Hide or die when the winds bring wings: predator avoidance by activity shift in a mountain snake

doi:10.21203/rs.3.rs-2096701/v1

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Research Article

Hide or die when the winds bring wings: predator avoidance by activity shift in a mountain snake

https://doi.org/10.21203/rs.3.rs-2096701/v1

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published 16 May, 2023

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Background

Understanding predator-prey relationships is fundamental in many areas of ecology and conservation. Basking time often increases the risk of predation and one way to minimise this risk is to reduce activity time and to stay within a refuge. However, this implies costs of lost opportunities for foraging, reproduction, and thermoregulation. We aimed to determine the main potential and actual predators of Vipera graeca, to estimate the incidence and the age and sex distribution of predation events based on body injuries to infer predation pressure, and to assess whether and how the activity of V. graeca individuals is modified by predation pressure.

Results

We observed n = 12 raptor bird species foraging at the study sites, and we determined Circaetus gallicus, Falco tinnunculus and Corvus cornix as predators of V. graeca. We found injuries and wounds on 12.5% of studied individuals (n = 319). The presence-absence of injuries were significantly positively influenced by estimated age of vipers, and were more frequent on females than on males, while interaction of age and sex showed a significant negative effect. The overlap between the activity of raptors showed significantly smaller overlap with observed viper activity than with potential viper activity.

Conclusion

The time being active on the surface by the snakes has cost: the incidence of predation-related injuries increased with age, were more frequent in females than in males and they occurred earlier in age for females than for males. The vipers show a shift in the bimodal activity time-frame by being active earlier in the morning and later in the afternoon than could be expected based on thermal conditions suggesting that there is no maximalization to exploit the whole time frame available to reach the preferred body temperature in a cold environment.

prey capture

thermoregulation

basking

Serpentes

Understanding predator-prey relationships is fundamental in many areas of ecology and conservation. Knowledge of these interactions is essential for mapping trophic networks, understanding community organisation and structure, demography, behavioural strategies, evolutionary processes, for threatened species conservation and conservation planning (Yoshida et al., 2007; Tylianakis et al., 2010; Christensen et al., 2014). Predation has strong direct and indirect effects on prey populations (Lima & Dill, 1990; Kats & Dill, 1998; Kraus & Rodel, 2004; Apfelbach et al., 2005), and predation pressure as a selective force has triggered physiological, morphological and behavioural adaptations in prey species (Nilsson et al., 1995; Teplitsky et al., 2005) such as camouflage colouration and morphology, bad taste or poisons, signalling or mimicking dangerous model species and many other active behaviours facilitating predator avoidance, e.g. escaping or counter-attacking (Monclús et al., 2009). Predator-avoidance behaviours have an unambiguous short-term benefits in terms of survival but the long-term effects on fitness components vary. The activity pattern of prey is often influenced by predator activity, which can lead to a trade off with other actions in prey species (Higdon et al., 2019). Reduced activity is associated with increased survival in prey species, but it also decreases time spent on feeding, foraging success, growth rate and/or reproductive success. The reproductive status of individuals can also influence predation risk. For example, in viviparous snakes, mortality can be either lower or higher for pregnant females than for other individuals, which can lead to biased sex ratio within populations (Wang et al., 2003; Brito & Rebelo, 2003). Predation risk also shows temporal patterns over daily, lunar and seasonal cycles, depending on the environment and activity of both predator and prey (Lima & Bednekoff, 1999). Further, environmental changes, interruption of natural processes or arrival of a novel predator can lead to population decline of prey, and eventually to extinction in extreme cases (Wilmers et al., 2007).

