Short Communication |
Corresponding author: Yurii V. Kornilev ( yukornilev@gmail.com ) Academic editor: Peter Mikulíček
© 2020 Angel Dyugmedzhiev, Kostadin Andonov, Georgi Popgeorgiev, Borislav Naumov, Yurii V. Kornilev.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Dyugmedzhiev A, Andonov K, Popgeorgiev G, Naumov B, Kornilev YV (2020) Crepuscular and nocturnal activity of the Nose-horned viper, Vipera ammodytes (Linnaeus, 1758) is more common than previously reported. Herpetozoa 33: 165-169. https://doi.org/10.3897/herpetozoa.33.e56520
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Different snake species may be active at various times of the day. In Europe, most snake species are predominantly diurnal, but about a third are partially or principally crepuscular and/or nocturnal. Here, we report the first instance of multiple in situ observations of the crepuscular and nocturnal activity of V. ammodytes in Bulgaria. Overall, usually as a result of general herpetological surveys and chance observations between 2001–2020, we recorded crepuscular/nocturnal activity of twenty-seven individuals from both sexes and all age classes (juvenile to adult), observed from April to September, following warm (maximum daily Tair = 20–28 °C) and hot (Tair > 28 °C) days. These records represent less than 1.5% of all our personal viper observations. However, given that our observations occurred throughout the country, within five different climatic zones, we hypothesise that nocturnal activity of V. ammodytes is more common than previously reported.
behavior, ecology, snake, temperature, Viperidae
Nocturnal activity in ectotherms might lead to suboptimal performance due to depressed body temperature (Tbody) compared to preferred temperature (Tpreferred), potentially incurring costs such as slower digestion. However, changes in activity timing might lower predation risk and increase prey availability (
Throughout its range (NE Italy and S Austria, most of the the Balkan Peninsula, Anatolia, and the Transcaucasia), the Nose-horned viper, V. ammodytes (Linnaeus, 1758) may exhibit diverse diurnal activity patterns based on the particular location’s characteristics and seasonality (
In Bulgaria, the species’ activity has been described succinctly as ‘almost exclusively diurnal’ (Beshkov and Nanev 2002) and ‘diurnal, with some crepuscular/nocturnal activity following warm summer days’ (
We compiled the author’s personal records of V. ammodytes, collected during viper-specific and general herpetological surveys carried throughout Bulgaria in 2001–2020 and during the species active season (mostly April to September). Most searches were non-systematic, varied in time and intensity, and occurred throughout the country. However, between 2014 and 2019, some of the search effort was systematic, with viper-specific surveys conducted monthly during the active season of the species in five different localities, as part of an ongoing ecological study on the species (for more details see
We considered an individual as active if it was found on the surface and not utilizing cover. When possible, immediately after hand-capturing an active viper, we used a quick-reading digital thermometer (precision: 0.1 °С) to measure the snake’s body temperature at the cloaca (Tbody), temperature of the substrate (Tsubstrate) and air temperature (Tair) at 15 cm above the ground. We estimated temperature of the microhabitat (Tmicrohabitat) as the average of Tsubstrate and Tair (
For each observation, we recorded the geographical coordinates (GCS WGS 84), the date and time, and subsequently identified the astronomical sunset time and the day length for the specific date and locality. We defined activity as crepuscular if an individual was found from 15 min before sunset to 30 min after sunset (usually finding snakes was still possible without an artificial light source) and as nocturnal if found more than 30 min after sunset and before next sunrise. In most cases at the same localities where we found crepuscular/nocturnal snakes, we also searched during the day and measured daily Tair throughout. Thus, we considered days as warm when Tair was 20–28 °C and hot when the maximum recorded daily Tair > 28 °C; we have identified that above 28 °C, the detectability of V. ammodytes decreases, as most animals retreat to shelters or in shade (
Using QGIS (v. 3.14), for each observation we extracted elevation data based on a 40-m Digital Elevation Model and the Köppen-Geiger climate classification based on a high-resolution (1km pixel size) map for 1980–2016 (
Overall, we recorded 11 crepuscular and 16 nocturnally active individuals (Table
Observations of crepuscular/nocturnally active Vipera ammodytes. Time – local time (UTC +3); Ss – minutes after sunset; M% – percent of moon illuminated, numbers in parentheses denote cases when the moon rise was after Time, question mark denotes cases when the moon rise was 7–9 h after Time; A/S – age class (J – juvenile, S – subadult, A – adult) and sex (F – female; M – male); L – total body length (cm); Tbody – snake temperature (°C); Tmh – microhabitat temperature (°C); Dlen – day length in hh:mm; Td – warm (W) or hot (H) day; KG – Köppen-Geiger class; Elev – elevation. See the text for details.
