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Scarcity in the prey community yields anti-predator benefits
Acta Oecologica 37 (2011) 314e320
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Original article
Scarcity in the prey community yields anti-predator benefits Matt W. Hayward* Mammal Research Institute, Polish Academy of Science, ul. Waszkiewicza 1, 17-230 Białowiez_ a, Poland1 Centre for African Conservation Ecology, Nelson Mandela Metropolitan University, PO Box 77000, Port Elizabeth 6031, South Africa School of Biological, Earth and Environmental Science, University of New South Wales, Sydney 2052, Australia
a r t i c l e i n f o
a b s t r a c t
Article history: Received 28 July 2010 Accepted 16 March 2011 Available online 8 April 2011
The majority of individuals in a community belong to a small number of abundant species. Understanding why some species are rare and others are common has been a long-held goal for ecologists. Africa’s large carnivore guild preferentially preys on a small number of species within a limited weight range. Within this weight range however, some species that are expected to be significantly preferred as prey are not. I tested whether these species avoid preferential predation through their low densities. Records of over 40,000 kills from up to 48 different communities were used to test if non-preferred species within the expected prey weight ranges of each large predator avoid preferential predation and why. Species expected to be prey of Africa’s large predators based on their body mass, that are preferred are preyed upon significantly more frequently at low densities than non-preferred prey. This results in a negative relationship between relative abundance and preference for preferred prey, but a positive relationship for non-preferred prey. The non-preferred prey species that are within the expected prey weight ranges of Africa’s large predators are significantly less abundant within the prey community than significantly preferred prey. Rarity in African ungulates may convey an anti-predator benefit in that it was suboptimal for predators to evolve morphological or behavioral strategies to optimally forage on them or in that prey species can avoid predators by existing in habitats with low carrying capacity. Ó 2011 Elsevier Masson SAS. All rights reserved.
Keywords: African large carnivores Density-dependence Predation Predator avoidance strategy Predatoreprey interactions Prey switching Top-down limitation
1. Introduction In animal and plant communities, the majority of individuals belong to a small number of abundant species, while most species are represented by a small number of individuals (Hughes, 1986; May, 1975). Understanding why some species are rare and others common within local communities has long been a goal of ecologists (Gaston, 1994) and there is a growing body of evidence to suggest that naturally rare species have traits that differ from naturally common species (Kunin and Gaston, 1993). Predators and their prey are often considered to be in an evolutionary arms race to eat or be eaten (Dawkins and Krebs, 1979). This analogy implies that predators evolve improved abilities to capture prey, which leads to prey evolving abilities to avoid capture (Abrams, 1986). Theoretical and mathematical models do not support this analogy however (Abrams, 1986; Brodie and Brodie, 1999). One reason for this may be the presence of secondary prey
* Present address: Australian Wildlife Conservancy, PO Box 432, Nichol’s Point 3501, Australia. Tel.: þ613 50245859; fax: þ613 50271200. E-mail address: [email protected]. 1 Tel.: þ4885 6827781; fax: þ4885 6827752. 1146-609X/$ e see front matter Ó 2011 Elsevier Masson SAS. All rights reserved. doi:10.1016/j.actao.2011.03.003
species that provide a buffer to predators in times of primary prey shortages (Pech et al., 1995). Primary prey are likely to be those that a predator has evolved to preferentially and optimally prey upon, whereas secondary prey are likely to be prey species that a predator has not evolved to preferentially prey upon but rather are preyed upon during prey switching (Garrott et al., 2007). Predators exhibit two distinct preference categories of prey: preferred prey species and the preferred weight range of prey (Hayward et al., 2006a). Preferred prey species are those preyed upon by predators significantly more frequently than expected based on the relative abundance of that prey species in the prey community (akin to primary prey). The preferred weight range is a range of prey body masses that a particular predator preys upon more frequently than expected (hereafter termed ‘expected prey’). Amongst this group of species that are expected to be preyed upon, there are species that are significantly preferred (primary prey), but also species that are not preferentially killed by predators (secondary prey). One hypothesis for the presence of these nonpreferred prey species within the expected weight range is that they are intrinsically rare in the prey community, which has meant that predators have not evolved morphological or behavioral adaptations that allow preferential predation (Hayward, 2009). Species outside the expected prey weight range are not preferred
M.W. Hayward / Acta Oecologica 37 (2011) 314e320
because they are too small to provide sufficient energetic reward for hunting them or are too large and thereby are too risky to hunt optimally (Hayward, 2009). High abundance is itself not necessarily the most successful evolutionary strategy a species can employ. Individuals obtain relatively short-term advantages by existing in high abundance through reducing the likelihood of any single individual being preyed upon (Hamilton, 1971; Morrell et al., 2010). An alternative evolutionary strategy is for individuals to persist at lower density and thereby avoid predators evolving morphological or behavioral adaptations to prey specifically on them. In this study, we aimed to test whether these non-preferred prey species within the expected prey weight ranges of Africa’s large predator guild (African wild dogs Lycaon pictus, cheetahs Acinonyx jubatus, leopards Panthera pardus and lions Panthera leo) avoid predation through their low densities. We then discuss whether occurring at low densities could be an evolutionary strategy to minimize top-down limitation as predators were less likely to evolve features to preferentially prey on rare species. The key tenet of this study is that some species are inherently rare in their natural environments and even when freed from competition and predation, these species never reach the densities of the dominant members of the community. There is evidence elsewhere to support this. For example, dormice Muscadinus avellanarius are relatively K-selected small mammals that have an inherently low population density and intrinsic rate of increase because their lack of a caecum necessitates diet specialization and, therefore, specific habitat requirements (Bright and Morris, 1996). Similarly, 91% of 57 locally rare open forest plant species occurred in high density somewhere in their range, but the remaining species were rare throughout their entire distributions (Murray and Lepschi, 2004). Other botanical studies have also found a proportion of the community is inherently rare (McIntyre et al., 1993; Rabinowitz et al., 1986). Carnivores are inherently rare due to their trophic position, however even within large carnivore guilds some species are much rarer than others (Creel and Creel, 2002). It is acknowledged that the term ‘rare’ describes an array of spatial and temporal patterns of abundance (Kunin and Gaston, 1993), but here it is used where no particular measure or pattern is implied. 2. Materials and methods Published records of over 40,000 kills from up to 48 different spatial locations or temporal periods were compiled in the derivation of the prey preferences and preferred weight range of Africa’s large predator guild (Hayward, 2009; Hayward and Kerley, 2008). These data come from numerous published and unpublished sources and are referred to in the original prey preference studies (Hayward, 2006; Hayward et al., 2006a; Hayward et al., 2006b, 2007a; Hayward and Kerley, 2005, 2008; Hayward et al., 2006c). All sites were from sub-Saharan African savannas. The database housing this information was interrogated and information on the preference of each prey species and its relative abundance in the prey community of a site was extracted. Preference was determined using Jacobs’ index (Jacobs, 1974):
