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Use of Quercus Acorns and Leaf Litter by North African Thorectes Species (Coleoptera: Scarabaeoidea: Geotrupidae)

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Use of Quercus Acorns and Leaf Litter by North African Thorectes Species (Coleoptera: Scarabaeoidea: Geotrupidae) Use of Quercus acorns and leaf litter by North African Thorectes species (Coleoptera: Scarabaeoidea: Geotrupidae) § F. Sánchez-Piñero1* , J.R. Verdú2 , J.M. Lobo3 & J.L. Ruiz4 1Departamento de Zoología, Facultad de Ciencias, Universidad de Granada, E-18071 Granada, Spain 2I.U.I. CIBIO, Universidad de Alicante, Alicante E-03080, Spain 3Departamento de Biogeografía y Cambio Global, Museo Nacional de Ciencias Naturales, CSIC, E-28006 Madrid, Spain 4Instituto de Estudios Ceutíes, Paseo del Revellín, 30, 51001 Ceuta, Spain Acorn burial and consumption by geotrupid dung beetles is an interesting trophic interac- tion recently reported for Iberian Thorectes and North American Mycotrupes species. In Iberian Thorectes species, this interaction provides not only ecophysiological and reproduc- tive advantages to the beetles but also more effective dispersal for Quercus acorns. The genus Thorectes is particularly diverse in the Iberian Peninsula and North Africa, where most species of the genus occur. Due to the high diversity of Thorectes in North Africa, especially in Morocco, where Quercus forests are widely distributed, we investigated whether acorn burial and consumption by Thorectes beetles also occurred in this region. For this, field sampling was conducted in northern Morocco by searching for beetles buried and consum- ing acorns within 1 m2 quadrats in areas where Thorectes species and Quercus forests occur jointly. Three beetle species (T. distinctus, T. laevigatus and T. trituberculatus) were found con- suming buried acorns of Q. suber in the field. Most of the beetles were found feeding on acorns, while only 20 % were found in dung-provisioned burrows. These results suggest that acorns constitute the staple food of some North African Thorectes species. In addition, we found T. trituberculatus and T. distinctus burrows and nests provisioned with oak leaf litter. Burrows and nests provisioned with Quercus litter also suggest a tighter interaction of Thorectes beetles with oaks. Feeding and nesting with relatively predictable and abundant resources in oak forests, such as acorns and leaf litter, may be especially important to explain the diversification and success of flightless Thorectes species in Mediterranean ecosystems such as those of the Iberian Peninsula and North Africa. Key words: plant–animal interaction, dung beetles, seed-feeding beetles, saprophagy, leaf-litter nesting. INTRODUCTION Dung beetles in the families Scarabaeidae species feed on different dung types, plant detri- (including Scarabaeinae and Aphodiinae) and tus, and fungus (Howden 1955, 1964; Palestrini & Geotrupidae comprise a diverse array of species Zunino 1985; Martín-Piera & López-Colón 2000). which exploit faeces, mainly from large herbivores An interesting trophic interaction in geotrupid (Hanski & Cambefort 1991). Although there are dung beetles involves acorn consumption, which often local preferences for different types of excre- provides ecophysiological and reproductive ment (Hanski & Cambefort 1991; Martín-Piera & advantages to the beetles and has implications in Lobo 1996; Finn & Giller 2002; Tshikae et al. 2013), the dynamics and regeneration of Mediterranean many of these beetles are not specialised in the use Quercus forests (Verdú et al. 2010, 2011; Pérez- of a specific type of dung. Furthermore, many Ramos et al. 2013). Feeding on acorns has been species can feed on carrion, decaying plant reported in two Iberian species of the genus material, and fungi (Halffter & Matthews 1966; Thorectes (T. lusitanicus (Jekel, 1866)) and T. baraudi Hanski 1983; Walter 1983; Philips et al. 2004; López-Colón, 1981; Verdú et al. 2007, 2011] and in Halffter & Halffter 2009). Trophic generalism is one North American species of the genus Myco- especially widespread in Geotrupidae, as many trupes (M. lethroides (Westwood, 1837); Beucke & *Author for correspondence. E-mail: [email protected] Received 20 October 2017. Accepted 6 June 2018 ISSN 1021-3589 [Print]; 2224-8854 [Online] African Entomology 27(1): 10–17 (2019) DOI: https://doi.org/10.4001/003.027.0010 ©Entomological Society of Southern Africa Sánchez-Piñero et al.: Use of acorns and leaf litter by Thorectes species 11 Choate 2009). In the case of Iberian species, acorn (Shay 2001) and oak forests are widely distributed, consumption by T. lusitanicus increases the inges- raises the question of whether the interaction tion of fatty acids, which in turn provides an between the beetles and Quercus occurs in this ecophysiological advantage to the beetles, allow- region. Finding this interaction in North African ing them to withstand more extreme cold