately four times the escape effort (Fig. 4) than the UND animals (p < 0.001). Animals in the DIS also displayed heightened alarm responses as indicated by a greater percentage of clumped flights, more bouts with piloerected rumps, and delayed resumption of feeding (Fig. 4) when compared with UND pronghorn. DISCUSSION Group size determinants Enhanced reproductive success has been viewed correctly as the ultimate cause of social foraging (Alexander, 1974; Jarman, 1974; Pyke et al.,
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1977; Caraco, 1979a,b; Hoogland, 1979; Bertram, 1980) and it is achieved by foraging efficiently and avoiding predators. Here we consider the roles of habitats and predators in proximate causation only. The hypothesis that feeding group size in large herbivorous mammals is influenced more by resource levels than by immediate predator pressures is supported by two arguments. First, when disjunct populations from similar habitats differing in resource bases are compared and predator pressures are roughly equivalent (i.e. the same predators occur in equal numbers in each area), mean group size differences occur. Second, feeding group sizes vary seasonally with food availability despite constant predator pressures. Empirical data for bighorn sheep Ovis canadensis (Berger, 1979b), white-tailed deer Odocoileus virginianus (Hirth, 1977), red deer and tule elk Cervus e laphus; (McCuUough, 1969; Staines, 1974), impala Aepyceros melampus (Jarman & Jarman, 1979), topi Damaliscus korrigum (Jarman & Jarman, 1979), kudu Tragelaphus stresiteros (Owen-Smith, 1979), and wildebeest Connochaetes taurinus (Rodgers, 1977) support one or both of these relationships concerning group size and resource level. The problem, however, is deceptively more complex and many variables are involved in group size formation. For instance, Caraco (1979a,b) found that wintering juncos incurred energy debits due to thermoregulatory stress but counterbalanced them by enhanced foraging benefits in larger groups. In these groups vigilance decreased although an animal's social status also influenced harvesting rate, a relationship also noted for mule deer O. hemionus (D. Koutnik, pers. comm.). On our two study sites, the quality of food patches was apparently equivalent (see Fig. 1) yet disparities in the distribution and size of patches occurred. In the DIS greater foraging efforts coincided with increasing group size, presumably because patches were depleted rapidly as individuals foraged in proximity. In contrast, foraging effort was essentially constant in the UND, indicating that group size co-varied with patch size. In other words, animals in the UND were more attuned to their food resources than were those in the DIS. Foraging economy and habitat
Based on food considerations alone, animals should abandon feeding areas and search for new ones when they no longer forage profitably
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(Charnov, 1976; Pyke et al., 1977). This prediction was supported for kudu, which abandoned an Acaia nigrescens savanna when the harvesting rate exceeded 50 paces 100s -1 (Owen-Smith, 1979). Similarly, impala avoided increased intraspecific competition by spreading out or forming smaller groups when food items were widely dispersed (Jarman & Jarman, 1979). When resources and social foraging are considered, increased companionship should yield enhanced foraging benefits until a minimum food intake/individual is exceeded. Constraints should then be reflected in several parameters including vigilance and/or foraging effort. We detected an increase in pronghorn vigilance for group sizes greater or lesser than those assumed to represent peak foraging efficiency in each of our study sites (Fig. 3). However, animals in the DIS spent more time vigilant than those in the UND regardless of group size. Additionally, increases in foraging effort were tolerated by animals in the DIS, suggesting that different strategies of resource exploitation occurred between the sites. The frequency distribution of group sizes (Fig. 2) also indicates that groups larger than the optimal size for foraging efficiency were more than twice as common in the DIS than those in the UND. Because animals in the former remained aggregated despite increased foraging costs and decreased efficiency, we concluded that food base alone was not the most important variable affecting resource exploitation between the two study sites and suggest that recent historical factors pertaining to disturbance influenced foraging and anti-predatory behaviour. Historical factors and implications for conservation
The extent to which historical factors influenced foraging became evident after comparing disturbances at the two study areas. Pronghorn in the DIS were subjected to heavy traffic (about 200 vehicles week -1) associated primarily with mining activities, construction, and a limited one-week hunting season. These activities were most likely responsible for increased foraging costs and greater alertness. In addition to lower foraging efficiency caused by overcrowding on food patches, DIS pronghorn responded more vigorously to both potential and real predators than UND animals. Escape efforts, vigilance, and the frequency of clumped and piloerected flights were consistently greater in the DIS than in the UND. Conversely, pronghorn in the UND were subjected to only about 15 vehicles week- 1, none of which was associated with
