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Biol. Rev. (2017), pp. 000–000.
doi: 10.1111/brv.12344

Managing consequences of climate-driven
species redistribution requires integration of
ecology, conservation and social science
Timothy C. Bonebrake1∗ , Christopher J. Brown2 , Johann D. Bell3,4 ,Julia L. Blanchard5,6 , Alienor Chauvenet7,8 , Curtis Champion5 , I-Ching Chen9 ,Timothy D. Clark5,10 , Robert K. Colwell11,12,13,14 , Finn Danielsen15 ,Anthony I. Dell16,17 , Jennifer M. Donelson18,19 , Birgitta Evengård20 , Simon Ferrier21 ,Stewart Frusher5,6 , Raquel A. Garcia22,23 , Roger B. Griffis24 , Alistair J. Hobday6,25 ,Marta A. Jarzyna26 , Emma Lee6 , Jonathan Lenoir27 , Hlif Linnetved28 ,Victoria Y. Martin29 , Phillipa C. McCormack30 , Jan McDonald6,30 ,Eve McDonald-Madden8,31 , Nicola Mitchell32 , Tero Mustonen33 , John M. Pandolfi34 ,Nathalie Pettorelli35 , Hugh Possingham8,36 , Peter Pulsifer37 , Mark Reynolds38 ,Brett R. Scheffers39 , Cascade J. B. Sorte40 , Jan M. Strugnell41 , Mao-Ning Tuanmu42 ,Samantha Twiname5 , Adriana Vergés43 , Cecilia Villanueva5 , Erik Wapstra44 ,Thomas Wernberg32,45 and Gretta T. Pecl5,6
1

School of Biological Sciences, The University of Hong Kong, Hong Kong SAR, 999077, China
Australian Rivers Institute, Griffith University, Nathan 4111, Australia
3
Australian National Centre for Ocean Resources and Security, University of Wollongong, Wollongong, NSW 2522, Australia
4
Conservation International, Arlington, VA 22202, U.S.A.
5
Institute for Marine and Antarctic Studies, University of Tasmania, Hobart, TAS 7001, Australia
6
Centre for Marine Socioecology, University of Tasmania, Hobart, TAS 7001, Australia
7 Centre for Biodiversity and Conservation Science, University of Queensland, St Lucia, 4072, Australia
8
ARC Centre of Excellence for Environmental Decisions, School of Biological Sciences, The University of Queensland, Brisbane, 4072, Australia
9Department of Life Sciences, National Cheng Kung University, Tainan 701, Republic of China
10 CSIRO Agriculture and Food, Hobart 7000, Australia
11
Center for Macroecology, Evolution and Climate, University of Copenhagen, Natural History Museum of Denmark, 2100, Copenhagen, Denmark
12
Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, CT 06269, U.S.A.
13 University of Colorado Museum of Natural History, Boulder, CO 80309, U.S.A.
14
Departmento de Ecologia, Universidade Federal de Goiás, CP 131, 74.001-970 Goiânia, Brazil
15
Nordic Foundation for Development and Ecology (NORDECO), Copenhagen, DK-1159, Denmark
16 National Great Rivers Research and Education Center (NGRREC), East Alton, IL 62024, U.S.A.
17
Department of Biology, Washington University in St. Louis, St. Louis, MO 631303, USA
18
School of Life Sciences, University of Technology, Sydney, 2007, Australia
19
ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville 4811, Australia
20
Division of Infectious Diseases, Department of Clinical Microbiology, Umea University, 90187 Umea, Sweden
21
CSIRO Land and Water, Canberra 2601, Australia
22
Department of Statistical Sciences, Centre for Statistics in Ecology, the Environment and Conservation, University of Cape Town, Rondebosch,
7701 South Africa
23
Faculty of Science, Department of Botany and Zoology, Centre for Invasion Biology, Stellenbosch University, Matieland 7602, South Africa
24
NOAA National Marine Fisheries Service, Office of Science and Technology, Silver Spring, MD 20910, U.S.A.
25
CSIRO, Oceans and Atmosphere, Hobart 7000, Australia
2* Address for correspondence (Tel: +852 2299 0675; E-mail: tbone@hku.hk)
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Timothy C. Bonebrake and others

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Department of Ecology and Evolutionary Biology, Yale University, New Haven, CT 06511, U.S.A.
UR « Ecologie et dynamique des systèmes anthropisés » (EDYSAN, FRE 3498 CNRS-UPJV), Université de Picardie Jules Verne,
FR-80037, Amiens Cedex 1, France
28
Faculty of Science, Institute of Food and Resource Economics, University of Copenhagen, DK-1958 Frederiksberg C, Denmark
29
Cornell Lab of Ornithology, Cornell University, Ithaca, NY 14850, U.S.A.
30
Faculty of Law, University of Tasmania, Hobart, 7001, Australia
31
School of Geography, Planning and Environmental Management, The University of Queensland, Brisbane 4072, Australia
32 School of Biological Sciences, University of Western Australia, Crawley 6009, Australia
33
Snowchange Cooperative, University of Eastern Finland, 80130 Joensuu, Finland
34
School of Biological Sciences, ARC Centre of Excellence for Coral Reef Studies, The University of Queensland, Brisbane 4072, Australia
35 Institute of Zoology, Zoological Society of London, NW1 4RY, London, U.K.
36
Grand Challenges in Ecosystems and the Environment, Silwood Park, Imperial College, London, SW7 2AZ, UK
37
National Snow and Ice Data Center, University of Colorado Boulder, Boulder, CO 80309, U.S.A.
38 The Nature Conservancy, San Francisco, CA 94105, U.S.A.
39
Department of Wildlife Ecology and Conservation, University of Florida/IFAS, Gainesville, FL 32611, U.S.A.
40
Department of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697, U.S.A.
41 Centre for Sustainable Tropical Fisheries and Aquaculture, College of Science and Engineering, James Cook University, Townsville 4811,
Australia
42
Biodiversity Research Center, Academia Sinica, Taipei 115, Republic of China
43
Centre for Marine Bio-Innovation and Evolution & Ecology Research Centre, School of Biological, Earth and Environmental Sciences,
University of New South Wales, Sydney 2052, Australia
44
School of Biological Sciences, University of Tasmania, Tasmania 7001, Australia
45
UWA Oceans Institute, University of Western Australia, Perth 6009, Australia
27

