1999. The Journal of Arachnology 27:470±480

THERMAL TOLERANCES AND PREFERENCES OF THE CRAB ASPERATUS AND FORMOSIPES (ARANEAE, )

Victoria R. Schmalhofer: Graduate Program in Ecology and Evolution; Department of Ecology, Evolution, and Natural Resources; Rutgers University, Cook College; 14 College Farm Road, New Brunswick, New Jersey 08901±8551 USA

ABSTRACT. Misumenops asperatus (Hentz 1847) and (Walckenaer 1837) are diurnally-active, ¯ower-dwelling crab spiders (Thomisidae) commonly inhabiting open ®elds. In lab- oratory experiments, both remained active over a temperature range of approximately 46 ЊC. The spring-maturing M. asperatus tolerated signi®cantly lower temperatures than the summer-maturing M. formosipes (CTmin ϭϪ1.4 ЊC and 2.2 ЊC, respectively), while M. formosipes tolerated signi®cantly higher temperatures than M. asperatus (CTmax ϭ 48.2 ЊC and 45.1 ЊC, respectively). Misumenops asperatus displayed thermal discomfort over a broader range of temperatures (36±44 ЊC) than did M. formosipes (41±46 ЊC). In a laboratory thermal gradient apparatus M. asperatus tended to prefer cooler temperatures than M. formosipes (14.4 ЊC and 18.4 ЊC, respectively). Regression analysis of literature data for 21 species of spiders showed a signi®cant positive relationship between the thermal preference of a species and its

CTmax. For their CTmax's, which were high compared to most other species, M. asperatus and M. formosipes preferred low temperatures. The coupling of low thermal preferences and high thermal toler- ances displayed by M. asperatus and M. formosipes is unusual for ectothermic organisms.

Spiders are strict ectotherms (Humphreys ences, upper tolerance limits, or thermoregu- 1987; Pulz 1987) and are important predators latory behaviors of spiders inhabiting temper- in many terrestrial systems (Riechert 1974; ate regions (for exceptions see Almquist 1970; Wise 1993), yet the thermal ecology of spiders Sevacherian & Lowrie 1972; Tolbert 1979; is generally less well understood than is that Suter 1981; references from Table 2 in Pulz of their insect prey (Humphreys 1987). Ther- 1987). mal relations (i.e., thermoregulatory behav- Information regarding an 's thermal iors, thermal tolerances and preferences) have tolerances and preferences is necessary to de- been examined in less than 0.1% of spider scribe the thermal ecology of the animal and species (Humphreys 1987), and most research to evaluate the thermal suitability of its habitat has concentrated on large tropical and sub- (Hertz et al. 1993). In the experiments report- tropical orb-weavers (e.g., Krakauer 1972; ed here, I examined the thermal tolerances and Carrel 1978; Robinson & Robinson 1978), de- preferences of two ¯ower-dwelling crab spi- sert-dwelling spiders (e.g., Mouer & Eriksen ders (Thomisidae), Misumenops asperatus and 1972; Seymour & Vinegar 1973; Humphreys Misumenoides formosipes. These experiments 1974, 1987; Riechert & Tracy 1975; Lubin & were part of a larger study investigating tem- Henschel 1990; Henschel et al. 1992; Turner perature effects on crab spider microhabitat et al. 1993), and winter-active species (e.g., selection and hunting performance. Because Aitchison 1978). Studies of temperate-zone M. asperatus and M. formosipes prey primar- spiders inhabiting moderate environments ily on insect pollinators, most foraging op- have generally focused on cold resistance and portunities and events occur diur- super-cooling capabilities (e.g., Almquist nally (Schmalhofer 1996). Compared to 1970; Kirchner 1973, 1987; Schaefer 1977; nocturnal spiders, which are active when heat Duman 1979; Bayram & Luff 1993) or tem- stress is minimal, M. asperatus and M. for- perature effects on growth and metabolic rate mosipes, as well as other diurnally-active in- (e.g., Anderson 1970; Hagstrum 1970; Moul- ¯orescence spiders, likely experience greater der & Reichle 1972; Li & Jackson 1996). temperature variability and extremes of tem- Fewer studies have examined thermal prefer- perature. Consequently, diurnal spiders might

