1996. The Journal of Arachnology 24:111-128

ESTIMATING RICHNESS IN A SOUTHERN APPALACHIAN COVE HARDWOOD FOREST

Jonathan A. Coddington: Dept. of Entomology, National Museum of Natural History, Smithsonian Institution, Washington, D.C. 20560 USA

Laurel H. Young and Frederick A. Coyle: Dept. of Biology, Western Carolina University, Cullowhee, North Carolina 28723 USA

ABSTRACT. Variation in species richness at the landscape scale is an important consideration in con- servation planning and natural resource management. To assess the ability of rapid inventory techniques to estimate local species richness, three collectors sampled the spider fauna of a "wilderness" cove forest in the southern Appalachians for 133 person-hours during September and early October 1991 using four methods: aerial hand collecting, ground hand collecting, beating, and leaf litter extraction. Eighty-nine species in 64 genera and 19 families were found. To these data we applied various statistical techniques (lognormal, Poisson lognormal, Chao 1, Chao 2, jackknife, and species accumulation curve) to estimate the number of species present as adults at this site. Estimates clustered between roughly 100-130 species with an outlier (Poisson lognormal) at 182 species. We compare these estimates to those from Bolivian tropical forest sites sampled in much the same way but less intensively. We discuss the biases and errors such estimates may entail and their utility for inventory design. We also assess the effects of method, time of day and collector on the number of adults, number of species and taxonomic composition of the samples and discuss the nature and importance of such effects. Method, collector and method-time of day interaction significantly affected the numbers of adults and species per sample; and each of the four methods collected clearly different sets of species. Finally, we present recommendations to guide future research on the estimation of spider species richness.

Measures that describe or discriminate pop- useful input to conservation and land man- ulations or communities, such as standing agement decisions (Coddington et al. 1991). crop, basal area, population abundance, or Although species richness is but one compo- species diversity indices, are useful tools for nent of biological diversity and only one of conservation, natural resource management, many criteria conservationists and planners environmental monitoring, and land use plan- may use when evaluating sites (compare ning (Magurran 1988). Many of these statis- Vane-Wright et al. 1991; Williams et al. 1991; tics, such as Shannon's diversity index or Faith 1992; Williams & Humphries 1994), it Fisher's log series, have been thoroughly test- becomes especially important as the global ed by theoretical studies of their statistical be- loss of species by extinction accelerates and havior and accuracy and by use in many prac- the need for species preservation increases. tical situations. It is a curious fact that Regional or landscape diversity depends both similarly proven techniques to estimate spe- on alpha (local) and beta (habitat) diversity; cies richness of conservation units or com- but because the latter measure also depends munities are lacking, given that the number of on estimates of alpha diversity that are re- species is surely a fundamental, important and peated across the larger spatial scale at which simple community parameter (May 1975, beta diversity operates, the ability to estimate 1988, 1992; Pielou 1975; Palmer 1990; Bunge alpha diversity accurately assumes special im- & Fitzpatrick 1993; Col well & Coddington portance. Estimating local richness for a de- 1994; Gaston 1994; Samu & Lovei 1995). fined place at a defined time is fundamental Quick, inexpensive and reliable methods for to estimates of at larger spatial estimating the species richness of taxa at par- and temporal scales. ticular sites (alpha diversity) could provide Our knowledge of the structure and pattern