ABSTRACT
Climate change is driving a pervasive global redistribution of the planet’s species. Species redistribution poses newquestions for the study of ecosystems, conservation science and human societies that require a coordinated andintegrated approach. Here we review recent progress, key gaps and strategic directions in this nascent research area,emphasising emerging themes in species redistribution biology, the importance of understanding underlying drivers andthe need to anticipate novel outcomes of changes in species ranges. We highlight that species redistribution has manifest
implications across multiple temporal and spatial scales and from genes to ecosystems. Understanding range shifts from
ecological, physiological, genetic and biogeographical perspectives is essential for informing changing paradigms inconservation science and for designing conservation strategies that incorporate changing population connectivity andadvance adaptation to climate change. Species redistributions present challenges for human well-being, environmental
management and sustainable development. By synthesising recent approaches, theories and tools, our review establishes
an interdisciplinary foundation for the development of future research on species redistribution. Specifically, wedemonstrate how ecological, conservation and social research on species redistribution can best be achieved byworking across disciplinary boundaries to develop and implement solutions to climate change challenges. Future studies
should therefore integrate existing and complementary scientific frameworks while incorporating social science andhuman-centred approaches. Finally, we emphasise that the best science will not be useful unless more scientists engage
with managers, policy makers and the public to develop responsible and socially acceptable options for the global
challenges arising from species redistributions.
Key words: adaptive conservation, climate change, food security, health, managed relocation, range shift, sustainable
development, temperature.
CONTENTS
I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
II. Species redistribution as a field of research . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
III. Species redistribution ecology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(1) Physiological and ecological factors underpinning species redistribution . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(2) Biotic interactions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Biological Reviews (2017) 000–000 © 2017 Cambridge Philosophical Society

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3(3) Community redistribution and historical ecology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(4) Climate trends, scale mismatch and extreme events . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(5) Anticipating future redistributions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
IV. Conservation actions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(1) Adapting management in current conservation landscapes and seascapes . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(2) Facilitating natural species movement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(3) Resource-management systems for species redistribution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(4) Managed relocation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
V. Social and economic impacts of species redistribution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(1) Food security . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(2) Indigenous livelihoods, governance and cultures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(3) Human health . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(4) Need for monitoring . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
VI. Interdisciplinary approaches to address species redistribution challenges . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
VII. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
VIII. Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
IX. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
X. Supporting Information . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

I. INTRODUCTION
Species across the globe, in all ecosystems, are shifting theirdistributions in response to recent and ongoing climatechange (Parmesan & Yohe, 2003; Sorte, Williams & Carlton,
2010; Pinsky et al., 2013; Alofs, Jackson & Lester, 2014; Lenoir& Svenning, 2015; Poloczanska et al., 2016; Scheffers et al.,2016). These shifts are faster at greater levels of warming(Chen et al., 2011) and are projected to accelerate into the
future with continued changes in the global climate system(Urban, 2015). Thus, there is a clear need to understand theimpacts and consequences of global species redistribution forecosystem dynamics and functioning, for conservation andfor human societies (Pecl et al., 2017).
Species range dynamics and climate have an intertwined
history in ecological research going back centuries (Grinnell,
1917; Parmesan, 2006). However, research on species range
shifts driven by contemporary climate change is relatively
recent, dating back only 20 years (Southward, Hawkins& Burrows, 1995). In the past decade, research on thesubject has increased dramatically (Fig. 1). While coverage
is far from complete methodologically, geographically or
taxonomically (Lenoir & Svenning, 2015; Brown et al.,2016; Feeley, Stroud & Perez, 2017), this increased
research effort highlights growing awareness that species
are moving in response to climate change, worldwide (IPCC,
2014).
We believe that ‘species redistribution science’ hasemerged as a field in its own right. However, to date thefield has lacked strategic direction and an interdisciplinary
consideration of research priorities. Historically, researchers
have used ‘species range shifts’ or ‘species distribution
shifts’ as favoured descriptive terms for climate-driven
species movements. Here we use the term ‘species
redistribution’ to encapsulate not only species movement,
but also its consequences for whole ecosystems andlinked social systems. Despite accumulating evidence

