Ant Versus Bird Exclusion Effects on the Arthropod Assemblage of an Organic Citrus Grove

Ecological Entomology (2010), 35, 367–376 DOI: 10.1111/j.1365-2311.2010.01190.x

Ant versus bird exclusion effects on the arthropod assemblage of an organic citrus grove

JOSEP PINOL,˜ 1,2 XAVIER ESPADALER,1,2 N URIA´ CANELLAS,˜ 3 JORDI MARTINEZ-VILALTA,´ 1,2 JOSE´ A. BARRIENTOS1 and DANIEL SOL2 1Department of Animal Biology, Plant Biology and Ecology, Universitat Autonoma` de Barcelona, Spain, 2Centre for Ecological Research and Forestry Applications (CREAF), Universitat Autonoma` de Barcelona, Barcelona, Spain and 3I. Rubio´ i Tudurí, Marques` de Comillas, 36, 08038 Barcelona, Spain

Abstract. 1. Predation-exclusion experiments have highlighted that top-down control is pervasive in terrestrial communities, but most of these experiments are simplistic in that they only excluded a single group of predators and the effect of removal was evaluated on a few species from the community. The main goal of our study was to experimentally establish the relative effects of ants and birds on the same arthropod assemblage of canopy trees. 2. We conducted 1-year long manipulative experiments in an organic citrus grove intended to quantify the independent effects of bird and ant predators on the abundance of arthropods. Birds were excluded with plastic nets whereas ants were excluded with sticky barriers on the trunks. The sticky barrier also excluded other ground dwelling insects, like the European earwig Forﬁcula auricularia L. 3. Both the exclusion of ants and birds affected the arthropod community of the citrus canopies, but the exclusion of ants was far more important than the exclusion of birds. Indeed, almost all groups of arthropods had higher abundance in ant-excluded than in control trees, whereas only dermapterans were more abundant in bird-excluded than in control trees. A more detailed analysis conducted on spiders also showed that the effect of ant exclusion was limited to a few families rather than being widespread over the entire diverse spectrum of spiders. 4. Our results suggest that the relative importance of vertebrate and invertebrate predators in regulating arthropod populations largely depends on the nature of the predator–prey system. Key words. Forﬁcula auricularia, Mediterranean, spiders, Theridiidae, Thomisidae, Xysticus.

Introduction do exclude multiple predators, studies excluding more than one predator group factorially on a shared prey assemblage to allow Since the pioneering work of Paine (1966), the experimental measuring the individual effects of each group are rather scarce exclusion of predators has been regarded as a major tool for (Pacala & Roughgarden, 1984; Spiller & Schoener, 1994; Halaj uncovering interactions among species in ecological commu- et al., 1997; Hooks et al., 2003; Philpott et al., 2004; Mooney, nities. Such exclusions have revealed that predators often exert 2007; Kalka et al., 2008; Williams-Guillen´ et al., 2008). Fol- top-down control on herbivores and that the effect sometimes lowing Philpott et al. (2004) and Mooney (2007), we argue that cascades down to primary producers in terrestrial ecosystems the simultaneous exclusion of several predators might provide (Marquis & Whelan, 1994; Pace et al., 1999; Schmitz et al., a more realistic view on the top-down processes that regu- 2000; Halaj & Wise, 2001). Whereas most predator exclusions late communities, providing in addition important clues about Correspondence: Josep Pinol,˜ CREAF, Facultat de BioCiencies,` the appropriateness of aggregating species into trophic groups Universitat Autonoma` de Barcelona, 08193 Bellaterra, Spain. E-mail: to describe food webs (Philpott et al., 2004) and, in a more [email protected] applied setting, informing us about which predators are worth