470 SCHMALHOFERÐCRAB SPIDER THERMAL ECOLOGY 471 tolerate greater thermal stress. This study spe- August 1993. A given spider was used in only ci®cally addressed the following questions: 1) one experimental manipulation. What are the thermal tolerances and prefer- Because hunger has been shown to in¯u- ences of M. asperatus and M. formosipes?2) ence thermal sensitivity in spiders (Pulz When comparing ®eld-active adult female spi- 1987), I maintained the experimental spiders ders, does the summer-maturing species, M. on a diet of one house¯y per week for three formosipes, display higher tolerances and weeks prior to the initiation of the experi- preferences than the spring-maturing species, ments. This regimen equalized hunger-states M. asperatus? 3) How do the thermal toler- among individuals of a given species and ances and preferences of these ¯ower-dwell- maintained spider body mass at relatively con- ing thomisids compare with the thermal tol- stant levels (Anderson 1970; Schmalhofer un- erances and preferences of other spiders? 4) publ. data). Does data drawn from the literature indicate Misumenops asperatus and M. formosipes that diurnally-active spiders, in general, have were not acclimated to similar temperatures in higher thermal tolerances and preferences than the lab prior to testing. Although this con- nocturnally-active spiders? founds species identity with seasonal temper- Information concerning the thermal rela- ature differences when comparing the two tions of M. asperatus and M. formosipes is of species, I was not attempting to separate these additional interest because thomisids rank in¯uences, but, rather, was interested in com- among the most diverse families of spiders paring the responses of ®eld-active adults. (Coddington & Levy 1991) and are among the Also, other researchers (e.g., Sevacherian & most common cursorial spiders found in the Lowrie 1972; Seymour & Vinegar 1973) have herb stratum of open ®elds. However, the ther- found that temperature acclimation does not mal ecology of this family is virtually un- affect thermal preferences or upper tolerance known, consisting only of a few anecdotal ob- limits of spiders. However, I maintained spi- servations (Morse 1979; Lockley et al. 1989). ders at ambient ®eld temperature, rather than a constant temperature, to reduce any possi- METHODS bility of spider responses to experimentally in- Study .ÐMisumenops asperatus duced temperature changes being in¯uenced and M. formosipes are sit-and-wait ambush by acclimation to an arti®cial temperature re- predators that use their raptorial forelimbs, gime. Under natural conditions, the two spe- rather than a web, to restrain prey. In central cies experienced different temperature re- New Jersey, M. asperatus matures in spring gimes; average daily temperature, based on (mid-April to early May), females lay a single data collected from the weather station at the egg sac in late May or June, and spiderlings Hutcheson Memorial Forest Research Center emerge in June and July and overwinter as (HMF) in Somerset County, New Jersey (the late instar juveniles (pers. obs.). Misumeno- site of later ®eld experiments), for 30 days ides formosipes matures in mid-summer (Au- prior to the initiation of experiments was 16.5 gust), females lay a single egg sac in Septem- Ϯ8.7 ЊC for M. asperatus and 22.8 Ϯ7.9 ЊC ber or early October, and spiderlings generally for M. formosipes. overwinter in the egg sac (pers. obs.). Thermal tolerances.ÐCritical thermal

Only adult female spiders were used in maximum (CTmax) and critical thermal mini- these experiments. Like many other spiders, mum (CTmin) describe the highest and lowest male M. asperatus and M. formosipes seldom temperatures, respectively, at which an animal capture prey as adults, instead spending their is capable of displaying coordinated locomo- time searching for and guarding prospective tory behavior (i.e., the animal can still escape mates (Foelix 1996; Dodson & Beck 1993; unfavorable temperatures). An animal's ther- Pollard et al. 1995). Spiders were collected in mal tolerance range is delimited by these crit- Middlesex and Somerset Counties, New Jer- ical temperatures. Outside its tolerance range sey, and voucher specimens have been depos- an ectotherm enters a state of heat stupor or ited at the American Museum of Natural His- cold torpor, which may result in death if ex- tory. Experiments involving M. asperatus posure to extreme temperatures is prolonged. occurred in May and June 1993, and experi- Critical temperatures of M. asperatus and M. ments involving M. formosipes occurred in formosipes were determined by placing spi- 472 THE JOURNAL OF ARACHNOLOGY ders con®ned in petri dishes in a controlled was recorded with a Bailey BAT-12 thermo- temperature box (VWR Scienti®c model 2015 couple thermometer. low-temperature incubator) initially set to 25 Spiders were released singly into the center ЊC. Box temperature was then raised to 50 ЊC of the arena, and the number of each square

