Herpetology Notes, volume 13: 583-586 (2020) (published online on 30 July 2020)

The first documented case of arboreal foraging by two male adders (Vipera berus) raiding the nest of a blue tit (Cyanistes caeruleus)

Jelmer Groen1,*, Gerry Kaastra-Berga2, and Simon Kaastra2

Feeding habits are an important element of snake proportion of amphibians, lizards or small birds ecology, with foraging modes (ambush vs. active (Prestt, 1971; Šebela, 1980; Kjærgaard, 1981; Luiselli foraging) often being correlated with a range of and Anibaldi, 1991; Kowalewski and Profus, 2007). morphological, physiological and behavioural traits However, in some areas amphibians account for a large (Glaudas et al., 2019). The diets of several snake percentage of prey found as stomach content (Pielowski, species are well studied based on the examination of 1962; Pomianowska-Pilipiuk, 1974). These observed prey remains in their digestive tracts or faeces (e.g. differences in diet composition are likely correlated Goddard, 1984; Luiselli and Anibaldi, 1991; Sant’Anna with the availability of potential prey. Birds are rarely and Abe, 2007; Reading and Jofré, 2013), including documented to be predated, with unidentified nestlings the molecular analyses of excrements (e.g. Brown accounting for most of the avian prey (e.g. Prestt, 1971). et al., 2013). In addition, direct field observations Bird species that have been documented as being part of can lead to new insights regarding the behaviour of the adder’s diet include ground or shrub nesting species foraging and consumed prey species that have so far like water pipit, Anthus spinoletta (Luiselli and Anibaldi, been overlooked. We here report the observation of two 1991), garden warbler, Sylvia borin (Pielowski, 1962), adders (Vipera berus (Linnaeus, 1758)) that showed meadow pipit, Anthus pratensis (Nigel Hand, pers. foraging behaviour peculiar for at least three reasons: i) comm.), goldfinch, Carduelis carduelis (footage, BBC the snakes belonging to a species, which predominantly Springwatch) and bluethroat, Luscinia svecica (Judith is a terrestrial ambush forager, actively climbed a tree; Bouma, pers. comm.). ii) they entered a tree hollow to raid a bird’s nest; iii) The observation that we report herein was made on this behaviour was performed independently and almost May 19, 2019 by the second and third authors during a simultaneously by two different individuals. hike in the Merskenheide, an isolated, 28-hectare nature The adder is a medium-sized viper that grows to reserve in the eastern part of the Province of Friesland, a maximum length of 65–90 cm and has the widest The Netherlands (0–10 m). The nature reserve consists and northernmost distribution of all terrestrial snakes of dry sandy heath surrounded by mixed forests (Schiemenz, 1985; Speybroeck et al., 2016). In the and agricultural landscape. The habitat where the Netherlands, it is restricted to specific areas on sandy observation took place is comprised of a narrow stretch soils in the eastern part of the country (0–100 m), where of mixed forest, harbouring the following dominating it mostly inhabits heathlands and moorlands (Janssen trees and shrubs: common oak (Quercus robur), silver and van Hoof, 2009; van Delft and Janssen, 2015). birch (Betula pendula), rowan (Sorbus aucuparia), The diet of adult adders generally consists of alder buckthorn (Frangula alnus) and black cherry small mammals (rodents and shrews) and to a lower (Prunus serotina). Upon arriving at the specific locality at 15:19 h, one adult male adder was observed that immediately disappeared into the undergrowth. At 15:34 h, a second adult male (hereafter: adder no. 2) emerged from the undergrowth and started to climb an old rowan tree. This tree had a hollow branch, in which 1 Ecologisch Adviesbureau FaunaX, Badweg 40B, 8401 BL Gorredijk, The Netherlands. the nest of a blue tit (Cyanistes caeruleus (Linnaeus, 2 Lyts Blijema 21, 9001 LH Grou, The Netherlands. 1758)) was located. The observers noted the existence * Corresponding author. E-mail: [email protected] of the nest, because a blue tit with food in its beak 584 Jelmer Groen et al. landed in the tree, reluctant to feed its young. The nest a final attempt to get to the nest, but eventually went in the tree hollow was accessible through two connected down the tree and disappeared into the undergrowth entrances that were 1.13 m and 1.74 m above ground at 15:51 h. At this point, both adders were no longer level (Fig. 1). While adder no.2 was making its way up visible and the observers left the location. At 17:27 the tree (Fig. 2A), a third adult male adder (hereafter: h, the observers returned to the tree, and noticed that adder no. 3) of similar size as adder no. 2 appeared the blue tit was still present and remained reluctant to and also started to climb the tree. The two adders were enter the hollow. Twenty-seven minutes later an adult photographically distinguished by the colour markings male adder, with the characteristics of adder no. 3, left on their head and neck (see Sheldon and Bradley, the hollow by its lower entrance and carried a blue tit 1989). Both adders simultaneously but separately made nestling in its mouth, indicating that at least two adders several attempts to reach the nest before adder no. 2 raided the nest. Adder no. 3 left the entrance with its entered the hollow through the upper entrance at 15:40 tail first and was immediately attacked by the blue tit h (Fig. 2B). Initially, its tail was still sticking out of the (Fig. 2D). Following the attacks, the adder dropped on hollow. Based on the observed caudal movements, this the ground (Fig. 2E), where it continued swallowing its was probably the instance where it found the nest and prey (Fig. 2F). The process of swallowing took more bit and took one or more nestlings. At this time adder than 15 min, after which the observers decided to leave no. 3 was still attempting to reach the nest (Fig. 2C). the location at 18:13 h. The time span between spotting Five minutes later, adder no. 2 moved its tail into the the first adder and leaving the location for the last time hollow and disappeared out of sight. Adder no. 3 made was 2 h and 54 min.