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environmental exploitation. The increased responses to disturbance by DIS pronghorn undoubtedly involved increased energy costs. The fact that many native populations of large mammals in urban and agricultural areas (e.g. roe deer Capreolus capreolus; Turner, 1979) and national parks (e.g. mule deer; Geist, 1981) become habituated to many different kinds of disturbances fails to diminish the importance of our arguments concerning reduced foraging efficiency. In many habituated populations individuals receive gradual exposure (usually over many years) to disturbances. Rarely are such animals shot. However, the results reported in this paper suggest rather that immediate changes occur in the foraging behaviour of animals previously unexposed to a high level of peripheral stimuli. The method of data collection presented here represents a novel approach at integrating basic research with applied biology to understand better social foraging and in predicting impacts upon large herbivorous mammals. However, the idea that disturbance (whether it be natural predation or human-induced) mediates behavioural shifts in patterns of home range exploitation is not new. Mech (1977) reported that deer formed large concentrations at the interface of contiguous wolf territories. More surprising, however, is that very distantly related taxa are also very sensitive to changes in the activities of predators. For instance, female iguana Iguana iguana shifted nesting sites to a small islet a few hundred metres off the shore of Barro Colorado Island when terrestrial predators there were presumably increasingly destructive to eggs (Rand, 1968). Nevertheless, it is clear that as population, recreation, and construction activities increase not only in the Great Basin but throughout many of the world's ecosystems as well, decreases in disturbance-free habitats are assured. Unless development proceeds carefully and wise mitigation efforts are employed, foraging stress and escape efforts may be expected to increase to the point of energy imbalance and declining reproductive rates in most species. Future research will inevitably cast additional light on the mechanics of foraging and its bearing on evolutionary theory and biological conservation. ACKNOWLEDGEMENTS We thank Eric Charnov, Stephen Jenkins, Deborah Koutnik, Gail Michener, Bart O'Gara, Peter Stacey, and John Wehausen for reading a
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prior draft or discussing these ideas. Benjamin Beck and George Rabb of the Chicago Zoological Society provided a unique environment in which to work. N o r m Harris and T o m Mulroy of H D R Sciences deserve special thanks for support.
REFERENCES Alexander, R. D. (1974). The evolution of social behavior. Ann. Rev. Ecol. Syst., 5, 325-83. Beale, D. M. & Smith, A. D. (1970). Forage use, water consumption, and productivity of pronghorn antelope in western Utah. J. Wildl. Mgmt, 34, 570-82. Belovsky, G. E. (1978). Diet optimization in a generalist herbivore, the moose. Theo. Pop. Biol., 14, 105-34. Berger, J. (1978). Group size, foraging, and antipredator ploys: an analysis of bighorn sheep decisions. Beh. Ecol. Sociobiol., 4, 91-100. Berger, J. (1979a). Social ontogeny and behavioral diversity: consequences for bighorn sheep inhabiting desert and mountain environments. J. Zool. Lond., 188, 251-66. Berger, J. (1979b). Weaning, social environments, and the ontogeny of spatial associations in bighorn sheep. Biol. Beh., 4, 363-72. Bertram, B. C. R. (1980). Vigilance and group size in ostriches. Anim. Beh., 28, 278-86. Caraco, T. (1979a). Time budgeting and group size: a theory. Ecology, 60, 611-17. Caraco, T. (1979b). Time budgeting and group size: a test of a theory. Ecology, 60, 618-27. Charnov, E. L. (1976). Optimal foraging: the marginal value theorem. Theo. Pop. Biol., 9, 129-36. Crook, J. H., Ellis, J. E. & Goss-Custard, J. D. (1976). Mammalian social systems; structure and function. Anita. Beh., 24, 261-74. Diamond, J. M. (1975). The island dilemma: lessons of modern biogeographic studies for the design of natural preserves. Biol. Conserv., 7, 129-46. Diamond, J. M. (1976). Island biogeography and conservation: strategy and limitations. Science, 193, 1027-9. Eisenberg, J. F. (1981). The mammalian radiations: a study in evolution and adaptation. Chicago, University of Chicago Press. Frankel, O. H. & Soul6, M. E. (1981). Conservation and evolution. Cambridge, Cambridge University Press. Hirth, D. H. (1977). Social behavior of white-tailed deer in relation to habitat. Wildl. Monog., 53, 1-55. Hoogland, J. L. (1979). The effect of colony size on individual alertness of prairie dogs (Sciuridae: Cynomys, Spp.). Anim. Beh., 27, 394-407.
