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Belowground thermoregulation in Namibian desert spiders that burrow their own chemostats
Acta Oecologica 96 (2019) 18–23
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Belowground thermoregulation in Namibian desert spiders that burrow their own chemostats
T
Christian Mulder∗,1, Erminia Conti1, Giovanni Costa Department of Biological, Geological and Environmental Sciences, University of Catania, 95124 Catania, Italy
ARTICLE INFO
ABSTRACT
Keywords: Ariadna Body mass and size Burrows Central Namib desert Metabolic theory of ecology Temperature Trait distribution
Body size aggregates multiple traits, ranging from body mass and feeding behaviour up to reproductive strategies and individual performance, and depicts the environmental fitness. Some environmental predictors like temperature can therefore be seen as multilayer factors, causing trait distribution to be multifaceted. This is remarkably evident for Ariadna Audouin (Araneae: Segestriidae) spiders, also known as corolla spiders, which were sampled at the end of the Austral Summer in the Central Namib Desert (Namibia). Here we show that these peculiar sit-and-wait spiders are able to thermoregulate behaviourally by digging until the most appropriate soil depth. This ecological process makes the actual habitat temperature at the bottom of the burrow the strongest determinant for a constant metabolic rate of soil ectotherms as computed according to the Metabolic Theory of Ecology.
1. Introduction Soil is an extremely complex system due to the huge amount of three-dimensionally structured habitats featuring different physical and chemical microgradients in depth. Many invertebrates inhabiting sandy soils are known for their burrowing activity, ranging from spiders (Albín et al., 2015; Foelix et al., 2017; Conti et al., 2018) and scorpions (Koch, 1978; Polis et al., 1986), up to other animals such as woodlice, myriapods, solifugids and even vertebrates, for example, mole rats (Costa, 1995; Cloudsley-Thompson, 1977; Ward, 2009). In particular, Namibian nocturnal sit-and-wait predatory spiders belonging to the cosmopolitan genus Ariadna Audouin (Araneae: Segestriidae) excavate nearly vertical cylindrical burrows. These burrows are inhabited by sedentary females and are thickly lined with silk having site-specific chemical properties (Conti et al., 2015). All burrows are radially surrounded by a stone ring of mostly seven small quartz pebbles at the burrow edge that amplify the vibration of moving preys like ants (Costa et al., 1995; Henschel, 1995). After their moult, males swarm like vagabonds from their burrows searching for mates, although with a rather restricted dispersal (Dippenaar-Schoeman and Jocqué, 1997). Besides the high risk of being captured by predators, males can also be attacked by female spiders after courtship and mating. Both of these aforementioned aspects contribute to explain why Ariadna males are so rarely found and why the males have been described just in few cases. An
excess of adult females in some groups of spiders (spanandry) is wellknown among arachnologists, despite some studies of inverted sex ratio and opposite behaviours which have been recorded in other genera (e.g., Albín et al., 2019). Still, many previous observations that were reported in literature (Costa et al., 1995; Henschel, 1995) only address the ethological implications of species diversity of spiders (animals that live typically at the top of the food chain) and neither the biophysics nor the metabolic implications of functional traits like mass and size. In fact, in the black box of belowground soil systems any quantification of thermal dependence of the behavioural traits of living invertebrates, encompassing how temperature influencing the velocities of predator and prey could affect encounter rates, remained ignored. Higher soil temperatures force efficient handling times, increasing consumption and faster decomposition rates (Mulder, 2006; Dell et al., 2011, 2014). Thus, if the resource availability is low because prey is scarce like in extreme environments such as deserts, the predator–prey dynamics will be further constrained by temperature. Furthermore, soil temperature strongly fluctuates, varying less with increasing soil depth. Therefore, many soil ectotherms are seeking for a kind of “steady state” deep into the soil. For these spiders, extreme soil temperatures can be compensated only by digging belowground, often in a one-night burrowing activity, providing a strong empirical evidence for behavioural adaptation. Dimensionality matters in the magnitude of thermal dispersion, as
Corresponding author. E-mail address: [email protected] (C. Mulder). 1 Contributed equally to this paper. ∗
https://doi.org/10.1016/j.actao.2019.02.003 Received 11 September 2018; Received in revised form 6 February 2019; Accepted 27 February 2019 Available online 18 March 2019 1146-609X/ © 2019 Elsevier Masson SAS. All rights reserved.
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shown by two-dimensional heat transport equation for a vertically uniform flow in homogeneous soils (Lu et al., 2018), and in the foraging behaviour of animals. For sit-and-wait foragers like Ariadna spiders, the (passive) search rate is the speed at which resources move through the consumer's attack space (sensu Pawar et al., 2012) and the relative velocity is the rate at which predator–prey pairs converge. Hence, this relative velocity can be seen merely as a function of the prey velocity, since the foraging behaviour of our predatory spiders implies no movement until the final attack. Both rates (relative velocity and passive search) are affected by temperature and heat events. As ectotherms depend per definition on external heat sources, and the temperature of their body is changing with the temperature of their environment, it is rather surprising that the functional traits of ectotherms in extreme environments like hot deserts have so extensively been neglected in literature. Sand digging is costly for burrowing spiders in terms of both the kinetic activity required for digging as well because of the high energetic costs of producing so many silk layers to stabilize the built burrows (Henschel and Lubin, 1992; Conti et al., 2015). From the metabolic point of view, burrowing invertebrates like spiders have high energetic flux values.