(to determine CTmax) or lowered to Ϫ5 ЊC (to in which a spider stopped and the amount of determine CTmin). Temperature changed at a time it stayed within the square was recorded rate of approximately 1 ЊC every ®ve minutes. during a 10 minute period. A spider's pre- This rate of change was similar to that used ferred temperature (Tp) was determined ac- in other studies examining tolerance limits cording to the formula (e.g., Almquist 1970; Krakauer 1972; Sey- T ϭ⌺[(T )(t /t )] mour & Vinegar 1973). For every temperature p i i q change of 1 ЊC, the spiders were prodded to where Ti is the temperature (ЊC) of square i, ti ascertain their ability to initiate an escape re- is the time (s) spent in square i, and tq is the sponse. The last temperature at which a spider total time (s) a spider was quiescent (n ϭ 9 responded to prodding (by moving away from spiders per species). The preferred tempera- the probe, raising its raptorial forelimbs, or ture range of a species was calculated as one grabbing hold of the probe) was recorded as standard deviation around its average Tp. its critical temperature. Spiders were removed Field temperature.ÐTemperature data ob- from the temperature box once they ceased to tained from the weather station at HMF were respond to prodding. Spiders are known to averaged over three years (1993±1995) to de- spontaneously initiate vigorous activity at termine average monthly high and low tem- peratures. These data were compared with the high temperatures preceding CTmax; this activ- ity indicates thermal discomfort as maximal preferred temperature ranges of M. asperatus tolerance is approached (Lubin & Henschel and M. formosipes. By graphing the data and calculating the appropriate area encompassed 1990). The temperature ranges over which M. within the high-low temperature curves, a asperatus and M. formosipes displayed ther- rough estimate of the frequency with which mal discomfort were noted. Five spiders of mature female spiders experienced ambient each species were used to determine CT , max temperatures (shaded air temperature) within and ®ve different spiders of each species were their preferred ranges was determined. Aver- used to determine CT (total n ϭ 10 spiders min age daily temperatures calculated over a ten per species). Another set of spiders (n ϭ 9) day period at the beginning and end of a spe- was prodded at ®ve minute intervals under cies' adult stage were compared to determine constant temperature conditions (25 ЊC) to as- the seasonal temperature shifts experienced by certain whether a lack of response to prodding adult M. asperatus and M. formosipes. was due to habituation rather than tempera- Analyses.ÐDue to small sample sizes, ture. nonparametric statistics were used to analyze Thermal preferences.ÐA temperature are- the results. A Mann-Whitney U test was used na was established by placing a box (50 cm to compare CTmin data of M. asperatus and M. ϫ 50 cm), the bottom of which was demar- formosipes. Because CTmax and thermal pref- cated into numbered squares (2 cm ϫ 2 cm), erence data of M. asperatus and M. formosi- in a controlled temperature room at 2 ЊC. By- pes were also compared to CTmax and thermal tac Te¯on௢ paper lined the sides of the box preference data of other spider species taken to prevent spiders from escaping. A 650 W from the literature, Kruskal-Wallace tests were photo¯ood lamp (equivalent color temperature used, and all possible pairwise posthoc com- 3400 K) mounted on a ringstand and suspend- parisons were made using Mann-Whitney U ed 1 m above a corner of the arena served as tests, with a Bonferroni correction for multiple a radiant heat source. A temperature map of comparisons (adjusted ␣ϭ0.009). Spider spe- the arena was created by determining the tem- cies for which data were available in the lit- perature of each square within the arena; a erature were separated into two groups: diur- spider model (freeze-dried female thomisid) nally active and nocturnally active. For with a ®ne thermocouple attached to the ven- comparative purposes, species that were ac- tral side of its abdomen was placed in each tive both nocturnally and diurnally were square and, after two minutes, its temperature counted as diurnally active. Information con- SCHMALHOFERÐCRAB SPIDER THERMAL ECOLOGY 473

Table 1.ÐCritical thermal tolerances (CTmax's and CTmin's) and preferred temperatures (Tp's) of Misu- menops asperatus and Misumenoides formosipes, and the range of temperature over which spiders dis- played thermal discomfort. Values are in ЊC. Critical thermal values and preferred temperatures are given as means (Ϯ 1 SD). For CTmin data, a signi®cant difference occurs at ␣ϭ0.05; for CTmax and Tp data, adjusted ␣ϭ0.009.

Mann-Whitney Measurement M. asperatus M. formosipes U test P-value

CTmin Ϫ1.4 (0.6) 2.2 (1.8) Ϫ2.660 0.0098 CTmax 45.1 (1.3) 48.2 (0.2) Ϫ2.627 0.0086 Tp 14.4 (3.4) 18.4 (5.4) Ϫ1.810 0.0703 thermal discomfort 36±44 41±46

cerning the activity times of the various spe- played thermal discomfort over a wider tem- cies came from the original studies and from perature range than did M. formosipes (Table Roberts (1995). In cases where information 1). No evidence of low-temperature thermal concerning a species' activity time could not discomfort was observed during the CTmin ex- be found, the species was presumed to be noc- periments (i.e., there was no period of spon- turnally active. Literature values for CTmax and taneous activity).

