PHYSIOLOGICAL ECOLOGY Effect of Diet on Development and Reproduction of the Harvestman opilio (: )

1 CORA M. ALLARD AND KENNETH V. YEARGAN

Department of Entomology, University of Kentucky, Lexington, KY 40546

Environ. Entomol. 34(1): 6Ð13 (2005) Downloaded from https://academic.oup.com/ee/article/34/1/6/478711 by guest on 29 September 2021 ABSTRACT The harvestman Phalangium opilio L. is an abundant predator in an array of , including agricultural systems. In these systems, P. opilio has been noted to feed on pest (e.g., Colorado potato beetle larvae, various aphid species, and lepidopteran eggs). Although the potential importance of P. opilio has been recognized, little is known about this harvestmanÕs development or reproductive biology. We investigated the inßuence of diet on development time, survival, repro- duction, and female longevity. We compared the effects of two diets, (Boddie) eggs and Aphis glycines Matsumura, on development of P. opilio because this predator is known to feed on those prey in soybean agroecosystems. Individuals fed A. glycines from emergence to adulthood suffered from higher mortality, longer development time, and smaller body size than those fed H. zea eggs. Four diet treatments were used in a separate study to test their effects on reproduction: standard laboratory diet (cornmeal, bacon, and H. zea eggs), H. zea eggs only, A. glycines only, and mixed diet (A. glycines and H. zea eggs). A diet of A. glycines alone yielded higher mortality, smaller body size, and lower fecundity than the standard laboratory diet. The presence of A. glycines in a monotypic or mixed diet lengthened the preoviposition period compared with diets without this prey and yielded a smaller Þrst clutch and smaller average clutch sizes compared with the standard laboratory diet. A. glycines is detrimental to the growth and reproduction of this predator.

KEY WORDS predator, Arachnida, Helicoverpa zea, Aphis glycines

MEMBERS OF THE ORDER Opiliones (Arachnida) are om- nigripes Weed, Leiobunum vittatum (Say), Leiobunum nivorous, but their diet consists primarily of small, politum Weed, Leiobunum calcar (Wood), and Hadro- soft-bodied organisms (Sankey and Savory 1974). As bunus maculosus (Wood)] was earthworms (Halaj predators, primarily at night, harvestmen consume and Cady 2000). Opilionids have been observed con- other harvestmen, gastropods, small earthworms, mil- suming eggs of the corn earworm, Helicoverpa zea lipedes, spiders, mites, earwigs, ßies, springtails, (Boddie) (Lepidoptera: Noctuidae), in soybean Þelds aphids, leafhoppers, and additional types of insects in Kentucky. Pfannenstiel and Yeargan (2002) found (Bristowe 1949, Sankey 1949, Sankey and Savory 1974, that opilionids in the family Phalangiidae were the Nyffeler and Symondson 2001). The prevalence of third most frequent predators on H. zea eggs in Ken- opilionids in agroecosystems has been noted in pre- tucky soybean Þelds in 1993 and the second most vious studies. Predation by opilionids has been re- frequent predators in 1994. Another study in Kentucky ported in agricultural and horticultural systems found that opilionids were the second most frequent (Ashby and Pottinger 1974, Leathwick and Winter- predators of H. zea eggs, next to damsel bugs, Nabis bourn 1984, Brust et al. 1986, Butcher et al. 1988, spp. (Hemiptera: Nabidae) (Anderson 1996). Newton Drummond et al. 1990, Clark et al. 1994, Sivasubra- and Yeargan (2002) found that P. opilio represented maniam et al. 1997, Halaj and Cady 2000, Pfannenstiel Ϸ96% of the opilionid fauna in Kentucky soybeans and Yeargan 2002), orchards (Carroll 1982), wood- during a 2-yr study; thus, it is probable that P. opilio lands (Adams 1984), and urban environments (Hanks was the opilionid most frequently observed in the and Denno 1993). earlier studies by Anderson (1996) and Pfannenstiel Studies conducted in the midwestern United States and Yeargan (2002). have elucidated the feeding behavior of opilionids in The quality of prey can impact the Þtness of a soybean Þelds. In Ohio soybean Þelds, the most com- predator. In the wolf spider genus Schizocosa, prey mon prey item for Þve opilionid species [Leiobunum quality was determined indirectly by measuring the effect of prey on different life history traits of the spiders (e.g., survival and development) (Toft and 1 Corresponding author: Department of Entomology, University of Kentucky, S-225 Ag Science North, Lexington, KY 40503 (e-mail: Wise 1999). Schizocosa species that fed on the collem- [email protected]). bolan, Tomocerus bidentatus Folsom (Collembola:

