Download Introduction to the Symposium: Beyond the Mean

Integrative and Comparative Biology
Integrative and Comparative Biology, volume 56, number 1, pp. 11–13
doi:10.1093/icb/icw020
Society for Integrative and Comparative Biology
SYMPOSIUM
Introduction to the Symposium: Beyond the Mean: Biological
Impacts of Changing Patterns of Temperature Variation
Michael E. Dillon1,* and H. Arthur Woods†
*Department of Zoology and Physiology and Program in Ecology, University of Wyoming, 1000 E. University Ave Dept
3166, Laramie, WY 82071, USA; †Division of Biological Sciences, University of Montana, Missoula, 32 Campus Drive
HS104, MT 59812, USA
From the symposium ‘‘Beyond the Mean: Biological Impacts of Changing Patterns of Temperature Variation’’ presented
at the annual meeting of the Society for Integrative and Comparative Biology, January 3–7, 2016 at Portland, Oregon.
1
E-mail: [email protected]
‘‘Variation is the hard reality, not a set of imperfect measures for a central tendency. Means and
medians are the abstractions.’’1
–Stephen Jay Gould
Beetles aside, biologists have an inordinate fondness
for means. Means and other measures of central tendency help us to describe complex phenomena in
simple ways, and they facilitate quantitative comparisons of traits among treatment groups, populations,
and species. For organisms, however, means are abstractions; they confront only variation. In the context
of organism–environment interactions, means are
used to characterize not only the biological traits of
interest but also the environments in which those
traits are expressed. But variation in traits among individuals (e.g., Careau et al. 2014) and in environments across space (Sears et al. 2011; Woods et al.
2015) and time (Niehaus et al. 2012; Wang and Dillon
2014) can profoundly alter the outcomes of organism–environment interactions (e.g., Svancara et al.
2002; Williams 2008; Bonebrake and Deutsch 2011;
Montalto et al. 2014; Boersma et al. 2016).
Measuring and predicting the biological impacts of
climate change has become one of the pressing ecological challenges of our time, and the field has been
dominated by central tendencies. Mean values of behavioral, physiological, and ecological traits paired with
averages of temperature, precipitation, snowpack, etc.
provide inferences about past and predictions about
future climate impacts (Walther et al. 2002; Field et
al. 2014). Increasingly, however, ecologists are recognizing that variation, in both biology and climate, is as
important, if not more, in determining the effects of
climate change (Paaijmans et al. 2013; Vasseur et al.
2014; Lawson et al. 2015; Chan et al. 2016).
In this symposium and associated journal issue, we ask
a particular question: What are the biological impacts of
changing patterns of temperature variation? We focused
on temperature because it is perhaps the most measured
environmental variable with the best-known effects on
organisms (Kingsolver 2009). In addition to traditional
papers from symposium speakers, the issue includes three
synthetic papers that address the biological effects of: (1)
spatial variation in temperature (Pincebourde et al. 2016,
this issue), (2) temporal variation in temperature (Dillon
et al. 2016, this issue), and (3) rare but extreme events
(Williams et al. 2016a, this issue). These synthetic contributions were written by working groups of symposium
speakers and attendees. The symposium focus on variation complements the 2014 HETEROCLIM conference
that took place in Loches, France, as well as several
recent Society for Integrative and Comparative Biology
symposia examining other aspects of organismal responses to climate change: the 2011 symposium titled
‘‘A synthetic approach to the response of organisms to
climate change: The role of thermal adaptation’’ (Sears
and Angilletta 2011), and the 2013 symposium titled
‘‘Physiological responses to simultaneous shifts in multiple environmental stressors: relevance in a changing world
(Todgham and Stillman 2013).
Several contributions in this issue (Pincebourde et
al. 2016, this issue; Pincebourde and Suppo 2016,
1
Thanks to Wes Dowd and Mark Denny for pointing us to this quote.
Advanced Access publication June 1, 2016
ß The Author 2016. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved.
For permissions please email: [email protected].