Figure 1. Rowan tree with the blue tit nest in a hollow. The red arrow indicates the upper entrance to the nest at 1.74 m above ground level, the blue arrow indicates the lower entrance to the nest at 1.13 m above ground level. Photo by Jelmer Groen. The first documented case of arboreal foraging by two male Vipera berus 585

Figure 2. Two adders observed while raiding a blue tit nest in a tree hollow in the Merskenheide, Province of Friesland, The Netherlands: A – Adder no. 2 makes its way up the tree; B – Adder no. 2 enters the hollow through the upper entrance; C – Adder no. 3 attempts to reach the nest after adder no. 2 has already entered the hollow. The tail of adder no. 2 is still sticking out of the upper entrance; D – Adder no. 3 leaves the lower entrance tail first with a nestling in its mouth and is attacked by the blue tit; E – Following the attacks, adder no. 3 drops to the ground; F – Adder no. 3 continues to swallow its prey on ground level. Photos by Gerry Kaastra-Berga. 586 Jelmer Groen et al.

During a visit by the first author on May 30, 2019 to in common viper (Vipera berus) in Denmark. Natura Jutlandica measure the heights at which the entrances of the tree 19: 45–48. hollow were located, and to assess if these entrances Kowalewski, L., Profus, P. (2007): Rozmieszczenie, biometria i ekologia żmii zygzakowatej Vipera berus L. na Górnym Śląsku were connected, the nest proved to be abandoned and i Wyżynie Częstochowskiej. Chrońmy Przyrodę Ojczystą 63: there was no trace of dead nestlings in or around the tree. 58–90. To the best of our knowledge, this is the first documented Luiselli, L.M., Anibaldi, C. (1991): The diet of the adder (Vipera case of an adder raiding the nest of a bird that breeds in berus) in two alpine environments. Amphibia-Reptilia 12: a tree hollow far above the ground. Furthermore, this 214–217. observation is of interest, because it shows a clear case Pielowski, Z. (1962): Untersuchungen über die Ökologie der of active arboreal foraging by a species of snake that is Kreuzotter (Vipera berus L.). Zoologisches Jahrbuch, Abteilung Systematik 89: 479–500. generally considered a terrestrial sit-and-wait predator. Pomianowska-Pilipiuk, I. (1974): Energy balance and food The fact that multiple adders raided the nest suggests requirements of adult vipers Vipera berus (L.). Ekologia Polska that some aspects of this behaviour, e.g. the raiding of 22: 195–211. bird nests in general and active foraging, may be more Prestt, I. (1971): An ecological study of the viper Vipera berus in common than recorded so far, at least in specific types southern Britain. Journal of Zoology 164: 373–418. of habitats. Future studies may shed more light on this Reading, C., Jofré, G. (2013): Diet composition changes correlated subject. with body size in the smooth snake, Coronella austriaca, inhabiting lowland heath in southern England. Amphibia-