111 112 THE JOURNAL OF ARACHNOLOGY of biodiversity at landscape scales is especial- ness Area in Rabun County, Georgia (34°59'N, ly poor for those "megadiverse" groups such 83°06'W). The US Forest Service classified this as terrestrial that are responsible site as a mature white oak/northern red oak/ for the vast majority of extant species diver- hickory timber stand originating in about 1858. sity (May 1988, 1992; Stork 1988); yet it is Winter aerial photos reveal that white pine trees at a landscape scale that conservation often are more common here than in most southern operates, and at which faunas may actually be Appalachian hardwood coves. Schafale & preserved or fragmented, as the case may be Weakely (1990) classify this site as a rich cove (Cornell & Lawton 1992). Various attributes forest with a transition into montane oak-hick- and research initiatives point to the potential ory forest. The site contains one of 57 perma- usefulness of as indicators of nent vegetative diversity plots established in species diversity in terrestrial communities. 1990-1991 for monitoring habitat change in the Spiders are a typical "megadiverse" group of Ellicott Rock Wilderness Area (Patterson 1994). substantial ecological importance. They are 1) Data collection.•Four collection methods among the most speciose orders of were chosen to access the most diverse com- (Coddington & Levi 1991), 2) generalist pred- ponents of the spider fauna: aerial hand col- ators which have an important collective im- lection, ground hand collection, beating and pact on invertebrate herbivore populations Tullgren funnel litter extraction. We used time (Riechert 1974; Riechert & Bishop 1990), 3) as a measure of sampling effort to make the ubiquitous and easy to collect, and 4) nonspe- first three methods comparable. One sample cialists can be quickly trained to make re- unit equalled one hour of uninterrupted time markably accurate counts of spider morpho- during which all putatively adult spiders were species (Oliver & Beattie 1993). Coddington collected into 80% ethanol. A 1 h sample unit et al. (1991) developed and field-tested a rel- yielded a statistically tractable number of in- atively simple protocol to sample and estimate dividuals per sample and allowed for a suffi- the species richness (alpha diversity) of spi- cient number of replicate samples to conduct ders in tropical forests. statistical analyses. Day (900-1800 h) and This study assesses the usefulness of this night (2000-0300 h) samples were collected protocol in estimating species richness in a in order to access both diurnal and nocturnal temperate forest community by 1) examining species. Each collector was limited to five or the effects of method, time of day and collec- fewer sample hours for each day or night col- tor on the number of individuals, number of lection period. Total sampling intensity was species and species composition of the sam- dictated by the number of adult spiders re- ple, and 2) comparing the richness estimates quired for richness estimation. Coddington et provided by different analytical approaches. al. (1991) guessed that roughly ten times as Secondarily, we are interested in comparing many specimens as species in diverse tropical the species richness of a site in one of the communities might yield sufficiently accurate floristically richest regions of temperate North estimates of species richness. Since Coyle's America (Whittaker 1972) with that of the (1981) study suggested that 60-120 species tropical Bolivian sites sampled by Coddington were accessible in a mature pine-hardwood et al. (1991). While the collecting methods forest within 5 km of our site, and since pre- used here were chosen for their efficiency in liminary sampling (2 September 1991) at our sampling spiders, we hope the overall ap- site averaged 12 adult spiders per hour, we proach, and especially the analytical methods, judged that 100 sampling hours would be ad- can be generalized to other diverse taxa. The equate. fundamental rule is to choose sampling meth- The three time-based collection methods in- ods according to the natural history of the tax- volved capturing spiders by hand and with an on without sacrificing heuristic measures of aspirator. The aerial and ground hand collec- sampling effort. tion methods are synonymous with the "look- ing up" and "looking down" methods, re- METHODS spectively, of Coddington et al. (1991). Aerial Study site.•The study site is a southern Ap- sampling required searching vegetation from palachian cove hardwood forest at 750-850 m knee height up to maximum arm's reach over- elevation, located in the Ellicott Rock Wilder- head. Ground collection required searching on CODDINGTON ET AL.•ESTIMATING SPECIES RICHNESS 113 hands and knees, exploring the leaf litter, logs, extraction of area-based litter samples, ex- rocks and plant surfaces that were below knee tending sampling to as many as 10 h (rather level. Beating entailed striking vegetation than only 5) in a 24 h period, avoiding resam- with a stick, catching the falling organisms on pling of areas, and in accessing a larger area a 0.5 m2 canvas sheet held horizontally below (2.5 ha) rather than confining collectors to one the vegetation, and aspirating and picking the hectare. spiders off the sheet. The number of such Only adult spiders were identified, counted beating/collecting events averaged 22 per one and used in the analyses because identifying hour sample. Two of the three collectors in juveniles to species level is difficult, time con- this study were experienced collectors with suming and fundamentally ambiguous in moderate practice at identifying southern Ap- many cases. Voucher specimens for each spe- palachian spiders; the third had no prior ex- cies identified in this study and a portion of perience collecting or identifying spiders. the duplicates have been deposited in the Plotless areas (ca. 500 m2) that allowed for Smithsonian Institution (USNM). adequate sampling opportunities and preclud- Statistical analysis.•Richness estimates ed collection interference were roughly delim- were obtained using six different approaches ited in the field. The collectors, each using a that differ in theoretical assumptions and the different method, operated simultaneously in kind of data required. The classic continuous each such area for one hour. Flagged bound- lognormal distribution (Preston 1948; Magur- aries prevented resampling on subsequent vis- ran 1988; Ludwig & Reynolds 1988; Colwell its. In order to restrict collecting to a fairly & Coddington 1994) is a parametric technique homogeneous vegetative type, distinctly dif- requiring relative abundance data. We also fit- ferent habitats, such as ridge tops, steep rock ted the Poisson lognormal (Bulmer 1974) be- outcrops, and Rhododendron thickets were cause its assumptions are better suited to dis- avoided. Approximately 2.5 ha were sampled. crete data than are those of the continuous Leaf litter was removed by hand from a 2 lognormal. We tested the fit of both lognormal m2 area and placed in a plastic bag. In the models to the data with Chi square statistics. laboratory this litter was placed in 50-60 cm The estimator proposed by Chao (1984), here- diameter Tullgren funnels with 60 W light after "Chao 1," is non-parametric, but also bulbs and 6-8 mm mesh screens, and spiders requires relative abundance data. The remain- were extracted into alcohol until the litter was ing three techniques are non-parametric but dry or nearly so. Data from the 11 litter sam- require only presence-absence data: the ples were included in richness estimates but "Chao 2" estimator (Chao 1987), the jack- omitted from time-based comparisons. knife (Heltshe & Forrester 1983), and species Sampling dates and number of one hour accumulation curves fitted to a rectangular hy- samples (n = 122) were as follows: 2 Septem- perbola (the "Michaelis-Menten equation") ber 1991 (« = 2); 6-9 September in = 50); (Lamas et al. 1991). We programmed SYS- 13-15 September (n = 35); 22 September (n TAT (Version 5.02) routines to calculate all = 18); and 5-6 October (n = 17). The Oc- richness estimates except the Poisson lognor- tober collection was added primarily to see if mal, for which we used Ross (1987). We also species represented by penultimate instars in used EstiMateS 3.1 (R. K. Colwell unpubl.) the September collections would mature be- to investigate the behavior of estimators under fore winter. Collectors were assigned methods randomized sample orders (see below). Where so that analysis of variance cells were equably possible we provide variance estimates for the represented; no more than two replicates of richness estimates. Point estimates of species any one collector/method combination oc- richness are most valuable when combined curred in any single 5 h collecting period. with measures of variability because the reli- Each of the 11 litter samples was treated as ability or precision of the estimates is con- equivalent to 1 h of collector effort for the veyed as well. purposes of richness estimation. Total sample We followed Magurran (1988) in fitting the number for estimation was thus 133. lognormal model (Preston 1948) to the data. This protocol differed from that used by Octaves falling to the left of the zero octave Coddington et al. (1991) by using time as a represent species that could have been col- measure for beating, adding Tullgren-funnel lected if more sampling had been done, while 114 THE JOURNAL OF ARACHNOLOGY octaves to the right represent actual sampling Chao 2 reaches its maximum of about one- results. The null hypothesis that relative abun- half the square of the observed richness when dances are lognormally distributed is assessed all species save one are uniques, and, con- by a Chi square statistic (df = number of oc- versely, considers the inventory "complete" taves - 3). The area under the normal curve when all species occur in at least two samples. estimates the number of species in the uni- The non-parametric jackknife estimator verse being sampled. There is no analytic for- proposed by Heltshe & Forrester (1983) is mula for the variance of the area under the curve (Pielou 1975), so measures of variabil- S•h* ' '-' (4) ity are not available for the lognormal esti- mate. where n is the number of samples. The vari- Chao (1984) proposed the following non- ance is parametric estimator (Chao 1, Colwell & Cod- dington 1994) for species richness (S*): l var(S;) = ^• -fcpfj-£), (5) 2 n \ o n &i ~ Sol (a /2b) (1) where Sobs is the number of species observed, where f} is the number of samples with j of a is the number of singletons, and b is the the L unique species. The jackknife reaches number of doubletons. Chao originally used a its maximum of ^2Sohs when all species are bootstrapping procedure to calculate a vari- uniques and considers an inventory complete ance, but later work suggests the same alge- when all species are known from at least two braic formula for the variance of the Chao 2 samples. estimator (see below) may serve for Chao 1 Species accumulation curves are a classic, (Chao 1984, 1987, pers. comm.). Note that the but informal way to assess the completeness Chao 1 estimator reaches its maximum of of an inventory (Pielou 1975; Soberon & Llo- about one-half the square of the observed rente 1993). As individuals of a population are richness when all species save one are single- sampled, new species are encountered rapidly tons and considers the inventory complete at first, but subsequently appear less frequent- when all species are represented by at least ly as the asymptote of species accumulation two individuals. is approached (Miller & Wiegert 1989). An The Chao 2 estimator (Chao 1987; Colwell equation for a two parameter hyperbola, pop- & Coddington 1994) originally dealt with the ularly known as the Michaelis-Menten equa- estimation of population size when the capture tion, has been used to estimate the asymptotes probabilities of individuals vary. This is for- of such curves, simply because it fits many mally equivalent to estimating the richness of data sets reasonably well (e.g., Lamas et al. a community when the abundance of species 1991). It is vary, and therefore her technique may also be B + n used to estimate species richness. Chao 2 re- "4 Sobs(h) (6) quires replicated samples (unlike Chao 1) and takes the same algebraic form as the Chao 1 where S*4 is the estimate of the asymptote (the estimator, above. Thus, species richness) and B is a fitted constant (ac- SI = S + (LV2M), (2) tually the number of samples needed to collect obs half the total species). As noted by Raaijmak- where L is the number of species found in ers (1987) and Colwell & Coddington (1994), only one sample ("uniques", regardless of most efforts to calculate a variance for this abundance in those samples), and M is the estimator (e.g., by least squares or regression) number of species found in just two samples are flawed by assuming independence among ("dupes", regardless of their abundance). The data points. However, one can at least calcu- variance is late SI for a large number of randomized ac- LJM cumulation orders and calculate the variance var = M 3 (3) of this sample of estimates (Colwell & Cod- 4 (L/M) m dington 1994). This statistic measures the The formula for var (S*,) is the same, but with variability in the data due to sample composi- a replacing L and b replacing M. Note that tion and richness. Richer samples added earlier CODDINGTON ET AL.•ESTIMATING SPECIES RICHNESS 115