3. Material and methods We have chosen one of the hottest and oldest deserts in the world, the Namib Desert, and focused on its northern gravel plains. These plains are dominated by gypsum, calcretes and quartz pebble pavements (Eckardt et al., 2013). During a field survey conducted between 19 March and 13 April 2012, 88 Ariadna spp. burrows were identified and the living specimens were collected by hand, measured and weighted. For each specimen we estimated body mass using a Sartorius balance (model CPA225D); total body size (length) and burrows depth were measured using a Borletti caliper (measurement error of 0.02 mm). Soil temperature was measured in the field both at the surface and the bottom of the burrow using a Salmoiraghi 301 digital thermometer with a 0.1 °C resolution. The features of our sampling sites (henceforth, G, K, M, R, and W according to the locations shown in Fig. 1) are summarized in Table 1. As we were interested in the trait-responses of Ariadna populations to soil temperature, irrespective of other environmental factors, the Metabolic Theory of Ecology provides the most appropriate tool to link body mass with temperature. For all these sites, we computed MTE at the surface and the bottom of these 88 burrows using the classical MTE formula. Despite comprehensive studies by Meehan (2006), Ehnes et al. (2011) and Sohlström et al. (2018), no empirical parameters were available for Ariadna spiders in particular or Segestriidae in general. Therefore, we preferred the more general phylogenetic model calibrated for 1134 microarthropods by Ehnes et al. (2011):
2. Metabolic theory of ecology One of the most charismatic frameworks of modern science, the Metabolic Theory of Ecology (afterwards: MTE) as defined by Brown et al. (2004) and Sibly et al. (2012), is very appropriate to detect the extent to which temperature may affect the activity of ectotherms, whose body temperatures will rise and fall along with their habitat temperature. We hypothesize that the variation in MTE will be a function of the surrounding environment of depth-inhabiting soil invertebrates. MTE is supposed to be able to forecast effects of daily temperature on the metabolism of soil invertebrates because it is searching for a mechanistic compromise between individual thermal biology and surrounding physical characteristics at multiple levels (Stevenson, 1985). However, although MTE relies on an empirical justification built on body-size effects in autotrophs and endotherms, the same MTE remains also tenuously linked through an exponential temperature-dependence term to a theoretical framework based on biochemical kinetics and activation energy of molecules (Schrodinger, 1941). Rising temperatures are a “hot” topic, making MTE an appealing tool because temperature and size do not always scale (in)dependently from each other (Peters, 1983; Kingsolver and Huey, 2008; Conti et al., 2019). Arachnids have been widely investigated regarding their body temperature, their weight and their gas exchanges since decades (Anderson, 1970; Humphreys, 1978), making spiders in general (and burrowing spiders in particular) an appropriate tool to investigate the energetic costs of their behaviour (e.g., digging, foraging, etc.) and as such their metabolic activity. It should also be mentioned here that Hemmingsen (1950) already demonstrated that metabolism was mostly a ¾ power function of mass, wherefore the relationship between weight (body mass) or length (body size) and metabolism has to be seen as a function of the metabolic rate proportional to the surface areas of animals. It was Von Bertallanffy (1957) who pointed out that the metabolic rate could be proportional to either fresh weight (mass) and/or to animal surface (size). Given these relationships, it is challenging to figure out the distribution of spider's mass and size in a hyperarid area with such high temperatures as in Namibia (Fig. 1). For the first time an empirical investigation on the extent to which temperature at two different spatial scales (the temperature of the microenvironment and the temperature of the local habit) is influencing two fundamental traits, mass and size, and their response traits, burrows and MTE, has been done in adult spiders inhabiting natural microcosms in Namibia, southern Africa.
