Investigating onychophoran gas exchange and water balance as a means to inform current controversies in arthropod physiology

Abstract

SUMMARYSeveral controversies currently dominate the fields of arthropod metabolic rate, gas exchange and water balance, including the extent to which modulation of gas exchange reduces water loss, the origins of discontinuous gas exchange, the relationship between metabolic rate and life-history strategies, and the causes of Palaeozoic gigantism. In all of these areas, repeated calls have been made for the investigation of groups that might most inform the debates, especially of taxa in key phylogenetic positions. Here we respond to this call by investigating metabolic rate, respiratory water loss and critical oxygen partial pressure (P c ) in the onychophoran Peripatopsis capensis, a member of a group basal to the arthropods, and by synthesizing the available data on the Onychophora. The rate of carbon dioxide release (V CO 2) at 20°C in P. capensis is 0.043 ml CO 2 h -1 , in keeping with other onychophoran species; suggesting that low metabolic rates in some arthropod groups are derived. Continuous gas exchange suggests that more complex gas exchange patterns are also derived. Total water loss in P. capensis is 57 mg H 2 O h -1 at 20°C, similar to modern estimates for another onychophoran species. High relative respiratory water loss rates (~34%; estimated using a regression technique) suggest that the basal condition in arthropods may be a high respiratory water loss rate. Relatively high P c values (5-10% O 2 ) suggest that substantial safety margins in insects are also a derived condition. Curling behaviour in P. capensis appears to be a strategy to lower energetic costs when resting, and the concomitant depression of water loss is a proximate consequence of this behaviour. Supplementary material available online at

Phenotypic plasticity of gas exchange pattern and water loss in Scarabaeus spretus (Coleoptera: Scarabaeidae): deconstructing the basis for metabolic rate variation

“…Buck and Keister, 1955;Lighton, 1988;Quinlan and Lighton, 1999;Vogt and Appel, 2000;Duncan and Dickman, 2001), in others burst volume remains unaltered (Davis et al, 1999;Chappell and Rogowitz, 2000;Shelton and Appel, 2001;Klok and Chown, 2005;Kovac et al, 2007) (but see Terblanche and Chown, 2010). Similar plastic responses to acute changes in other environmental conditions have also been shown in insects and other tracheated arthropods, for example, as oxygen or carbon dioxide levels are altered (Lighton and Berrigan, 1995;Chown and Holter, 2000;Hetz and Bradley, 2005;Lighton and Ottesen, 2005;Clusella-Trullas and Chown, 2008;Lighton and Turner, 2008;Terblanche et al, 2008) (for a review, see Harrison et al, 2006). However, variation in the form of acute change comprises only one aspect of the response of gas exchange pattern and metabolic rate to environmental variation.…”

Evolution of Air Breathing: Oxygen Homeostasis and the Transitions from Water to Land and Sky

“…These shared features between crustacean gills and insect tracheae support a common origin (231). While sluggish arthropods, for example, velvet worms (onychophorans), breathe continuously at relatively high respiratory rates, highly active insects, for example, flies, mosquitos, gnats, and midges (Diptera), breathe discontinuously and can reduce metabolic rates to near zero, thereby increasing the safety margins in their respiratory capacity (143). …”

Can respiratory physiology predict thermal niches?

“…For example, Nauphoeta cinerea cockroaches that show DGE have lower water‐loss rates and live longer than individuals not showing DGE . One way to effect a change is through modification of the spiracular (or tracheal) cross‐sectional area (e.g., via spiracular behavior, shifts in gas‐exchange pattern, or modulation in gross metabolic rate), thus influencing the basic Fick equation for gas transfer . Precisely how respiratory water loss might be modulated by metabolic rate is unclear and controversial .…”

“…85 One way to effect a change is through modification of the spiracular (or tracheal) cross-sectional area (e.g., via spiracular behavior, shifts in gas-exchange pattern, or modulation in gross metabolic rate), thus influencing the basic Fick equation for gas transfer. 86 Precisely how respiratory water loss might be modulated by metabolic rate is unclear and controversial. 83,87 Regardless, insect eggs typically exert rapid control over the oxygenwater trade-off, 88 indicating a selective advantage thereof.…”