Table 1.•Summary values and richness estimates for the Ellicott Rock samples. Sampling intensity is ratio of number of adults to observed species richness. See "Methods" section for explanation of bounds on estimates.

Sample'. sets A B C (Samples collected (Samples collected (All except Oct. D Sept. 2-13) Sept. 14-Oct. 6) samples) (All samples) Summary values No. of samples 64 69 114 133 No. of adults 751 878 1452 1629 Observed richness 67 74 85 89 No. of singletons 25 24 25 26 Sampling intensity 11.2 11.9 17.1 18.3 Estimators Poisson lognormal 207 ± 315 157 ± 127 179 ± 156 182 ± 126 Chao2 101 ± 35 135 ± 69 131 ± 49 128 ± 40 Chaol 102 ± 37 110 ± 40 124 ± 43 123 ± 35 Jackknife 93 ± 10 101 ± 12 111 ± 11 117 ± 11 Lognormal 98 92 106 114 Michaelis-Menten 89 ± 14 87 ± 18 100 ± 12 104 ± 13

tend to cause a more pronounced shoulder and treatment variables (collector, method and earlier asymptote. We performed 100 such ran- time of day) in both number of adults and domizations and calculated informal bounds on number of species collected, and Tukey HSD the estimate (2 SD) of the resulting 100 as- tests were used in determining pairwise sig- ymptote values. nificant differences (at P < 0.05). Descriptive Finally, to gauge the adequacy of the inven- statistics, ANOVAs, and Tukey tests were cal- tory for estimating richness, we again comput- culated using SYSTAT. The Bray-Curtis ed 100 replicate accumulation curves by ran- (1957) index of similarity, domized sample order, and, after the addition 2vv of each sample, calculated three estimators C = (7) (Chao 1, Chao 2, and jackknife), which Col- (x + y) well & Coddington (1994) found to be es- where x is the total number of adults collected pecially effective. Means of observed species by one method, y is the total number of adults accumulation and each estimator were plotted collected by the other method, and w is the against sample number. This analysis reveals sum of the lesser values for those species the behavior of the richness estimators as in- present in both samples, was used to assess formation accumulates (the empirical species the effect of collection method on the taxo- accumulation curve). A good estimator should nomic composition of samples. reach a stable asymptote long before the em- pirical curve (i.e., given few data). If the rich- RESULTS ness estimators do reach a stable plateau, even A total of 6666 spiders was collected in the if the observed curve is still rising by the last 133 samples, including 1629 adults represent- sample, the inventory may be adequate to es- ing 19 families, 64 genera, and 89 species (see timate richness of the fauna (Colwell & Cod- Appendix). We define "sample intensity" to dington 1994). Conversely, if the estimators are be the ratio of individuals (adults) to species, still climbing by the end of the inventory, rich- here 18.3:1. We define "inventory complete- ness estimates may still be subject to under- ness" to be the percentage of species repre- sampling bias. sented by singletons, here 29% (Table 1). Effect of sampling methods on results.• While inventory completeness rarely goes to Analyses of variance were used to identify zero, in well-sampled faunas it is likely to be significant differences (P < 0.05) among the low, whereas in sparse samples from rich 116 THE JOURNAL OF ARACHNOLOGY

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0 - 01 2345678 Octave Figure 1.•Fit of the data of Appendix ("observed") to the continuous lognormal distribution (esti- mated). X2 = 6.8; df = 6; 0.5 > P > 0.1. The distribution is truncated on the left. communities it is likely to be high. The col- representing the mean values of the Chao 1, lected data conformed to an expected skewed Chao 2, and jackknife estimators at each sam- frequency distribution (Williams 1964), with ple increment for 100 randomizations of sam- many species represented by few individuals ple sequence have not reached asymptotes and few species by many individuals. Only (Fig. 3). three species had abundances greater than Effects of method, time of day and col- 100, the most abundant being 186. lector.•Table 2 summarizes the data in the Richness estimates.•For the complete Appendix on numbers of adults and species data set, the richness estimates derived from collected by method and time of day. The all estimators except the Poisson lognormal number of adults collected per sample was agreed fairly closely and their confidence in- highly variable for all methods but especially tervals overlapped (Table 1). In general, esti- so for the litter samples. Three-way ANOVA's mates derived from approximate halves of the of the 122 time-based samples (litter samples data (subsets A and B) were lower than those omitted) showed that method and collector, based on nearly all (subset C) or all (set D) but not time of day, significantly affected both of the samples. For all these sample sets but the number of adults and species per sample set A, the rank order (from low to high) of and that the method-time of day interaction estimators was Michaelis-Menten, lognormal, significantly affected both the number of jackknife, Chao 1, Chao 2, and Poisson log- adults and species per sample. Tukey tests normal. showed that aerial and ground collecting The truncated species abundance distribu- yielded significantly more adults per sample tion for the complete data set spans eight oc- than beating, and significantly more species taves (Fig. 1). The frequency distribution was than litter sampling. slightly bimodal, but the continuous lognor- The Bray-Curtis similarity indices are low mal model fit reasonably well (0.1 < P < 0.5). for all pairwise comparisons of the samples of Acceptable fits were also obtained for all four each of the four collection methods (Table 3). partitions of the data, as judged by a Chi Even samples collected with the most similar square goodness of fit test. methods (aerial and beating; ground and lit- The species accumulation curve (Fig. 2) re- ter), were quite distinct taxonomically. Of the veals that new species were still being added 57 species collected by aerial and/or beating when sampling stopped and that the asymp- methods, 17 (30%) were unique to aerial col- tote had not been reached, despite the rela- lections and 13 (23%) were unique to beating. tively high sample intensity. Likewise, curves Of the 59 species collected by ground search- CODDINGTON ET AL.•ESTIMATING SPECIES RICHNESS 117