© 2010 The Authors Journal compilation © 2010 The Royal Entomological Society 367 368 Josep Piñol et al. manipulating to improve the control of agricultural and forest of ca 300 Clementine trees grafted on the hybrid rootstock insect pests. Carrizo citrange (Poncirus trifoliata (L.) Raf. × Citrus sinen- Two of the most important predator groups of terrestrial sis (L.) Osb.). The grove complies with all organic agriculture arthropod-dominated communities are ants and birds. Ant and standards, i.e. no pesticides, fungicides or herbicides were bird exclusion from communities has frequently been shown applied and only organic manure was used as fertiliser. Trees to increase herbivore abundance (Schmitz et al., 2000; Halaj were regularly watered during dry periods. & Wise, 2001; and references therein). The meta-analytical studies of Schmitz et al. (2000) and Halaj and Wise (2001) Bird- and ant-exclusion experiments also showed that predatory effects were of similar magnitude for vertebrate and invertebrate predators. However, a more Twenty-four trees from three rows of 23 trees each planted in controversial picture emerges when one focuses on the few 1999 were randomly chosen. Each of these trees was randomly studies that excluded ants and birds from the same community assigned to one of three groups: control trees (n = 8), to which and that studied their effect on the entire arthropod assemblage birds and crawling insects had free access; bird-excluded trees rather than on one or a few species (Philpott et al., 2004; (n = 8) that were covered with a net to prevent bird access to Mooney, 2007). While Philpott et al. (2004) found that birds their canopies (exclosures); and banded trees (n = 8) in which had stronger negative effects on arthropods than ants in a coffee a sticky barrier was applied to the trunk to prevent the access farm in Chiapas (Mexico), Mooney (2007) reported that the of crawling insects to the canopies. As we were interested effects of birds were consistently weaker than those of ants in in the main effects of ants and birds, we did not perform a a ponderosa pine stand in Colorado (U.S.A.). It is important to fourth treatment with both predators excluded; consequently remember that ants have a dual role in ecological communities, possible additive, competitive, and synergistic effects of ants as they are not only arthropod predators, but also hemipteran and birds were not explored (Haemig, 1994). The trunk-barrier mutualists (Styrsky & Eubanks, 2007). consisted of a polibutene-based sticky barrier (Rata Stop®) Here we present a comparative study of the relative effects applied on an alimentary plastic film tightly attached over of the exclusion of the ant and bird communities on a terrestrial a padding cylinder in contact with the trunk (Samways & arthropod assemblage. The ecological setting of this study, Tate, 1985). The trunk barrier was highly effective in keeping a Mediterranean organic citrus grove, is more similar to the ants away from the canopies but, occasionally, some were coffee plantation of Philpott et al. (2004) than to the natural still found in the experimental trees. Ants normally found forest of Mooney (2007). Like Philpott et al. (2004), we their way into the canopy via tall weeds or, more often, by expected that studying a system (an organic farm) that is less crossing the glue barrier using dead insects as stepping stones. diverse than a natural forest would facilitate the identification Trees were inspected on a weekly basis and, when a problem of functional relationships that are difficult to detect in natural was detected it was immediately solved by cutting the tall ecosystems. We studied all canopy arthropods present in the weeds or by adding more glue to the trunk barrier. Trees trees, but we paid particular attention to the effect of ant and had a trunk diameter of 8.4 ± 1.2 cm (mean ± SD) and bird exclusion on spiders. We selected spiders as a test group a crown diameter of ca 2.5 m. The net for bird exclusion because of their abundance in the community, and because (mesh 20 × 20 mm) was supported by a parallelepipedic they often increase their abundance following the removal metallic structure with a base of 3 × 3 m and 2 m height of both ants (Mody & Linsenmair, 2004; Mooney, 2007) that covered the whole tree. Mesh size allowed vespid wasps and birds (Gruner, 2004; Gunnarsson, 2008). As spiders are inside the exclosures, but probably prevented the access of intermediate predators, their consumption by ants and birds larger arthropods like butterflies. Treatments were established has to be considered in the context of intra-guild predation; in January 2006 and thereafter, trees were sampled on a in particular, if spider abundance was affected by ant or bird monthly basis. The exclosures were dismantled after the exclusion, the effect could cascade down to other arthropod November 2006 sampling. Thus, there is one pre-experiment groups in their diet. In addition, given the variety in size and sample (January), and 10 monthly samples from control and behaviour of spiders, the effect of ant and bird predation on experimental trees (February to November). them could be family-specific. We asked three main questions: (i) Do birds and/or ants affect arthropod assemblages in canopy trees? (ii) Do birds and ants differ in their relative effects on Arthropod sampling and classification arthropods? (iii) Is the effect of birds and ants different for Arthropods on the tree canopy were sampled once a month, different families and species of spiders? using beating trays, captured with entomological pooters and immediately preserved in 70% alcohol. The collection tray was 2 Material and methods a white square of 0.5 m , normally positioned ca 50 cm below the foliage. Arthropods were dislodged with three vigorous Study site hits in the tree crown; this was repeated twice at opposite sides of the tree on each sampling date. In the laboratory, The study site was a plantation of citrus trees located at all spiders (Araneae), beetles (Coleoptera), bugs (Hemiptera: ◦ La Selva del Camp (Tarragona, northeast Spain; 41 135N, Heteroptera), earwigs (Dermaptera), and ants (Hymenoptera: ◦ 1 97E). Climate is Mediterranean, with a rainy spring and Formicidae) were identified to species. Insects of other groups autumn and a dry winter and summer. The grove consisted were also counted and identified to family or order.

As coleopterans and heteropterans were determined to When the manovas showed a significant treatment effect, species level, it was possible to calculate the total number we proceeded with the analysis of the effect on the abundance of predatory and herbivorous species in each sample. Preda- of each individual arthropod group, spider family, and on tors were calculated as the sum of all Araneae, all Neuroptera, the diversity of spider species using a repeated-measures predatory Coleoptera (mainly Coccinellidae, but also a few anova design, with ‘month’ as a within-subjects factor and Staphylinidae, Cantharidae, Malachiidae, and Carabidae), and ‘treatment’ as between-subjects factor. Finally, we conducted predatory Heteroptera (Anthocoridae, Reduviidae, and some an additional set of repeated measures anovas comparing Miridae and Pentatomidae). Herbivores were calculated as the ant-excluded versus bird-excluded trees. Only 10 months sum of Hemiptera: Sternorrhyncha, herbivorous Coleoptera were considered (February to November), as the January (Apionidae, Elateridae, Curculionidae, and Chrysomelidae), sampling was conducted before the establishment of the herbivorous Hemiptera: Heteroptera (some Miridae, most Pen- treatments. When the interaction between treatment and tatomidae and Lygaeidae, Tingidae, Phyrrocoridae, and Alydi- time was statistically significant, we conducted Tukey HSD dae), Thysanoptera, Lepidoptera, Orthoptera, and the fly Cer- post hoc analyses to highlight periods when the difference atitis capitata (Wiedemann) (Diptera: Tephritidae). between treatments was statistically significant. Abundance were square-root transformed to achieve normality. Analyses were conducted with Statistica v.6 (StatSoft Inc., 2001). Bird censuses