12
this issue) highlight the paucity of studies that explicitly measure spatial variation in temperature, particularly at scales relevant to organisms (cf Potter et
al. 2013). The ‘‘grain’’ of spatial variation with respect to the size of the organism (Levins 1968) will
likely determine whether that variation is a resource
to be exploited or a threat to be managed. From a
meta-analysis, Pincebourde et al. (2016, this issue)
found similar levels of spatial heterogeneity in temperature across scales from single leaves to landscapes. Their random walk model suggests that, up
to a point, high spatial heterogeneity helps organisms
thermoregulate, highlighting the need to incorporate
spatial variation into climate models and predictions
(Sears et al. 2011; Woods et al. 2015). Detailed measurements at multiple spatial scales suggest that microhabitats may allow small tropical organisms to
escape the heat (Tewksbury et al. 2008): even
during the hottest parts of the day, more than 70%
of potential micro-habitats had surface temperatures
that would permit activity by small ectotherms
(Pincebourde and Suppo 2016, this issue).
At any location on a landscape, temperatures also
vary in time from seconds to decades to geologic eras
(Dillon et al. 2016, this issue; Poertner et al. 2016, this
issue). Changes in temporal variation in temperature
associated with climate change (Wang and Dillon
2014; Dillon et al. 2016, this issue) can drastically
alter our estimates of how much climate will affect
organisms (Sheldon and Dillon 2016, this issue). Our
ability to estimate past and to predict future effects
will be greatly enhanced by new approaches to measuring and manipulating variation at different timescales, as illustrated by the frequency domain
approach outlined by Dillon et al. (2016, this issue).
Over longer timescales, changes in the magnitudes of
climate oscillations may alter community composition, as more variable climates should select for
broader thermal tolerances (eurythermy; Poertner et
al. 2016, this issue). Collectively, our synthetic symposium efforts have revealed that the relative importance of variation over different timescales will depend
on: (1) organism size (Stevenson 1985; Woods et al.
2015) and life history (Levins 1968; Gilchrist 1995;
Chan et al. 2016), and (2) the timescales over which
thermal performance curves shift (Williams et al.
2016a, this issue; Dillon et al. 2016, this issue).
Even when they are rare, extreme temperatures
may disproportionately affect the physiology, ecology, and evolution of organisms and populations
(Buckley and Huey 2016, this issue; Dowd et al.
2015). Changes in temperature variation at different
timescales alter the probability that an organism will
M. E. Dillon and H. A. Woods
experience an extreme and perhaps lethal event
(Dillon et al. 2016, this issue). Even when not
lethal, extremes can have profound consequences;
exposure to sublethal extremes induces a cascade of
physiological responses that can have carryover effects leading to increased tolerance of or susceptibility to subsequent exposures to extremes (Williams et
al. 2016a, this issue). Williams et al (2016b, this
issue) pose the novel hypothesis that, over longer
timescales, metabolic compensation (a macrophysiological ‘‘rule’’; Gaston et al. 2009) may be a direct
response to adaptation to extremes rather than a
compensatory response to maintain growth rates.
And both lethal (Buckley and Huey 2016, this
issue) and sublethal (Williams et al. 2016a, this
issue) extremes may shape the evolution of thermal
performance curves much more than do temperatures around the mean (that are most often experienced by most organisms most of the time). Clearly,
we need to study extremes explicitly using both
theory and experiments.
Altogether, the papers in this issue call for us to
meld climate science and biology in ways that move
us beyond means. Doing so will require novel
approaches to methods, experiments, and theory.
We need new, more standardized methods for collecting meteorological and microclimatic data to
characterize spatial and temporal variation of temperature and other abiotic factors at scales more relevant to organisms. We need to develop new theory
for translating abiotic conditions into organismal
and population performance, and we need more
and better experiments elucidating the effects of
both fluctuating and extreme temperatures (Colinet
et al. 2015) on the plasticity and evolution of thermal
performance curves (Kingsolver and Woods 2016).
Understanding the forces that shape performance
curves over multiple timescales will be key to
making better predictions about how climate
change will affect organisms.
Acknowledgments
We thank Lynn Martin for helpful comments on the
manuscript.
Funding
The symposium was made possible by generous support from the National Science Foundation (IOS1545787), the Society for Integrative and Comparative
Biology, and The Company of Biologists. Michael E.
Dillon was supported by NSF IOS-1457659, and H.
Arthur Woods was supported by NSF IOS-1341485.
Beyond the mean Introduction
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