Elevational changes in the composition of insects and other terrestrial

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Feb 2, 2009 - JENNIFER GUEVARA and LETICIA AVILÉS Department of Zoology, ... more representative range of insect types from its environment. ... areas, however, is essential to understanding whether and to ... 2200 m, Napo Province) and a privately owned ranch near .... Nocturnal flying insects (i.e. nocturnal.
Insect Conservation and Diversity (2009) 2, 142–152

doi: 10.1111/j.1752-4598.2008.00043.x

Elevational changes in the composition of insects and other terrestrial arthropods at tropical latitudes: a comparison of multiple sampling methods and social spider diets Blackwell Publishing Ltd

J E N N I F E R G U E VA R A and L E T I C I A AV I L É S

Department of Zoology, University of British Columbia, Biological Science Building, 6270 University Boulevard, Vancouver, BC, Canada

Abstract. 1. We explored the extent to which differences between elevations in arthropod composition – insects and arachnids – are reflected by different sampling methods and in the diet of local social and subsocial spiders. 2. We surveyed two low-elevation tropical rainforest and two upper montane cloud forest sites in eastern Ecuador using blacklighting, sweeping, malaise traps, beating, and visual search. We also observed the prey captured by social (lowland rainforest) and subsocial (upper montane cloud forest) spider colonies in each habitat and related their diets to the insect composition yielded by the individual and combined set of techniques. 3. The most notable differences between high- and low-elevation sites in eastern Ecuador were an increase in the relative abundance of Hymenoptera, in particular ants, and a concomitant reduction in the representation of homopterans, dipterans and coleopterans at lower elevations. Differences between elevations, however, were only detected by three of the techniques employed (beating, sweeping and blacklighting). 4. The proportions of major taxa categories in the spider diets were only significantly different from samples from their respective environments for the upper elevation subsocial spider against blacklighting and the combined set of all techniques, excluding blacklighting. Nonetheless, only sweeping had similarity indices greater than 75% for both species, with beating and malaise being the next most similar. The more advanced level of sociality and larger nests of the social species may facilitate exploitation of a more representative range of insect types from its environment. Key words. Altitudinal gradients, Anelosimus, arthropod community, Ecuador, insect diversity, sampling methods, social behaviour, spiders.

Introduction While the vast majority of studies of tropical arthropod communities along elevational gradients have focused on discerning patterns of species richness (review in McCoy, 1990; Hodkinson, 2005) or explored diversity changes within single arthropod taxa (e.g., Turner & Broadhead, 1974; Hebert, 1980; Samson et al., 1997; Bruhl et al., 1999; Brehm & Fiedler, 2003; Brehm et al., 2007), only a handful have reported the relative Correspondence: Jennifer Guevara, Department of Zoology, University of British Columbia, Biological Science Building, 6270 University Boulevard, Vancouver, BC, Canada V6T 1Z4. E-mail: [email protected]

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abundances of different arthropod groups (Janzen, 1973; Janzen et al., 1976; Wolda, 1987; Olson, 1994). Knowledge of how the relative abundances of insects and other arthropods vary across areas, however, is essential to understanding whether and to what extent trophic interactions change along altitudinal and other environmental gradients (e.g., Turner & Broadhead, 1974; Olmstead & Wood, 1990; Andrew et al., 2003; Hodkinson, 2005). A few studies (reviewed in Hodkinson, 2005), for instance, indicate that predation and parasitism decline with elevation, an outcome that may result from a greater representation at lower elevations of arthropod groups more likely to be predatorial (e.g., ants, Bruhl et al., 1999; Punttila et al., 2004) or parasitic (e.g., parasitic wasps, Brenner et al., 2002; Saaksjarvi et al., 2004). Similarly, spatial changes in the © 2009 The Authors Journal compilation © 2009 The Royal Entomological Society

Arthropod sampling techniques and spider diets abundance of different arthropod groups may have a significant effect on the spatial distribution of those species that predate on them (Olmstead & Wood, 1990; Dejong & Ahlen, 1991; Kato et al., 2003; Kusch et al., 2004). Social spiders of the genus Anelosimus (Theridiidae) exhibit a distinct geographical distribution that appears to be partly related to insect size distribution patterns (Avilés et al., 2007; Guevara & Avilés, 2007; Powers & Avilés 2007). In the New World, in particular, social Anelosimus species appear to be concentrated at low to mid-elevation moist forests, whereas related subsocial species are absent from the lowland rainforest but are common at higher elevations and latitudes (Agnarsson, 2006; Avilés et al., 2007). We have suggested that this pattern may be related to the considerably larger sizes that characterise insects in lowland rainforests relative to higher elevations (Avilés et al., 2007; Guevara & Avilés, 2007; Powers & Avilés, 2007) and latitudes (Powers & Avilés, 2007). We have not explored, however, whether differences in the taxonomic composition of potential prey at different elevations may also contribute to the observed distribution patterns of spider sociality in the Neotropics or whether spiders of different levels of sociality differ in their ability to capture different types of prey. Using a variety of sampling methods, this study attempted to determine whether the frequencies of different insect and other arthropod groups caught with these techniques differ across elevations in Ecuador, and the extent to which the various sampling techniques reflect these differences. A second goal was to determine the extent to which the diets of social and subsocial spiders present at the upper and lower elevation habitats surveyed differ from each other and from the samples obtained with the different collecting methods.

