Raquel Monclús

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Abstract: Early life parameters such as litter size and growth are frequently associated with an animal’s behavioral performance or motor skills as well as with its stress responsiveness. All these traits can be involved in the ontogeny of behavioral phenotypes, and therefore we wanted to know whether features such as early growth also show long-term correlations with the animals’ behavioral responses to challenges around maturity. We collected data on the early postnatal development of individually marked European rabbits living in a field enclosure and conducted two standardized behavioral tests shortly before the animals matured. In small enclosures, we experimentally tested their behavioral responses (1) in this novel environment and (2) to the confrontation with predator odor. Animals, which were more exploratory during the novel environment test showed lower behavioral signs of anxiety during the predator test. Both responses were correlated with individual pup body mass, with subjects with higher body mass being more exploratory in the first test and showing lower levels of anxiety in the second. The animals’ current body mass or age when being tested, were not correlated with any of their responses. First, the correlated responses of the animals during the different contexts of the applied tests strongly suggest the existence of behavioral types in European rabbits. Second, and most importantly, our study provides evidence that an animal’s early development can exert long-term effects on its personality type, although it is not clear whether body mass per se or some correlated physiological features drive the observed relationships.

Abstract: Human disturbance may differentially affect the behavior of wild animals and such behavioral perturbations may have fitness consequences. To understand the effects of specific types of human disturbance on antipredator behavior, a behavior whose performance enhances survival, we studied yellow-bellied marmots (Marmota flaviventris). We quantified both antipredator vigilance and the flight initiation distance of the marmots to an approaching human in six different colony sites where we also quantified the frequency and type of human visitation. We developed an analysis framework, using linear mixed models, and found that: (1) when the presence of motorized vehicles and bicycles was high, marmots increased the proportion of time spent vigilant (pseudo R2=0.33 and 0.31 for motorized vehicles and bicycles, P<0.05) and decreased the time spent foraging (pseudo R2=0.29 and 0.23 for motorized vehicles and bicycles, P<0.05), (2) there was no significant effect of the presence of pedestrians on the time allocated to vigilance and foraging (pseudo R2=0.25 and 0.19, P>0.05), (3) marmots decreased the flight initiation distance as disturbance of motorized vehicles (pseudo R2=0.85) and pedestrians (pseudo R2=0.84) increased (P<0.05), and (4) when we considered bicycles as the disturbance, juveniles tolerated closer approaches than adults or yearlings (P<0.001). Marmots thus responded to some human disturbance by adjusting time spent in foraging and shortening the tolerance distance. Since these behavioral responses could have significant implications for survival and reproduction, we should generally view human disturbance as something that can influence natural antipredator behavior. Importantly, based on an understanding of the differential effects of human activities on wildlife, reducing human disturbance should be taken into account for wildlife management. In addition, our approach will be useful to quantify differential effects of humans on wildlife and to enhance our ability to manage those impacts. © 2010 Elsevier B.V.

Abstract: Predation is a strong selective force with both direct and indirect effects on an animal's fitness. In order to increase the chances of survival, animals have developed different antipredator strategies. However, these strategies have associated costs, so animals should assess their actual risk of predation and shape their antipredator effort accordingly. Under a stressful situation, such as the presence of predators, animals display a physiological stress response that might be proportional to the risk perceived. We tested this hypothesis in wild European rabbits (Oryctolagus cuniculus), subjected to different predator pressures, in Doñana National Park (Spain). We measured the concentrations of fecal corticosterone metabolites (FCM) in 20 rabbit populations. By means of track censuses we obtained indexes of mammalian predator presence for each rabbit population. Other factors that could modify the physiological stress response, such as breeding status, food availability and rabbit density, were also considered. Model selection based on information theory showed that predator pressure was the main factor triggering the glucocorticoid release and that the physiological stress response was positively correlated with the indexes of the presence of mammalian carnivore predators. Other factors, such as food availability and density of rabbits, were considerably less important. We conclude that rabbits are able to assess their actual risk of predation and show a threat-sensitive physiological response. © 2008 Springer-Verlag.