The behavioural traits of ectotherms depend on body temperature (Huey, 1982), which in turn depends on the available environmental temperatures and behavioural choices related to thermoregulation. Ectotherms such as reptiles attempt to keep their body temperature in a narrow optimal range to optimise physiological processes (Berk & Heath, 1975; Barber & Crawford 1977; Huey, 1982; Van Berkum et al., 1986). The two main behavioural options to regulate body temperature and to keep body temperature within the thermal window bounded by thermal tolerance are the timing of activity (Angiletta, 2009) and the choice of microhabitats from the thermal landscape (Harvey & Weatherhead, 2010). In temperate climates, the preferred body temperature can only be reached by basking, with associated costs of time and energy required for thermoregulation and of risks of predation (Webb & Whiting, 2005; Herczeg et al., 2008). Because basking time increases the chance of being noticed by visually searching predators (Webb & Whiting, 2005), as an anti-predator strategy, activity time can be reduced by staying within a refuge to minimise the risk of predation, however this implies costs of lost opportunities for foraging, reproduction, and thermoregulation (Lima & Dill, 1990; Martín & López, 1999). Avian predators usually have higher success in hunting snakes than mammals have, possibly due to better detectability by visual searching than by olfactory searching and to the poorer escape ability of snakes from predators searching for them from a distance (Schalk & Cove, 2018).

Reptiles are among the most threatened vertebrates and are known to decline globally and in Europe (Gibbons et al., 2000; Cox et al., 2022). In Europe, the meadow and steppe vipers (Vipera ursinii complex) are among the most threatened reptiles: lowland populations of this complex have lost almost all of their habitats due to the transformation of grasslands to croplands, and have become extinct in a large proportion of their former distribution, while alpine populations are threatened by overgrazing and climate change (Mizsei et al., 2018). In addition, meadow viper populations with low densities are also threatened by high predation pressure (Móré et al., 2022). The conservation of these threatened snake species requires a full understanding of the factors limiting the growth of populations, and predation is very likely one of these factors.

The general aim of this study was to assess predator-prey relationships involving visually foraging bird species as predators and the Greek Meadow Viper Vipera graeca (Nilson & Andrén, 1988), a rare, globally endangered, cold-adapted, mountain-dwelling venomous snake as prey. We specifically aimed to determine the main potential and actual predators of V. graeca, to estimate the incidence and the age and sex distribution of predation events based on body injuries to infer predation pressure, and to assess whether and how the activity of V. graeca individuals is modified by predation pressure. To these ends, we surveyed predators in 14 of 17 known populations of V. graeca, examined V. graeca individuals for signs of predation-related injuries, and collected observational data on the daily activity of predators in the two largest V. graeca populations, used thermobiological measurements (V. graeca preferred body temperature, environmental temperature) to estimate the thermal niche and potential activity window of V. graeca and compared the potential and observed activity of V. graeca and both against predator activity to study predator avoidance.

We observed 12 raptor bird species in the viper habitats from which Falco tinnunculus, Circaetus gallicus and Buteo buteo were the most common. We collected evidence on predation on V. graeca by C. gallicus (pellets, n = 5), F. tinnunculus (pellets and direct observations of predation event, n = 4) and Corvus cornix (direct observation, n = 1) (Fig. 1.). Based on a review of the literature, reptiles make up more than 10% of the diet of five raptor species that were regularly observed in the study areas (Aquila chrysaetos, B. buteo, C. gallicus, F. tinnunculus, Hieraaetus pennatus).

We examined 319 V. graeca individuals in 14 populations (mean ± S.E. 22.8 ± 5.27) for injuries. The apparent sex ratio was 0.64:1 for all individuals and 0.51:1 for adults. Mean SVL was 279 ± 3.88 mm, and the estimated age ranged between 0 (observed in the year of birth) and 10, with a mean of 5.7 ± 0.14 year. We found injuries and wounds on 40 individuals (12.5%) The majority of these injuries were on the middle and the posterior halves of the body, including the tail (Fig. 2.).

The presence-absence of injuries/wounds on vipers’ body were significantly positively influenced by the estimated age (estimate = 2.793 ± 0.471 SE, Z = 5.934, P < 0.0001) of viper individuals and were more frequent on females than on males (estimate = 10.769 ± 1.918 SE, Z = 5.614, P < 0.0001). The interaction of age and sex showed a significant negative effect (estimate=-1.349 ± 0.257 SE, Z=-5.255, P < 0.0001), as expected, because injuries were less frequent in males. Hazard functions showed that females obtained injuries at an earlier age than males (Fig. 3.).