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Geist, V. (1978). Life strategies, human evolution, environmental design; toward a theory of health. New York, Springer-Verlag. Geist, V. (1981). Behavior; adaptive strategies in mule deer. In Mule and blacktailed deer of North America, ed. by O.C. Wallmo, 157-223. Lincoln, University of Nebraska Press. Jarman, P. J. (1974). The social organization of antelope in relation to their ecology. Behaviour, 48, 215-66. Jarman, P. J. & Jarman, M. V. (1979). The dynamics of ungulate social organization. In Serengeti, dynamics of an ecosystem, ed. by A. R. E. Sinclair & N. Norton-Griffiths, 185-22 Chicago, University of Chicago Press. Kitchen, D. W. (1974). Social behavior and ecology of the pronghorn. Wildl. Monog., 38, 1-96. Lipetz, V. E. (1980). Grouping as an antipredator strategy in the pronghorn antelope (Anilocapra americana ORD). Unpublished Master's thesis. University of Colorado, Boulder. MacArthur, R. H. & Wilson, E. O. (1967). The theory of island biogeography. Princeton, Princeton University Press. McCullough, D. R. (1969). The tule elk; its history, behavior, and ecology. Univ. Calif. Publ. Zool., 88, 1-209. Mech, L. D. (1977). Wolf-pack buffer zones as prey reservoirs. Science, 198, 320-1. O'Gara, B. (1978). Antilocapra americana. Mammalian Sp., 90, 1-7. Owen-Smith, N. (1977). On territoriality in ungulates and an evolutionary model. Quart. Rev. Biol., 52, 1-38. Owen-Smith, N. (1979). Assessing the foraging efficiency of a large herbivore, kudu. S. Afr. J. Wildl. Res., 9, 102-10. Pulliam, R. H. (1974). On the theory of optimaldiets. Amer. 'Nat., 108, 59-75. Pulliam, R. H. (1980). Do chipping sparrows forage optimally? Ardea, 68, 75-82. Pyke, G. H., Pulliam, H. R. & Charnov, E. L. (1977). Optimal foraging: a selective review of the theory and tests. Quart. Rev. Biol., 52, 137-54. Rand, A. S. (1968). A nesting aggregation of iguanas. Copeia, 3, 552-61. Rodgers, W. A. (1977). Seasonal changes in group size amongst five wild herbivore species. E. Afr. Wildl. J., 15, 175-90. Schoener, T. W. (1971). Theory of feeding strategies. Ann. Rev. Ecol. Syst., 2, 369-403. Sinclair, A. R. E. (1979). Dynamics of the Serengeti ecosystem. In Serengeti; dynamics of an ecosystem, ed. by A. R. E. Sinclair & N. Norton-Griffiths, 1-30. Chicago, University of Chicago Press. Soul6, M. E. & Wilcox, B. A. (1980). Conservation biology; an evolutionaryecological perspective. Sunderland, MA, Sinauer Associates. Staines, B. W. (1974). A review of factors affecting dispersion in deer and their relevance to management. Mammalian Review, 4, 79-91. Terborgh, J. (1974). Preservation of natural diversity: the problem of extinction prone species. Bioscience, 24, 715-22.
