Ecology, 61(5). 1980. pp. 125!G1258 One exclusively predaceous group, the spiders, @I1980 by the Ecological Sociely of America demonstrates a more unusual energetic adaptation, exhibiting resting metabolic rates about half those FORAGING STRATEGY AND measured for other poikilothermic animals of equal METABOLIC RATE IN SPIDERS' mass (Anderson 1970). This already low metabolic level makes even more remarkable the suggestion of Carrel and Heathcote (1976) that spiders of two fam- Matthew H. Greenstone2s3and Albert F. BennettZ ilies, Loxoscelidae and Scytotidae, have substantially Predators are by definition at least two trophic lower mass-specific resting metabolic rates than do levels removed from primary production. Because of other members of the order Araneae. Members of low efficiencies of secondary productivity (Slobodkin these two families are sit-and-wait predators, the scy- 1961) and fluctuations in prey availability, they may totids snaring passing insects by squirting them with be expected to experience food shortages of varying a gluey secretion, and the loxoscelids employing ir- duration and intensity. Many predators have the abil- regular sticky webs. Their lower metabolic rate was ity to gorge and to store surplus energy as lipid or supposedly related to their foraging styles as "prim- glycogen when prey are plentiful and to lower res- itive hunters and weavers," reflecting a low-energy piratory rates temporarily when prey are scarce. foraging strategy. However, Carrel and Heathcote These traits have been interpreted as adaptations to (1976) did not directly measure metabolic rates of unpredictable food availability (Bustard 1967, Martof these animals. Rather, they based their inference on 1969, Greenstone 1978). the relationship between heart rates, which they mea- 1256 NOTES AND COMMENTS Ecology, Vol. 61, No. 5

TABLE1. Masses and resting metabolic rates of spiders studied. Metabolic rates determined at 22OC and corrected to STPD) conditions.

Mass Vo, Family Species (mg) (do&) Theraphosidae (Tarantulas) Aphonopelma eutylenum Aphonopelma eutylenum Loxoscelidae (Brown spiders) Loxosceles laeta Loxosceles laeta Loxosceles laeta Loxosceles laeta Loxosceles laeta Loxosceles laeta Loxosceles laeta Loxosceles laeta Loxosceles laeta Loxosceles deserta Loxosceles deserta Plectreuridae (Plectreurids) Plectreurys tristis Plectreurys tristis Plectreurys sp. Theridiidae (Cobweb weavers) Steatoda medialis Latrodectus mactans Latrodectus mactans Latrodectus mactans Linyphiidae (Sheetweb weavers) Frontinella pyramitela Frontinella pyramitela Frontinella pyramitela Araneidae (Orb weavers) Cyclosa conica Cyclosa conica Neoscona oaxacensis Neoscona oaxacensis Argiope aurantia Argiope aurantia Argiope aurantia Agelenidae (Funnel web weavers) Agelenopsis aperta Agelenopsis aperta Agelenopsis aperta Lycosidae (Wolf spiders) Schizocosa pacifica Oxyopidae (Lynx spiders) Peucetia viridans Peucetia viridans Peucetia longipalpis Gnaphosidae (Gnaphosids) Zelotes rusticus Clubionidae (Sac spiders) Liocranoides sp. Thomisidae (Crab spiders) Misumenoides formosipes Misumenops sp. Misumenops sp. Misumenops sp. Misumenops sp. Salticidae (Jumping spiders) Metaphiddipus vitis Menemerus bivittatus Phiddipus johnsoni

sured, and published respirometry data which did not oscelids and comparing them with those of other spi- include the two families of interest. Their primary ob- ders. servations are that resting heart rates in loxoscelids and scytotids are substantially lower than those of and Methods other spiders. No measurements of metabolic rate Forty-seven animals, comprising 21 species in 13 have been reported previously for these groups. The families, were collected in central and southern Cal- object of this project was to test their hypothesis di- ifornia during the spring and summer of 1978 Fable rectly by measuring resting metabolic rates in lox- 1). They ranged in mass from 4.6 mg to 15 g and ran October 1980 NOTES AND COMMENTS 1257

for Argiope and Aphonopelma. The manometric flasks contained water to establish saturated humidity conditions and 5% KOH to absorb carbon dioxide. All animals known to be diurnally active (salticids, oxyopids, thomisids, and agelenids) were measured at 2200-2400 local time since Anderson (1970) has shown that diurnal spiders achieve their lowest rest- ing metabolic rates at night; all others were measured during the day (1 100-1500 local time). Animals were equilibrated in their flasks for 1 h and oxygen con- sumption was measured continuously for 2 h; the low- est observed 30-min interval was utilized as resting oxygen consumption. All reported gas volumes are mass (mg) corrected to standard temperature and pressure dry FIG. 1. Oxygen consumption (V,J as a function of body (STPD) conditions. Oxygen consumption in Argiope mass in spiders at 22OC (47 individuals, 20 species. 13 was determined from the decrement in oxygen con- families). Familial designations: A = Araneidae, Ag = tent measured with an Applied Electrochemistry oxy- Agelenidae. C = Clubionidae, G = Gnaphosidae, L = gen analyzer in a closed metabolic chamber fash- Linyphiidae, Ly = Lycosidae, 0 = Oxyopidae, P = Plectreuri- dae, S = Salticidae, T = Thornisidae, Th = Theridiidae, ioned from a glass syringe. Oxygen consumption of Tr = Theraphosidae, = Loxoscelidae. Aphonopelma was determined with the oxygen ana- lyzer with open flow oxygen analysis as described by Depocas and Hart (1957).

