New statistical tools for analyzing the structure of animal groups

The statistical characterization of the spatial structure of large animal groups has been very limited so far, mainly due to a lack of empirical data, especially in three dimensions (3D). Here we focus on the case of large flocks of starlings (Sturnus vulgaris) in the field. We reconstruct the 3D positions of individual birds within flocks of up to few thousands of elements. In this respect our data constitute a unique set. We perform a statistical analysis of flocks' structure by using two quantities that are new to the field of collective animal behaviour, namely the conditional density and the pair correlation function. These tools were originally developed in the context of condensed matter theory. We explain what is the meaning of these two quantities, how to measure them in a reliable way, and why they are useful in assessing the density fluctuations and the statistical correlations across the group. We show that the border-to-centre density gradient displayed by starling flocks gives rise to an anomalous behaviour of the conditional density. We also find that the pair correlation function has a structure incompatible with a crystalline arrangement of birds. In fact, our results suggest that flocks are somewhat intermediate between the liquid and the gas phase of physical systems.     

Behavioural and hormonal effects of social isolation and neophobia in a gregarious bird species, the European starling (Sturnus vulgaris)

Separating gregarious individuals from their group members often results in behavioural and physiological changes, like increased levels of corticosterone. Testosterone and corticosterone, in particular, have been implicated in the response of mammals to novelty. Data in birds are, however, rare. The presence or absence of group members may also influence an individual's response to novel stimuli. We assessed the behaviour and hormonal response of European starlings (Sturnus vulgaris) to a novel object in two different situations and seasons: each starling was tested when separated and when in contact with its group members in May/June (breeding season) and again in September/October (non-breeding season). Starlings are gregarious throughout the year, but as foraging flocks are small during the breeding season and large during the non-breeding season, we assumed that non-breeding starlings would be more affected by social isolation. Overall, starlings had higher levels of corticosterone, lost more body mass, and were more active when they were separated from their group. Isolated individuals, however, did not show a greater neophobic response than individuals in the presence of their group members in either season. Circulating levels of testosterone and corticosterone were higher after a test with novel object than after a test with only the familiar feeding dish in both sexes and seasons. However, control tests for handling effects confirmed only the increase in testosterone. Our study shows that social isolation is stressful for unrelated and unpaired members of a wild flocking bird species and demonstrates that novelty can lead to a rise in testosterone in birds.     

Vigilance responding to number of conspecifics among mixed groups of cranes in demilitarized zone

Numerous studies have addressed antipredatory benefits of mixed-species flocks of foragers, but studies on individual's vigilance as a function of group size are limited. In the Cheolwon area of the Korean Demilitarized Zone, vigilance of the subordinate White-naped cranes (Grus vipio) in 11 groups composed of conspecifics and the dominant Red-crowned cranes (Grus japonensis) was examined. Vigilance correlated negatively with group size due to negative correlation with the number of conspecifics, but not the dominant heterospecifics. This is consistent with the hypothesis that a decrease in vigilance in larger groups is due to antipredatory benefits from increased predator detection in larger groups (associated with the presence of a larger number of conspecifics). This suggested that the mechanism leads to canceling out of the otherwise expected antipredatory benefits to the subordinate species from the increased predator detection by larger group size (associated with larger number of dominants). This is one of only a few behavioral studies of these endangered crane species in the relatively inaccessible wintering area of international importance in the areas of high conservation value.     

Innate and Learned Components of Defence by Flickers Against a Novel Nest Competitor, the European Starling

Defence against predators is an important component of fitness in wild birds but the first step of defence, predator recognition, is not well understood. Anti‐predator behaviour may innate, in which case the individual responds without prior contact with that predator, and/or there may be a learned component that develops only after direct experience. In the wild, the development of anti‐predator behaviour is studied by exposing naive individuals to novel predators. I studied responses of 71 naive and experienced northern flickers Colaptes auratus, to a novel nest predator and competitor, the European starling Sturnus vulgaris that was introduced to North America. Naive individuals responded more intensely to the model starling than to the control model suggesting an innate component to recognition. However, there was also a learned component to defence because flickers nesting near to starlings reacted more aggressively than naive individuals far from starlings. Consistent with theory on life histories and optimal defence levels, no significant differences in aggression were found between the sexes or between age classes. Selection should favour more intense, and possibly innate, defence against the introduced starling. Variation in responses of naive individuals suggests that there may already be some alleles in the population associated with higher defence, but that these may not be uniform within the population.     

