Low Metabolic Rates in Primitive Hunters and Weaver Spiders

Physiological Entomology (2015), DOI: 10.1111/phen.12108

Low metabolic rates in primitive hunters and weaver spiders

MAURICIO CANALS1,2, CLAUDIO VELOSO3, LUCILA MORENO2 andRIGOBERTO SOLIS4 1Departamento de Medicina and Programa de Salud Ambiental, Escuela de Salud Pública, Facultad de Medicina, Universidad de Chile, Santiago, Chile, 2Departamento de Zoología, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, Santiago, Chile, 3Departamento de Ciencias Ecológicas, Facultad de Ciencias, Universidad de Chile, Santiago, Chile and 4Departamento de Ciencias Biológicas Animales, Facultad de Ciencias Veterinarias y Pecuarias, Universidad de Chile, Santiago, Chile

Abstract. The rates of oxygen consumption and carbon dioxide release of primitive hunters and weaver spiders, the Chilean Recluse spider Loxosceles laeta Nicolet (Araneae: Sicariidae) and the Chilean Tiger spider Scytodes globula Nicolet (Araneae: Scytodidae), are analyzed, and their relationship with body mass is studied. The results are compared with the metabolic data available for other spiders. A low metabolic rate is found both for these two species and other primitive hunters and weavers, such as spiders of the families Dysderidae and Plectreuridae. The metabolic rate of this group is lower than in nonprimitive spiders, such as the orb weavers (Araneae: Araneidae). The results reject the proposition of a general relationship for metabolic rate for all land arthropods (related to body mass) and agree with the hypothesis that metabolic rates are affected not only by sex, reproductive and developmental status, but also by ecology and life style, recognizing here, at least in the araneomorph spiders, a group having low metabolism, comprising the primitive hunters and weaver spiders, and another group comprising the higher metabolic rate web building spiders (e.g. orb weavers). Key words. Haplogynae, metabolism, spiders.

Introduction 1982; Canals et al., 2007; Nentwig, 2013). In addition, spiders may reduce their metabolic rate significantly when they expe- Spiders have very low resting metabolic rates (Anderson, 1970; rience periods of food limitation (Ito, 1964; Miyashita, 1969; Greenstone & Bennett, 1980; Prestwich, 1983a, 1983b; Wilder, Anderson, 1974; Tanaka & Ito, 1982; Canals et al., 2007; Phillip 2011), which may be associated with adaptation to environments & Shillington, 2010; Stoltz et al., 2010; Canals et al., 2011). of low predictability and low prey availability (Anderson, 1970; Lighton et al. (2001) propose that spiders have metabolic rates Greenstone & Bennett, 1980). Physiologically, this could be the similar to those of other land arthropods. They suggest that result of spiders using hydrostatic pressure for the extension of resting metabolic rate may be considered very conservative and their appendages, maintaining a posture with constant hydro- that a general allometric rule between body mass and resting static pressure with a small number of active muscles instead metabolic rate may be assessed for all land arthropods except for of the permanent use of all muscles with consequent metabolic tarantulas (Araneae: Theraphosidae) (Shillington, 2002, 2005), activity (Carrel & Heathcote, 1976; Anderson & Prestwich, as well as scorpions and ticks (Lighton et al., 2001). However, 1982). A low resting metabolic rate may be a factor that allows there is a great diversity of spiders with different life styles. spiders to extend their survival without food (Tanaka & Ito, The suborder Mygalomorphae in general comprises primitive hunter wandering spiders, whereas the suborder Araneomorphae Correspondence: Mauricio Canals, Departamento de Medicina comprises the Haplogynae spiders that are primitive hunters and and Programa de Salud ambiental, Escuela de Salud Pública, weavers, and also the Entelegynae, which includes the ‘modern’ Facultad de Medicina, Universidad de Chile, Independencia 939, spiders, such as the orb weaving spiders and the RTA clade (i.e. Postal Code 8380453, Santiago, Chile. Tel.: +56 2 9788596; e-mail: categorized by the presence of a retrolateral tibial apophisis) [email protected] that tend to have more ‘energetically expensive’ life habits