Monthly censuses were conducted during the 2006 breeding Results season (April to July) to roughly estimate the abundance of insectivorous bird species at the studied grove and variation Bird and ant communities over time. Each census consisted of two 10-min point counts (Bibby et al., 2000) conducted on two consecutive days. The The abundance of insectivorous and omnivorous passer- first count was performed approximately 1 h before sunset, and ines in the study area remained relatively high over the study the second count was conducted 1 h after sunrise. Upon arrival period, although was lower during the last census, conducted we waited 10 min, and then all birds seen or heard from the in July (Table S1). In summary, a total of 13 insectivorous centre of the grove were recorded, indicating whether they had or omnivorous species were detected, five of them being been detected inside or outside the grove. For the purpose of known foliage gleaners. The most abundant species were the this study, birds were classified as insectivores if their diet Spotless Starling (Sturnus unicolor Temminck; Sturnidae) and consisted at least partially of insects during the nesting season two sparrows (Passer domesticus L. and Passer montanus (according to Cramp, 1988–1994). L.; Passeridae) which, together, included 74% of all detected individuals. These three species had important nesting populations in several large, farm-like buildings nearby the study Spider diversity grove; one of them being within less than 50 m. Other abundant bird species included Serinus serinus L., Carduelis car- The diversity of spiders was estimated in each sample (24 duelis L. (Fringillidae), Parus ater L. (Paridae) and Sylvia trees × 11 months = 264 samples) with the number of species melanocephala Gmelin (Sylviidae). S and as the Shannon diversity index H: Ten species of ants were found in the canopies of the trees sampledbybeatingtrays.Ofthese,Lasius grandis Forel (43% i=S of the individuals), Plagiolepis pygmaea (Latreille) (31%), H =− p · log p (1) i 2 i Formica rufibarbis Fabricius (16%), Tapinoma nigerrimum i=1 (Nylander) (5%), and Formica subrufa Roger (4%) were the where pi is the proportion of individuals of each species (up most abundant. All these species, except P . pygmaea,which to a total of S species) in a sample. is nectarivorous, are known aphid tenders. The remaining In some samples, not all specimens could be identified to less abundant species were Pheidole pallidula (Nylander), species, thus we proceeded conservatively when counting the Camponotus cruentatus (Latreille), C. sylvaticus (Olivier), C. number of species. By doing so, the reported values of S and aethiops (Latreille), and Tetramorium semilaeve Andre.´ H must be considered as a minimum value of spider diversity.

Effect of bird exclusion and ant exclusion on arthropod Analyses groups’ abundance

The ﬁrst step in the analysis was a manova of all arthropod The beating trays produced ca 13 000 arthropod individ- groups abundance with ‘treatment’ as between-subjects factor. uals, considering all 24 control and experimental trees and The response variables were the cumulative abundance of each 11 months of sampling. Of these, 30.8% were Psocoptera, group in each tree from February to November. Two different 16.1% Araneae, 13.0% non-Aphididae Hemiptera: Sternor- manovas were conducted, one to compare ant-excluded versus rhyncha, 10.6% Hymenoptera: Formicidae, 8.8% Coleoptera, control trees, and a second one to compare bird-excluded 6.2% Diptera, 6.2% Aphididae Hemiptera: Sternorrhyncha, versus control trees. 2.5% non-Formicidae Hymenoptera, 2.4% Dermaptera, 1.9%

Hemiptera: Heteroptera, 0.9% Neuroptera, and the rest were a the abundance of all arthropod groups (except Heteroptera and few Collembola, Thysanoptera, Lepidoptera, and Orthoptera. non Aphididae Hemiptera: Sternorrhyncha) differed between Before the start of the experiment (January), manovasdid treatments (Table S2). This result reinforces the main outcome not show any difference between treatment and control trees in of the experiment, i.e. that in this particular grove and year, the abundance of arthropods (Ant-excluded vs. control: Wilks the effect of ants was larger than the effect of birds on the = 0.43, F8,7 = 1.15, P = 0.43; Bird-excluded vs. control: abundance of canopy arthropods. Wilks = 0.55, F8,7 = 0.69, P = 0.69).