D ¼
rp r þ p 2rp
where r is the proportion of a predator’s total kills of a certain prey species at a site and p is the proportional abundance of that prey species in that prey community. Many selectivity indices have been described (Krebs, 1989); however, all have biases at small proportions and none is considered superior to the rest (Chesson, 1978; Strauss, 1979). Consequently,
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researchers often overstate the accuracy of their preference results (Norbury and Sanson, 1992), particularly with the most commonly used techniques such as the forage ratio and Ivlev’s electivity index (Ivlev, 1961). These two indices suffer from non-linearity, bias to rare food items, increasing confidence intervals with increasing heterogeneity, being unbound or undefined, and lacking symmetry between selected and rejected values (Jacobs, 1974). Confidence intervals also become excessive for proportions below about 10% (Strauss, 1979). Jacobs’ index is one method that minimize these biases (Krebs, 1989), however measures of preference also exist (e.g. Owen-Smith and Mills, 2008b). We have used Jacobs’ index because it was used to derive the original prey preference data (Hayward, 2006; Hayward et al., 2006a,b,c; Hayward and Kerley, 2005) and solving Jacobs’ index has allowed the accurate prediction of predator diet (Hayward et al., 2007a; Meena et al., in press) and carrying capacity (Hayward et al., 2007b). A Jacobs’ index value was calculated for all prey species at each site. Values approaching 1 reflect a preference, those approaching 1 reflect avoidance, and those near 0 indicate a species is killed as frequently as expected based on its relative abundance at a site. Preferred prey species were calculated using t- or sign tests against means of 0 for each prey species, while the expected prey weight range of each predator was estimated as the body mass range encompassing the preferred prey species (Hayward et al., 2006a). Site-specific Jacobs’ index values (D) of each significantly preferred prey species or those expected prey of each large African predator were then related to their relative abundance (p) in the community at that site. The slopes of these linear regressions for
Table 1 Prey species expected to be preferentially killed by each large African predator (i.e. those within the preferred prey weight range), their body mass, the slope of the regression between their relative abundance in the prey community and their preference by the predator (based on Jacobs’ index), and whether they are significantly preferred or not. Species
Scientific name
Mass Predator
Slope
Preferred
Blesbok Bushbuck Impala Thomson’s gazelle Grant’s gazelle Nyala Reedbuck Springbok Warthog Buffalo Eland Gemsbok Giraffe Roan Sable Waterbuck Wildebeest Zebra Bushbuck Duiker Impala Klipspringer Reedbuck Springbok Thomson’s gazelle Bushbuck Duiker Impala Kudu Reedbuck Springbok Thomson’s gazelle Wildebeest
Damaliscus dorcas Tragelaphus scriptus Aepyceros melampus Gazella thomsoni G. granti T. angusi Redunca redunca Antidorcas marsupialis Phacochoerus africanus Syncerus caffer T. oryx Oryx gazelle Giraffa cameloparalis Hippotragus equines H. niger Kobus ellipsiprymnus Connochaetes taurinus Equus burchelli
52.5 23 30 15 38 47 32 26 45 435 345 158 550 220 180 190 135 175 23 16 30 10 32 26 15 23 16 30 135 32 26 15 135
6.43 1.94 0.34 0.56 0.37 4.14 1.25 1.18 3.19 1.48 4.94 0.48 4.78 10.65 1.66 0.91 1.34 1.72 0.01 1.98 0.19 8.92 0.14 2.8 0.15 9.01 0.21 0.32 2.09 5.91 17.28 1.28 0.88
Yes No Yes Yes Yes No No Yes No Yes No Yes Yes No No No Yes Yes Yes Yes Yes No No No No Yes Yes No Yes No No Yes No
Sylvicapra grimmia Oreotragus oreotragus
T. strepsiceros
Cheetah Cheetah Cheetah Cheetah Cheetah Cheetah Cheetah Cheetah Cheetah Lion Lion Lion Lion Lion Lion Lion Lion Lion Leopard Leopard Leopard Leopard Leopard Leopard Leopard Wild dog Wild dog Wild dog Wild dog Wild dog Wild dog Wild dog Wild dog
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significantly preferred and non-preferred prey species were then compared using a t-test. The data were normally distributed. Given relative abundance (p) is used in the derivation of Jacobs’ index (D), I hypothesized that there should be a negative relationship between these two variables if the proportional kills (r) remained constant and relative abundance (p) varied. A positive relationship would indicate a predator kills a prey species (r) proportionally more frequently as it becomes more common within the prey community (p). That is, prey species lose the protection of rarity. The preferred prey species of the African wild dog are kudu, Thomson’s gazelle, bushbuck and common duiker, and the bimodal expected prey weight range is from 16 to 32 kg and from 120 to 140 kg (Hayward et al., 2006c). Blesbok, impala, springbok and Thomson’s and Grant’s gazelles are significantly preferred by cheetahs, and their expected prey weigh from 23 to 56 kg (Hayward et al., 2006b). Leopard prefer prey within a range of 10e40 kg and significantly prefer bushbuck, impala and common duiker (Hayward et al., 2006a). Lions significantly prefer blue wildebeest, buffalo, gemsbok, giraffe and plain’s zebra, and are expected to kill prey within a range of 190e550 kg (Hayward and Kerley, 2005). Spotted hyaenas were not included in this study because they do not have any significantly preferred prey species (Hayward, 2006). These species were determined to be significantly preferred using t-tests against a mean of 0 throughout the entire distribution of
each predator (Hayward, 2009; Table 1). Species whose body mass was within 10% of the lower value of the expected prey were also included because of the less precise derivation of the expected weight range. I used the preferred prey weight range derived from this series of studies rather than using other ranges (e.g. OwenSmith and Mills, 2008a) to maintain similar data sources and because this present series of studies looked at prey preferences from throughout the range of each predator rather than sitespecific preferences. 3. Results Species that are within the expected weight range of Africa’s large predators but are not preferred are significantly less abundant within the prey communities than preferred prey (ManneWhitney U ¼ 18730.5, n ¼ 475, p < 0.001). Non-preferred prey are significantly less abundant within the expected prey weight range of lion (U ¼ 1527, n ¼ 210, p < 0.001), cheetah (U ¼ 309, n ¼ 81, p < 0.001), and wild dog (U ¼ 972, n ¼ 109, p ¼ 0.008), but not leopard (U ¼ 494.5, n ¼ 75, p ¼ 0.090). For the prey of lion, all preferred species become less preferred at higher density whereas non-preferred species within the expected prey weight range became increasingly preferred at higher density (Fig. 1; Table 1). Leopard preferred and non-preferred but expected
Fig. 1. Relationship between the relative abundance in the available prey community of preferred and expected prey of lions and the preference lions’ have for it (based on Jacobs’ index).