Materials and methods Study sites We surveyed two lowland tropical rainforest sites – the Estación Biológica Jatun Sacha (1°42′N, 77°36′W; elevation: 385–410 m, Napo Province) and the Reserva Faunísta Cuyabeno (0°1′N, 76°19′W; elevation: 200 –300 m, Sucumbíos Province) – and two upper montane cloud forest sites – the Yanayacu Biological Station near Cosanga (0°36′N, 77°52′W; elevation: 2200 m, Napo Province) and a privately owned ranch near Baeza (0°34′N, 77°46′N; elevation: 2100 m, Napo Province), all located in eastern Ecuador. Surveys were conducted in two separate years, which included at least one lowland and one upper elevation site each year (Jatun Sacha, Cuyabeno, and Yanayacu in May–August 2005 and Jatun Sacha and Baeza in July 2006. A detailed description of the four sites is provided in Guevara and Avilés (2007).

Species description Anelosimus baeza. Agnarsson 2006 is a subsocial species that occurs from Panama to Peru at elevations between 200 m and 2500 m (Agnarsson, 2006). In eastern Ecuador, however, the

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species is rarely found below ~500 m (Avilés et al., 2007). We studied A. baeza at both of our high-elevation cloud forest sites where it is relatively common. As in other subsocial spiders (Buskirk, 1982), A. baeza individuals disperse from the natal nest as subadults to mate and establish individual webs (Agnarsson, 2006). Before dispersal, A. baeza nests in the Yanayacu area contain up to a few dozen individuals (median = 65, range 8– 197, N = 26; L. Avilés and J. Purcell, unpubl.). These colonies most often consist of the offspring of a single female, although occasionally nests may contain more than one female and their offspring (L. Avilés, unpubl.). During their social phase, nest mates cooperate in the capture of prey as well as in the maintenance of the nest and prey capture snare (Avilés, 1997). At the Yanayacu site, colonies were most abundant in naturally open and swampy areas and along road edges. At the Baeza site, colonies were also most common in relatively open habitats and pastures. We studied this species just before dispersal when most colonies consisted mainly of late juveniles and subadults, or subadults and young adults. Some of the colonies, however, contained recently dispersed solitary females, thus allowing us to cover most of the range of colony sizes of this species. The A. baeza colonies in our study ranged in size from 13 to 56 cm in length (longest axis). Anelosimus eximius. Keyserling 1884 is a lowland rainforest species found from Panama to southern Brazil (Levi, 1963; Avilés et al., 2001; Agnarsson, 2006). Unlike its subsocial counterparts, A. eximius individuals do not disperse from the natal nest except at very large colony sizes, thus forming, after several generations of internal mating and reproduction, relatively large colonies (Avilés, 1997). Anelosimus eximius nests thus range in size from a single female plus her offspring to tens of thousands of spiders (Avilés, 1997; Avilés et al., 2001). In this species, cooperation among colony members lasts through adulthood and involves, in addition to the cooperative behaviours displayed by A. baeza, cooperative care of the brood (Avilés, 1997). We studied this species at the two low-elevation sites where nests are typically found in the forest interior and along forest and river edges (pers. obs). In this study, we only observed nests inside the forest, where they tend to be small to medium sized (Purcell & Avilés, 2007). The colonies we studied ranged in size from 4 to 133 cm in length (longest axis).

Prey capture by spider colonies As in most species in the genus, A. eximius and A. baeza build dense tri-dimensional communal webs with superior prey capture lines for the interception of insect prey that is later subdued by the spiders (Brach, 1975; Nentwig, 1985; Avilés, 1997; Agnarsson, 2006; Yip et al., 2008). In both years, we conducted an intense search along existing trails and other accessible areas at each site in order to locate as many nests as possible. We sampled a total of 34 A. eximius (Jatun Sacha 31, Cuyabeno 3) and 27 A. baeza colonies (Yanayacu 18, Baeza 9) between 2005 and 2006, excluding only colonies that were too difficult to observe (> ~2 m above-ground). Each spider nest was visited every 1–1.5 h between 07:30 hours and 18:30 hours. During each survey, we recorded all new prey caught in the web or being consumed by

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the spiders. We note that even though our early morning samples may have included some insects caught by the spiders at night, our samples reflect primarily the diurnal diets of the spiders as, due to logistic reasons, our observations were conducted during the day only.

at night near the field stations. Except for visual searches, all insects and arachnids collected by the different techniques were taken to the laboratory and sorted carefully with the naked eye to order, and, for Hymenoptera, to two subgroups – ants and other Hymenoptera.