MTE = EXP[21.97+ 0.76 × ln(m)
0.47 × (kT ) 1]
with T the soil temperature in Kelvins (site-specific T values were always measured twice, both at the surface and the bottom of a spider's burrow), m the site-specific weight of the spider of that burrow as in the field and k the Boltzmann's constant (8.62 × 10−5 eV K−1) according to biokinetics. Temperature-related trait-responses have been extensively described elsewhere. Close relationships between size and macroecology (latitudinal trends as recognized in Bergmann, 1847), size and temperature (palaeoclimatical trends as in Smith et al., 1995), size and soil ecology (environmental gradients as described in Reuman et al., 2009) and size and mesocosms (meta-analysis as in Stewart et al., 2013) are well-demonstrated and underline the crucial importance of considering temperature-dependence of allometric scaling (Allen et al., 2002; Sibly et al., 2012). We used all these novel field data over the five Namibian sampling sites for the spider analyses and their site-specific visualized trait distribution using violin plots as realized with the “ggplot2” program by the “geom_violin ()” utility in R-3.5.1 to test for temperature-driven differences and performed a non-parametric Kruskal-Wallis Analysis of Variance (α = 0.01). 4. Results and discussion Size S and mass m of our spiders are closely related to each other (Fig. 2), where m is overall a power function of S, hence m = aSb: b is a parameter statistically undistinguishable from 3 that measures the trait heterogeneity level of the entire ensemble of 88 spiders, and a is a parameter likely of relatively little biological significance. The heterogeneity levels of m are captured by the coefficients of variation (100 × SD ⁄ mean), which were 32.36%, 50.64%, 54.86%, 57,89% and 80.96% for R, G, W, M and K, respectively, with an overall CV of 69.81% for all sites. The relationships between S and m thus change according to the sites, ranging from site R with the most elongated spiders (the shallowest correlation between m and S) to site K with the most heavy spiders (the steepest correlation between m and S), as shown in Fig. 3 by site-specific distribution of empirical m and S values. According to the Kruskal-Wallis test, not all five sites have either 19
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Fig. 1. Location of the five sampled sites in Namibia and annual temperature average in degrees Celsius (in sequence: G for Gobabeb, K for Khorixas, M for Mirabib, R for Rooikop, and W for Welwitschia Wash). Four of these sites (G, M, R and W) are within the Namib Naukluft Park (as shown in the enlargement on the left) and one, K, is outside the Namib Desert. One picture of a female Ariadna specimen from the W site on the right. Annual temperature map redrawn from http://www.met.gov. na/files/files/National%20Climate%20Change%20Strategy%20&%20Action%20Plan%202013%20-%202020.pdf. More details are provided in Table 1. Table 1 Summary of the five investigated sites in Namibia and the abbreviation used throughout the text. ID
Site name
Coordinates
Coastal distance
Soil surface temperature
Brief description
G
Gobabeb
56 km
36–48 °C
Gravel plains characterize this area where the sand (76.95%) is predominant.
K
Khorixas
115 km
23–45 °C
Dry savannah area of the Great Escarpment external to the Namib Desert
M
Mirabib
70 km
36–49 °C
With an 88.05% sand fraction this area exhibits the highest sand percentage of our sites
R
Rooikop
22 km
20–39 °C
Gravel area within the Lichen Field
W
Welwitschia Wash
23°19.0′38.4″S 15°02.0′23.3″E 20°25.0′53.1″S 14°20.0′44.9″E 23°32.0′53.2″S 15°08.0′23.8″E 23°00.0′32.7″S 14°43.0′38.0″E 23°36.0′32.9″S 15°10.0′02.7″E
72 km
21–46 °C
Ravine that runs through the gravel plain with a sandy channel
equal medians for surface temperature, Tsoil, or median Tsoil-derived MTE flux (p < 0.001), in sharp contrast to the bottom of the burrows (p > 0.01). Fig. 4 (A,B) shows that the actual habitat temperature for the spiders is strictly that at the bottom of the burrow, Tdepth, averaging 28.13 °C ( ± 4 SD), and not the surface temperature around the burrow averaging 35.09 °C ( ± 6.8 SD). Despite overall comparable Tdepth values across the Central Namib Desert, the spiders inhabiting the burrows sampled within the R sites had substantially lower MTE fluxes (Fig. 4C and D). It is also noteworthy that all the burrows at the K site were more than 10 cm deep, in sharp contrast to most of the burrows at the four Central Namib sites (Fig. 3C). According to Brose et al. (2005), in the case of mobile prey the even occurrence of small and abundant sessile predators like our spiders suggest a high resource availability in the landscape. This is evident only in the nutrient-rich Lichen Fields of the R site (Fig. 4C). Given that each individual spider waits in its burrow for prey moving on the soil surface, it must be mentioned that the burrow density at the R site, and hence the prey availability around all burrows, is remarkable (Costa et al., 2000). MTE for heterotrophic organisms might be more site-dependent than size-dependent and this aspect has likely been underestimated. Therefore, it might seem hard to figure out under which circumstances functional traits and soil temperature can be used as major fitness predictors within our natural microcosms. To address this first question
Fig. 2. Relationships between body size (length) and body mass (weight) of 88 adult Ariadna spiders for five Namibian locations, indicating the power law by which these two traits are closely linked to each other. Besides K (Khorixas in brown) which is scattered along the entire curve, the values appear in the sequence R and G (Rooikop in green and Gobabeb in yellow, respectively), M (Mirabib in red) and W (Welwitschia Wash in olive green). (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)
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Fig. 3. From left to right, the trait distribution of body size (A), body mass (B) and burrow depth (C) of Ariadna spiders in five Namibian locations plotted on the horizontal axis. Same codes and colours as in the previous figure. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)