M.W. Hayward / Acta Oecologica 37 (2011) 314e320
prey follow the same trends (Fig. 2; Table 1). Cheetah preferred prey species also exhibit these relationships, although preferred gazelles (Antilopinae) are similarly preferred irrespective of their relative abundance (Fig. 3; Table 1). Conversely, reedbuck and warthog are most preferred by cheetahs when they are at low relative abundance. Non-preferred prey that are expected to be preferentially hunted by wild dogs exhibit similar relationships, however the preferred bushbuck and kudu are more frequently preyed upon when they are relatively abundant members of the prey community, while impala are preyed upon relatively frequently irrespective of abundance (Fig. 4; Table 1). As hypothesized, prey within the expected weight ranges of large predators that are preferred are killed significantly more frequently at low densities than non-preferred prey. This results in a negative relationship between relative abundance and preference for preferred prey (Fig. 5). Prey species that are expected to be killed preferentially but are not, exhibit a positive relationship (Fig. 5). The difference between the slopes of preferred and non-preferred prey species are significant (t ¼ 2.363, d.f. ¼ 31, p ¼ 0.025; Fig. 5). 4. Discussion Species within the expected prey weight range of each large, African predator are all expected to be preferentially preyed upon, however several prey species exist within this range that are not preferentially killed. These species are avoided at low density, and only become preferentially preyed upon at high densities reflecting their status as secondary prey upon which predators turn to by prey switching (Garrott et al., 2007; Murdoch, 1969). These prey species are killed at greater frequency (r) when they are more abundant (p) within the prey community, which leads to increased preference (D). The benefits these species derive from the low predation rates at low density is reflected in the mean density of these species within the prey community where they occur. These non-preferentially preyed upon species are rarer throughout sub-Saharan Africa than
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the species within the expected weight ranges of Africa’s large predators that are preferentially preyed upon. This indicates that these species have evolved to occur naturally at low densities and thereby avoid entering into an evolutionary ‘arms race’ with a large predator to optimally forage upon them. In essence, their rarity within the prey community means that it is suboptimal for a predator to have evolved morphological or behavioral strategies to optimally forage on them. These species are unlikely to be limited by top-down factors, but rather bottom-up and competitive factors. This is not to say predation is the limiting factor here, as bottom-up (morphological specialization, competitive influences or social factors) limitations are far more likely to be the reason. Rather, predators have not evolved strategies to preferentially prey on these species because they are invariably rare in the environment and when their habitat is invaded by range expanding preferred prey (such as zebra moving into roan habitat in South Africa’s Kruger National Park) the rare species may become selected for (Harrington et al., 1999). That is, the rare prey species reduce their risk of predation by occupying habitats with low carrying capacity. The negative relationship between preference and abundance for preferred prey (Fig. 5) may be an artifact of the derivation of Jacobs’ index, which is theoretically biased as prey become less relative abundant (Jacobs, 1974; Strauss, 1979). For example, if a theoretical lion population rigidly made 50% of their kills as wildebeest (40% of available prey), 40% as zebra (40% of available prey) and 10% other species (20% of available prey), then the Jacobs’ index value for wildebeest is 0.2. However if buffalo made up 50% of the available prey community but are not killed and wildebeest and zebra comprise the remainder under the same predation rates, then this value for wildebeest increases by 250% to 0.5. However, lion are not inflexible model organisms and appear to follow optimal foraging rules (Hayward and Kerley, 2005). Furthermore, the ability of the Jacobs’ index equation to be solved to accurately predict the diet of lions in Africa and India (Hayward et al., 2007a; Meena et al., in press) suggests it is highly robust to these potential biases.
Fig. 2. Relationship between the relative abundance in the available prey community of leopard preferred prey species or those expected to be preyed upon and the preference leopards’ have for it (based on Jacobs’ index).
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M.W. Hayward / Acta Oecologica 37 (2011) 314e320
Fig. 3. Relationship between the relative abundance in the available prey community of cheetah preferred prey species or those expected to be preyed upon and the preference leopards’ have for it (based on Jacobs’ index).