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of recent climate-driven species redistributions (Lenoir& Svenning, 2015; Poloczanska et al., 2016; Scheffers
et al., 2016), integrated and interdisciplinary frameworks
that can effectively predict the ecological, conservationand societal consequences of these changes remain
uncommon [but see Williams et al. (2008) for a framework
highlighting species vulnerability and potential management
responses]. A long-term strategy for the field of species
redistribution research is required to capitalise on, andrespond to, the ‘global experiment’ of large-scale changes
in our natural and managed ecosystems. What canbe implemented now to build scientific and social
capacity for adaptation to species redistribution overthe next decade, the next century and beyond (IPCC,
2014)?
The ‘Species on the Move’ conference (held in Hobart,
Australia, 9–12 February 2016) brought together scientists
from across the physical, biological and social sciences. Here,
we build on the outcomes of this conference by identifying key
research directions to meet the global challenge of preparing
for the impacts of climate-driven species redistribution on
the biosphere and human society. We focus on directions
and needs around three focal points for understanding
species redistribution and its impacts: (i) species redistribution
ecology, (ii) conservation actions, and (iii) social andeconomic impacts and responses. For each focal point wesummarise recent trends in the field and propose priority
questions for future research. We identify promising research
directions and approaches for addressing these questions,placing emphasis on the potential benefits from integrating
approaches across multiple disciplines and sub-disciplines. In
so doing, we argue that greater interdisciplinary synthesis isfundamental to ensuring that species redistribution researchcontinues to advance beyond simple documentation of
species range shifts, to develop research programs andachieve outcomes that will inform policy and management
decisions.
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Timothy C. Bonebrake and others

Fig. 1. Publication trends for papers on species range shifts. (A) Proportion of publications addressing species redistribution over atime, as a fraction of all papers in environmental sciences/ecology fields. (B) Number of journals publishing species redistribution
papers over time. (C) Median annual citation rate of species redistribution papers decreases to the median annual citation rate ofpapers in the general environmental sciences/ecology field.

II. SPECIES REDISTRIBUTION AS A FIELD OFRESEARCH
To support our synthesis of future directions, we firstestablish how the research field of climate-driven species
redistributions has evolved and quantify, bibliometrically,
the prevailing research foci. To understand this history inthe context of the broader scientific literature, we analysed
publication trends in the peer-reviewed literature on species
range shifts over the past 25 years. In total we extracted
1609 publications from Thompson Reuters Web of Sciencethat contained search terms relating to distribution changeor range shift (see online Appendix S1 for details).
In 2006, both the proportion of range shift publicationsin the ‘environmental sciences’ and the diversity of journals
publishing research on range shifts showed a clear increase(Fig. 1). At the same time, citation rates dropped relative
to the discipline’s baseline heralding that publications about
range shifts had shifted from a few high-profile publications
to mainstream ecological science (Fig. 1).
We analysed this corpus to identify research trends in
two ways. First, we identified ‘trending’ terms. Terms were
defined based on word stems, and trending terms were thosethat showed a significant increase in use in titles, abstracts or
key words since 1995. Second, we identified ‘high-impact’
terms, i.e. those associated with higher than average citation
rates, once we had accounted for the confounding effect ofpublication year. The trends analysis indicated that range
shift science has become increasingly interdisciplinary overtime. Terms associated with socioeconomic approaches,such as ‘ecosystem services’ have also become increasingly
prevalent and tend to be associated with high-impact
papers (Fig. 2). Management-oriented studies, with terms
including ‘priority’ (referring to management priorities) arealso increasing in use. Both socioeconomic (‘social’, ‘socioeconomic’) and management-related terms (‘complement*’
referring to complementary protection) were associatedBiological Reviews (2017) 000–000 © 2017 Cambridge Philosophical Society

with higher than average citation rates during the period
2010–2015 (Fig. 2). Thus, we find clear evidence for the
emergence of a new field that is generating increasing
interest, while expanding to link with other existing andemerging fields.

III. SPECIES REDISTRIBUTION ECOLOGYSpecies redistribution has been widely documented (Scheffers
et al., 2016) and well-developed theories have been proposed
to explain how and why range shifts occur (Bates et al.,2014) and how future species redistribution may proceed
under global climate change (Urban et al., 2016). Hence,
we can consider the ecology of species redistribution
under two broad and complementary areas: explanatory
ecology and anticipatory ecology. Explanatory ecology
generally aims to evaluate models and theory to enhancescientific understanding of the processes that drive species
redistribution. For detailed reviews on subject areas specificto explanatory ecology we refer the reader to Somero (2010)(physiological factors), Blois et al. (2013) (biotic interactions),
Maguire et al. (2015) (historical ecology), and Garcia et al.
(2014) (climate trends/extreme events). Anticipatory ecology,
by contrast, intends to forecast future states by inferring
possible trajectories or behaviours of the system, basedon parameters likely to be impacted by anthropogenic
factors, such as predicting the effects of climate change on
species, communities and ecosystems. For detailed reviews ofanticipatory ecology we recommend Urban et al. (2016) andCabral, Valente & Hartig (2016).
In this section, we do not duplicate former reviewsof the explanatory and anticipatory ecology of species
redistribution. Our review focuses, instead, on gaps inexplanatory and anticipatory ecology (Table 1) that need
to be filled in order to predict the impacts of species
redistribution on biodiversity and human well-being.

Research directions in species redistribution

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Fig. 2. Analysis of trends used within the species redistribution literature: (A) top 20 trending words that increased significantly inusage, and (B) top 20 high-impact words that correspond with increased citation rates of papers published between 2010 and 2015.
See online Appendix S1. sdm, species redistribution model.

