Revista Brasileira de Entomologia 61 (2017) 300–306 REVISTA BRASILEIRA DE Entomologia A Journal on Insect Diversity and Evolution www.rbentomologia.com Biology, Ecology and Diversity Daily activity of Dichotomius geminatus (Arrow, 1913) and Deltochilum verruciferum Felsche, 1911 (Coleoptera: Scarabaeinae) facing carrion: from resource perception to feeding a,b,∗ b b Renato Portela Salomão , Bruna Martins Bezerra , Luciana Iannuzzi a Instituto de Ecología, A. C., Red de Ecoetología, Xalapa, Mexico b Universidade Federal de Pernambuco, Centro de Biociências, Departamento de Zoologia, Recife, PE, Brazil a b s t r a c t a r t i c l e i n f o Article history: Dung beetles (Scarabaeinae) interact with resources in different ways and are classified according to Received 7 December 2016 resource relocation guilds. Dichotomius geminatus (Coprini) and Deltochilum verruciferum (Canthonini) Accepted 3 July 2017 are two of the most abundant and ecologically important species of the semi-arid region of Brazil, and Available online 16 July 2017 understanding their behaviour may facilitate the comprehension of strategies associated to competition Associate Editor: Lúcia Almeida for resources. The aim of the present study was to investigate the behavioural repertoire of D. geminatus (tunneler) and D. verruciferum (roller), in isolation and controlled setting in the Brazilian semi-arid biome, Keywords: using carrion as a food resource. Our hypothesis was that, due to the distinct food relocation strategies Arena presented by these species, distinct behaviours would occur involving resource utilization. We also com- Activity budget Scarabaeidae pared the behaviour of the two species and investigated the period of diel activity. Both species were more Semi-arid active during the night, but D. geminatus presented a shorter peak of nocturnal activity when compared Foraging to D. verruciferum. Although there was activity during the day, feeding was only observed during the night, for both species. During the periods of inactivity, D. verruciferum commonly went underneath the carrion, remaining still. As the target species of the study are very abundant, the differences in behaviour associated with the distinct relocation guilds may indicate a strategy to avoid direct competition. © 2017 Sociedade Brasileira de Entomologia. Published by Elsevier Editora Ltda. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). Introduction 2010), such as the presence of predators and the availability of food resources (Young, 1982; Hanski and Cambefort, 1991; Scholtz et al., Arid and semi-arid environments are strongly restrictive due to 2009). its scarce resource availability for both plants and animals (Dayton The Caatinga forest is a semi-arid biome restricted to Brazil and Fitzgerald, 2006; Ma et al., 2008; Holter et al., 2009; Valera (Andrade-Lima, 1981; Leal et al., 2003). This region has very high et al., 2011). To cope with such limitations, animals may adopt temperatures throughout the year and low irregularly distributed different behavioural strategies (Leal et al., 2003; Ocampo and annual rainfalls, concentrated within few months, presenting years Philips, 2005; Liberal et al., 2011; Nobre et al., 2012). Dung beetles of drought during months commonly classified as rainy (Leal et al., (Coleoptera: Scarabaeinae), for example, exhibit temporal variation 2003; Prado, 2003). In Caatinga areas, as in many tropical regions of in behaviours, which constitutes one of the main mechanisms to the world, necrophagy is a common habit among dung beetles, and avoid unfavourable habitat conditions, contributing to their ecolog- many species are known to be copro-necrophagous (Hernández, ical success (Hanski and Cambefort, 1991; Hernández, 2002; Feer 2007; Neves et al., 2010; Medina and Lopes, 2014). Overall, and Pincebourne, 2005; Hernández, 2007; Halffter and Halffter, dung beetles rely on animal faeces, mainly of mammals, for food 2009; Lopes et al., 2011; Valera et al., 2011). The daily activity of and reproduction (i.e. coprophagy). However, the coprophagous dung beetles is generally classified as either diurnal, nocturnal or behaviour could be replaced or supplemented by other resources crepuscular, and is regulated by a number of factors (Hernández, including dead animals (i.e. necrophagy) or decaying material (i.e. 2002; Feer and Pincebourne, 2005; Hernández, 2007; Gillett et al., saprophagy) (Gill, 1991; Halffter and Halffter, 2009; Scholtz et al., 2009). The relatively low species richness of the native mammals of Caatinga (Mares et al., 1985; but see Albuquerque et al., 2012) is one ∗ of the factors reflecting the poor diversity of the dung beetles in this Corresponding author. biome, which may be explained by the low availability of different E-mail: [email protected] (R. Portela Salomão). http://dx.doi.org/10.1016/j.rbe.2017.07.001 0085-5626/© 2017 Sociedade Brasileira de Entomologia. Published by Elsevier Editora Ltda. This is an open access article under the CC BY-NC-ND license (http:// creativecommons.org/licenses/by-nc-nd/4.0/). R. Portela