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Terborgh, J. (1976). Island biogeography and conservation: strategy and limitations. Science, 193, 1029-30. Turner, D. C. (1979). An analysis of time-budgeting in roe deer (Capreolus capreolus) in an agricultural area. Behaviour, 71,246-90. Wilson, E. O. (1975). Sociobiology, the new synthesis. Cambridge, Belknap Press.
Pronghorn Foraging Economy and Predator Avoidance in a Desert Ecosystem: Implications for the Conservation of Large Mammalian Herbivores Joel Berger Smithsonian Research Associate, Granite Range Field Project, Gerlach, Nevada 89412, USA
Dennis Daneke,* Jim J o h n s o n t & Stephen H. Berwick* * HDR Sciences, 804 Anacapa St., Santa Barbara, California 93101, USA t Department of Wildlife and Fisheries Biology, University of California, Davis, California, USA
ABSTRACT Assumptions of optimal foraging theory were applied to the feeding ecology of pronghorn Antilocapra americana to address issues of immediate relevance to conservation biology in the Great Basin Desert of North America. The relationships between foraging efficiency and." (1) group size; (2) habitat; and (3) disturbance history were examined in two study sites. Individual foraging efficiency increased with group size to a point in both study sites, but animals in the disturbed area remained in larger groups despite foraging less profitably. The hypothesis that individuals in a disturbed environment remain together for enhanced protection from (human ?) predators was supported and interpreted in the light of proposed habitat alterations in vast portions of this unique desert ecosystem.
INTRODUCTION 'Since man is creating disturbances in most ecosystems now, it is imperative that we learn to predict their impact, and the likelihood that they will shift the system's equilibrium.' (Sinclair, 1979) 193
Biol. Conserv. 0006-3207/83/0025-0193/$03.00 England, 1983. Printed in Great Britain
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Joel Berger, Dennis Daneke, Jim Johnson, Stephen H. Berwick
Progress in habitat preservation during the past decade has resulted from the application of basic biological thought (Soul6 & Wilcox, 1980; Frankel & Soul6, 1981), such as the theory of 'insular ecology' (MacArthur & Wilson, 1967; Terborgh, 1974, 1976; Diamond, 1975, 1976) to entire ecosystems. In this paper we apply two additional ecological concepts--optimal foraging theory and antipredator grouping behaviour--to the conservation of large mammalian herbivores. Specifically, these topics are integrated so that a broader understanding of the changes in the spatial and foraging ecology of a species confronted with local extirpation may be predicted. Recent studies of optimal foraging (Schoener, 1971; Pulliam, 1974, 1980; Pyke et al., 1977; Belovsky, 1978) have yielded empirical data on optimisation processes, social foraging, and vigilance (Berger, 1978; Hoogland, 1979; Bertram, 1980; Lipetz, 1980). Clearly, our knowledge of these related events has progressed sufficiently so that it may now be applied to problems in biological conservation. Assuming, as theory suggests (see above references), that animals maximise their reproductive fitness by compromising their foraging activities with predator surveillance, the extent to which behavioural responses mediate extrinsic disturbances and are governed by ecological factors should be detectable. If individuals or populations differ in foraging and anti-predator strategies and the parameters responsible are known, wise mitigation in areas of animal-human interactions is possible. In many areas of western North America massive construction projects associated with mining or military defence are planned or currently underway. The Great Basin Desert of Nevada and Utah is one such area. This topographically diverse region is inhabited by a comparatively rich mammalian fauna including pronghorn Antilocapra americana (O'Gara, 1978), the sole extant species of ungulate endemic to North America. These highly selective feeders live in gregarious societies and exploit low desert shrub and grassland communities. To assess the potential responses of pronghorn to increased human activity associated with construction projects we evaluated social and ecological variables influencing foraging mechanics and determined how the juxtaposition of such variables affected anti-predator responses. Specifically, we asked: (1) to what extent is foraging behaviour influenced by the dispersion of food items and group sizes ? (2) how is foraging economy related to prior and current disturbances? and (3) what are the implications of optimal foraging models to the conservation of large mammalian herbivores ?