we have to look at the distribution of three original traits (individual body size and body mass weighted in the field and depth of burrows) as shown in Fig. 3. Despite surface temperature fluctuations (Fig. 4A), close correlations between either size and temperature or mass and temperature (“The hotter the smaller”) remained undetected, similar to a meta-analysis study by Klok and Harrison (2013), who found contrasting correlations between size or mass and temperature for most arthropods and no evidence for such correlations in the case of spiders. Temperatures of ectotherms like spiders are supposed to be approximately equal to that of their habitats (Foelix, 2011). In the case of sit-and-wait predators like these spiders, capable to survive more seasons without any food, such daily heat pressures force them to a strict nocturnal behaviour. This provides strong evidence for an adaptation to compensate transpiration rates and to minimize water loss. However, body-masses of adult spiders seem to remain under 80 mg weight across this desert study area, confirming that higher temperature mostly results in maturation at a smaller adult size (Li and Jackson, 1996). And here the second question arises, to which extent can MTE mirror any physiological compensation to heat? To address this latter question on heat compensation, we used the same individual body mass weighted in the field and computed MTE values at the surface and the bottom of our burrows (Fig. 4C and D). Thermal biology implies that MTE must be low to increase reproductive fitness. To turn to our empirical data, the MTE values make clear that what matters the most is not the trait-dependence of MTE, but the temperature used. Hence, any inaccurate temperature measurement will bias the allometric response, affecting the large consensus that underpins MTE. Only Tdepth, in fact, reflects the optimal environmental conditions for our female spiders that always covered the young at the bottom of their burrows until their second moult, resulting in dozens of spiderlings during the sampling period (Conti, pers. obs.). Hence, the exponential temperature-dependence term needs to be derived from local T-values measured strictly on the same way, making a careful calibration of MTE of greatest importance when addressing global warming size effects in terrestrial ectotherms, as even in our one-species soil systems, biokinetics and thermal biology are complicated. Very large systems like pelagic open oceans are supposed to have some steady-state characteristics due to their chemostat-like qualities (Jannasch, 1974). This seems to happen at a very small scale as well, especially in soil systems. Especially in deserts, soil is the only
Fig. 4. Field temperatures at the surface (A) and at the bottom (B) and metabolic fluxes as derived from the temperature at the surface (C) and the bottom (D) of the burrows. Same codes and colours as in the previous figures. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)
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insulating layer. In a successful attempt to keep physicochemical conditions like temperature at the bottom of their burrows constant (any constant temperature in the field can be seen as a rather unnatural situation), these desert spiders built their own chemostat-like habitat, digging into the soil until the temperature becomes acceptable for their own metabolic purposes. From this perspective, the appropriate soil temperature is crucial. Our approach was useful when MTE was predicted accurately for our spiders because it illuminated potential thermoregulation mechanisms and when MTE apparently failed because it provided a benchmark from which to assess protocols in the temperature predictor to be chosen. Climatologists and ecologists seem to be more interested in the temperature of the upper soil surface in order to fully understand the energy balance between earth and space, but it is the temperature in the soil that is triggering the behavioural activity on many ectotherms that are burrowing deep into the soil to escape heat. Although it is not our purpose to test the MTE theory, it is more than evident that any standard application of environmental temperature should be avoided, as only the true habitat temperature must be used to compute the actual metabolic rates. Only then, these sensitive MTE rates become closely related to ecosystem functions and services and therefore powerful proxies for global warming scenarios through a quantitative model.
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Foelix, R.F., 2011. Biology of Spiders. Oxford University Press, New York, NY. Foelix, R., Rechenberg, I., Erb, B., Albín, A., Aisenberg, A., 2017. Sand transport and burrow construction in sparassid and lycosid spiders. J. Arachnol. 45, 255–264. Hemmingsen, A.M., 1950. The relation of standard (basal) energy metabolism to total fresh weight of living organisms. Reports Steno Memorial Hospital and the Nordisk Insulin Laboratorium 4, 7–58. Henschel, J.R., 1995. Tool use by spiders: stone selection and placement by corolla spiders Ariadna (Segestriidae) of the Namib Desert. Ethology 101, 187–199. Henschel, J.R., Lubin, Y.D., 1992. Environmental factors affecting the web and activity of a psammophilous spider in the Namib Desert. J. Arid Environ. 22, 173–189. Humphreys, W.F., 1978. The thermal biology of Geolycosa godeffroyi and other burrow inhabiting Lycosidae (Araneae) in Australia. Oecologia 31, 319–347. Jannasch, H.W., 1974. Steady state and the chemostat in ecology. Limnol. 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5. Conclusions This study may be the first to examine, quantitatively model, and interpret structural metabolic variation in an extreme habitat in one of the hottest and oldest deserts in the world with empirical soil temperature measurements and added trait data of predatory spiders. Here we demonstrate in an ensemble of 88 natural microcosms that only by using strict sampling protocols and by entering site-specific parameters into MTE it will become possible to unravel challenging interactions between MTE and global warming, linking the knowledge gleaned from a trait-based framework with a biophysical interpretations at habitat scale. Even if temperature drops during the night, the exact location for the measurements of soil temperature is crucial for burrowing invertebrates. Size always matters, but soil temperature matters even more. Author contributions CM and EC conceived the study. CM led the writing. CM and EC performed the statistical analyses. All authors drafted or revised the manuscript. Acknowledgements Financial support was provided by the Ministry for Education, University and Research of Rome, Italy, and E.C. and G.C. thank the Ministry of Environment and Tourism, in Windhoek, Namibia, for the permit 1675/2012 to conduct research work in the Namib-Naukluft Park. The anonymous referees are both gratefully acknowledged. Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.actao.2019.02.003. References Albín, A., Simó, M., Aisenberg, A., 2015. Characterisation of burrow architecture under natural conditions in the sand-dwelling wolf spider Allocosa brasiliensis. J. Nat. Hist. 50, 201–209. Albín, A., Bardier, G., Peretti, A.V., Simó, M., Aisenberg, A., 2019. A matter of choice: substrate preference by burrow-digging males of a sand-dwelling spider. J. Ethol. 37, 13–20. Allen, A.P., Brown, J.H., Gillooly, J.F., 2002. Global biodiversity, biochemical kinetics,
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M., Woodward, G., 2013. Mesocosm experiments as a tool for ecological climatechange research. Adv. Ecol. Res. 48, 71–181. Von Bertallanffy, L., 1957. Quantitative laws in metabolism and growth. Quart. Rev. Biol. 32, 217–231. Ward, D., 2009. The Biology of Deserts. Oxford University Press, Oxford.