Conspicuous blue tails,dorsal pattern morphs and escape behaviour in hatchling Iberian wall lizards (Podarcis hispanicus)

Predation has profound effects on the phenotypes of animal prey and, in lizards, the relationship between coloration and antipredatory behaviour has been studied in depth. However, studies that address the relationships between dorsal patterns and tail coloration with escape behaviour in polymorphic lizards are absent in the literature. We describe dorsal morphs and measured tail coloration and escape behaviour in hatchling Iberian wall lizards, Podarcis hispanicus, a species with a previously undescribed female‐restricted dorsal polymorphism (reticulated‐blotched males, and either striped or reticulated‐blotched females) and juvenile tails with conspicuous blue coloration, which is probably used to divert predator attacks towards the autotomizable tail. Overall we provide evidence for the existence of sexual dimorphism in tail ultraviolet reflectance between reticulated females and males, with striped females being intermediate. We identified sex/dorsal morph, body size and tail brightness as predictors of different aspects of escape behaviour and suggest the existence of two alternative escape strategies between striped and reticulated‐blotched females that may be dependent on dorsal morph differences, independently of sex. Reticulated‐blotched females, and also males (all reticulated‐blotched), ran faster and spent less time paused than striped females, which might reflect an escape behaviour strategy based on endurance in striped females. In addition, lowland males displayed tail waving as a ‘last resort’ antipredator strategy that may be related to fatigue. We concluded that hatchling antipredatory behaviour is influenced by both dorsal pattern and tail conspicuousness. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 1094–1106.     

Egg concealment is an antipredatory strategy in a cavity‐nesting bird

Birds have developed different behavioural strategies to reduce the risk of predation during the breeding period. Bird species that nest in the open often cover their eggs to decrease the risk of predators detecting the clutches. However, in cavity nesters, the potential functions of egg covering have not been explored despite some bird species that nest in cavities also covering their eggs as open nesters do. We analysed whether egg covering is an antipredatory behaviour in the blue tit (Cyanistes caeruleus). We simulated an increase in the perceived risk of predation at experimental nests by adding predator scent inside the nest boxes during the egg‐laying period, whilst adding lemon essence or water to control nest boxes. Birds exposed to predator chemical cues in the nest of experimental pairs more frequently covered their eggs than birds exposed to an odorous control. These results suggest that egg covering may have evolved as an antipredatory behaviour also in cavity nesters to reduce the risk of egg predation and thus increase reproductive success in birds.     

Antipredatory behaviour in lizards: interactions between group size and predation risk

Group size effects on antipredatory behaviour are well documented in numerous animals, but little is known about how the level of predation risk influences this process. We tested the hypothesis that group size and level of risk interact to affect the levels of antipredatory behaviour in the group-living sun skink, Lampropholis delicata. We controlled the size of lizard groups (N=1, 2, 4, 8 or 12 females) and altered predation risk by providing either a basking tile covered with chemical cues from a predator (high risk) or one without scent (low risk). The time allocated to individual antipredatory behaviour decreased significantly with increasing group size. The relation between group size and time allocated to individual antipredatory behaviour was nonlinear and asymptotic, and did not change under low and high risks of predation. However, group size and predation risk interacted to affect significantly the time that lizards allocated to antipredatory behaviour. When the overall risk from predators was high, individual responsiveness decreased strongly as group size became larger. In contrast, when the overall risk from predators was low, individual responsiveness decreased weakly as group size became larger. Consequently, the time that lizards allocated to antipredatory behaviour under different risks of predation converged as group size increased.     