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C O N C E P T U A L M O D E L A N D CORROBORATIVE EVIDENCE It is necessary to develop a scenario depicting the most efficient methods of energy exploitation by individuals in any given environment. We concentrate here on large mammalian herbivores. An abundant literature indicates that movements and foraging aggregations are inextricably linked to food quality, dispersion, and productivity (Jarman, 1974; Owen-Smith, 1977, 1979; Geist, 1978), social organisation (Wilson, 1975; Crook et al., 1976; Berger, 1979a; Eisenberg, 1981), and predator pressures (Alexander, 1974). Consequently, we reasoned that behavioural measures of foraging animals reflect, in part, food quality and dispersion, a fact often documented (Jarman, 1974; Owen-Smith, 1979). Of central importance is the idea that animals maximise their energy intake and minimise its expenditure (Pyke et al., 1977). Given that other factors are equal, we assume: (1) animals ranging more widely than conspecifics do so because preferred food items are highly dispersed; (2) individuals switching from one p l a n t to the next more often than conspecifics do so because rates of energy decline to unprofitable levels ('the marginal value theorem' (Charnov, 1976)); (3) the number of paces taken during a standardised foraging bout indicates the relative distance between preferred food items simply because widely dispersed resources require more movement; and (4) the number of times a foraging animal moves to other food plants per unit time indicates relative food quality. Items (1) and (2) (above) introduce the ideas upon which this paper is based and (3) and (4) are the actual measures through which foraging is assessed. For example, consider two foraging pronghorn, A and B, feeding under ecological regimes differing only in the quality and dispersion of food items. A consumes morsels (designated as 'chew') from a single bush for 200 s, moves 5 paces (1 pace/s) without chewing, and immediately feeds on the next bush for 95 s. Thus, A fed for 295/300 s and interrupted non-mobile chewing only once to move to another plant. In contrast, B feeds for 5 s at a bush, moves to another food item that requires 45 paces (1 pace/s) and does not chew (hence no net gain in food accrued because mastication has not occurred), feeds at another bush for 5 s, moves an additional 45 paces again without chewing, and so forth until 300 s have elapsed. The chewing time per unit foraging period is greater in A than B because the former not only chewed longer but moved and interrupted chewing less frequently.
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With this example in mind, it is possible to identify and measure specific components of a foraging animal's time budget. The time allocated to securing energy (i.e. eating) and expending it (i.e. moving without chewing) provides a basis from which foraging effort can be assessed. Foraging effort is defined as the distance of walking movement associated with chewing or searching for food per unit time. It is indicated (Fig. 1) by
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the interplay of food quality (the independent variable) measured by the frequency of movements between food plants per unit time; and food dispersion (the dependent variable) measured by the mean number of paces per movement. According to this model, as foraging effort loci approach the origin in Fig. 1, food patch quality increases. These areas contain voluminous closely associated food items and the subsequent rate of energy expenditure is low because animals move relatively little. Conversely, animals expressing foraging effort further from the origin move more frequently and/or further per foraging bout. A multiplicative function of the two variables (xy) was avoided so that the effects of food quality and food dispersion could be separated.
