Robert L. Edwards.
Can the species richness of spiders be determined?
Psyche 100:185-208, 1993.

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CAN THE SPECIES RICHNESS OF SPIDERS
BE DETERMINED?
Research Associate, USNM
Box 505, Woods Hole, MA 02543
The jackknife estimate of species richness for spiders in a study area on southwest Cape Cod was 373.1 species, with a confidence interval of 28.2 species. Over a period of six years 390 species had been recorded in that area. Fourteen habitats were sampled using conventional sampling techniques. The sample data for each habi- tat was examined for various aspects of comparability. It is sug- gested that for the purposes of calculating the jackknife estimate of species richness, a minimum number of individuals be collected from each habitat.
Following the development of the species diversity concept by Fisher et al. (1943), the subject has received a great deal of atten- tion by biostatisticians and ecologists. Recently attention has shifted from counting the number of individuals and species in a sample on the assumption that populations were being adequately sampled. Populations are seldom, if ever, uniformly distributed. It is now appreciated that one is usually sampling area, not popula- tions directly (Kempton, 1979; Smith and Grassle, 1977). Cape Cod is richly endowed with spiders. After six years of col- lecting, the number of species I have recorded in Falmouth town- ship, Barnstable County, is 468. Additional species are still showing up (Edwards, 1993). One hundred fifty-eight species were reported associated with rural delivery mail boxes in the nearby township of Mashpee (Edwards et al., 1991); seven of these species have not yet been taken in Falmouth. Martha's Vineyard, an island barely four kilometers south of Falmouth, also has sev- eral species that have not been collected in Falmouth (Thomas Manuscript received 29 April 1993.
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Chase, pers. comm.). The large number of species found in the area of Falmouth township (circa 250 square kilometers) is compa- rable to what one might expect to find in warmer tropical regions. Such species richness provides a useful test area in which to exam- ine certain aspects related to the complex task of estimating species diversity.
Heltshe and Forrester (1983) produced a nonparametric jack- knife estimator for species richness based on quadrat sampling. Computer simulation techniques were used to study the perfor- mance of the jackknife procedure for different quadrat sizes and total area sampled as well as the number of samples (quadrats), coupled with simulated high and low skew populations. Although the confidence interval coverage for highly skewed populations can be very poor and the jackknife underestimates species when the number of rare species is large, it does offer a new and poten- tially useful approach to the estimation of species richness. The results of such simulations are not directly transferable to the field but do provide some general guidance.
This paper briefly explores the variability and species diversity of samples obtained in two study areas. It has the particular goal of estimating the total number of species in one of the study areas (FCWMA). The utility of the jackknife estimator of species rich- ness, J(ESR), of Heltshe and Forrester (1983) is given particular attention.
DESCRIPTION OF THE STUDY AREAS
Spiders were collected in two localities, both in Falmouth town- ship, Barnstable County, Cape Cod, Massachusetts. One locality in East Falmouth was chosen for an extended examination on one habitat. A second locality, the Frances Crane Wildlife Management Area (FCWMA), was chosen to estimate the number of species in an area with a wide array of habitats.
East Falmouth
Sampling was limited to leaf litter of a mixed oak-pine second growth woods (20 hectare). The needle-deciduous leaf litter aver- aged ca. 10 cm in depth, and had a thin layer of decomposed mate- rial at the bottom next to sandy soil. The understory was a spotty mixture of small shrubs (å± m), largely ericaceous heaths. Eleva- tion 15 m, climate as detailed in paragraph below.