(Coddington & Levi, 1991; Penney et al., 2003; Bell et al., 2005; ˙ ∘ and carbon dioxide release (VCO2) measured at 20 and 30 C, Kawamoto et al., 2011). respectively, during the day, which corresponds to the resting Several studies fail to show metabolic differences that may phase of both species (Alfaro et al., 2013; Canals et al., 2013, be a consequence of ecological differences between different 2015). The respiratory quotient (RQ) was calculated as the ratio groups of spiders, other than those as a result of body mass, ˙ ˙ VCO2 : VO2, and the temperature coefficient Q10 (i.e. metabolic (Greenstone & Bennett, 1980; Anderson, 1994). For example, change with the increase of 10 ∘C in temperature) was calculated ˙ ∘ ˙ ∘ Anderson (1994), when analyzing species of the family Theridi- using the ratio VO2 at 30 C/VO2 at 20 C. idae with different life habits, reports differences that are only In the experiments, each individual was introduced into a attributable to food restriction. However, Shillington (2005) sealed 20-mL syringe for 2 h inside a photo and thermoregulated reports higher resting metabolic rates in the more active males cabinet. At the same time, two empty syringes were introduced than females of the Texas tarantula Aphonopelma anax, sug- into the same cabinet as controls. After 2 h, 50% of the volume gesting that sexual differences in the habits of this spider could of the syringe (10 mL) was introduced at a speed of 1 mL s−1 explain the metabolic differences. Similarly, Kawamoto et al. in an open continuous flow system, which aspired air with a (2011) contradict the idea that spiders can be accepted as land flow Q = 50 mL min−1. Water was removed from the air by pas- arthropods in energetic terms (Lighton et al., 2001) by show- sage through columns of calcium sulphate anhydride (Drierite; ing allometric differences in resting metabolic rates between WA Hammond Drierite Co., Ltd, Xenia, Ohio). Subsequently, ecribellate and cribellate orb weaver spiders, probably as a the dry air was passed through a CO2 trap, then filtered with result of behavioural and activity differences associated with barium hydroxide (Baralyme; Bionetics, Canada) and, finally, web building. through the O2 analyzer of a FOXBOX O2-CO2 respirome- Based on measurements of low heart rate in primitive hunters try system (Sable Systems International, Las Vegas, Nevada). and weaver spiders [Araneaea: Loxoscelidae (Sicariidae) and Data were corrected with respect to standard temperature and Scytodidae], Carrel & Heathcote (1976) propose that these pressure and drift (baseline) and were analyzed using expe- groups would have low metabolic rates, and suggest that this data, version 1.0.3 (Sable Systems International). The curves −1 would be an energy-conserving adaptation in spiders that invest of O2 and CO2 were transformed to flow units (mL h ) with the ̇ ⋅ ⋅ ̇ little effort in prey capture and, consequently, feed only occa- relationships: QO2 = (–60 Q O2/100)/(1 – 0.2095) and QCO2 = ⋅ ⋅ sionally. However, Greenstone & Bennett (1980) report no 60 Q CO2/100, respectively (Withers, 1977). The area under metabolic differences, other than those as a result of body mass, the curve: Vi, i = O2 or CO2 (mL) was measured, representing between spiders of the genus Loxosceles and other araneids. the total O2 consumed and the total CO2 released by the spi- Carrel & Heathcote (1976) suggest that the almost constant ratio ders. Then, O2 consumption and CO2 release were estimated as: ˙ of 2.5 between heart rate and metabolism is indicative for Sicari- Vi = 2(Vi – V0)/t,whereV0 corresponds to the average of the idae and Scytodidae having low resting metabolic rates. By con- area under the curve of the two control syringes. The factor 2 trast, Greenstone & Bennett (1980) reject that idea and suggest originates from testing half of the volume, and t is the exact that heart rate is an unreliable predictor of metabolic rate. experimental time of each individual tested. To resolve these conflicting views, the present study measures the rates of oxygen consumption and carbon dioxide release in the primitive hunters and weaver spiders, the Chilean Recluse Statistical analysis Loxosceles laeta Nicolet (Araneae: Sicariidae) and Chilean Tiger Scytodes globula Nicolet (Araneae: Scytodidae), and Metabolic variables were compared by two-way (species and analyses their relationship(s) with body mass, comparing the temperatures) covariance analysis considering body mass as results with the metabolic data available for other primitive and a covariate. The response variables were log transformed to nonprimitive spiders. satisfy normality and homoscedasticity assumptions studied with Shapiro–Wilk and Bartlett tests, respectively. Allometric relationships between oxygen consumption and body mass for Materials and methods both species were determined using regression analysis.