0046-225X/05/0006Ð0013$04.00/0 ᭧ 2005 Entomological Society of America February 2005 ALLARD AND YEARGAN:PREDATORÕS DIET 7

Entomobryidae), exhibited high rates of survival and which were the components of our standard labora- development. Schizocosa that were fed intermediate- tory diet. Food was provided by placing into the con- quality prey, Drosophila melanogaster Meigen (Diptera: tainer a small piece of paper (Ϸ3 by 3 cm) on which Drosophilidae), initially had good rates of survival and H. zea eggs had been oviposited and sprinkling the development, but rates declined over time. Diets con- cornmeal and bacon bits onto the paper. Water was sisting of low-quality prey (i.e., sciarid gnats or conspe- provided in a 9-ml vial held at a 45Њ angle by sculpting ciÞc spiders) resulted in impeded rates of development compound (Super Sculpey), with a cotton wick in- and low survival (Toft and Wise 1999). Similarly, the serted into the opening of the vial. High humidity was predator Geocoris punctipes (Say) (Hemiptera: Geoco- maintained by placing open containers of water in the ridae) survived four times longer when fed H. zea bottom of the incubators. Similar conditions have eggs than when fed Acyrthosiphum pisum (Harris) been used to successfully rear P. opilio (Bachmann and (Hemiptera: Aphididae) (Eubanks and Denno 2000). Schaefer 1983). Each pair was provided with ovipo- P. opilio is a polyphagous forager and, with its diverse sitional substrate that consisted ofa5by1-cm (diam- range, it encounters a broad array of prey species, eter by height) dish Þlled with sterile soil anda1by Downloaded from https://academic.oup.com/ee/article/34/1/6/478711 by guest on 29 September 2021 including aphids. In general, aphids are considered to be 1 by 1-cm piece of ßoristÕs foam (green) on the soil low-quality prey for many arthropod predators (Bilde surface. The ovipositional substrate was moistened and Toft 1994, Toft 1995). and checked for eggs daily. Eggs were clearly visible We have observed P. opilio feeding on the soy- on lifting the piece of foam, because virtually all eggs bean aphid, Aphis glycines Matsumura (Hemiptera: were laid at the foamÐsoil interface. In the event of Aphididae), an Asian pest species recently found in oviposition, the ovipositional substrate was replaced , including Kentucky. As noted above, with an identical new substrate, and the substrate with P. opilio also feeds on H. zea eggs in Kentucky soybean eggs was placed into a 8.5 by 1.5-cm (diameter by Þelds (Pfannenstiel and Yeargan 2002). In the labo- height) petri dish. Eggs were incubated under the ratory, P. opilio has been successfully reared on a same temperature and photoperiod described above mixed diet of cornmeal, bacon, and lepidopteran eggs for maintaining adults. If no oviposition occurred (Newton and Yeargan 2001). In the study reported within 7 d, the ovipositional substrate was replaced here, our primary objective was to compare the suit- with new substrate on the seventh day as a precaution ability of A. glycines with that of H. zea eggs as prey for against growth of mold or other contaminating organ- P. opilio. We compared effects of H. zea eggs versus isms. Clutches of eggs were monitored daily and A. glycines on the development and survival of im- sprayed with water every other day. mature P. opilio in the laboratory. In a separate labo- Diet and Development. On eclosion, Ϸ20 offspring ratory experiment, we evaluated P. opilio reproduc- from each of 16 Þeld-collected females were assigned tion and adult female longevity on four different diets: to a diet treatment of H. zea eggs or a diet treatment A. glycines, H. zea eggs, a mixed diet of A. glycines and of A. glycines. All females contributed a similar pro- H. zea eggs, and the standard laboratory diet consisting portion of offspring to each diet treatment (i.e., 3:1 to of cornmeal, bacon, and lepidopteran eggs. the respective treatments). Approximately three times as many offspring were assigned to the aphid diet (231) as were assigned to the egg diet (78) be- Materials and Methods cause we anticipated higher nymphal mortality on the Laboratory colonies of both H. zea and A. glycines aphid diet. were maintained at the University of Kentucky for Harvestmen were housed individually in 8.5 by each