To achieve this aim, we examine multiple elementsof explanatory ecology, including the physiological andecological factors underpinning species redistribution, biotic
interactions and historical ecology, as well as climate trends
and extreme events. We conclude this section with a
discussion of the challenges of anticipatory ecology.
(1) Physiological and ecological factors
underpinning species redistribution
Climate change is causing pervasive impacts on ectothermic
animals because of their reliance on environmental
temperature to regulate body temperature (Deutsch et al.,2008; Kearney & Porter, 2009). Thermal performance
curves, which quantify how an ectotherm’s body temperature
affects its performance or fitness, are used to understandrange shifts and to predict future distributions (Sunday,
Bates & Dulvy, 2012; Sunday et al., 2014). While thermal
tolerance and performance patterns have been well studied
for ectothermic taxa (Dell, Pawar & Savage, 2011), similar
trends in large-scale patterns of climatic niche, e.g. heat
tolerance conserved across lineages, are also apparent
for endotherms and plants (Araújo et al., 2013). The
use of thermal performance curves in predicting species
distributions often disregards ecological interactions (e.g.
competition, predation, mutualism) that may be critical topopulation establishment and persistence (but see Urban,
Tewksbury & Sheldon, 2012). In addition, the form of eachspecies’ performance curve has important effects on species

interactions, with asymmetries in the thermal performance
curves between interacting species likely having important
impacts on the strength and outcome of interactions (Dellet al., 2011; Dell, Pawar & Savage, 2014). Physiologicalplasticity (e.g. thermal acclimation), resource specialisation,competitive interactions and behavioural thermoregulation(Thomas et al., 2001; Burton, Phillips & Travis, 2010; Fearyet al., 2014; Sunday et al., 2014; Tunney et al., 2014; Tedeschi
et al., 2016) are additional factors that can modify thermal
performance curves and/or impact the nature and outcomeof species range shifts.
Future research would therefore benefit from approaches
that connect mechanistic processes across biological levelsof organisation, from genes to ecosystems. For example,
because selection acts on individual genotypes/phenotypes,
an understanding of intraspecific variation in key functional
traits will help in forecasting species’ breadth of tolerance
and capacity for range shifts (Norin, Malte & Clark, 2016). In
general, both low and high variability in thermal tolerances
can exist within and among populations and may vary withextrinsic factors such as environmental filtering, which causes
a convergence in tolerance (i.e. heat hardening; Phillips et al.,2015), or intrinsic factors such as body size or life-history
stages, which might result in thermal tolerance dispersion(Ray, 1960; Angilletta, Steury & Sears, 2004; Daufresne,
Lengfellner & Sommer, 2009; Cheung et al., 2013; Scheffers
et al., 2013).
The mechanistic basis behind variability in thermal
tolerance remains poorly understood (Clark, Sandblom &Biological Reviews (2017) 000–000 © 2017 Cambridge Philosophical Society

Timothy C. Bonebrake and others

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Table 1. Key questions posed by attendees of the 2016 Species on the Move conference and additional questions developed for eachresearch focus: Ecology, Conservation and Society. Also included for each key question are cross-cutting themes (sensu Kennicutt
et al., 2015). ECO, Ecology; CONS, Conservation; SOC, Society; SDM, species redistribution model

Key questions and topics
Ecology
To what extent will novel species combinations
impact future change to ecological communities?
CONS/SOC
How much do biotic interactions affect range shifts,
compared to the effects on ranges from species
traits, geographic context and physical rates ofchange? CONS
How can we predict species responses to extreme
events? Much empirical physical research is
focused on extreme events, but most
biological/ecological modelling evaluates slow
long-term change. CONS/SOC
What is the role of plasticity (physiological,
behavioural) in mediating species responses within
and between populations, and how does plasticity
affect modelling predictions? CONS
What are the main determinants of time lags in biotic
responses to climate change (the climatic debt)?
CONS
How will uncertainty in climate change projections
affect predictions of species redistribution? CONS
How can co-occurring taxa/communities best be
modelled under changing climates? CONS
Conservation
How can we integrate uncertainty into theconservation planning process? What time frame
allows for robust actions while minimising
uncertainty? SOC
How can we monitor large-scale landscapes andseascapes and complex natural and social
interactions best across regions? ECO/SOC
What are the values and risks associated with novelcommunities that arise from individual species
range shifts? What are the effects of invasive
species on the maintenance of phylogenetic andfunctional diversity? ECO
How do we apply prescriptive/assisted evolution toaccommodate species redistribution? ECO
How can we build dynamic conservation
management strategies that cope with changes in
species distributions? SOC
How does climate change interact with other driversof biodiversity change (e.g. invasive species, land
use and fire) to influence outcomes for biodiversity(all species)? ECO/SOC
Will microrefugia allow species to persist locally as
climate changes? If so, where are they? ECOSociety
How do species redistributions impact ecosystemservices through biodiversity reshuffling? ECO
What are the key messages we need to communicate
to the public about shifting distribution of marine
and terrestrial species? How do we communicate
them effectively? ECOApproaches and interdisciplinary
cross-cutting

References

Experimental manipulation
Modelling

Urban et al. (2012) and Alexander et al.
(2015)

Incorporation of species interactions
into SDMs
Palaeoecological methods

Ferrier et al. (2007), Wisz et al. (2013),
Blois et al. (2013) and Fitzpatrick et al.
(2013)

Incorporate extreme climatic events
into modelling/predictions
Measure key mechanistic processes

Zimmermann et al. (2009), Azzurro et al.
(2014) and Briscoe et al. (2016)

Accounting for intraspecific differencesin realised niche

Valladares et al. (2014) and Bennett et al.
(2015)

Explaining magnitude of lags in
response to climate change in
addition to the magnitude of the shift
Multi-model ensemble averaging

Bertrand et al. (2016)
Fordham et al. (2011)

Community-level models

Maguire et al. (2016)

Decision science

Shoo et al. (2013)

Monitoring to adjust (adaptive)
conservation actions continuouslyInterpretation of satellite
remote-sensing, population surveys
Assessing functional and phylogenetic
diversity
Palaeoecological methods