Twenty-three individuals (13 females and 10 males) of L. laeta (average body mass = 127.55 ± 90.47 mg) and 26 individ- Comparative analysis uals (16 females and 10 males) of S. globula (average body ˙ −1 −1 ˙ mass = 82.79 ± 51.74 mg) were captured during the autumn and For comparative purposes, VO2 (μLg h )andVCO2 spring inside houses of Santiago, Chile. The individuals were (μLg−1 h−1) were measured at 20 ∘C in five individuals of maintained in the laboratory for 2 weeks under an LD 12 : 12 h Dysdera crocata (Aranaea: Dysderidae) (mean body mass photocycle at ambient environmental temperature with food pro- 122.92 ± 41.02 mg), as additional representatives of primitive vided ad libitum consisting of Tenebrio molitor larvae. After a hunters and weavers, as well as two individuals of Phol- lapse of 1 day without a meal because the short specific dynamic cus phalangioides (Aranaea: Pholcidae) (mean body mass action of spiders (Nespolo et al., 2011), a first group of 14 indi- 82.78 ± 8.55 mg), a haplogynae spider species but representing viduals of L. laeta and 16 individuals of S. globula, as well as a web-weaving spiders (Bruvo-Madaric et al., 2005). Also, the ˙ −1 −1 second group of nine individuals of L. laeta and 10 of S. globula, VO2 (μLg h ) of several species of primitive hunters and ˙ were selected randomly and their oxygen consumption (VO2) weavers, comprising the present data on L. laeta and S. globula,

Table 1. Relationships between metabolic rate and body mass for arthropods (mass scaling equations) derived from various studies.

Original relationship REU Source of equation ˙ −1 ˙ −0.29 Log(VO2; μLh ) =−0.133 + 0.710log (Mb in mg) VO2 = 736 Mb Greenstone & Bennett (1980) ˙ −1 −1 −0.408 ˙ −0.408 VO2 (μLg h ) = 947 Mb (Mbinmg) VO2 = 947 Mb Anderson (1974) 0.856 ˙ −0.144 M(μW) = 973 Mb , M the metabolic rate and Mb in g VO2 = 452.5 Mb Lighton et al. (2001)