Observation times of 38 individuals in two populations (Tymfi and Lakmos mountains) showed that the diurnal activity of V. graeca is bimodal, with one peak in early morning and another peak in late afternoon (Fig. 4A). The comparison of the observed viper activity and the potential activity estimated based on environmental temperature and thermoregulation showed that the observed morning activity peak is earlier than could be expected based on the environmental temperature and preferred T_b, and the observed afternoon activity peak is later than expected (Fig. 4A). The observed and potential activity of vipers showed moderate overlap (Fig. 4A, Δ_Tymfi = 0.459, Δ_Lakmos = 0.401).

During data collection on raptor diurnal activity, we observed six bird species, F. tinnunculus (53.1% of 98 observations), C. gallicus (22.4%), B. buteo (18.4%), F. peregrinus (3.1%), A. chrysaetos (2.0%), and H. pennatus (1.0%). The activity pattern of raptors (data pooled across species) was unimodal, with a peak at mid-day (Fig. 4B). The overlap between the activity of raptors showed significantly smaller overlap (W_Tymfi=57662, P_Tymfi<0.0001; W_Lakmos=2, P_Lakmos<0.0001; Fig. 5.) with observed viper activity (Δ_Tymfi = 0.287, Δ_Lakmos = 0.321) than with potential viper activity (Δ_Tymfi = 0.443, Δ_Lakmos = 0.835).

Our study of predator-prey relationships involving V. graeca and its avian predators provided four key results. First, we detected a large number of avian predator species present in the viper habitats and found evidence (pellets, direct observations) of predation on vipers by several raptor species. Second, we found a relatively high proportion (12.5%) of injured V. graeca individuals, with more injuries on the posterior than on the anterior body parts. Third, the incidence of predation-related injuries increased with age, were more frequent on females than on males and they occurred earlier in age for females than for males. Finally, two results suggested that vipers may adjust their diurnal period of activity due to predation because (i) their daily activity was bimodal, probably to avoid the mid-day peak in raptor activity, and (ii) there was only moderate overlap with predicted potential activity because the observed activity of vipers shifted earlier in the morning and later in the afternoon than could be expected based only on thermal conditions. These differences in activity patterns were consistent in two large populations on separate mountain ranges.

We directly observed three avian predator species to consume vipers (C. cornix, C. gallicus, F. tinnunculus). Based on the literature review, this is the first documented case of predation by C. cornix on snakes, even though this species is a generalist predator often considered as a pest for conservation and studied as a nuisance bird mainly in urban environments (Kövér et al., 2015, 2019). In addition, five other reptile-specialist predators were also regularly observed in the viper habitats and we also obtained evidence on predation on vipers by finding V. graeca remains (scales) in faeces of two mammal species (Eurasian Badger Meles meles and Red Fox Vulpes vulpes).

With regard to the large number of predators, it is not surprising that a relatively large proportion of viper individuals had injuries, i.e. signs of past failed attempts at predation. It is surprising, however, that so many of viper individuals were able to survive predator attacks. Most of these injuries were on the posterior body parts, which likely indicates that the individuals were actively escaping from the predators. The shortage of injuries on anterior body parts indirectly suggests that predation attempts are probably more successful if predators can get a hold of the head or the neck of the viper.

We did not find injuries on juvenile vipers and the incidence of injuries increased with age, which can emerge from multiple alternative explanations. Simply, adult snakes had more time to get injured than juveniles or juveniles may more easy to catch thus they are less likely to survive attacks (Gregory & Isaac, 2005). The preferred body temperature of juveniles might be lower than adults as an antipredator adaptation (Herczeg et al., 2007). Also, juveniles may spend less time basking, again, as an antipredator tactic, trading heat for safety (Webb & Whiting, 2005). Females were also more likely to get injured and they did so at an earlier age than males. Two explanations for this difference can be that (i) gravid females spend more time sunbathing than males (Viitanen, 1967; Shine, 1980) and (ii) gravid females carrying offspring (V. graeca is viviparous) can be slower to escape, which may increase their exposure to predators. Again, an alternative explanation is if males, that are usually smaller than females, are more often the victims of successful predation attempts, when predators take the entire individual.