Tøttrup et al. (2008), Pettorelli et al.
(2014) and Kays et al. (2015)
Buisson et al. (2013) and Albouy et al.
(2015)

Molecular ecology
Conservation genomics
Sequential dynamic optimsation

Smith et al. (2014) and Hoffmann et al.
(2015)
Alagador et al. (2014)

Management of local stressors
Coupled population and SDMs

Russell et al. (2009), Bonebrake et al.
(2014) and Jetz et al. (2007)

Climate change metrics
Fine-scale grids

Keppel et al. (2012) and Ashcroft et al.
(2012)

Coupled SDM and trait-based methods

Moor et al. (2015)

Creating opportunities for respectful
dialogue between scientists and the
publicImproving ecological and science
literacy

Jordan et al. (2009)
Groffman et al. (2010)

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Table 1. Continued

Key questions and topics
How can people and communities contribute further
to monitoring the impacts of changes in the
distributions and relative abundances of species
caused by climate change? ECO/CONS
What is the effect of climate change on soil
biodiversity, and how does climate change affectsoil health and agriculture? ECO/CONS
How can marine spatial planning be reorganised toreconcile biodiversity conservation and foodsecurity? ECO/CONS
What practical adaptations for agriculture, fisheries
and aquaculture can be promoted to minimise therisks to food security and maximise theopportunities that are expected to arise fromaltered species distributions? ECO/CONS
How will climate change impact the redistribution of
disease-associated species and influence infectious
disease dynamics? ECO
How can international environmental agreementsthat influence resource-management decisions
incorporate local community observations andinsights into their guidance and policy-making
objectives? CONS

Approaches and interdisciplinary
cross-cutting

References

Community-based observation systems

Higa et al. (2013) and Chandler et al.
(2016)

SDMs and soil science

Hannah et al. (2013) and le Roux et al.
(2013)

Adaptive management
Restoration

Garcia & Rosenberg (2010), Rice &Garcia (2011) and Sale et al. (2014)

Adaptive management
Restoration

Bradley et al. (2012) and Bell et al. (2013)

Host and vector SDMs

Rohr et al. (2008) and Harrigan et al.
(2014)

Evidence-based legal processes
Multiple evidence-based frameworks

Tengö et al. (2017)

Jutfelt, 2013) but may be revealed through new genetic
tools (Bentley et al., 2017). Measuring genetic diversity asorganisms expand their range and documenting genetic
structure during and after colonisation can provide a wealthof information on evolutionary dynamics of range shifts(McInerny et al., 2009; Sexton, Strauss & Rice, 2011; Duputié
et al., 2012), but requires new, dedicated research programs
and/or careful analysis of historical museum collections.
Knowledge of the genetics underpinning thermal tolerance
can directly inform species conservation and ecosystem
restoration through assisted evolution applications (Van
Oppen et al., 2015).
The magnitude of range shifts can be population,
species, and ecosystem dependent, suggesting determinants
or mediators of species redistribution other than climate(Rapacciuolo et al., 2014; Rowe et al., 2015). Species
redistribution studies have commonly sought to identify
ecological traits that explain species responses (see Fig. 2;
McGill et al., 2006; Sunday et al., 2015; Pacifici et al., 2015).
However, trait-based studies have had mixed success at
identifying predictors of range shifts, with thermal niches
and climate trends remaining in general the strongest
explanatory variables (Buckley & Kingsolver, 2012; Pinsky
et al., 2013; Sommer et al., 2014; Sunday et al., 2015). Key
traits may include those related to dispersal and establishment(Angert et al., 2011; Sunday et al., 2015; Estrada et al.,2016), local persistence, such as intrinsic ability to toleratechanging climate (physiological specialisation; Bertrand
et al., 2016), phenotypic plasticity (Valladares et al., 2014),
micro-evolutionary processes (genetic adaptation; Duputié

et al., 2012), capacity to utilise microhabitat buffering effects(Scheffers et al., 2013), fossorial habits (Pacifici et al., 2017),
and tolerance to habitat fragmentation (Hodgson et al.,2012). Determining the contexts and conditions under which
different traits mediate species redistribution, and to what
degree those traits determine redistribution, is an importantavenue of future research.
(2) Biotic interactions
In general, biotic interactions remain under-measured inrange-shift studies, yet they likely play a key role in mediating
many climate-induced range shifts (Davis et al., 1998;
HilleRisLambers et al., 2013; Ockendon et al., 2014). Shifts
in species interactions will occur as a result of differential
responses to climate by individual species that can lead toasynchronous migrations within communities and creation ofnovel assemblages (Pörtner & Farrell, 2008; Hobbs, Higgs &Harris, 2009; Gilman et al., 2010; Urban et al., 2012; Kortschet al., 2015; Barceló et al., 2016). Asynchronous shifts can also
cause decoupling of trophic interactions, for example whensymbiont–host interactions break down (Hoegh-Guldberg
et al., 2007) through mismatches in the phenology between
consumers and their resources (Winder & Schindler, 2004;
Durant et al., 2005; Post & Forchhammer, 2008; Thackeray
et al., 2016) or through differential thermal sensitivity of
consumers and their resources (Dell et al., 2014). Conversely,
climate change and species distribution shifts can create novel
species interactions through range expansions, as species thathave evolved in isolation from one another come into contact
Biological Reviews (2017) 000–000 © 2017 Cambridge Philosophical Society