˙ −1 −1 REU represents the same relationships in equivalent units (VO2 in μLg h and Mb in mg). together with published data of the species L. laeta, Loxosceles ˙ Body mass affected both VO2 (F1,42 = 9.56, P = 0.004) and deserta and Plectreurys spp. (Greenstone & Bennett, 1980) ˙ VCO2 (F1,42 = 4.08, P = 0.049). There was also an effect of exper- and P. phalangioides (present study), were compared with the ˙ imental temperature on both VO2 (F1,42 = 16.48, P = 0.0002) and data of various nonprimitive araneomorph spiders (Greenstone ˙ VCO2 (F1,42 = 21.90, P = 0.00003). There were no differences in & Bennett, 1980) using covariance analysis. Only taxa with the RQ between species (F1,42 = 0.953, P = 0.335) or between two or more data points were included. The primitive group experimental temperatures (F1,42 = 0.05, P = 0.82). included: Sicariidae (brown spiders), Scytodidae (spitting spi- Combining the oxygen consumption values of the two ders), Dysderidae, Pholcidae (daddy long legs spiders) and ∘ ˙ ⋅ −0.46±0.27 species at 20 C, the relationships VO2 = 573.85 Mb Plectreuridae (plectreurid spiders) because these are among ˙ ⋅ −0.41±0.22 and VCO2 = 288.72 Mb were obtained (with metabolic the most generalized of all the haplogyne ecribellate spiders measurements in μLg−1 h−1, and body mass in mg), although (Gertsch, 1958). Group nonprimitive group included: Theridi- the regressions were not significantF ( 1,26 = 2.84, P = 0.103, idae (cobweb weavers), Lyniphiidae (sheetweb weavers), 2 2 ˙ r = 0.12, and F1,26 = 3.45, P = 0.075, r = 0.10 for VO2 and Araneidae (orb weavers), Agenelidae (funnel web weavers), ˙ VCO2, respectively) (Fig. 1). This can be explained by some Oxyopidae (lynx spiders), Thomisidae (crab spiders), Salticidae spiders potentially showing activity inside the measurement (jumping spiders), Lycosidae (wolf spiders) and Gnaphosidae syringe and because only a single measure of metabolic rate and Clubionidae (sac spiders). Also, a cluster analysis was was undertaken. performed with the unweighted pair group method with arith- For D. crocata,theV˙ and V˙ were 97.18 ± 38.00 metic mean using V˙ (μLg−1 h−1) as the response variable and O2 CO2 O2 and 63.57 ± 27.69 μLg−1 h−1, respectively; and, for P. pha- the Euclidean distance. The phylogenetic relationships of the langiodes,theV˙ and V˙ were 187.57 ± 15.79 and spiders used for comparisons were considered by measuring O2 CO2 110.66 ± 34.43 μLg−1 h−1, respectively. the phylogenetic signal in V˙ and performing phylogenetic O2 The mass-specific metabolic rates of L. laeta and S. globula contrast regressions based on phylogenetic hypotheses from were low compared with the expected (published) values for Coddington & Levi (1991), Bell et al. (2005) and Penney et al. spiders and for arthropods of their body mass (Table 3). For (2003). V˙ −1 −1 Oxygen consumption values were compared with the expected example, O2 values in the present study (μLg h ) are 45.1% values for respective body mass obeying mass scaling relation- (S. globula) and 60.2% (for L. laeta) of the expected values, ships according to the relationships of Greenstone & Bennett respectively, according to the mass scaling relationship derived (1980) and Anderson (1994), as based on Carrel & Heathcote from Greenstone & Bennett (1980), and 59.0% (S. globula)and (1976) and Lighton et al. (2001) (Table 1). 82.84% (L.laeta) of the expected values according to Anderson (1994). Using the average of the values of oxygen consumption ∘ ∘ ˙ at 20 and 30 C as a proxy of oxygen consumption at 25 C, VO2 Results (μLg−1 h−1) estimates obtained in the present study were 56.4% (S. globula) and 63.5% (L. laeta), respectively, of the expected ˙ −1 −1 No differences were found in VO2 (μLg h )(F1,42 = 0.28, values derived from the mass scaling relationship of Lighton ˙ −1 −1 P = 0.596) or VCO2 (μLg h )(F1,42 = 1.01, P = 0.319) et al. (2001) (Table 3). ˙ −1 −1 between the species L. laeta and S. globula in the present study. The VO2 (μLg h )inD. crocata was 53.3% of the expected ˙ −1 −1 ˙ Also, there were no differences in VO2 (μLg h )orVCO2 value according to Greenstone & Bennett (1980) and 92.43% −1 −1 ˙ (μLg h ) between the sexes (F1,42 = 2.40, P = 0.124 and of the value according to Anderson (1994); the VO2 of P. pha- F1,42 = 0.40, P = 0.53, respectively) (Table 2). langioides was 91.7% of the expected value from Greenstone &

˙ ˙ Table 2. Oxygen consumption (VO2), CO2 release (VCO2) and respiratory quotient (RQ) of primitive hunters and weaver spiders Scytodes globula and Loxosceles laeta at two temperatures.