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0 10 20 30 40 50 60 70 80 90 100 110 120 130 Sample Number Figure 2.•The empirical species accumulation curve for the data of Appendix. Samples were accu- mulated randomly 100 times, and the mean ± two standard deviations plotted.

ing and/or litter extraction, 37 (63%) were ods (Table 3), indicating that contrasts be- unique to ground samples and 6 (10%) were tween methods are much stronger than con- unique to litter. Of the total 89 species ob- trasts between day and night. Nevertheless, 14 served, 12 species were caught only by aerial species (16% of the total) were collected only collecting, 15 only by ground collecting, 8 at night and 18 species (20% of the total) were only by beating, and 5 only by litter extrac- collected only during the day. tion. Of these 40 species, 26 (65%) were sin- Tukey tests attributed the significant effect gletons. Day and night samples for a given of collector on both the mean number of method have much higher indices of similarity adults and species to the difference between than do samples collected by different meth- collectors 1 and 2 (the most versus the least

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0 10 20 30 40 50 60 70 80 90 100 110 120 130 Sample Number Figure 3- -Mean values of observed species richness and Chao 1, Chao 2, and jackknife estimators at each sample increment for 100 random orders of sample addition. 118 THE JOURNAL OF ARACHNOLOGY

Table 2.•Summary of numbers of adults and species by collection method and time of day. Standard deviations of the mean number of adults and species per sample are given for method subtotals and for totals, n = number of samples.

Mean no. of % of Mean no. of % of No. of adults per total No. of species per total n adults sample adults species sample species Aerial Day 21 322 15.3 20 28 6.0 31 Night 21 315 15.0 19 33 6.5 37 Subtotal 42 637 15.2 ± 7.8 39 44 6.2 ± 2.1 49 Ground Day 20 222 11.0 13 41 6.1 46 Night 20 351 17.6 22 34 6.7 38 Subtotal 40 573 14.3 ± 6.7 35 53 6.4 ± 2.4 60 Beating Day 20 195 9.8 12 30 5.0 34 Night 20 113 5.7 7 26 3.8 29 Subtotal 40 308 7.7 ± 4.5 19 39 4.3 ± 2.0 44 Litter 11 111 10.1 ± 14.9 7 22 3.8 ± 3.4 25 Total 133 1629 12.2 ± 8.1 100 89 5.5 ± 2.5 100

experienced and productive collectors, respec- slightly during the final sampling period (Ta- tively). Each collector's performance (mea- ble 4). sured by average number of adults/sample) varied considerably during the study (Table DISCUSSION 4). A two-way ANOVA of the effects of date These methods estimate only the portion of and collector indicated a significant effect of the total Ellicott Rock spider fauna present as collector on the number of adults collected, adults in the area we sampled, during the time due to the difference between collectors 1 and we sampled, and accessible to the methods we 2 during the first sampling period. After this used. These are, therefore, estimates of the first period, there were no significant produc- "instantaneous" species richness of the tivity differences among the collectors. Al- ground and understory strata of that forest though not significant, the average number of site. They certainly underestimate the true adults collected per sample did decrease species richness, meaning all those species

Table 3.•Bray-Curtis similarity indices.

A. Collecting methods Ground Beating Litter Aerial 0.091 0.261 0.003 Ground 0.066 0.175 Beating 0.029 B. Method and time of day combination Aerial Ground Ground Beating Beating Litter night day night day night (day) Aerial day 0.575 0.088 0.048 0.116 0.128 0.005 Aerial night 0.086 0.084 0.180 0.257 0.005 Ground day 0.496 0.077 0.167 0.144 Ground night 0.059 0.082 0.147 Beating day 0.494 0.163 Beating night 0.045 CODDINGTON ET AL.•ESTIMATING SPECIES RICHNESS 119

Table 4.•Mean number of adults collected per spiders living on the ground and in the un- sample by collector and sampling period. Number derstory of this hardwood cove forest was of sample hours in parentheses. roughly 100-130 species (Table 1). The Pois- son lognormal gave consistently high esti- Sampling period mates with almost unusably broad confidence 1 2 3 4 limits. The similarity among the former esti- (Sept. (Sept. (Sept. (Oct. mates suggests either that they were measur- 6-9) 13-15) 22) 5-6) ing the true species richness, or that, if biased, Collector they all were affected similarly. The some- 1 14.8(20) 15.5(14) 21.0(4) 10.6(5) what lower estimates generated for the parti- 2 9.0(20) 12.5(14) 9.0(9) 6.0(6) tioned data sets of this study reveal that most 3 13.0(10) 11.6(7) 16.4(5) 12.0(6) estimators show substantial negative bias with small sample size (Colwell & Coddington 1994; Chao & Lee 1992), although the con- that successfully bred at that site during the fidence intervals usually overlap and the effect annual cycle in which we sampled. Even giv- is not consistent (Table 1). Since Chao 1, en this definition of the "local" fauna, species Chao 2, and the jackknife estimators are ex- may go locally extinct or immigrate from one plicit functions of the number of species ob- year to the next, to say nothing of showing served, such sensitivity is to be expected. This great variation in abundance (Wolda 1978). is not necessarily true for the continuous log- "Local species richness" necessarily varies normal nor the Michaelis-Menten models, al- with the time scale on which it is defined. though the former is well-known to require These estimates are snapshots•they should extremely large samples (Magurran 1988). We underestimate species richness over longer partitioned the data by date rather than a ran- time scales. On the other hand, if a proportion dom selection of samples, and thus our test of of the species actually observed are "tourists" the effect of sample size may have confound- or waifs, the richness estimate will be high ed the influence of sample size with that of because such rare species increase the esti- date, collector experience, or climate effects. mates but are not permanent members of the When sample order was randomized, the same community being estimated. These two effects trend was observed (Fig. 3). will tend to counteract each other. While field Fitting the continuous truncated lognormal guides or checklists may provide accurate lists model to these sample data was problematic, of species for larger areas accumulated by and different estimates of species richness can years of observation, it is difficult to know the be obtained depending on the method used. "true" species richness of an area small May (1975) did not recommend fitting the enough to be feasibly sampled in a short time lognormal to data sets containing many fewer period. Since the true species richness is gen- than 100 species, and certainly the grouped erally not known in such circumstances, and and log-transformed data in Fig. 1 do not form certainly not for Appalachian spider faunas, anything approaching a smooth curve. Al- the accuracy of the richness estimates can though the three Bolivian data sets reported only be assessed indirectly. The agreement by Coddington et al. (1991) were based on among the estimates and the coverage of their many fewer collecting hours and included associated confidence intervals can be as- fewer adults (Table 5), each fit a lognormal sessed, the estimates can be compared against distribution. Since the sampling intensity at common sense guesses, checklists, and other the Ellicott Rock site was roughly four times studies, and the performance of the estimators higher than at the Bolivian sites, the relative on subsets of the data can be assessed. Among abundances of species at the Ellicott Rock site the estimators we used, only the continuous are better known. May (1975) pointed out that lognormal and poisson lognormal are based a lognormal pattern of species abundance is on models that allow explicit tests of the fit often observed in stable (equilibrium) com- of the model to the data. munities, while disturbed communities will Temperate richness estimates.•Five of show increased dominance and exhibit instead the six estimators used in this study suggest a log series distribution, but this pattern is far that the species richness of late summer adult from reliable. Most really diverse communi- 120 THE JOURNAL OF ARACHNOLOGY