8for the first time (Vergés et al., 2014; Sánchez-Guillén et al.,2015).
Some of the most dramatic impacts of communitychange are likely to arise through the assembly ofnovel species combinations following asynchronous range
shifts associated with climate change (Urban et al., 2012;
Alexander, Diez & Levine, 2015). These predictions aresupported by palaeoecological studies that show how novel
species interactions resulting from past climatic changes
drove profound community-level change (Blois et al., 2013).
The emergence of novel ecological communities will posesignificant conservation and societal challenges, because mostmanagement paradigms are insufficient to cope with major
reorganisation of ecosystems (Morse et al., 2014; Radeloff
et al., 2015). Studies of the response of linked social-ecologicalsystems to historical climatic changes are needed to informthe management of ecosystems under ongoing and futureclimate change (e.g. Hamilton, Brown & Rasmussen, 2003).
Contemporary observations of extreme events suggest thatshifts in species interactions are particularly important when
redistribution occurs in foundation (i.e. habitat-forming) or
keystone species. Shifts in foundation species can initiatecascading effects on other species and act as biotic multipliersof climate change (Zarnetske, Skelly & Urban, 2012). For
example, many of the greatest ecosystem impacts of climatechange in marine systems have been caused by the lossof habitat-forming species such as corals, kelp forests andseagrasses (Hoegh-Guldberg & Bruno, 2010; Thomson et al.,2015; Vergés et al., 2016; Wernberg et al., 2016).
Explanatory ecology is now shifting its focus from single
species to the role of biotic interactions in mediating range
shifts. A key research priority is to identify the importanceof biotic interactions relative to species traits, geographic
context and physical rates of change (Sunday et al., 2015).
A limiting factor has been the lack of multi-species ‘climatechange experiments’ (Wernberg, Smale & Thomsen, 2012)and long time-series data that follow multiple trophic levels(Brown et al., 2016). Thus, there is a need to join multiple
data sets in order to understand how biotic interactions shaperange shifts. Understanding the role of biotic interactions in
species redistribution is important to inform conservation andsocietal challenges. For instance, models of three interacting
invasive pests (potato tuber moths) in the Andes predictedthat their redistribution would alter biotic interactions, which
would in turn impact the level of crop damage (Crespo-Pérez
et al., 2015).
(3) Community redistribution and historicalecology
Despite species redistribution science being born of ecology,
we are still a long way from understanding how species
redistribution will drive changes in ecological communities(Marzloff et al., 2016). Historical ecology suggests that climatechange can result in dramatic alterations in community
structure. For example, the equatorial dip in diversity
evident in modern marine communities (Tittensor et al.,2010) was most pronounced for reef corals during the
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Timothy C. Bonebrake and others
warmer intervals of the last interglacial period (125 ka),
indicating that both leading and trailing edges of species
ranges were responding to increases in ocean temperature(Kiessling et al., 2012). Pleistocene reef records suggest thatspecies and communities are relatively robust to climatechange and that ecological structure generally has persisted
within reef coral communities over multiple climatic cycles(Pandolfi, 1996; Pandolfi & Jackson, 2006). By contrast, many
North American tree species have shifted their individual
distributions and adapted genetically to Quaternary climaticchanges (Davis & Shaw, 2001). Human migrations,settlement patterns, and species use have also been linked
to environmental change (Graham, Dayton & Erlandson,2003). However, the rate of contemporary climate change,
genetic constraints on rapid adaptation and dramatic land
cover changes over the past century will challenge ‘natural’species redistribution in the Anthropocene (Hoffmann &Sgro, 2011; Moritz & Agudo, 2013) and complicate human
responses to these changes.
A key question for historical ecology is to determine
the extent to which community change is driven by multiple
species-specific responses to climate, versus shifts in key species
driving cascading community change. Historical ecology
can fill an important gap in our understanding, given that
it focuses on systems that were, in most cases, far lessinfluenced by humans than occur presently. Furthermore,studies in deep time allow us a glimpse into the outcomeof processes similar to those that we are watching in theirinfancy today.
(4) Climate trends, scale mismatch and extreme
eventsClimate trends are a key predictor of range shifts due to theimportance of climatic tolerances (or thermal performance
curves) in controlling species ranges. Observational evidenceof the direction of range shifts in terrestrial andaquatic environments are overwhelmingly consistent withexpectations required for species to track temperaturechanges (Sorte et al., 2010; Chen et al., 2011; Comte et al.,2013; Poloczanska et al., 2013). Longitudinal range shifts, aswell as shifts towards the tropics or lower elevations (which
run counter to intuitive expectations), can be attributed tothe complex mosaic of regional climate changes expectedunder global change that involve not only temperature but
also other factors such as precipitation and land-use changes(Lenoir et al., 2010; Crimmins et al., 2011; McCain & Colwell,2011; Tingley et al., 2012; Pinsky et al., 2013; VanDerWal
et al., 2013).
Multi-directional distribution shifts stem partly fromthe spatial arrangement of mountain ranges on landand continental shelves in the ocean, which areimportant physiographic features constraining (as barriers) or
enhancing (as corridors) species redistribution (VanDerWal
et al., 2013; Burrows et al., 2014). For example, the ranges ofsome forest plants are shifting equatorward and upward as
the climate warms in France, likely due to the fact that themain mountain ranges in France are located in the south