METHODS Study sites Two study sites were established, each in Pine Valley, west central Utah (see Beale & Smith, 1970 for a more thorough description). The northern study site was located on the Desert Range Experiment Station, an area of about 130 km 2 of undisturbed habitat. We designated this the 'undisturbed' site (UND) because public access was restricted. The second study site was located about 20 km south in the same desert valley at the same altitude. This area was called the disturbed site (DIS) because public access was unrestricted and hunting, mining, and construction activities have occurred there, these latter two activities primarily during the past 6 years. We used the DIS as a representative example of an area where previously undisturbed animals were confronted with a new construction project. The densities of pronghorn and their natural predators were similar at both study sites. Animals were observed for about 800 h between July through October 1980. Definitions and rationale A 'foraging bout' was defined as a continuous 300-s period which commenced after pronghorn first ingested food. Time spent for allogrooming, elimination, and social interactions were subtracted from the
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300 s to restrict the analysis to only foraging and antipredator components. Foraging bouts included two general types of behaviour patterns, each concerning energy balance. Those relating directly to ingestion were designated 'energy enhancing activities' (EEAs) and included biting plants, masticating, ruminating, and searching for food. Searching occurred when an animal oriented its head toward the ground without chewing. The ratio of chew time per foraging bout measured mean 'foraging efficiency'. This measure is therefore a ratio based on time commitments to various activities and it does not imply caloric intake. The Foraging Effort Model (Fig. 1) is based solely on EEAs. Behaviours not directly associated with the pursuit of food were energy debits and called 'energy consuming activities' (ECAs). These included walking with the head in an upright position, scanning (i.e. standing with the head up), and alert postures (see Kitchen, 1974). 'Vigilance' was the time an animal spent with its head up per bout without chewing or walking. Anti-predator behaviours associated with flight were also quantified. 'Escape effort' (defined as the sum of the products of distance fled and speed) was determined. Distance fled was estimated visually by how far an animal moved when first disturbed until its next bite of food. Speed was estimated by using five gaits; (1)walk, (2) trot, (3) slow run or lope, (4) full run, and (5) maximum sprint. Piloerection of hair follicles on the rump and tendencies for pronghorn to clump together or remain dispersed were also recorded when 50 ~o or more of a group's members engaged in those behaviours. Data collection
The number of paces taken by focal animals and the times allocated to components of EEAs and ECAs were recorded for different sized groups. Observations from both study sites were based on at least 130 different animals and occurred just after sunrise or before dusk, periods when foraging activity was greatest. Data on males were excluded because part of the study occurred during the rut. Broad variability in foraging occurred since we sampled animals feeding under a wide range of ecological conditions. Our observations were indeed quite different from prior studies (cf Berger, 1978; Lipetz, 1980) of ungulate foraging ecology where sampling procedures were restricted to animals feeding in uniform habitats.
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Group sizes of foraging animals were lumped into categories to maintain sample size consistency. The position of an individual within a group was recorded as central or peripheral only when animals were clearly situated within such positions. Following the collection of foraging data, pronghorn were disturbed systematically on foot or by a moving vehicle. Our perturbations were standardised by: (1) walking toward the study animals from 400-800 m distant when pronghorn visibility was unobscured; and (2) driving slowly ( < 32 km h-1) along dirt roads beginning at distances 1.6 km or greater with visibility conditions as above. RESULTS Patch size and quality If the study sites differed in the distriiaution, size, or quality of food patches, then differences should be detectable in at least two parameters associated with social foraging: (1) group sizes, and (2) foraging effort. Although these parameters are not distinctly different, evidence concerning each are presented separately for the sake of clarity. The UND had both a significantly larger mean group size (X = 5.2, N = 199; p < 0.05; t Test) than the DIS 02, = 4-0, N = 258) and a greater proportion of larger groups (Fig. 2). This evidence suggests that the U N D was richer in food quality and/or had larger food patches than the DIS when only food resources were considered. Little is indicated pertaining to the mechanics of patch exploitation in groups of varying size from either site (see below). Differences in the quality (and indirectly size) of food patches should be reflected in foraging effort. This index was standardised between environments by holding EEA time constant and using absolute measures of distances (paces) and interruptions (frequency). If the U N D was indeed characterised by food patches of higher nutritional value than the DIS habitat and not simply by larger patches of equivalent food value, then individuals foraging in patches from the UND should expend less foraging effort. This appears not to be the case. The lack of significant differences in foraging effort between individuals in equal sized groups from each site suggests that patch quality did not differ between our two study sites. It therefore appears that larger groups in the U N D are explained by larger food patches than those located on the DIS.
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Furthermore, foraging effort increased with group size on the DIS (the differences between groups 1-2 and 5-7 were significant; p < 0-05; Fig. 1) whereas it was similar among all group sizes on the UND.
