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Energy metabolism and the postprandial response of the Chilean tarantulas, Euathlus truculentus (Araneae: Theraphosidae)
Comparative Biochemistry and Physiology, Part A 159 (2011) 379–382
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Comparative Biochemistry and Physiology, Part A j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / c b p a
Energy metabolism and the postprandial response of the Chilean tarantulas, Euathlus truculentus (Araneae: Theraphosidae) Roberto F. Nespolo a,⁎, Loreto Correa a, Cristian X. Pérez-Apablaza b, Pablo Cortés a, José L. Bartheld a a b
Instituto de Ecología y Evolución, Facultad de Ciencias, Universidad Austral de Chile, Campus Isla Teja, Valdivia, Chile Centro de Rehabilitación de Fauna “Casa Noé. Mundo Animal” Camino a San Antonio 044, Linares, Chile
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Article history: Received 27 January 2011 Received in revised form 7 April 2011 Accepted 7 April 2011 Available online 17 April 2011 Keywords: Specific dynamic action Arachnida Standard metabolic rate Repeatability
a b s t r a c t One of the most ubiquitous consequences of feeding in animals is specific dynamic action (SDA), a drastic increment in metabolic rate after a meal, which lasts from a few hours to several days. According to a recent exhaustive review by Secor (2009), studies in SDA are abundant, encompassing all kinds of vertebrates and invertebrates. However, important exceptions are arachnids, as few studies have characterized SDA in this group. Here, we measured the standard metabolic rate (SMR) of the Chilean tarantulas Euathlus truculentus (body mass = 7.32± 0.7 g; N = 32; TA = 25 °C), its inter-individual variation (i.e., repeatability) and its SDA. We measured SMR three or four times in each individual, and we also conducted predation experiments where a prey was consumed by each spider, during a respirometry trial. The SMR of E. truculentus was 0.00049 ± 0.000079 mlCO2 g−1 min−1 which corresponds to 1524 μW (assuming a protein-based diet), 108.4% of the predicted value for arachnids. According to the standard nomenclature for SDA studies, the scope of the SDA for a meal size of 1.26± 0.04 g (18% of the spider size) was 6.55 ± 1.1 times the baseline, the time to peak was 45 min, and the magnitude of the SDA was 0.28± 0.03 kj, which is 85% of the expected value for invertebrates. Our SMR data are in concordance with previous findings suggesting remarkably low energy metabolism in arachnids, compared with other arthropods. On the other hand, the exceedingly high scope of the postprandial response contrasts with the comparatively low SDA. This fact suggests that spiders spend most of the energy for digestion in a short period after prey capture, which could be a consequence of their external digestion. © 2011 Elsevier Inc. All rights reserved.
1. Introduction In order to fulfill the energy requirements of maintenance, growth and reproduction, animals need to obtain their nutrient from autotrophic organisms or by consuming other animals (Weiner, 1992). The later strategy, also known as predation, entails the costs of searching for, catching and manipulating the prey, but has the benefit of more complete and rich source of nutrients (Sibly and Calow, 1986). Several metabolic responses are related with the process of searching, capturing and digesting the prey. However, the metabolic elevation that follows feeding, also known as the specific dynamic action (SDA), is the one that has attracted most of the interest of physiological ecologists (Chappell et al., 1997; MacArthur and Campbell, 1994; Nespolo et al., 2003; Rosen and Trites, 1997; Secor, 2009; Secor and Diamond, 2000; Secor and Nagy, 1994). The SDA consists in an increase of energy metabolism after a meal, ranging from 20% to 300% above resting levels, and lasting from a few hours to several days or weeks (Lighton and Fielden, 1995; Secor, 2009). This response is a consequence of the processes of digestion
⁎ Corresponding author. Tel.: + 56 63 221704; fax: + 56 63 221344. E-mail address: [email protected] (R.F. Nespolo). 1095-6433/$ – see front matter © 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.cbpa.2011.04.003