condi- Thorectes species is relevant for conservation and tions and, consequently, to maintain a broader management of Mediterranean ecosystems in activity period during winter (Verdú et al. 2010). the region. On the one hand, apterism and low At the same time, because acorn production and dispersal ability of these beetles would explain the consumption by T. lusitanicus coincides with the high vulnerability of Thorectes species from a con- reproduction period of the beetles, acorn feeding servation perspective (see Verdú & Galante 2006 increases the reproductive potential because of for factors threatening the Iberian species). Thus, enhanced ovarian development due to the higher due to restricted distributions and habitat frag- metabolic reserves of the fat body (Verdú et al. mentation, six out of 22 species belonging to the 2010). genus Thorectes have been catalogued as threat- Acorn burial and consumption not only affects ened (IUCN 2016). On the other hand, the high the ecophysiology of Thorectes species, but also has degree of endemism of Thorectes species increases an important role in acorn dispersal (Pérez-Ramos the need to study this interaction because of its et al. 2007; Verdú et al. 2007, 2011). Because T. lusi- effects on Quercus dispersal and recruitment, tanicus individuals bury a large number of acorns especially in the Iberian Peninsula and northern that are partially consumed without damaging the Morocco where Thorectes registers its highest cotyledons, feeding on acorns by the beetles does diversity. not negatively affect seedling germination. As a In this study we report the use of Quercus acorns result, the beetles are more effective dispersers by Thorectes beetles in North Africa and the novel than rodents, which generally consume the whole finding of nesting with Quercus leaf litter in these acorn (Pérez-Ramos et al. 2013). These results geotrupid dung beetles. suggest an interesting ecological interaction between Thorectes beetles and Quercus species, MATERIAL AND METHODS which are key components of the Mediterranean forest vegetation. This interaction has further Study area connections to the vertebrate herbivores, whose Sampling was conducted in January 2014 in faeces are buried by these beetles for feeding and northern Morocco (Fig. 1, Table 1), in areas where nesting, indirectly favouring acorn dispersal Thorectes species may be found within forests of (Verdú et al. 2007) and likely enhancing soil- Quercus ilex, Q. suber, Q. faginea and/or Q. cana- nutrient cycling (Nichols et al. 2008). riensis. All the surveyed sites registered high sheep The genus Thorectes (excluding species belong- and cattle densities and thus high dung availabil- ing to genera Jekelius López-Colón, 1989 and ity. Due to acorn consumption by livestock and, in Silphotrupes Jekel, 1866 (López-Colón 1989, 1996; some cases, gathering by local people, acorns Cunha et al. 2011; Lobo et al. 2015; Schoolmeesters seldom appeared on the ground surface, prevent- 2016) is particularly diverse in the Iberian Penin- ing estimations of acorn availability. sula and North Africa, where 16 out of the 22 species of the genus occur (Schoolmeesters 2016). Sampling Within North Africa, the highest diversity of A total of 17 sites were sampled within the study Thorectes is found in Morocco, where seven out of area (Fig. 1), but only nine corresponded to the 11 North African species of the genus are dis- Quercus forests inhabited by Thorectes species tributed: T. laevigatus (Fabricius, 1798), T. distinctus (Table 1). To determine whether Thorectes species Marseul, 1878, T. trituberculatus Reitter, 1893, buried and fed on acorns, at each site we looked T. coloni Ruiz, 1998, T. armifrons Reitter, 1893, for buried beetles (either with or without acorns T. coiffaiti Baraud, 1969, and T. variolipennis and/or excrement) as well as for nests provisioned Marseul, 1876 (Baraud 1985; Ruiz 1998; with litter (see below) or excrement under Quercus Schoolmeesters 2016; see also http://www.biogeo- trees. To find buried beetles and nests, we grafia.org/). The diversity of the genus Thorectes in exhaustively searched under the leaf litter and Morocco, where six species of Quercus also occur up to 25 cm depth in the soil within randomly 12 African Entomology Vol. 27, No. 1, 2019 Fig. 1. Location of sampling sites in northern Morocco. Sites where both Thorectes and Quercus species were found are showed as large circles (see Table 1), while white squares represent sites with Quercus species in which no evidence of Thorectes species burying or consuming acorns was found. Black dots represent the location of the remaining surveyed sites. selected 1 m2 quadrats under tree canopies of RESULTS Q. suber, Q. ilex, Q. faginea and Q. canariensis.At each site, we searched 6–15 quadrats 100 m apart Four species of the genus Thorectes were found: in a total of 88 plots at the nine sites where both Thorectes
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