Thermoregulation, energetics, and behavior.

Abstract

Temperature affects all aspects of biological function, including behavior (see Haynie, 2001). All behavior thus occurs within a thermodynamic context and is bounded by thermal and energetic constraints (see Careau, Killen, & Metcalfe, 2015; Mathot & Dingemanse, 2015). Some of these arise within biological systems, directly out of the mechanics of physics, biochemistry, and geometry. For example, chemical reaction rates are temperature dependent, as are many critical characteristics of enzymes and other proteins, including structure and function. The same is true for many properties of biological membranes (Hazel, 1995), including the permeability of chorionic and amniotic membranes (e.g., Bara & Guiet-Bara, 1986) and the blood-brain barrier (Kiyatkin & Sharma, 2009). There are thus thermal optima for the myriad functions and complex biochemical reactions that drive living systems-optima that are carefully balanced and adjusted dynamically in the face of internal and external challenges. 1 Neurons are among the most temperaturesensitive cells in the body (Kiyatkin, 2010; Rango, Arighi, & Bresolin, 2012). Many critical parameters of neuronal functioning (e.g., conduction velocity, refractory period) covary with temperature, implying coupling between brain temperature and neural processing (e.g., Blessing, Mohammed, & Ootsuka, 2012, 2013; Thiessen, 1983a) and optima for neuronal functioning (see Gisolfi & Mora, 2000; Kiyatkin, 2010). Indeed, the energetic efficiency of action potentials improves with increased temperature within the mammalian physiological range, with optimal efficiency at 37° C (Yu, Hill, & McCormick, 2012). Even small elevations (3° C-4° C) above this (e.g., because of fever, stroke, or ingestion of drugs such as MDMA [3,4-methylenedioxymethamphetamine]) can trigger neuronal dysfunction resulting in hallucinations, seizures, and damage (e.g., Brown & Kiyatkin, 2004). Likely because of these trade-offs, some of the most fascinating thermoregulatory adaptations have emerged in the context of regulating brain temperature (see Blumberg, 2002). Other constraints on temperature regulation are imposed from outside the animal. For example, by beginning life in the same locale in which their parents reproduced, most animals inherit basic ecological and climatic conditions and, within that context, select among or create microclimates. Add to this variation from daily and seasonal temperature rhythms, and we can recognize the bases of complex and varied adaptive strategies. In response to seasonal changes, some species migrate; others hibernate, estivate, or become hypometabolic (see Storey, 2015); many show season-specific changes in fur density, fat composition, and other metabolic and thermoregulatory phenotypes (Blumberg, 2002). With respect to daily changes, most species exhibit closely coordinated circadian rhythms of behavior and physiology, thereby optimizing the acquisition, utilization, and conservation (or loss) of thermal energy. For example, on a

Oxytocin and the warm outer glow: Thermoregulatory deficits cause huddling abnormalities in oxytocin-deficient mouse pups

“…Porges, 2011). Social and energetic niches often covary significantly, whether considering circadian, seasonal, developmental, or evolutionary timescales (e.g., Harshaw et al, 2017; Ondrasek, 2016). Social and metabolic mechanisms are thus likely to be co-selected during phylogeny and co-regulated by environmental cues (e.g., light, temperature, the presence of conspecifics) during ontogeny (e.g., Kapheim et al, 2015; Woodard et al, 2014).…”

“…Although interest in the social versus homeostatic functions of OT has fueled largely separate areas of research, it is unlikely that social and homeostatic processes are the output of entirely separate systems, particularly for highly social species (see Harshaw et al, 2017). This principle is particularly evident in species that modulate their gregariousness or sociability with fluctuations in ambient temperature and/or humidity.…”

Development of behavioral responses to thermal challenges

“…The pattern we see in general, and in the data with altricial rodents in particular, suggests that infant mammals are ill-equipped to combat warm challenges, in comparison to their specializations of behavior and physiology for combating cold challenge. The mechanisms that are used by developing mammals for body temperature regulation integrate physiology and behavior (Gordon, 2012; Harshaw et al, 2017; Tattersall et al, 2012). In some cases, such as those involving huddling, group behavior, such as that of an aggregate of littermates is essential to effective thermoregulatory function.…”

“…The study of thermoregulation in adults is focused on how large animals expend heat to prevent overheating, which is in contrast to small infants where the emphasis on thermoregulation involves reducing loss of body heat to the environment, facilitating transfer from external sources of heat to their body, and then judiciously expending energy for heat production (Blumberg, 2001; Blumberg & Sokoloff, 1998). Consequently, most of the experimental literature on the development of body temperature regulation involves responses to cold challenges (Blumberg & Sokoloff, 1998; Harshaw, Blumberg, & Alberts, 2017; Satinoff, 1996), for this is the challenge typically faced by immature mammals. In contrast, the present paper is a selective review and discussion of data and knowledge about the ontogeny of regulatory responses to warm challenges, the less well known side of thermoregulation, but needed for general understanding and applicable to several basic concerns.…”

Anticipated effects of abiotic environmental change on intraspecific social interactions

“…Increased temperatures are well established to lead to increased aggression in many aquatic organisms, although the mechanism for the increase in aggression is not always clear. It could be due to the lifting of metabolic constraints on energetically costly behaviour, due to increases in metabolic rates that result in organisms operating outside their optimal thermal window, or due to neurons operating outside of their thermal range, producing maladaptive behaviour (Huey et al, 2012;Harshaw, Blumber & Alberts, 2017). For example, both dominant and subordinate Amazonian dwarf cichlids (Apistogramma agassizii) increase how often they bite at higher temperatures compared to dominant fish in control conditions (Kochhann, Campos & Val, 2015), while another cichlid, Julidochromis ornatus, also exhibits more mirror-elicited aggression in experimental high-temperature groups compared to control groups (Kua et al, 2020).…”