Results the gamut in foraging style from web spinners (Age- lenidae, Araneidae, Linyphiidae, Loxoscelidae, Ther- Rates of resting energy utilization measured as idiidae) to active pursuers (Lycosidae, Oxyopidae, oxygen consumption are given in Table 1 and Fig. 1. Salticidae), with intermediate styles represented by Before comparing the loxoscelid mass-metabolism the remaining families. We were unable to find any regression with that for all other spiders, the two data scytotids in our area and assume that the loxoscelids sets were tested for homogeneity of variances (Sokal are representative of the superfamily Scytodoidea, to and Rohlf 1969). The variances are significantly dif- which both families belong. In accordance with es- ferent (F,,, = 5.65, P < .01). It is obvious from in- tablished procedure (Anderson 1970; Carrel and spection of Fig. 1 that the larger variance of the non- Heathcote 1976). we used only females in our anal- loxoscelid set is due to the inclusion of data from 12 yses. Of the 36 nonloxoscelid individuals, 33 were families, as opposed to just one for the loxoscelids. adult females and 3 were penultimate females; the 11 The data were therefore broken down into families loxoscelids represented two species and comprised and a comparison made of the regressions for all fam- 6 adult and 5 penultimate females. ilies represented by at least three data points (this The protocols for maintenance and metabolic rate eliminated only the Theraphosidae, Lycosidae, Gna- determinations were similar to those of Anderson phosidae and Clubionidae). Among the nine regres- (1970) and Carrel and Heathcote (1976). Animals sions there are no significant differences in slope were maintained individually in containers for 3 wk (F,,, = 1.065, P > .5) but highly significant differ- in July and August at 20°C (+lo) on a 16 h light-8 h ences in elevation = 49.68, P << ,001). In order dark photoperiod. For the first 2 wk, the spiders were to test Carrel and Heathcote's (1976) hypothesis that fed appropriate prey in sufficient quantity to maintain loxoscelids have lower resting metabolic rates than constant body mass. They were then fasted for 1 wk other spiders, we compared the elevation of the lox- before experimentation. Water was available to all oscelid regression with that of each of the other fam- animals except the loxoscelids and theridiids, since ilies by Scheffe's (1959) method of simultaneous con- these are known to be xeric-adapted and the loxos- fidence intervals. Since the hypothesis of equality of celids, at least, will languish under prolonged con- elevations was soundly rejected with P << ,001, the ditions of high humidity (M. H. Greenstone, personal smallest confidence interval employed for the detec- observation). The spiders remained healthy, many tion of differences should be .99. Using this interval produc~ngegg cases during the acclimation period. only the theridiids differ in elevation from the loxos- Rates of oxygen consumption were determined celids, and even at the .90 level no new differences manometrically at 22 2 loin Warburg-type flasks of are detected. a Gilson microrespirometer and water bath, except If all of the data collected in the study are com- 1258 NOTES AND COMMENTS Ecology, Vol. 61, No. 5 bined, a general expression for the mass depen- ators, and the species studied here are all charac- dence of resting metabolic rates in spiders can be teristic of desert habitats. obtained: log microlitres 0, per hour = - 0.133 + Our results confirm Anderson's (1970) conclusion 0.710 (log mass in milligrams) (n = 47, r2= .91, P < that spiders as a group have lower resting metabolic ,001). This regression is substantially below that cal- rates than the majority of other poikilothermic ani- culated for other poikilothermic animals: the meta- mals. Other aspects of their metabolic efficiency in- bolic rate of a 100-mg spider is only 74% of predicted clude very low resting metabolic rates for embryonic values for other poikilothermic organisms (Hemming- spiders (Anderson 1978), and the ability to depress sen 1960). This result agrees with that of Anderson metabolic rates below resting levels during transient (1970), who first pointed out the low energetic de- periods of starvation (It6 1964, Miyashita 1969, Nak- mands of this group. It is interesting that the highest amura 1972, Anderson 1974, Humphreys 1977). This