Abstract: Chemical signals are widely used in inter and intraspecific communication in many animals. The importance of scent marks in communication has led to a variety of strategies in animals to increase the detectability and persistence of their scent marks. We studied the scent marking of foxes in relation to the role of plants as scent posts in a suburban Mediterranean forest in Madrid. Twice a month, from October 2005 to April 2006, we prospected 16 fixed 50 × 50 m plots, randomly distributed along the study area. We registered all fox faeces and their association to different plants, as well as the potential availability of the different plant species in our study area. Our results indicate that faeces were associated with plants mainly in the clearings, foxes preferred wooden species to grasses as scent posts and holm oak shrubs and rockroses to other wooden species. These data suggest that red foxes select certain plants as substrates for their faeces and pose the possibility that they are guided by searching images when looking for scent posts.

Abstract: An animal's level of vigilance depends on various environmental factors such as predator presence or the proximity of conspecific competitors. In addition, several individual traits may influence vigilance. We investigated the effects of body condition, social rank and the state of pregnancy on individual vigilance (scanning) rates in individually marked European rabbits (Oryctolagus cuniculus) of a field enclosure population. We found lower rates in young rabbits than in adult females, but male and female juveniles did not differ. Vigilance of juveniles was positively correlated with their age-dependent body mass (used as a measure of body condition), i.e. young rabbits with lower body condition scanned less. We suggest that juveniles with low body condition were trading off vigilance against feeding to maximise their growth. In contrast, there was no significant correlation between body mass and vigilance in adult females. Adult females increased scanning rates during late pregnancy, which might constitute a behavioural compensation because of their lower capacity to escape predator attacks. In addition, adult females with low social ranks scanned more than high ranking individuals, likely because of their higher risk of attacks by conspecifics. In summary, our results highlight various individual characteristics that influence vigilance behaviour in European rabbits. © 2009 Blackwell Verlag GmbH.

Abstract: Lactating rabbit females (Oryctolagus cuniculus) emit abdominal, ventral odour cues that are involved in guiding the pups to the nipples. We tested the impact of the females' social rank and age on the emission of this odour signal; both factors are highly collinear in wild rabbits and we did not aim to disentangle them in our study. We predicted that the abdominal odours of young, low-ranking females, which are usually more stressed and have a comparatively lower body condition, should be less attractive to pups than those of older, high-ranking females. For the experiment, we caught females from a population of wild-type European rabbits living in a large field enclosure. Pairs of adult females were placed in boxes with wire-mesh floor fixed over an arena with three rabbit pups aged 4-7 days old. First, we evaluated the effectiveness of our two-choice design by testing lactating females (LF) against non-lactating (NLF) controls (n = 17 pairs). In accordance with recent studies, the pups showed a clear preference for lactating females by means of a higher exploration time and more local searching under the ventral region of these females. In a second experiment, the pups chose between lactating 1-year-old, low-ranking females (Y/LRF) and older, high-ranking females (O/HRF) (n = 10 pairs). These latter assays suggested a comparatively lower attractiveness of Y/LRF females to pups searching for milk. Although the pups showed no significant preference in exploration behaviour, they preferably directed local searching events to the abdominal region of O/HRF females. In conclusion, our study suggests that mother-offspring chemosensory communication is modified by the mother's age and social rank, i.e., by a complex of factors that are strongly linked in rabbit females in the wild. © Japan Ethological Society and Springer 2008.

Abstract: One of the functions of chemical communication is territorial signalling. To achieve this, animals should mark their territories in a manner that increases the detectability of the marks, thereby maximising the probability that other animals detect the scent marks. In this study, we focused on the scent-marking behaviour of red foxes in relation to the abundance of their main prey, the European rabbit, in a suburban forest in Madrid, Spain. Our results reveal that foxes scent-marked more and increased the detectability of their marks in areas of higher rabbit density. It would appear that foxes defend food resources from competitors by increasing the number and the detectability of their scent marks. © 2008 Japan Ethological Society and Springer.

