SALAMANDRA 54(3) 222–228 15 AugustAlena 2018 MarcellaISSN 0036–3375 Schäfer et al. Carabid predation on Bombina variegata metamorphs: size at and timing of metamorphosis matter Alena Marcella Schäfer, Francesca Schäfer, Thomas Wagner & Ulrich Sinsch Universität Koblenz – Landau, Institut für Integrierte Naturwissenschaften, Abteilung Biologie, Universitätsstr. 1, 56070 Koblenz, Germany Corresponding author: Ulrich Sinsch, e-mail: [email protected] Manuscript received: 8 May 2018 Accepted: 16 July 2018 by Stefan Lötters Abstract. The potential impact of carabid predation on dispersingBombina variegata metamorphs was studied in the field at the Schmidtenhöhe (Rhineland-Palatinate, Germany) and performing experimental trials in the laboratory. At least four carabid species were demonstrated to feed on metamorphs, with Carabus violaceus and Pterostichus niger mainly prey- ing on the smallest individuals, and Abax parallelepipedus and Harpalus rufipes indiscriminately attacking smaller and larger individuals. Predation rates were mostly low (5–15% of metamorphs) despite of high prey densities (83 metamorphs per m²), but hungry beetles consumed up to 60% within five days. Plasticity in the timing of metamorphosis (about two months) and in the size at metamorphosis (11–19 mm) observed in the field seemed to reflect mainly the variability in the spawning date and of aquatic environment during the tadpole development. Still, the tendency of metamorphs to be become larger on average towards the end of the metamorphosis period reduced their risk of being predated because the abundance of potential carabid predators did neither vary among habitat types crossed by dispersing metamorphs nor during the period of metamorphosis. Consequently, informed conservation management of endangered B. variegata populations should focus on larval habitats producing large-sized metamorphs to reduce loss of metamorphs by size-as- sortative carabid predation. Key words. Amphibia, Anura, Insecta, Coleoptera, Abax parallelepipedus, Carabus violaceus, Pterostichus niger, Harpalus rufipes, size-assortative mortality. Introduction represent carryover effects from the aquatic stage Chel( - gren et al. 2006). Amphibians with complex life cycles have evolved life- For example, larval density is negatively correlated history strategies to optimize timing of and size at meta- with the size of metamorphs in Epidalea calamita (Golay morphosis as key adaptations (Wilbur & Collins 1973). A & Durrer 1995), Anaxyrus fowleri (Yagi & Green 2018), wide range of possible sizes at metamorphosis is expected Pelophylax lessonae and its hybridogenetic form “esculen­ in species living in variable environments, compared to a tus” (Altwegg & Reyer 2003). Postmetamorphic growth narrower range in species inhabiting more stable environ- is uniform among toadlets of any size and does not com- ments. In fact, environmental heterogeneity favours phe- pensate for size differences at metamorphosis in these spe- notypic plasticity in morphology and life-history traits of cies (Golay 1996). Large Pelophylax metamorphs enjoy an Rhinella spinulosa (Márquez-García et al. 2009, 2010). increased chance of survival to adulthood, faster growth Fast desiccation of ponds triggered accelerated tadpole de- and larger size at maturity as compared with small-sized velopment resulting in an early metamorphosis and small- metamorphs (Altwegg & Reyer 2003). In Rhinella ma­ sized metamorphs, low desiccation rates caused late meta- rina metamorph size also varies within a wide range and morphosis and individuals with longer hindlimbs and larger individuals show better locomotor performance larger heads (Márquez-García et al. 2009). Thus, plas- on land and in water, are more successful in preying and ticity in timing of and size at metamorphosis traits may be have enhanced survival and growth rate (Cabrera-Guz- adaptive to larval growth environment reflecting the influ- mán et al. 2013). One of the proximate causes of variability ence of aquatic stressors, and affects fitness in a range of in size and body mass at metamorphosis is the timing of amphibian species (Altwegg & Reyer 2003). Population- metamorphosis. Plasticity of this trait has been observed level impacts of larval traits on fitness often do not become in many amphibians, e.g. Ambystoma talpoideum (Sem- visible before reaching the terrestrial stage and therefore, litsch & Wilbur 1988), Dryophytes versicolor (Beachy © 2018 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Mannheim, Germany Available222 at http://www.salamandra-journal.com Carabid predation on Bombina variegata metamorphs et al. 1999), Rana temporaria (Merilä et al. 2000), and Materials and methods R. aurora (Chelgren et al. 2006). In Phrynobatrachus Study