Vigilance, in the field of behavioural ecology, refers to an animal’s examination of its surroundings in order to heighten awareness of predator presence. Vigilance is an important behaviour during foraging as animals must often venture away from the safety of shelter to find food. However being vigilant comes at the expense of time spent feeding so there is a trade-off between the two. The length of time animals devote to vigilance is dependent on many factors including predation risk and hunger.
Vigilance is often observed in animals that forage in groups, such as yellow-eyed juncos (Junco phaeonutus) and meerkats (Suricata suricatta). Foraging in groups dilutes an individual’s risk of predation, and allows them to reduce their own vigilance while the vigilance of the group is maintained [1]. Alarm signals may be used to alert the group to the presence of predators. Groups of some species have at least one individual on sentry duty who looks out for predators on a perch while the rest of the group forages [1].
Feeding and predation risk trade-off edit
Vigilance and feeding (both searching for and handling food) are generally mutually exclusive activities, leading to foragers facing a trade-off between energy intake and safety from predation. As time allocated to scanning reduces the time spent feeding, vigilant individuals must devote more time on foraging to obtain the required food intake [2]. This impedes on other activities in their time budget such as mating and prolongs their exposure to predation as foraging occurs away from shelter [2]. When foraging time is limited, vigilant animals are left with a reduced energy intake [2].
Optimality models can be used to predict foraging decisions of an animal based on costs (predation risk, starvation) and benefits (safety, food), which are also affected by physiology such as hunger levels [1].
Grey squirrels (Sciurus carolinensis) alter their behaviour according to the relative costs and benefits when foraging in the open [3]. Small food items are consumed immediately to maximise energy intake, as they require little handling time so the cost of predation risk is low [3]. Large items that require a long handling time, and hence time exposed to predators, are carried back to the safety of a tree to minimise predation risk [3]. Although there is an energetic cost to transporting food, large food items have a high contribution to nutrient intake so the cost outweighs the benefits [3].
The overall predation risk is a function of the abundance, activity and ability of predators to detect the forager, as well as the likelihood that the forager can escape the predator if it is not vigilant [4]. Animals prioritise vigilance over feeding when the predation risk is high. For example, yellow-eyed juncos spend more time scanning for predators when a potential predator, a Harris's hawk (Parabuteo unicinctus), is present compared to when the hawk is absent [5].
Another factor that influences vigilance is the ‘forager’s survivor’s fitness’ - the benefit that is expected from foraging in the absence of predation [4]. This is dependent on the quality of the food as well as the energetic state of the individual. If there is much to be gained from feeding, foragers may forgo vigilance. Similarly, if hungry animals have a higher chance of dying from starvation than from predation, it is more beneficial to sacrifice vigilance to fulfill their energy requirements. When three-spined sticklebacks (Gasterosteus aculeatus) are deprived of food, they prefer to feed in locations with a high density of water fleas [6]. The cost to this choice is that the sticklebacks must concentrate on picking out the prey so are less able to scan for predators however the risk of starvation is relatively higher than the risk of predation [6]. Similarly, juncos that have been deprived of food exhibit lower levels of vigilance, instead focusing on rapid feeding which is a behaviour incompatible with scanning [7].
Habitat and food choice edit
The state of an animal can change due to its behaviour and vice versa due to the dynamic feedback between foraging, body reserves and predation risk [1]. The feedback can influence an individual’s choice of where, when and what to feed on. If the predation risk is so great that an animal must maintain a level of vigilance that drastically inhibits feeding, it may opt for an alternative.
For example, the bluegill sunfish (Lepomis macrochirus) has the choice of foraging on plankton in the safety of reeds or on benthic invertebrates which are a better quality food source [8]. When a predator (the largemouth bass) is present, smaller sunfish spend the majority of their time foraging in the reeds despite this choice reducing their food intake and seasonal growth rate [8]. Sunfish that are too large to be eaten by the bass forage almost entirely on benthos. Although staying in the reeds means a slower growth rate and a longer period of being a size vulnerable to predators, for maximum survival sunfish choose to remain in the reeds feeding on plankton until they reach a certain size and then leave to feed on benthos [8].