Table 5.•Summary values and richness estimates for the Ellicott Rock and Bolivian sites. Bolivian data from Coddington et al. (1991 and unpubl. data). Sampling intensity is ratio of number of adults to observed species richness. See "Methods" section for explanation of bounds on estimates.

Ellicott El Rio Cerro Rock Trapiche Tigre Uchumachi Summary values No. of samples 132 51 69 37 No. of adults 1629 875 1109 654 Observed richness 89 191 329 158 No. of singletons 26 89 147 70 % singletons 29 47 45 44 Sampling intensity 18.3 4.6 3.4 4.1 Estimators Poisson lognormai 182 ± 126 616 ± 428 691 ± 200 375 ± 188 Chao2 128 ± 40 329 ± 77 583 ± 105 278 ± 73 Chaol 123 ± 35 319 ± 73 506 ± 77 256 ± 63 Jackknife 117 + 11 283 ± 27 497 ± 40 235 ± 26 Lognormai 114 247 374 191 Michaelis-Menten 104 ± 13 322 ± 104 578 ± 152 277 ± 113

ties are likely to have been so sparsely sam- According to Chao (1984), her method gen- pled that either model will fit the data ade- erates lower bounds on estimates and ought to quately. For example, Turnbull (1966) found work best when "most of the information is a log series fit for spider species abundance concentrated on low order occupancy num- data collected from May to September in a bers," i.e., when most species in the sample north temperate early field succession where are observed as singletons or doubletons. dominance by colonizers would be predicted, About 40% of the species were singletons or but the lognormai fits his data also (our cal- doubletons in the Ellicott Rock data versus an culations). average of 62% in the Bolivian data. Since The greater seasonality of temperate com- tropical samples often have a greater propor- munities should foster narrower, species-spe- tion of "rare" species than temperate samples, cific breeding seasons and thus may cause a Chao 1 ought to yield better estimates of trop- sample of adults collected in a short period (a ical richness than of temperate richness. How- few weeks or less) to mimic the dominance of ever, despite great disparities in the frequency a low diversity, early successional stage. Just ranges of the temperate versus the tropical three species ( mitrata, Micrath- data, this estimator clustered about in the mid- ena gracilis, and Wadotes hybridus) com- dle of other estimates. If poor behavior of an prised 29% of all adults in the Ellicott Rock estimator due to violation of assumptions samples. Sampling methodology may also af- shows up in aberrant values, we did not ob- fect the observed species abundance distribu- serve it for Chao 1. tion. We may have been biased toward the By generating richness estimates from collection of more apparent (less cryptic and/ quadrat sampling of a known community of or more active) species (Stork 1988), especial- forest floor herbs and shrubs, Palmer (1990, ly since the plotless areas sampled in this 1991) determined that Heltshe & Forrester's study were not resampled as they were in the jackknife procedure yielded the best richness Bolivian study. On the other hand, unbiased estimates out of several estimators tested (al- samples are unobtainable in practical terms, though he did not test Chao's estimators). The and our use of experienced collectors is prob- jackknife method is biased by dominance, but ably no more biased than many other collect- this effect can be reduced by increasing sam- ing techniques. The ideal is to use an array of ple size (Heltshe & Forrester 1983). The collecting techniques that complement each heavy dominance in the Ellicott Rock samples other, rather than trying to design one tech- may have been offset by a large sample size nique with minimal bias. because, although lower than some of the oth- CODDINGTON ET AL.•ESTIMATING SPECIES RICHNESS 121 er estimates, the jackknife estimate is not methods we used. Nevertheless, although markedly deviant. "edge" effects may explain rare species to All six of these estimators rely on the pro- some extent, they still are valid indicators that portion of "rare" species, whether the latter, an inventory is incomplete. somewhat intuitive, notion is defined more The richness estimates derived from this precisely as either uniques or singletons. study must be interpreted critically due to the Common sense suggests that if all species in spatial and temporal (seasonal) bias of the the sample are known from "many" individ- sampling methods utilized. This study esti- uals after much sampling, the sample is prob- mated only that proportion of the total fauna ably exhaustive. Therefore, a better under- that was 1) available to the collecting methods standing of the status of singleton species may used and 2) adult during the course of the help to evaluate and refine estimator perfor- study. Perhaps the most significant omissions mance. (Since propinquity in time and space are the canopy fauna and those species present are highly related in this protocol, species only as juveniles. Examination of about 4200 unique to a sample is more a question of of the 5037 juveniles (76% of all specimens patchiness than rarity.) The 26 singleton spe- collected in the samples) revealed that be- cies collected in our study are distributed rath- tween 25-40 species were not represented by er evenly among collecting methods, families, adults in any of the samples. As noted above, and guilds (see Appendix). A survey of the richness estimates are biased upwards by in- taxonomic literature, the third author's multi- clusion of "tourist" or waif species that may year collecting records from this region, and be ecologically "out of place" or merely pass- data from a springtime inventory at our study ing through the site, and they are biased site (Dobyns in press) indicate that 22 of these downwards by low sampling effort and phe- species are spatially uncommon, i.e., more nology. However, if one presumes that the to- common either outside the southern Blue tal fauna available to the methods during the Ridge Province (14 species) or in other habi- collecting period was observed either as adults tats (6 species) or in the forest canopy (2 spe- or juveniles, then the true species richness of cies) (see Appendix). The other four single- the site was 114-129 species. The estimates tons are temporally uncommon, i.e., they are of Table 1 all agree fairly well with this com- species that are common at the site but whose mon sense figure. breeding seasons are past. On the other hand, the behavior of all es- One can view these rare species as caused timators in Fig. 3 is reason to believe that the by a variety of "edge" effects, of which the true species richness is still underestimated. most important are habitat, time and method. Col well & Coddington (1994) reported one Habitat edge effects explain the singleton sta- data set in which even the empirical curve tus of canopy species in subcanopy samples, reached an obvious asymptote. As expected, or of species not usually found in mature "good" estimators achieved this asymptote hardwood forest, but known to be more com- (or very close to it) much sooner than the em- mon elsewhere. Time edge effects explain the pirical curve. The sampling intensity of that four species in fact common at the site, but data set was over 30:1; but the Ellicott Rock that were "out of season" at the time we sam- inventory was 18:1, and the three Bolivian in- pled. Finally, method edge effects may ex- ventories were less than 4:1. If sampling in- plain some of the 14 species not known to be tensity is a rough guide to required effort, then anywhere common in the region. It is a eco- it appears that the 10:1 figure guessed at by logical truism that all species must be com- Coddington et al. (1991) is seriously low. mon somewhere, or, alternatively, that breed- The only previous study of spider species ing populations have a species-specific spatial richness in a southern Appalachian forest is structure. Although we cannot be certain, we that of Coyle (1981). Using aerial hand (2.25 doubt that few of these 14 species naturally h), ground hand (2.25 h), Tullgren litter (ten occur at such low densities that nearest neigh- 0.25 m2 samples), sweep net (about 2 h), and bor distances are greater than 100 meters. pitfall trap (eight traps for 15 weeks) methods More likely, these "rare" species occur in the between June and October, he collected 217 area we sampled, but have natural histories individuals and 51 species as adults (and 9 that make them difficult to collect by the more as juveniles) from a mature mixed pine- 122 THE JOURNAL OF ARACHNOLOGY hardwood site in the Ellicott Rock Wilderness Effects of method, time of day and col- Area, and about 5 km from the site we sam- lector on results.