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I remain sceptical whether Addo-Bediako, Chown & Gaston's (2002) paper clarifies our understanding of metabolic processes in ectotherms or extends the earlier conclusions of Chown & Gaston (1999) regarding the nature and significance of metabolic cold adaptation. The authors themselves recognize some of the problems inherent in their study but tend to play down their significance. Their particular meta-analysis requires huge simplification and extrapolation from limited data sets, which undermines the veracity of their conclusions. It is based on a restricted knowledge of the organisms involved and of the limitations of the data sets used. Furthermore, the appropriateness of the comparative procedures employed is questionable. Metabolic processes in cold-adapted species are not simple and often, when studied in detail, prove highly subtle and species specific. This subtlety makes realistic comparison of different species across latitudinal or altitudinal thermal gradients difficult. Are we truly comparing like with like? Issues raised by Addo-Bediako, Chown & Gaston's (2002) analyses are explored below and the debate is broadened to include additional data for related arthropods, where they are thought to have general implications for metabolic cold adaptation. Insect species are poorly represented in extreme cold environments, where Collembola and mites are usually the dominant terrestrial arthropods, and it is these organisms that most frequently display cold adaptation.
the basic assumptions used in the meta-analysis
To compare animals living in different climatic regimes metabolic rates corrected for body mass were standardized to 25 °C by extrapolation from measured data using a Q10 value of 2. A respiratory quotient (RQ) value of 0·84 was assumed in converting CO2 output into metabolic rate. Habitat temperature at each geographical site was taken as the annual mean temperature, obtained from the Intergovernmental Panel on Climate Change Data Distribution Centre.
the issues raised
The appropriateness of annual mean temperatures to characterize an animal's effective environment
Microhabitat temperatures to which arthropods are effectively exposed usually differ markedly from the annual mean temperatures used in the meta-analysis. For cold-adapted organisms, which spend the winter in a state of inactivity or diapause, extreme low subzero temperatures during winter (Coulson et al. 1995b), which contribute negatively to the annual mean, are largely irrelevant as long as the animals survive. The effective temperatures at which organisms show significant metabolic activity occur during a short summer active season, although the Antarctic Mite Alaskozetes antarcticus (Michael) shows significant respiration down to −4 °C (Young & Block 1980). During this summer season in the high Arctic, with 24 h per day insolation, maximum soil surface temperatures may exceed the typical mean monthly value of about 27 °C experienced by tropical rainforest soil fauna (Coulson et al. 1993; Block & Convey 1995; Hodkinson et al. 1996). Many high-latitude arthropods are thermophilic, actively occupying the warmest microhabitats (Bale et al. 1997). For example, the Seed Bug Nysius groenlandicus (Zetterstedt) in Greenland has a microhabitat temperature preferendum of 30 °C (Böcher & Nachman 2001). How appropriate then are mean annual screen temperatures for characterizing an animal's effective thermal environment? In such environments it is the ability rapidly to exploit rising temperature from a low initial threshold and/or the ability to select warm microsites that are the important adaptations.
The shape of the log metabolism–temperature response curve and variation within Q10 values
Figure 1(a) shows the log metabolism–temperature response curve for the Arctic collembolan Onychiurus arcticus (Block et al. 1994) and serves to illustrate that in many species this relationship deviates far from the straight line relationship, with a Q10 value of 2, assumed in the meta-analysis. Here metabolism shows a swift initial response to rising temperature over the range 0–10 °C (Q10 = 7·0), slows over the range 10–25 °C (Q10 < 2) and then rises again (25–35 °C, Q10 = 5·8) as the animal becomes thermally stressed and undergoes hyperactive behaviour. Similar wide variation in Q10 values over the activity range of a species is widespread across many polar/alpine taxa but is not apparent in all species (Table 1). Furthermore, variation in the characteristics of the response may depend on the temperature to which animals are acclimated (Sustr 1996). MacLean (1981) noted that even among the invertebrates on Devon Island in Arctic Canada some had a decreasing Q10 with increasing temperature (linear response), some had a constant Q10 (exponential response) whereas in others Q10 increased with increasing temperature (steeper than exponential). However, the mean Q10 over the temperature range of 2–12 °C was 4·0, far higher than the value of 2 for a standard chemical reaction. High Q10 values over the lower temperature range thus allow cold-adapted species to respond rapidly to small rises in temperature. Non-linear relationships, however, make extrapolation beyond the studied temperature range unreliable.