Abstract: Blind and deaf at birth, rabbit newborns need, as all mammal newborns, to rapidly interact with the mother to find the nipples and suck. This usually occurs only once per day, during an interaction drastically limited in time, both in domestic and natural conditions. After days 10-15, the mother-young interactions change progressively, leading to weaning between 4 and 6 weeks. In this context of rapid development of the young, lactating rabbit females and pups have developed some sensory, physiological and behavioural adaptations allowing them to communicate, and allowing the young to ingest milk then solid food efficiently. Here, we present some of these adaptations, taking examples from experimental studies run by several groups during the last decades. This paper is a summary of a chapter and communication recently presented during the last World Rabbit Congress (Coureaud et al 2008b).

Abstract: In group-living mammals, the major functions of vigilance are to detect the presence of predators and to monitor the movements of conspecific competitors, i.e. of potential opponents in agonistic encounters. The minimum distance to such a conspecific competitor that an animal considers safe is usually lower than to a predator, whereas the frequency of encounters with conspecifics is higher. Therefore, the acquisition of information about a predator or about a conspecific could lead to the existence of at least two different modes of vigilance behaviour. The aim of the present study was to describe and compare different forms of vigilance behaviour that European rabbits, Oryctolagus cuniculus, display in anti-predator and social contexts. We conducted an observational study on individually marked animals from a field enclosure population. We recorded social interactions of the animals, the presence of aerial predators (common buzzard Buteo buteo), and the vigilance behaviour of the rabbits. We distinguished between two forms of vigilance of different intensity: subtle and overt. The frequencies of both forms of vigilance displayed by the rabbits differed significantly in occurrence, duration, and distribution over time. Females and males showed higher frequencies of overt but not subtle vigilance when buzzards were present. In contrast, the presence of conspecifics in close proximity affected the display of subtle but not overt vigilance: males increased the frequency of subtle vigilance when other males were close. Females increased subtle vigilance in proximity of males and females; however, this effect was only apparent in females with a more unstable social situation. In conclusion, European rabbits differentially increased two different forms of vigilance behaviour in social and anti-predator contexts. © 2008 The Authors.

Abstract: The recognition of predator odours is a well-known mechanism in many prey species which may lead to various behavioural and physiological responses. This has been shown for many mammal species under laboratory conditions, but efforts to validate the results in the field often have led to inconclusive results. We investigated the behavioural reactions and the physiological stress response of European rabbits (Oryctolagus cuniculus) to the odour of a mammalian predator (red fox, Vulpes vulpes) under semi-natural conditions. The study was conducted on a rabbit population living in an outdoor enclosure of 2 ha. We compared the rates of vigilance and exploration, the time allocated to self-directed behaviours, the home range sizes and the physiological responses of an experimental and a control group. Only animals from the experimental group were confronted with fox faeces. These animals increased their vigilance rate whereas the control animals did not respond. The increase did not differ between adult and subadult individuals. Furthermore, the experimental animals frequently approached the odour of the predator which might indicate an increase in investigative behaviour. Home-range size, feeding and other self-directed behaviours did not change in response to fox odour. Moreover, the animals of the experimental and the control group did not differ in serum corticosterone concentrations (measured after adrenocorticotrophic hormone challenge) that we determined in the beginning and in the end of the experiment. We suggest that the observed behavioural responses represent a low-cost strategy for lowering the individual risk of predation. © 2006 The Authors.

