Author's personal copy Acta Oecologica 47 (2013) 74e80 Contents lists available at SciVerse ScienceDirect Acta Oecologica journal homepage: www.elsevier.com/locate/actoec Original article Bird predation affects diurnal and nocturnal web-building spiders in a Mediterranean citrus grove L. Mestre a,b,*, N. Garcia a,b, J.A. Barrientos b, X. Espadaler a,b, J. Piñol a,b a CREAF, Cerdanyola del Vallès 08193, Spain b Univ. Autònoma Barcelona, Cerdanyola del Vallès 08193, Spain article info abstract Article history: Spiders and birds can greatly decrease insect populations, but birds also limit spider densities in some Received 2 May 2012 habitats. Bird predation is thought to be one of the causes behind nocturnal activity in spiders, so night- Accepted 4 January 2013 active spiders that hide in retreats during the day should be less affected by bird foraging than day-active Available online spiders. However, this hypothesis has not yet been tested. We investigated the importance of bird predation on the spider community of a Mediterranean organic citrus grove. We excluded birds by Keywords: placing net cages over the trees and we conducted visual searches in the canopies to sample web- Araneidae building spiders. As there are many nocturnal species in the family Araneidae, we conducted searches Diel activity Hunting spider both by day and by night to compare the abundance of active araneids in these two time periods. We Night sampled the tree trunks with cardboard bands to collect hunting spiders. In bird-excluded canopies there Theridiidae were more spiders of the families Araneidae and Theridiidae. There were higher numbers of active Web-building spider Araneidae at night, but these were just as negatively affected by bird predation as day-active Araneidae, so there was no evidence of nocturnal activity serving as an anti-predator strategy. We did not find any negative impact of birds on hunting spiders. Our results contrast with other studies reporting a negative effect of birds on hunting but not on web-building spiders. Ó 2013 Published by Elsevier Masson SAS. 1. Introduction forage during day, bird predation is thought to be one of the causes behind nocturnal activity in spiders (Foelix, 2010); Spiders and birds are abundant predators that can reduce in- accordingly, night-active spiders should be less affected by bird sect pest populations in terrestrial habitats (Buddle et al., 2000; foraging than day-active spiders. However, this hypothesis has Gruner, 2004) and even curtail plant damage by lowering the received very little attention (Rypstra, 1984). In contrast, patterns numbers of herbivores (Mols and Visser, 2002; Sanders et al., of diel vertical migration in aquatic vertebrate and arthropod 2011; Van Bael et al., 2003). Some experimental studies, howev- communities are well known, and their potential causes such as er, have shown that birds can sometimes limit spider populations predator avoidance have been examined for a long time (Eggers, (Philpott et al., 2004; Wiens et al., 1991; reviewed by Gunnarsson, 1978; Fancett and Kimmerer, 1985; Mehner, 2012; Rinke and 2007). Petzoldt, 2008). Although many spider species are nocturnal, remaining inac- Our aim was to investigate the importance of bird predation in tive and hidden in retreats during the day, studies of bird preda- the spider community of a Mediterranean organic citrus grove. tion are based on sampling schedules that do not distinguish Mestre et al. (2012) had already excluded birds (and ants) from between nocturnal and diurnal species (Cardoso et al., 2008; trees on the same site and sampled arthropods with beating trays. Coddington et al., 1996; Richardson and Hanks, 2009). As birds Although spiders were not found to be affected by bird predation, visual inspection of the canopies suggested that this negative result could be due to the chosen sampling method, particularly as beating trays under-represent some groups of spiders, such as web- * Corresponding author. Departament de Biologia Animal, Biologia Vegetal i builders (Costello and Daane, 1995). Ecologia (BABVE), Facultat de BioCiències, Edifici C, Universitat Autònoma de Bar- celona, 08193 Bellaterra, Spain. Tel.: þ34 93 581 3744; fax: þ34 93 581 1321. In the present work we study the effect of birds on the spider E-mail address: [email protected] (L. Mestre). assemblage, using different sampling methods, both by day and 1146-609X/$ e see front matter Ó 2013 Published by Elsevier Masson SAS. http://dx.doi.org/10.1016/j.actao.2013.01.001 Author's personal copy L. Mestre et al. / Acta Oecologica 47 (2013) 74e80 75 by night. We wanted to answer the following questions. First, did individuals to species on the basis of their shape and colour bird predation affect the spider assemblage of the grove? If so, markings (see below). Two trained observers (LM and