Elsevier

Journal of Insect Physiology

Volume 59, Issue 9, September 2013, Pages 870-880
Journal of Insect Physiology

Can temperate insects take the heat? A case study of the physiological and behavioural responses in a common ant, Iridomyrmex purpureus (Formicidae), with potential climate change

https://doi.org/10.1016/j.jinsphys.2013.06.003Get rights and content

Highlights

  • Meat ants voluntarily live close to their thermal maxima.

  • They dynamically alter their thermal biology to cope with low temps and seasons.

  • They readily adjust behaviour to cope with high trail temperatures.

  • Indices of thermal stress are strongly influenced by the scale used.

  • Behaviour and local population responses are critical for climate change predictions.

Abstract

Insects in temperate regions are predicted to be at low risk of climate change relative to tropical species. However, these assumptions have generally been poorly examined in all regions, and such forecasting fails to account for microclimatic variation and behavioural optimisation. Here, we test how a population of the dominant ant species, Iridomyrmex purpureus, from temperate Australia responds to thermal stress. We show that ants regularly forage for short periods (minutes) at soil temperatures well above their upper thermal limits (upper lethal temperature = 45.8 ± 1.3 °C; CTmax = 46.1 °C) determined over slightly longer periods (hours) and do not show any signs of a classic thermal performance curve in voluntary locomotion across soil surface temperatures of 18.6–57°C (equating to a body temperature of 24.5–43.1 °C). Although ants were present all year round, and dynamically altered several aspects of their thermal biology to cope with low temperatures and seasonal variation, temperature-dependence of running speed remained invariant and ants were unable to elevate high temperature tolerance using plastic responses. Measurements of microclimate temperature were higher than ant body temperatures during the hottest part of the day, but exhibited a stronger relationship with each other than air temperatures from the closest weather station. Generally close associations of ant activity and performance with microclimatic conditions, possibly to maximise foraging times, suggest I. purpureus displays highly opportunistic thermal responses and readily adjusts behaviour to cope with high trail temperatures. Increasing frequency or duration of high temperatures is therefore likely to result in an immediate reduction in foraging efficiency. In summary, these results suggest that (1) soil-dwelling temperate insect populations may be at higher risks of thermal stress with increased frequency or duration of high temperatures resulting from climate change than previously thought, however, behavioural cues may be able to compensate to some extent; and (2) indices of climate change-related thermal stress, warming tolerance and thermal safety margin, are strongly influenced by the scale of climate metrics employed.

Introduction

Climate change is one of the most pressing scientific issues facing humanity (AAS, 2010). Across Australia, average daily maximum temperatures have increased by 0.75 °C since 1910 (CSIRO-ABM, 2012) and future predictions are for a generally warmer and drier continent by 2030 (CSIRO, 2007). The likely impacts of climate change are expected to be complex and highly variable across Australia and world-wide (Walther et al., 2002). This may lead to a larger number of extreme maximum temperature events, but fewer and more intense minimum temperature extremes (WMO, 2011, Hansen et al., 2012). Major challenges are to predict how organisms will respond to such changes and to identify species at risk of thermal stress, population decline and possible extinction (Root et al., 2003, Deutsch et al., 2008, Huey et al., 2009, Chown et al., 2010, Diamond et al., 2012, Andrew and Terblanche, in press), and how this may impact on ecosystem function.

Ants are one of the most ubiquitous animals in terrestrial ecosystems and play crucial roles in ecosystem functioning on all continents except Antarctica (Lach et al., 2010, CAS, 2012). The essential role that ants play in natural ecosystems, including predation, seed dispersal, pollination, nutrient recycling, herbivore ‘farming’ and as a food source for other invertebrates and vertebrates (Lach et al., 2010), will likely be modified by a changing climate. Therefore understanding how ants will respond to climate variation is of fundamental importance in understanding, and sustaining, global biodiversity. Ants play a key role in providing ecosystem services and are habitat engineers making them flagship taxa to identify responses to changing abiotic factors (Gaston, 2011).

Ectothermic insects, particularly ants in the tropics have been argued to be more susceptible to climate warming due to their relatively low warming tolerance (WT) than more temperate or high latitude species (Deutsch et al., 2008, Diamond et al., 2012). This pattern is largely a result of the fact that upper temperature limits for survival and activity are relatively constant across the planet (e.g. Addo-Bediako et al., 2000, Deutsch et al., 2008, Overgaard et al., 2011, Sunday et al., 2011, Kellermann et al., 2012), and tropical species live in environments that are warmer and are therefore closer to their upper thermal limits and optimal performance temperatures (Topt). In addition, plasticity of tolerance may be intrinsically coupled to basal tolerance levels, further complicating prediction and forecasting efforts (e.g. Stillman, 2003, Calosi et al., 2008, Nyamukondiwa et al., 2011). For example, Stillman (2003) found that tolerance to higher temperatures may come at the expense of acclimation capacity in marine invertebrates. By contrast, among Drosophila species, Nyamukondiwa et al. (2011) found little evidence for trade-offs between basal high temperature tolerance and acute plasticity thereof, and instead, they found the exact opposite pattern (more plasticity accompanied more tolerance) (but see also Sgro et al., 2010 for intraspecific patterns).

Recently, several of the thermal stress risk generalisations have been questioned on the basis of microsite opportunities which are typically not accounted for in models of thermal stress and extinction risk (e.g. Sinervo et al., 2010, Clusella-Trullas and Chown, 2011, Sinervo et al., 2011), and that several ectotherm groups are potentially at greater risk in sites further from the tropics (e.g. Clusella-Trullas et al., 2011, Kellermann et al., 2012). In addition, exposure to different sub-lethal temperatures for a range of time durations might enhance ants survival over short time-scales (e.g. during foraging for a few minutes up to 4.5 h: Jumbam et al., 2008).