experiment. H. zea was maintained using meth- 1.5-cm petri dishes in incubators set at the same con- ods similar to those of Ignoffo (1965). A colony of ditions as described above. On reaching the Þfth in- A. glycines was kept on soybean in a greenhouse at star, they were transferred individually into 8.5 by 16:8 (L:D) and 24Ð30ЊC. The amount of prey provided 8.5-cm paper cartons with petri dish bottoms placed always exceeded the predatorÕs daily consumption in inside the base of the cartons. The tops of the paper both experiments. cartons were covered with plastic wrap, and each For both experiments, P. opilio were collected at the carton top was covered with one-half of a cardboard University of KentuckyÕs North Farm near Lexington, lid to provide partial shade from the incubator lights. KY. Field-collected individuals were either large Harvestmen were reared from egg eclosion until adult nymphs, which were reared to maturity in the labo- emergence or until nymphal mortality occurred. In- ratory, or adults. In the laboratory, adult males and dividuals were checked daily for molts and mortality. females were paired and housed in large petri dishes, Water was supplied in the same manner as described 15 by 4 cm (diameter by height), with mesh-covered above for adult P. opilio and was refreshed as needed. holes (9 cm diameter) in the tops. Males and females Live A. glycines (Ϸ100) were provided on an ex- were distinguished by the presence (on males) or cised soybean leaf to individuals in the A. glycines diet absence of a prominent apophysis on the distal seg- treatment. Before introducing the soybean leaf and ment of the chelicera. Pairs were provided with food aphids into the P. opilio containers, the leaves were and water and were stored in incubators at 24 Ϯ 1ЊC examined under a microscope, and parasitized aphids, (15:9 L:D). Food for each pair consisted of Ϸ0.2 g thrips, spider mites, and other nonaphid organisms cornmeal (Quaker Oats), Ϸ0.25 g bacon (Real Bacon were removed. P. opilio in the H. zea egg diet treat- Bits; Hormel Foods, Austin, MN), and 50 H. zea eggs, ment were fed Ϸ100 frozen H. zea eggs on a small 8ENVIRONMENTAL ENTOMOLOGY Vol. 34, no. 1 piece of white paper (cut from a larger sheet on which containers, occurred as needed. Between 7 and 20 d they had been oviposited). Fresh eggs were killed (by after adult emergence, males and females from the freezing) to prevent emergence of Þrst-instar cater- same treatment were paired and housed in the manner pillars. Old prey were replaced with fresh prey every previously described for Þeld-collected male/female other day. pairs. Monitoring and recording of data (date of ovi- Mortality was recorded in each treatment, and position, clutch number, clutch size, interval between when individuals reached adulthood, their sex and the clutches, and female longevity) occurred daily until date were recorded. Cephalothorax width of adults female death. Females were preserved in 70% ethanol from each treatment was determined by measuring immediately on discovery, and their cephalothorax the distance between the third pair of coxae with an width was determined by measuring the distance be- ocular micrometer. tween their third pair of coxae. Diet and Reproduction. Phalangium opilio were Statistical Analyses. For the diet and development reared from the beginning of the seventh (ϭpenulti- experiment, mortality was analyzed witha2by2 mate) instar until their death on four different diets contingency table (dead or alive; H. zea eggs or Downloaded from https://academic.oup.com/ee/article/34/1/6/478711 by guest on 29 September 2021 (i.e., only A. glycines, only H. zea eggs, a mixed diet of A. glycines) using ␹2. For surviving individuals, A. glycines and H. zea eggs, or the standard laboratory time required for development was analyzed by ranks diet of cornmeal, bacon, and H. zea eggs). Before the using a one-way analysis of variance (ANOVA; SAS seventh instar, all individuals were reared on the stan- Institute 2000), and the size of both sexes of adults was dard laboratory diet. In this experiment, we were pri- analyzed using a two-way ANOVA (SAS Institute marily interested in the effect of diet on reproduction 2000), using Box-Cox transformed data (Sokal and (interval between adult emergence and