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Bad Moon Rising? the Influence of the Lunar Cycle on Amphibian Roadkills

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Bad Moon Rising? the Influence of the Lunar Cycle on Amphibian Roadkills European Journal of Wildlife Research (2019) 65: 58 https://doi.org/10.1007/s10344-019-1285-3 ORIGINAL ARTICLE Bad moon rising? The influence of the lunar cycle on amphibian roadkills F. Mestre1 & H. Lopes2 & T. Pinto2 & L. G. Sousa2 & A. Mira2 & S. M. Santos2 Received: 16 October 2018 /Revised: 1 May 2019 /Accepted: 8 May 2019 /Published online: 28 June 2019 # Springer-Verlag GmbH Germany, part of Springer Nature 2019 Abstract Annually, roads, and their associated users, are responsible for millions of roadkills worldwide. Mortality affects multiple taxonomic groups, but amphibians are particularly vulnerable, due to their size and underreporting. In fact, very high mortality frequencies can occur, mostly during short periods of time, when individuals migrate to and from reproduction areas (e.g., ponds). In this study, we assess the influence of the lunar cycle on amphibian roadkills, while accounting for weather conditions. As expected, the main environmental effects explaining roadkill numbers were weather related, with increases in minimum air temperature, average relative air humidity, and cumulative rainfall during the previous 24 h having a positive effect on roadkill numbers for all studied species. However, the lunar cycle also affected roadkills for two of the studied species. Darker nights had higher numbers of roadkills of Pleurodeles waltl, while moonlit nights had higher numbers of Salamandra salamandra.Assuch, these moon effects are species specific. Animals that are more active in moonlight may be at an advantage if their visual acuity is better than that of their predators. We hypothesize that differences between species in the response to moonlight may be due to differences perceived in predation risk. This information should be considered when designing mitigation measures. Volunteer actions, for instance, can be planned and coordinated keeping in mind the most appropriate weather conditions for the general amphibian community and specific phases of the lunar cycle for particular species. Keywords Lunar effects . Migration . Moonlight . Roads . Weather conditions Introduction Benítez-López et al. 2010; van der Ree et al. 2015; Richardson et al. 2017; Santos et al. 2017). In particular, road The threat posed to biodiversity by linear infrastructures, in- networks have three mainly reported negative impacts (van cluding roads and railways, is widely acknowledged in the der Ree et al. 2015): (i) indirect landscape effects (habitat scientific literature (Seiler and Helldin 2006; Coffin 2007; degradation or loss and barrier effect); (ii) direct mortality (e.g., roadkill); and (iii) avoidance behavior, due to the high disturbance caused by the road traffic to its surroundings. By comparison, some positive effects have been reported. In fact, This article is part of the Topical Collection on Road Ecology some species find the road margins an attractive and suitable Guest Editor: Marcello D’Amico habitat as in the case of several birds (reviewed in Morelli Electronic supplementary material The online version of this article et al. 2014) and small mammals, like the Cabrera’s vole (https://doi.org/10.1007/s10344-019-1285-3) contains supplementary (Microtus cabrerae) in studies conducted in Portugal (Santos material, which is available to authorized users. et al. 2007a) and the common vole (Microtus arvalis) and crowned shrew (Sorex coronatus) in studies in France * F. Mestre [email protected] (Redon et al. 2015). Moreover, some studies have document- ed the use of road verges as preferential movement corridors such as for the hazel dormouse (Muscardinus avellanarius)in 1 ‘ ’ Cátedra Rui Nabeiro de Biodiversidade, University of Évora, Casa Germany (Encarnação and Becker 2015). However, this at- Cordovil 2° Andar, Rua Dr. Joaquim Henrique da Fonseca, 7000-890 Évora, Portugal traction to road surroundings may also transform the road into an ecological trap, leading animals to suffer increased mortal- 2 ICAAM - Instituto de Ciências Agrárias e Ambientais Mediterrânicas; UBC – Conservation Biology Lab, University of ity (Morelli et al. 2014), with the positive effects of roads Évora, Mitra, 7002-554 Évora, Portugal resulting in negative consequences. 