Sampling methods

Data analysis

Our sampling focused on flying and vegetation-dwelling specimens 1 mm in length or longer since our goal was to survey insects and other arthropods that could potentially form part of the spider diets. Sampling was carried out at each site concurrently with surveys of prey being captured by colonies of the local social (lowland tropical rainforest) or subsocial (upper montane cloud forest) spider (see below). We employed five collecting techniques: no-kill malaise traps, sweep nets, beating sheets, visual searching, and light traps (Table 1), except in Baeza where only three techniques were used due to logistic reasons (no-kill malaise traps, sweep nets, and visual search). Five no-kill malaise traps (height = 1.2 m, base = 1.2 m) made of fine-mesh white tulle were set up in different areas at approximately 5–10 m away from existing spider colonies and at a minimum distance of 10 m from one another. We checked the traps daily every 3 h for insects and other arthropods caught in the preceding period. Specimens caught were removed each time ensuring that the traps were empty for the next observation period. Daily sampling ranged from 3 to 9 h (1–3 observation periods) between 07:30 hours and 18:30 hours. Sweeping, beating, and visual searching were carried out from one to six times a day – weather permitting – (mode twice a day) between 07:30 hours and 6:30 hours at each site. Sweeping was performed on shrubs and other ground vegetation for 3 min at a time with an entomological heavy duty sweep net (diameter = 38.1 cm). Beating was carried out using a canvas beating sheet (a 0.71 m per side square or 0.5 m2). Shrubs and other ground vegetation were shaken vigorously each time for 3 min. All specimens knocked onto the fabric were collected either using a kill jar or mouth aspirator. Visual searching involved actively searching for five consecutive minutes insects and other arthropods flying or sitting on or under the surrounding vegetation. Areas where sweeping, beating, and visual searches were performed were selected randomly using the location of spider colonies as reference points. The area or distance covered by these techniques depended on the time allotted for each. For all the collecting techniques, sampling bouts of identical effort and procedure were used at the four sites by the same observer. Although the surveys of spider colonies were performed during the day only, for the sake of comparing the two environments we also surveyed nocturnally active insects using light traps. Starting at different times every night (earliest starting time 20:00 hours), a black light (15-watt black light, 18″ long tube) set against a white sheet was run on different nights at each of the sites. We checked the sheet after 1-h periods for 3 h and all specimens found on it were collected and sorted in the laboratory. The same sheet was used every time at all four sites. We conducted all surveys during the day in the vicinity of the spider colonies, except for blacklighting, which was carried out

We used nominal logistic regression to test for differences between habitats and techniques in the relative proportions of the five most common taxa (number of specimens) – Coleoptera, Diptera, Hymenoptera, Homoptera, Lepidoptera – plus an ‘other’ category that included all other arthropods (mainly other insects and arachnids). Our response variable were the taxa categories (‘taxa’) with associated frequencies corresponding to the number of specimens collected by an individual malaise trap over the entire sampling period at a given locality or in 1 day beating, sweeping, visual search, or blacklighting. We initially run a combined mixed model regression with ‘habitat’ (rainforest and cloud forest), ‘technique’, and ‘habitat × technique’ interaction as factors, and ‘trap ID’ or ‘sampling day’ as random effects nested within the ‘habitat × technique’ interaction. Further comparisons between habitats were performed separately for each individual technique, including the spider colonies, using also a mixed model where the response variable was ‘taxa’ (five insect and other arthropod categories) and the factor was ‘habitat’. For the colonies, data were combined over the entire sampling period (sample sizes per colony ranging from 1– 48 specimens). As before, each sampling day or trap/colony ID was treated as a random effect nested within ‘habitat’. We compared differences between the spider colonies and each sampling technique – as well as between pairs of techniques – within each habitat by running separate analyses in which the spider colonies were treated as an additional technique. Here, we used a nominal logistic model where the response variable was ‘taxa’ (five insect and ‘other’ categories) and the factor was ‘technique’ (daily samples/trap or colony ID as a random effect). We also compared the spider catches against all sampling techniques combined, except for blacklighting. We excluded blacklighting from this comparison as all colony prey capture observations were performed during the day. In assessing significance levels, Bonferroni corrections were applied, as appropriate, when multiple comparisons were involved (Bonferroni correction numbers for comparisons: A. eximius and techniques = 5, A. baeza and techniques = 5, among techniques at low elevations = 10, among techniques at high elevations = 10). For the same set of comparisons as above, but using the original taxonomic categories (Table 2), we estimated two abundancebased similarity indices – the percentage similarity (PS) coefficient and the Morisita–Horn (MH) similarity index (Wolda, 1981; Krebs, 1999), the latter as implemented in the computer program spade (Chao & Shen, 2003) with 2000 bootstrap replicates for the estimation of standard errors. With the percentage similarity coefficient expressed as proportions, both indices range between 0 (no similarity) and 1.0 (complete similarity). We found that the more recently developed abundance-based Jaccard and Sørensen indices (Chao et al., 2005) provided very little separation between

© 2009 The Authors Journal compilation © 2009 The Royal Entomological Society, Insect Conservation and Diversity, 2, 142–152

Technique

Target arthropod group

Sampling period

Pros

Cons

References

Blacklighting (UV light)

Nocturnal flying insects (i.e. nocturnal Lepidoptera, Trichoptera, Diptera)

Night

Relatively selective of certain groups of arthropods Large sample sizes

Excludes taxa active in daytime

Williams et al., 1955; Walker & Galbreath, 1979; Bowden, 1982; Taylor 1986; Yela & Holyoak, 1997; Butler et al., 1999

Malaise

Active flyers (i.e. Diptera, Hymenoptera, Lepidoptera, Homoptera, Trichoptera, Coleoptera)

Night and day

Sweeping

Arthropods found in the understorey vegetation (e.g. Coleoptera, Homoptera, Araneae) Resting understorey arthropods [i.e. Araneae, Coleoptera, Hymenoptera, Lepidoptera (larvae)]