Irrespectively, this potential bias holds in the same direction for less common, expected prey species and this departure from a neutral pattern must therefore reflect a positive behavioral response by the predator to increased prey availability. Kunin and Gaston (1993) describe four processes which may bias the creation and maintenance of rarity. Firstly, it may be the characteristics of a species that cause it to be rare, rather than being a consequence of rarity. This seems unlikely in predatoreprey interactions as predation is a factor reducing population density. Secondly, extinction risk may influence the list of rare species (Kunin and Gaston, 1993), however there was no evidence of this here. Thirdly, rarity has behavioral, ecological or genetic consequences that may influence the perception of rarity (Kunin and Gaston, 1993), however this seems unlikely to occur in such widely distributed species as studied here. Consequently, we are
left with the possibility that the rare species studied here have evolved the adaptation of rarity over evolutionarily meaningful time periods, which in this case appears to convey protection from preferential predation (Kunin and Gaston, 1993). It is not surprising that rare species differ in characteristics of predatoreprey interactions given the breadth of differences they have been shown to have (Kunin and Gaston, 1993). Furthermore, among insects there are differences in functional and numerical responses of common versus rare species (Hong and Ryoo, 1991). Predators that are inherently rare in the environment may have evolved the same strategy to avoid intraguild predation and competition because of their high dietary overlap (Owen-Smith and Mills, 2008a). Cheetahs and African wild dogs are orders of magnitude less abundant than the dominant members of the guild (lions, hyaenas and leopards) (Creel and Creel, 2002). This may also
M.W. Hayward / Acta Oecologica 37 (2011) 314e320
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Fig. 4. Relationship between the relative abundance in the available prey community of African wild dog preferred prey species or those expected to be preyed upon and the preference leopards’ have for it (based on Jacobs’ index).
be caused by changes in the availability of preferred prey species (Hayward and Kerley, 2008). The preferred prey of leopard are not significantly more abundant in the prey community than non-preferred prey, in contrast to
the rest of the guild. This illustrates the opportunistic nature of leopard predation and is reflected in its ability to persist amongst a diverse range of prey communities throughout its vast African and Asian range. Spotted hyaenas exhibit non-preferential predation
Slope of relationship between Jacobs' index value and relative abundance
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M.W. Hayward / Acta Oecologica 37 (2011) 314e320
4
3
2
1
0 Not significantly preferred
Significantly preferred
-1
-2 Species within preferred prey weight range or that were significantly preferred
Fig. 5. Mean (1 S.E.) of the slopes of the relationship between prey relative abundance and Jacobs’ preference value for large African carnivores.
(Hayward, 2006) and, like leopards, are unlikely to be significant top-down influences on primary prey because of the frequency with which they switch to secondary prey species. Predatoreprey interactions in temperate climates may not function in the manner seen in Africa. This is likely to be due to the simplified nature of these ecosystems where there are insufficient resources available to support more than a single predator e single prey interaction. There are conservation implications for this research. In unaltered environments, rare species may be largely immune to topdown population regulation. However, when disturbances occur that alter equilibrium states (e.g. the creation of artificial water points), then factors might arise that lead to high, preferential predation rates. This occurred in Kruger National Park, South Africa, and ultimately led to the decline of the roan antelope Hippotragus equines population (Harrington et al., 1999; Hayward et al., 2007a). 5. Conclusions Data obtained from over 40,000 kill records have revealed that Africa’s large predators preferential prey on a few species within a preferred weight range. Species occurring within the weight range but are uncommon are not preferentially preyed upon suggesting rarity in African ungulates may convey an anti-predator benefit in that it was suboptimal for predators to evolve morphological or behavioral strategies to optimally forage on them or, more likely, because scarce prey species occupy habitats that do not support sufficient individuals to allow predators a satisfactory likelihood of encounter. Acknowledgments MWH was supported by the Marie Curie Transfer of Knowledge project e BIORESC MTKD-CT-2005-029957 e financed by the 6th Framework Programme of the European Union. References Abrams, P.A., 1986. Is predator-prey coevolution an arms race? Trends in Research of Ecology and Evolution 1, 108e110. Bright, P.W., Morris, P.A., 1996. Why are dormice rare? A case study in conservation biology. Mammal Review 26, 157e187. Brodie III, E.D., Brodie Jr., E.D., 1999. Predator-prey arms races. BioScience 49, 577e588. Chesson, J., 1978. Measuring preference in selective predation. Ecology 59, 211e215. Creel, S., Creel, N.M., 2002. The African Wild Dog: Behavior, Ecology, and Conservation. Princeton University Press, Princeton.
Dawkins, R., Krebs, J.R., 1979. Arms races between and within species. Proceedings of the Royal Society of London (Series B) 205, 489e511. Garrott, R.A., Bruggeman, J.E., Becker, M.S., Kalinowski, S.T., White, P.J., 2007. Evaluating prey switching in wolf-ungulate systems. Ecological Applications 17, 1588e1597. Gaston, K.J., 1994. Rarity. Chapman & Hall, London, UK. Hamilton, W.D., 1971. Geometry of the selfish herd. Journal of Theoretical Biology 31, 295e311. Harrington, R., Owen-Smith, N., Viljoen, P.C., Biggs, H.C., Mason, D.R., Funston, P.J., 1999. Establishing the causes of the roan antelope decline in the Kruger National Park, South Africa. Biological Conservation 90, 69e78. Hayward, M.W., 2006. Prey preferences of the spotted hyaena Crocuta crocuta and evidence of dietary competition with lion Panthera leo. Journal of Zoology 270, 606e614. doi:610.1111/j.1469-7998.2006.00184.x. Hayward, M.W., 2009. Moving beyond the descriptive: predicting the responses of top-order predators to reintroduction. In: Hayward, M.W., Somers, M.J. (Eds.), Reintroduction of Top-order Predators. Blackwell Publishing, Oxford, UK, pp. 345e370. Hayward, M.W., Henschel, P., O’Brien, J., Hofmeyr, M., Balme, G., Kerley, G.I.H., 2006a. Prey preferences of the leopard (Panthera pardus). Journal of Zoology 270, 298e313. Hayward, M.W., Hofmeyr, M., O’Brien, J., Kerley, G.I.H., 2006b. Prey preferences of the cheetah Acinonyx jubatus: morphological limitations or the need to capture rapidly consumable prey before kleptoparasites arrive? Journal of Zoology 270, 615e627. doi:610.1111/j.1469-7998.2006.00184.x. Hayward, M.W., O’Brien, J., Hofmeyr, M., Kerley, G.I.H., 2006c. Prey preferences of the African wild dog Lycaon pictus: ecological requirements for their conservation. Journal of Mammalogy 87, 1122e1131. Hayward, M.W., Hofmeyr, M., O’Brien, J., Kerley, G.I.H., 2007a. Testing predictions of the prey of the lion (Panthera leo) derived from modelled prey preferences. Journal of Wildlife Management 71, 1567e1575. Hayward, M.W., O’Brien, J., Kerley, G.I.H., 2007b. Carrying capacity of large African predators: predictions and tests. Biological Conservation 139, 219e229. doi:210.1016/j.biocon.2007.1006.1018. Hayward, M.W., Kerley, G.I.H., 2005. Prey preferences of the lion (Panthera leo). Journal of Zoology 267, 309e322. Hayward, M.W., Kerley, G.I.H., 2008. Prey preferences and dietary overlap amongst Africa’s large predators. South African Journal of Wildlife Research 38, 93e108. Hong, Y.S., Ryoo, M.I., 1991. Effect of temperature on the functional and numerical responses of Lasiophagus distinguendus (Hymenoptera: Pteromalidae) to various densities of the host, Sitophilus oryzae (Coleoptera: Curculionidae). Journal of Economic Entomology 84, 837e840. Hughes, R.G., 1986. Theories and models of species abundance. American Naturalist 128, 879e899. 