and absorption, which entail important energy costs. According to the comprehensive review of Secor (2009), hundreds of experimental studies have been published to date describing SDA in a wide range of animals. These studies indicate that this response is taxa and meal specific. Others factors that affect the magnitude and duration of SDA are body size, meal temperature and size, and ambient temperature in ectotherms (see Secor, 2009). Despite the large number of studies addressing SDA in animals, less than 30% have been performed in invertebrates and only 3 in arachnids (Young and Block, 1980; Jensen et al., 2010; Shillington, 2010). For instance, Jensen et al. (2010) reported for the wolf spider (Pardosa prativagaa) a meal size of 8.5% of spider mass, a postpandrial metabolic scope of 4 times within the 3-h period after prey ingestion and a SDA coefficient of 21%. Arachnids, and especially tarantulas (Araneae: Theraphosidae), are sit-and-wait predators that attack their prey by surprise and exhibit low standard metabolic rate (SMR), compared with other arthropods (Anderson, 1970; Greenstone and Bennett, 1980; Lighton and Fielden, 1995; Lighton and Joos, 2002). This relatively low metabolic rate has been attributed to an adaptation related with this mode of foraging, as they need to minimize maintenance costs with such unpredictable source of food (Anderson, 1970, 1974; Lighton et al., 2001, Shillington, 2005, Canals et al., 2008). The general framework to infer the adaptative value of a trait is to test whether there exists a consistent correlation
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between the trait and fitness and that it exhibits significant heritability (Falconer and Mackay, 1996; Chown et al., 2006). A preliminary assessment of heritability is repeatability. Repeatability is defined as the consistency of a trait over time, and is measured by the intraclass correlation coefficient from multiple measurements and variance decomposition (Lessells and Boag, 1987; Nespolo and Franco, 2007). This coefficient can be interpreted as the upper bound for heritability (Falconer and Mackay, 1996), gives an idea of how the trait can respond to natural selection and tells whether it is also correlated with other traits (Maciak and Konarzewski, 2010). This work was aimed in order to explore the SDA in a predatory spider, the Chilean tarantula (Euathlus truculentus). We designed this study with three aims: (1) to determine the standard metabolic rate (SMR) of this species in order to compare it with the expectation for arachnids; (2) to compute the repeatability of SMR in order to evaluate the inter-individual variation in this trait and (3) to measure SDA in records after a predation event. 2. Materials and methods
cricket was confined in a small metallic cage that was attached to the chamber walls by a magnet located outside the chamber. Then, the record started with both animals located in the chamber, but physically separated and we could eliminate the separation (by removing the magnet) after 15 min of resting measurement, without opening the chamber or stopping the record. By direct observation, we could identify the moment of prey capturing and the metabolic elevation that followed. Although we tried to induce predation events with all the 32 spiders, we only obtained 10 records in which the spider successfully captured and killed the cricket in the first half hour after the release. We discarded all the remainder records, with the exception of those were the same spider was recorded but did not attack and consume the cricket, to use them for comparative purposes. In other words, for each 1 of the 10 spiders, we present a complete metabolic measurement with predation and another without predation (i.e., where the cricket survived) using a cricket of similar size. We recorded the mass of the spider before each predation experiment, as well as the mass of the cricket. We also weighed the leftovers of the cricket at the end of each experiment, which were 26.8 ±2% (mean ±SE) of the live cricket.
We captured 32 adults Chilean tarantulas (Euathlus truculentus) from central Chile (MB = 7.3 ± 0.72 g), which were maintained in the laboratory at 20 °C, in small plastic cages of 10 × 10 × 5 cm with bedding and fed with Chilean red crickets (Cratomelus armatus) and mealworms (Tenebrio molitor) every 2 days. We also captured from the field, male crickets (C. armatus, MB = 1.72 ± 0.13 g) as prey in the measurements of postprandial metabolism. The Chilean fauna of theraphosids is diverse, including possibly more than 20 species (C. Perez-Apablaza, personal communication); however we were unable to find more than two specialized publications regarding any aspect their biology. These are the works of Canals and collaborators (Canals et al., 2008; Figueroa et al., 2010), which describe respiration and evaporative water loss of two species of Chilean theraphosids. E. truculentus is a medium-sized tarantula (ca. 8 cm of length, without appendages; 7 g of weight), that lives in semi-arid scrublands and also in the low parts of the Andes range, in central Chile (between 32° and 39° S).
2.3. SDA variables
2.1. Respirometry
All statistical analyses were performed with Statistica 7.0. The intraclass correlation coefficient was computed as τ = (between individual variance component) / (total phenotypic variance) from a standard variance-component analysis. In the predation experiments, we computed one-way ANOVA and Tukey post hoc tests to compare metabolic rate of each hour after prey capturing, with the SMR of the spider (=baseline, according to Secor, 2009).