Þrst oviposi- Rohlf 1995). tion, number and size of clutches, interval between For the diet and reproduction experiment, ANOVA clutches) and adult female longevity. These traits was used to analyze all data except mortality. Data that likely reßected effects of diet during both the seventh did not meet the assumptions of ANOVA were trans- instar and the adult stage. We also recorded mortality formed using Box-Cox transformation (Sokal and that occurred during the seventh instar and the size of Rohlf 1995). Asymmetric distributions were Box-Cox adult females, which solely reßected the effect of the transformed using the procedure TRANSREG in SAS diet treatments during the seventh instar. (SAS Institute 2000). If, after Box-Cox transformation, On emergence, Þrst-instar offspring from Þeld-col- the ANOVA assumptions were not met, the data were lected individuals were randomly assigned to one of transformed to ranks, and an ANOVA was performed four diet treatments, although they did not receive on the ranked data. This procedure, which was used those treatments until they reached the seventh instar. for preoviposition period, female longevity, and num- They were housed individually in the same environ- ber of clutches, is a good alternative to common non- mental conditions as experimental subjects in the de- parametric statistical tests because it maintains the velopment experiment described earlier. Offspring power of parametric tests (Conover and Iman 1981) used in the experiment came from a total of 22 females, and allows the inclusion of additional factors that can- with each female contributing Ϸ5 individuals to each not be included in a Kruskal-Wallis test (Siegel and treatment, for a total of Ϸ110 Þrst instars per treatment Castellan 1988). This was necessary because there (of which 37Ð50 individuals per treatment survived to were signiÞcant block effects that needed to be cor- the beginning of the seventh instar). All individuals rected by including a block factor in some analyses. If were fed the same standard laboratory diet until the ANOVAs were signiÞcant, they were followed by a beginning of the seventh instar, i.e., a mixture of corn- posthoc Bonferroni test (i.e., least signiÞcant differ- meal, bacon, and H. zea eggs. From the beginning of ence [LSD] with Bonferroni correction) (Rice 1989). the seventh instar until their death, individuals were After transformation to ranks, preoviposition period provided their assigned diet treatment: only A. glycines data were analyzed with an analysis of covariance (n ϭ 42), only H. zea eggs (n ϭ 37), a mixed diet of (ANCOVA) to control for the confounding effects of A. glycines and H. zea eggs (n ϭ 47), or the standard date of pairing; date of pairing was included as the laboratory diet of cornmeal (Ϸ0.2 g), bacon (Ϸ0.25 g), covariate in this analysis. Mortality during the penul- and H. zea eggs (n ϭ 50). The amount of A. glycines and timate instar was analyzed witha2by4contingency H. zea eggs and the manner in which they were pro- table (dead or alive; four diet treatments). Linear vided to P. opilio were the same as in the development regression analyses were used to correlate female fe- experiment. In the mixed diet, aphids and H. zea eggs cundity with female size for each diet treatment and were provided in amounts equivalent to the mono- for all treatments combined. typic aphid diet plus the monotypic H. zea egg diet. We did not attempt to quantify the amount of food con- Results sumed in any treatment, but it was apparent from observations of surviving prey that predators in the Diet and Development. Mortality from eclosion mixed diet treatment consumed both types of prey. through the last nymphal instar was signiÞcantly dif- Food was replenished every other day. Some main- ferent for the diet treatments of H. zea eggs and tenance (i.e., checking for molts and ovipositional A. glycines (␹2 ϭ 30.9; df ϭ 1; P Ͻ 0.001). P. opilio that substrate maintenance) occurred every day; other fed on a monotypic diet of A. glycines suffered higher maintenance, such as providing water and cleaning mortality than those fed on a monotypic diet of H. zea February 2005 ALLARD AND YEARGAN:PREDATORÕS DIET 9 Downloaded from https://academic.oup.com/ee/article/34/1/6/478711 by guest on 29 September 2021