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Belowground thermoregulation in Namibian desert spiders that burrow their own chemostats
T
Christian Mulder∗,1, Erminia Conti1, Giovanni Costa Department of Biological, Geological and Environmental Sciences, University of Catania, 95124 Catania, Italy
ARTICLE INFO
ABSTRACT
Keywords: Ariadna Body mass and size Burrows Central Namib desert Metabolic theory of ecology Temperature Trait distribution
Body size aggregates multiple traits, ranging from body mass and feeding behaviour up to reproductive strategies and individual performance, and depicts the environmental fitness. Some environmental predictors like temperature can therefore be seen as multilayer factors, causing trait distribution to be multifaceted. This is remarkably evident for Ariadna Audouin (Araneae: Segestriidae) spiders, also known as corolla spiders, which were sampled at the end of the Austral Summer in the Central Namib Desert (Namibia). Here we show that these peculiar sit-and-wait spiders are able to thermoregulate behaviourally by digging until the most appropriate soil depth. This ecological process makes the actual habitat temperature at the bottom of the burrow the strongest determinant for a constant metabolic rate of soil ectotherms as computed according to the Metabolic Theory of Ecology.
1. Introduction Soil is an extremely complex system due to the huge amount of three-dimensionally structured habitats featuring different physical and chemical microgradients in depth. Many invertebrates inhabiting sandy soils are known for their burrowing activity, ranging from spiders (Albín et al., 2015; Foelix et al., 2017; Conti et al., 2018) and scorpions (Koch, 1978; Polis et al., 1986), up to other animals such as woodlice, myriapods, solifugids and even vertebrates, for example, mole rats (Costa, 1995; Cloudsley-Thompson, 1977; Ward, 2009). In particular, Namibian nocturnal sit-and-wait predatory spiders belonging to the cosmopolitan genus Ariadna Audouin (Araneae: Segestriidae) excavate nearly vertical cylindrical burrows. These burrows are inhabited by sedentary females and are thickly lined with silk having site-specific chemical properties (Conti et al., 2015). All burrows are radially surrounded by a stone ring of mostly seven small quartz pebbles at the burrow edge that amplify the vibration of moving preys like ants (Costa et al., 1995; Henschel, 1995). After their moult, males swarm like vagabonds from their burrows searching for mates, although with a rather restricted dispersal (Dippenaar-Schoeman and Jocqué, 1997). Besides the high risk of being captured by predators, males can also be attacked by female spiders after courtship and mating. Both of these aforementioned aspects contribute to explain why Ariadna males are so rarely found and why the males have been described just in few cases. An
excess of adult females in some groups of spiders (spanandry) is wellknown among arachnologists, despite some studies of inverted sex ratio and opposite behaviours which have been recorded in other genera (e.g., Albín et al., 2019). Still, many previous observations that were reported in literature (Costa et al., 1995; Henschel, 1995) only address the ethological implications of species diversity of spiders (animals that live typically at the top of the food chain) and neither the biophysics nor the metabolic implications of functional traits like mass and size. In fact, in the black box of belowground soil systems any quantification of thermal dependence of the behavioural traits of living invertebrates, encompassing how temperature influencing the velocities of predator and prey could affect encounter rates, remained ignored. Higher soil temperatures force efficient handling times, increasing consumption and faster decomposition rates (Mulder, 2006; Dell et al., 2011, 2014). Thus, if the resource availability is low because prey is scarce like in extreme environments such as deserts, the predator–prey dynamics will be further constrained by temperature. Furthermore, soil temperature strongly fluctuates, varying less with increasing soil depth. Therefore, many soil ectotherms are seeking for a kind of “steady state” deep into the soil. For these spiders, extreme soil temperatures can be compensated only by digging belowground, often in a one-night burrowing activity, providing a strong empirical evidence for behavioural adaptation. Dimensionality matters in the magnitude of thermal dispersion, as
Corresponding author. E-mail address: [email protected] (C. Mulder). 1 Contributed equally to this paper. ∗
https://doi.org/10.1016/j.actao.2019.02.003 Received 11 September 2018; Received in revised form 6 February 2019; Accepted 27 February 2019 Available online 18 March 2019 1146-609X/ © 2019 Elsevier Masson SAS. All rights reserved.