area guineensis the increase of mortality rate in drying habitats represents a time constraint that promotes a reduced lar- In 2017, metamorphs of Bombina variegata were sampled in val period, also allowing a trade-off between development four clusters of breeding ponds at the former military training time and body mass (Rudolf & Rödel 2007). area Schmidtenhöhe near Koblenz (area: ca. 700 ha) (Rhine- Timing of and size at metamorphosis does not only af- land-Palatinate, Germany; cf. Sinsch et al. 1995). All local fect growth trajectories and fitness of juveniles and even waterbodies are manmade, most are remains of tank tracks, adults, but also may have direct consequences for surviv- others were constructed for the conservation management of al during the dispersal of metamorphs into the terrestri- yellow-bellied toads. Pond cluster 1 (50.201°N, 7.393°E, 298 m al habitats surrounding the breeding pond. Small-sized a.s.l.) is located in a former clay pit with a central large quarry meta morphs are more vulnerable to lethal attacks by spi- pond and about 15 smaller, often temporary ponds. Raw soil ders and carabid beetles than are large-sized ones. Specifi- areas and developing grassland are surrounded by deciduous cally, predation of carabids on temperate-zone amphibians woodland. Breeding ponds of B. varie gata were often locat- has been reported, but information given is mostly anecdo- ed within 10 m of the forest edge. Pond cluster 2 (50.346° N, tal (Toledo 2005). Not only anurans (Bufotes viridis, Hyla 7.644° E, 279 m a.s.l.) is located in an area used occasionally savignyi, Pelophylax bedriagae), but also urodeles (Triturus for training with heavy vehicle and includes up to 10 per- vittatus, Salamandra infraimmaculata) are attacked by manent and temporary ponds and ditches within an area of carabids. Different amphibian life stages are affected, adults bare soil, surrounded with a 30–210 m broad belt of grass- as well as metamorphs. Documented cases are reported for land followed by deciduous woodland. Cluster 3 (50.207° N, Epomis dejeani and E. circumscriptus in Israel (Wizen & 7.402° E, 333 m a.s.l.) includes 7 mostly permanent ponds Gasith 2011b), as well as for Chlaenius darlingensis in Aus- within a grassland and 200–430 m distant from deciduous tralia (Robertson 1989). Small specimens were observed woodland. The grassland is grazed by Konik horses and Tau- to be especially prone to carabid attacks, e.g. Scaphinotus rus cattle. Cluster 4 (50.209° N, 7.406° E, 338 m a.s.l.) com- angusticollis and Pterostichus melanarius prefer small ju- prises 16 shallow to deep former tank tracks within grassland venile Plethodon vehiculum (Ovaska & Smith 1987). Even with shrubs. The forest edge is between 10 and 60 m distant the larvae of some carabid species lure their potential prey from the ponds. Carabid surveys took place in the vicinity of and show predation behaviour on amphibians. Carabid pond clusters 1 and 3 (for details see below). larvae role-reversal has been reported for Chlaenius (E.) simba in South Africa (Scholtz & Ralston 2017), Epomis dejeani and E. circumscriptus in Israel (Wizen & Gasith Monitoring of recently metamorphosed toadlets 2011a) as well as for E. circumscriptus in Spain (Escoriza et al. 2017). Amphibians are also exposed to carabid attacks Mid-July of 2017, we observed the first toadlets of B. varie­ outside their activity period, as reported for Lissotriton gata near the breeding ponds and started at July, 21, a vulgaris while sharing a winter shelter with Pterostichus ni­ roughly weekly survey for metamorphs within a 1-m-belt ger in Poland (Bernard & Samolag 2014). However, the around the pond shores. All toadlets observed were collect- risk of predation by arthropods seems to be highest during ed, and snout–vent length (SVL, to the nearest 0.5 mm) and breeding season when metamorphs are leaving water (To- mass (to the nearest mg) were recorded for each individu- ledo 2005). al. We considered all toadlets of a SVL of less than 20 mm In the framework of a demographic study on yellow- as metamorphs because the largest late-metamorphic tad- bellied toads Bombina variegata in the low mountain poles of Gosner stages 44 and 45 with a tail bud remain- range of Rhineland-Palatinate (Germany), we found that ing had 19 mm SVL. The condition index (studentized re- metamorphs dispersing from the breeding ponds are ex- siduals of the SVL-mass relationship using a multiplicative posed to a variety of carabid species that forage in the sur- model ln(mass) = a + b × ln(SVL), with a = intercept and rounding grassland areas and forests (Taupp et al. 2015). b = slope; Reading 2007, equivalent to the residual index So far, there are no documented cases of carabids preying in Băncilă et al. 2010)