Spider community Effects on ants and other ground-dwelling arthropods. As planned, there were more ants in control trees than in banded Spiders belonged to 15 families. The most abundant trees (Fig. 1a; Table 1). Only on one occasion was there a ones were Theridiidae (31.4% of the captured individuals), noticeable number of ants in the canopies of the banded trees Philodromidae (16.6%), Araneidae (15.7%), Salticidae (8.5%), (Fig. 1a); the conspicuous peak of ants of July in banded Thomisidae (8.0%), and Linyphiidae (6.9%). In the statistical trees corresponded almost entirely to 75 individuals of the analyses of the next section, these six most abundant families P. pygmaea tiny sampled from a single tree. As the exclu- were considered separately, whereas the remaining nine less sion of this single sample from the statistical analyses did abundant families were pooled together. A complete list of not change appreciably any result, we kept the data from this the spiders of the community and their abundance is given as tree in the database. There were no differences in ant abun- supplementary material (Table S3). dance between bird-excluded and control trees (F = 0.73, 1,14 Before the start of the experiment (January), there were P = 0.41; Fig. 1a). no differences between treatment and control trees in the The sticky barrier was also effective against other crawling abundance of any of the families of spiders (Ant-excluded insects, such as the earwig Forficula auricularia L., the only vs. control: Wilks = 0.52, F = 1.04, P = 0.47; Bird- dermapteran in the community (Fig. 1b). Consequently, this 7,8 excluded vs. control: Wilks = 0.70, F = 0.49, P = 0.81) ant-exclusion experiment has to be interpreted as the exclusion 7,8 of ants and other ground-dwelling arthropods. However, to keep it short, we will use the term ant-exclusion throughout the paper. On the other hand, bird-excluded trees had a Effect of bird exclusion and ant exclusion on spiders significantly higher abundance of earwigs than control trees (F1,14 = 5.78, P = 0.03; Fig. 1b). Abundance of spiders was higher on ant-excluded compared to control trees mainly due to increases of Theridi- idae and Thomisidae (Table 2; Table S4). The increase in Effects on other arthropod groups. manova showed a signifi- Theridiidae abundance in ant-excluded compared to control cant overall effect of ant-exclusion on the abundance of other trees started in late summer and remained high during autumn arthropod groups (Wilks = 0.13, F9,6 = 4.14, P = 0.049; (Fig. 3a). In contrast, the higher abundance of Thomisidae ant and earwig abundance were not included as response vari- in ant-excluded trees occurred only in June (Fig. 3e), and ables as they were purposely excluded by the experimental it was due to a single genus, Xysticus.AstheXysticus treatment). On the contrary, the manova comparing bird- peak of June followed the aphid peak of May, we calcu- excluded versus control trees revealed no significant overall lated the correlation (log–log) between the abundance of effect of birds on the abundance of all other arthropod groups Xysticus sp. in June and the abundance of aphids in May (Wilks = 0.13, F11,4 = 2.53, P = 0.19). on a tree basis, and found it to be statistically significant The difference between ant-excluded and control trees (r = 0.53; n = 24; P = 0.008). The pool of the nine less was statistically significant for all individual groups except abundant families was also slightly more abundant in ant- Heteroptera and non Aphididae Hemiptera: Sternorrhyncha excluded than in control trees in the second half of the year (mainly scale insects, especially Ceroplastes sinensis Del (Fig. 3g; Table 2). It was mainly due, at its peak of August to Guercio) (Fig. 1c–k; Table 1). There were also more carni- September, to Miturgidae (Cheiracanthium sp.) and Clubion- vores in ant-excluded than in the control ones (P<0.001; idae (Clubiona genevensis L. Koch). One more spider family, Fig. 2; Table 1). Herbivores were also more abundant in ant- Philodromidae, had a significant treatment × time interaction excluded trees, but the difference was only marginally signifi- (Table 2). The post hoc analysis showed that the abundance of cant (P = 0.08; Fig. 2; Table 1). Philodromidae was higher in ant-excluded trees only in July All arthropod groups, except ants and earwigs, had a (Fig. 3b). significant interaction ant-exclusion × time (Table 1). Post hoc Ant exclusion significantly increased the diversity of the analyses of the interaction revealed that ant exclusion did not spider assemblage, measured both as the number of species have a significant effect on any group until May. Later on there S (P<0.001 Fig. 4a; Table 2) or as the Shannon diversity were significant effects on some groups every month except in index H (P = 0.007 Fig. 4b; Table 2). On the contrary, neither August (Fig. 1). S nor H was affected by the exclusion of birds (Fig. 4; A second set of repeated measures anova comparing the F1,14 = 0.48, P = 0.50 for S and F1,14 = 0.13, P = 0.72 treatments of ant exclusion versus bird exclusion showed that for H).

25 8 A - For Control B - Der 20 Banded Exclosure 6 15 4 10

2 5 individuals persample

0 0 70 50 *** 60 C - Pso D - Ste *** 40 50 *** 40 30

30 ** 20 20 10 10 individuals per sample

0 0 25 25 F - Col *** E - Ara * 20 20 ** ** * 15 * 15 ** 10 10 *

5 5 individuals per sample

0 0 15 G - Dip 75 H - Aph ***

10 50 **

5 25 individuals perindividuals sample

0 0 2 I - Hym J - Neu 15 *** Fig. 1. Temporal variation of arthropod abundance in ant-excluded (banded), bird-excluded 10 1 (exclosures) and in control trees from January to November 2006. Each value corresponds to the ± 5 mean ( SE) value of individuals per beat tray sample in each of the eight trees of each treat- individuals per sample ment. When the interaction treatment × time of 0 0 1234567891011 an arthropod group was signiﬁcant (Table 1) it 5 Month is also shown in which months the abundance K - Het was signiﬁcantly different between control and 4 ant-excluded trees according to a Tukey HSD

3 post hoc comparison. Signiﬁcance: ***P < 0.001; **P < 0.01; *P < 0.05. Codes: For, 2 Hymenoptera: Formicidae; Der, Dermaptera; Pso, Psocoptera; Ste, non-Aphididae Stenor- 1 rhyncha; Ara, Araneae; Col, Coleoptera; Dip, individuals per sample per individuals Diptera; Aph, Hemiptera: Stenorrhyncha: Aphi- 0 1234567891011 didae; Hym, non-Formicidae Hymenoptera; Month Neu, Neuroptera; Het, Hemiptera: Heteroptera.