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Meena, V., Jhala, Y.V., Chellam, R., Pathak, B., Implications of diet composition of Asiatic lions for their conservation. Journal of Zoology, in press. Morrell, L.J., Ruxton, G.D., James, R.E., 2010. Spatial positioning in the selfish herd. Behavioral Ecology 21, 1367e1373. Murdoch, W.W., 1969. Switching in general predators: experiments on predator specificity and stability of prey populations. Ecological Monographs 39, 335e354. Murray, B.R., Lepschi, B.J., 2004. Are locally rare species abundant elsewhere in their geographical range? Austral Ecology 29, 287e293. Norbury, G.L., Sanson, G.D., 1992. Problems with measuring diet selection of terrestrial, mammalian herbivores. Australian Journal of Ecology 17, 1e7. Owen-Smith, N., Mills, M.G.L., 2008a. Predator-prey size relationships in an African large-mammal food web. Journal of Animal Ecology 77, 173e183. Owen-Smith, N., Mills, M.G.L., 2008b. 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Original article
Scarcity in the prey community yields anti-predator benefits Matt W. Hayward* Mammal Research Institute, Polish Academy of Science, ul. Waszkiewicza 1, 17-230 Białowiez_ a, Poland1 Centre for African Conservation Ecology, Nelson Mandela Metropolitan University, PO Box 77000, Port Elizabeth 6031, South Africa School of Biological, Earth and Environmental Science, University of New South Wales, Sydney 2052, Australia
a r t i c l e i n f o
a b s t r a c t
Article history: Received 28 July 2010 Accepted 16 March 2011 Available online 8 April 2011
The majority of individuals in a community belong to a small number of abundant species. Understanding why some species are rare and others are common has been a long-held goal for ecologists. Africa’s large carnivore guild preferentially preys on a small number of species within a limited weight range. Within this weight range however, some species that are expected to be significantly preferred as prey are not. I tested whether these species avoid preferential predation through their low densities. Records of over 40,000 kills from up to 48 different communities were used to test if non-preferred species within the expected prey weight ranges of each large predator avoid preferential predation and why. Species expected to be prey of Africa’s large predators based on their body mass, that are preferred are preyed upon significantly more frequently at low densities than non-preferred prey. This results in a negative relationship between relative abundance and preference for preferred prey, but a positive relationship for non-preferred prey. The non-preferred prey species that are within the expected prey weight ranges of Africa’s large predators are significantly less abundant within the prey community than significantly preferred prey. Rarity in African ungulates may convey an anti-predator benefit in that it was suboptimal for predators to evolve morphological or behavioral strategies to optimally forage on them or in that prey species can avoid predators by existing in habitats with low carrying capacity. Ó 2011 Elsevier Masson SAS. All rights reserved.
Keywords: African large carnivores Density-dependence Predation Predator avoidance strategy Predatoreprey interactions Prey switching Top-down limitation
1. Introduction In animal and plant communities, the majority of individuals belong to a small number of abundant species, while most species are represented by a small number of individuals (Hughes, 1986; May, 1975). Understanding why some species are rare and others common within local communities has long been a goal of ecologists (Gaston, 1994) and there is a growing body of evidence to suggest that naturally rare species have traits that differ from naturally common species (Kunin and Gaston, 1993). Predators and their prey are often considered to be in an evolutionary arms race to eat or be eaten (Dawkins and Krebs, 1979). This analogy implies that predators evolve improved abilities to capture prey, which leads to prey evolving abilities to avoid capture (Abrams, 1986). Theoretical and mathematical models do not support this analogy however (Abrams, 1986; Brodie and Brodie, 1999). One reason for this may be the presence of secondary prey
* Present address: Australian Wildlife Conservancy, PO Box 432, Nichol’s Point 3501, Australia. Tel.: þ613 50245859; fax: þ613 50271200. E-mail address: [email protected]. 1 Tel.: þ4885 6827781; fax: þ4885 6827752. 1146-609X/$ e see front matter Ó 2011 Elsevier Masson SAS. All rights reserved. doi:10.1016/j.actao.2011.03.003
species that provide a buffer to predators in times of primary prey shortages (Pech et al., 1995). Primary prey are likely to be those that a predator has evolved to preferentially and optimally prey upon, whereas secondary prey are likely to be prey species that a predator has not evolved to preferentially prey upon but rather are preyed upon during prey switching (Garrott et al., 2007). Predators exhibit two distinct preference categories of prey: preferred prey species and the preferred weight range of prey (Hayward et al., 2006a). Preferred prey species are those preyed upon by predators significantly more frequently than expected based on the relative abundance of that prey species in the prey community (akin to primary prey). The preferred weight range is a range of prey body masses that a particular predator preys upon more frequently than expected (hereafter termed ‘expected prey’). Amongst this group of species that are expected to be preyed upon, there are species that are significantly preferred (primary prey), but also species that are not preferentially killed by predators (secondary prey). One hypothesis for the presence of these nonpreferred prey species within the expected weight range is that they are intrinsically rare in the prey community, which has meant that predators have not evolved morphological or behavioral adaptations that allow preferential predation (Hayward, 2009). Species outside the expected prey weight range are not preferred