Tp were subjected to simple linear regression Values for the CTmax's of other spider spe- to determine whether CTmax increased with in- cies are presented in Table 2. Comparing creasing Tp. CTmax values of M. asperatus and M. formo- sipes with literature data for diurnally-active RESULTS and nocturnally-active spiders revealed signif- Thermal tolerances.ÐCessation of spider icant differences (Kruskal-Wallace test: H ϭ responses to prodding was due to temperature, 16.271, df ϭ 3, P ϭ 0.001). Diurnal spiders not habituation to prodding. Under constant and nocturnal spiders had similar CTmax's, and temperature conditions, spiders did not be- diurnal spiders and M. asperatus had similar come habituated in 45 consecutive prodding CTmax's (Fig. 1). However, CTmax's of M. as- trials. In the CTmin and CTmax experiments, a peratus and nocturnal spiders differed signif- given spider was prodded less than 30 times. icantly, and M. formosipes had a signi®cantly Also, spider posture changed noticeably when higher CT than M. asperatus, nocturnal spi- critical temperature was reached. Throughout max ders, or diurnal spiders (Fig. 1). most of the experimental temperature range, Thermal preferences.ÐTemperature in the spiders maintained the classic crab spider experimental arena ranged from 9±57 ЊC. Spi- hunting posture (raptorial forelimbs held out- ders encountering hotter areas moved rapidly stretched, slightly upraised, and approximate- ly perpendicular to the long axis of the body). to cooler areas, holding their bodies well-el- Within approximately 1 ЊC of upper or lower evated above the substrate (stilting) until they critical temperature, spiders abandoned the settled in a cooler section of the arena. Al- classic hunting posture and huddled with their though spiders moved more slowly (relative forelimbs held close to the body. to the speed at which they vacated hot areas) Misumenops asperatus and M. formosipes at the cooler end of the arena, no evidence of proved to be broadly temperature tolerant. cold-trapping (i.e., spider activity was so re- Misumenops asperatus had a signi®cantly duced by the cold that they could not emigrate from cooler areas) was observed. Spiders did lower CTmin than did M. formosipes (Table 1). Conversely, M. formosipes had a signi®cantly not stilt in areas cooler than 30 ЊC. Misumen- higher CTmax than did M. asperatus (Table 1). ops asperatus preferred cooler temperatures Spontaneous initiation of escape behavior by than M. formosipes, but this trend was not sig- spiders (i.e., a spider moved vigorously ni®cant (Table 1). around the petri dish without prompting from Preferred temperatures of other spider spe- the investigator) was observed during the cies are presented in Table 2. Comparing Tp's CTmax experiments, and M. asperatus dis- of M. asperatus and M. formosipes with lit- 474 THE JOURNAL OF ARACHNOLOGY