Fig. 2. Width of adult P. opilio cephalothorax (mm) when reared on H. zea eggs or soybean aphids (A. glycines) (mean Ϯ SE). Means were signiÞcantly different between treatments and between sexes within treatments (P Ͻ 0.05, LSD with Bonferroni correction).

0.002). Females in both the monotypic and mixed diet treatments containing A. glycines had a signiÞcantly longer preoviposition period (time from adult emer- gence to Þrst oviposition) than those in diet treat- ments that did not contain aphids (Fig. 4A).

Fig. 1. Effect of diet on P. opilio (A) percentage mortality suffered during development and (B) time from eclosion to adult emergence (d; mean Ϯ SE). Eggs, H. zea eggs; aphids, A. glycines. *SigniÞcant differences between treatments (P Ͻ 0.05, ␹2 and LSD with Bonferroni correction, respectively). eggs (Fig. 1A). The diet treatments had a signiÞcant effect on the rate of development for P. opilio (ANOVA by ranks; F ϭ 136.72; df ϭ 1,61; P Ͻ 0.001). Individuals fed A. glycines required almost twice as long to mature as those fed H. zea eggs (Fig. 1B). There was a signiÞcant difference in the size of the newly emerged adults that had developed in different diet treatments (F ϭ 258.21; df ϭ 1,61; P Ͻ 0.001; Box-Cox transformation with ␭ ϭϪ1). Individuals fed a mo- notypic diet of H. zea eggs had a larger body size than those that fed on a monotypic diet of A. glycines; females were larger than males regardless of diet (Fig. 2). Diet and Reproduction. Mortality, measured from the beginning of the seventh instar to the adult stage, was marginally different among diet treatments (␹2 ϭ 7.69; df ϭ 3; P ϭ 0.053). Greatest mortality occurred in the monotypic A. glycines diet, and there were no apparent differences in seventh-instar mortality among the other three treatments (Fig. 3A). There was a signiÞcant treatment effect on adult female size (F ϭ 6.716; df ϭ 3,59; P Ͻ 0.001) as a result of diet treatment during the seventh instar. Females Fig. 3. Effect of four diet treatments on P. opilio (A) percentage mortality suffered in the seventh instar and fed only A. glycines had a signiÞcantly smaller cepha- (B) width of adult female cephalothorax (mm; mean Ϯ SE). lothorax width than females fed the standard labora- Bars that do not share the same letter are signiÞcantly dif- tory diet of cornmeal, bacon, and H. zea eggs (Fig. 3B). ferent (P Ͻ 0.05, LSD with Bonferroni correction). Aphids, Preoviposition period was signiÞcantly affected by A. glycines; eggs, H. zea eggs; mixed, aphids and eggs; stan- diet (ANCOVA by ranks; F ϭ 5.58; df ϭ 3,83; P ϭ dard, cornmeal, bacon bits, and H. zea eggs. 10 ENVIRONMENTAL ENTOMOLOGY Vol. 34, no. 1 Downloaded from https://academic.oup.com/ee/article/34/1/6/478711 by guest on 29 September 2021

Fig. 4. Effect of four diet treatments on P. opilio (A) preoviposition period (least squares mean Ϯ SE), (B) number of eggs in the Þrst clutch (mean Ϯ SE), (C) number of clutches laid per female (mean Ϯ SE), (D) average clutch size (mean Ϯ SE), (E) lifetime fecundity (mean Ϯ SE), and (F) adult female longevity (mean Ϯ SE). Sample sizes for all six graphs are 20, 21, 22, and 25 for the respective bars left to right. Bars within a graph that do not share the same letter are signiÞcantly different (P Ͻ 0.05, LSD with Bonferroni correction). Letters over bars were omitted if ANOVA indicated no signiÞcant differences (P Ͼ 0.05). Diet treatments are the same as those in Fig. 3.

Diet treatment signiÞcantly affected the number of transformation with ␭ ϭ 0.25). Females fed only A. gly- eggs laid in the Þrst clutch (F ϭ 3.385; df ϭ 3,83; P ϭ cines had signiÞcantly lower fecundity compared with 0.022; Box-Cox transformation with ␭ ϭ 0.25). Females those fed the standard laboratory diet (Fig. 4E). fed a standard laboratory diet had a signiÞcantly larger Female longevity (from adult emergence to death) Þrst clutch compared with either of the diets that was not affected by treatment (F ϭ 0.8811; df ϭ 3,83; contained A. glycines, while the monotypic diet of P ϭ 0.456). Females lived Ϸ6Ð8 wk regardless of diet H. zea eggs was intermediate and not signiÞcantly (Fig. 4F). Linear regression showed no signiÞcant different from any other diet (Fig. 4B). Statistical relationship between female size and longevity (F ϭ analysis of the effect of diet treatment on number of 2.05; df ϭ 1,61; P ϭ 0.157). clutches laid per female produced equivocal results; There was a signiÞcant correlation between body ANOVA (by ranks; F ϭ 2.751; df ϭ 3,83; P ϭ 0.048) size and fecundity (r ϭ 0.4443, P Ͻ 0.001), in that indicated a signiÞcant effect, but means comparisons larger females laid more eggs (Fig. 5). When female (LSD) showed no signiÞcant differences in number of size was included as a covariate in an ANCOVA com- clutches among diet treatments after data were Bon- paring the difference in fecundity among treatments, ferroni corrected (Fig. 4C). There was, however, a the signiÞcance of the treatment effect disappeared trend of females that were fed the monotypic diets (F ϭ 1.51; df ϭ 3,58; P ϭ 0.221), suggesting that the (i.e., only A. glycines or only H. zea eggs) to lay a fewer observed differences in fecundity were caused by the number of clutches than females fed the mixed diet or effect of diet on female body size. The ANCOVA standard laboratory diet (Fig. 4C). showed there was no signiÞcant treatment by size Average clutch size was signiÞcantly affected by diet interaction (F ϭ 0.17; df ϭ 3,55; P ϭ 0.915), indicating (Fϭ37.526; df ϭ3,83; PϽ0.001; Box-Cox transformation the slopes of the regression lines are not signiÞcantly with ␭ ϭ 0.25). Treatments that included A. glycines (i.e., different from each other. only aphids or A. glycines mixed with H. zea eggs) had signiÞcantly lower average clutch sizes than those fed the Discussion standard laboratory diet (Fig. 4D). Diet treatment sig- niÞcantly affected fecundity (total number of eggs laid Several factors affect the development and repro- per female; F ϭ 3.676; df ϭ 3,83; P ϭ 0.016; Box-Cox duction of predators, including the quality and com- February 2005 ALLARD AND YEARGAN:PREDATORÕS DIET 11 Downloaded from https://academic.oup.com/ee/article/34/1/6/478711 by guest on 29 September 2021