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because they are too small to provide sufficient energetic reward for hunting them or are too large and thereby are too risky to hunt optimally (Hayward, 2009). High abundance is itself not necessarily the most successful evolutionary strategy a species can employ. Individuals obtain relatively short-term advantages by existing in high abundance through reducing the likelihood of any single individual being preyed upon (Hamilton, 1971; Morrell et al., 2010). An alternative evolutionary strategy is for individuals to persist at lower density and thereby avoid predators evolving morphological or behavioral adaptations to prey specifically on them. In this study, we aimed to test whether these non-preferred prey species within the expected prey weight ranges of Africa’s large predator guild (African wild dogs Lycaon pictus, cheetahs Acinonyx jubatus, leopards Panthera pardus and lions Panthera leo) avoid predation through their low densities. We then discuss whether occurring at low densities could be an evolutionary strategy to minimize top-down limitation as predators were less likely to evolve features to preferentially prey on rare species. The key tenet of this study is that some species are inherently rare in their natural environments and even when freed from competition and predation, these species never reach the densities of the dominant members of the community. There is evidence elsewhere to support this. For example, dormice Muscadinus avellanarius are relatively K-selected small mammals that have an inherently low population density and intrinsic rate of increase because their lack of a caecum necessitates diet specialization and, therefore, specific habitat requirements (Bright and Morris, 1996). Similarly, 91% of 57 locally rare open forest plant species occurred in high density somewhere in their range, but the remaining species were rare throughout their entire distributions (Murray and Lepschi, 2004). Other botanical studies have also found a proportion of the community is inherently rare (McIntyre et al., 1993; Rabinowitz et al., 1986). Carnivores are inherently rare due to their trophic position, however even within large carnivore guilds some species are much rarer than others (Creel and Creel, 2002). It is acknowledged that the term ‘rare’ describes an array of spatial and temporal patterns of abundance (Kunin and Gaston, 1993), but here it is used where no particular measure or pattern is implied. 2. Materials and methods Published records of over 40,000 kills from up to 48 different spatial locations or temporal periods were compiled in the derivation of the prey preferences and preferred weight range of Africa’s large predator guild (Hayward, 2009; Hayward and Kerley, 2008). These data come from numerous published and unpublished sources and are referred to in the original prey preference studies (Hayward, 2006; Hayward et al., 2006a; Hayward et al., 2006b, 2007a; Hayward and Kerley, 2005, 2008; Hayward et al., 2006c). All sites were from sub-Saharan African savannas. The database housing this information was interrogated and information on the preference of each prey species and its relative abundance in the prey community of a site was extracted. Preference was determined using Jacobs’ index (Jacobs, 1974):
D ¼
rp r þ p 2rp
where r is the proportion of a predator’s total kills of a certain prey species at a site and p is the proportional abundance of that prey species in that prey community. Many selectivity indices have been described (Krebs, 1989); however, all have biases at small proportions and none is considered superior to the rest (Chesson, 1978; Strauss, 1979). Consequently,
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researchers often overstate the accuracy of their preference results (Norbury and Sanson, 1992), particularly with the most commonly used techniques such as the forage ratio and Ivlev’s electivity index (Ivlev, 1961). These two indices suffer from non-linearity, bias to rare food items, increasing confidence intervals with increasing heterogeneity, being unbound or undefined, and lacking symmetry between selected and rejected values (Jacobs, 1974). Confidence intervals also become excessive for proportions below about 10% (Strauss, 1979). Jacobs’ index is one method that minimize these biases (Krebs, 1989), however measures of preference also exist (e.g. Owen-Smith and Mills, 2008b). We have used Jacobs’ index because it was used to derive the original prey preference data (Hayward, 2006; Hayward et al., 2006a,b,c; Hayward and Kerley, 2005) and solving Jacobs’ index has allowed the accurate prediction of predator diet (Hayward et al., 2007a; Meena et al., in press) and carrying capacity (Hayward et al., 2007b). A Jacobs’ index value was calculated for all prey species at each site. Values approaching 1 reflect a preference, those approaching 1 reflect avoidance, and those near 0 indicate a species is killed as frequently as expected based on its relative abundance at a site. Preferred prey species were calculated using t- or sign tests against means of 0 for each prey species, while the expected prey weight range of each predator was estimated as the body mass range encompassing the preferred prey species (Hayward et al., 2006a). Site-specific Jacobs’ index values (D) of each significantly preferred prey species or those expected prey of each large African predator were then related to their relative abundance (p) in the community at that site. The slopes of these linear regressions for
Table 1 Prey species expected to be preferentially killed by each large African predator (i.e. those within the preferred prey weight range), their body mass, the slope of the regression between their relative abundance in the prey community and their preference by the predator (based on Jacobs’ index), and whether they are significantly preferred or not. Species
Scientific name
Mass Predator
Slope
Preferred
Blesbok Bushbuck Impala Thomson’s gazelle Grant’s gazelle Nyala Reedbuck Springbok Warthog Buffalo Eland Gemsbok Giraffe Roan Sable Waterbuck Wildebeest Zebra Bushbuck Duiker Impala Klipspringer Reedbuck Springbok Thomson’s gazelle Bushbuck Duiker Impala Kudu Reedbuck Springbok Thomson’s gazelle Wildebeest
Damaliscus dorcas Tragelaphus scriptus Aepyceros melampus Gazella thomsoni G. granti T. angusi Redunca redunca Antidorcas marsupialis Phacochoerus africanus Syncerus caffer T. oryx Oryx gazelle Giraffa cameloparalis Hippotragus equines H. niger Kobus ellipsiprymnus Connochaetes taurinus Equus burchelli
52.5 23 30 15 38 47 32 26 45 435 345 158 550 220 180 190 135 175 23 16 30 10 32 26 15 23 16 30 135 32 26 15 135
6.43 1.94 0.34 0.56 0.37 4.14 1.25 1.18 3.19 1.48 4.94 0.48 4.78 10.65 1.66 0.91 1.34 1.72 0.01 1.98 0.19 8.92 0.14 2.8 0.15 9.01 0.21 0.32 2.09 5.91 17.28 1.28 0.88
Yes No Yes Yes Yes No No Yes No Yes No Yes Yes No No No Yes Yes Yes Yes Yes No No No No Yes Yes No Yes No No Yes No
Sylvicapra grimmia Oreotragus oreotragus
T. strepsiceros
Cheetah Cheetah Cheetah Cheetah Cheetah Cheetah Cheetah Cheetah Cheetah Lion Lion Lion Lion Lion Lion Lion Lion Lion Leopard Leopard Leopard Leopard Leopard Leopard Leopard Wild dog Wild dog Wild dog Wild dog Wild dog Wild dog Wild dog Wild dog
