The Effect of Fasting and Body Reserves on Cold Tolerance in 2 Pit-Building Insect Predators

Current Zoology, 2017, 63(3), 287–294 doi: 10.1093/cz/zow049 Advance Access Publication Date: 9 May 2016 Article Article The effect of fasting and body reserves on cold tolerance in 2 pit-building insect predators a, a b a Inon SCHARF *, Alma DANIEL , Heath Andrew MACMILLAN , and Noa KATZ aDepartment of Zoology, Faculty of Life Sciences, Tel Aviv University, POB 39040, 69978 Tel Aviv, Israel and bDepartment of Biology, York University, 4700 Keele St., Toronto, Ontario, Canada *Address correspondence to Inon Scharf. E-mail: scharﬁ@post.tau.ac.il. Received on 6 March 2016; accepted on 11 April 2016 Abstract Pit-building antlions and wormlions are 2 distantly-related insect species, whose larvae construct pits in loose soil to trap small arthropod prey. This convergent evolution of natural histories has led to additional similarities in their natural history and ecology, and thus, these 2 species encoun- ter similar abiotic stress (such as periodic starvation) in their natural habitat. Here, we measured the cold tolerance of the 2 species and examined whether recent feeding or food deprivation, as well as body composition (body mass and lipid content) and condition (quantiﬁed as mass-to-size residuals) affect their cold tolerance. In contrast to other insects, in which food deprivation either enhanced or impaired cold tolerance, prolonged fasting had no effect on the cold tolerance of either species, which had similar cold tolerance. The 2 species differed, however, in how cold tolerance related to body mass and lipid content: although body mass was positively correlated with the wormlion cold tolerance, lipid content was a more reliable predictor of cold tolerance in the antlions. Cold tolerance also underwent greater change with ontogeny in wormlions than in antlions. We discuss possible reasons for this lack of effect of food deprivation on both species’ cold tolerance, such as their high starvation tolerance (being sit-and-wait predators). Key words: chill coma, deprivation, ecophysiology, fat content, food, hunger, morphometrics, Myrmeleontidae, Vermileonidae. When experiencing multiple stressors, the physiological response to 1 starvation by either increasing activity, in order to locate new food stress could enhance tolerance for another (cross-tolerance). For in- resources, or decreasing activity, in order to conserve energy (Graf stance, mild starvation improves desiccation tolerance in fruit flies and Sokolowski 1989; Knoppien et al. 2000). When deprived of (Bubliy et al. 2012), and there is often a cross-tolerance between cold food, many animals limit behaviors that require energy, such as and desiccation tolerance, which may be adaptive (Sinclair et al. courting and mating (Travers and Sih 1991; Papadopoulos et al. 2013). Generally, mild (but not harsh) stress can have beneficial ef- 1998) and/or take higher risks in order to obtain food (Kohler and fects on various traits, such as the positive contribution of a mild cold McPeek 1989; Reis and Miller 2011). Sit-and-wait predators do not stress to longevity, fungal resistance and climbing activity (Le Bourg actively search for their prey in contrast to widely foraging predators 2009). In contrast, prior experience of certain stressors may impair re- that actively search for prey. Instead, they choose an ambush site sistance to a different stress type. One such example is an apparent and wait for prey. Sit-and-wait predators are prone to long periods trade-off between starvation and cold tolerance in both Ceratitis flies of time without food, owing to their low probability of encountering and flour beetles (Nyamukondiwa and Terblanche 2009; Scharf et al. prey relative to their widely foraging relatives (Huey and Pianka 2016). Furthermore, if the stress is too high or several stress sources 1981). Consequently, predators adopting the sit-and-wait foraging are combined, even a stress type that otherwise would induce cross- mode have developed a remarkable ability to lower their metabolic tolerance could turn destructive (Le Bourg 2015). rate in the absence of prey (Anderson 1974; Nagy et al. 1984). Starvation occurs if animals do not consume sufficient food to The effects of starvation on behavior are diverse and well maintain their energy demands (McCue 2010). Animals respond to studied, but its effects on thermal preference and tolerance are less VC The Author (2016). Published by Oxford University Press. 