All you can eat: autochthonous vertebrate and invertebrate predation by the alien spider Parasteatoda tepidariorum (C.L. Koch, 1841) (Araneae: Theridiidae) in two anthropogenic habitats of Italy
Abstract
We report the two main autochthonous prey items of the alien spider Parasteatoda tepidariorum (C.L. Koch, 1841) in two anthropogenic habitats of the Italian Alps, namely a lizard and a scorpion species: Podarcis siculus (Rafinesque, 1810) and Alpiscorpius sigma Kovařík, Štundlová, Fet & Šťáhlavský, 2019. Additionally, we briefly describe the predatory behavior of this spider with both preys, highlight the scarcity of records of invertebrate predation on vertebrates in Europe, and address some concerns regarding how this might affect autochthonous populations.
Keywords: Araneae; Theridiidae; Parasteatoda tepidariorum; Europe; Ecology; Vertebrate predation; Podarcis siculus; Alpiscorpius sigma.
Resumen
Todo lo que puedas comer: depredación de vertebrados e invertebrados autóctonos por parte de la araña introducida Parasteatoda tepidariorum (C.L. Koch, 1837) (Araneae: Theridiidae) en dos hábitats antropogénicos de Italia
Reportamos las dos principales presas autóctonas de la araña introducida Parasteatoda tepidariorum (C.L. Koch, 1841) en dos hábitats antropogénicos de los Alpes italianos, específicamente una especie de lagartija y una especie de escorpión: Podarcis siculus (Rafinesque, 1810) y Alpiscorpius sigma Kovařík, Štundlová, Fet & Šťáhlavský, 2019. Además, describimos brevemente el comportamiento depredador de esta araña con ambas presas, destacamos la escasez de registros de depredación de invertebrados sobre vertebrados en Europa y comentamos posibles efectos negativos sobre las poblaciones autóctonas.
Palabras clave: Araneae; Theridiidae; Parasteatoda tepidariorum; Europa; Ecología; Depredación sobre vertebrados; Podarcis siculus; Alpiscorpius sigma.
CONTENTS
Predation was early identified as one of the primary elements involved in community stability (Glasser, 1979; Polis et al., 1989). In the ‘invertebrate world’, the remarkable diversity of predators that interact and coexist with each other promotes the formation of guilds (Root, 1967; Polis et al., 1989), which are composed of species that exploit and compete for similar and often limited resources. Along with the rest of the trophic levels, they form complex food-webs in which the imperative rule is basically ‘eat or be eaten’. This spawns generalist predators (Levins & MacArthur, 1969), which have been identified as one of the main stabilizers in food-webs (Parsons, 1992; Gross et al., 2009; Brechtel et al., 2019). Nevertheless, when generalist predators have been accidentally introduced by humans to new environments, they have frequently caused a negative impact on autochthonous species (Dickman, 1996; Nentwig, 2015).
One example of generalist predators are webbing spiders, which include several cases of invasive or potentially invasive species (Vink et al., 2011; Nentwig, 2015; Hänggi & Straub, 2016). Parasteatoda tepidariorum (C.L. Koch, 1841), a cobweb spider belonging to the family Theridiidae, native to Asia and now considered cosmopolitan, was originally introduced in Europe and other parts of the world (Bonnet, 1930; Nentwig, 2015; World Spider Catalog, 2022). Despite comprehensive molecular and developmental studies (Mittmann & Wolff, 2012; Schomburg et al., 2015), scarce information regarding its diet in the newly invaded territories is available. Although diet specializations have been reported in some spiders of the family Theridiidae (i.e., dipterophagy) (Pekár et al., 2012), they mainly exhibit an euryphagous diet, practically feeding on everything that gets trapped on their webs (Salomon, 2011; Pompozzi et al., 2013; Mora-Rubio & Parejo-Pulido, 2021).
Here, we report the two main autochthonous prey items of this alien spider in two anthropogenic habitats of the Italian Alps. Additionally, we briefly describe the predatory behavior of this spider with both prey and address some concerns regarding how this might affect autochthonous populations.
Fig. 1.— Map showing the two localities in which predation events involving Parasteatoda tepidariorum (C.L. Koch, 1837) were observed.
Fig. 1.– Mapa que muestra las dos localidades en las que se observaron los eventos de depredación de Parasteatoda tepidariorum (C.L. Koch, 1837).
The observation of the predation events took place at two different anthropogenic habitats located along the Italian Alps (Fig. 1). The first habitat was a wooden cabin next to a mountain road in the village of Sonvico [45.814664ºN, 10.1394958ºE, 623 m.a.s.l.]. The beams were full of spider webs with several Parasteatoda tepidariorum individuals and their trapped prey (Fig. 2A-B). In this location, the spiders were mainly feeding on a lizard species very abundant in the area (see below). The second habitat was a concrete ‘mossy’ wall on the roadside of the main road towards Studena Bassa [46.518557ºN, 13.28285ºE, 674 m.a.s.l.]. Different arthropods inhabited the site such as woodlice or millipedes; however, the most abundant animals were Parasteatoda tepidariorum and scorpions of the genus Alpiscorpius Gantenbein et al., 1999 (Fig. 2C-D), which were the main prey item trapped in the spider webs.