Nocturnal animals alter the timing of their foraging based on the level of light – avoiding feeding when the moonlight is bright as this is when predation risk is highest [9].
A raised head is the most commonly used indicator of vigilance, as many animals require their heads to be lowered to search for and handle food [10]. Different foods require different handling that can affect the amount of vigilance an animal can maintain. Seeds without husks, for example, require little handling by birds so are rapidly pecked up with the birds head down which is incompatible with vigilance [11]. In situations of high predation risk, animals may choose foods that can be foraged while maintaining vigilance. When dark-eyed juncos (Junco hymenalis) feed in small flocks, they prefer to feed on larger pieces of food than when they are part of a larger flock [11]. As individuals in a small flock have a greater need to be vigilant (see more in Vigilance in groups), large pieces of food are more beneficial as they require a longer handling time that can be simultaneously spent scanning, whereas birds feeding on small pieces must intermittently stop foraging to scan their environment [11].
Vigilance in groups edit
Group foraging edit
Further information: Group foraging
Both solitary and group foraging come with a variety of costs and benefits, but for many animals, foraging in a group is the optimal strategy.
Advantages edit
A group of animals may be better at both finding and capturing food than solitary animals. For species that feed on food that is patchy, the likelihood of locating food is greater if individuals search for food independently and inform the rest of the group when a food patch is found [12]. Information sharing in this way has little cost to the individual who locates the food if it occurs in high abundance in the patch.
Group hunting allows predators to take down larger prey, as well as prey that can outrun the predator but can be caught by an ambush. For example, lionesses hunt cooperatively for large prey such as zebra (Equus burchelli) and wildebeest (Connochaetes taurinus), with each lioness adopting particular positions in a formation [13]. The presence of many predators also causes panic in prey, often leading to them fleeing in different directions making it easier for the predators to single out a target [1].
Foraging in a group also has some benefits that reduce the risk of predation. Being part of a group dilutes an individual’s risk of being attacked, as the more group members there are, the lower the probability that that individual will be the victim [14]. Grouping may swamp the predator’s capacity to capture prey - for example, hawks are unable to capture more than one yellow-eyed junco per attack [5]. Large groups also cause predator confusion as it makes it difficult to focus on one target and may engage in communal defences, such as mobbing, for further protection [1].
Grouping also helps to reduce predation risk by improving vigilance.
Disadvantages edit
Dilution of predation risk only occurs if groups of animals are not more prone to attack than individuals [1]. Often large groups are more conspicuous to predators so may increase the risk of attack. For example, blue acara cichlid fish (Aequidens pulcher) choose to attack shoals of guppies (Poecilia reticulate) based on how visually conspicuous they are, preferring shoals that are larger or exhibit more movement [15]. Foraging in groups requires sharing so may also lead to greater competition for food.
Effect of group size edit
Larger groups may have a greater overall vigilance than small groups due to the ‘many eyes’ hypothesis: more eyes scanning for predators means that the proportion of time that at least one individual is vigilant (collective vigilance) is higher [16][17]. This improved vigilance may allow an individual to decrease it’s own time allocated to vigilance without any increase in it’s personal risk of being attacked, particularly as large groups have a diluted predation risk [18]. This phenomenon of lower individual levels of vigilance with increasing group size has been observed in many bird, mammal and fish species [7]. Individual ostriches (Struthio camelus) and greater rheas (Rhea americana) in large groups both spend less time with their head up than individuals in small groups, however collective vigilance increases with group size in ostriches but not rheas [19][17]. Therefore the many eyes hypothesis does not always hold. Although individuals in groups may be able to decrease the time spent scanning, and hence reach their energy requirements in a shorter period of time, the increased competition for food in groups may mean that animals need to devote more time overall to foraging due to an increased allocation of time for aggressive behaviour during foraging [18]. For example, the rate of fighting between house sparrows (Passer domesticus) increases with the size of the flock [20].