Table Table 1. . Variation in Q10 values with respect to temperature in a range of terrestrial polar/alpine invertebrates demonstrating the non-linear response of log metabolism to temperature and the high Q10 values found in some species, particularly at lower temperatures. Aquatic invertebrates living in a strongly temperature buffered environment are excluded
Effects of locomotor activity on metabolism in cold-adapted species
Measured metabolic rate in any arthropod species is partly determined by the extent of locomotor activity. Metabolic differences between active and inactive states at a single temperature are considerable but notoriously difficult to characterize in small arthropods (e.g. Testerink 1982) and the activity state of experimental animals is rarely recorded in the literature. In general the temperature threshold for activity is lower in cold-environment dwelling arthropods than in their temperate/tropical counterparts and the transition from zero to optimum activity occurs over a more restricted temperature range (Bertram 1935). Many such species exhibit significant locomotor activity at subzero temperatures (Sømme & Block 1991; Coulson et al. 1995a; Zettel 2000). At the other extreme the upper lethal temperature given adequate access to water, in many Arctic arthropods can extend from 30 to 50 °C and often differs little from temperate/tropical species (Aunaas, Baust & Zachariassen 1983; Hodkinson et al. 1996; Böcher & Nachman 2001). There are, however, some cold-adapted species such as Grylloblattodea that do not even survive at the comparison temperature of 25 °C used in the meta-analysis (Morrisey & Edwards 1979). Thus, if we compare say a polar and a tropical species at 25 °C then both are likely to be active. However, if we compare at 5 °C then the polar species is likely to be active whereas the tropical species is likely to be inactive (or dead!). Are these species really comparable across a full range of temperatures? Why use 25 °C as a standard temperature? Why not 5 °C? Would the results be the same? Which result is the most meaningful? Why compare respiration at temperatures an organism may never experience?
Natural diel cycles of activity, within species at a fixed temperature, tend to be extended at higher (colder) latitudes because of the effects of increasing summer day length (Erikstad 1989). Intensity of locomotor activity and thus metabolic rate at a fixed temperature also varies within this 24-h period in groups as diverse as ants and spiders at high altitude (Steigen 1976; MacKay 1982). When within the diel cycle should ‘typical’ respiration be measured as a basis for comparisons?
Seasonal influences on metabolism in cold-adapted species
Most data on metabolism in non-diapausing arthropods are obtained as replicated observations made over a restricted time interval. There are few observations for species throughout the year. However, where such observations have been made for cold-adapted species, marked seasonal differences in metabolism have been found for a given temperature. Good examples include larvae of the Arctic Moth Gynaephora groenlandica (Wöcke) and the Alpine Beetle Calathus melanocephalus (L.) in which active late season individuals have metabolic rates significantly lower than early or mid-season animals at equivalent temperatures (Nylund 1991; Bennett, Kukal & Lee 1999). Reduced metabolism later in the season is a metabolic adaptation to conserve energy but it raises the question of which metabolism value is typical.
Geographical and local variation in metabolism within species
Few studies have investigated variations in metabolism across the geographical range of a species but where such data exist they may show surprising trends. In the beetle Calathus melanocephalus, for example, individuals collected from an alpine site in Norway displayed inverse metabolic cold adaptation, i.e. a lower metabolic rate at comparable temperatures when compared with individuals of the same species from a warmer lower site in the Netherlands (Nylund 1991). Similarly, the shape of the response curve of metabolism to temperature in the beetle Amara quenseli Schonherr differed between the high Arctic and alpine sites in south Norway (Strømme 1989). On a more local scale, snow-surface dwelling populations of the collembolan Isotoma hiemalis Schott have enhanced metabolism at 0 °C compared with forms living in leaf litter (Zettel 1985). This raises the issue of whether there is a fixed metabolic rate characteristic of the species across its entire range.
Effects of feeding on metabolism in cold-adapted species
The nutritional state of experimental arthropods in metabolism experiments is usually unknown. The act of feeding may, however, produce a marked stimulation in metabolic activity in some polar arthropods. Respiration rate of Gynaephora groenlandicus larvae increased fourfold following feeding at 15 °C and the effect was apparent within 3 h (Bennett, Kukal & Lee 1999). A similar rapid decline in metabolism followed the digestion of the ingested food. Similar effects of feeding on metabolism have been demonstrated in several invertebrate species including the Antarctic Mite Alaskozetes antarcticus (Michael) (Block & Convey 1995), the Montane Spider Pardosa palustris (L.) (Steigen 1976) and the collembolan Isotoma viridis (Bourlet) (Zettel 1982). By contrast, the predatory sub-Antarctic carabid beetles Trechisibus antarcticus and Oopterus soledadinus showed no such response (Todd 1997). Reduced metabolism in non-feeding animals is again a particular adaptation to conserve energy in cold environments.
Low-temperature effects on metabolism in cold-adapted species
Polar arthropods, unlike their temperate/tropical counterparts, are often subjected to subzero temperatures during the active season and this may impact on rates of metabolism determined subsequently. Measurements on two sub-Antarctic beetles Perimylops antarcticus Müller and Hydromedion sparsutum Müller showed that chilling at (−4 °C) had only a marginal effect on metabolism measured at 10 °C but that freezing at down to −5·3 °C stimulated subsequent respiration by between 34 and 77% (Sømme et al. 1989; Block, Worland & Bale 1998). Similar metabolic acclimation to prevailing conditions can be induced in many cold-adapted species (e.g. Nylund 1991). This may involve increasing metabolism at lower temperatures and lowering metabolism at higher temperatures.