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19931 Edwards 187
Frances Crane Wildlife Management Area
This location was chosen for the principal part of the study. The entire 1,255 hectare (ha) area was once farmed. At present it is maintained for multiple recreational purposes. Much of the area is now an older second growth forest about 50 years old. With the exception of one small pond, there are no streams or other bodies of water. The topography is relatively flat; average elevation varies from 20 to 30 meters above sea level. The soils are sandy loams. Annual rainfall ranges from 16 to 20 cm. The annual temperature varies from -2O to 21å¡C Because of the area's proximity to the ocean, spring is relative cool and autumn warm. The principal vegetation and percent total area of FCWMA include: 1) a second growth scarlet and white oak forest (Quercus coccinea and Q. alba) with a well defined, dense understory of waist high ericaceous heaths, dominated by Gaylussacia (ca. 35%); 2) fields dominated by forbs, some with scattered red cedars (Juniperus virginiana) and other introduced and invasive species, (ca. 25%), some of which are periodically cut over or plowed and planted to support various game birds and animals; 3) less defined regions of coniferous woodland dominated by pitch pine (Pinus rigida), and with a substantial 2 m high understory of scrub oak (Quercus ilicifolia) and other large woody shrubs (ca. 15%); and 4) fields dominated by grasses, some maintained as such by mow- ing (ca. 5%). The remainder of the area includes a small pond and its immediate surroundings, power line clearings, roads, paths, and parking lots. There is a great deal of clearly defined 'edge' between each of these components. Within a few kilometers of the FCWMA, there are decidedly different habitats, including those bordering the ocean shore and brackish estuaries. These have dif- ferent assemblages of spiders, and are not included in this study. MATERIALS AND METHODS
East Falmouth
Eighty quadrats (each 0.25 m2) of mixed coniferous-deciduous forest litter (M82L) were sampled. Generally, the underlying con- solidated duff was excluded. Collections were made at weekly intervals, weather permitting, in January and February, 1990, when the duff would normally be frozen. However, following a record cold December (ca. 7OC below normal), January and February



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were unexpectedly warm (4' to 5OC above normal). Consequently some of the samples included small portions of thawed, underlying duff.
Frances Crane Wildlife Management Area
Collecting in the FCWMA took place from the middle of June through September of both 1989 and 1991. This period was chosen to maximize the probability of collecting mature individuals. Some spider species were immature throughout this period and were dif- ficult or impossible to identify to species. Fourteen well defined habitats were chosen. Based on the author's collecting experience, these habitats supported different species assemblages, differed in their physical structure, and were large enough to sustain extensive sampling. The data base codes for each habitat (below in parentheses) are used in some of the fig- ures and graphs.
There was no single sampling technique that could be used for each different habitat. The techniques chosen represented the author's best judgment for selecting the method that provided the greatest probability of taking all species present. Each of the habi- tats was sampled periodically, but not on a strictly random or systematic basis. Each sampling sequence took place in non-over- lapping areas of each chosen habitat. For example, 4 pitfall traps were placed randomly, separated by more than 15 m, in a particu- lar habitat for two cycles of five days, and then moved to the same habitat in a different part of the overall area. Only the grass habitat was too small to avoid some overlap in sampled area. 1. Red cedar foliage (C43S): The cedars sampled included scat- tered trees and small clumps of trees in open fields. Samples were obtained by beating the lower crown foliage. A rectangular plastic pan (surface area of 0.083 m2) was held under branches that com- pletely 'shadowed' the pan. The foliage was then struck sharply with a wooden paddle (7.5 cm X 45 cm), until no more spiders fell. Each quadrat consisted of 12 repetitions of this procedure and represented an area of ca. 1 m2 of foliage. 2. Pitch pine foliage (C40S): The same sampling procedure was used, i.e., beating foliage (see 1 above). 3. Pine understory (C73S): The pine understory is typically made up of large shrubs dominated by scrub oak (Quercus ilicifo- lia), and averaged 2 m in height. Because this shrubbery was too difficult to sweep, it was sampled by beating (see 1 above).