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shown by two-dimensional heat transport equation for a vertically uniform flow in homogeneous soils (Lu et al., 2018), and in the foraging behaviour of animals. For sit-and-wait foragers like Ariadna spiders, the (passive) search rate is the speed at which resources move through the consumer's attack space (sensu Pawar et al., 2012) and the relative velocity is the rate at which predator–prey pairs converge. Hence, this relative velocity can be seen merely as a function of the prey velocity, since the foraging behaviour of our predatory spiders implies no movement until the final attack. Both rates (relative velocity and passive search) are affected by temperature and heat events. As ectotherms depend per definition on external heat sources, and the temperature of their body is changing with the temperature of their environment, it is rather surprising that the functional traits of ectotherms in extreme environments like hot deserts have so extensively been neglected in literature. Sand digging is costly for burrowing spiders in terms of both the kinetic activity required for digging as well because of the high energetic costs of producing so many silk layers to stabilize the built burrows (Henschel and Lubin, 1992; Conti et al., 2015). From the metabolic point of view, burrowing invertebrates like spiders have high energetic flux values.
3. Material and methods We have chosen one of the hottest and oldest deserts in the world, the Namib Desert, and focused on its northern gravel plains. These plains are dominated by gypsum, calcretes and quartz pebble pavements (Eckardt et al., 2013). During a field survey conducted between 19 March and 13 April 2012, 88 Ariadna spp. burrows were identified and the living specimens were collected by hand, measured and weighted. For each specimen we estimated body mass using a Sartorius balance (model CPA225D); total body size (length) and burrows depth were measured using a Borletti caliper (measurement error of 0.02 mm). Soil temperature was measured in the field both at the surface and the bottom of the burrow using a Salmoiraghi 301 digital thermometer with a 0.1 °C resolution. The features of our sampling sites (henceforth, G, K, M, R, and W according to the locations shown in Fig. 1) are summarized in Table 1. As we were interested in the trait-responses of Ariadna populations to soil temperature, irrespective of other environmental factors, the Metabolic Theory of Ecology provides the most appropriate tool to link body mass with temperature. For all these sites, we computed MTE at the surface and the bottom of these 88 burrows using the classical MTE formula. Despite comprehensive studies by Meehan (2006), Ehnes et al. (2011) and Sohlström et al. (2018), no empirical parameters were available for Ariadna spiders in particular or Segestriidae in general. Therefore, we preferred the more general phylogenetic model calibrated for 1134 microarthropods by Ehnes et al. (2011):
2. Metabolic theory of ecology One of the most charismatic frameworks of modern science, the Metabolic Theory of Ecology (afterwards: MTE) as defined by Brown et al. (2004) and Sibly et al. (2012), is very appropriate to detect the extent to which temperature may affect the activity of ectotherms, whose body temperatures will rise and fall along with their habitat temperature. We hypothesize that the variation in MTE will be a function of the surrounding environment of depth-inhabiting soil invertebrates. MTE is supposed to be able to forecast effects of daily temperature on the metabolism of soil invertebrates because it is searching for a mechanistic compromise between individual thermal biology and surrounding physical characteristics at multiple levels (Stevenson, 1985). However, although MTE relies on an empirical justification built on body-size effects in autotrophs and endotherms, the same MTE remains also tenuously linked through an exponential temperature-dependence term to a theoretical framework based on biochemical kinetics and activation energy of molecules (Schrodinger, 1941). Rising temperatures are a “hot” topic, making MTE an appealing tool because temperature and size do not always scale (in)dependently from each other (Peters, 1983; Kingsolver and Huey, 2008; Conti et al., 2019). Arachnids have been widely investigated regarding their body temperature, their weight and their gas exchanges since decades (Anderson, 1970; Humphreys, 1978), making spiders in general (and burrowing spiders in particular) an appropriate tool to investigate the energetic costs of their behaviour (e.g., digging, foraging, etc.) and as such their metabolic activity. It should also be mentioned here that Hemmingsen (1950) already demonstrated that metabolism was mostly a ¾ power function of mass, wherefore the relationship between weight (body mass) or length (body size) and metabolism has to be seen as a function of the metabolic rate proportional to the surface areas of animals. It was Von Bertallanffy (1957) who pointed out that the metabolic rate could be proportional to either fresh weight (mass) and/or to animal surface (size). Given these relationships, it is challenging to figure out the distribution of spider's mass and size in a hyperarid area with such high temperatures as in Namibia (Fig. 1). For the first time an empirical investigation on the extent to which temperature at two different spatial scales (the temperature of the microenvironment and the temperature of the local habit) is influencing two fundamental traits, mass and size, and their response traits, burrows and MTE, has been done in adult spiders inhabiting natural microcosms in Namibia, southern Africa.