not included in this analysis. Addition of M. asperatus and M. formosipes data to the re- gression resulted in a loss of the signi®cant relationship (F ϭ 1.615, df ϭ 1, 21, P ϭ 0.2177, r2 ϭ 7.1%). For similar reasons, data for winter-active spiders were also excluded. Field temperature.ÐMisumenoides for- mosipes experienced preferred temperatures under ®eld conditions more frequently than did M. asperatus. Ambient temperature fell within the preferred temperature range (PTR) of adult M. asperatus 43% of the time, ex- ceeded PTR 47% of the time, and fell below PTR 10% of the time (Fig. 4). In contrast, ambient temperature fell within PTR of adult M. formosipes 65% of the time, exceeded PTR 10% of the time, and fell below PTR 25% of the time (Fig. 4). During their adult phase, M. asperatus experienced an increase in average Figure 1.ÐCritical thermal maxima (CT 's) of max daily temperature of 5.3 ЊC, and M. formosi- Misumenops asperatus, Misumenoides formosipes, nocturnally-active spiders and diurnally-active spi- pes experienced a decrease in average daily ders. Data for nocturnal and diurnal spiders were temperature of 6.5 ЊC. taken from Table 2; winter-active species were not DISCUSSION included in the analysis. Values with different let- ters are signi®cantly different using post-hoc Mann- Comparing the thermal tolerances and pref- Whitney U tests with adjusted ␣ϭ0.009. Error bars erences of the spring-maturing M. asperatus represent one SE for nocturnal and diurnal spiders with those of the summer-maturing M. for- and one SD for M. asperatus and M. formosipes. mosipes yielded the expected results. Adult fe- Standard errors could not be used for M. asperatus male M. asperatus, which experienced lower and M. formosipes since species averages were cal- ambient temperatures than did adult female M. culated from individual values. In contrast, noctur- nal and diurnal averages were calculated from spe- formosipes, had a lower CTmin, while M. for- cies averages, making use of the standard error mosipes had a higher CTmax. Thermal prefer- appropriate. ences of the two crab spider species were sim- ilar. Of greater interest is a comparison of the thermal tolerances and preferences of these erature data for diurnally-active and noctur- ¯ower-dwelling spiders with those of other nally-active spiders revealed signi®cant dif- spider species. ferences (Kruskal-Wallace test: H ϭ 23.878, There is little information available regard- df ϭ 3, P Յ 0.0001). Preferred temperatures ing CTmin in spiders. In the single study of were similar between M. formosipes and M. which I am aware, Hagstrum (1970) reported asperatus, and between M. formosipes and aCTmin of 6 ЊC for a southern California wolf nocturnal spiders (Fig. 2). However, Tp's of M. spider, Alopecosa kochi (Keyserling 1877) (as asperatus and nocturnal spiders differed sig- Tarentula kochi in Hagstrum 1970). Much ni®cantly, and Tp of diurnal spiders was sig- more data is available concerning lower lethal ni®cantly higher than that of M. formosipes, temperatures and temperature effects on de- M. asperatus, or nocturnal spiders (Fig. 2). velopmental rates (e.g., Almquist 1970; Li &

Relationship between CTmax and thermal Jackson 1996). Data from other studies indi- preference.Ð Using the literature data shown cates that temperate-climate spiders are gen- in Table 2, a signi®cant positive relationship erally capable of activity at relatively low was found between a spider species' Tp and temperatures. Ford (1978) showed that a Eu- its CTmax (F ϭ 6.707, df ϭ 1, 19, P ϭ 0.018, ropean wolf spider, Pardosa amentata Clerck r2 ϭ 26.1%) (Fig. 3). Because M. asperatus 1757, remained active at 5 ЊC, and Moulder and M. formosipes had unusually high CTmax's & Reichle (1972) obtained similar results for for their Tp's, data for these two species were the litter-spider fauna of a Tennessee Lirio- SCHMALHOFERÐCRAB SPIDER THERMAL ECOLOGY 475 dendron forest. Aitchison (1984) found that One would expect that because diurnally- both winter-active and winter-inactive Cana- active spiders experience higher temperatures dian spiders fed at 2 ЊC, with winter-active than nocturnally-active species, diurnally-ac- species continuing to feed at temperatures as tive spiders would prefer higher temperatures. low as Ϫ5 ЊC. These studies, coupled with the Evaluation of data from the literature showed

CTmin values calculated for M. asperatus and that this was indeed the case (Fig. 2). How- M. formosipes, suggest that temperate-zone ever, Tp's of M. asperatus and M. formosipes spiders from moderate climates may generally were lower than those of other diurnally-ac- be expected to have CTmin's near 0 ЊC. tive species, and Tp of M. asperatus was also Misumenops asperatus, and particularly M. lower than that of nocturnally-active species! formosipes, had high thermal tolerances. In Pulz (1987) suggested that, barring winter-ac- general, CTmax's of these ¯ower-dwelling tive spiders, lower thermal preference corre- thomisids were more similar to the upper le- lates with lower thermal tolerance. Regression thal temperatures than to the CTmax's of other analysis of the available literature data sup- spider species (see Table 2). Of the 27 species ported Pulz's hypothesis of a positive relation- for which data was available, only six species ship between Tp and CTmax. Interestingly, the had comparable CTmax's: Phurolithus festivus CTmax's of M. asperatus and M. formosipes (C.L. Koch 1835), Euophrys frontalis (Wal- predicted from the regression equation (40.2 ckenaer 1802), Cyrtophora citricola (ForskaÊl ЊC and 41.3 ЊC, respectively) were much low- 1775), Zelotes longipes (L. Koch 1866) (as Z. er than the measured values; alternatively, serotinus in Almquist 1970), Hogna caroli- predicted Tp's (32.1 ЊC and 43.4 ЊC, respec- nensis (Walckenaer 1805) (as Lycosa caroli- tively) were much higher than the measured nensis in Moeur & Eriksen 1972), and Seo- values. Thus, depending on how one looks at thyra henscheli (Dippenaar 1991). Misu- it, M. asperatus and M. formosipes have ex- menoides formosipes had the second highest ceptionally high thermal tolerances or excep-