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4. Deciduous understory (D73S): Heaths comprised the under- story of the second growth oak woods, and were swept with a 36 cm diameter canvas sweep net. A set of 50 non-overlapping sweeps of upper plant portions constituted a quadrat. The heaths varied in their coverage of the forest floor from site to site. A set of 50 sweeps was estimated to have sampled a volume of ca. 5 m3. 5. Pitch pine litter (C81L): Litter in the pine woods was domi- nated by pine needles, sometimes exclusively, but occasionally with an admixture of leaves from deciduous plants. It varied in depth from 3.5 to 6 cm with a thin layer (å± cm) of decomposed needles at the bottom. Each quadrat was 0.25 m2 and included material down to the consolidated duff. The collected material was placed in cloth bags for transport to the laboratory, where spiders were sorted out by hand, usually within 24 hours, but always within 48 hours.
6. Deciduous litter (D80L): Sampled as in the case of pine litter (see 5 above). Deciduous leaf litter varied in depth from 4 to 8 cm, and only occasionally had a thin layer of consolidated duff beneath. Typically there was a year-round cover of undecayed oak leaves.
7. Pitch pine forest floor (C81P): Pitfall traps were similar to those described by Houseweart et al. (1979). The funnel had a rim diameter of 20 cm (surface area = 314 cm2), and an elevated cover (ca. 10 cm) provided some protection from rain. The traps were examined every five days, weather permitting. Each five-day col- lection period was defined as a quadrat. Denatured ethanol was used in the trap for preservation. During the study there were sev- eral extended periods of heavy rain, occasionally flooding the col- lecting jar and spoiling the sample. Only those samples taken during periods with no significant rain were used. The traps were frequently upset by animals, including humans, thus rendering the sampling procedure both time consuming and frustrating. 8. Deciduous forest floor (D80P): Pitfall traps and procedure same as in pine woods floor (see 7 above). 9. Old field ground surface (F31P): Sampled with pitfall traps; procedure same as in pine woods (see 7 above). These old fields were dominated by forbs, typically Compositae and Umbelliferae, and had minimal litter at ground level. Some fields were being invaded by cedars, pitch pine, and Russian olive (introduced).




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10. Grass field ground surface (F30P): Pitfall traps and collec- tion procedures same as in pine woods (see 7 above). The grass dominated fields were of two types: successional grasses with interspersed patches of reindeer lichen which dominated the sur- faces of old gravel and sand borrow pits, and areas maintained as grass by seasonal mowing.
1 1. Grass field foliage (F30S): Fields dominated by grasses (35-70 cm in height), were swept with a 36 cm canvas sweep net. Each quadrat consisted of 50 non-overlapping sweeps. Areas with widely separated grassy clumps and those regularly mowed were avoided.
12. Old field foliage (F31S): Same procedure as in grass fields (see 11 above). Forbs dominated these fields and all were densely vegetated. The plants varied in height (0.3 to 1.5 m). 13. Oak tree trunks (D47T): Only white oaks were sampled. The trunks of white oaks are usually smooth with scattered patches of moss and lichen. Two methods of collecting were used simulta- neously, First, a 15 by 45 cm band of burlap, folded over length- wise and with the open side down, was stapled to each tree trunk sampled ca. 1 m above the ground. This procedure was used to attract spiders that inhabit the deep hollows and crevices of tree trunks. Second, a 0.2 m2 area of each sampled trunk was swept with a broad (15 cm), relatively stiff whitewash brush. Sampled trunk areas were 1.5 to 2.5 m above ground. A plastic pan was held underneath to catch the spiders as they were dislodged. Each quadrat consisted of five burlap strips and five trunk sweepings. 14. Pitch pine trunks (C40T): Pitch pines have scaly, rough, thick, and easily removed outer bark. A quadrat consisted of 1 m2 of outer bark (pried and scraped off with a trowel) taken from 3 to 5 trees in close proximity. The collected bark was broken up to expose and collect any spiders. Bark removal was followed by a careful examination of the trunk surface. This procedure was not feasible for smooth-barked pines (e.g., white pine). All active collecting (e.g., sweeping and beating) was carried out in the afternoon. Specimens were preserved in 75% denatured ethyl alcohol. Each individual was identified to species if possible; otherwise, to genus. Specimens that could not be identified to species were saved until all material had been studied. Each indi- vidual was then carefully compared and identified as being the same or a different species. In most cases where individuals could