Time | Ss | М% | A/S | L | Tbody | Tmh | Dlen | Td | KG | Elev | Latitude and Longitude | Date |
---|---|---|---|---|---|---|---|---|---|---|---|---|
19:38 | -15 | ?38 | A/F | 76.1 | 17.7 | 15.3 | 12:44 | W | Dfb | 709 | 42.8553, 23.2529 | 02.04.17 |
19:38 | -15 | ?38 | A/F | 75.2 | 22.7 | 15.1 | 12:44 | W | Dfb | 709 | 42.8553, 23.2529 | 02.04.17 |
20:55 | -11 | 98 | A/F | 58.6 | 25.1 | 23.9 | 15:10 | W | Dfb | 520 | 43.0889, 23.3820 | 07.07.17 |
20:56 | -9 | 100 | J/F | 27.2 | 28.2 | 26.9 | 15:20 | H | Dfa | 165 | 43.1796, 24.0603 | 20.06.16 |
20:25 | 1 | 99 | A/M | 62.3 | 30.4 | 26.4 | 13:48 | H | Dfb | 508 | 43.0896, 23.3860 | 17.08.16 |
21:00 | 1 | (4) | A/M | ~55 | – | – | 14:53 | H | BSk | 222 | 41.7631, 23.1562 | 14.07.18 |
20:11 | 6 | (23) | S/M | 33.3 | 28.5 | 24.6 | 13:21 | H | Dfa | 165 | 43.1795, 24.0604 | 27.08.16 |
20:58 | 8 | (58) | S/F | 36.9 | 22.6 | 21.4 | 15:18 | H | Dfb | 543 | 43.0895, 23.3848 | 16.06.17 |
20:39 | 12 | 67 | J/M | 25 | 22.7 | 17.2 | 14:13 | H | Dfa | 170 | 43.1801, 24.0575 | 04.05.17 |
21:02 | 24 | 100 | A/F | 62.8 | 27.1 | 24.5 | 14:13 | H | Dfb | 521 | 43.0895, 23.3836 | 07.08.17 |
20:13 | 27 | ?34 | J/M | 26.4 | 24 | 20.3 | 12:50 | W | Dfa | 209 | 43.1803, 24.0562 | 07.09.16 |
20:47 | 31 | (1) | A/F | 52.9 | 20.7 | 19.1 | 13:35 | W | Dfb | 447 | 43.0888, 23.3819 | 22.08.17 |
21:30 | 31 | (4) | A/M | ~63 | – | – | 14:53 | H | BSk | 214 | 41.7618, 23.1560 | 14.07.18 |
21:38 | 32 | (27) | A/M | 58.8 | 26.1 | 23.8 | 15:18 | H | Dfa | 167 | 43.1801, 24.0571 | 28.06.17 |
20:09 | 34 | (24) | A/F | 52.8 | 23.9 | 22.9 | 12:28 | H | Dfb | 521 | 43.0895, 23.3836 | 15.09.17 |
21:39 | 42 | (28) | A/M | 59.8 | 24.7 | 19.8 | 14:56 | H | Dfa | 170 | 43.1801, 24.0577 | 18.07.17 |
21:54 | 52 | 97 | S/F | 41.9 | 26.3 | 24.9 | 15:09 | H | BSk | 212 | 41.7662, 23.1554 | 15.06.19 |
21:10 | 69 | (59) | A/F | – | – | – | 13:24 | H | Csa | 322 | 41.4282, 26.0670 | 25.08.05 |
21:21 | 85 | (66) | J/M | ~20 | – | – | 13:31 | H | BSk | 9 | 42.7373, 27.8923 | 23.08.16 |
21:22 | 96 | ?34 | A/F | 61.1 | 21.5 | 19.6 | 12:50 | W | Dfa | 303 | 43.1516, 24.1013 | 07.09.16 |
22:48 | 104 | 84 | A/M | 49.4 | 27.6 | 26.4 | 15:06 | H | BSk | 210 | 41.7662, 23.1554 | 04.07.17 |
22:40 | 112 | ?76 | A/M | – | – | – | 15:04 | W | Cfa | 438 | 41.9328, 25.2894 | 06.06.06 |
22:06 | 135 | 98 | J/F | 24.6 | 27.9 | 14.8 | 13:00 | H | Dfa | 166 | 43.1799, 24.0549 | 04.09.17 |
23:10 | 144 | (61) | A/F | – | – | – | 15:03 | W | Cfa | 296 | 41.7034, 25.9668 | 08.06.04 |
23:00 | 149 | (0) | A/F | – | – | – | 14:16 | H | Cfa | 380 | 41.8677, 25.3264 | 04.08.05 |
22:25 | 158 | 94 | J/– | – | – | – | 12:45 | H | BSk | 92 | 41.4130, 23.3174 | 09.09.11 |
1:00 | 252 | (17) | A/M | – | – | – | 14:56 | H | Csa | 333 | 41.5975, 26.0507 | 11.07.05 |
We recorded active snakes from 2 April to 15 September. Activity seems to shift slightly to later hours of the night with the increase in the daily temperature; in April and May we only observed crepuscular activity.