287 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact [email protected] 288 Current Zoology, 2017, Vol. 63, No. 3 clear. Starving ectotherms resist starvation longer at lower tempera- and may or may not have consumed a large quantity of food imme- tures (Da Lage and David 1989; Scharf et al. 2015) and actively seek diately before the test. Thus, both the nature of the starvation or habitats with lower temperature in order to reduce their metabolic fasting stress, as well as the manner in which cold tolerance is meas- rate (Lazzari 1991; Porter and Tschinkel 1993). Cold tolerance is ured, could lead to confusion regarding the effects of starvation on influenced by environmental factors, such as habitat of origin, and cold tolerance. growth and acclimation temperatures (Gibert and Huey 2001; Here, we measured the cold tolerance (CCRT) on the larvae of Wilson and Franklin 2002; Sgro et al. 2010). Relative to the envir- 2 pit-building insect predators, antlions and wormlions. These spe- onmental effects on thermal tolerance, the effects of physiological cies are members of 2 different insect orders (Neuroptera and status and other abiotic stressors on cold tolerance have been largely Diptera, respectively), but present a unique example of convergent neglected (Bowler and Terblanche 2008). One exception to this is evolution, owing to similar natural history and foraging mode the observed cross-tolerance between desiccation and cold tolerance, (Dor et al. 2014). We compared the cold tolerance of both antlions which may share similar underlying mechanisms, such as the home- and wormlions following food deprivation, when fed immediately oviscous adaptation of biological membranes, the production of before the cold tolerance test, and when fed 2 days prior to the compatible osmolytes, and the upregulation of heat shock proteins test. Our goals were: (1) to understand the effect of mild starvation (Sinclair et al. 2013). and recent feeding on cold tolerance, which can affect cold toler- For some animals, such as tardigrades, there is no apparent link ance in different directions; (2) to investigate the effect of body between starvation and cold tolerance (Hengherr et al. 2009). Other mass, condition, and morphology on cold tolerance; and (3) to ex- studies on a range of distantly related terrestrial arthropods (e.g., plore an aspect of the convergent evolution between antlions and beetles, isopods and fruit flies), however, have reported a negative wormlions. We predicted that either long fasting or feeding imme- effect of starvation on cold tolerance (Lavy et al. 1997; diately before the test would impair cold tolerance, whereas feed- Nyamukondiwa and Terblanche 2009; Scharf et al. 2016). This ing 2 days before the test would lead to the best cold tolerance (a negative link is further supported by a trade-off between starvation trade-off between fasting and cold tolerance). Alternatively, fast- and cold tolerance in fruit flies (at least for females; Hoffmann et al. ing, especially when not too harsh, might also enhance cold toler- 2005; but see MacMillan et al. 2009). This relationship is suggested ance (a cross-tolerance induced by one stress type against another to be driven by either an energetic trade-off between these 2 stres- one). We further predicted a positive effect of body mass and con- sors (i.e., mediated through lipid reserves; Hoffmann et al. 2005), or dition on cold tolerance (e.g., Terblanche et al. 2008), and ex- an effect of starvation on the hemolymph osmotic balance, leading pected a similar response by antlions and wormlions. to slower recovery from cold stress (MacMillan et al. 2012, 2015; Scharf et al. 2016). Other studies, on freeze-avoiding insects, in contrast, found a positive effect of starvation on cold tolerance. Materials and Methods Emptying of the gut through fasting or mild starvation may prevent ice formation and thereby lower the supercooling point of a freeze- Studied insects and collection avoiding insect (Sømme 1982; Salin 2000). For chill-susceptible Both antlions and wormlions occur in loose soil, sometimes in the insects that die from effects of temperature, unrelated to ice forma- same habitat. Larvae of both species are ambush predators, digging tion, fasting may have different effects on low temperature survival. pits that serve to trap insect prey (Wheeler 1930). Although the For example, fasting locusts recover their osmotic balance faster fol- morphology of each species is strikingly different (see Figure 1 in the lowing chilling stress (Andersen et al. 2013) and mildly fasting fruit Supplementary Material), their pits are almost indistinguishable. flies survive cold stress better than fed flies (Le Bourg 2013, 2015). Other similarities include a high starvation tolerance (typical of any Thus, whether starvation and cold tolerance

Load more