Behavioural thermoregulation and climatic range restriction in the globally threatened Ethiopian Bush‐crow Zavattariornis stresemanni

Climate may influence the distribution and abundance of a species through a number of demographic and ecological processes, but the proximate drivers of such responses are only recently being identified. The Ethiopian Bush‐crow Zavattariornis stresemanni is a starling‐like corvid that is restricted to a small region of southern Ethiopia. It is classified as Endangered in the IUCN Red List of globally threatened species. Previous work suggested that this range restriction is almost perfectly defined by a climate envelope that is cooler than surrounding areas, but the proximate mechanism remains unexplained. The heavily altered habitats which the species inhabits are widespread across Africa, and recent work has shown that the Bush‐crow is behaviourally adaptable and has a catholic diet. We assess whether its enigmatic distribution can be explained by behavioural responses to the higher temperatures that surround its current range. Using environmental niche models and field observations of thermally mediated behaviour, we compare the range restriction and behavioural thermoregulation of the Ethiopian Bush‐crow with those of two sympatric control species that are similar in size and ecology, but have much larger ranges that include hotter environments. White‐crowned Starling Lamprotornis albicapillus and Superb Starling L. superbus occupy similar habitats to the Ethiopian Bush‐crow and all three frequently forage together. We found that the Bush‐crow's range is limited primarily by temperature, with a secondary effect of dry season rainfall, whereas the ranges of the two starling species are better predicted by wet season rainfall alone. Bush‐crows exhibited panting behaviour and moved into the shade of trees at significantly lower ambient temperatures than did the starlings, and their food intake declined more steeply with increasing temperature. These results indicate that the limited geographical range of the Bush‐crow reflects an inability to cope with higher temperatures. This suggests that a species' response to climate change might not be easily predicted by its ecological generalism, and may represent an inherited debt from its evolutionary history.     

Energy,predators and the behavior of feeding hummingbirds

Summary Current evidence suggests that many animals trade off energy gain against the risk of predation while feeding. In contrast, energetic considerations alone have proven successful in explaining and predicting the behaviour of feeding hummingbirds. This success may reflect the relative lack of natural predation on hummingbirds, but this study suggests that it may additionally reflect the lack of studies taking a predation perspective. In particular, when Anna's hummingbirds (Calypte anna) are faced with an obstructed view of their surroundings, they engage in behaviour suggestive of anti-predatory vigilance. In doing so, they voluntarily reduce their rate of energy intake. These birds also forgo better feeding opportunities that occur close to the ground, where observations suggest they are wary of opportunistic predators such as roadrunners (Geococcys californianus). While energy-based concepts will remain useful in the study of hummingbird feeding behaviour, the lack of predation on these birds should not be equated with an insensitivity to the risk of predation. This realization may lead to further insights into hummingbird-plant interactions, and hummingbird biology in general.     

Avian pest control in tea plantations of sub-Himalayan plains of Northeast India: Mixed-species foraging flock matters

This study reports on the biocontrol role birds play in caterpillar pest control of tea plantations of Northeast India. In this area large tracts of tea plantations have been extensively defoliated by the recent invasion of two forest-dwelling geometrid looper caterpillars, Hyposidra spp. and a lymantriid hairy caterpillar, Arctornis submarginata. This exacerbated tea herbivory by two resident pest caterpillars, Biston suppressaria and Eterusia magnifera. Currently there are no identified resident insect predators for any life stage of Hyposidra spp. and A. submarginata. Larvae of these pests drop from tea bushes using salivary thread, allowing caterpillars to escape from insect predators. The study identified 38 native insectivorous bird species in tea plantations, of which four species (Asian-pied starling, Chestnut-tailed starling, Jungle Myna, Red-vented Bulbul) could be potential control agents of looper and hairy caterpillar pests. These species had high population densities. Their cumulative abundances represented a major proportion of the total bird community during both the infested (86.44%) and non-infested phase (75.34%). They foraged in mixed-species flocks in both tea foliage and on the ground. This behavior is suited to capture foliage-living and dropped caterpillars that were flushed from tea bushes by foraging birds. Abundance and species richness of overall tea layer-foraging birds were higher in infested phase when compared to non-infested phase. The predation rate of four bird species of the foraging flock varied significantly. These results suggest that birds should be considered as important biological control agent of caterpillar pests of tea and considered in pest management plans.     