Most (70%) of the crepuscular and nocturnally active vipers were recorded on hot days and the remaining on warm days (χ2 = 4.48, df = 1, p = 0.034). Mean Tbody (± SD) was 24.66 ± 3.89 °C (range: 17.7–30.4, N = 9) for the crepuscular vipers and 25.09 ± 2.61 °C (20.7–27.9, N = 9) for the nocturnal individuals. Mean Tmicrohabitat (± SD) was 21.23 ± 4.57 °C (15.1–26.9, N = 9) for the crepuscular vipers and 21.76 ± 3.68 °C (14.8–26.4, N = 9) for the nocturnal vipers.
Vipera ammodytes occurs throughout the country at elevations below 1450 m; crepuscular/nocturnally active individuals were found across both N-S and E-W gradients, at ~0–700 m a.s.l. (Fig.
In seven cases, when it could have potentially influenced snakes’ activity, the moon’s illumination was approaching full moon (>90%); in four of the five cases when the moonrise was 7–9 h before the time of observation, illumination was 34–38%. In 13 cases, regardless of the illumination percentage, the moon was likely not visible due to rising after the observation or setting beforehand; these cases also tend to have low illumination percentages.
Nocturnal activity has been demonstrated for several species of European vipers (
Furthermore, the observations fall within five climatic classes which are well-represented throughout the range of the species, suggesting that environmental conditions suitable for low/no-light activity should exist for many populations; why at certain locations the species seemingly might not exhibit this behavior (e.g.
Although based on a post hoc evaluation and a low sample size, it seems that lunar illumination might play a role in the observed activity, as most of our observations were either in the close-to-full moon or no moonlight conditions. The effects of moon illumination on V. ammodytes behavior need to be studied further, with data related to it collected in the field. Previous research on crotaline vipers suggests a complicated relationship. The full moon visually benefits snakes in prey acquisition, while potentially increasing predation (
It seems that the species is more likely to exhibit crepuscular or nocturnal activity mainly following hot days, substituting potentially unsuitable diurnal thermal conditions with ones optimizing physiological performance (e.g., locomotion and prey acquisition). However, snakes were also active after warm days. Vipera ammodytes prefers to adjust its Tbody between 28–33 °C (Saint Girons 1978;
This study was partially supported by the Bulgarian National Science Fund under Grant contract “KP-06-N21/11” from 14.12.2018. Scientific permits were issued by the Ministry of Environment and Waters (№520/23.04.2013, №656/08.12.2015). We thank Ivan Dikovski for the information about the individual from Irakli Beach. We thank two anonymous reviewers for suggestions that improved the manuscript.