NG) con- which spiders were involved in these changes? Third, was the ducted the searches and each of them was assigned 4 exper- effect of bird predation lower on night-active spiders? imental blocks so that they would examine an equal number of trees from each treatment. We set the searching time at 15 min per tree and we established a searching protocol to avoid double counts of individuals. We began at the eastern part of the canopy 2. Material and methods and we looked for spider webs counter-clockwise until we reached the starting point; we followed this procedure at 3 2.1. Study site canopy heights defined for each tree: lower, middle and upper height. The grove is located at La Selva del Camp (Catalonia, NE Spain; 41 130 0700N, 1 80 3500E). The climate is Mediterranean, with 2.3.1.1. Diurnal searches. At noon (12e14 h) we looked for in- a rainy spring and autumn and a dry winter and summer. There dividuals belonging to all web-building spider families. The most are ca. 300 Clementine trees (Citrus clementina var. clemenules) abundant families of web-builders in the grove are Araneidae, grafted on the hybrid rootstock Carrizo citrange (Poncirus trifo- Theridiidae, and Linyphiidae (Piñol et al., 2010). We included liata (L.) Raf. Â Citrus sinensis (L.) Osb.), which are watered during occupied as well as empty but intact webs because abandoned dry periods. The grove complies with all organic agriculture webs degenerate in a few days (Toft et al., 1995), and we assumed standards, i.e. no pesticides, fungicides or herbicides are applied, intact empty webs of Araneidae to belong to a spider hidden in and only organic manure is used as fertiliser. Grasses and other aretreatinthecanopy(Foelix, 2010). ruderal vegetation form a permanent ground cover, which is mowed 3e4 times per year between rows and 5e6timesper 2.3.1.2. Nocturnal searches. Because many species of Araneidae year beneath trees. are nocturnal (Scharff and Coddington, 1997), a second visual search for araneid spiders was performed at midnight (24e02 h) 2.2. Experimental design with headlamps. We only found a few individuals from species that have no distinct dayenight activity patterns but sit per- We set up a randomised complete block design (RCBD) to manently on their webs (Argiope bruennichi, Cyclosa oculata,and exclude birds from the tree canopies. The experimental area Cyrtophora citricola; Blanke, 1972; Scharff and Coddington, consisted of 4 tree rows of 16 trees planted in 2001, each row 1997). e being divided into 2 blocks of 7 trees separated by 2 3 non- In order to quantify differences in the activity of araneid spiders experimental trees. These blocks were divided into 2 plots of 3 by day and by night, we defined an araneid spider as “active” if it trees each, generally separated by 1 non-experimental tree. The was sitting on its web instead of hiding in the canopy (Ceballos “ ” “ ” plots were randomly assigned to either a cage or a no cage et al., 2005; Chuang et al., 2008). Therefore, for the comparisons treatment so that the 2 treatments were present in each of the 8 between day-time and night-time activity in spiders from the ¼ blocks (thus N 8 plots for each treatment). Net cages of ca. family Araneidae we only took into account occupied webs. 10.5 Â 3 Â 2m,withaplasticmeshof30Â 30 mm, were built around the multiple-tree plots to prevent birds from accessing the 2.3.2. Cardboard bands fl canopies; the mesh size allowed large insects such as butter ies Fifteen days before the first sampling date, one half-corrugated and grasshoppers to enter the cages but not small birds such as cardboard band was wrapped around the tree trunks. The band warblers. We inspected the cages weekly to check for potential was 15 cm wide and had 4 mm-wide corrugations, which were put fi problems. Occasionally we would nd a bird inside a cage because in contact with the trunk. Cardboard bands are used as temporary of an accidental hole in the mesh, which we repaired right away. shelters by hunting spiders, and they can hide either among the The treatments were operative between February 2008 and corrugations or between the trunk and the band (Isaia et al., October 2009. 2006). At each sampling date, the bands were collected and replaced 2.3. Sampling methodology with new ones. Before removing a band, a plastic collar was placed around the tree trunk just below the band to intercept We randomly assigned 2 of the 3 trees in each plot to a sampling spiders that were escaping, which were then captured and pre- method: (1) visual searches in the canopies, and (2) cardboard served in 70% alcohol. The removed bands were put in plastic bands on the trunks. In this way, we prevented any potential bags with a piece of cotton damped with ethyl acetate to kill the interference between different sampling methods conducted in the remaining spiders.