Table 1. Summary of a repeated measures anova of arthropod 35 abundance between control and ant-excluded trees from February to A - Carnivores *** ** November. 30 * *** × 25 Control * Treatment Time Treatment time Banded 20 Group F1,14 PF9,126 PF9,126 P Exclosure For 74.13 <0.001 4.08 <0.001 1.92 0.06 15 Der 85.58 <0.001 2.59 0.02 1.94 0.07 10 Pso 25.49 <0.001 13.91 <0.001 4.33 <0.001 5

Ste 0.32 0.58 12.45 <0.001 3.87 <0.001 persample individuals Ara 30.15 <0.001 17.81 <0.001 3.70 <0.001 0 Col 17.12 0.001 15.68 <0.001 7.33 <0.001 Dip 14.04 0.002 19.27 <0.001 2.35 0.02 80 Aph 6.11 0.03 29.43 <0.001 3.73 <0.001 * B - Herbivores Hym 13.71 0.002 6.09 <0.001 5.11 <0.001 70 Neu 15.35 0.002 2.91 0.004 2.54 0.01 60 Het 2.22 0.15 4.59 <0.001 2.13 0.031 Car 21.85 <0.001 28.20 <0.001 7.65 <0.001 50 Her 3.47 0.08 14.07 <0.001 2.31 0.02 40

Codes for arthropod groups: For, Hymenoptera: Formicidae; Der, 30 Dermaptera; Pso, Psocoptera; Ste, non Aphididae Stenorrhyncha; 20 Ara, Araneae; Col, Coleoptera; Dip, Diptera; Aph, Stenorrhyncha: individuals per sample 10 Aphididae; Hym, non-Formicidae Hymenoptera; Neu, Neuroptera; Het, Heteroptera; Car, all carnivores; Her, all herbivores. 0 1234567891011 Month

Discussion Fig. 2. Temporal variation of carnivore (a) and herbivore (b) abundance in ant-excluded (banded), bird-excluded (exclo- The reported experiments showed that both the exclusion of sures) and in control trees from January to November 2006. Each ants and birds affected the arthropod community of the stud- value corresponds to the mean (±SE) value of individuals per beat ied citrus canopies and that the exclusion of ants was far tray sample in each of the eight trees of each treatment. When the more important than the exclusion of birds. Indeed, almost interaction treatment × time was significant (Table 1) it is also shown all groups of arthropods had higher abundance in ant-excluded in which months the abundance was significantly different between than in control trees, whereas only dermapterans were signif- control and ant-excluded trees according to a Tukey HSD post hoc icantly more abundant in bird-excluded than in control trees. comparison. Significance: ***P < 0.001; **P < 0.01; *P < 0.05. Our results are thus similar to those of Mooney (2007) who also reported that the effects of birds were consistently weaker Table 2. Summary of a repeated measures anova of the abundance of spider families and of spiders’ diversity (both measured as the than those of ants on the arthropod community of Pinus pon- number of species S and as the Shannon diversity index H ). derosa trees of the Rocky Mountains and contrast with those of Philpott et al. (2004) who found a stronger effect of birds Treatment Time Treatment × time than ants in the canopies of a coffee plantation. Tanhuanpaeae F PFPFP et al. (2001) also reported a more important effect of birds Group 1,14 9,126 9,126 than ants, but in their study the focus was on the abundance of The 23.67 <0.001 13.14 <0.001 3.27 0.001 a single caterpillar species rather than on the entire arthropod Phi 3.86 0.07 3.74 <0.001 2.02 0.04 assemblage. Ara 2.75 0.12 6.37 <0.001 1.22 0.29 The reasons why ants and birds vary in the top-down control Sal 1.57 0.23 8.89 <0.001 0.96 0.47 they exert on arthropod communities remain obscure, but they Tho 18.15 <0.001 6.80 <0.001 3.40 <0.001 Lin 0.31 0.59 6.10 <0.001 0.74 0.63 may be related to the species richness of insectivorous birds in Oth 8.65 0.01 3.73 <0.001 0.99 0.44 a given community. A recent meta-analysis of bird predation S 19.12 <0.001 15.02 <0.001 2.98 0.003 on arthropods in tropical agroecosystems (Philpott et al., 2009) H 9.90 0.007 9.71 <0.001 0.96 0.48 showed that no functional attribute of the bird community pre- dicted arthropod removal better than species richness. They Between groups factor: treatment (control vs. ant-excluded); within provide an empirical equation relating arthropod reduction and groups: time (February to November). Codes for spider families: The, number of species of insectivorous birds (Fig. 2 of Philpott Theridiidae; Phi, Philodromidae; Ara, Araneidae; Sal, Salticidae; Tho, Thomisidae; Lin, Linyphiidae; Oth, all other minor families added up. et al., 2009). Using the insectivorous species richness of our community (13; Table S1) in the equation predicts a 0.6% of arthropod reduction by birds. Such a small value would not In the studied community ants play a dual role, as they be detectable experimentally, which is in agreement with our act as hemipteran mutualists and as generalist predators. The results. increased abundance of Coleoptera (mostly the predaceous

12 6

A - Theridiidae ** B - Philodromidae ** 10 ** 5 Control 8 Banded 4 6 Exclosure * 3

4 2

2 1 individuals perindividuals sample

0 0 5 3 C - Araneidae D - Salticidae 4 2 3

2 1 1 individuals per sample

0 0 7 4

6 E - Thomisidae *** F - Linyphidae 3 5

4 2 3

2 1 1 individuals perindividuals sample

0 0 1234567891011 4 Month G - Other families 3

1 individuals per sample

0 1234567891011 Month

Fig. 3. Temporal variation of the spider’s abundance in ant-excluded (banded trees), bird-excluded (exclosures), and in control trees from January to November 2006. The six most abundant families are considered individually (a–f) and the remaining nine families are pooled together (g). Each value corresponds to the mean (±SE) value of spiders per beat tray sample in each of the eight trees of each treatment. When the interaction treatment × time of a spider family was significant (Table 2) it is also shown in which months the abundance was significantly different between control and ant-excluded trees according to a Tukey HSD post hoc comparison. Significance: ***P < 0.001; **P < 0.01; *P < 0.05.