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not be identified as a particular species, such specimens occurred in more than one quadrat, and were not counted as unique. Aggre- gations of the earliest instars-e.g., lycosid spiderlings taken with a female; aggregations of recently hatched, but not yet dispersed spiderlings-were excluded from the counts. The jackknife species diversity equation developed by Heltshe and Forrester (1983) was used for this study. The equation is: where, J(ESR) = Jackknife estimate of species richness, s = total number of species observed in all quadrats, n = number of quadrats sampled, and k = number of unique species. The equation for calculating variance is: where, varJ(ESR) = variance of jackknife estimate of species rich- ness, j = number of quadrats with f unique species, and f = number of unique species in a quadrat.
The confidence limits for J(ESR) are obtained by: where, t = Student's t value for n-1 degrees of freedom. The term 'unique' is defined as a species that occurs in only one quadrat, regardless of how many individuals may be involved. The J(ESR) equation cannot provide an estimate in excess of twice the number of species in a sample. Further, note that the sum of the number of species plus the number of species that are unique closely approximates the estimate of species richness. The failure to include a non-unique species decreases the J(ESR) by 1 (approximately); adding a species incorrectly increases J(ESR) by +1 (approximately). The error in J(ESR) when a unique species is incorrectly included is +2 (approximately) since this increases both the observed number of species and number of uniques. In the case



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192 Psyche [vo~. 100
of spiders the greatest source of error would probably lie in failing to recognize an immature as a unique species. East Falmouth samples
Eighty litter quadrats (each 0.25m2) were collected in sets of 10 at weekly intervals during January and February, 1990. In all, 2 16 1 specimens were taken, representing 98 species and 71 genera. The purpose of this collection was to examine the behavior of the para- meters of the jackknife estimator with a large number of samples from a single, well defined habitat. The winter period was chosen to reduce bias created by active movements of spiders from area to area.
Jackknife estimates of numbers of species for each succeeding set of ten quadrats are provided in Fig. 1 and Table 1A. The J(ESR) ranged from 48.7 to 67.5 species, with considerable varia- tion in estimates and variances among sets. For all 80 quadrats, Ì
-.*.-.
J (ES R)
... 'H
NO. OF UNIQUES
1 1 -20 31 -40 51 -60 71 -80
QUADRATS
Figure 1. Species richness estimates, J(ESR), and number of unique species for each successive set of 10 samples. Bars indicate confidence interval limits. Litter samples from a mixed pine-oak forest, East Falmouth, January-February, 1990.



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NO. SPECIES
OBSERVED
4oK I I I I I I
10 20 30 40 50 60 70
NUMBER OF QUADRATS
Figure 2. Species richness estimates, J(ESR), and species-effort curve for East Falmouth quadrats, accumulated by 10's. Litter samples from a mixed pine-oak for- est, East Falmouth, January-February, 1990. J(ESR) is 122.7 species, with a variance of 18.9 and a confidence interval of 8.7 (Table 1B).
J(ESR) leveled off after 50 quadrats at about 120 species (Fig. 2). This suggests that 50 quadrats provided an adequate sample for this particular habitat. However, the number of species (species- effort curve) was still slowly increasing after 80 quadrats. FCWMA samples
Over 12,000 individuals, representing 147 genera and 304 species, were collected. Percentage representation by number of individuals of the twelve most abundant families of spiders in each habitat detailed above are shown in Fig. 3. The spider assemblages may be divided into three main groups: 1) those on vegetation above ground (first six habitats); 2) those inhabiting vertical sur- faces, in FCWMA tree trunks (last two habitats); and 3) those liv- ing on or in material on the ground (middle six habitats). Erigonine spiders, particularly one species of the genus Ceraticelus, tend to dominate in the foliage of trees and understory shrubbery, with salticids and orb weavers also well represented. The two field habitats, grass and old field, are a distinctive subgroup of this first