Our respirometry system was similar to the one described in Lighton and Turner (2004). We measured carbon dioxide production (VCO2 as mL min−1 at 25 °C) of spiders using open system respirometry. Ambient air was passed (400± 4 mL min−1) through a column of Drierite/soda lime to remove water vapour and CO2 before entering metabolic chambers (1 L). Carbon dioxide levels of excurrent air from the chambers were measured with an infra-red CO2 analyzer (model Li 6251, LI-COR). The CO2 analyzer was calibrated periodically using a controlled gas mixture. Each trial was recorded with a computer, using the Expe Data (Sable Systems) software. We quantified SMR from hour long measurements of VCO2 taken between 9 AM to 4 PM when the spiders are naturally inactive. From each record, we selected the lowest, constant 5-min measurements. For each spider, we repeated measurements of SMR at 2 week intervals until we had three or four measurements for each spider. This data allowed us to assess repeatability of SMR as the intraclass correlation coefficient (see below). Because in most invertebrates, the post-absorptive state is achieved in after 5 days (Shillintgon, 2005; Secor, 2009) all spiders were fasted during 1 week before metabolic measurements, see below). 2.2. Predation experiments We induced predation by placing together a live cricket and the spider in the same chamber used for SMR measurements (TA =25 ±1 °C). Records were obtained during the active period for this species (nightime). Whereas the spider could freely move in the chamber, the
The energy content of the crickets was estimated using pump calorimetry (Instituto de Producción Animal, Universidad Austral de Chile). From predation trials, and according to Secor (2009), we computed the meal size as the difference between the mass of the prey and the remainders of the prey after predation. We also estimated the postprandial metabolic scope as the maximum value of metabolism (=peak metabolic rate) divided by the baseline (the SMR of the spider alone). Also, we estimated time to peak as the duration of time of feeding to peak metabolic rate and duration of the postprandial response as the time from feeding to when metabolic rate was not longer significantly greater than baseline (Secor, 2009). Finally, SDA was calculated as the area below the curve and above SMR base line in each metabolic trial (see Secor, 2009). 2.4. Statistics
3. Results 3.1. Standard metabolic rate The standard metabolic rate (SMR) of E. truculentus (body mass = 7.32 ± 0.7 g; N = 32) was 0.00049 ± 0.000079 mlCO2 g−1 min−1 (measurements of the first trial). The outcome of the variancecomponent analysis for repeatability (32 individuals, measured three or four times) was non-significant (F27,51 = 0.94; P = 0.56) and near-zero estimations of the intraclass correlation coefficient were obtained (i.e., repeatability of SMR was near zero). 3.2. Predation experiments All spiders survived the experiment, and increased body mass during their stay in the laboratory. During predation trials, when the spider captured the prey, the cricket died almost instantaneously, as it was visibly smashed by the chelicerae. The meal size was 1.26 ± 0.04 g cricket wet mass (18.3 ± 2.9% of the spider mass). The energy content of the crickets was 29.3 kj/g dry mass. Then, the energy content of the meal
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was 9.5±0.7 kj. The baseline of the postprandial response was the SMR of the spiders, indicated before (see also Fig. 1). The postprandial peak in VCO2, reached 45 min after prey capture, was 0.0031±0.0003 mL g−1 min−1, 6.55±1.1 times SMR. The duration of the postprandial response was 8 h. The magnitude of the SDA was 9.54±1.1 mLCO2 (N=10), assuming a diet of pure protein, the SDA turns into 0.28±0.03 kj and the SDA coefficient was 3% for a 7.3±0.7 g adult spider mass. Thus, 3% of the ingested energy was respired due to the obligatory costs of meal digestion and assimilation.
4. Discussion 4.1. Repeatability In this study, we found that the standard metabolic rate (SMR) of the Chilean tarantula is lower in comparison with arthropods in
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Time (h) Fig. 1. Metabolic rate measured as the rate of carbon dioxide production (VCO2; mean±SE), in (N=10) individuals of Chilean tarantulas, Euathlus truculentus (MB =7.3±0.72 g) which were offered a single (alive) prey of Cratomelus armatus crickets (MB =1.4±0.15 g). The test consisted in maintaining physically separated the spider and the cricket in the chamber during the first hour of measurement, and releasing the cricket in order to let the spider to capture it without interrupting the record. Upper panel: the spiders captured the prey (in all cases, the attack occurred during the first 30 min after the release, and the cricket died almost instantaneously, see text for details). Lower panel: the spiders (same individuals as in the upper panel) did not eat, and the cricket remained alive, together with the spider, within the chamber during the complete trial. Asterisks denote significant differences between baseline (SMR of the spider) and the metabolic rate at each hour after meal consumption (after a Tukey post-hoc test, and one-way ANOVA). In the lower panel, although the metabolic elevation after the release of the cricket is lower than in the upper panel (because there was no feeding), the rest of the record never reach the baseline level (i.e., the SMR of the spider) because the cricket remained alive within the chamber.