In order to avoid predators, animals use different strategies, and previous studies have shown that the choice of a thermoregulatory period can also be part of a predator avoidance strategy in reptiles (Pérez-Tris et al., 2004). Our results suggest that the daily activity peaks of vipers are shifted towards thermobiologically suboptimal periods to minimize overlap with the activity peak of predators, which can be a predator avoidance. In the summer, V. graeca usually bask for approximately 1–2 hrs after sunrise, which is the best time period to find individuals compared to other times of the day. Thermal updrafts arrive from the valleys 2–3 hrs after sunrise, which soaring birds of prey exploit to visit viper habitats on the mountain. The overlap between the sunbathing period and the appearance of thermal updrafts offers the best chances of preying on vipers for predators because V. graeca individuals tend to retreat to their burrows later due to increasing soil and air temperature and/or the appearance of predators. In the late afternoon, when the air cools back, vipers have a second, smaller peak of activity just before sunset, when a smaller number of individuals come out of their burrows for sunbathing and/or feeding than in the morning. While the activity peaks of both vipers and predators can be explained by large-scale patterns in daily temperature, it is important to emphasize that even though periods later in the morning and earlier in the afternoon would similarly be thermobiologically suitable for V. graeca for sunbathing, the activity peaks are shifted earlier in the morning and later in the afternoon that could be expected based on temperature changes alone. These patterns indicate that predator avoidance can play a role in the bimodal nature of diurnal activity and the shifting of the activity peaks and that V. graeca does not exploit the whole extent of the thermally available activity window, likely due to risks of predation.

Our study offers several novelties in understanding predator-prey relationships involving snakes as prey. This study presents a detailed survey of potential and actual predators of a viper species in open mountain grassland ecosystems based on a large dataset from 14 of 17 known populations of V. graeca, covering much of the geographic range of the species. Our most important findings, i.e., the bimodal activity pattern of vipers and the shift in observed activity from the thermobiologically most suitable period to suboptimal periods, are both likely to be influenced by the activity of predators, have not been demonstrated in snakes before.

However, we note that there are further possibilities for improvement that are necessary to consider for a correct interpretation of our results. Most importantly, our data on injuries may not be adequate to assess predation pressure or the full spectrum of predation patterns because we have no information on individuals that perished in successful predation attempts. For example, if most of the predation attempts on juveniles or smaller males were successful, it may lead to the observed overrepresentation of predation-related injuries on females, whereas in reality, females may be better at escaping from predators. Overall predation pressure is probably greatly underestimated by the injury-based method and many of the detected differences can be explained in either of two ways, as elaborated above, because we do not know anything about individuals suffering successful predation attempts. More detailed observation of predators and, if possible, predation events or evidence from predation events such as scales in pellets or faeces etc. are necessary to assess predation pressure and its population-level consequences. Experimental studies using clay models would further inform us about the relative importance of avian vs. mammalian predation, the spatial and temporal patterns of predation attempts and so on, which would provide a more accurate assessment of predator activity and predation pressure. Similarly, an experimental study based on the observations or measurements of viper behavior upon the presentation of a predator decoy would throw more light on whether the activity shift occurs due to behavioral responses triggered by perceived predation risk or to daily temperature changes.

The most important conservation implications of this study is that predation is probably an important cause of mortality in populations of the rare and endangered V. graeca. The conservation of this species may thus require the control of predators, at least those species that are not protected such as C. cornix or V. vulpes., e.g. by trapping and translocation of individuals of predator species. Alternatively, fencing of areas may at least keep mammalian predators away from areas of high density of V. graeca. Predator control may also become necessary as more predators appear in the high-mountain viper habitats with the upward altitudinal shifting of predator home ranges and feeding grounds expected with climate change.

Our results on the importance of predation as an important cause of mortality will be relevant in other rare and/or threatened snake species of open grassland ecosystems. For example, the Hungarian Meadow Viper Vipera ursinii rakosiensis has been subject of intensive conservation actions since 2004, and new data suggest that predation is also an important source of mortality in this species (Móré et al., 2022). Because many of our findings point to the central importance of predation in the population biology of V. graeca and other viper species, a better understanding of mortality patterns due to predation will be directly applicable in the conservation of rare and threatened snake species.