MTE = EXP[21.97+ 0.76 × ln(m)
0.47 × (kT ) 1]
with T the soil temperature in Kelvins (site-specific T values were always measured twice, both at the surface and the bottom of a spider's burrow), m the site-specific weight of the spider of that burrow as in the field and k the Boltzmann's constant (8.62 × 10−5 eV K−1) according to biokinetics. Temperature-related trait-responses have been extensively described elsewhere. Close relationships between size and macroecology (latitudinal trends as recognized in Bergmann, 1847), size and temperature (palaeoclimatical trends as in Smith et al., 1995), size and soil ecology (environmental gradients as described in Reuman et al., 2009) and size and mesocosms (meta-analysis as in Stewart et al., 2013) are well-demonstrated and underline the crucial importance of considering temperature-dependence of allometric scaling (Allen et al., 2002; Sibly et al., 2012). We used all these novel field data over the five Namibian sampling sites for the spider analyses and their site-specific visualized trait distribution using violin plots as realized with the “ggplot2” program by the “geom_violin ()” utility in R-3.5.1 to test for temperature-driven differences and performed a non-parametric Kruskal-Wallis Analysis of Variance (α = 0.01). 4. Results and discussion Size S and mass m of our spiders are closely related to each other (Fig. 2), where m is overall a power function of S, hence m = aSb: b is a parameter statistically undistinguishable from 3 that measures the trait heterogeneity level of the entire ensemble of 88 spiders, and a is a parameter likely of relatively little biological significance. The heterogeneity levels of m are captured by the coefficients of variation (100 × SD ⁄ mean), which were 32.36%, 50.64%, 54.86%, 57,89% and 80.96% for R, G, W, M and K, respectively, with an overall CV of 69.81% for all sites. The relationships between S and m thus change according to the sites, ranging from site R with the most elongated spiders (the shallowest correlation between m and S) to site K with the most heavy spiders (the steepest correlation between m and S), as shown in Fig. 3 by site-specific distribution of empirical m and S values. According to the Kruskal-Wallis test, not all five sites have either 19
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Fig. 1. Location of the five sampled sites in Namibia and annual temperature average in degrees Celsius (in sequence: G for Gobabeb, K for Khorixas, M for Mirabib, R for Rooikop, and W for Welwitschia Wash). Four of these sites (G, M, R and W) are within the Namib Naukluft Park (as shown in the enlargement on the left) and one, K, is outside the Namib Desert. One picture of a female Ariadna specimen from the W site on the right. Annual temperature map redrawn from http://www.met.gov. na/files/files/National%20Climate%20Change%20Strategy%20&%20Action%20Plan%202013%20-%202020.pdf. More details are provided in Table 1. Table 1 Summary of the five investigated sites in Namibia and the abbreviation used throughout the text. ID
Site name
Coordinates
Coastal distance
Soil surface temperature
Brief description
G
Gobabeb
56 km
36–48 °C
Gravel plains characterize this area where the sand (76.95%) is predominant.
K
Khorixas
115 km
23–45 °C
Dry savannah area of the Great Escarpment external to the Namib Desert
M
Mirabib
70 km
36–49 °C
With an 88.05% sand fraction this area exhibits the highest sand percentage of our sites
R
Rooikop
22 km
20–39 °C
Gravel area within the Lichen Field
W
Welwitschia Wash
23°19.0′38.4″S 15°02.0′23.3″E 20°25.0′53.1″S 14°20.0′44.9″E 23°32.0′53.2″S 15°08.0′23.8″E 23°00.0′32.7″S 14°43.0′38.0″E 23°36.0′32.9″S 15°10.0′02.7″E
72 km
21–46 °C
Ravine that runs through the gravel plain with a sandy channel
equal medians for surface temperature, Tsoil, or median Tsoil-derived MTE flux (p < 0.001), in sharp contrast to the bottom of the burrows (p > 0.01). Fig. 4 (A,B) shows that the actual habitat temperature for the spiders is strictly that at the bottom of the burrow, Tdepth, averaging 28.13 °C ( ± 4 SD), and not the surface temperature around the burrow averaging 35.09 °C ( ± 6.8 SD). Despite overall comparable Tdepth values across the Central Namib Desert, the spiders inhabiting the burrows sampled within the R sites had substantially lower MTE fluxes (Fig. 4C and D). It is also noteworthy that all the burrows at the K site were more than 10 cm deep, in sharp contrast to most of the burrows at the four Central Namib sites (Fig. 3C). According to Brose et al. (2005), in the case of mobile prey the even occurrence of small and abundant sessile predators like our spiders suggest a high resource availability in the landscape. This is evident only in the nutrient-rich Lichen Fields of the R site (Fig. 4C). Given that each individual spider waits in its burrow for prey moving on the soil surface, it must be mentioned that the burrow density at the R site, and hence the prey availability around all burrows, is remarkable (Costa et al., 2000). MTE for heterotrophic organisms might be more site-dependent than size-dependent and this aspect has likely been underestimated. Therefore, it might seem hard to figure out under which circumstances functional traits and soil temperature can be used as major fitness predictors within our natural microcosms. To address this first question
Fig. 2. Relationships between body size (length) and body mass (weight) of 88 adult Ariadna spiders for five Namibian locations, indicating the power law by which these two traits are closely linked to each other. Besides K (Khorixas in brown) which is scattered along the entire curve, the values appear in the sequence R and G (Rooikop in green and Gobabeb in yellow, respectively), M (Mirabib in red) and W (Welwitschia Wash in olive green). (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)
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Fig. 3. From left to right, the trait distribution of body size (A), body mass (B) and burrow depth (C) of Ariadna spiders in five Namibian locations plotted on the horizontal axis. Same codes and colours as in the previous figure. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)