We collected the lizard prey items, the scorpion prey items and Parasteatoda tepidariorum specimens of both sexes. All specimens were preserved in 95% EtOH and were later determined using a Leica MZ16A dissection scope. Prey items were identified using a field guide of European reptiles (Speybroeck et al., 2017) for the lizards, and following an identification key provided by Kovařík et al. (2019) in the case of scorpions. Spiders were identified following the online keys provided for the European species (Nentwig et al., 2022). Photographs were taken with a Sigma 105mm macro lens attached to a Nikon D3500 camera. Voucher specimens have been deposited in the Entomological collection of the University of Valencia (Dr. J. Selfa).
Fig. 2.— Parasteatoda tepidariorum (C.L. Koch, 1837) feeding on the two different prey items. A) Predation of Podarcis siculus (Rafinesque, 1810). B) ‘Biting the lizard’s tail and running-away’: strategy adopted by P. tepidariorum to feed on P. siculus. C) Predation of Alpiscorpius sigma Kovařík, Štundlová, Fet & Šťáhlavský, 2019. D) ‘Rolling up the scorpion weaponry’: strategy adopted by P. tepidariorum to feed on A. sigma.
Fig. 2.– Parasteatoda tepidariorum (C.L. Koch, 1837) alimentándose de las dos presas diferentes. A) Depredación de Podarcis siculus (Rafinesque, 1810). B) ‘Morder la cola de la lagartija y huir’: estrategia adoptada por P. tepidariorum para alimentarse de P. siculus. C) Depredación de Alpiscorpius sigma Kovařík, Štundlová, Fet & Šťáhlavský, 2019. D) ‘Enrollando el armamento del escorpión’: estrategia adoptada por P. tepidariorum para alimentarse de A. sigma.
The lizards captured by the Parasteatoda tepidariorum specimens were determined as Podarcis siculus (Rafinesque, 1810) (Fig. 2A-B). In most of the cases, Podarcis siculus individuals were barely entangled in the spider webs. They could move freely and were actively trying to release themselves. Accordingly, the strategy adopted by the spiders to prey on them was to continuously bite the lizard’s tail (Fig. 2B), move up and down the web avoiding a possible counterattack, and progressively paralyze it after several bites. Once the whole body was completely immobilized, the spiders started digesting the lizards (Fig. 2A).
On the other hand, the scorpions were identified as Alpiscorpius sigma Kovařík, Štundlová, Fet & Šťáhlavský, 2019 (Fig. 2C-D). As shown in Figure 2C-D, once the scorpion was trapped in the webs, P. tepidariorum individuals rapidly started rolling up its pincers and stinger with silk, preventing a possible pedipalp or metasomal strike.
Whereas scorpions and spiders are natural enemies worldwide (Williams et al., 2006; Blasco-Aróstegui et al., 2020; Duberstein & Sherwood, 2020; Mora-Rubio & Parejo-Pulido, 2021; Da Silva et al., 2021), most of the interactions having an arthropod as the predator and a vertebrate as the prey normally occur in tropical areas of the world (Valdez, 2020). In Europe, the scarce records of this type of encounters generally involve a spider, often from the family Theridiidae (Nyffeler & Pussey, 2014; O’Shea & Kelly, 2017). This might be determined by the potent venom within the family and its specific toxins targeting vertebrates (e.g., α-latrotoxin) (Gendreau et al., 2017).
Parasteatoda tepidariorum represents an ideal model organism to study this idea: a potentially invasive, true generalist predator with a great plasticity in its diet, often synanthropic and with a venom capable of killing small vertebrates (Fig. 2A-B). This is remarkable, as contrarily to other Theridiidae, α-latrotoxin is absent in the venom composition of this species (reported by Gendreau et al., 2017). From our observations, we hypothesize that this spider might be adapting its diet depending on prey availability in each area. This phenomenon is called ‘prey switching’ and has long been associated with foraging adaptation (Murdoch, 1969; Chesson, 1984; Baudrot et al., 2016). Whether this switching is having a positive effect (i.e., predator over-consumes a prey or another predator whose proportion increases and regulates its density) or a negative effect (i.e., predator over-consumes a prey or another abundant predator but severely decreases its numbers leading to extinction in the ecosystem) has yet to be investigated. In this sense, a change in top predator presence or abundance may dramatically alter food-web structure or even ecosystem state (Terborgh et al., 2001; Dobson et al., 2006). Uncovering how this might be affecting the autochthonous populations of the species P. tepidariorum prey upon –including their possible depletion– and how this may affect trophic chain stability in Europe or other invaded territories, would be of extreme importance if we intend to preserve native biodiversity.
Acknowledgements[Up]
We want to thank Dr. Jesús Selfa and the University of Valencia (Valencia, Spain) for granting us access to the facilities and allowing us to use their equipment. Thanks are extended to Alberto Sánchez-Vialas and Ignazio Avella for their help confirming the lizard species.
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