Night and day

Large visible arthropods (i.e. Araneae, Lepidoptera, Orthoptera, Odonata)

Night and day

Beating

Visual search

Day

Yields narrowest range of taxa relative to other light traps Catches affected by moonlight, wind, and temperature Excludes ground and non-flying taxa. Misses taxa that drop down when hitting the net

Yields a wide range of flying taxa, including taxa that fly up when hitting the net Functions continuously for days Small sample sizes Yields a wide range of taxa Excludes ground and canopy arthropods Extensive training and Catches affected by vegetation type, sweep experience not required speed and height, time of day, and weather Targets taxa attached to Biased against small or active taxa. Excludes vegetation ground arthropods Simple and fast. Inefficient at night Extensive training and Suitable vegetation challenging to find experience not required Non-destructive Excludes small, non-obvious taxa Straightforward and fast. Efficiency affected by experience of collector. Specimens may be counted more than once Small sample sizes

Darling & Parker, 1988; Longino & Colwell, 1997; Butler et al., 1999; Ulyshen et al., 2005 DeLong, 1932; Beall, 1935; Allan et al., 1973; Basset et al., 1997; Sorensen et al., 2002 Harris et al., 1972; Basset et al., 1997; Southwood & Henderson, 2000; Sorensen et al., 2002

Sorensen et al. 2002; Southwood & Henderson, 2000

Arthropod sampling techniques and spider diets

© 2009 The Authors Journal compilation © 2009 The Royal Entomological Society, Insect Conservation and Diversity, 2, 142–152

Table 1. Five sampling methods used to survey communities of insects and arachnids at different elevations in eastern Ecuador.

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Table 2. Arthropod composition (given as proportions) yielded by the combination of collecting techniques, individual techniques, and spider colonies at lowland tropical rainforest (Jatun Sacha and Cuyabeno combined) and upper montane cloud forest (Yanayacu and Baeza combined) sites in eastern Ecuador. All techniques percentage

Black light percentage

Malaise percentage

Sweeping percentage

Beating percentage

Visual percentage

Spiders percentage

Order

H

L

H

L

H

L

H

L

H

L

H

L

H

L

Acari Araneae Blattodea Collembola Coleoptera Dermaptera Diptera Ephemeroptera Hemiptera Homoptera Hymenoptera Isoptera Lepidoptera Mantodea Mecoptera Neuroptera Odonata Opiliones Orthoptera Phasmatodea Plecoptera Psocoptera Thysanoptera Trichoptera Other Insecta

0.1 5.1 0.01 0.5 20.4 0.02 21 0 7.6 19 9.6 0 8.6 0 0 0.1 1 0 4.8 0.3 0 0.3 0.4 1.1 0.1

0 5 2.5 0 14.1 0.04 14.9 0.01 1.6 6.6 33.5 0.1 10.1 0.3 0.02 0.1 0.8 0.1 7.5 0.6 0.1 0.1 0.2 1.6 0.3

0 0.2 1.8 0 9.9 0 19.8 0.1 0.6 8.4 9.1 0.3 31.8 1.2 0 0.3 0.1 0 6.9 0.5 0.4 0.4 0.1 7 1.2

0 0 0 0 5.2 0 42.2 0 0.3 11.4 4.7 0 29.5 0 0 0.5 0 0 0.3 0.1 0 0.7 0 5.1 0

0 2.8 4 0 11.5 0.1 35.8 0 1 8.5 24.9 0 5.1 0 0.1 0 0 0 5 0 0 0.1 0.2 0.8 0

0.5 1.4 0 0.1 16.7 0 38.5 0 2.2 17.2 13.3 0 6.6 0 0 0.1 0 0 1.6 0 0 0.1 0.1 1.1 0.6

0 6.1 1.7 0 25.5 0 7.8 0 3.4 8.5 32.3 0 1.5 0.1 0 0.1 0.1 0.1 11.7 1 0 0.1 0.1 0 0

0 7 0 0 27.5 0 14.7 0 10.5 23.8 8.4 0 1.7 0 0 0 0 0 5.1 0.3 0 0.4 0.5 0.1 0

0 11.1 3.2 0 10 0.1 0.3 0 0.8 3 64.1 0.1 1.2 0.1 0 0 0 0.2 4.9 0.8 0 0 0.2 0.1 0.1

0.1 12.8 0.1 4.1 26.1 0.2 0.3 0 12.1 19.4 15 0 0.5 0 0 0 0 0 6.9 0.7 0 0 1.4 0.1 0.3

0 0.5 1.1 0 9.4 0 13.9 0 2.2 3.2 25.6 0 22.5 0.3 0 0 8.8 0 11.4 1.1 0 0 0 0.1 0

0 0 0 0 7.3 0 13.3 0 8.8 7.7 13.5 0 21.4 0 0 0 12.8 0 15.4 0 0 0 0 0 0

0 0 2.2 0 31.5 0.3 5.9 0 1.0 14.5 31.1 0 4 0 0 0 0.5 0 8.7 0.2 0 0 0 0 0

0 0 0 0 44.9 0 10 0 2.7 24.9 11.4 0.1 2.8 0 0 0 0 0 1.8 0 0 0.5 0 0.1 0.7

H, high elevation; L, low elevation.