We detected a large number of avian predator species present in the habitats of the endangered Greek meadow viper (Vipera graeca) and found evidence (pellets, direct observations) of predation on vipers by three species out of these. The relatively high proportion (12.5%) of injured V. graeca individuals observed suggests high predation pressure. The frequency of injuries was higher on the mid and posterior body part compared to the head and anterior body parts likely caused by higher foraging success of predators when targeting the head. The time being active on the surface (thermoregulation and forage) by the snakes has cost: the incidence of predation-related injuries increased with age, were more frequent in females than in males and they occurred earlier in age for females than for males. The studied viper species deal with that trade-off by adjusting the diurnal period of activity to predator activity, as we measured a high overlap between viper potential activity and predator activity in contrast to the moderate overlap between observed activity and predator activity. The vipers show a shift in the bimodal activity time-frame by being active earlier in the morning and later in the afternoon than could be expected based on thermal conditions suggesting that there is no maximalization to exploit the whole time frame available to reach the preferred body temperature in a cold environment.

Study species

The prey species in this study is Vipera graeca, which is among the least known endangered snake species in Europe (Mizsei et al., 2016). The 17 known populations of V. graeca are found in subalpine meadows above the tree line, between 1,600–2,200 meters above sea level in isolated ranges of the Pindos Mountains in southern Albania and central Greece (Mizsei et al., 2021). V. graeca is the smallest viper of Europe, the body length of adult individuals averages 35–40 cm, with a maximum of 45 cm, and females are larger than than males. These grassland snakes are dietary specialists on locusts and bush-crickets (Mizsei et al., 2019). Due to climate change and unsustainable land use, approximately 90% of the current habitats are likely to become unsuitable by the 2080s, thus conservation actions need to be implemented urgently to avoid extinction (Mizsei et al., 2021).

Data collection

We collected data in 14 of the 17 known populations of V. graeca. In each population, we intensively searched for snakes during the vipers’ active season between April and September in 2010–2019. We carefully checked the captured individuals for wounds and injuries that potentially originated from attacks of predators, and recorded both the sex and the snout-vent length (SVL). After data collection, all individuals were released at the exact location of capture.

To assess the daily activity of vipers, we collected data on the thermoregulation and the thermal environment in two of the largest populations, on Tymfi and Lakmos mountains in Greece in July and August of 2017. We chose these summer months because the species is most active and easiest to capture in this period based on our previous experience. To capture snakes, we searched characteristic V. graeca habitats throughout the day as described in Mizsei et al. (2016). We then measured the selected body temperature (T_b) of captured snakes in a 100×30×30-cm terraria in which we established a thermal gradient ranging from 20°C to 40°C and measured T_b hourly by a Testo 826-T4 thermocouple inserted in the snakes’ cloaca. We collected environmental temperature data called operative temperature (T_o), the temperature that a non-thermoregulating animal could attain based on heat radiation, conduction, and convection. We measured T_o by using a physical model made of copper that mimicked the size, shape, and heat absorption of the study species. To measure T_o, we equipped the models with temperature data loggers (Thermochron iButton DS1921G-F5#) pre-set to record data in 5-minute intervals and placed the models in four different micro-environments: in burrows, under rocks, in shade of vegetation, and on soil exposed to sun. The models were placed in the micro-environments closest to the exact location of capture of V. graeca individuals.

During snake searches, we also surveyed avian predators in the snake habitats to assemble checklists of avian predators observed in each studied population. We also collected pellets from predator species in each studied population during the active season of V. graeca between April and September in 2010–2019. In addition, we reviewed the literature on the dietary preferences of the observed predator species. To obtain detailed data on the daily activity of predators, we recorded bird activity in both the Tymfi and Lakmos mountains during the peak activity of vipers for 10–10 days in July and August of 2017. To record predator activity, two observers watched for potential predator birds from a mountain peak in each studied location, which enabled us to simultaneously monitor approximately 100 ha area of viper habitat.