CTmax recorded for a spider; only S. henscheli, tionally low thermal preferences. This com- an eresid from the Namib desert (Lubin & bination of high thermal tolerance and low Henschel 1990), had a higher thermal toler- thermal preference is unusual for an ecto- ance. The natural histories of M. asperatus therm; preferred temperature is usually nearer and M. formosipes may provide an explana- the upper than the lower tolerance limit (May tion for their unusually high thermal toleranc- 1985). es. These thomisids do not stalk prey, but, Broad temperature tolerances and relatively rather, position themselves close to a ¯ower's low thermal preferences displayed by M. as- nectaries and/or anthers (pollen-bearing struc- peratus and M. formosipes may be viewed as tures) in order to ambush ¯ower-visiting in- adaptations that facilitate their diurnal preda- sects (pers. obs.). On the plants used by M. tory lifestyles in potentially thermally stress- asperatus and M. formosipes, the ¯oral sur- ful habitats (sun-exposed ¯owers). Hymenop- face from which nectaries and anthers are ac- terans and dipterans comprise most of the prey cessed by insects is typically exposed to the captured by these thomisids (Schmalhofer sun (pers. obs.). Under conditions of high ra- 1996). Dipterans are well known for their diant intensity and low wind speed, body tem- ability to ¯y at low temperatures (reviewed in peratures of spiders on sun-exposed ¯oral sur- Heinrich 1993); and large hymenopterans, faces can exceed ambient temperature by 15 such as honeybees and , require ЊC or more (Schmalhofer 1996). A high ther- thoracic temperatures of 30±35 ЊC in order to mal tolerance would allow M. asperatus and ¯y (reviewed in Heinrich 1993). The capacity M. formosipes to continue hunting at ambient to endothermically generate heat by shivering temperatures near 30 ЊC, when ¯oral surface wing muscles allows these bees to ¯y at low temperatures could be in excess of 40 ЊC. Am- ambient temperatures; honeybees can ¯y bient temperatures approaching 30 ЊC are not when ambient temperature is as low as 15 ЊC, an uncommon occurrence in late spring and and some bumblebees can ¯y when ambient summer in central New Jersey: from April temperature is less than 10 ЊC (reviewed in through September in 1993±1995 there were, Heinrich 1993). Both M. asperatus and M. on average, 52 days per year having a daily formosipes prey on honeybees, and M. for- high temperature of at least 30 ЊC. mosipes is also capable of capturing bumble- 476 THE JOURNAL OF ARACHNOLOGY of a esert biting a Source ) lethal temperatures of LL T Almquist 1970 Almquist 1970 table 2 in PulzSuter 1987 1981 table 2 in PulzAlmquist 1987 1970 Almquist 1970 Almquist 1970 Almquist 1970 table 2 in Pulztable 1987 2 in Pulz 1987 table 2 in Pulz 1987 ), and lower ( LL 9.5² 8.3 6.8 7.1 UL T 11.1 Almquist 1970 T Ϫ Ϫ Ϫ Ϫ Ϫ UL T 44.0 53.7² table 2 in Pulz 1987 's), and upper ( p T p T 4.1 1.2² 17.1 23.0 23.5² 45.0 27.0² 22.3 16.0 19.4 27.5 16.8 and indicates that locomotor capacity has been lost). max HS HS HS HS max 41.8 40.8² 40.6² 42.1² 42.1 37.4 45.6 41.4 39.6 's), preferred temperatures ( d, 1 n/d, 5 46.0 n, 1 n, 1 d, 5 d, 2 41.5² n*, 4 48.2² table 2 in Pulz 1987 n, 1 d, 1 n, 1 n, 1n*, 3 46.4d, 1 n*, 3 n*, 1 23.1 Almquist 1970 max C. ``Code'' describes the period of activity and climatic zone inhabited by a species: nÐnocturnal hunter, Њ Êl 1775 in Pulz 1987) Êl 1775 L. 1758 n, 1 40.5 14.4 Hentz 1850 Spider code CT Blackwall 1850 Forska C. L. Koch 1835 Denis 1965 Roewer 1951 Forska Dippenaar 1991 n/d, 4 49.0 Lubin & Henschel 1990 Thorell 1856 Blackwall 1859 C. L. Koch 1843 in Almquist 1970) O. P.