estimates in our data set, as most values obtained ranged between 0.95 to 1.0; we thus do not report them in our results. We report taxonomic compositions in terms of relative proportions of each insect and arachnid group. For the purposes of comparing the two altitudinal ranges, we estimated overall percentages with all techniques combined making sure that the relative contributions of the various techniques to the combined estimate were the same across habitats. This was accomplished by scaling up or down the number of specimens (per taxa category) collected by a given technique so as to even out the representation of the technique across habitats at the between-habitat average frequency with which the technique was applied. Thus, for instance, since we had 14 blacklighting samples (1-day averages) from the lower elevations and seven from the upper elevations (betweenhabitat average = 10.5 samples), we multiplied by 0.75 (= 10.5/14) the number of specimens collected by this technique at lower elevations and by 1.5 (= 10.5/7) those collected at upper elevations, resulting in the technique being represented at both habitats at the equivalent of 10.5 1-day samples. We emphasise that in obtaining a combined estimate of all techniques, our goal was the comparison across habitats, rather than estimation of the actual proportions of the different taxonomic groups in their respective environments, as the latter is essentially an unattainable

goal (Godfray et al., 1999). With the exception of the similarity indices (see above), all tests were carried out using the statistical software jmp in (version 5.1).

Results There were no significant differences in taxonomic composition between the two lowland sites (Cuyabeno vs. Jatun Sacha, Wald- x(25,295) = 4.7, P = 0.5, PS = 0.80; MH = 0.90 ± 0.04) or between the two high-elevation sites (Yanayacu vs. Baeza Wald- x(25,165) = 2.04, P = 0.8, PS = 0.92; MH = 0.98 ± 0.02). We thus ran all analyses on the combined samples for each elevation.

Elevational differences in the composition of insects and other arthropods A total of 14 803 specimens from 25 different orders were collected by the combination of techniques (low elevation: 7290 specimens from 23 orders; high elevation: 7513 specimens from 19 orders). There were significant differences in the proportions of the six major taxa categories between low- and high-elevation

© 2009 The Authors Journal compilation © 2009 The Royal Entomological Society, Insect Conservation and Diversity, 2, 142–152

Arthropod sampling techniques and spider diets

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Fig. 1. Relative proportions of insects and some arachnid taxa captured by a combination of five collection techniques (including and excluding blacklighting – see Methods) and Anelosimus spider colonies at a low-elevation rainforest and high-elevation cloud forest in eastern Ecuador. Six major categories are reported: Coleoptera, Diptera, Hymenoptera, Homoptera, Lepidoptera, Other (other insects and some arachnids). Table 3. Comparison of arthropod compositions between lowland tropical rainforest (Jatun Sacha and Cuyabeno combined) and upper montane cloud forest (Yanayacu and Baeza combined) based on each of the five collecting techniques and the spider colonies. Nominal logistic analyses are based on the six major taxonomic categories (Coleoptera, Diptera, Hymenoptera, Homoptera, Lepidoptera, other) and similarity indices on the arthropod orders listed on Table 2 (see methods). Both abundance-based similarity indices – the percentage similarity coefficient and the Morisita–Horn similarity index – range between 0 (no similarity) and 1.0 (complete similarity). Lowland rainforest vs. upper montane cloud forest Technique Beating Sweeping Spider colonies Black light Visual search Malaise traps

Nominal logistic

= 101.8, P < 0.001 = 83.9 , P < 0.001 = 2.9, P = 0.7 = 19.0, P < 0.001 = 11.1, P = 0.05 = 5.8 , P = 0.3

2 ( 5,90 ) 2 ( 5,130 ) 2 ( 5,340 ) 2 ( 5,90 ) 2 ( 5,75) 2 ( 5,105)

x x x x x x

sites in the combined analysis [x(25,490) = 50.9, P < 0.001; PS = 0.67, MH = 0.74 ± 0.10; Fig. 1]. At low elevations, Hymenoptera, Diptera, and Coleoptera, in this order, accounted for 63% of all arthropod collected, whereas at high elevations, Diptera, Coleoptera, and Homoptera, in this order, contributed with 61% to the overall number of arthropods collected (Fig. 1, Table 2). The relative contribution of Hymenoptera diminished by a factor of three from high elevations to low elevations (33.9%, N = 2394 vs. 9.5%, N = 762). Ants made up 73% (N = 1883) of the hymenopterans at low elevations, whereas at high elevations they represented only 34% of the hymenopteran sample (N = 289). The next most notable difference was a threefold increase in the representation of Homoptera, from 6.3% (N = 481) at low elevations to 19.1% (N = 1410) at high elevations. Proportions of dipterans were higher at high elevations (21.1%, N = 1680) than at the low-elevation sites (15.0%, N = 980). Coleoptera was the second dominant group at high elevations (20.4%, N = 1512), being considerably more highly represented there than at low

Percentage similarity coefficient

Morisita–Horn index

0.47 0.67 0.69 0.74 0.81 0.79

0.49 ± 0.16 0.75 ± 0.11 0.86 ± 0.09 0.87 ± 0.07 0.92 ± 0.04 0.94 ± 0.06

elevations (13.9%, N = 1064). Lepidoptera occurred in smaller proportions, with a slightly better representation at the low elevations (9.9%, N = 801 vs. 8.6%, N = 618).