Foraging efficiency and predator surveillance Because animals in large groups tend to forage more efficiently than those in smaller groups (Berger, 1978), we hypothesised that pronghorn in the U N D would experience greater chew time/bout as mean group sizes were larger there. Overall, this prediction was supported. Average foraging efficiency per individual differed between study sites and approached statistical significance. In the U N D mean foraging efficiency per individual increased with group size and it attained the maximum for groups of 5-7 animals declining only slightly thereafter (Fig. 3). This slight decrease was attributed to peripheral animals which were significantly (p < 0.05) more vigilant than their centrally located conspecifics. In smaller groups this relationship was obscured possibly because of our inability in clearly assigning animals into a central versus peripheral dichotomy.
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The maximum foraging efficiency for DIS pronghorn occurred in groups of 3-4 animals and declined thereafter. When pronghorn in equal sized groups were compared between study sites, U N D animals in groups 5-7 or larger foraged significantly (p < 0.05) more efficiently than those from the DIS. With regard to vigilance, DIS pronghorn spent more time/bout scanning than did U N D animals (Fig. 3). Flight effort and perturbations No significant differences were noted in flight characteristics (see below) between large and small groups. Therefore, data were pooled and the
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responses of individuals from each study site compared. Those in the DIS expended approximately four times the escape effort (Fig. 4) than the UND animals (p < 0.001). Animals in the DIS also displayed heightened alarm responses as indicated by a greater percentage of clumped flights, more bouts with piloerected rumps, and delayed resumption of feeding (Fig. 4) when compared with UND pronghorn. DISCUSSION Group size determinants Enhanced reproductive success has been viewed correctly as the ultimate cause of social foraging (Alexander, 1974; Jarman, 1974; Pyke et al.,
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1977; Caraco, 1979a,b; Hoogland, 1979; Bertram, 1980) and it is achieved by foraging efficiently and avoiding predators. Here we consider the roles of habitats and predators in proximate causation only. The hypothesis that feeding group size in large herbivorous mammals is influenced more by resource levels than by immediate predator pressures is supported by two arguments. First, when disjunct populations from similar habitats differing in resource bases are compared and predator pressures are roughly equivalent (i.e. the same predators occur in equal numbers in each area), mean group size differences occur. Second, feeding group sizes vary seasonally with food availability despite constant predator pressures. Empirical data for bighorn sheep Ovis canadensis (Berger, 1979b), white-tailed deer Odocoileus virginianus (Hirth, 1977), red deer and tule elk Cervus e laphus; (McCuUough, 1969; Staines, 1974), impala Aepyceros melampus (Jarman & Jarman, 1979), topi Damaliscus korrigum (Jarman & Jarman, 1979), kudu Tragelaphus stresiteros (Owen-Smith, 1979), and wildebeest Connochaetes taurinus (Rodgers, 1977) support one or both of these relationships concerning group size and resource level. The problem, however, is deceptively more complex and many variables are involved in group size formation. For instance, Caraco (1979a,b) found that wintering juncos incurred energy debits due to thermoregulatory stress but counterbalanced them by enhanced foraging benefits in larger groups. In these groups vigilance decreased although an animal's social status also influenced harvesting rate, a relationship also noted for mule deer O. hemionus (D. Koutnik, pers. comm.). On our two study sites, the quality of food patches was apparently equivalent (see Fig. 1) yet disparities in the distribution and size of patches occurred. In the DIS greater foraging efforts coincided with increasing group size, presumably because patches were depleted rapidly as individuals foraged in proximity. In contrast, foraging effort was essentially constant in the UND, indicating that group size co-varied with patch size. In other words, animals in the UND were more attuned to their food resources than were those in the DIS. Foraging economy and habitat
Based on food considerations alone, animals should abandon feeding areas and search for new ones when they no longer forage profitably