Research directions in species redistribution(Alps, Massif Central and Pyrenees; Kuhn et al., 2016). Suchgeographic features may thus represent potential climatic
traps or ‘cul-de-sacs’ for living organisms facing climatechange. The northern Mediterranean Sea, for example, will
likely act as a cul-de-sac for endemic fishes under futureclimate change (Lasram et al., 2010).
A challenge in using climate variables to explain species
redistribution is that species may respond to different climate
variables than those available from historical measurements,
due to a spatial mismatch between the size of thestudied organisms and the scale at which climate data
are collected and modelled (Potter, Woods & Pincebourde,2013). For instance, relationships between climate velocity
and marine species redistribution are weak or non-existentusing global sea-surface temperature data sets to calculate
climate velocity (Brown et al., 2016), but can be strong using
locally measured temperatures that coincide with organism
sampling (Pinsky et al., 2013). Therefore, we consider it aresearch priority to find ways to reconstruct high spatial- andtemporal-resolution temperature histories that are relevantto the organisms under study (Franklin et al., 2013; Kearney,
Isaac & Porter, 2014; Levy et al., 2016). This objective
requires better communication and more collaboration
among climatologists, remote sensing specialists and globalchange biologists to produce climatic grids at spatial andtemporal resolutions that match organism size and thus are
more meaningful for forecasting species redistribution underanthropogenic climate change.
The study of extreme events has been instrumental tospecies redistribution research, because punctuating events
provide distinct natural experiments for the study of
biological responses to climate change. The frequency andamplitude of extreme events is increasing with climate change(IPCC, 2013), placing increasing emphasis on studying
extreme events in the context of longer-term change. Impactsof climate change on biological communities are often
mediated by extreme events (Fraser et al., 2014; Thomson
et al., 2015; Wernberg et al., 2016). For example, ocean
temperatures along the western Australian coast increased
for over 40 years, with kelp forests exhibiting little noticeable
ecological change, but a marine heat wave drove a 100 km
kelp forest range contraction in only 2 years (Wernberg et al.,2016). The infrequent nature of extreme events means thatlong time series are required to document the cumulative
impacts on ecosystems. For example, in Australia, severe
wildfires in quick succession brought about an ecosystem
regime shift in mountain ash forests (Bowman et al., 2014).
A research priority is therefore to extend studies that
document changes arising from a short-term extreme event
into longer time series that may allow us to understand thecumulative effects of changes in frequency of extreme events.
(5) Anticipating future redistributions
The urgency of responding to anthropogenic climate change
has stimulated a shift towards anticipatory ecology thataims to predict future ecological change. The shift toanticipatory ecology is indicated by our literature analysis,

9which found an increased frequency of terms related to
prediction [Fig. 2; terms ‘sdm’ (species distribution model)and ‘maxent’ (a popular tool for such modelling); Phillips &Dudík (2008)]. Approaches to predicting the consequencesof climate change for biodiversity are varied and include
correlative species distribution models (SDMs; Guisan &Zimmermann, 2000) as well as mechanistic and hybrid SDMs
that account for physiological constraints, demographic
processes or environmental forecasts (Kearney & Porter,
2009; Hartog et al., 2011; Webber et al., 2011; Dullinger et al.,2012; Cheung et al., 2015; Table 1). The emergence of thestudy of species redistributions during the era of rapidly
increasing computing power and growing availability ofclimate data has also contributed to the dominance of spatialmodelling techniques. The emphasis on forecasting has
been paralleled by a development of predictive techniques,
including machine-learning algorithms such as maxent(Phillips & Dudík, 2008).
Anticipatory models have recently been progressing on
two fronts. First, mechanistic and process-based models,often including physiology, biotic interactions, and/or
extreme events, are increasingly being used and developedfor biogeographic prediction (Kearney & Porter, 2009;
Cabral et al., 2016). Bioenergetics models, for example, canovercome traditional species distribution model limitations
when making predictions under novel climates, modelling
extreme events and understanding the importance of timingof weather events (e.g. Briscoe et al., 2016). Mechanistic
models tend to be data intensive and have so far been little
used in conservation planning despite significant potential(Evans, Diamond & Kelly, 2015; Mitchell et al., 2016).
However, prospects for process-based models integratingconservation and society are positive, as models become
more flexible, accurate, and accessible (Kearney & Porter,2009).
The second trend with predictive models has been
an increasing focus on physical drivers at appropriate
spatial and temporal scales (Potter et al., 2013). In thisregard, a key perspective in species redistribution is thevelocity of climate change – which measures the geographic
movement of temperature isotherms (Loarie et al., 2009;
Burrows et al., 2011) to project changes in species ranges
and community composition (Hamann et al., 2015). Climate
velocity trajectories (Burrows et al., 2014) based on sea surface
temperatures, for example, were recently combined withinformation on thermal tolerances and habitat preferencesof more than 12000 marine species to project that range
expansions will outnumber range contractions up to theyear 2100. Broadened ranges, in turn, are projected toyield a net local increase in global species richness, withwidespread invasions resulting in both homogenised andnovel communities (Molinos et al., 2015). However, velocity
measures have limitations and can underestimate climatechange exposure for some communities (Dobrowski &Parks, 2016). For marine systems, changes in the speed
and direction of currents can potentially influence dispersal
and therefore population connectivity, and may also need
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10
to be considered for a more complete understanding of
the relationship between climate drivers and rates andmagnitudes of range shifts (Sorte, 2013; Cetina-Heredia
et al., 2015). High-resolution particle-transport Lagrangianmodels may be useful in this context (van Gennip et al., 2017).
Ultimately, examining multiple climate change metrics andlinking them to the threats and opportunities they represent
for species could overcome the limitations of individual
metrics and provide more-robust impact estimates (Garcia
et al., 2014).