12 Earwigs were the only group of arthropods that changed their A - Number of species *** abundance following bird exclusion. Gunnarsson et al. (2009) 10 also reported a very important increase of earwig abundance Control in a bird-exclusion experiment in Sweden. This would suggest 8 Banded that earwigs are an important prey of insectivorous birds

S 6 Exclosure in the study site, consistent with what is known about the diet of these bird species (Table S1). This result was not 4 surprising also, because the earwig Forficula auricularia is the largest common arthropod species in the canopies of the 2 grove, making them a valuable prey item for insectivorous 0 birds. Maybe one important reason for not detecting significant effects of birds on the abundance of more arthropod groups in 4 this study is that most of them are in general rather small and, B - Shannon diversity probably, not really attractive prey for gleaning birds. 3 The effect of bird predation on earwigs, combined with their possible role in aphid control, points to earwigs as an important species in the studied grove community. Earwigs have also H 2 proved to be able to control populations of aphids in apple orchards of temperate areas in Europe (Solomon et al., 2000), 1 the U.S.A. (Carroll & Hoyt, 1984), Australia (Nicholas et al., 2005), and New Zealand (Suckling et al., 2006). Since less environmentally aggressive agricultural practices that favour 0 1234567891011 earwig lifestyle, such as integrated pest management and Month organic agriculture, are currently expanding, their role as generalist predators in the control of agricultural pests could Fig. 4. Temporal variation of the diversity of spiders measured as become more important in the near future (Pinol˜ et al., 2009b). the number of species (a) or Shannon’s diversity index (b) in ant- The negative effect of ants on spiders has already been excluded (banded), bird-excluded (exclosures) and in control trees documented in previous studies (Buckley, 1990; Heikkinen, from January to November 2006. Each value corresponds to the 1999; James et al., 1999; Sanders & Platner, 2007; but see Vogt mean (±SE) value of individuals sampled in each of the eight et al., 2002). Nevertheless, the possibility that this effect varies trees of each treatment. When the interaction treatment × time was significant (Table 2) it is also shown in which months the diversity according to spider identity has been more rarely reported was significantly different between control and ant-excluded trees (but see Halaj et al., 1997). Our results showed that the according to a Tukey HSD post hoc comparison. Significance: ***P < negative effect of ants on spiders was not present in all 0.001; **P < 0.01; *P < 0.05. spider groups, but it manifested only in a subset of families, especially in Thomisidae and Theridiidae. It is worth noticing Coccinellidae), Araneae, Neuroptera, and non-Formicidae that Thomisidae are cursory and Theridiidade are web-spinning Hymenoptera (mostly Chalcidoidea parasitoids) would fit with spiders, so the effect of ants is not limited to a single functional the notion that ants exert physical interference on aphid group of spiders. The case of Thomisidae is especially striking and coccid enemies (Bartlett, 1961; Way, 1963; Bishop & because ants affected one single species, Xysticus sp. Recently, Bristow, 2001; Kaneko, 2003). The increased abundance of Birkhofer et al. (2008) clearly showed using molecular markers other herbivores or detritivorous insects like Psocoptera and that Xysticus cristatus (Clerck) feed on aphids and this could Diptera and, in general, of all arthropod groups is consistent explain the peak of Thomisidae in June (Fig. 3) following the with the generalist predatory role of ants. peak of aphids in May (Fig. 1). The negative effect of ants on The higher abundance of aphids in ant-excluded than in spider diversity complies with the classical view that predator control trees is more difficult to explain for three reasons: exclusion reduces prey diversity (Paine, 1966). Unexpectedly, (i) the most abundant ant in the canopies was Lasius gran- and in contrast with many results reporting a marked negative dis, an aphid-tending specialist (Paris & Espadaler, 2009); (ii) effect of birds on spiders (Greenberg et al., 2000; Philpott all aphid species (the most abundant ones were Aphis spi- et al., 2004; Recher & Majer, 2006; Gunnarsson, 2008), we raecola Patch and A. gossypii Glover) found in the grove could not detect any significant effect of bird exclusion on are ant tended (Suay-Cano et al., 2002); and (iii) carnivores as spider abundance or assemblages through the year. a whole and several groups of arthropods that contain impor- In conclusion, in the studied citrus grove, both birds and tant aphid predators were also more abundant in ant-excluded ants affected the composition and abundance of the arthropod trees. The most likely explanation for this phenomenon is the community of the tree canopies. However, the effect of bird concurrent exclusion of earwigs with ants. Earwigs are known exclusion was weaker than that of ant exclusion. The exclusion to predate on aphids (Solomon et al., 2000) and in this partic- of ants, and other ground-dwelling arthropods like earwigs, had ular site the negative effect of earwigs on aphid populations a widespread effect on most groups of arthropods, whereas the seems to be stronger that the positive effect of aphid-tending exclusion of birds only increased the abundance of earwigs. ants (Pinol˜ et al., 2009a). Like in previous studies of ant and bird exclusion on the same