∘ ˙ −1 −1 ˙ −1 −1 Species Experimental temperature ( C) VO2 (μLg h ) VCO2 (μLg h )RQ Scytodes globula 20 92.22 ± 54.44 51.52 ± 18.46 0.71 ± 0.47 Loxosceles laeta 20 108.51 ± 108.60 63.01 ± 43.48 0.67 ± 0.33 Scytodes globula 30 177.82 ± 76.15 133.52 ± 41.41 0.74 ± 0.27 Loxosceles laeta 30 172.69 ± 124.00 85.95 ± 49.66 0.58 ± 0.24

˙ −1 −1 Table 3. Comparison of the expected values of VO2 (μLg h )forthe primitive hunters and weaver spiders in the present study assuming the mass scaling relationships by Greenstone & Bennett (1980) and Anderson (1994), as based on Carrel & Heathcote, 1976) and Lighton et al. (2001), respectively (the observed/estimated ratios obtained experimentally are shown in parenthesis).

Greenstone & Anderson Lighton Species Bennett (1980) (1994) et al. (2001)

Loxosceles laeta 180.40 (60.15) 130.99 (82.84) 225.13 (62.45)* Scytodes globula 204.49 (45.09) 156.25 (59.02) 239.58 (56.36)* Dysdera crocata 182.34 (53.30) 132.98 (73.08) — Pholcus phalangioides 204.49 (91.72) 156.26 (120.04) —

˙ Asterisks indicate that, in these cases, the experimental VO2 was calculated as the average between metabolic values at 20 and 30 ∘C.

general allometric tendency was maintained as indicated by the

slope: –0.246 ± 0.132 (F1,13 = 3.45, P = 0.08) (Fig. 3).

Discussion

The resting metabolic rates of the primitive hunters and weaver spiders L. laeta, S. globula and D. crocata are lower (by approximately 60%) than expected for their body mass, regardless of the allometric relationship used in the comparisons. As in other spiders, this could be explained by the use of hydrostatic pressure to maintain body posture instead of the energetically expensive utilization of all muscles (Carrel & Heathcote, 1976; Anderson & Prestwich, 1982; Wilder, 2011). Another expla- nation for the lower rates of metabolism could be the smaller number of mitochondria in the muscle fibres of spiders (Linzen ˙ & Gallowitz, 1975). This low level of resting metabolic rate Fig. 1. (A) Log-log relationship of oxygen consumption (VO2; μLg−1 h−1) and body mass of primitive hunters and weaver spiders Scy- may be an important factor that allows certain species to sur- todes globula and Loxosceles laeta at 20 ∘C. (B) Log-log relationship of vive and save energy for long periods without food (Anderson, ˙ −1 −1 CO2 release (VCO2; μLg h ) and body mass (mg) of S. globula and 1974; Tanaka & Ito, 1982; Nentwig, 2013). Also, spiders are L. laeta at 20 ∘C. able to reduce their metabolic rates to lower values than usual during periods of food restriction, which can reach values close Bennett (1980) and 120.04% of the derived value from Ander- to 50% of those for a well-fed spider (Ito, 1964; Miyashita, 1969; son (1994). In these cases, the expected values according to the Anderson, 1974; Tanaka & Ito, 1982; Canals et al., 2007; Stoltz mass scaling relationship from Lighton et al. (2001) were not et al., 2010; Canals et al., 2011). calculated because this relationship is for arthropods at 25 ∘C. Most spiders are able to raise their metabolism above the ˙ −1 −1 ∘ The average VO2 (μLg h )at20 C of the primitive group resting rates by two- to six-fold (Anderson & Prestwich, (all measurements) was lower than that of the nonprimitive 1982; Prestwich, 1983a, 1983b; Nespolo et al., 2011; Canals group (F1,76 = 3.91, P = 0.05), although without differences in et al., 2012); however, web building spiders may increase their the slopes (F1,76 = 0.94, P = 0.13). A weak but significant phylo- metabolic rate above resting levels by almost ten- to 20-fold ˙ −1 −1 genetic signal in VO2 (μLg h ) was found (Moran’s I = 0.034, when building a web (Wilder, 2011). P = 0.02). Cluster analysis showed that, from a metabolic point Discounting the effect of the body mass, the present study of view, there are three clusters: (i) Dysderidae–Sicariidae– finds no effect of sex on the resting metabolic rate; however, Clubionidae–Plectreuridae–Scytodidae–Gnaphosidae; (ii) other studies report differences attributable to high energetic Pholcidae–Thomisidae–Agelenidae–Lycosidae–Oxiopidae– requirements of males during the reproductive period (Watson Salticidae–Araneidae; and (iii) Lyniphiidae–Theridiidae. The & Lighton, 1994; Kotiaho, 1998; Uetz et al., 2002; Lomborg & first cluster includes mainly primitive hunters and weaver Toft, 2009). This may be explained by the fact that spiders are spiders and the second and third clusters include active analyzed during the nonbreeding season in the present study. ˙ predators and web weaving spiders (Fig. 2). Analyzing VO2 The estimates of Q10 reported in the present study are not mea- (μLg−1 h−1) as a function of body mass in all spiders yields sured directly in the analyzed species because the individuals ∘ ∘ a slope: –0.248 ± 0.146 (F1,13 = 2.88, P = 0.11). The slope measured at 20 C are different from those measured at 30 C, is similar when excluding primitive spiders: –0.224 ± 0.123 and the Q10 reflects the capacity of change in metabolic rate (F1,9 = 3.31, P = 0.10). When correcting by phylogeny, the relative to changes in temperature, considered as an individual