Taxonomic composition captured by the different techniques The five collecting techniques yielded sample sizes ranging from 59–274 specimens for malaise trapping (individual trap totals over the entire sampling period) and, 1-day totals of 35–542 specimens for beating, 35–514 specimens for sweeping, 21–151 specimens for visual, and 79–359 specimens for blacklighting. The five methods captured for the most part distinct arthropod 2 assemblages at the two elevations [ x(20 ,490) = 256.8 , P < 0.001; Fig. 2]. When analysed separately, only beating, sweeping, and blacklighting yielded significant differences between elevations 2 [habitat × technique interaction: x(20 ,490) = 115.5, P < 0.001; Table 3 and Fig. 2].

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Fig. 2. Relative proportions of arthropod taxa captured by five collection techniques (blacklighting, malaise traps, sweeping, beating, and visual search) at a low-elevation rainforest and high-elevation cloud forest in eastern Ecuador. Only the most common orders are reported.

Beating yielded a total of 2752 specimens from 19 orders (low elevations: 1732 specimens from 17 orders; high elevations: 1020 specimens from 16 orders), with relatively low compositional similarity between elevations (Table 3). At low elevations, beating collected mostly hymenopterans (64.1%, N = 1110) followed by arachnids (11.1%, N = 192) and coleopterans (10%, N = 173). At high elevations, the dominant insect groups were coleopterans (26.1%, N = 266), homopterans (19.4%, N = 198), and hymenopterans (12.8%, N = 153). Ants made up the majority of hymenopterans in beating samples at both elevations (low elevations: 97.3%, N = 1080; high elevations: 73%, N = 112). Sweeping caught a total of 5225 specimens from 17 orders (low elevations: 2092 specimens from 16 orders; high elevations: 3133 specimens from 12 orders), with a significant difference in composition between elevations (Table 3). At low elevations, the predominant orders were Hymenoptera and Coleoptera (32.3%, N = 675, and 25.5%, N = 534 respectively) whereas at high elevations Coleoptera and Homoptera were present in greater proportions (27.5%, N = 863 and 23.8%, N = 747 respectively; Fig. 2). Within the Hymenoptera, ants were twice as much represented at low elevations (64%, N = 675) than at higher elevations (33%, N = 262). Blacklighting yielded 2815 specimens from 21 orders (low elevations: 1643 specimens from 18 orders; high elevations: 1172 specimens from 11 orders), with a significant compositional difference between elevations and intermediate similarity indices (Table 3). At low elevations, the predominant orders captured by this method were nocturnal Lepidoptera followed by Diptera (31.8%, N = 523, and 19.8%, N = 325 respectively; Fig. 2). At high elevations, Diptera were the dominant order, followed by Lepidoptera (42.2%, N = 494, and 29.5%, N = 346 respectively; Fig. 2).

Visual search yielded 1231 specimens from 13 orders (low elevations: 763 specimens from 13 orders; high elevations: 468 specimens from 8 orders). The compositional difference between elevations for the five major taxonomic categories was not significant given a Bonferroni correction to account for five multiple comparisons (Table 3). At low elevations, visual search yielded mostly hymenopterans and lepidopterans (25.6%, N = 195, and 22.5%, N = 172 respectively), and lepidopterans and orthopterans at high elevations (22.5%, N = 100, and 15.4%, N = 72 respectively; Fig. 2). Ants made up only 24% (N = 46) of the hymenopterans yielded by visual search at low elevations. Malaise traps collected 2780 specimens belonging to 19 orders (low elevations: 1060 specimens from 14 orders; high elevations: 1720 specimens from 15 orders). At both elevations, the predominant taxon captured was Diptera (low elevations: 35.8%, N = 380; high elevations: 38.5%, N = 662; Fig. 2) and the compositional similarity at the level of orders between elevations was relatively high (Table 3). In general, individual sampling techniques captured arthropod groups in proportions significantly different from one another 2 within each habitat [rainforest x(20 ,280) = 239.3 , P < 0.001; cloud 2 forest x(20 , P < 0.001; Fig. 2]. In the rainforest, = 192 . 1 ,210) pairwise comparisons revealed significant differences (nominal logistic P-values for different pairs of techniques < 0.001) and generally low similarity (PS values ranged from 0.32 to 0.68 and MH indices from 0.26 to 0.83; Table 4) between pairs of techniques. A similar pattern held at the cloud forest (Pvalues ≤ 0.001; PS values ranged from 0.39 to 0.68 and MH indices from 0.48 to 0.84; Table 4), except that beating did not differ significantly from other techniques in the nominal logistic analyses (P-values > 0.5). Because calculations of PS and MH indices include the original taxa categories (Table 2), as opposed to only the five taxa considered in the nominal logistic model,

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Table 4. Percentage similarity and Morisita–Horn similarity index (MH) values for all combination of techniques and spider colonies in the upper montane cloud forest (above diagonal) and lowland tropical rainforest (below diagonal). Both abundance-based similarity indices – the percentage similarity coefficient and the Morisita–Horn similarity index – range between 0 (no similarity) and 1.0 (complete similarity). Technique Black light Percentage similarity coefficient MH Malaise Percentage similarity coefficient MH Sweeping Percentage similarity coefficient MH Beating Percentage similarity coefficient MH Visual Percentage similarity coefficient MH A. eximius Percentage similarity coefficient MH