Data analysis

To assess the age and sex distribution of injuries, we estimated the age of individuals based on the SVL and capture day of the year. To this end, we classified the individuals to n = 10 size categories based on SVL, then calculated the most likely age (number of days since birth) by the following formula using the ‘lubridate’ package in R (Grolemund & Wickham, 2011):

age_days = (day of year_capture+365×age_years) – mean(day of year(date_births))

where day of year_capture is the day of year of capture date (number of days since January 1), age_year is the most likely age of individual in years based on size categories, and date_births is the date of viper birth observations. To estimate the age and sex distribution, we fitted negative binomial generalized linear mixed models (glmm) to analyse the effect of age and sex on the presence of injuries using the ‘lme4’ package of R (Bates et al., 2015). The binary dependent variable was the presence-absence of injuries, while the explanatory variables were the sex and age of the individuals (estimated number of days since birth). We controlled for potential spatial bias by including population identity as a random factor. We used hazard functions to compare the probability of getting injured for male and female vipers with smoothing spline functions of the ‘gss’ package of R (Gu, 2014).

We estimated activity patterns by probability density functions (PDF) by kernel density estimation or by fitting parametric trigonometric sum distributions of observation time, which was regarded as a circular random variable where the underlying density was expected to be bimodal. We created three set of PDFs for the Tymfi and Lakmos study sites separately: 1) the daily activity of raptors based on observation times, pooled across the species known to be preying on V. graeca; 2) the observed daily activity of V. graeca based on observation times; 3) the potential daily activity of V. graeca based on thermoregulation measurements. To predict the potential activity of V. graeca, we first fitted a function to the frequency of T_b values selected in the thermal gradient by viper individuals using the ‘rpearson’ function of the ‘PearsonDS’ package (Becker & Klößner 2022), based on the variance, skewness and kurtosis of data, which were estimated by the ‘descdist’ function of the ‘fitdistrplus’ package (Delignette-Muller & Dutang, 2015). We scaled the estimates of the fitted distribution to range between 0–1 and regarded this as activity probability. Second, we calculated the average T_o for each 5-min interval, and joined these data with the activity probability values. To obtain time data representing the potential activity of V. graeca, we randomly resampled the time of mean T_o by regarding activity probability as a probability weight by the ‘sample’ base function of R. We measured the overlap of two activity patterns by calculating the coefficient of overlapping (Δ) using the ‘overlapEst’ function of the ‘overlap’ package (Ridout & Linkie, 2009), which is the area under the curve that is formed by taking the minimum of the two density functions at each time point. Δ can range between 0 (no overlap) and 1 (complete overlap), and is interpreted as the proportion of activity that differs between the two activity patterns by less than 1-Δ in any time period. We calculated the 95 percent confidence intervals for Δ as percentile intervals from 1000 bootstrap samples. All data processing and analyses were implemented in the R 4.0.2 statistical environment (R Core Team, 2021).

Ethics approval and consent to participate

Permits for fieldwork and data collection on animal individuals were provided by the Ministry for Environment and Energy of Greece (n. 158977/1757) and the Ministry of Environment of Albania (n. 6584).

Consent for publication

Not applicable.

Availability of data and material

All data and R codes produced during the preparation of this manuscript are available and deposited at Zenodo repository (DOI link will be provided upon acceptance of the manuscript).

Competing interests

The Authors declare no conflict of interest.

Funding

Financial support was provided by Chicago Zoological Society’s Chicago Board of Trade (CZS CBOT) Endangered Species Fund and the Development and Innovation Office of Hungary (NKFIH-OTKA K106133, GINOP2.3.3-15-2016-00019). Supported by the ÚNKP-22-4-II-DE-201 New National Excellence Program of the Ministry for Innovation and Technology from the source of the National Research, Development and Innovation Fund.

Authors' contributions

All authors collected data. DR and EM analyzed and interpreted the data. EM was a major contributor in writing the manuscript. All authors read and approved the final manuscript.

Acknowledgements

We thank Zoltán Boros, Barnabás Bancsik, Gergő Rák, Mátyás Budai, Gergely Babocsay, László Kövér and volunteers of the Greek Meadow Viper Working Group for their assistance in the field.