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general (Lighton et al., 2001). Also, our values of SMR (at TA = 25 °C) are similar with other studies in other Chilean theraphosids (Figueroa et al., 2010) and somewhat higher than other species around the world (Shillington, 2005). In fact, assuming a protein-based diet (Walsberg and Wolf, 1995; Willmer et al., 2005), the SMR of E. truculentus (7.3 ± 0.7 g) is 1524 μW, which is 108.4% of the predicted value for arachnids, according to the allometric equation provided by Lighton et al. (2001). However, and contrary to what is known for energy metabolism in other animals including insects (Nespolo and Franco, 2007), and also in other arachnids (Lardies et al., 2008; Terblanche et al., 2004), SMR exhibits low (non-significant) repeatability. Repeatability studies have provided important clues into the nature of phenotypic variation in animal populations (Boake, 1989; Lessells and Boag, 1987), since they indicate whether a trait exhibit consistent variation, which reflects interindividual variation within populations. Then, repeatability studies have become of common use by physiological and evolutionary ecologists (see Nespolo and Franco, 2007, and references therein). Although the repeatability of energy metabolism, both in vertebrates and invertebrates in general is high, some authors have found low and non-significant estimations in some species (Russel and Chappell, 2007). Low repeatability represents low inter-individual variation (i.e., the ranking of trait values in the population is not maintained over time), which would be the case of Chilean tarantulas. The common rationale to interpret this kind of finding is that the trait is fixed because of past directional or stabilizing selection (Nespolo and Franco, 2007). This is consistent with the idea of an adaptation for sit-and-wait predatory behaviour: animals needs to minimize maintenance costs in order to economize energy expenditure (Lighton and Fielden, 1995; Shillington, 2005). According to this logic, natural selection would have acted directionally on reducing SMR, which in turn would have eroded genetic variation in this trait. As a consequence, near-zero repeatability in SMR would be found, as our results suggest. However, additional information would be needed in order to confirm this conclusion, as repeatability is just a preliminary assessment of the upper bound of heritability (see Dohm, 2002). Other explanation to the low repeatability that we found can be some practical problems associated with the measurement, such as residual error and an erroneous choice of the ecologically relevant time frame for the measurement (Arnold et al., 1995). This is important as tarantulas life span can reach up to 20 years (Anderson, 1974; Locht et al., 1999). Other arachnids (with varied modes of foraging) also exhibit low SMR, and the provided explanations to such pattern are diverse. For instance, Lighton et al. (2001) proposed that the low maintenance metabolism of scorpions would be an adaptation to live in ecosystems characterized by low primary productivity. Canals et al. (2008), on the other hand, found that the book lungs of mygalomorph spiders are exceedingly efficient in oxygen extraction, which contrasts with the low SMR they exhibit. Similarly, Terblanche et al. (2004) assumed that the low (but repeatable) metabolic rate in the whip-spider is due to its sedentary habits. Other authors have attributed the low SMR of some arachnids (harvestman) to their fossorial mode of life (Lardies et al., 2008) or to the sit-and-wait lifestyle of some ticks (Lighton and Fielden, 1995). This varied interpretation of a common pattern warrants further research into the causes of low metabolic rates in arachnids, especially to determine whether this pattern is a generalized characteristic of the clade, or an adaptation for certain modes of life. 4.2. Specific dynamic action (SDA) Since only 3 studies addressing the specific dynamic action of spiders have been published so far (Young and Block, 1980; Jensen et al., 2010; Shillington, 2010) and the magnitude and duration of the SDA response can be significantly affected by several factors (Secor, 2009) it is difficult to contrast our results with previously published works. Taking this into consideration our results suggest that the SDA to feeding in the Chilean
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tarantulas is relatively short (8 h), compared with other predatory species (Secor, 2009). However, the duration of the postprandial response in carnivorous invertebrates could range from 3 to 300 h (Secor, 2009). The SDA scope that we found, which is up to 600% baseline levels, whereas it ranges from 150 to 350% in most invertebrates (Secor, 2009) and higher to the 400% observed by Jensen et al. (2010). The meal size is comparatively large (18.3% of spider mass) which partially explain the great metabolic increment that we found and the high magnitude of SDA. In fact, the predicted SDA value according to the allometric equation for invertebrates (Secor, 2009, pp. 12), and our values of spider and meal mass is 0.32 kj. Given that our computed SDA was 0.28 ± 0.03 kj, the SDA of E. truculentus is 87.5 ± 0.07% of the expected value for invertebrates. 4.3. Possible confounding effects of living prey It could be argued that the response of the spiders in our experiments was confounded with metabolic rate of the crickets. This is true to a certain point, since our observations suggest that crickets died within the first hour of measurement (and the metabolic elevation was maintained several more hours). However, we are aware of the fact that the need of providing living prey (that has their own metabolic rate) to the spiders potentially can complicate our experimental settings and interpretations. Because of this reason, we included in the analysis the replicated measurements of the spider and a cricket of similar size, where predation did not occur. In these records the spiders did not consume the prey (mostly because they could not catch the cricket in the first place, and then they remained quiet), and show a small metabolic increase just after cricket release, which can be attributed to the stress of pursuing/escaping. This increase is considerable lower than the SDA response in the records where predation occurred, and ends after the third hour of measurement. The high scope of the postprandial response that we found suggests that Chilean tarantulas spend most of the energy for digestion in a short period after capture. The postprandial response of Chilean tarantula E. truculentus suggests that these arthropods exhibit perhaps different patterns of energy expenditure during digestion, compared with other predatory animals. It is possible that since they need to inject the prey with proteolytic enzymes, instead of swallowing it, changes the time-course of the postprandial response as described in this work. However, further studies are needed to confirm our findings, in order to determine the generality of the energy pattern of digestion in arachnids. Acknowledgements This work was funded by FONDECYT grant 1090423. We thank Bruno Todeschini for help with the experimental setup and spider maintenance. Loreto Correa, Pablo Cortés and José L. Bartheld thank a Conicyt fellowship. References Anderson, F., 1970. Metabolic rates of spiders. Comp. Biochem. Physiol. A 33, 51–72. Anderson, F., 1974. Responses to Starvation in the Spiders Lycosa lenta and Filistata hibernalis. Ecology 55, 576–585. Arnold, S., Peterson, C., Gladstone, J., 1995. Behavioural variation in natural populations. VII. Maternal body temperature does not affect juvenile thermoregulation in a garter snake. Anim. Beh 50, 623–633.