Black light

Malaise

Sweeping

Beating

Visual

Anelosimus baeza

0.68 0.84 ± 0.14

0.39 0.48 ± 0.16

0.23 0.20 ± 0.19

0.53 0.65 ± 0.15

0.35 0.38 ± 0.18

0.64 0.78 ± 0.08

0.54 0.53 ± 0.16

0.52 0.61 ± 0.10

0.62 0.67 ± 0.12

0.78 0.90 ± 0.10

0.52 0.56 ± 0.12

0.77 0.90 ± 0.07

0.45 0.50 ± 0.14

0.62 0.83 ± 0.15

0.61 0.68 ± 0.14 0.59 0.48 ± 0.08

0.65 0.73 ± 0.14

0.32 0.26 ± 0.14

0.51 0.56 ± 0.24

0.61 0.78 ± 0.09

0.68 0.83 ± 0.08

0.64 0.75 ± 0.11

0.64 0.75 ± 0.16

0.48 0.61 ± 0.19

0.47 0.50 ± 0.14

0.63 0.69 ± 0.16

0.84 0.97 ± 0.06

0.54 0.72 ± 0.16

they are probably a better indicator of differences in taxonomic composition between pairs of techniques.

Taxonomic composition of prey captured by spider colonies The spider colonies captured a total of 1467 specimens, all insects, from 17 orders (A. eximius: 578 insects from 11 orders at low elevations; A. baeza: 880 insects from 13 orders at high elevations). The proportions of the different insect categories captured were not significantly different for the two spider 2 species [ x(5 ,340) = 2.9, P = 0.7; PS = 0.69; MH = 0.86 ± 0.09; Fig. 1). The majority of insect prey captured by A. eximius colonies were coleopterans (31.9%, N = 182), hymenopterans (31.3%, N = 180), and homopterans (14.1%, N = 84). Anelosimus baeza colonies captured mostly coleopterans (44.9%, N = 395), homopterans (24.9%, N = 219), and hymenopterans (11.4%, N = 100). Ants made up about half of the hymenopterans captured by the colonies (low elevations: 55%, N = 99; high elevations: 45%, N = 45). At low elevations, the major insect taxa captured by A. eximius were in similar proportions to the insects collected by each of the individual sampling techniques (P-values ranged from 0.28 to 0.99) and the combined set of all techniques, excluding blacklighting 2 [ x(5 ,400) = 0.096 , P = 0.9; PS = 0.75; M-H = 0.89]. Similarity indices for individual techniques ranged from 0.47 to 0.84 (PS) or 0.50 to 0.97 (MH), with blacklighting having the lowest and sweeping the highest similarity to the spider diets (Table 4). At upper elevations, the proportion of major insect taxa captured by A. baeza differed significantly from those in the combined 2 sample of techniques, excluding blacklighting [ x(5 ,325) = 13.5, P = 0.02; PS = 0.72; MH = 0.86], but not from those sampled by individual techniques, except for blacklighting [blacklighting

0.44 0.43 ± 0.13 0.59 0.71 ± 0.13

2 x(5 ,215) = 16.8, P = 0.005; other techniques P > 0.01, given five multiple comparisons]. As with A. eximius, sweeping had the highest similarity to the spider diets (0.77 PS; 0.90 MH), followed by beating (0.62 PS; 0.83 MH), and then malaise trapping (0.62 PS; 0.67 MH) (Table 4).

Discussion Compositional differences between low and high elevations There were significant differences in arthropod composition (insects and arachnids) across forest habitats at two different elevations in Ecuador, as detected by three sampling methods (beating, sweeping, and blacklighting) and the combination of the five sampling techniques. The most marked differences were an increase in the relative abundance of Hymenoptera, especially ants, at lower elevations, and a concomitant decrease in the frequency of Homoptera, Diptera and Coleoptera (Table 2). The observed pattern in the elevational distribution of hymenopterans seems to be associated with the greater abundance of ants in the lowlands and their apparent paucity at higher elevations. A pattern of decreasing ant abundance with increasing elevation has been reported for other tropical areas including Venezuela and Costa Rica (Janzen et al., 1976), the Philippines (Samson et al., 1997) and Malaysia (Bruhl et al., 1999). Given that ants may be important predators or competitors of social insects and other organisms (Kaspari & O’Donnell, 2003), their over-representation in lowland tropical areas should significantly impact trophic interactions and the structure of those communities. Elsewhere we suggest that predation by ants may be one of the factors responsible for the absence of subsocial Anelosimus spiders in the lowland tropical rainforest (Avilés et al., 2007; Purcell &

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Avilés, 2007). The increase in the relative proportion of dipterans at higher elevations agrees with patterns observed by Whittaker (1952) in the temperate Smokey Mountains, although opposite trends were obtained using sweep samples in the tropics (Janzen et al., 1976). Similarly, the observed pattern of decreased coleopteran abundance at lower elevations does not concur with previous studies that have reported the opposite trend in some temperate (e.g., Whittaker, 1952) and tropical areas (e.g., Janzen et al., 1976), with the exception of some groups (e.g., carabids, Olson, 1994). In the case of Lepidoptera, we found that its relative contribution decreases slightly at higher elevations. Although a similar trend has been reported by previous studies (Whittaker, 1952), there seems not to be a general elevational pattern for this particular order as relative abundances have been also observed to either increase with elevation or peak at mid-elevations (Janzen et al., 1976; Brehm & Fiedler, 2003).