Fig. 5. Regression of P. opilio lifetime fecundity on female body size for four diet treatments and for combined data. Diet treatments are the same as those in Fig. 3. plexity of diet. Some predators may incur low survival, better than those fed the other diets. Compared with long developmental periods, and lower fecundity this diet, the adverse effects of a monotypic diet of when they feed on low-quality prey (Toft and Wise H. zea eggs on P. opilio life history traits were less 1999). Toft (1995) found that the linyphiid spider severe than those seen with a monotypic diet of Erigone atra (Blackwall) had increased reproductive A. glycines. Mixing H. zea eggs with aphids seemed to success when fed a mixed diet compared with a mo- partially ameliorate the negative effects of the mono- notypic diet, and he hypothesized that the effect of typic aphid diet. Our results seem to support the con- dietary mixing depends on the quality of the prey tention of Toft (1995) that effects of dietary mixing species being mixed. Atypena formosana (Oi), another depend on the quality of the prey species being mixed. linyphiid, also experienced higher fecundity when fed Lepidopteran eggs generally are considered to be a mixed diet compared with a diet of only Collembola higher-quality prey than aphids (Eubanks and Denno (Entomobryidae) (Sigsgaard et al. 2001). In general, 2000), but few studies have directly compared the these studies suggest that mixed diets are better than nutritional composition of these two prey groups. monotypic diets for reproduction, although the qual- Specty et al. (2003) analyzed the protein, lipid, and ity of the prey species involved can inßuence the carbohydrate content of the aphid Acyrthosiphon pi- effects of a mixed diet. sum (Harris) and eggs of the lepidopteran Ephestia Phalangium opilio incurred higher mortality, longer kuehniella Zeller. They found the lepidopteran eggs developmental periods, and smaller adult body size were two times richer in amino acids and three times when fed a monotypic diet of A. glycines. Fecundity richer in lipids than the aphids, whereas the aphids also was compromised when fed A. glycines. A mixed were 1.5 times richer in glycogen. If the biochemical diet containing A. glycines caused some adverse effects composition of the prey used in our study follows this on reproduction compared with the standard labora- pattern, differences in nutritional composition of the tory diet, which did not contain aphids. P. opilio reared prey could account for the superior performance of on the standard laboratory diet, which was the most P. opilio on H. zea eggs compared with soybean aphids. complex diet tested, generally performed equal to or We cannot rule out, however, the possibility that soy- 12 ENVIRONMENTAL ENTOMOLOGY Vol. 34, no. 1 bean aphids may possess chemicals that have toxic Brust, G. E., B. R. Stinner, and D. A. McCartney. 1986. effects on P. opilio. Predation by soil inhabiting in intercropped In spiders, there is a positive correlation between and monoculture agroecosystems. Agric. Ecosyst. female body size and female fecundity, both within Environ. 18: 145Ð154. species (Petersen 1950, Enders 1976, Beck and Connor Butcher, M. R., D. R. Penman, and R. R. Scott. 1988. Field 1992, Wagner and Wise 1996, Arnqvist and Henriksson predation of twospotted spider mite in a New Zealand strawberry crop. Entomophaga. 33: 173Ð183. 1997) and across species (Marshall and Gittleman Carroll, D. 1982. Studies on apple aphid and its natural 1994, Simpson 1995). We found a similar correlation enemies in Central Washington. Proc. Wash. State between female P. opilio size and fecundity. Our Entomol. Soc. 44: 633Ð635. ANCOVA indicated that the negative impact of Clark, M. S., J. M. Luna, N. D. Stone, and R. R. Youngman. A. glycines on predator fecundity was mediated 1994. Generalist predator consumption of armyworm through this prey speciesÕ effect on female body size. (Lepidoptera: Noctuidae) and effect of predator re- Overall, our study showed that A. glycines was det- moval on damage in no-till corn. Environ. Entomol. 23: rimental to several Þtness traits of P. opilio, including 617Ð622. Downloaded from https://academic.oup.com/ee/article/34/1/6/478711 by guest on 29 September 2021 some traits that were compromised even when the Conover, W. J., and R. L. Iman. 1981. Rank transformations aphids were mixed with lepidopteran eggs. While it is as a bridge between parametric and nonparametric sta- tistics. Am. Statist. 35: 124Ð129. unlikely that P. opilio would typically feed on a mo- Drummond, F., Y. Suhaya, and E. Groden. 