resting metabolic rate measured by Anderson also metabolic versatility is part of a suite of physiological, belonged to a theridiid, Achaearanea tepidariorum, anatomical, and behavioral adaptations which have although two other theridiid species did not appear the net effect of making energy less limiting for spi- to have excessively high resting metabolic rates (An- ders than for other animals of their size and trophic derson 1970: Fig. 4). position (Greenstone 1978). This may have profound implications for the role of spiders in terrestrial com- Discussion munities. It may account for a general lack of numer- Our data do not support the contention that loxos- ical responses to insect prey availability, at least in celid spiders have unusually low metabolic rates. We temperate zone spiders (Greenstone 1978). Freedom are unable to discriminate the resting rate of energy from energetic constraints also may permit feeding utilization of these animals from those of other spiders behavior that optimizes acquisition of nutrients, rather of comparable mass which we measured, except for than one that merely maximizes energy intake the theridiids. Metabolic rates certainly are not one- (Greenstone 1979). The ability to tolerate low food fifth those of other spiders, as the differential in their availability may also buffer spiders against environ- heart rates would otherwise suggest (Carrel and mental fluctuations and make it unnecessary for them Heathcote 1976). Our results underscore the dangers to emigrate from momentarily unproductive habitats of making inferences about metabolic rates from (M. H. Greenstone, personal observation). Spiders measurements of rates of other processes. Heart rate therefore may be a more consistent part of the envi- in particular is known to be an unreliable predictor of ronment for other populations with which they inter- metabolic rate in other groups (Johnson and Gessa- act, principally as insectivores and as prey of arthro- man 1973). podivorous vertebrates. Consistency of residence, We consequently find no support for the assertion coupled with phenomenal densities (Dondale 1970), that "primitive hunting and weaving" spiders have a would make spiders the most important group of in- low metabolic rate linked to a low-energy foraging sectivores in some terrestrial habitats. strategy. Carrel and Heathcote's (1976) suggestion Studies of other groups suggest that reduced met- that Loxosceles possess such a foraging strategy abolic rates are not necessarily an adaptation to re- was apparently based on the misconception that they duced mean food availability as a consequence of a are much less active than other spiders. On the con- predatory existence. Rather, they may be found spo- trary, experienced collectors would agree with radically throughout the animal kingdom in animals Gertsch's (1958) authoritative description of Loxos- with an unpredictable food supply (McNab 1969, celes as "quite active" animals. The misconception 1973, 1974). In the case of spiders this may have is probably due to their well-known ability to survive contributed to their ubiquity in terrestrial habitats, much longer periods of starvation than do other spi- making it possible for them to exist in environments ders. Rather than low resting metabolic rates, this which are closed to some other groups of insectivores probably indicates an extreme development of the (Swan 1961). We do not, however, find any interfam- ability, already known from some other spiders, to ilial differences among spiders in resting rates of en- depress metabolic rates below resting rates during ergy utilization which are reflective of different modes prolonged periods of starvation (It6 1964, Nakamura of prey capture or foraging strategy. 1972, Anderson 1974). The lack of a connection be- tween foraging strategy and resting metabolic rate is Acknowledgments: We thank Rudi Berkelhamer, underscored by the one significant difference which David Greenstone, and Sandra Greenstone for field was found, that between the loxoscelids and the ther- assistance, Willis Gertsch and Susan Riechert for aid idiids. Members of these two families are very similar in spider species identification, David Faulkner for in habit and habitat. Like the loxoscelids, the theri- the loan of the theraphosids, and Franklin Ennik for diids are sedentary, web-building, sit-and-wait pred- information on the location of Loxosceles popula- October 1980 NOTES AND COMMENTS 1259 tions. We are most grateful to Howard Tucker and lt6, Y. 1964. Preliminary studies on the respiratory energy Patrick Williams for assistance with the statistical loss of a spider, Lycosa pseudoannulata. Researches on Population Ecology (Kyoto) 6:13-21. analysis. The study was supported in part by a Bio- Johnson, S. F., and J. A. Gessaman. 