Anoxia and anaerobic respiration
Metabolic cold adaptation, as currently defined, assumes that aerobic respiration with unrestricted oxygen availability is the norm. Invertebrates living at subzero temperatures, however, may survive extended periods of oxygen starvation encased in ice. For some animals, such as the beetle Pelophia borealis Paykull, this involves a switch from aerobic to anaerobic metabolism (Conradi-Larsen & Sømme 1973). Such mechanisms are a characteristic element of true metabolic cold adaptation but fall outside the scope of the meta-analysis.
Effect of life stage on metabolism in cold-adapted species
Some polar/alpine arthropods, in which there are a series of morphologically similar life stages, show significant variation between stages in their metabolic response to temperature (Block 1979: Mackay 1982). For example, mass corrected metabolism was 2·3 higher at 5 °C in female adults than in deuteronymphs of the Antarctic mite Nanorchestes antarcticus Strandtmann (Block 1976). Similarly, Q10 values over 0–10 °C for larval, nymphal and adult stages of the mite Alaskozetes antarcticus ranged from 1·50 to 3·46 (Young 1979a) and in the collembolan Cryptopygus antarcticus Willem (Michael) from 1·99 to 2·54 among five size classes (Block & Tilbrook 1975). Which is the characteristic value?
Declining metabolic rates in cultured animals
Several cold-adapted species kept in long-term culture often show reduced metabolism compared with their free-living counterparts (Steigen 1976; Young 1979a,b; Young & Block 1980). Metabolism has frequently been measured in animals taken from culture.
Metabolism and water loss
Polar and high alpine environments are cold dry environments in which organisms potentially face problems of respiratory water loss during gas exchange. It is conceivable that in some species raised metabolism may be a hyperactive response to drought stress. Some evidence to support this idea is suggested by the increased rate of respiration at higher (potentially drier) altitude sites found in populations of some species of beetle and grasshopper (Massion 1983; Sømme et al. 1989; Rourke 2000). This effect may be induced or accentuated by the reduced partial pressure of oxygen at higher elevations, necessitating more frequent opening of the spiracles.
Meta-analysis is a valuable tool in ecology but it must be applied wisely and appropriately. This should not involve extrapolating beyond the measured range of data, making linear extrapolations from non-linear data or interpolating data that are inherently variable.
Organisms living in cold ecosystems often show particular metabolic adaptations to their environment. Whether this is best illustrated by a meta-analysis comparing species at 25 °C is, however, debatable. There is a great danger that such an analysis averages out species responses in that those showing a strong response are diluted by those exhibiting little measurable response to produce a weak overall relationship. There is no such thing as an ‘average animal’. Individual species, or even life stages of the same species, differ widely in their metabolic cold responses, which, as demonstrated above, may be subtle and hard to measure. Thus, relationships based on such means have little predictive value. Yet it is the subtleties that epitomize cold adaptation, particularly the manner in which metabolic rate is adjusted and modified to suit prevailing conditions and conserve energy. Metabolism in many polar invertebrates living in the field is not just a function of temperature, it is influenced by food availability, prior cold exposure and seasonal exposure effects, among several other factors.
What then constitutes metabolic cold adaptation? Such adaptation is best demonstrated at low temperatures, not 25 °C. It involves comparatively higher rates of metabolism at temperatures, typically in the range −5–10 °C and is often associated with significant locomotor activity at temperatures below 5 °C. It often involves a rapid Q10 response to temperature over this lower temperature range, enabling species quickly to take advantage of small rises in their environmental temperature and to exploit fully a highly restricted growing season. However, it may also involve the depression of metabolism to conserve hard-won energy gains under conditions of resource limitation. Not all organisms living in cold environments exhibit such responses, which are often species specific. Perhaps the intermediate cold-metabolic responses observed in insects on sub-Antarctic islands, such as Marion Island with cool but relatively equitable mean monthly temperatures exceeding 0 °C (Crafford & Chown 1993), reflects weaker selection for a fast-responding metabolism.
Leaving aside confounding factors discussed above, cold adaptation is probably, as pointed out by several authors, best expressed through the activation energy of metabolism calculated from the gradient of the Arrhenius plot of log metabolism against 1/temperature (K) (see Young 1979b; Lee & Baust 1982a; Aunaas, Baust & Zachariessen 1983; Sømme & Block 1991). The better cold adapted the species, the lower the activation energy and the more likely that Q10 values well in excess of 2 will be observed over the lower temperature register. This is reflected in a lower temperature threshold of measurable metabolic activity in cold-adapted species (Block & Convey 1995). Nevertheless, extrapolation from non-linear Arrhenius plots may also mislead as demonstrated by the data for O. arcticus (Fig. 1b) where the gradient of the line changes dependent on the temperature range within which the measurements were made.