Reptilia 34: 463–470. Acknowledgements. The field survey by the first author was Sant’Anna, S.S., Abe, A.S. (2007): Diet of the rattlesnake Crotalus carried out under the permit FF/75A/2016/015 issued by Reptile, durissus in southeastern Brazil (Serpentes, Viperidae). Studies Amphibian and Fish Conservation the Netherlands (RAVON), and on Neotropical Fauna and Environment 42: 169–174. with a permission from the nature association Staatsbosbeheer. Schiemenz, H. (1985): Die Kreutzotter. Die Neue Brehm Bücherei. We would like to thank Dirk Bauwens (Department of Biology, Wittenberg Lutherstadt, Germany, A. Ziemsen. University of Antwerp) for his comments to previous versions of Šebela, M. (1980): The diet of the common viper (Vipera berus) in this article and for writing a pre-peer review. We wish to thank the area of Mt. Králický Sněžník. Folia Zoologica 29: 117–123. Sven Mecke (Naturkundemuseum Paderborn) for editing and Sheldon, S., Bradley, C. (1989). Identification of individual adders reviewing the MS. (Vipera berus) by their head markings. Herpetological Journal 1: 392–396. References Speybroeck, J., Beukema, W., Bok, B., Voort, J., van der (2016): BBC Springwatch (2014): Goldfinch cam live. Adder in the Field Guide to the Amphibians & Reptiles of Britain and Europe. goldfinch nest: Available at https://www.bbc.co.uk/programmes/ London, United Kingdom, Bloomsbury Publishing Plc. p020n70b. Accessed on 19 April 2020. Brown, D.S., Ebenezer, K.L., Symondson, W.O.C. (2013): Molecular analysis of the diets of snakes: changes in prey exploitation during development of the rare smooth snake Coronella austriaca. Molecular Ecology 23: 3734–3743. Delft, J.J.C.W., van, Janssen, P. (2015): The adder in the Netherlands: distribution, status, and trends. Litteratura Serpentium 35: 29–54. Glaudas, X., Glennon, K.L., Martins, M., Luiselli, L., Fearn, S., Trembath, D.F., Jelić, D., Alexander, G.J. (2019): Foraging mode, relative prey size, and diet breadth: a phylogenetically explicit analysis of snake feeding ecology. Journal of Animal Ecology 88: 757–767. Goddard, P. (1984): Morphology, growth, food habits and population characteristics of the smooth snake Coronella austriaca in southern Britain. Journal of Zoology 204: 241–257. Janssen, P., Hoof, P.H., van (2009): Adder, Vipera berus. In: Nederlandse Fauna 9. De Amfibieën en Reptielen van Nederland, p. 313–323. Creemers, R.C.M., Delft, J.J.C.W., van, Ed., Leiden, The Netherlands, Nationaal Natuurhistorisch Museum Naturalis, European Invertebrate Survey. Kjærgaard, J. (1981): A method for examination of stomach Accepted by Sven Mecke content in live snakes and some information on feeding habits