•Although some methods pled. Only 29 species, or 33% of the species (aerial and ground) were more productive than present in our total sample, are common to his others (beating and litter), the Bray-Curtis in- sample and ours. Both samples are similar in dices and the numbers of collected species the percent of sampled species of adults in unique to each method suggest that each three (ground web-builders, aerial web-build- method is sampling a distinctly different array ers, and aerial hunters) of the four guilds, but of species. Of course, species that are single- the Coyle sample had 18% ground hunters tons cannot appear in more than one sample, versus 9% in ours (9 of 51 versus 8 of 89 and these may artificially inflate the distinc- species, respectively). The greater duration of tiveness suggested by such comparisons. Al- the Coyle study and his low ratio of hand col- though aerial collecting and beating both ac- lecting effort to pitfall trap effort (which bi- cessed similar vegetative habitats, aerial ased his study in favor of ground hunters) help sampling accessed larger spiders (araneids) account for these differences. while beating accessed a higher proportion of Comparison of temperate and tropical smaller cryptic species (especially linyphiids; richness estimates.•It is no surprise that the see Appendix) which are likely to be over- species richness estimates for tropical sites looked during aerial hand collection. Ground (Coddington et al. 1991; Silva & Coddington hand collection accesses far more microhabi- in press) are much greater than for the tem- tats than does litter collection, but is less like- perate (Ellicott Rock) site (Table 5). Of the ly to sample the smallest-bodied litter-dwell- tropical sites, Rio Tigre was most nearly com- ing species. The extensive use of aspirators in parable in elevation to the Ellicott Rock site ground hand collection probably reduces this (500 m versus 800 m). Comparison of ob- difference between the two methods in the served species richness indicates that Rio Ti- size of the spiders collected. It is logical to gre had 3.7 times more species than Ellicott expect that methods which depend heavily on Rock, but comparison of the six estimated visual searching (aerial and ground) are biased species richness values indicates ratios from against small-bodied species. The higher ra- 3.8-5.6. Comparing Georgia to Bolivia is not tios of large to small spiders in the aerial and the point, but rather that comparisons of raw ground samples compared to beating and litter sample data can mislead. In this case, the low- samples, respectively, conform to that predic- er intensity tropical sample apparently ac- tion. Additional evidence of this bias is the cessed a much smaller proportion of the total high female to male ratio (13.5:1) for aerial fauna present. Use of statistical procedures collections of three common species with may emend such biased comparisons and en- much larger females than males (Micrathena able better comparison of the results of inven- gracilis, Micrathena mitrata, and tories that differ in method, circumstances and flavidus) and the much more normal ratio (1.5: completeness. This higher tropical species 1) for ground collections of large-bodied spe- richness resembles the north temperate to cies with little sexual size dimorphism (Wa- tropical latitudinal gradient observed for many dotes hybridus, Wadotes bimucronatus, and other taxa (Fischer 1960; Ehrlich & Wilson gulosa). As Poole (1974) has not- 1991; Platnick 1991). Interestingly, all the es- ed, the whole question of "true" relative timators for the tropical data sets show the abundance of species in nature as compared same rank order. With the exception of the to relative abundance in samples is nearly in- species accumulation curve, the same ranking soluble, however fundamental it may be to as- is repeated in the temperate data set. This rath- sessing bias. er startling consistency in rank order among The especially high variability of the litter estimators suggests a systematic bias with re- sample data may be the result of heterogeneity spect to each other (and therefore with respect in spider distribution, variation in litter depth to the true richness), at least for the data sets (Uetz 1975), or variation in Tullgren funnel tested thus far. It therefore remains to be dem- technique (funnels were sometimes overload- onstrated, perhaps through simulation studies, ed and the litter not allowed to dry complete- which estimator most accurately tracks the ly). Sampling equal volumes (rather than ar- true richness. eas) of litter, placing a constant and moderate CODDINGTON ET AL.•ESTIMATING SPECIES RICHNESS 123 volume in each funnel and continuing the ex- for hour 3, and 22 for hour 4; and the plan to traction process until the litter is completely collect for another hour was aborted due to dry should reduce this variability and make fatigue. comparisons between sites more meaningful. The data analysis suggests that naive and Sorting spiders from litter by hand in the field experienced collectors do differ in their abil- on a white tray for one hour might allow litter ities and that the sampling time required for a to be analyzed as a time-based method, but richness survey can be reduced by selecting this probably would not be as efficient as Tull- particularly able collectors. We suspect that gren funnel extraction and would be less like- the collectors in the Bolivian study, who av- ly to capture very small spiders. eraged 16.4 adults per sample (Coddington et Although time of day had no significant ef- al. 1991), would have averaged significantly fect on the number of adults and number of more than the 12.2 adults per sample average species collected, and Bray-Curtis indices in- productivity of the Ellicott Rock team because dicated that time of day affected the taxonom- the most experienced Ellicott Rock collector ic composition of samples less than method almost equalled the Bolivian average but had did, the relatively large number of species far less spider-collecting experience than four unique to either day or night samples indicates of the five collectors in Bolivia. However, this that both night and day collecting may be de- study and the Bolivian study both showed that sirable if the sampling is to approach closely the sampling productivity of inexperienced the real species richness of the site. These data collectors can improve so that they soon be- (see Appendix) support the generalization that came statistically indistinguishable from the many spider species are either predominantly more experienced