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significantly preferred and non-preferred prey species were then compared using a t-test. The data were normally distributed. Given relative abundance (p) is used in the derivation of Jacobs’ index (D), I hypothesized that there should be a negative relationship between these two variables if the proportional kills (r) remained constant and relative abundance (p) varied. A positive relationship would indicate a predator kills a prey species (r) proportionally more frequently as it becomes more common within the prey community (p). That is, prey species lose the protection of rarity. The preferred prey species of the African wild dog are kudu, Thomson’s gazelle, bushbuck and common duiker, and the bimodal expected prey weight range is from 16 to 32 kg and from 120 to 140 kg (Hayward et al., 2006c). Blesbok, impala, springbok and Thomson’s and Grant’s gazelles are significantly preferred by cheetahs, and their expected prey weigh from 23 to 56 kg (Hayward et al., 2006b). Leopard prefer prey within a range of 10e40 kg and significantly prefer bushbuck, impala and common duiker (Hayward et al., 2006a). Lions significantly prefer blue wildebeest, buffalo, gemsbok, giraffe and plain’s zebra, and are expected to kill prey within a range of 190e550 kg (Hayward and Kerley, 2005). Spotted hyaenas were not included in this study because they do not have any significantly preferred prey species (Hayward, 2006). These species were determined to be significantly preferred using t-tests against a mean of 0 throughout the entire distribution of
each predator (Hayward, 2009; Table 1). Species whose body mass was within 10% of the lower value of the expected prey were also included because of the less precise derivation of the expected weight range. I used the preferred prey weight range derived from this series of studies rather than using other ranges (e.g. OwenSmith and Mills, 2008a) to maintain similar data sources and because this present series of studies looked at prey preferences from throughout the range of each predator rather than sitespecific preferences. 3. Results Species that are within the expected weight range of Africa’s large predators but are not preferred are significantly less abundant within the prey communities than preferred prey (ManneWhitney U ¼ 18730.5, n ¼ 475, p < 0.001). Non-preferred prey are significantly less abundant within the expected prey weight range of lion (U ¼ 1527, n ¼ 210, p < 0.001), cheetah (U ¼ 309, n ¼ 81, p < 0.001), and wild dog (U ¼ 972, n ¼ 109, p ¼ 0.008), but not leopard (U ¼ 494.5, n ¼ 75, p ¼ 0.090). For the prey of lion, all preferred species become less preferred at higher density whereas non-preferred species within the expected prey weight range became increasingly preferred at higher density (Fig. 1; Table 1). Leopard preferred and non-preferred but expected
Fig. 1. Relationship between the relative abundance in the available prey community of preferred and expected prey of lions and the preference lions’ have for it (based on Jacobs’ index).
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prey follow the same trends (Fig. 2; Table 1). Cheetah preferred prey species also exhibit these relationships, although preferred gazelles (Antilopinae) are similarly preferred irrespective of their relative abundance (Fig. 3; Table 1). Conversely, reedbuck and warthog are most preferred by cheetahs when they are at low relative abundance. Non-preferred prey that are expected to be preferentially hunted by wild dogs exhibit similar relationships, however the preferred bushbuck and kudu are more frequently preyed upon when they are relatively abundant members of the prey community, while impala are preyed upon relatively frequently irrespective of abundance (Fig. 4; Table 1). As hypothesized, prey within the expected weight ranges of large predators that are preferred are killed significantly more frequently at low densities than non-preferred prey. This results in a negative relationship between relative abundance and preference for preferred prey (Fig. 5). Prey species that are expected to be killed preferentially but are not, exhibit a positive relationship (Fig. 5). The difference between the slopes of preferred and non-preferred prey species are significant (t ¼ 2.363, d.f. ¼ 31, p ¼ 0.025; Fig. 5). 4. Discussion Species within the expected prey weight range of each large, African predator are all expected to be preferentially preyed upon, however several prey species exist within this range that are not preferentially killed. These species are avoided at low density, and only become preferentially preyed upon at high densities reflecting their status as secondary prey upon which predators turn to by prey switching (Garrott et al., 2007; Murdoch, 1969). These prey species are killed at greater frequency (r) when they are more abundant (p) within the prey community, which leads to increased preference (D). The benefits these species derive from the low predation rates at low density is reflected in the mean density of these species within the prey community where they occur. These non-preferentially preyed upon species are rarer throughout sub-Saharan Africa than
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the species within the expected weight ranges of Africa’s large predators that are preferentially preyed upon. This indicates that these species have evolved to occur naturally at low densities and thereby avoid entering into an evolutionary ‘arms race’ with a large predator to optimally forage upon them. In essence, their rarity within the prey community means that it is suboptimal for a predator to have evolved morphological or behavioral strategies to optimally forage on them. These species are unlikely to be limited by top-down factors, but rather bottom-up and competitive factors. This is not to say predation is the limiting factor here, as bottom-up (morphological specialization, competitive influences or social factors) limitations are far more likely to be the reason. Rather, predators have not evolved strategies to preferentially prey on these species because they are invariably rare in the environment and when their habitat is invaded by range expanding preferred prey (such as zebra moving into roan habitat in South Africa’s Kruger National Park) the rare species may become selected for (Harrington et al., 1999). That is, the rare prey species reduce their risk of predation by occupying habitats with low carrying capacity. The negative relationship between preference and abundance for preferred prey (Fig. 5) may be an artifact of the derivation of Jacobs’ index, which is theoretically biased as prey become less relative abundant (Jacobs, 1974; Strauss, 1979). For example, if a theoretical lion population rigidly made 50% of their kills as wildebeest (40% of available prey), 40% as zebra (40% of available prey) and 10% other species (20% of available prey), then the Jacobs’ index value for wildebeest is 0.2. However if buffalo made up 50% of the available prey community but are not killed and wildebeest and zebra comprise the remainder under the same predation rates, then this value for wildebeest increases by 250% to 0.5. However, lion are not inflexible model organisms and appear to follow optimal foraging rules (Hayward and Kerley, 2005). Furthermore, the ability of the Jacobs’ index equation to be solved to accurately predict the diet of lions in Africa and India (Hayward et al., 2007a; Meena et al., in press) suggests it is highly robust to these potential biases.