Does risk of predation by mammalian predators affect the spacing behaviour of rodents? Two large-scale experiments

Predator-prey interactions between small mammals and their avian and mammalian predators have attracted much attention. However, large-scale field experiments examining small-mammal antipredatory responses under the risk of predation by mammals are rare. As recently pointed out, the scale of experiments may cause misleading results in studies of decision-making under predation risk. We studied the effect of small mustelid predators on the spacing behaviour of the gray-tailed vole (Microtus canicaudus) and the bank vole (Clethrionomys glareolus) in two separate field enclosure experiments. The experiments were conducted during the breeding season in North America and northern Europe, where small mustelids have been suggested to be important mammalian predators of voles. As in most of the earlier laboratory studies, predation risk was simulated using fresh mustelid faeces and urine. This made it possible to compare the results from experiments at different spatial scales. We did not find any effect of increased predation risk on spacing behaviour (mean and/or maximum distance moved and home range size) or trappability in either vole species. Simulated predation risk did not affect the breeding of females in gray-tailed voles, as has previously been shown in bank voles. The results disagree with most of the studies conducted in laboratory conditions with small mammals. We discuss whether this discrepancy could be caused by differences in the scale of the experiments. Received: 12 April 1999 / Accepted: 7 October 1999     

Where two oceans meet: distribution and offshore interactions of great-winged petrels Pterodroma macroptera and Leach’s storm petrels Oceanodroma leucorhoa off southern Africa

During seabird surveys off southern Africa, great-winged petrel Pterodroma macroptera and Leach’s storm petrel Oceanodroma leucorhoa were widespread and relatively common. Similar aerial displays, frequent (social) interactions, a tendency to “huddle” in tight (mixed) gatherings and interactions during foraging inspired a study of their behaviour and distribution. Both species peaked at >2,000-m-deep ocean waters, with lower densities over the shelf and with Leach’s storm petrels (ca. 0.5 km⁻²) twice as abundant as great-winged petrels (ca. 0.25 km⁻²). The results suggest half a million great-winged petrels and well over a million Leach’s storm petrels occurring over deep waters off southern Africa. Active fishing vessels elevated background densities of petrels in some areas, indicating the utilisation of discarded material, but in most areas hardly any fisheries were encountered and on the shelf with no discernable effect on petrel densities. Both species showed an association with meso-scale hydrographic features in the Agulhas current retroflection region. High densities of Leach’s storm petrels occurred in offshore areas with steep salinity and sea surface temperature gradients. No such tendency was found in great-winged petrels. Great-winged petrels spent relatively little time feeding during daylight (10.3% of birds observed) in comparison to Leach’s storm petrels (66.2%), but were frequently seen to join feeding Leach’s storm petrels where they profited from the searching skills of Leach’s. Both species performed displays as individuals, in pairs, in larger groups and in mixed-species groups. Tight gatherings of petrels swimming at sea (huddling) occurred, consisting either of one species or both. When disturbed, such flocks would disperse after take off and often engage in aerial displays. It is speculated that the formation of these flocks is part of the anti-predator strategy of petrels against attacks from under water.     

Flocking behaviour in the twilight ascents of Common Swifts Apus apus

Among the many unique flight behaviours of Common Swifts Apus apus, the most puzzling may be their ascents to high altitudes during both dusk and dawn. Twilight ascents have been hypothesized to be functionally related to information acquisition, including integration of celestial orientation cues, high‐altitude visual landmarks and sampling of weather conditions. However, their exact purpose remains unknown. We tracked Common Swifts with tracking radar at their breeding grounds in southern Sweden, and present evidence that during the dusk ascent and dawn descent they often occur in flocks, whereas during the dusk descent and dawn ascent phase they do not. This flocking behaviour suggests that swifts may benefit from conspecific interactions during twilight ascents and descents, possibly through more robust cue acquisition and information exchange in groups, or extending social behaviour also seen in screaming parties before dusk.     

Oviposition in Yponomeuta cagnagellus: the importance of contact cues for host plant acceptance

Small ermine moths (Yponomeutidae: Lepidoptera) are specialist herbivores. Species within the genus Yponomeuta are each specialized on a limited number of plant species, mainly within genera belonging to the Celastraceae. European Yponomeuta species have developed new specialized host affiliations, mainly on rosaceous hosts. Since these host shifts are reputed to be of consequence for speciation, the role of the ovipositing female is of particular interest. Study of the pre-oviposition behaviour of gravid Y. cagnagellus (Hb.) moths on host (Euonymus europaeus), non-host (Crateagus monogyna) and artificial oviposition substrates, provided information on the nature of the cues used for host plant acceptance and the insect’s perception of these cues. Host selection by adult females occurs with contact chemoreceptors probably located on the antennae or tarsi. MeOH-soluble, non-volatile phytochemical compounds washed from the host plant’s surface and applied on an artificial twig are sufficient to stimulate a complete sequence of behavioural elements leading to oviposition. Volatiles do not have a large effect on the pre-oviposition behaviour.     