we have to look at the distribution of three original traits (individual body size and body mass weighted in the field and depth of burrows) as shown in Fig. 3. Despite surface temperature fluctuations (Fig. 4A), close correlations between either size and temperature or mass and temperature (“The hotter the smaller”) remained undetected, similar to a meta-analysis study by Klok and Harrison (2013), who found contrasting correlations between size or mass and temperature for most arthropods and no evidence for such correlations in the case of spiders. Temperatures of ectotherms like spiders are supposed to be approximately equal to that of their habitats (Foelix, 2011). In the case of sit-and-wait predators like these spiders, capable to survive more seasons without any food, such daily heat pressures force them to a strict nocturnal behaviour. This provides strong evidence for an adaptation to compensate transpiration rates and to minimize water loss. However, body-masses of adult spiders seem to remain under 80 mg weight across this desert study area, confirming that higher temperature mostly results in maturation at a smaller adult size (Li and Jackson, 1996). And here the second question arises, to which extent can MTE mirror any physiological compensation to heat? To address this latter question on heat compensation, we used the same individual body mass weighted in the field and computed MTE values at the surface and the bottom of our burrows (Fig. 4C and D). Thermal biology implies that MTE must be low to increase reproductive fitness. To turn to our empirical data, the MTE values make clear that what matters the most is not the trait-dependence of MTE, but the temperature used. Hence, any inaccurate temperature measurement will bias the allometric response, affecting the large consensus that underpins MTE. Only Tdepth, in fact, reflects the optimal environmental conditions for our female spiders that always covered the young at the bottom of their burrows until their second moult, resulting in dozens of spiderlings during the sampling period (Conti, pers. obs.). Hence, the exponential temperature-dependence term needs to be derived from local T-values measured strictly on the same way, making a careful calibration of MTE of greatest importance when addressing global warming size effects in terrestrial ectotherms, as even in our one-species soil systems, biokinetics and thermal biology are complicated. Very large systems like pelagic open oceans are supposed to have some steady-state characteristics due to their chemostat-like qualities (Jannasch, 1974). This seems to happen at a very small scale as well, especially in soil systems. Especially in deserts, soil is the only
Fig. 4. Field temperatures at the surface (A) and at the bottom (B) and metabolic fluxes as derived from the temperature at the surface (C) and the bottom (D) of the burrows. Same codes and colours as in the previous figures. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)
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insulating layer. In a successful attempt to keep physicochemical conditions like temperature at the bottom of their burrows constant (any constant temperature in the field can be seen as a rather unnatural situation), these desert spiders built their own chemostat-like habitat, digging into the soil until the temperature becomes acceptable for their own metabolic purposes. From this perspective, the appropriate soil temperature is crucial. Our approach was useful when MTE was predicted accurately for our spiders because it illuminated potential thermoregulation mechanisms and when MTE apparently failed because it provided a benchmark from which to assess protocols in the temperature predictor to be chosen. Climatologists and ecologists seem to be more interested in the temperature of the upper soil surface in order to fully understand the energy balance between earth and space, but it is the temperature in the soil that is triggering the behavioural activity on many ectotherms that are burrowing deep into the soil to escape heat. Although it is not our purpose to test the MTE theory, it is more than evident that any standard application of environmental temperature should be avoided, as only the true habitat temperature must be used to compute the actual metabolic rates. Only then, these sensitive MTE rates become closely related to ecosystem functions and services and therefore powerful proxies for global warming scenarios through a quantitative model.
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5. Conclusions This study may be the first to examine, quantitatively model, and interpret structural metabolic variation in an extreme habitat in one of the hottest and oldest deserts in the world with empirical soil temperature measurements and added trait data of predatory spiders. Here we demonstrate in an ensemble of 88 natural microcosms that only by using strict sampling protocols and by entering site-specific parameters into MTE it will become possible to unravel challenging interactions between MTE and global warming, linking the knowledge gleaned from a trait-based framework with a biophysical interpretations at habitat scale. Even if temperature drops during the night, the exact location for the measurements of soil temperature is crucial for burrowing invertebrates. Size always matters, but soil temperature matters even more. Author contributions CM and EC conceived the study. CM led the writing. CM and EC performed the statistical analyses. All authors drafted or revised the manuscript. Acknowledgements Financial support was provided by the Ministry for Education, University and Research of Rome, Italy, and E.C. and G.C. thank the Ministry of Environment and Tourism, in Windhoek, Namibia, for the permit 1675/2012 to conduct research work in the Namib-Naukluft Park. The anonymous referees are both gratefully acknowledged. Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.actao.2019.02.003. References Albín, A., Simó, M., Aisenberg, A., 2015. Characterisation of burrow architecture under natural conditions in the sand-dwelling wolf spider Allocosa brasiliensis. J. Nat. Hist. 50, 201–209. Albín, A., Bardier, G., Peretti, A.V., Simó, M., Aisenberg, A., 2019. A matter of choice: substrate preference by burrow-digging males of a sand-dwelling spider. J. Ethol. 37, 13–20. Allen, A.P., Brown, J.H., Gillooly, J.F., 2002. Global biodiversity, biochemical kinetics,
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M., Woodward, G., 2013. Mesocosm experiments as a tool for ecological climatechange research. Adv. Ecol. Res. 48, 71–181. Von Bertallanffy, L., 1957. Quantitative laws in metabolism and growth. Quart. Rev. Biol. 32, 217–231. Ward, D., 2009. The Biology of Deserts. Oxford University Press, Oxford.
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