Alarm signals edit
Further information: Alarm signal
Large groups of animals are able to detect predators earlier because of the higher probability that at least one individual is being vigilant when the predator approaches. As many predators rely on the element of surprise in successful attacks, early detection of predators reduces predation risk [1]. The detection of a predator by one individual only translates to collective detection if that individual makes some sort of signal to alert the rest of the group. The signal may be a deliberate call made by the vigilant individual (as in the case of meerkats) or simply the departure of the individual who has detected the predator.
Flocks of birds often exhibit collective detection. One or more birds initially detect the threat, and other birds that did not perceive the threat detect their departure and also respond by fleeing [7]. The departure of multiple birds simultaneously is likely to be a more effective alarm signal as birds regularly depart flocks for reasons other than the detection of predators [7].
Water skaters (Halobates robustus) transmit predator avoidance behaviour through the group as individuals at the edge of the flotilla detect a predator and move, bumping into their neighbours, who in turn start moving and bumping into more water skaters [21]. This ‘wave’ of alarm has been termed the ‘Trafalgar Effect’ [21].
Sentinels edit
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In some species, individuals in a foraging group take on sentry duty. The sentinels look out for predators, often from a good vantage point, while the rest of the group forages and sound an alarm when they spot a predator [1]. Sentry duty is particularly important for species whose foraging activity is incompatible with vigilance, and feed in areas where they are highly exposed to predation risk. For example, dwarf mongoose (Helogale parvula) dig up arthropods from the ground, which requires fixation of both their vision and olfaction on the prey [22].
Often, the sentry makes quiet calls that function as a ‘watchman’s song’ that alerts the rest of the group that an individual is on guard [23]. In response to a vocalising sentry, pied babblers (Turdoides bicolor) decrease their own vigilance, spread out further from the group and forage in more exposed patches resulting in a higher intake of biomass [24] .
Guarding seems to be an altruistic behaviour as an individual on sentry duty is unable to feed and may be more exposed to predators. However meerkats on sentry duty are at no greater risk of predation as they are generally the first to detect predators and flee to safety [25]. Meerkats also only go on guard once they are satiated so if no other individual is on sentry duty, guarding may be the most beneficial behaviour as the individual has no requirement for feeding and can benefit from early predator detection [25].
Cheating edit
In a large group, it is possible for an individual to cheat by scanning less than other members of the group without having any negative effect on the collective vigilance of the group. Cheating would seem to be the most beneficial strategy as the individual still benefits from the collective detection of the group while being able to feed more than other individuals. However if this were the case, then cooperation would not be a stable strategy [26]. The evolutionarily stable (ESS) scanning rate is the rate that if all group members adopted, an individual that scanned more or less frequently would have a lower chance of survival [26].
Maintaining individual vigilance may be a more beneficial strategy if vigilant animals gain some sort of advantage [27]. Non-vigilant individuals are often the last to flee to safety, as groups flee in succession from the individual who spots the predator, individuals who were vigilant when the first animal departs, and finally the non-vigilant individuals [28]. Cheetahs (Acinonyx jubatus) select less vigilant Thomson's gazelles (Eudorcas thomsonii) before initiating a chase and target them for attack [29].