However, several testable predictions have generally been poorly examined. Furthermore, there has been a lack of information incorporating physiological tolerances with microclimatic and behavioural optimisation of insects in the field in assessing their risk to climate change, and the data for tropical and temperate zone species is, in some cases, notably sparse (see e.g. Kearney et al., 2009, Clusella-Trullas et al., 2011, Bonebrake and Deutsch, 2012). Both warming tolerance and thermal safety margins (TSM) are important indices as they characterise the geographic covariances of thermal performance curves (reviewed in Angilletta, 2009) and climate: warming tolerance is the difference between upper thermal tolerance and habitat ambient temperature and therefore defines how much warming an ectotherm can tolerate before performance is reduced to lethal levels; thermal safety margins is the difference between an organism’s thermal optimum for performance and the current habitat ambient temperature and therefore gives an indication of how close animals thermal optima are to the current climatic temperature within their environment (Deutsch et al., 2008). While it is generally clear that different estimates of climate can influence these indices in profound ways (Clusella-Trullas et al., 2011, Diamond et al., 2012, Huey et al., 2009), few studies have considered microclimatic data at ecologically relevant times or spatial scales for ants (e.g. temperatures at the main foraging times on ant trails throughout the hottest months; differences between open and shaded habitats along foraging routes, and changes at different depths and galleries of the nest), and systematically examined the influence of these variables on estimates of susceptibility to climate change (though see e.g. Clusella-Trullas et al., 2011).

In Australia, one of the most common animal taxa, and with the highest biomass of all vertebrate and invertebrate taxa, are meat ants (Iridomyrmex spp.) (Andersen, 2000). Relative to the phylogenetic and climatic diversity occupied by ant species worldwide it is perhaps surprising that there is not more research on their physiological responses to climate change (though for research on other ant species see e.g. Diamond et al., 2012, Jumbam et al., 2008, Maysov and Kipyatkov, 2009, Jayatilaka et al., 2011, Oberg et al., 2012, Ribeiro et al., 2012), and a particular dearth of information on the responses of Australian native insect fauna (but see Christian and Morton, 1992, Jayatilaka et al., 2011). Temperature also plays an important role in ant locomotion (Shapley, 1920, Shapley, 1924, Greenaway, 1981, Hurlbert et al., 2008) by determining activity times and absolute speed (Cerda et al., 1998) but not necessarily influencing the overall costs of transport (i.e. the integration of energy consumption and distance travelled per unit time, Joules/meter/second) (Lighton and Duncan, 2002, Clusella-Trullas et al., 2010).

Here we test a key climate change assumption, namely that temperate insect species are at low risk of thermal stress, by estimating thermal safety margins and warming tolerance and a range of physiological and behavioural responses to temperature variation. We further identify whether plasticity of high temperature tolerance can mediate the responses observed, and examine the effects of exposure duration on thermal limits. In addition, to further understand performance in the field and likely climate change impacts, we also assessed voluntary locomotion performance and its temperature-dependence. Finally we consider methodological influences in the measurement of habitat and insect body temperature, as different temperature measurement methods may result in dissimilar conclusions being made about species or population extinction risk.

Section snippets

Study site and laboratory conditions

Ant activity and physiological tolerances were measured in the Austral summer (October/November 2009, 2010) and Austral winter (June/July 2011). Iridomyrmex purpureus (meat ants) were collected from a single nest on the University of New England campus, Armidale, NSW, Australia (30°29′26.02″S, 151°38′38.43″E), 980 masl. Up to 1500 worker ants were dug up at a time from the nest and placed into a 50 cm3 box with nest soil, then taken back to the laboratory. Worker ants of this species can survive

Lethal limits

Ant survivorship across the high and low temperature lethal spectrum was dependent on season (Fig. 1). Winter-collected field-fresh ants had significantly higher survival than summer-collected summer-acclimated or winter-collected summer-acclimated ants at −13, −11, and −7 °C. By contrast, at −9, −5 and −3 °C summer-collected lab-acclimated ants had significantly lower survival compared to other treatments (Fig. 1; Table 1). At high temperatures, summer-collected lab-acclimated ants had

Ant survival and thermal stress

Assessing physiological responses of organisms to climate change is crucial (Williams et al., 2008) and is surprisingly not a major focal area of research examining insect responses to climate change (6% of papers studied assessed insect physiological responses to both simulated and realised climate change; Andrew et al., 2013). Moreover, it is critical to understand changes to populations of common species (Gaston, 2011) as changes in population structure may lead to the collapse in trophic

Conclusions

We have shown, at least for our temperate meat ant population, that they are voluntarily exposing themselves, or active, close to their thermal maxima, and these upper limits have limited flexibility within a single generation or even between seasons. Furthermore, given results from other insects examined to date (e.g. Kellermann et al., 2012) they may generally be constrained from an evolutionary perspective (see also Hoffmann et al., 2012). For ants, this means the colony may have to employ a

Acknowledgements

This work was funded, in part, by an ARC Discovery Grant DP0769961 to NRA, an Australian Government Endeavour Award and a Rural Development Administration Fund (South Korea: PJ009353) to M.-P.J. and a UNE Travel Grant to J.S.T. J.S.T. was supported by South African National Research Foundation Incentive Funding for Rated researchers during the writing of this manuscript. We thank Mike Angilletta, Casper Nyamukondiwa and anonymous referees for constructive comments on earlier versions of this

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