1990. Predation notypic diet in the Þeld, this predator may consume on the Colorado potato beetle (Coleoptera: Chryso- large numbers of A. glycines in situations where these melidae) by Phalangium opilio (Opiliones: Phalangidae). aphids are particularly abundant, as would occur in J. Econ. Entomol. 83: 772Ð778. outbreak situations. If this occurs, P. opilio populations Enders, F. 1976. Clutch size related to hunting manner of could be adversely affected. In turn, this could ad- spider species. Ann. Entomol. Soc. Am. 69: 991Ð998. versely affect the contribution of P. opilio to the nat- Eubanks, M. D., and R. F. Denno. 2000. Health food versus ural biological control of other pests, such as H. zea. fast food: the effects of prey quality and mobility on prey selection by a generalist predator and indirect interac- tions among prey species. Ecol. Entomol. 25: 140Ð146. Halaj, J., and A. B. Cady. 2000. Diet composition and sig- Acknowledgments niÞcance of earthworms as food of harvestmen (Arach- The authors thank J. Harwood and M. Lutz for reviewing nida: Opiliones). Am. Mid. Nat. 143: 487Ð491. an earlier version of the manuscript and J. Moya-Loran˜ o for Hanks, L. M., and R. F. Denno. 1993. Natural enemies and statistical advice. Support for this research was provided by plant water relations inßuence the distribution of an the USDA (CRIS 0188764). This investigation (04-08-053) armored scale insect. Ecology. 74: 1081Ð1091. was conducted in connection with a project of the Kentucky Ignoffo, C. M. 1965. The nuclear-polyhedrosis virus of Agricultural Experiment Station. Heliothis zea (Boddie) and Heliothis virescens (Fabricus). II. Biology and propagation of diet-reared Heliothis. J. Invertebr. Pathol. 7: 217Ð226. Leathwick, D. M., and M. J. Winterbourn. 1984. Arthropod References Cited predation on aphids in a lucerne crop. New Zealand Adams, J. 1984. The habitat and feeding ecology of wood- Entomol. 8: 75Ð80. land harvestmen (Opiliones) in England. Oikos. 42: 361Ð Marshall, S. D., and J. L. Gittleman. 1994. Clutch size in 370. spiders: is more better? Funct. Ecol. 8: 118Ð124. Anderson, A. C. 1996. Inßuence of soybean canopy closure Newton, B. L., and K. V. Yeargan. 2001. Predation of on generalist predator abundance and predation on Helicoverpa zea (Lepidoptera: Noctuidae) eggs and Þrst corn earworm eggs. MS thesis, University of Kentucky, instars by Phalangium opilio (Opiliones: Phalangiidae). Lexington, KY. J. Kansas Entomol. Soc. 74: 199Ð204. Arnqvist, G., and S. Henriksson. 1997. Sexual cannibalism Newton, B. L., and K. V. Yeargan. 2002. Population charac- in the Þshing spider and a model for the evolution teristics of Phalangium opilio (Opiliones: Phalangiidae) in of sexual cannibalism based on genetic constraints. Kentucky agroecosystems. Environ. Entomol. 31: 92Ð98. Evol. Ecol. 11: 225Ð273. Nyffeler, M., and W.O.C. Symondson. 2001. Spiders and Ashby, J. W., and R. P. Pottinger. 1974. Natural regulation harvestmen as gastropod predators. Ecol. Entomol. 26: of Pieris rapae Linnaeus (Lepidoptera: Pieridae) in 617Ð628. Canterbury, New Zealand. New Zealand J. Agric. Res. 17: Petersen, B. 1950. The relation between size of mother and 229Ð239. number of eggs and young in some spiders and its sig- Bachmann, E., and M. Schaefer. 1983. Notes on the life niÞcance for the evolution of size. Experientia. 6: 96Ð98. cycle of Phalangium opilio (Arachnida: Opilionida). Pfannenstiel, R. S., and K. V. Yeargan. 2002. IdentiÞcation Verh. Naturwiss. Ver. Hamburg. 26: 255Ð263. and diel activity patterns of predators attacking Helico- Beck, M. W., and E. F. Connor. 1992. Factors affecting the verpa zea (Lepidoptera: Noctuidae) eggs in soybean and reproductive success of the crab spider Misumenoides sweet corn. Environ. Entomol. 31: 232Ð241. formosipes: the covariance between juvenile and adult Rice, W. R. 1989. Analyzing tables of statistical tests. Evo- traits. Oecologia (Berl.). 92: 287Ð295. lution. 43: 223Ð225. Bilde, T., and S. Toft. 1994. Prey preference and egg pro- Sankey, J.H.P. 1949. British harvest-spiders. Essex Natural- duction of the carabid beetle Agonum dorsale. Entomol. ist. 28: 181Ð191. Exp. Appl. 73: 151Ð156. Sankey, J.H.P., and T. H. Savory. 1974. British harvestmen. Bristowe, W. S. 1949. The distribution of harvestmen Synopsis of the British Fauna, No. 4. Academic, London. (Phalangida) in Great Britain and Ireland, with notes on SAS Institute. 2000. Software release 8.0. SAS Institute, their names, enemies and food. J. Anim. Ecol. 18: 100Ð114. Cary, NC. February 2005 ALLARD AND YEARGAN:PREDATORÕS DIET 13