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Contents lists available at ScienceDirect
Comparative Biochemistry and Physiology, Part A j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / c b p a
Energy metabolism and the postprandial response of the Chilean tarantulas, Euathlus truculentus (Araneae: Theraphosidae) Roberto F. Nespolo a,⁎, Loreto Correa a, Cristian X. Pérez-Apablaza b, Pablo Cortés a, José L. Bartheld a a b
Instituto de Ecología y Evolución, Facultad de Ciencias, Universidad Austral de Chile, Campus Isla Teja, Valdivia, Chile Centro de Rehabilitación de Fauna “Casa Noé. Mundo Animal” Camino a San Antonio 044, Linares, Chile
a r t i c l e
i n f o
Article history: Received 27 January 2011 Received in revised form 7 April 2011 Accepted 7 April 2011 Available online 17 April 2011 Keywords: Specific dynamic action Arachnida Standard metabolic rate Repeatability
a b s t r a c t One of the most ubiquitous consequences of feeding in animals is specific dynamic action (SDA), a drastic increment in metabolic rate after a meal, which lasts from a few hours to several days. According to a recent exhaustive review by Secor (2009), studies in SDA are abundant, encompassing all kinds of vertebrates and invertebrates. However, important exceptions are arachnids, as few studies have characterized SDA in this group. Here, we measured the standard metabolic rate (SMR) of the Chilean tarantulas Euathlus truculentus (body mass = 7.32± 0.7 g; N = 32; TA = 25 °C), its inter-individual variation (i.e., repeatability) and its SDA. We measured SMR three or four times in each individual, and we also conducted predation experiments where a prey was consumed by each spider, during a respirometry trial. The SMR of E. truculentus was 0.00049 ± 0.000079 mlCO2 g−1 min−1 which corresponds to 1524 μW (assuming a protein-based diet), 108.4% of the predicted value for arachnids. According to the standard nomenclature for SDA studies, the scope of the SDA for a meal size of 1.26± 0.04 g (18% of the spider size) was 6.55 ± 1.1 times the baseline, the time to peak was 45 min, and the magnitude of the SDA was 0.28± 0.03 kj, which is 85% of the expected value for invertebrates. Our SMR data are in concordance with previous findings suggesting remarkably low energy metabolism in arachnids, compared with other arthropods. On the other hand, the exceedingly high scope of the postprandial response contrasts with the comparatively low SDA. This fact suggests that spiders spend most of the energy for digestion in a short period after prey capture, which could be a consequence of their external digestion. © 2011 Elsevier Inc. All rights reserved.
1. Introduction In order to fulfill the energy requirements of maintenance, growth and reproduction, animals need to obtain their nutrient from autotrophic organisms or by consuming other animals (Weiner, 1992). The later strategy, also known as predation, entails the costs of searching for, catching and manipulating the prey, but has the benefit of more complete and rich source of nutrients (Sibly and Calow, 1986). Several metabolic responses are related with the process of searching, capturing and digesting the prey. However, the metabolic elevation that follows feeding, also known as the specific dynamic action (SDA), is the one that has attracted most of the interest of physiological ecologists (Chappell et al., 1997; MacArthur and Campbell, 1994; Nespolo et al., 2003; Rosen and Trites, 1997; Secor, 2009; Secor and Diamond, 2000; Secor and Nagy, 1994). The SDA consists in an increase of energy metabolism after a meal, ranging from 20% to 300% above resting levels, and lasting from a few hours to several days or weeks (Lighton and Fielden, 1995; Secor, 2009). This response is a consequence of the processes of digestion
⁎ Corresponding author. Tel.: + 56 63 221704; fax: + 56 63 221344. E-mail address: [email protected] (R.F. Nespolo). 1095-6433/$ – see front matter © 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.cbpa.2011.04.003
and absorption, which entail important energy costs. According to the comprehensive review of Secor (2009), hundreds of experimental studies have been published to date describing SDA in a wide range of animals. These studies indicate that this response is taxa and meal specific. Others factors that affect the magnitude and duration of SDA are body size, meal temperature and size, and ambient temperature in ectotherms (see Secor, 2009). Despite the large number of studies addressing SDA in animals, less than 30% have been performed in invertebrates and only 3 in arachnids (Young and Block, 1980; Jensen et al., 2010; Shillington, 2010). For instance, Jensen et al. (2010) reported for the wolf spider (Pardosa prativagaa) a meal size of 8.5% of spider mass, a postpandrial metabolic scope of 4 times within