Angiletta MJ. Thermal adaptation, A theoretical and empirical synthesis. OUP. 2009.
Apfelbach R, Blanchard CD, Blanchard RJ, Hayes RA, McGregor IS. The effects of predator odors in mammalian prey species: A review of field and laboratory studies. Neurosci Biobehav Rev. 2005;29:1123–44.
Barber BJ, Crawford EC. A stochastic dual-limit hypothesis for behavioral thermoregulation in lizards. Physiol Zool. 1977;50:53–60.
Bates D, Mächler M, Bolker B, Walker S. Fitting Linear Mixed-Effects Models Using lme4. J Stat Softw. 2015;67:1–48.
Becker M, Klößner S. PearsonDS. Pearson Distribution System. R package version 1.2.2. https://CRAN.R-project.org/package=PearsonDS. Accessed 29 March 2022.
Berk ML, Heath JE. An analysis of behavioral thermoregulation in the lizard, Dipsosaurus dorsalis. J Therm Biol. 1975;1:15–22.
Brito JC, Rebelo R. Differential growth and mortality affect sexual size dimorphism in Vipera latastei. Copeia. 2003;2003:865–71.
Christensen V, Coll M, Piroddi C, Steenbeek J, Buszowski J, Pauly D. A century of fish biomass decline in the ocean. Mar Ecol Prog Ser. 2014;512:155–66.
Cox N, Young BE, Bowles P, et al. A global reptile assessment highlights shared conservation needs of tetrapods. Nature. 2022;605:285–90.
Delignette-Muller ML, Dutang C. fitdistrplus: An R package for fitting distributions. J Stat Softw. 2015;64:1–34.
Gibbons JW, Scott DE, Ryan TJ, Buhlmann KA, Tuberville TD, Metts BS, Greene JD, Mills T, Leiden Y, Poppy S, Winne CT. The Global Decline of Reptiles, Déjà Vu Amphibians: Reptile species are declining on a global scale. Six significant threats to reptile populations are habitat loss and degradation, introduced invasive species, environmental pollution, disease, unsustainable use, and global climate change. Bioscience. 2000;50:653–66.
Gregory PT, Isaac LA. Close encounters from the worst kind: patterns of injury in a population of grass snakes (Natrix natrix). Herpetol J. 2005;15:213–9.
Grolemund G, Wickham H. Dates and times made easy with lubridate. J Stat Softw. 2011;40:1–25.
Gu C. Smoothing spline ANOVA models: R package gss. J Stat Softw. 2014;58:1–25.
Harvey D, Weatherhead PJ. Habitat selection as the mechanism for thermoregulation in a northern population of massasauga rattlesnakes (Sistrurus catenatus). Ecoscience. 2010;17:411–9.
Herczeg G, Gonda A, Perälä J, Saarikivi J, Toumola A, Merilä J. Ontogenetic differences in the preferred body temperature of the European adder Vipera berus. Herpetol J. 2007;17:58–61.
Herczeg G, Herrero A, Saarikivi J, Gonda A, Jäntti M, Merilä J. Experimental support for the cost–benefit model of lizard thermoregulation: the effects of predation risk and food supply. Oecologia. 2008;155:1–10.
Higdon SD, Diggins CA, Cherry MJ, Ford WM. Activity patterns and temporal predator avoidance of white-tailed deer (Odocoileus virginianus) during the fawning season. J Ethol. 2019;37:283–90.
Huey RB. Temperature, physiology, and the ecology of reptiles. In: Gasc C, Pough F, editors. Biology of the Reptilia. London: AP; 1982. pp. 25–91.
Kats LB, Dill LM. The scent of death: Chemosensory assessment of predation risk by prey animals. Écoscience. 1998;5:361–94.
Kövér L, Gyüre P, Balogh P, Huettmann F, Lengyel S, Juhász L. Recent colonization and nest site selection of the Hooded Crow (Corvus corone cornix) in an urban environment. Landsc Urban Plan. 2015;133:78–86.
Kövér L, Lengyel S, Takenaka M, Kirchmeir A, Uhl F, Miller R, Schwab C. Why do zoos attract crows? A comparative study from Europe and Asia. Ecol Evol. 2019;9:14465–75.
Kraus C, Rödel HG. Where have all the cavies gone? Causes and consequences of predation by the minor grison on a wild cavy population. Oikos. 2004;105:489–500.
Lima SL, Bednekoff PA. Back to the basics of antipredatory vigilance: can nonvigilant animals detect attack? Anim Behav. 1999;58:537–43.