© 2010 The Authors Journal compilation © 2010 The Royal Entomological Society, Ecological Entomology, 35, 367–376 Ant and bird exclusion effects on arthropods 375 prey assemblage (Philpott et al., 2004; Mooney, 2007), ants This work has been supported by grants from MCYT- and birds differed in their effects both qualitatively and quanti- FEDER (CGL2004-05240-C02-01/BOS and CGL2007-64080- tatively; thus, aggregating bird and ant species into one trophic C02-01/BOS). group would not be warranted, despite the overlapping of their diets. The more detailed analysis that we conducted on spi- References der families also showed that the effect of ant exclusion was limited to a few families rather than being widespread over Bartlett, B.R. (1961) The influence of ants upon parasites, predators, the entire diversity spectrum of spiders, hindering again the and scale insects. Annals of the Entomological Society of America, possibility of including all spiders into one trophic group. 54, 543–551. 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Complete list of all spiders collected using beating Greenberg, R., Bichier, P., Cruz, A., MacVean, C., Perez, R. & trays in 11 samplings dates from January to November 2006 Cano, E. (2000) The impact of avian insectivory on arthropods and and from 24 citrus trees (8 control, 8 ant-excluded, 8 bird- leaf damage in some Guatemalan coffee plantations. Ecology, 81, excluded). A total of 2051 specimens were analysed, of which 1750–1755. only 158 (7.7%) were adults (105 females and 53 males). Gruner, D.S. (2004) Attenuation of top-down and bottom-up forces in As most of the specimens were juveniles their determination a complex terrestrial community. Ecology, 85, 3010–3022. was difficult and, in many cases, it was not possible to Gunnarsson, B. (2008) Bird predation on spiders: ecological mecha- nisms and evolutionary consequences. Journal of Arachnology, 35, go beyond the genera level (Anyphaena, Cyclosa, Lathys, 509–529. 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Between groups factor: treatment (ant- 313–322. excluded vs. bird-excluded); within groups: time (February to Heikkinen, M. (1999) Negative effects of the western thatching ant November). Codes for spider families as in Table 2. (Formica obscuripes) on spiders (Araneae) inhabiting big sagebrush Please note: Neither the Editors nor Wiley-Blackwell (Artemisia tridentata). Great Basin Naturalist, 59, 380–383. are responsible for the content or functionality of any Hooks, C.R.R., Pandey, R.R. & Johnson, M.W. (2003) Impact of supplementary material supplied by the authors. Any queries avian and arthropod predation on lepidopteran caterpillar densities and plant productivity in an ephemeral agroecosystem. Ecological (other than missing material) should be directed to the Entomology, 28, 522–532. corresponding author for the article. James, D.G., Stevens, M.M. & Faulder, R.J. (1999) Ant foraging reduces the abundance of beneficial and incidental arthropods in citrus canopies. 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2 Table S1. Average number of individuals detected in the monthly bird censuses (point

3 counts) inside the grove (or flying over it) and outside the grove. Only species

4 considered as insectivorous are reported (see text). An asterisk (*) indicates that the

5 species feeds on earwigs, and a (#) symbol indicates that the species can feed on canopy

6 insects (in both cases the information is taken from Cramp et al., 1988-1994).

April May June July

Species Common In Out In Out In Out In Out name Galerida cristata (L.) Crested Lark 1 Luscinia megarhynchos Nightingale 1 C.L. Brehm Turdus viscivorus L. (*, #) Mistle 0.5 Thrush Sylvia melanocephala Sardinian 0.5 1 (Gmelin) (*, #) Warble Lanius senator L. (*) Woodchat 0.5 Shrike Parus ater L. (*, #) Coal tit 0.5 Pica pica (L.) (*, #) Magpie 1.5 Sturnus unicolor Spotless 9 17.5 0.5 11.5 37.5 2.5 Temminck (*, #) Starling Passer domesticus (L.) (*) House 3 4.5 4.5 10 2.5 5.5 4.5 5.5 Sparrow Passer montanus (L.) (*) Tree 1 1.5 0.5 4 1.5 3 0.5 1.5 Sparrow Serinus serinus (L.) (*) Serin 5 4 1.52.5 3.5 4 1 2 Carduelis chloris (L.) Greenfinch 1 Carduelis carduelis (L.) Goldfinch 3 2 0.5 1 3 1.5 2.5 1.5 8

1 9 Table S2. Summary of a repeated measures ANOVA of arthropod abundance between

10 ant-excluded and bird-excluded trees from February to November. Codes for arthropod

11 groups as in Table 1.

Group treatment time treatment x time

F1,14 P F9,126 P F9,126 P

For 36.46 < 0.001 5.43 < 0.001 2.13 0.03

Der 55.14 < 0.001 4.13 < 0.001 4.06 < 0.001

Pso 19.50 < 0.001 15.81 < 0.001 3.33 0.001

Ste 0.14 0.71 21.42 < 0.001 3.16 0.002

Ara 6.40 0.02 27.15 < 0.001 1.79 0.08

Col 7.25 0.02 20.21 < 0.001 4.17 < 0.001

Dip 19.18 < 0.001 16.48 < 0.001 3.00 0.003

Aph 16.30 0.001 33.37 < 0.001 13.77 < 0.001

Hym 8.65 0.01 6.86 < 0.001 4.00 < 0.001

Neu 11.92 0.003 2.34 0.02 1.50 0.15

Het 3.56 0.08 3.66 < 0.001 1.70 0.09

Car 7.06 0.02 36.89 < 0.001 2.96 0.003

Her 5.55 0.03 15.39 < 0.001 6.41 < 0.001

2 16 Table S3. Complete list of all spiders collected using beating trays in 11 samplings