Salomão et al. / Revista Brasileira de Entomologia 61 (2017) 300–306 301 resources. Furthermore, the Caatinga’s high temperatures and dry The data presented in our study provides comparative information climate (Leal et al., 2003) presents a limiting factor for dung beetles, on the behavioural ecology of two species of dung beetles and may since they depend on ephemeral resources that become unusable bring insights into evolutionary aspects of their foraging strategies. when desiccated (Theuerkauf et al., 2009). The use of carrion seems to be an attractive alternative in the Caatinga, as it stays attractive Material and methods for long periods when compared to faeces (Theuerkauf et al., 2009; Mayer and Vasconcelos, 2013). Study area and trapping method Deltochilum verruciferum, and Dichotomius geminatus, are two of the most common and abundant dung beetles in Caatinga forests The study was conducted in two fragments of Caatinga scrub for- (Hernández, 2007; Liberal et al., 2011; Medina and Lopes, 2014). est situated in northeastern Brazil: Area-1: located at “Boqueirão The high abundance of some dung beetle species are usually cor- ◦ ◦ da Onc¸ a” (10.9048 S, 41.2111 W), North of Bahia, Brazil; and Area- related with essential ecological services, since they remove large ◦ ◦ 2: located at Parnamirim city (8.5026 S, 39.3442 W), Pernambuco, portions of excrement, consequently dispersing seeds and improv- Brazil. Both fragments are well-preserved, thus presenting a dung ing the soil quality (Nichols et al., 2008). Species of Deltochilum beetle fauna with reduced environmental stressors. Both areas Eschscholtz, 1822 are usually associated with copro-necrophagy, have hot semi-arid climate (type “BSh”), according to the Köppen but there are also active predators within the genus (Hanski and climate classification (Velloso et al., 2002), presenting low varia- Cambefort, 1991; Cano, 1998). They have anatomical adaptations tion on the temperature throughout the year. The average annual such as clypeal teeth and well-developed tibiae, which help them to ◦ temperature in Boqueirão da Onc¸ a is 30 ± 0.68 C, whereas in Par- catch and process active preys. Deltochilum species are telecoprids ◦ namirim the average annual temperature is 26 ± 1.20 C (Velloso or rollers – they roll dung balls taking it away from the origi- et al., 2002; IBGE, 2013; Climate-Data, 2016). The average annual nal site (Halffter and Edmonds, 1982; Scholtz et al., 2009). They rainfall is 650 mm and 431 mm in Boqueirão da Onc¸ a and Par- are characterized by having strong posterior legs (Scholtz et al., namirim, respectively. The rainy period occurs irregularly from 2009), and travel relatively long distances (from many centime- October to April, and the rainfall usually is distributed on a few tres to a few metres) to store their resources, spending a great deal months of this season (Velloso et al., 2002; Beltrão et al., 2005). of energy in the process (Krell et al., 2003; Krell-Westerwalbesloh Dung beetle sampling and observation were conducted in Febru- et al., 2004). On the other hand, members of Dichotomius Hope, 1838 ary and March 2013 in Area-1, and April 2013 in Area-2, periods are associated with copro-necrophagy and saprophagy (Hanski and in which the studied species (D. geminatus and D. verruciferum) are Cambefort, 1991; Halffter and Halffter, 2009). They are paracoprids known to be active in these regions (Hernández, 2007; Liberal et al., (tunnellers group), which bury directly underneath the pile of dung. 2011). They have strong and well-developed anterior legs to help with the To capture the dung beetles, we used pitfall traps with two bait digging of galleries close to food resources (Hanski and Cambefort, types: human faeces and carrion (rotten bovine spleen). In total, 1991; Scholtz et al., 2009). we used 120 baited pitfall traps and, in each area, we used 60 pit- Species that share the same resource and dwell at the same sites, fall traps, 30 baited with carrion (50 g) and 30 baited with human as D. geminatus and D. verruciferum, may exhibit adaptive strategies faeces (50 g). For each trap, we suspended the bait beneath a lid to avoid excessive competition for resources (Medina and Lopes, directly above the pitfall. The lid was used to stop the rain from 2014). Microhabitat specialization, specific period of activity and getting into the traps. Inside the traps we added some of the local distinct foraging behaviours may result from competitive scenarios soil to allow the beetles to dig and hide, in an attempt to reduce (Larsen et al., 2006; Hernández, 2007). Dung beetles, for example, stress to the individuals. Traps were left on the site for 24 h and exhibit specific behaviours encompassing the resource exploita- the beetles were collected and kept in cylindrical plastic bottles tion that appears as result of the intensive competition of these (10 cm × 6 cm) also containing soil taken from the campsites. Those insects for decaying matter (Hanski and Cambefort, 1991; Halffter beetles were taken to observational studies in arenas on the site.