Lima SL, Dill LM. Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool. 1990;68:619–40.
Martín J, López P. When to come out from a refuge: risk-sensitive and state-dependent decisions in an alpine lizard. Behav Ecol. 1999;10:487–92.
Mizsei E, Boros Z, Lovas-Kiss Á, Szepesváry C, Szabolcs M, Rák G, Ujszegi J, Gál Z, Lengyel S, Puskás G. A trait‐based framework for understanding predator-prey relationships: Trait matching between a specialist snake and its insect prey. Funct Ecol. 2019;33:2354–68.
Mizsei E, Szabolcs M, Dimaki M, Roussos SA, Ioannidis Y. Vipera graeca, The IUCN Red List of Threatened Species. 2018:e.T53789650A53790137..
Mizsei E, Szabolcs M, Szabó L, Boros Z, Mersini K, Roussos SA, Lengyel S. Determining priority areas for an Endangered cold-adapted snake on warming mountaintops. Oryx. 2021;55:334–43.
Mizsei E, Üveges B, Vági B, Szabolcs M, Lengyel S, Pfliegler WP, Nagy TZ, Tóth JP. Species distribution modelling leads to the discovery of new populations of one of the least known European snakes, Vipera ursinii graeca, in Albania. Amphib-Reptil. 2016;37:55–68.
Monclús R, Palomares F, Tablado Z, Martínez-Fontúrbel A, Palme R. Testing the threat-sensitive predator avoidance hypothesis: physiological responses and predator pressure in wild rabbits. Oecologia. 2009;158:615–23.
Móré A, Mizsei E, Vadász C, Tóthmérész B, Heltai M. Analysis of mammal mesopredator scat samples indicates significant predation on the endangered Hungarian meadow viper (Vipera ursinii rakosiensis). Wildlife Biol. 2022:e01033.
Nilson G, Andrén C. A new subspecies of the subalpine meadow viper, Vipera ursinii (Bonaparte) (Reptilia, Viperidae), from Greece. Zool Scr. 1988;17:311–4.
Nilsson PA, Brönmark C, Pettersson LB. Benefits of a predtor-induced morphology in crucian carp. Oecologia. 1995;104:291–6.
Pérez-Tris J, Díaz JA, Tellería JL. Loss of body mass under predation risk: cost of antipredatory behaviour or adaptive fit-for-escape? Anim Behav. 2004;67:511–21.
Ridout MS, Linkie M. Estimating overlap of daily activity patterns from camera trap data. J Agric Biol Environ Stat. 2009;14:322–37.
Schalk CM, Cove MV. Squamates as prey: Predator diversity patterns and predator-prey size relationships. Food Webs. 2018;17:e00103.
Shine R. “Costs” of reproduction in reptiles. Oecologia. 1980;46:92–100.
R Core Team. R: a language and environment for statistical computing. Ed 4.0. 2. Vienna, Austria. 2021.
Teplitsky C, Plénet S, Joly P. Costs and limits of dosage response to predation risk: to what extent can tadpoles invest in anti-predator morphology? Oecologia. 2005;145:364–70.
Tylianakis JM, Laliberté E, Nielsen A, Bascompte J. Conservation of species interaction networks. Biol Conserv. 2010;143:2270–9.
Van Berkum FH. Evolutionary patterns of the thermal sensitivity of sprint speed in Anolis lizards. Evolution. 1986;40:594–604.
Viitanen P. Hibernation and seasonal movements of the viper, Vipera berus berus in southern Finland. Ann Zool Fenn. 1967;4:472–546.
Wang S, Lin HC, Tu MC. Skewed sex ratio of the Chinese green tree viper, Trimeresurus stejnegeri stejnegeri, at Tsao Chiao, Taiwan. Zool Stud. 2003;42:379–85.
Webb JK, Whiting MJ. Why don’t small snakes bask? Juvenile broad-headed snakes trade thermal benefits for safety. Oikos. 2005;110:515–22.
Wilmers CC. Understanding ecosystem robustness. Trends Ecol Evol. 2007;22:504–6.
Yoshida T, Ellner SP, Jones LE, Bohannan BJM, Lenski RE, Hairston NG. Cryptic Population Dynamics: Rapid Evolution Masks Trophic Interactions. PLOS Biol. 2007;5:e235.

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Hide or die when the winds bring wings: predator avoidance by activity shift in a mountain snake

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