-Cambridge 1871 O. P.-Cambridge 1862 n, 1 41.4 22.3 Almquist 1970 Wider 1834 L. Koch 1866 L. Koch 1866 Dictyna viridissima Z. serotinus (as (as Table 2.ÐLiterature values for critical thermal maxima (CT Stemonyphantes lineatus Agelena consociata Agelena labyrinthica Clerck 1757 Nigma walckenaeri Agroeca proxima Phurolithus festivus Scotina gracilipes Argiope trifasciata Cyrtophora citricola Clubiona diversa Clubiona similis Clubiona trivialis Seothyra henscheli Zelotes longipes Bolyphantes index Frontinella communis Macrargus rufus Oedothorax apicatus moderate environment, 2Ðpresumedspecies, to 5Ðtropical be or arange subtropical temperate-zone of species. species values inhabiting Other given a symbols in moderate within the environment, the source, 3Ðwinter-active table HSÐheat temperate-zone are stupor species, (this as 4Ðd measure follows: is ²Ðaverage higher value than based CT on multiple values or the endpoints n*Ðpresumed nocturnal hunter (information unavailable), dÐdiurnal hunter, n/dÐhunts nocturnally and diurnally, 1Ðtemperate-zone species inha various spider species. Values are presented in Agelenidae Dictynidae Liocranidae Araneidae Clubionidae Eresidae Gnaphosidae Linyphiidae SCHMALHOFERÐCRAB SPIDER THERMAL ECOLOGY 477 Source Almquist 1970 Almquist 1970 Almquist 1970 Almquist 1970 table 2 in PulzSevacherian 1987 & Lowrie 1972 Sevacherian & Lowrie 1972 table 2 in Pulztable 1987 2 in Pulztable 1987 2 in Pulztable 1987 2 in Pulz 1987 table 2 in PulzMoeur 1987 & Eriksen 1972 table 2 in Pulztable 1987 2 in Pulz 1987 Almquist 1970 table 2 in Pulz 1987 LL 9.3 T 10.8 Ϫ Ϫ UL T 43.0 35.3 47.3 48.0 45.0² 47.7 45.1 p T 23.1 19.0 19.6 15.5 32.0² 28.1² 34.6² 29.0² 21.0² 24.8 19.2 26.2² 21.0 23.7² HS max 41.8² 42.8 41.8 43.2 39.3 47.0 39.7 40.4 Table 2.ÐContinued. n/d, 1 n/d, 1 n*, 1 n*, 1 n*, 2 48.0² table 2 in Pulz 1987 n/d, 2 n/d, 4 n/d, 2 n/d, 2 n/d, 1 n/d, 1 n/d, 1 n/d, 2 n/d, 2 n/d, 1 n/d, 1 n/d, 2 n/d, 2 in Moeur & Eriksen 1972) in Pulz 1987) Clerck 1757 Spider code CT F. O. P.-Cambridge 1895 Blackwall 1834 Walckenaer 1805 Walckenaer 1802 d, 1 45.7 27.5 Almquist 1970 McCook 1893 Wider 1834 Thorell 1856 Walckenaer 1802 O. P.-Cambridge 1861 Simon 1876 Walckenaer 1802 Doleschall 1852 L. 1767 d, 5 41.6 Krakauer 1972 Clerck 1757 Sundevall 1833 d, 1 41.8 19.5 Almquist 1970 Clerck 1757 in Pulz 1987) Banks 1898 sp. n, 4 43.0 29.0² Seymour & Vinegar 1973 spp. Lycosa carolinensis P. chelata Theridion saxatile (as (as (as Euophrys frontalis Zora spinimana Tibellus oblongus Philodromus aureolus Pardosa Pardosa lugubris Hogna carolinensis Arctosa alpigena Nephila clavipes Aphonopelma Achaeranea riparia Crustulina guttata Dipoena inornata Pardosa sierra Pardosa nigriceps Pardosa pullata Pardosa pullata Pardosa ramulosa Pirata piraticus Pirata piraticus Trochosa robusta Trochosa spinipalpis Salticidae Zoridae Philodromidae Lycosidae Tetragnathidae Theraphosidae Theridiidae 478 THE JOURNAL OF ARACHNOLOGY