Fig. 3. (A) Log-log relationship of oxygen consumption (VO2; μLg−1 h−1) and body mass (mg) of spider families (Primitive and nonprimitive groups) at 20 ∘C. Only taxa with two or more points were included in the regression analysis of groups. The nonprimitive Fig. 2. (A) Phylogenetic relationships of the spider families considered group (white circles and line) comprises Theridiidae (cobweb weavers), for metabolic comparisons. Based on Coddington & Levi (1991), Bell Lyniphiidae (sheetweb weavers), Araneidae (orb weavers), Agenelidae ˙ (funnel web weavers), Oxyopidae (lynx spiders), Thomisidae (crab spi- et al. (2005) and Penney et al. (2003). (B) Cluster analysis of VO2 (μLg−1 h−1) in these spider families based on the unweighted pair group ders) and Salticidae (jumping spiders). The primitive group (black cir- method with arithmetic mean and Euclidean distances. cles, without line because it was not significant) included Sicariidae (brown spiders), Scytodidae (spitting spiders), Dysderidae and Plec- treuridae. Points from spider families not included in regression anal- attribute (Nespolo et al., 2003). Nevertheless, broad estimates yses comprise Lycosidae (white hexagon), Pholcidae (white square), ˙ of Q10 in the present study are derived from the ratio of VO2 Gnaphosidae (white rhombus) and Clubionidae (white triangle). (B) ∘ ˙ ∘ between 30 and 20 C and ratio of VCO2 between 30 and 20 C. Phylogenetic contrast of log-log relationship of oxygen consumption ˙ −1 −1 These are 1.92 and 2.59 for S. globula and 1.59 and 1.36 for L. (VO2; μLg h ) and body mass (mg) of all primitive and nonprimitive ∘ laeta, respectively. Values ranging from 1.35 to 3 are reported groups of spider families at 20 C. in various arachnids and insects (Anderson, 1970; Prestwich & Walker, 1981; Ashby, 1997; Davis et al., 1999; Rogowitz & finds that primitive hunters and weaver spiders have a resting Chappell, 2000; Rourke, 2000; Schmitz & Perry, 2001). metabolic rate lower than the nonprimitive group, in agreement The RQ value measured in the present study is approximately with the hypothesis of Carrel & Heathcote (1976), which is 0.7 in L. laeta and S. globula, suggesting the metabolism of based on the low heart rate of species of the Scytodidae and predominantly lipids, as expected according to the prey offered Sicariidae families compared with eight other araneomorph spi- during the pre-experimental period and according to the prey der families. This lower basal metabolic rate in primitive hunters that these spiders usually eat (small arthropods). and weaver spiders may have evolved in association with their ˙ The VO2 of D. crocata is also low, and similar to of the values life style and, in particular, their sit and wait predatory strat- ˙ for S. globula and L. laeta.However,theVO2 of P. phalan- egy in unpredictable environments with low prey availability, gioides is approximately equal or even superior to that expected similar to that proposed for mygalomorph spiders (Greenstone ˙ for its body mass. Despite the high VO2 in P. phalangioides,the & Bennett, 1980; Shillington, 2002; Canals et al., 2007, 2011). comparison made between primitive and nonprimitive groups It is interesting that Greenstone & Bennett (1980) reject the