References edit
- ^ a b c d e f g h i Davies, N.B., Krebs, J.R. & West, S.A. (2012) An Introduction to Behavioural Ecology 4th edn, Wiley-Blackwell, Oxford, UK
- ^ a b c Illius, A.W. & Fitzgibbon, C. (1994) Costs of vigilance in foraging ungulates. Animal Behaviour 47: 481-484
- ^ a b c Lima, S.L., Valone, T.J. & Caraco, T. (1985) Foraging-efficiency – predation-risk trade-off in the grey squirrel. Animal Behaviour 33: 155-165
- ^ a b Brown, J.S. (1999) Vigilance, patch use and habitat selection: foraging under predation risk. Evolutionary Ecology Research 1: 49-71
- ^ a b Caraco, T., Martindale, S. & Pulliam, H.R. (1980) Avian flocking in the presence of a predator. Nature 285: 400-401
- ^ a b Milinski, M. & Heller, R. (1978) Influence of a predator on the optimal foraging behaviour of sticklebacks (Gasterosteus aculeatus). Nature 275: 642-644
- ^ a b c d Lima, S.L. (1995) Back to the basics of anti-predatory vigilance: the group-size effect. Animal Behaviour 49: 11-20
- ^ a b c Gilliam, J.F. (1982) Foraging under mortality risk in size-structured populations. PhD thesis. Michigan State University, MI
- ^ Clarke, J.A. (1983) Moonlight’s influence on predator/prey interactions between short-eyed owls (Asio flammeus) and deermice (Peromyscus maniculatus). Behavioural Ecology and Sociobiology 13: 205-209
- ^ Makowska, J. & Kramer, D.L. (2007) Vigilance during food handling in grey squirrels, Sciurus carolinensis. Animal Behaviour 74: 153-158
- ^ a b c Lima, S.L. (1988) Vigilance and diet selection: a simple example in the dark-eyed junco. Canadian Journal of Zoology 66: 593-596
- ^ Clark, C.W. & Mangel, M. (1984) Foraging and flocking strategies: information in an uncertain envrionment. The American Naturalist 123(5): 626-641
- ^ Stander, P.E. (1992) Cooperative hunting in lions: the role of the individual. Behavioural Ecology and Sociobiology 29: 445-454
- ^ Foster, W.A. & Treherne, J.E. (1981) Evidence for the dilution effect in the selfish herd from fish predation on a marine insect. Nature 293: 466-467
- ^ Krause, J. & Godin, J.J. (1995) Predator preferences for attacking particular prey group sizes: consequences for predator hunting success and prey predation risk. Animal Behaviour 50: 465-473
- ^ Lima, S.L. & Dill, L.M. (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Canadian Journal of Zoology 68: 619-640
- ^ a b Fernandez, G.J., Capurro, A.F. & Reboreda, J.C. (2003) Effect of group size on individual and collective vigilance in greater rheas. Ethology 109: 413-425
- ^ a b Roberts, G. (1996) Why individual vigilance declines as group size increases. Animal Behaviour 51: 1077-086
- ^ Bertram, B.C.R. (1980) Vigilance and group size in ostriches. Animal Behaviour 28: 278-286
- ^ Barnard, C.J. (1980) Factors affecting flock size mean and variance in a winter population of house sparrows (Passer domesticus L.) Behaviour 74(1):114-127
- ^ a b Treherne, J.E. & Foster, W.A. (1981) Group transmission of predator avoidance behaviour in a marine insect: the Trafalgar Effect. Animal Behaviour 29: 911-917
- ^ Rasa, O.A.E. (1986) Coordinated vigilance in dwarf mongoose family groups: the ‘Watchman’s Song’ hypothesis and the costs of guarding. Ethology 71: 340-344
- ^ Wickler, W. (1985) Coordination of vigilance in bird groups, the ‘Watchman’s Song’ hypothesis. Zeitschrift fur Tierphysiologie, Tierernahrung und Futtermittelkunde 69: 250-253
- ^ Hollen, L.I., Bell, M.B.V. & Radford, A.N. (2008) Cooperative sentinel calling? Foragers gain increased biomass intake. Current Biology 18: 576-579
- ^ a b Clutton-Brock, T.H., O’Riain, M.J., Brotherton, P.N.M., Gaynor, D., Kansky, R., Griffin, A.S. & Manser, M. (1999) Selfish sentinels in cooperative mammals. Science 284: 1640-1644
- ^ a b Pulliam, H.R. (1982) The scanning behavior of juncos: a game-theoretical approach. Journal of Theoretical Biology 95: 89-103
- ^ McNamara, J.M. & Houston, A.I. (1992) Evolutionarily stable levels of vigilance as a function of group size. Animal Behaviour 43: 641-658
- ^ Lima, S.L. (1994) On the personal benefits of anti-predatory vigilance. Animal Behaviour 48: 734-736
- ^ Fitzgibbon, C.D. (1989) A cost to individuals with reduced vigilance in groups of Thomson’s gazelles hunted by cheetahs. Animal Behaviour 37(3): 508-510