17 dates from January to November 2006 and from 24 citrus trees (8 control, 8 ant-

18 excluded, 8 bird-excluded). A total of 2051 specimens were analyzed, of which only

19 158 (7.7%) were adults (105 females and 53 males). As most of the specimens were

20 juveniles their determination was difficult and, in many cases, it was not possible to go

21 beyond the genera level (Anyphaena, Cyclosa, Lathys, Zelotes, Cheiracanthium,

22 Oxyopes, Philodromus, Salticus, Heliophanus, Anelosimus, Archaearanea, Dipoena,

23 Xysticus, Ozyptila) and in a few cases beyond the family level (10 Araneidae, 1

24 Gnaphosidae, 81 Linyphiidae, 5 Salticidae and 6 Theridiidae)

26 Family Species # individuals 27 ANYPHAENIDAE Anyphaena sp. 3 28 ARANEIDAE Agalenatea redii (Scopoli, 1763) 98 29 Araneus angulatus Clerck, 1757 164 30 Araniella cucurbitina (Clerck, 1757) 10 31 Cyclosa sp. 1 32 Cyrtophora citricola (Forsköel, 1775) 38 33 Mangora acalypha (Walckenaer, 1802) 1 34 indet 10 35 CLUBIONIDAE Clubiona genevensis L.Koch, 1866 108 36 DICTYNIDAE Lathys sp. 1 37 Marilynia bicolor (Simon, 1870) 1 38 Nigma puella (Simon, 1870) 40 39 GNAPHOSIDAE Aphantaulax seminigra Simon, 1878 17 40 Zelotes sp. 3 41 indet 1 42 LINYPHIIDAE Ceratinopsis romana (O.P.Cambridge, 1872) 54 43 Erigone dentipalpis (Wider, 1834) 1 44 Meioneta rurestris (C.L.Koch, 1836) 5 45 Tenuiphantes tenuis (Blackwall, 1852) 1 46 indet 81 47 MIMETIDAE Ero furcata (Villers, 1789) 6 48 MITURGIDAE Cheiracanthium mildei L.Koch, 1864 3 49 Cheiracanthium montanum L.Koch, 1877 2 50 Cheiracanthium sp. 53 51 OXYOPIDAE Oxyopes sp. 10

3 52 53 PHILODROMIDAE Philodromus cespitum (Walckenaer, 1802) 7 54 Philodromus rufus Walckenaer, 1826 1 55 Philodromus sp. 331 56 Thanatus vulgaris Simon, 1870 2 57 SALTICIDAE Ballus chalybeius (Walckenaer, 1802) 16 58 Chalcoscirtus infimus (Simon, 1868) 3 59 Evarcha jucunda (Lucas, 1846) 7 60 Heliophanus sp. 3 61 Icius hamatus (C.L.Koch, 1846) 97 62 Macaroeris nidicicolens (Walckenaer, 1802) 38 63 Salticus sp. 5 64 indet 5 65 SPARASSIDAE Olios argelasius (Walckenaer, 1805) 15 66 67 THERIDIIDAE Anelosimus aulicus (C.L.Koch, 1838) 5 68 Anelosimus sp. 153 69 Anelosimus vittatus (C.L.Koch, 1836) 4 70 Archaearanea sp. 9 71 Dipoena melanogaster (C.L.Koch, 1837) 88 72 Dipoena sp. 3 73 Keijia tincta (Walckenaer, 1802) 47 74 Neottiura curvimana (Simon, 1914) 5 75 Simitidion simile (C.L.Koch, 1836) 6 76 Steatoda nobilis (Thorell, 1875) 1 77 Theridion impresum (L.Koch, 1881) 1 78 Theridion mystaceum L.Koch, 1870 302 79 Theridion sisyphium (Clerck, 1757) 12 80 Theridion varians Hahn, 1833 1 81 indet 6 82 THOMISIDAE Diaea dorsata (Fabricius, 1777) 39 83 Ozytpila sp. 2 84 Runcinia grammica (C.L.Koch, 1837) 24 85 Synema globosum (Fabricius, 1775) 14 86 Thomisus onustus Walckenaer, 1805 1 87 Tmarus staintoni (O.P.Cambridge, 1873) 7 88 Xysticus sp. 78 89 ULOBORIDAE Uloborus walckenaerius Latreille, 1806 1 90

4 91 Table S4. Summary of a repeated measures ANOVA of the abundance of spider

92 families and of spiders’ diversity (both measured as the number of species S and as the

93 Shannon diversity index H). Between groups factor: treatment (ant-excluded vs. bird-

94 excluded); within groups: time (February to November). Codes for spider families as in

95 Table 2.

Group treatment time treatment x time

F1,14 P F9,126 P F9,126 P

The 3.76 0.07 21.56 < 0.001 1.18 0.30

Phi 0.64 0.43 6.17 < 0.001 1.21 0.29

Ara 0.67 0.42 8.60 < 0.001 1.19 0.30

Sal 3.58 0.08 6.86 < 0.001 1.08 0.38

Tho 12.02 0.004 8.85 < 0.001 3.54 < 0.001

Lin 2.19 0.16 8.04 < 0.001 1.97 0.08

Oth 4.67 0.05 6.46 < 0.001 0.62 0.77

S 11.20 0.005 24.91 < 0.001 1.87 0.06

H 11.00 0.005 19.36 < 0.001 0.94 0.48