Fig. 2. Relationship between the relative abundance in the available prey community of leopard preferred prey species or those expected to be preyed upon and the preference leopards’ have for it (based on Jacobs’ index).
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Fig. 3. Relationship between the relative abundance in the available prey community of cheetah preferred prey species or those expected to be preyed upon and the preference leopards’ have for it (based on Jacobs’ index).
Irrespectively, this potential bias holds in the same direction for less common, expected prey species and this departure from a neutral pattern must therefore reflect a positive behavioral response by the predator to increased prey availability. Kunin and Gaston (1993) describe four processes which may bias the creation and maintenance of rarity. Firstly, it may be the characteristics of a species that cause it to be rare, rather than being a consequence of rarity. This seems unlikely in predatoreprey interactions as predation is a factor reducing population density. Secondly, extinction risk may influence the list of rare species (Kunin and Gaston, 1993), however there was no evidence of this here. Thirdly, rarity has behavioral, ecological or genetic consequences that may influence the perception of rarity (Kunin and Gaston, 1993), however this seems unlikely to occur in such widely distributed species as studied here. Consequently, we are
left with the possibility that the rare species studied here have evolved the adaptation of rarity over evolutionarily meaningful time periods, which in this case appears to convey protection from preferential predation (Kunin and Gaston, 1993). It is not surprising that rare species differ in characteristics of predatoreprey interactions given the breadth of differences they have been shown to have (Kunin and Gaston, 1993). Furthermore, among insects there are differences in functional and numerical responses of common versus rare species (Hong and Ryoo, 1991). Predators that are inherently rare in the environment may have evolved the same strategy to avoid intraguild predation and competition because of their high dietary overlap (Owen-Smith and Mills, 2008a). Cheetahs and African wild dogs are orders of magnitude less abundant than the dominant members of the guild (lions, hyaenas and leopards) (Creel and Creel, 2002). This may also
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Fig. 4. Relationship between the relative abundance in the available prey community of African wild dog preferred prey species or those expected to be preyed upon and the preference leopards’ have for it (based on Jacobs’ index).
be caused by changes in the availability of preferred prey species (Hayward and Kerley, 2008). The preferred prey of leopard are not significantly more abundant in the prey community than non-preferred prey, in contrast to
the rest of the guild. This illustrates the opportunistic nature of leopard predation and is reflected in its ability to persist amongst a diverse range of prey communities throughout its vast African and Asian range. Spotted hyaenas exhibit non-preferential predation
Slope of relationship between Jacobs' index value and relative abundance
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4
3
2
1
0 Not significantly preferred
Significantly preferred
-1
-2 Species within preferred prey weight range or that were significantly preferred
Fig. 5. Mean (1 S.E.) of the slopes of the relationship between prey relative abundance and Jacobs’ preference value for large African carnivores.
(Hayward, 2006) and, like leopards, are unlikely to be significant top-down influences on primary prey because of the frequency with which they switch to secondary prey species. Predatoreprey interactions in temperate climates may not function in the manner seen in Africa. This is likely to be due to the simplified nature of these ecosystems where there are insufficient resources available to support more than a single predator e single prey interaction. There are conservation implications for this research. In unaltered environments, rare species may be largely immune to topdown population regulation. However, when disturbances occur that alter equilibrium states (e.g. the creation of artificial water points), then factors might arise that lead to high, preferential predation rates. This occurred in Kruger National Park, South Africa, and ultimately led to the decline of the roan antelope Hippotragus equines population (Harrington et al., 1999; Hayward et al., 2007a). 5. Conclusions Data obtained from over 40,000 kill records have revealed that Africa’s large predators preferential prey on a few species within a preferred weight range. Species occurring within the weight range but are uncommon are not preferentially preyed upon suggesting rarity in African ungulates may convey an anti-predator benefit in that it was suboptimal for predators to evolve morphological or behavioral strategies to optimally forage on them or, more likely, because scarce prey species occupy habitats that do not support sufficient individuals to allow predators a satisfactory likelihood of encounter. Acknowledgments MWH was supported by the Marie Curie Transfer of Knowledge project e BIORESC MTKD-CT-2005-029957 e financed by the 6th Framework Programme of the European Union. References Abrams, P.A., 1986. Is predator-prey coevolution an arms race? Trends in Research of Ecology and Evolution 1, 108e110. Bright, P.W., Morris, P.A., 1996. Why are dormice rare? A case study in conservation biology. Mammal Review 26, 157e187. Brodie III, E.D., Brodie Jr., E.D., 1999. Predator-prey arms races. BioScience 49, 577e588. Chesson, J., 1978. Measuring preference in selective predation. Ecology 59, 211e215. Creel, S., Creel, N.M., 2002. The African Wild Dog: Behavior, Ecology, and Conservation. Princeton University Press, Princeton.
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