the 3-h period after prey ingestion and a SDA coefficient of 21%. Arachnids, and especially tarantulas (Araneae: Theraphosidae), are sit-and-wait predators that attack their prey by surprise and exhibit low standard metabolic rate (SMR), compared with other arthropods (Anderson, 1970; Greenstone and Bennett, 1980; Lighton and Fielden, 1995; Lighton and Joos, 2002). This relatively low metabolic rate has been attributed to an adaptation related with this mode of foraging, as they need to minimize maintenance costs with such unpredictable source of food (Anderson, 1970, 1974; Lighton et al., 2001, Shillington, 2005, Canals et al., 2008). The general framework to infer the adaptative value of a trait is to test whether there exists a consistent correlation
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between the trait and fitness and that it exhibits significant heritability (Falconer and Mackay, 1996; Chown et al., 2006). A preliminary assessment of heritability is repeatability. Repeatability is defined as the consistency of a trait over time, and is measured by the intraclass correlation coefficient from multiple measurements and variance decomposition (Lessells and Boag, 1987; Nespolo and Franco, 2007). This coefficient can be interpreted as the upper bound for heritability (Falconer and Mackay, 1996), gives an idea of how the trait can respond to natural selection and tells whether it is also correlated with other traits (Maciak and Konarzewski, 2010). This work was aimed in order to explore the SDA in a predatory spider, the Chilean tarantula (Euathlus truculentus). We designed this study with three aims: (1) to determine the standard metabolic rate (SMR) of this species in order to compare it with the expectation for arachnids; (2) to compute the repeatability of SMR in order to evaluate the inter-individual variation in this trait and (3) to measure SDA in records after a predation event. 2. Materials and methods
cricket was confined in a small metallic cage that was attached to the chamber walls by a magnet located outside the chamber. Then, the record started with both animals located in the chamber, but physically separated and we could eliminate the separation (by removing the magnet) after 15 min of resting measurement, without opening the chamber or stopping the record. By direct observation, we could identify the moment of prey capturing and the metabolic elevation that followed. Although we tried to induce predation events with all the 32 spiders, we only obtained 10 records in which the spider successfully captured and killed the cricket in the first half hour after the release. We discarded all the remainder records, with the exception of those were the same spider was recorded but did not attack and consume the cricket, to use them for comparative purposes. In other words, for each 1 of the 10 spiders, we present a complete metabolic measurement with predation and another without predation (i.e., where the cricket survived) using a cricket of similar size. We recorded the mass of the spider before each predation experiment, as well as the mass of the cricket. We also weighed the leftovers of the cricket at the end of each experiment, which were 26.8 ±2% (mean ±SE) of the live cricket.
We captured 32 adults Chilean tarantulas (Euathlus truculentus) from central Chile (MB = 7.3 ± 0.72 g), which were maintained in the laboratory at 20 °C, in small plastic cages of 10 × 10 × 5 cm with bedding and fed with Chilean red crickets (Cratomelus armatus) and mealworms (Tenebrio molitor) every 2 days. We also captured from the field, male crickets (C. armatus, MB = 1.72 ± 0.13 g) as prey in the measurements of postprandial metabolism. The Chilean fauna of theraphosids is diverse, including possibly more than 20 species (C. Perez-Apablaza, personal communication); however we were unable to find more than two specialized publications regarding any aspect their biology. These are the works of Canals and collaborators (Canals et al., 2008; Figueroa et al., 2010), which describe respiration and evaporative water loss of two species of Chilean theraphosids. E. truculentus is a medium-sized tarantula (ca. 8 cm of length, without appendages; 7 g of weight), that lives in semi-arid scrublands and also in the low parts of the Andes range, in central Chile (between 32° and 39° S).
2.3. SDA variables
2.1. Respirometry
All statistical analyses were performed with Statistica 7.0. The intraclass correlation coefficient was computed as τ = (between individual variance component) / (total phenotypic variance) from a standard variance-component analysis. In the predation experiments, we computed one-way ANOVA and Tukey post hoc tests to compare metabolic rate of each hour after prey capturing, with the SMR of the spider (=baseline, according to Secor, 2009).