collectors. This improve- night or day active. Wadotes hybridus, Glad- ment in collector performance is encouraging icosa gulosa, Mimetus interfector, Thiodina since it suggests that it is possible to train na- sylvana, , and Hyptiotes ive collectors rather quickly and thus to im- cavatus were species whose collection was plement efficient, long-term, continuous mon- strongly skewed toward the night (nocturnally itoring in the tropics. active species), while Micrathena gracilis, Collector (and method) productivity may fissiceps, Ceratinopsidis formosa, have been affected by climate-induced and Gonatium crassipalpum were far more changes in adult spider activity and/or abun- abundant in day collections (diurnally active dance. The reduced average sample size dur- species). Micrathena mitrata was the only ing period 4 (Table 4) was probably a result commonly sampled species that appeared to of a diminished number of active spiders due be equally active both night and day. Unlike to markedly colder and windier weather and these results, night sampling in the Bolivian not a reduction in collector performance. forests was significantly more productive Recommendations for future research.• (numbers of adults and species per sample) Since sampling protocols should access all com- than day sampling (Coddington et al. 1991), ponents of a fauna without bias, and since the supporting the oft quoted generalization that protocol used by Coddington et al. (1991) un- most kinds of spiders are most active at night, der-samples the litter fauna, methods that access and perhaps that diurnal predation pressure this fauna (litter extraction, pitfall traps) should may be more intense in tropical than in tem- be added wherever feasible. Hand sorting of lit- perate forests. ter for one hour on a tray would be logistically We should note, however, that collector fa- easier in remote areas due to the scarcity of elec- tigue may have markedly reduced the produc- tricity, but Tullgren funnel extraction may be tivity of night collecting in our study. While more productive and a study is needed to test the collectors in the Bolivian study in general that hypothesis; either way it would be more collected only 5 one-hour samples in any 24 informative to also record the volume of litter h period, the temperate sampling was done processed. We have shown that beating can be primarily on weekends with as many as 10 h performed as a time-based sampling method to of sampling per collector in a 24 h period. For make data analysis more straightforward. This example, the total numbers of adults collected study provides some, albeit weak, evidence for by the three collectors on the night of 14 Sep- the importance of night sampling; and it sug- tember were 48 for hour 1,51 for hour 2, 36 gests that sampling should be limited to 5-6 124 THE JOURNAL OF ARACHNOLOGY sample hours per 24 hour period to minimize Thesis presented by the second author (LY) to the effects of collector fatigue. Additional sam- the Department of Biology, Western Carolina pling of this and other hardwood coves in the University. This is contribution no. 83 from southern Appalachians should be undertaken in the Smithsonian Biological Diversity Pro- September, in May, and in July: 1) to see if the gram. species richness estimates of 104-128 are re- LITERATURE CITED peatable, 2) to explore the effect of season on richness estimates (see Dobyns in press), 3) to Bulmer, M.G. 1974. On fitting the Poisson lognor- compile a more accurate species list to which mal distribution to species abundance data. Bio- metrics, 30:101-110. the performance of richness estimators can be Bunge, J. & M. Fitzpatrick. 1993. Estimating the compared, and 4) to facilitate the identification number of species: a review. J. American Stat. of juveniles so that the effect of their inclusion Assoc., 88:364-373. on species abundance distributions and richness Bray, J. & J. Curtis. 1957. An ordination of the estimates can be studied. Simultaneous plotless upland forest communities of southern Wiscon- and quadrat sampling studies should be per- sin. Ecol. Monog., 27:325-349. formed to compare plotless richness estimates Chao, A. 1984. Nonparametric estimation of the with those based on 1) pooled quadrats (Pielou number of classes in a population. Scandinavian 1975) and 2) species-area relationships (Palmer J. Stat., 11:265-270. 1990, 1991). The hypothesis that repeated (in- Chao, A. 1987. Estimating the population size for capture-recapture data with unequal catchability. tensive) sampling in a plot will collect more co- Biometrics, 43:783-791. vert species than does non-repetitive collecting Chao, A. & S.M. Lee. 1992. Estimating the num- requires testing (see Dobyns in press). Statistical ber of classes via sample coverage. J. American research to develop confidence intervals for spe- Stat. Assoc, 87:210-217. cies accumulation curves and lognormal esti- Coddington, J.A. 1987. Notes on spider natural mates is required, as is further study of the de- history: the webs and habits of niveus pendence of estimates on sample size and their and Araneus cingulatus (Araneae, Araneidae). J. performance on data sets that display different ArachnoL, 15:268-270. degrees of ecological dominance (i.e., range of Coddington, J.A., C. Griswold, D. Davila, E. Pen- frequencies). Spider richness studies should be aranda, & S. Larcher. 1991. Designing and test- ing sampling protocols to estimate biodiversity located at sites where other or plant di- in tropical systems. Pp. 44-46, In The Unity of versity plots already exist so that the correlation Evolutionary Biology, Vol. 1. (E. Dudley, ed.). between spider richness and the richness of oth- Proc. Fourth Intern. Congr. Syst. Evol. Biol., er taxa can be explored. Dioscorides Press, Portland, Oregon. Coddington, J.A. & H.W. Levi. 1991. Systematics ACKNOWLEDGMENTS and evolution of spiders. Ann. Rev. Ecol. Syst., We thank Bob Dellinger and Trey McGarity 22:565-592. for helping to collect the spider samples, Dick Colwell, R.K. & J.A. Coddington. 1994. Estimat- Bruce, Allen Moore and Jackie Palmer for ing terrestrial biodiversity through extrapolation. their advice, encouragement and comments on Phil. Trans. Royal Soc. London (Ser. B), 345: 101-118. early drafts of this paper and Joe Beatty for Cornell, H.V. & J.H. Lawton. 1992. Species inter- identifying Graphomoa theridioides. Bob actions, local and regional processes, and limits Robbins offered helpful advice throughout on to the richness of ecological communities: a the- statistical issues, Rob Colwell made helpful oretical perspective. J. Anim. Ecol., 61:1-12. comments on the penultimate draft, and C. J. Coyle, EA. 1981. Effects of clearcutting on the Humphries and M. W Palmer provided help- spider community of a southern Appalachian for- ful reviews of the manuscript. We particularly est. J. ArachnoL, 9:285-298. thank Rob for making EstiMateS 3.1 avail- Dobyns, J.R. In press. The effects of seasonally able. The Highlands Biological Station, the and repetitive collecting on the estimation of spi- Western Carolina University Department of der species richness in a southern Appalachian cove hardwood forest. Environ. Entomol. Biology, and the Smithsonian Institution Ehrlich, P.R. & E.O. Wilson. 1991 Biodiversity (through its Scholarly Studies, Neotropical studies: science and policy. Science, 253:758- Lowlands, and Biological Diversity of Latin 762. America Programs) provided logistic support Faith, D.P. 1992. Conservation evaluation and phy- and funds. This paper is based on a Master's logenetic diversity. Biol. Conserv., 61:1-10. CODDINGTON ET AL.•ESTIMATING SPECIES RICHNESS 125