Taxonomic composition captured by individual sampling techniques Not surprisingly, the various techniques differed in the relative proportions in which they caught different taxa, thus giving a clear indication of their taxonomic bias (e.g., Juillet, 1963; Noyes, 1989; Kharboutli & Mack, 1993; Wells & Decker, 2006; Guevara & Avilés, 2007). As expected, blacklighting yielded mostly nocturnal Lepidoptera and Diptera at both elevations. Malaise traps, on the other hand, captured mostly dipterans and hymenopterans across elevations, as such devices have been recognised for their efficiency at intercepting small flying insects (Guevara & Avilés, 2007) as well as high canopy ants (Longino & Colwell, 1997). Using sweeping and beating, we recovered overwhelming proportions of hymenopterans – mostly ants – in the lowland rainforest, followed by similar proportions of coleopterans at both elevations. Visual searches recorded, for obvious reasons, insect and arachnid groups belonging to very large sizes (Guevara & Avilés, 2007), yielding mostly diurnal Lepidoptera. Despite these biases, differences between habitats were detected by three of the sampling techniques, including beating, sweeping and blacklighting (Table 3). Malaise and visual samples from the two elevations, however, did not differ significantly from one another (Table 3). As shown in this study, obtaining a representative sample of the arthropod community in a given area is difficult (e.g., Colwell & Coddington, 1994; Godfray et al., 1999; Longino et al., 2002). Given the biases of individual sampling techniques, it is thus surprising that studies reporting relative abundances of different arthropod groups at different elevations have not typically used a combination of collecting methodologies, particularly in areas such as the tropics where arthropod diversity is high at even small spatial scales (Willig et al., 2003). In our study, we did not include techniques that target canopy organisms (e.g., canopy fogging) or litter and ground-dwelling arthropods (i.e., pitfall traps), both important contributors to the overall tropical arthropod diversity (Olson, 1994; Stork & Grimbacher, 2006). To the extent that these areas of the forest differ in composition from the areas we sampled (e.g., Basset et al., 2001), some insect and arachnid groups are thus likely to be under-represented in our samples.

Taxonomic composition of prey captured by spider colonies We found that the spider diets did not differ significantly in terms of the six major taxonomic categories from the environmental samples at the low elevation and only slightly so at the higher elevation sites (see Results). However, similarity indices between the techniques and spider diets using the finer taxonomic categories (Table 2) varied broadly, with only sweeping having a greater than 75% similarity (for PS; > 90% for MH) for both species, with beating and malaise being the next most similar (Table 4). It is thus clear that no single sampling technique is likely to entirely recover insect prey in proportions similar to those captured by local spiders (see also Castillo & Eberhard, 1983). Interestingly, Guevara and Avilés (2007) found that it was also sweeping the technique that most closely matched the spider diets at both elevations in terms of insect sizes captured. Coleopterans, followed by hymenopterans, were the most abundant prey captured by colonies of A. eximius in the lowlands. Although ants made up 90% of hymenopterans collected by the combination of techniques at low elevations, ants represented a much lower proportion of the hymenopterans captured by A. eximius. Possible explanations include that ants walking on the vegetation supporting the nests are unlikely to get entangled in the spider webs, or that ants are rejected as prey by the spiders (e.g., Nentwig, 1980; Uetz, 1990). Overall, however, A. eximius captured insect prey in proportions similar to those caught by all techniques combined (excluding blacklighting), while A. baeza did not. The difference in the composition of insect prey captured by A. baeza relative to the combined environmental samples may be due to its smaller colony sizes and less developed level of cooperation, which may prevent it from taking full advantage of the abundance of different insect types in its environment. Capturing a narrower range of prey types, however, may also reflect greater specialisation in particular prey types than the more generalistic A. eximius in the lowlands. Alternatively, the discrepancy may be due to the inability of the arthropod collecting techniques we employed to obtain a truly representative sample of what is available to this spider in its environment or the fact that sampling of prey capture by colonies was performed during the day only, thus missing a period that could also potentially influence spider sociality in these habitats. More generally, our study shows that, given the sampling methods used, the arthropod communities in the Ecuadorian lowland rainforest where social Anelosimus species occur differ from those at higher-elevation cloud forests where subsocial species are found. It also emphasises the need to employ a combination of techniques for biodiversity assessments or between-site comparisons, as different techniques will target different arthropod groups. By comparing different sampling methods, we provide a means for the selection of appropriate methods for future studies.

Acknowledgements We thank the Museo Ecuatoriano de Ciencias Naturales and the Pontificia Universidad Católica del Ecuador in Quito for sponsoring our research in Ecuador, and the Instituto Ecuatoriano de Recursos Naturales and Vida Silvestre for research permits.

© 2009 The Authors Journal compilation © 2009 The Royal Entomological Society, Insect Conservation and Diversity, 2, 142–152

Arthropod sampling techniques and spider diets We also thank the staff of the Yanayacu Research Station, Cuyabeno River Lodge, and Jatun Sacha Research Station for their support throughout this project. Jessica Purcell, Natalia Chaikina, José Derraik, and one anonymous reviewer provided valuable comments on the manuscript. Funding was provided by a NSERC Discovery Grant to L.A. and an USRA NSERC to J.G.

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