58 Page 2 of 12 Eur J Wildl Res (2019) 65: 58 Mortality caused by roads affects all taxonomic groups, but susceptible to roadkill during their peak activity periods (Hels amphibians are particularly vulnerable (Síllero 2008; and Buchwald 2001;Puky2005). Holderegger and Di Giulio 2010; Colino-Rabanal and Lizana While season has a significant influence on species activity, 2012;D’Amico et al. 2015;Franchetal.2015). Due to their there are several examples in the literature acknowledging the small body size and lower conspicuousness, amphibian roadkill effects of moonlight on different species behaviors (reviewed is frequently underestimated (Hels and Buchwald 2001;Santos in Kronfeld-Schor et al. 2013). Many species, marine and et al. 2011). However, some studies have reported that an impor- terrestrial, show some kind of adjustment in their activity tant proportion of roadkill species belongs to this group, levels and movement patterns to the lunar cycle (Kronfeld- highlighting the relevance of the threat to amphibians Schor et al. 2013; Chakraborty 2018). The various moon (Ascensão and Mira 2005; Glista et al. 2007;Carvalhoand phases and their influence on tides and geomagnetic fields Mira 2011; Matos et al. 2012;Beebee2013). In a study conduct- are perceived by animals and affect their behavior ed in Portugal, Carvalho and Mira (2011) reported that amphib- (Kronfeld-Schor et al. 2013). For example, the reproductive ian mortality can reach values of up to 70% of total vertebrate activity of fiddler crabs (genus Uca) reflects the 14-day semi- mortality during the wet season and amphibians are one of the lunar cycle in the Atlantic Coast of USA, while deer mice taxa most affected by roadkills, along with passerine birds (which (Peromyscus maniculatus) foraged less during a full moon may reach 60–70% in certain spring months). In another study in when compared to the new moon in a study conducted in the same region (Ascensão and Mira 2005), amphibians repre- Santa Barbara Island, USA, to decrease predation risk by barn sented around 56% of the total mortality, while a study conducted owls (Tyto alba)(Chakraborty2018), and maned wolves in the USA (Glista et al. 2007) determined that amphibians rep- (Canis brachyurus) in Brazil responded to temporally reduced resent around 95% of total roadkills. Several factors impact am- prey availability by reducing their distance traveled on full phibian mortality numbers, with the more relevant being (i) moon nights when compared to other nights (Chakraborty movement ability, with species with higher vagility being more 2018). Geomagnetic fields are also influenced by the lunar affected by roads (Carr and Fahrig 2001; Colino-Rabanal and cycle, with peaks during the third quarter moon and decreases Lizana 2012;Meek2012); (ii) immobility in the face of an ap- at the first quarter (Stolov 1965). These fields provide naviga- proaching vehicle (Mazerolle et al. 2005;Limaetal.2015); (iii) tional cues for animals (Phillips 1986; Fischer et al. 2001; traffic intensity (Hels and Buchwald 2001; Mazerolle 2004); (iv) Grant et al. 2009;Mestreetal.2014)asbirdsarewellknown surrounding habitat (Síllero 2008; Matos et al. 2012; Heigl et al. to use geomagnetic fields for orientation when migrating long 2017); and (v) proximity to reproduction sites, such as ponds and distances (e.g., Ossenkopp and Barbeito 1978). streams (Ascensão and Mira 2005;Santosetal.2007b). With regard to amphibians, the effect of the moon as a cue High mortality numbers of amphibians are often aggregated to some phases of their phenological cycle has been discussed in time, particularly when individuals migrate to and from repro- in the literature (Grant et al. 2009, 2012; Vignoli and Luiselli duction areas (e.g., ponds) (Síllero 2008; Brzeziński et al. 2012). 2013; Underhill and Höbel 2018), raising the possibility that In fact, the complex reproduction cycles of most amphibian spe- the movement intensity of amphibians might be somewhat cies, which include both terrestrial and aquatic phases (for breed- affected by the moon, with indirect effects in roadkill num- ing), imply seasonal movements of large numbers of individuals bers, although this is species specific (Grant et al. 2012). For between different habitats which are performed mostly at night example, Bufonidae, Ranidae, Salamandridae, and Hylidae (Ferrand de Almeida et al. 2001; Hels and Buchwald 2001; are influenced more by lunar cycles than other families Loureiro et al. 2008;Langenetal.2009; Colino-Rabanal and (Grant et al. 2012), and while the adaptive significance for Lizana 2012). For most species residing in Mediterranean cli- amphibians of lunar-mediated behaviors is rare, predator mates, the onset of movement toward the aquatic breeding sites avoidance, reproductive synchronization, visual signaling, is determined by the first autumn rainfall (September– foraging, and navigation have all been observed (Grant et al. November), while monthly average temperatures are still mild 2012). The activity of several individuals of the genus Litoria (> 10 °C; Díaz-Paniagua 1992;IPMA2014) and ends in late was significantly greater close to full moon nights, possibly as spring (May) (Ferrand de Almeida et al. 2001;Richter-Boix an adaptation to predation by snakes (Brown and Shine 2002; et al. 2006; Loureiro et al. 2008). Following
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