Figure 2.ÐPreferred temperatures of Misumen- ops asperatus, Misumenoides formosipes, noctur- nally-active spiders and diurnally-active spiders. Data for nocturnal and diurnal spiders were taken from Table 2; winter-active species were not in- cluded in the analysis. Values with different letters are signi®cantly different using post-hoc Mann- Whitney U tests with adjusted ␣ϭ0.009. Error bars represent one SE.

Figure 4.ÐThe relationship between average dai- ly high and low temperatures and the preferred tem- perature ranges (PTR's) of Misumenops asperatus and Misumenoides formosipes. Periods of adult ac-

tivity are demarcated with vertical bars. CTmax (up- per dashed line), CTmin (lower dashed line), and zone of thermal discomfort (TD, dotted lines) are indicated for each spider species. The bounds of a species' PTR (dot-dashed lines) were calculated as

one standard deviation around mean Tp.

bees (Schmalhofer 1996). Presumably many of the other bees used by these spiders, such as anthophorids and megachilids, display tem- perature-¯ight relationships similar to those shown by honeybees and bumblebees. The Figure 3.ÐLinear regression of preferred tem- broad temperature tolerances shown by M. as- perature against CT . The regression was based max peratus and M. formosipes allow these spiders on literature data presented in Table 2. Regression to increase their foraging time, both daily and equation: y ϭ 0.275x ϩ 36.26. Although not in- cluded in the regression, for comparative purposes seasonally. Coupled with their ability to hunt data points for Misumenops asperatus and Misu- equally well over a wide range of tempera- menoides formosipes were included in the graph. tures (Schmalhofer 1996), and their low ther- Squares (Ⅲ) represent other spiders species, circles mal preferences, broad thermal tolerances (●) represent M. asperatus and M. formosipes. bene®t these spiders by affording them the op- SCHMALHOFERÐCRAB SPIDER THERMAL ECOLOGY 479 portunity to hunt prey that is itself active over (pers. obs.), spiders must remain near the an- a wide range of environmental temperatures. thers and/or nectaries in order to have access Assuming that an ectotherm bene®ts by to prey. In the open ®eld habitats where M. maintaining body temperature within some asperatus and M. formosipes are typically preferred range of temperature (Hertz et al. found, the upper surfaces of ¯owers, where 1993), comparing preferred temperature rang- the anthers and nectaries are located, are gen- es (PTR's) of M. asperatus and M. formosipes erally sun-exposed. Thus ¯ower-dwelling with the average range of temperatures nor- thomisids may be faced with a trade-off be- mally experienced by these spiders allows one tween maintaining access to prey and avoid- to make predictions concerning the likelihood ing high thermal stress. that the spiders will experience thermal stress ACKNOWLEDGMENTS (i.e., unfavorable temperatures that might lim- it activity or impair performance). Data indi- T. Casey, P. Morin, M. May, D. Morse, P. cate that M. asperatus experiences high ther- Harris, C. Kaunzinger, J. McGrady-Steed, J. mal stress (ambient temperature Ͼ PTR) more Fox, M. Cole, W. Schmalhofer, Y. Lubin, and frequently than low thermal stress (ambient an anonymous reviewer gave helpful critiques temperature Ͻ PTR), while M. formosipes ex- of earlier drafts of the manuscript. N. Platnick periences low thermal stress more frequently provided information concerning currently ac- than high thermal stress. In neither case did cepted species names and authorities. I thank average daily low temperature fall below spi- W., L., and V. Schmalhofer for their encour- agement and moral support. Partial support der CTmin. Thus, since ambient temperature did not fall to levels that would inhibit spider was provided by a National Science Founda- movement, M. asperatus and M. formosipes tion Dissertation Improvement Grant (DEB could alleviate low thermal stress by engaging 93±11203), and grants from the Anne B. and in behaviors designed to elevate body tem- James H. Leathem Scholarship Fund and the perature (e.g., basking in the sun). Normal William L. Hutcheson Memorial Forest Re- hunting behavior (i.e., sitting near a ¯ower's search Center. nectaries and/or anthers, provided the position LITERATURE CITED was exposed to the sun) would serve to Aitchison, C.W. 1978. Spiders active under snow achieve this result. in southern Canada. Symp. Zool. Soc., London, High thermal stress appears to be more of 42:139±148. a concern for these thomisids since ambient Aitchison, C.W. 1984. Low temperature feeding by temperature typically falls within or above a winter-active spiders. J. Arachnol., 12:297±305. spider's preferred range, and even when am- Almquist, S. 1970. Thermal tolerances and pref- bient temperature falls within the preferred erences of some dune-living spiders. Oikos, 21: range, ¯oral-surface temperatures, and thus 230±236. spider body temperatures, may be much high- Anderson, J.F. 1970. Metabolic rates of spiders. Comp. Biochem. Physiol., 33:51±72. er, potentially approaching CTmax. 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