European Roe Deer Increase Vigilance When Faced with Immediate Predation Risk by Eurasian Lynx

Prey animals must balance antipredatory behaviour with foraging behaviour. According to the risk allocation hypothesis, prey increase antipredatory behaviour and reduce foraging activity during pulses of high risk, but with continuous risk, other activities must continue and antipredatory behaviour decreases despite the risk. We studied the impact of lynx presence on the vigilance behaviour of wild roe deer under conditions of (i) a pulsed elevated risk by experimentally spreading lynx urine as an olfactory cue, and (ii) continuous risk by comparing an area where lynx was eradicated 160 years ago to an area where lynx has been re‐introduced 30 years ago. Roe deer were extremely vigilant in response to the predator olfactory cue; however, roe deer vigilance did not differ measurably among areas with or without potential lynx presence. Deer were more vigilant before sunset than during the night at both study areas, probably due to long‐term adaptation of roe deer to human hunting during daytime. Vigilance decreased from August to September even though activity of lynx increases in autumn, which may be a result either of increased foraging due to decrease in food quality in autumn, or of changes in social organization of the deer. Our results suggested that the degree of vigilance depends on environmental cues. We found that roe deer respond to lynx urine despite a long absence of lynx in the ecosystem. Our results support the risk allocation hypothesis for responses to pulses of high risk but not for responses to continuous elevated levels of risk.     

Familiarity Breeds Tolerance: the Development of Social Stability in Flocking Siskins (Carduelis spinus)

Behavioural integration associated with the fusion of two flocks is analyzed in captive siskins (Carduelis spinus) by quantifying changes in social behaviour with time since joining. In general there was an increase in the incidence of tolerant behaviour, supplanting attacks and hopping withdrawals with time since fusion of the flocks. However, the number of displays and flights showed the opposite, negative, trend. Taking dominance status into account, the greatest change in behaviour with time since joining is an increase in tolerance by dominants of new flock companions. Factorial analysis of correspondences was used to study how different birds changed their behaviour with time since joining a flock. This analysis showed that the introduction of new birds did not disrupt relationships with familiar birds, and that residents are dominant in interactions with the incoming new flock companions. The analysis also demonstrated that relationships within the new flock had stabilized 20 days after the flocks had joined. The characteristics of the socially integrated group of siskins are quite similar to those described by Rohwer & Ewald (1981) in their shepherds hypothesis: dominants tolerate their subordinates feeding in close proximity, offering them a profitable feeding area, but also supplant them to obtain food; both dominants and subordinates benefit from being in a flock. As a consequence, constant changes of membership in flocks is costly not only because birds lose dominance status, but also the advantages of clear dominant and subordinate roles.     

Experience‐ and age‐mediated oviposition behaviour in the yellow fever mosquito Stegomyia aegypti (=Aedes aegypti)

In repeated behaviours such as those of feeding and reproduction, past experiences can inform future behaviour. By altering their behaviour in response to environmental stimuli, insects in highly variable landscapes can tailor their behaviour to their particular environment. In particular, female mosquitoes may benefit from plasticity in their choice of egg‐laying site as these sites are often temporally variable and clustered. The opportunity to adapt egg‐laying behaviour to past experience also exists for mosquito populations as females typically lay eggs multiple times throughout their lives. Whether experience and age affect egg‐laying (or oviposition) behaviour in the mosquito Stegomyia aegypti (=Aedes aegypti) (Diptera: Culicidae) was assessed using a wind tunnel. Initially, gravid mosquitoes were provided with a cup containing either repellent or well water. After ovipositing in these cups, the mosquitoes were blood‐fed and introduced into a wind tunnel. In this wind tunnel, an oviposition cup containing repellent was placed in the immediate vicinity of the gravid mosquitoes. A cup containing well water was placed at the opposite end of the tunnel so that if the females flew across the chamber, they encountered the well water cup, in which they readily laid eggs. Mosquitoes previously exposed to repellent cups became significantly more likely to later lay eggs in repellent cups, suggesting that previous experience with suboptimal oviposition sites informs mosquitoes of the characteristics of nearby oviposition sites. These results provide further evidence that mosquitoes modify behaviour in response to environmental information and are demonstrated in a vector species in which behavioural plasticity may be ecologically and epidemiologically meaningful.     