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Appendix.•Species and number of adult spiders collected in Ellicott Rock species richness study. Collection method and time of day indicated (D = day, N = night). Guild designation: A = aerial, G = ground, W = web building, H = hunting. Status of singleton species: R = rare in southern Blue Ridge Province; U = uncommon to moderately common in southern Blue Ridge Province; J = juveniles common in samples (adults common at another time of year); P = at periphery of its geographic range; H = common locally in other, usually more open, habitats; C = probably common in forest canopy (Coddington 1987).

Collection method Sin- gle- Aerial Ground Beating ton Taxon Guild D N D N D N Litter status Agelenopsis pennyslvanica AGW 10 2 4 3 Calymmaria cavicola GW 22 40 arcuata GW 3 7 12 Cicurina breviaria GW 6 3 2 Cicurina sp. A GW 2 Cicurina sp. B GW 1 R Coras aerialis AW 1 U Coras taugynus GW 2 9 Cybaeus silicis GW 2 6 4 Wadotes bimucronatus GW 28 41 Wadotes hybridus GW 18 101 Amaruobiidae Callioplus armipotens GW Anyphaena pectorosa AH 1 u Wulfila alba AH 1 u Araneidae Araneus cingulatus AW 1 c Araneus marmoreus AW 25 10 1 Araneus niveus AW 1 c Araneus nordmanni AW 17 6 1 3 1 Araneus pegnia AW 1 H Araneus saevus AW 1 P Araneus thaddeus AW 1 5 2 Mangora maculata AW 1 1 Metepeira labyrinthea AW 7 1 1 Micrathena gracilis AW 111 39 1 1 4 1 Micrathena mitrata AW 77 99 1 2 1 6 Micrathena sagittata AW 1 u Neoscona arabesca AW 1 H Neoscona domiciliorum AW 18 17 1 1 2 1 Neoscona hentzi AW 1 U Wixia ectypa AW 3 2 2 Clubionidae Clubiona spiralis AH 1 Clubionoides excepta AH 1 1 1 5 3 Phrurotimpus alarius GH 1 Scotinella redempta GH 4 Trachelas similis AH 2 3 4 Trachelas sp. A AH 1 R Ctenidae Anahita punctulata GH 1 J Hahniidae GW 1 3 CODDINGTON ET AL.•ESTIMATING SPECIES RICHNESS 127

Appendix.•Continued.

Collection method Sin- gle- Aerial Ground Beating ton Taxon Guild D N D N D N Litter status Hypochilidae pococki GW 2 11 3 Leptoneta gertschi GW 13 7 19 Bathyphantes albiventris GW 1 1 Centromerus denticulatus GW 2 Ceraticelus carinatus GW 1 1 36 Ceraticelus fissiceps AGW 3 51 18 2 Ceraticelus minutus GW 3 Ceratinopsidis formosa AW 3 1 1 53 13 1 Drapetisca alteranda AW 11 8 2 Erigone autumnalis GW 1 J Frontinella pyramitela AW 6 4 1 Gonatium crassipalpum AW 15 2 1 Graphomoa theridioides GW 1 50 32 1 Lepthyphantes sabulosa GW 4 6 6 Lepthyphantes sp. A GW 1 2 Lepthyphantes turbatrix AGW 1 2 Meioneta micaria GW 1 H Meioneta sp. A AW 1 R Neriene radiata AW 2 Neriene variabilis GW 2 1 Pelecopsidis frontalis GW 1 R pallidus GW 1 P brevicornis GW 2 Lycosidae GH 7 3 61 3 Pirata montanus GH 6 1 1 Mimetidae Mimetus interfector AH 1 5 1 1 Mysmena guttata GW 1 J Salticidae Eris marginata AH I 1 8 6 Habrocestum parvulum GH 4 3 Habrocestum pulex GH 1 2 Maevia intermedia AH 1 1 1 8 2 Metaphidippus protervus AH 3 Thiodina sylvana AH 1 8 Tetragnathidae Glenognatha foxi AW 1 H Leucauge venusta AW 9 5 2 1 Meta menardi AGW 1 1 Tetragnatha elongata AW 1 H trigonum AW 2 1 1 1 Euryopis funebris AW 1 1 Paratheridula perniciosa AW 1 P Pholcomma hirsuta GW 1 3 128 THE JOURNAL OF ARACHNOLOGY

Appendix.•Continued.

Collection method Sin- gle- Aerial Ground Beating ton Taxon Guild D N D N D N Litter status Spintharus flavidus AW 1 44 11 18 albidum AW 2 Theridion flavonotatum AW 1 1 Theridion lyricum AW 5 Theridula opulenta AW Theridiosomatidae gemmosum AGW Thomisidae Misumena vatia AH H Xysticus fraternus GH Uloboridae Hyptiotes cavatus AW 7 35 Uloborus glomosus AW 1 U Totals 322 315 222 351 195 113 111