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(Charnov, 1976; Pyke et al., 1977). This prediction was supported for kudu, which abandoned an Acaia nigrescens savanna when the harvesting rate exceeded 50 paces 100s -1 (Owen-Smith, 1979). Similarly, impala avoided increased intraspecific competition by spreading out or forming smaller groups when food items were widely dispersed (Jarman & Jarman, 1979). When resources and social foraging are considered, increased companionship should yield enhanced foraging benefits until a minimum food intake/individual is exceeded. Constraints should then be reflected in several parameters including vigilance and/or foraging effort. We detected an increase in pronghorn vigilance for group sizes greater or lesser than those assumed to represent peak foraging efficiency in each of our study sites (Fig. 3). However, animals in the DIS spent more time vigilant than those in the UND regardless of group size. Additionally, increases in foraging effort were tolerated by animals in the DIS, suggesting that different strategies of resource exploitation occurred between the sites. The frequency distribution of group sizes (Fig. 2) also indicates that groups larger than the optimal size for foraging efficiency were more than twice as common in the DIS than those in the UND. Because animals in the former remained aggregated despite increased foraging costs and decreased efficiency, we concluded that food base alone was not the most important variable affecting resource exploitation between the two study sites and suggest that recent historical factors pertaining to disturbance influenced foraging and anti-predatory behaviour. Historical factors and implications for conservation
The extent to which historical factors influenced foraging became evident after comparing disturbances at the two study areas. Pronghorn in the DIS were subjected to heavy traffic (about 200 vehicles week -1) associated primarily with mining activities, construction, and a limited one-week hunting season. These activities were most likely responsible for increased foraging costs and greater alertness. In addition to lower foraging efficiency caused by overcrowding on food patches, DIS pronghorn responded more vigorously to both potential and real predators than UND animals. Escape efforts, vigilance, and the frequency of clumped and piloerected flights were consistently greater in the DIS than in the UND. Conversely, pronghorn in the UND were subjected to only about 15 vehicles week- 1, none of which was associated with
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environmental exploitation. The increased responses to disturbance by DIS pronghorn undoubtedly involved increased energy costs. The fact that many native populations of large mammals in urban and agricultural areas (e.g. roe deer Capreolus capreolus; Turner, 1979) and national parks (e.g. mule deer; Geist, 1981) become habituated to many different kinds of disturbances fails to diminish the importance of our arguments concerning reduced foraging efficiency. In many habituated populations individuals receive gradual exposure (usually over many years) to disturbances. Rarely are such animals shot. However, the results reported in this paper suggest rather that immediate changes occur in the foraging behaviour of animals previously unexposed to a high level of peripheral stimuli. The method of data collection presented here represents a novel approach at integrating basic research with applied biology to understand better social foraging and in predicting impacts upon large herbivorous mammals. However, the idea that disturbance (whether it be natural predation or human-induced) mediates behavioural shifts in patterns of home range exploitation is not new. Mech (1977) reported that deer formed large concentrations at the interface of contiguous wolf territories. More surprising, however, is that very distantly related taxa are also very sensitive to changes in the activities of predators. For instance, female iguana Iguana iguana shifted nesting sites to a small islet a few hundred metres off the shore of Barro Colorado Island when terrestrial predators there were presumably increasingly destructive to eggs (Rand, 1968). Nevertheless, it is clear that as population, recreation, and construction activities increase not only in the Great Basin but throughout many of the world's ecosystems as well, decreases in disturbance-free habitats are assured. Unless development proceeds carefully and wise mitigation efforts are employed, foraging stress and escape efforts may be expected to increase to the point of energy imbalance and declining reproductive rates in most species. Future research will inevitably cast additional light on the mechanics of foraging and its bearing on evolutionary theory and biological conservation. ACKNOWLEDGEMENTS We thank Eric Charnov, Stephen Jenkins, Deborah Koutnik, Gail Michener, Bart O'Gara, Peter Stacey, and John Wehausen for reading a
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prior draft or discussing these ideas. Benjamin Beck and George Rabb of the Chicago Zoological Society provided a unique environment in which to work. N o r m Harris and T o m Mulroy of H D R Sciences deserve special thanks for support.
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Terborgh, J. (1976). Island biogeography and conservation: strategy and limitations. Science, 193, 1029-30. Turner, D. C. (1979). An analysis of time-budgeting in roe deer (Capreolus capreolus) in an agricultural area. Behaviour, 71,246-90. Wilson, E. O. (1975). Sociobiology, the new synthesis. Cambridge, Belknap Press.