Parental Care Syndromes in House Sparrows: Positive Covariance Between Provisioning and Defense Linked to Parent Identity

Parents of many species provide multiple forms of care to their offspring. In many birds, parents often provision offspring with food and defend them from predators and/or nest‐site competitors. We tested how these two forms of parental care covary in a wild population of house sparrows (Passer domesticus). Using a behavioral reaction norm approach, we found that nestling provisioning exhibited between individual differences and positively covaried with a measure of nest defense: the propensity to attack a heterospecific nest box competitor, the European starling (Sturnis vulgaris). This result would seem to support parental investment theory and suggests that high‐provisioning parents have high‐value offspring, which they will defend more vigorously than low‐provisioning parents. In addition, we found that parents with nestlings that hatched earlier in the season and grew faster approached a model starling more frequently and tended to be more likely to strike the starling. However, we also found that although brood value explained significant variation in both nestling provisioning and nest defense, it did not eliminate the positive, between‐individual relationship between provisioning and defense. This suggests that some of the correlation between provisioning and defense is tied to individual identity and hence may be a behavioral syndrome in which differences between individuals in underlying attributes produce correlated behaviors.     

Predation processes: behavioural interactions between red fox and roe deer during the fawning season

Predation by red fox (Vulpes vulpes) is the most important mortality cause for neonatal roe deer (Capreolus capreolus) in Scandinavia. With the objective of investigating how the fox finds fawns and how antipredatory behaviour of roe deer females influences choice of hunting method, I analysed observations of interactions between red fox and roe deer females. The observations were collected over 14 years in a mixed forest/agricultural landscape in Sweden. Of 49 fox–doe encounters, the doe attacked the fox in 59%. In 90% of these attacks the fox was successfully deterred. In two observations a doe saved a fawn attacked by a fox. Two hunting methods used by the fox were discerned. In 28 cases foxes searched the ground, and in 18 cases they surveyed open areas, often from a forest edge. The latter behaviour seemed more directed at fawns and was seen leading to a capture attempt. Searching seemed less efficient and also difficult to conduct due to the aggressiveness of does. A surveying sit-and-wait type of hunting method thus appeared as the most successful. The possibility to use this method could explain why roe deer fawns are more vulnerable to fox predation in open habitats.     

Does interference competition explain why White Terns of Aride Island,Seychelles, breed predominantly when marine productivity is lower?

White Terns Gygis alba breed throughout the year on Aride Island but show a marked preference to nest during the northwest monsoon (November–March), when interspecific competition and also marine productivity are considered to be lower. In this study we investigated and compared breeding and foraging parameters of White Terns between the northwest and southeast (May–September) monsoons to assess whether interspecific competition affected foraging activity and explained the timing of breeding of White Terns. Goatfish (Mullidae) dominated the diet of White Terns and no significant differences were found in diet composition between the northwest and southeast monsoons. Similar diets and patterns of food provisioning of White Terns between the two monsoons do not support the hypothesis of strong exploitation competition during the southeast monsoon. On the other hand, foraging behaviour and frequency of capture attempts of White Terns differed between the two monsoons. The percentages of multi‐species flocks with White Terns and of large flocks with more than 25 noddies Anous and terns Onychoprion were significantly higher during the southeast monsoon. Moreover, capture attempt frequencies of White Terns foraging in multi‐species flocks were lower than those of solitary individuals, and both solitary and flocking White Terns had significantly lower capture attempt frequencies during the southeast monsoon in comparison with the northwest monsoon. These results suggest that interference competition depresses foraging activity of flock‐foraging White Terns, particularly during the southeast monsoon, which could potentially explain why White Terns breed preferentially during the northwest monsoon. However, and despite avoiding interference competition, White Terns nesting during the northwest monsoon did not show higher breeding success than those nesting during the southeast monsoon. Other hypotheses that might explain the preference of White Terns for breeding during the northwest monsoon, such as avoidance of agonistic interactions with Lesser Noddies Anous tenuirostris at nest sites, should also be investigated.