Abstract: The existence and consistency of individual behavioral types in response to challenging situations is of increasing interest in behavioral biology. In our study on European rabbits (Oryctolagus cuniculus), we (1) investigated correlations between social behavior during early development and responses to experimental stressors during later life, and (2) tested for consistencies in these responses across different situations. For this, we observed juveniles living in field enclosures in early summer and recorded agonistic and positive social interactions. In autumn, the animals were (a) introduced singly into a novel environment and were (b) confronted with predator (red fox Vulpes vulpes) odor. We recorded behavioral and physiological stress responses. In addition, we evaluated the predator odor test with an independent sample of animals. These latter results showed a correlation between the animals' behavioral and physiological response: Individuals, which reacted to the presence of fox odor by low scanning rates showed a high increase in serum corticosterone challenge concentrations, whilst the levels in high scanners remained stable. Overall, we found correlations among social behavior displayed during early development and behavioral responses in the two experimental tests, however the correlations between the different traits of social behavior and the responses during the two different experimental tests were not consistent. Animals which were involved in more agonistic interactions during their early development started to explore faster when entered into the novel environment. During the second test we found that rabbits which previously showed a higher frequency of positive social behavior responded to the presence of predator odor by more scanning. Moreover, the behavioral responses during both experimental tests were not correlated: fast explorers in the novel environment test did not show a more active response during the predator odor test. Due to this lack of consistent behavioral styles across both tests we conclude that the study fails to support the existence of domain-general behavioral phenotypes in European rabbits. © 2006 Elsevier Inc. All rights reserved.

Abstract: Stress has been widely studied in different mammals, but the physiological stress reaction that the odour of a predator could induce in preys has not received much attention. Besides, not all the animals would respond to the same extent to a known stressor. We developed an experimental procedure with eleven naïve European rabbits (Oryctolagus cuniculus) in order to determine the individual physiological response to the olfactory detection of a potential predator. The rabbits were housed singly in small enclosures with a concrete burrow system and food and water were available ad libitum. The animals followed a control trial, without odour, and an experimental trial where we confronted the rabbits with fox (Vulpes vulpes) odour. Furthermore, another sample of eleven rabbits followed a control procedure subjected to the same housing and handling procedures but without facing the predator odour. In order to assess the physiological response we analysed the concentration of glucocorticoid metabolites in the faeces of the rabbits. Therefore, everyday faecal samples were collected and analysed with an enzyme immunoassay in order to measure the corticosterone metabolites (CM), particularly, those metabolites with a 5α-3β, 11β-diol structure. After validating the assay for wild rabbits, we found that the simulated presence of a predator (fox odour) in the enclosure resulted in an increase in faecal CM concentrations. However, the stressor did not affect all the animals in the same way. We found a general increase in the individual differences. In particular, males experienced a higher increase than females, though the overall response was similar for both sexes. To our knowledge this is one of the first attempts to analyse the assessment of the risk of predation by means of non-invasive methods. © Birkhäuser Verlag, 2006.

Abstract: Animals show a variety of antipredator strategies in response to the presence of chemical cues from mammalian predators. Nevertheless, there is no general agreement as to whether recognition of predator odours is dependent upon experience. We conducted an experiment on European rabbits Oryctolagus cuniculus naïve to any contact with predators and we investigated (1) whether they possessed a mechanism for the recognition of the odour of a predator, and (2) how they responded behaviourally and physiologically to that odour. We used fox Vulpes vulpes faeces as the source of the predator odour and sheep Ovis aries faeces as a nonpredator control odour. The experiments were conducted in small outdoor enclosures where the animals were kept singly. We recorded patterns of vigilance, activity and feeding, and changes in glucocorticoids and body mass. The rabbits showed a clear antipredator response to the presence of fox faeces, whereas they behaved neutrally in response to sheep odour. The response consisted of increased avoidance and vigilance while feeding and more investigation before feeding. Furthermore, the rabbits showed a physiological alarm response, that is, an increased responsiveness of their adrenocortical system and weight loss. However, the total activity budget, measured as time spent outside the burrow, the time spent feeding, and the amount of food ingested remained largely stable during the experiment. We conclude that rabbits recognised predator odours and that this recognition was independent of experience. © 2005 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.