1973. An evaluation medical Research Support Grant, School of Biolog- of heart rate as an indirect monitor of free-living energy ical Sciences, University of California, Irvine, to Mat- metabolism. Pages 44-55 in J. A. Gessaman, editor. Eco- thew H. Greenstone and National Science Foundation logical energetics of homeotherms. Utah State University Grant PC M77-24208 and National Institutes of Health Press, Logan, Utah, USA. McNab, B. K. 1969. The economics of temperature regu- Grant KO4 AM00351-01 to Albert F. Bennett. lation in neotropical bats. Comparative Biochemistry and Physiology 31:227-268. Literature Cited -. 1973. The rate of metabolism of the spiny rat, Proe- Anderson. J. F. 1970. Metabolic rates of spiders. Compar- chimys semispinosis with comments on the ecological ative Biochemistry and Physiology 335-72. factors that influence the basal rate of metabolism in ro- -. -. 1974. Responses to starvation in the spiders Ly- dents and lagomorphs. Boletim de Zoologia e Biologia cosa lenta Hentz and Filistata hibernalis (Hentz). Ecology Marinha, N.S. 30:93-103. . 1974. The energetics of endotherms. Ohio Journal 55576-585.~~~ . 1978. Energy content of spider eggs. Oecologia of Science 74:370380. 37:4 1-57. Martof, B. S. 1969. Prolonged inanition in Siren lacertina. Bustard. H. R. 1967. Gekkonid lizards adapt fat storage to Copeia 1969:285-289. desert environments. Science 158:1197-1198. Miyashita, K. 1969. Effects of locomotoiy activity, temper- Carrel, J. E., and R. D. Heathcote. 1976. Heart rate in spi- ature, and hunger on the respiratory rate of Lycosa T-in- ders: influence of body size and foraging energetics. Sci- signata Boes. et Str. (Araneae: Lycosidae). Applied Ento- ence 193:148-150. mology and Zoology 4:105-113. Depocas. F., and J. S. Hart. 1957. use of the Pauling oxygen Nakamura. K. 1972. The ingestion in wolf spiders II. The analyzer for measurement of oxygen consumption of ani- expression of hunger and amount of ingestion in relation mals in open-circuit systems and in a short-lag, closed- to spider's hunger. Researches on Population Ecology circuit apparatus. Journal of Applied Physiology 10:388- (Kyoto) 14:82-96. 392. Scheffe. H. 1959. The analysis of variance. Wiley, New Dondale, C. D. 1970. Spiders of Heasman's field, a mown York, New York, USA. meadow near Belleville. Ontario. Proceedings of the En- Sokal, R. R., and F. J. Rohlf. 1969. Biometry. Freeman, San tomological Society of Ontario 101:62-69. Francisco, California, USA. Gertsch. W. J. 1958. The spider genus Loxosceles in North Slobodkin, L. B. 1961. Growth and regulation of animal America. Central America, and the West Indies. American populations. Holt, Rinehart and Winston, New York, New Museum Novitates 1907:146. York, USA. Greenstone, M. H. 1978. The numerical response to prey Swan. L. W. 1961. The ecology of the high Himalaya. Sci- availability of Pardosa ramulosa (McCook) (Araneae: Ly- entific American 205:68-78. cosidae) and its relationship to the role of spiders in the balance of nature. Symposia of the Zoological Society of London 42:183-193. . 1979. Spider feeding behaviour optimises dietary Manuscript received 8 August 1979; revised 14 April essential amino acid composition. Nature 282:501-503. 1980; accepted 30 April 1980. Hemmingsen, A. M. 1960. Energy metabolism as related to Department of Ecology and Evolutionary Biology body size and respiratory surfaces, and its evolution. Re- and School of Biological Sciences, University of port Number 9, Steno Memorial Hospital and the Nordisk California, Irvine, California 9271 7 USA Insulin Laboratorium, C. Hamburgers Bogtrykkeri, Copen- Present address: Department of Entomology and hagen, Denmark. Nematoloay,- - Universitv of Florida Humphreys. W. F. 1977. Respiration studies on Geolycosa 3 103 ~ccartyHall godeffrayi (Araneae: Lycosidae) and their relationship to Gainesville, Florida 3261 1 field estimates of metabolic heat loss. Comparative Bio- chemistry and Physiology 57A:255-263.