Siegel, S., and N. J. Castellan. 1988. Non-parametric statis- Specty, O., G. Febvay, S. Grenier, B. Delobel, C. Piotte, tics for the behavioral sciences. McGraw-Hill Interna- J.-F. Pageaux, A. Ferran, and J. Guillaud. 2003. tional, New York. Nutritional plasticity of the predatory ladybeetle Sigsgaard, L., S. Toft, and S. Villareal. 2001. Diet-dependant Harmonia axyridis (Coleoptera: Coccinellidae): compar- survival, development and fecundity of the spider ison between natural and substitution prey. Arch. Insect Atypena formosana (Oi) (Araneae: Linyphiidae)Ñimpli- Biochem. Physiol. 52: 81Ð91. cations for biological control in rice. Biocontrol. Sci. Toft, S. 1995. Value of Rhopalosiphum padi as food for cereal Technol. 11: 233Ð244. spiders. J. Appl. Ecol. 32: 552Ð560. Simpson, M. R. 1995. Covariation of spider egg and Toft, S., and D. H. Wise. 1999. Growth, development, and clutch size: the inßuence of foraging and parental survival of a generalist predator fed single- and mixed- care. Ecology. 76: 795Ð800. species diets of different quality. Oecologia (Berl.). 119: Sivasubramaniam, W., S. D. Wratten, and J. Klimaszewski. 191Ð197. 1997. Species composition, abundance, and activity of Wagner, J. D., and D. H. Wise. 1996. Cannibalism regulates predatory arthropods in carrot Þelds, Canterbury, densities of young wolf spiders: evidence from Þeld and

New Zealand. New Zealand J. Zool. 24: 205Ð212. laboratory experiments. Ecology. 77: 639Ð652. Downloaded from https://academic.oup.com/ee/article/34/1/6/478711 by guest on 29 September 2021 Sokal, R. R., and F. J. Rohlf. 1995. Biometry: the principles and practice of statistics in biological research. W. H. Freeman, New York. Received 24 May 2004; accepted 9 October 2004.