Our respirometry system was similar to the one described in Lighton and Turner (2004). We measured carbon dioxide production (VCO2 as mL min−1 at 25 °C) of spiders using open system respirometry. Ambient air was passed (400± 4 mL min−1) through a column of Drierite/soda lime to remove water vapour and CO2 before entering metabolic chambers (1 L). Carbon dioxide levels of excurrent air from the chambers were measured with an infra-red CO2 analyzer (model Li 6251, LI-COR). The CO2 analyzer was calibrated periodically using a controlled gas mixture. Each trial was recorded with a computer, using the Expe Data (Sable Systems) software. We quantified SMR from hour long measurements of VCO2 taken between 9 AM to 4 PM when the spiders are naturally inactive. From each record, we selected the lowest, constant 5-min measurements. For each spider, we repeated measurements of SMR at 2 week intervals until we had three or four measurements for each spider. This data allowed us to assess repeatability of SMR as the intraclass correlation coefficient (see below). Because in most invertebrates, the post-absorptive state is achieved in after 5 days (Shillintgon, 2005; Secor, 2009) all spiders were fasted during 1 week before metabolic measurements, see below). 2.2. Predation experiments We induced predation by placing together a live cricket and the spider in the same chamber used for SMR measurements (TA =25 ±1 °C). Records were obtained during the active period for this species (nightime). Whereas the spider could freely move in the chamber, the
The energy content of the crickets was estimated using pump calorimetry (Instituto de Producción Animal, Universidad Austral de Chile). From predation trials, and according to Secor (2009), we computed the meal size as the difference between the mass of the prey and the remainders of the prey after predation. We also estimated the postprandial metabolic scope as the maximum value of metabolism (=peak metabolic rate) divided by the baseline (the SMR of the spider alone). Also, we estimated time to peak as the duration of time of feeding to peak metabolic rate and duration of the postprandial response as the time from feeding to when metabolic rate was not longer significantly greater than baseline (Secor, 2009). Finally, SDA was calculated as the area below the curve and above SMR base line in each metabolic trial (see Secor, 2009). 2.4. Statistics
3. Results 3.1. Standard metabolic rate The standard metabolic rate (SMR) of E. truculentus (body mass = 7.32 ± 0.7 g; N = 32) was 0.00049 ± 0.000079 mlCO2 g−1 min−1 (measurements of the first trial). The outcome of the variancecomponent analysis for repeatability (32 individuals, measured three or four times) was non-significant (F27,51 = 0.94; P = 0.56) and near-zero estimations of the intraclass correlation coefficient were obtained (i.e., repeatability of SMR was near zero). 3.2. Predation experiments All spiders survived the experiment, and increased body mass during their stay in the laboratory. During predation trials, when the spider captured the prey, the cricket died almost instantaneously, as it was visibly smashed by the chelicerae. The meal size was 1.26 ± 0.04 g cricket wet mass (18.3 ± 2.9% of the spider mass). The energy content of the crickets was 29.3 kj/g dry mass. Then, the energy content of the meal
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was 9.5±0.7 kj. The baseline of the postprandial response was the SMR of the spiders, indicated before (see also Fig. 1). The postprandial peak in VCO2, reached 45 min after prey capture, was 0.0031±0.0003 mL g−1 min−1, 6.55±1.1 times SMR. The duration of the postprandial response was 8 h. The magnitude of the SDA was 9.54±1.1 mLCO2 (N=10), assuming a diet of pure protein, the SDA turns into 0.28±0.03 kj and the SDA coefficient was 3% for a 7.3±0.7 g adult spider mass. Thus, 3% of the ingested energy was respired due to the obligatory costs of meal digestion and assimilation.
4. Discussion 4.1. Repeatability In this study, we found that the standard metabolic rate (SMR) of the Chilean tarantula is lower in comparison with arthropods in
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Time (h) Fig. 1. Metabolic rate measured as the rate of carbon dioxide production (VCO2; mean±SE), in (N=10) individuals of Chilean tarantulas, Euathlus truculentus (MB =7.3±0.72 g) which were offered a single (alive) prey of Cratomelus armatus crickets (MB =1.4±0.15 g). The test consisted in maintaining physically separated the spider and the cricket in the chamber during the first hour of measurement, and releasing the cricket in order to let the spider to capture it without interrupting the record. Upper panel: the spiders captured the prey (in all cases, the attack occurred during the first 30 min after the release, and the cricket died almost instantaneously, see text for details). Lower panel: the spiders (same individuals as in the upper panel) did not eat, and the cricket remained alive, together with the spider, within the chamber during the complete trial. Asterisks denote significant differences between baseline (SMR of the spider) and the metabolic rate at each hour after meal consumption (after a Tukey post-hoc test, and one-way ANOVA). In the lower panel, although the metabolic elevation after the release of the cricket is lower than in the upper panel (because there was no feeding), the rest of the record never reach the baseline level (i.e., the SMR of the spider) because the cricket remained alive within the chamber.