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group, with relatively greater numbers of orb weavers (several genera and species). Both tree trunk habitats were dominated by relatively large numbers of comb-footed spiders, genera Theridion, Euryopis and Dipoena. The trunks of pitch pine (C40T) harbor large numbers of one philodromid species, Philodromus validus (Gertsch) and a thomisid spider species, Coriarachne versicolor Keyserling. The latter two species were seldom found on oak trunks (D47T). Wolf spiders (several genera and many species) characterized the surface habitats, especially those of fields (F31P, F30P). Litter habitats (D80L, C81L) were dominated by several erigonine genera.
C40S D73S F31S C81 L C81 P F30P C40T
HABITAT
SALTICIDAE PISAURIDAE GNAPHOSIDAE
LYCOSIDAE THERIDIIDAE ERIGONINAE
OXYOPIDAE IpsIJ AGELENIDAE THOMISIDAE
CLUBIONIDAE AFNNEIDAE @ PHILODROMIDAE
Figure 3. Percent representation of twelve of the most abundant families in each habitat. Percentages of less than 2.0 were not included. Habitats arrayed by eye. FCWMA samples.




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At the generic and species level, however, these habitats were not as similar as they might have appeared to be at the family level (Fig. 3). A phenogram (UPGMA), based on the modified Morisita similarity coefficient (Horn, 1966), provides a quantitative mea- sure of species similarity among habitats (Fig. 4). The three main groups mentioned above are clearly separated in the phenogram. Pine foliage (C40S) and pine understory (C73S) were relatively open environments, spatially close to one another, and had more species in common than any other set of habitats. The two tree trunk habitats (D47T, C40T) were quite different, having less than 25% of species in common. The relative similarity of old field (F3 1 P) and coniferous pitfall (C8 1P) assemblages may be a func- tion of the generally uncluttered ground surface (cf. Uetz, 1979). The forest surface habitats (D80P, C81P) did not share many species with the immediately adjacent litter (D80L, C81L), less than 50% in both cases.
Figure 4. Phenogram (unweighted pair-group method, arithmetic average) based on species using Horn's (1966) modification of Morisita's similarity coefficient, showing the relationships among the FCWMA study area habitats. Cophenetic matrix correlation = 0.9379.




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Sample comparability
Different sampling techniques were used depending upon the physical characteristics of each habitat. There is no single, logisti- cally feasible sampling technique that can be used for the array of habitats sampled. For the purposes of calculating J(ESR), there is no formal basis for quantifying the comparability of sample data between different types of habitats. Despite this, some generaliza- tions may be helpful in making such judgments, to the end that future studies might be improved.
Statistical data for the FCWMA habitats are provided in Table 2. The data are arrayed in decreasing order of number of individu- als collected. The series of ratios provided in the table were col- lected to examine how the difference in the number of individuals collected may have influenced other parameters. The ratio of unique species to species, (UlIS), shows a general increase associated with a decrease in the number of individuals (r2 = 0.661). This trend is also reflected in the increase of unique species found as the number of individuals decreases, (UllI) (r2 = 0.611). The number of unique species found in collections of spi- ders both here and in Costa Rica (Edwards, unpubl.) typically varies from 30 to 50 percent of the total. The number of species unique to specific habitats are listed in Table 2, column U2. These averaged 5.1 specieslhabitat, with the deciduous pitfall samples having none and the white oak trunks only 1. This suggests that these habitats offered little to specialists. In the case of the white oak trunk, the single unique species, Drapetisea alteranda Chamberlin, was a specialist and has been taken only on other smooth barked trees outside of the study area, for example beech. Coniferous litter and grass field pitfall trap samples had the largest number of unique species, 14 and 9 respec- tively.
Unique species that occurred in only one of the 509 quadrats, column U3 in Table 2, averaged 2.9 per habitat. Old field pitfall traps declined most relative to the number unique to that habitat, from 6 to 2. Four of these species had occurred in more than one quadrat, 2 in only one. Those unique to the deciduous understory habitat, 3, continued to be unique overall since each occurred in only one quadrat. These numbers do provide some insight into the specificity of the different habitats. However, given the proclivity



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Table 2. Collection data for FCWMA samples, arrayed by number of individuals in descending order. Ul - Unique species within habitat; U2 - Unique species when habitat treated as a single quadrat; and U3 - Unique species when all quadrats considered singly (without regard to habitat); I - number of individuals in sample; S - number of species; G - number of genera. Habitat
Cedar foliage
Coniferous litter
Deciduous understory
Deciduous litter