© 2015 The Royal Entomological Society, Physiological Entomology, doi: 10.1111/phen.12108 6 M. Canals et al. hypothesis of Carrel & Heathcote (1976), arguing that heart rate Acknowledgements is a bad predictor of metabolism. However, the findings from the present study are in agreement with Carrel & Heathcote We thank Lafayette Eaton for his review of the English and (1976), even when including the nine values for L. laeta and helpful comments on the manuscript submitted for publication. two for L. deserta from the study by Greenstone & Bennett The present study was funded by a FONDECYT 1110058 grant (1980) together with the present data. Also, the results for to M.C. ˙ ∘ −1 −1 L. laeta (mean VO2 at 20 C; μLh g ) from the present study are not different from those of Greenstone & Bennett (1980): 108.51 ± 108.60 (present study) versus 138.52 ± 34.52 References (Greenstone & Bennett, 1980), respectively. This implies that the differences between the conclusions of the present study Alfaro, C., Veloso, C., Torres-Contreras, H. et al. (2013) Thermal niche and that of Greenstone & Bennett (1980) are not explained by overlap of the brown recluse spider Loxosceles laeta (Araneae; Sicariidae) and its possible predator, the spitting spider Scytodes differences in metabolic rate values but rather by the increased globula (Scytodidae). Journal of Thermal Biology, 38, 502–507. sample size of spiders analyzed. Anderson, J.F. (1970) Metabolic rates of spiders. Comparative Biochem- The present study detects a weak phylogenetic signal in istry and Physiology, 33, 51–72. the metabolic rate, which may be explained by the primitive Anderson, J.F. (1974) Responses to starvation in the spiders Lycosa lenta group being composed of only Haploginae spiders. These are (Hentz) and Filistata hibernalis (Hentz). Ecology, 55, 576–585. mainly primitive spiders with low fertility (Fernandez et al., Anderson, J.F. (1994) Comparative energetics of comb-footed spiders 2002; Canals & Solís, 2014) and low energetic cost strategies (Araneae: theridiidae). Comparative Biochemistry and Physiology compared with the nonprimitive group that includes spiders of Part A, Comparative Physiology, 109, 181–189. the RTA clade and orbweb spiders that are characterized by high Anderson, J.F. & Prestwich, K.N. (1982) Respiratory gas exchange in energetic costs of web building and high fertility (Blackledge spiders. Physiological Zoology, 55, 72–90. Ashby, P.D. (1997) Conservation of mass-specific metabolic rate among et al., 2009). Cluster analysis not only shows that all haplogynae high- and low- elevation populations of the acridid grasshopper spiders (excepting Pholcidae) are clustered in a single group, Xanthippus corallipes. Physiological and Biochemical Zoology, 70, but also that the ‘entelegyneae sac’ spiders (Clubionidae) and 701–711. ground spiders (Gnaphosidea) are included in this group. 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