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general (Lighton et al., 2001). Also, our values of SMR (at TA = 25 °C) are similar with other studies in other Chilean theraphosids (Figueroa et al., 2010) and somewhat higher than other species around the world (Shillington, 2005). In fact, assuming a protein-based diet (Walsberg and Wolf, 1995; Willmer et al., 2005), the SMR of E. truculentus (7.3 ± 0.7 g) is 1524 μW, which is 108.4% of the predicted value for arachnids, according to the allometric equation provided by Lighton et al. (2001). However, and contrary to what is known for energy metabolism in other animals including insects (Nespolo and Franco, 2007), and also in other arachnids (Lardies et al., 2008; Terblanche et al., 2004), SMR exhibits low (non-significant) repeatability. Repeatability studies have provided important clues into the nature of phenotypic variation in animal populations (Boake, 1989; Lessells and Boag, 1987), since they indicate whether a trait exhibit consistent variation, which reflects interindividual variation within populations. Then, repeatability studies have become of common use by physiological and evolutionary ecologists (see Nespolo and Franco, 2007, and references therein). Although the repeatability of energy metabolism, both in vertebrates and invertebrates in general is high, some authors have found low and non-significant estimations in some species (Russel and Chappell, 2007). Low repeatability represents low inter-individual variation (i.e., the ranking of trait values in the population is not maintained over time), which would be the case of Chilean tarantulas. The common rationale to interpret this kind of finding is that the trait is fixed because of past directional or stabilizing selection (Nespolo and Franco, 2007). This is consistent with the idea of an adaptation for sit-and-wait predatory behaviour: animals needs to minimize maintenance costs in order to economize energy expenditure (Lighton and Fielden, 1995; Shillington, 2005). According to this logic, natural selection would have acted directionally on reducing SMR, which in turn would have eroded genetic variation in this trait. As a consequence, near-zero repeatability in SMR would be found, as our results suggest. However, additional information would be needed in order to confirm this conclusion, as repeatability is just a preliminary assessment of the upper bound of heritability (see Dohm, 2002). Other explanation to the low repeatability that we found can be some practical problems associated with the measurement, such as residual error and an erroneous choice of the ecologically relevant time frame for the measurement (Arnold et al., 1995). This is important as tarantulas life span can reach up to 20 years (Anderson, 1974; Locht et al., 1999). Other arachnids (with varied modes of foraging) also exhibit low SMR, and the provided explanations to such pattern are diverse. For instance, Lighton et al. (2001) proposed that the low maintenance metabolism of scorpions would be an adaptation to live in ecosystems characterized by low primary productivity. Canals et al. (2008), on the other hand, found that the book lungs of mygalomorph spiders are exceedingly efficient in oxygen extraction, which contrasts with the low SMR they exhibit. Similarly, Terblanche et al. (2004) assumed that the low (but repeatable) metabolic rate in the whip-spider is due to its sedentary habits. Other authors have attributed the low SMR of some arachnids (harvestman) to their fossorial mode of life (Lardies et al., 2008) or to the sit-and-wait lifestyle of some ticks (Lighton and Fielden, 1995). This varied interpretation of a common pattern warrants further research into the causes of low metabolic rates in arachnids, especially to determine whether this pattern is a generalized characteristic of the clade, or an adaptation for certain modes of life. 4.2. Specific dynamic action (SDA) Since only 3 studies addressing the specific dynamic action of spiders have been published so far (Young and Block, 1980; Jensen et al., 2010; Shillington, 2010) and the magnitude and duration of the SDA response can be significantly affected by several factors (Secor, 2009) it is difficult to contrast our results with previously published works. Taking this into consideration our results suggest that the SDA to feeding in the Chilean
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tarantulas is relatively short (8 h), compared with other predatory species (Secor, 2009). However, the duration of the postprandial response in carnivorous invertebrates could range from 3 to 300 h (Secor, 2009). The SDA scope that we found, which is up to 600% baseline levels, whereas it ranges from 150 to 350% in most invertebrates (Secor, 2009) and higher to the 400% observed by Jensen et al. (2010). The meal size is comparatively large (18.3% of spider mass) which partially explain the great metabolic increment that we found and the high magnitude of SDA. In fact, the predicted SDA value according to the allometric equation for invertebrates (Secor, 2009, pp. 12), and our values of spider and meal mass is 0.32 kj. Given that our computed SDA was 0.28 ± 0.03 kj, the SDA of E. truculentus is 87.5 ± 0.07% of the expected value for invertebrates. 4.3. Possible confounding effects of living prey It could be argued that the response of the spiders in our experiments was confounded with metabolic rate of the crickets. This is true to a certain point, since our observations suggest that crickets died within the first hour of measurement (and the metabolic elevation was maintained several more hours). However, we are aware of the fact that the need of providing living prey (that has their own metabolic rate) to the spiders potentially can complicate our experimental settings and interpretations. Because of this reason, we included in the analysis the replicated measurements of the spider and a cricket of similar size, where predation did not occur. In these records the spiders did not consume the prey (mostly because they could not catch the cricket in the first place, and then they remained quiet), and show a small metabolic increase just after cricket release, which can be attributed to the stress of pursuing/escaping. This increase is considerable lower than the SDA response in the records where predation occurred, and ends after the third hour of measurement. The high scope of the postprandial response that we found suggests that Chilean tarantulas spend most of the energy for digestion in a short period after capture. The postprandial response of Chilean tarantula E. truculentus suggests that these arthropods exhibit perhaps different patterns of energy expenditure during digestion, compared with other predatory animals. It is possible that since they need to inject the prey with proteolytic enzymes, instead of swallowing it, changes the time-course of the postprandial response as described in this work. However, further studies are needed to confirm our findings, in order to determine the generality of the energy pattern of digestion in arachnids. Acknowledgements This work was funded by FONDECYT grant 1090423. We thank Bruno Todeschini for help with the experimental setup and spider maintenance. Loreto Correa, Pablo Cortés and José L. Bartheld thank a Conicyt fellowship. References Anderson, F., 1970. Metabolic rates of spiders. Comp. Biochem. Physiol. A 33, 51–72. Anderson, F., 1974. Responses to Starvation in the Spiders Lycosa lenta and Filistata hibernalis. Ecology 55, 576–585. Arnold, S., Peterson, C., Gladstone, J., 1995. Behavioural variation in natural populations. VII. Maternal body temperature does not affect juvenile thermoregulation in a garter snake. Anim. Beh 50, 623–633.
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