IV. CONSERVATION ACTIONS
Faced with climate change as a novel and substantial threat, a
new species-management paradigm has emerged (Stein et al.,2013): to be effective, conservation strategies must accountfor both present and future needs and must be robust to
future climate change. Such strategies will require integrationof species redistribution science with consideration of thesocial and economic consequences (Table 1). Managers
have several options for conserving species and ecosystems
faced with range shifts: adapt conservation managementin current landscapes and seascapes; facilitate natural
species movement; manage resources to support species
redistribution; and/or move species as a conservationintervention, i.e. managed relocation. Important reviews
on conservation under climate change, such as Heller &Zavaleta (2009) and Mawdsley, O’Malley & Ojima (2009),
provide context for adaptation strategies under warming.
In this section we specifically aim to synthesise recent
advances in species redistribution science and conservation
actions that attempt to accommodate species redistributions,requiring the involvement of multiple stakeholders for
effective implementation.
(1) Adapting management in current conservation
landscapes and seascapes
Mitigating the impacts of climate change on species
and ecosystems in situ is challenging, because it requires
management decisions that are robust to future change
and the development of adaptive solutions for specificpopulations (e.g. providing shelter or supplemental food;Correia et al., 2015). Systematic conservation planning efforts
are increasingly incorporating the principles of climatechange adaption into the protected-area design process(Carvalho et al., 2011; Groves et al., 2012), ensuring thatexisting protected areas are resilient to climate change
by maintaining and increasing the area of high-quality
habitats, prioritising areas that have high environmental
heterogeneity, and controlling other anthropogenic threats(Hodgson et al., 2009). Habitat engineering may also be
required to provide effective recovery and maintenanceof populations, for example, through the installation of
microclimate and microhabitat refuges or enhancement andrestoration of breeding sites (Shoo et al., 2011). Identification
Biological Reviews (2017) 000–000 © 2017 Cambridge Philosophical Society

Timothy C. Bonebrake and othersof microrefugia, small areas robust to warming impacts overlong time periods, will also be key for long-term planning(Lenoir, Hattab & Pierre, 2017). In many countries, the legal
and governance framework underpinning protected-areamanagement may not yet allow for these types of active
management interventions (McDonald et al., 2016a), so legal
reform may be needed.
(2) Facilitating natural species movement
As the most suitable habitat conditions for species are
shifting geographically under climate change and species
redistribute themselves, forward planning is increasingly
essential, both temporally and spatially (Mawdsley et al.,2009). Although most palaeoecological studies (e.g. Williams& Jackson, 2007) indicate that range shifts alone do not drive
widespread extinction events [but see Nogués-Bravo et al.
(2010) who did find evidence for extinctions], range-restricted
species potentially face high climate-driven extinction risks(Finnegan et al., 2015; Urban, 2015).
Reserve networks must consider current biodiversity,
probable patterns of future biodiversity, corridors suitablefor projected range shifts, and cost (Lawler et al., 2015;
Scriven et al., 2015), anticipating the need for protected-areaestablishment in newly suitable areas (Carvalho et al., 2011).
Climate-velocity methods (Burrows et al., 2014) or the analysis
of fine-scaled climatic grids (Ashcroft et al., 2012) can be used
to identify climate refugia – places where microclimates aredecoupled from macroclimatic fluctuations and are thus
more stable and less likely to change quickly – as potentiallygood candidates for future protected areas. Information
on future habitat suitability for threatened species (e.g.
obtained using SDMs) can be coupled with information on
climate refugia to target areas likely to maximise conservation
benefits (see Hannah et al., 2014; Slavich et al., 2014). To assesslandscape or seascape connectivity with greater realism,
patterns of habitat fragmentation (McGuire et al., 2016) andflow must be considered, i.e. wind and oceanic currents(Péron et al., 2010; Sorte, 2013; van Gennip et al., 2017).
In some cases, facilitating species redistribution canbe achieved through the expansion or realignmentof existing protected area boundaries. Where publicconservation funding is limited, it may be necessary
in some circumstances to release protection of someareas in order to secure others of higher priority(Alagador, Cerdeira & Araújo, 2014). In addition tomaintaining connectivity through reserve network design,
market-based instruments and public–private partnerships
can be harnessed to accommodate species redistribution.
Conservation easements, for example, while popular andpotentially effective in environmental protection of private
land, rarely consider climate change impacts or species
redistribution (Rissman et al., 2015). New mechanisms
for private land stewardship and management, including
Indigenous Protected Area (IPA) agreements, will also beneeded.
Conservation interventions designed to meet contemporary environmental challenges can conflict with climate

Research directions in species redistributionchange planning objectives. For example, fences in Africa
around wildlife reserves have been good for minimising
human–wildlife conflict but poor for maintaining landscapeconnectivity (Durant et al., 2015). Similarly, shifts in agriculturally suitable areas in the Albertine region of Africa,
as a result of changing climate, may cause a displacementof agriculture into protected areas, significantly complicatingclimate-driven species redistribution impacts on conservationplans for the region (Watson & Segan, 2013).
(3) Resource-management systems for species
redistribution
Some existing resource-management systems can beextended for adaptive management of species on the move.
For example, a real-time management system is used ineastern Australia to predict the distribution of a tuna species
over the cycle of a fishing season (Hobday & Hartmann,
2006; Hobday et al., 2011). The changing distribution of the
fish requires dynamic responses to zones that restrict fishingactivity. While this example of species redistribution is on aseasonal timescale, the management system can also respondto long-term species redistribution, based on regular updatesof the management zones. Such real-time management
responses to changing species distributions are relatively
advanced in marine systems and are being formalised in thefield of dynamic ocean management (Hobday et al., 2014;
Lewison et al., 2015; Maxwell et al., 2015).
Conservation strategies for mobile and range-shifting
species can also utilise innovative market-based instruments
and develop new partnerships involving private landholders.
A promising example is The Nature Conservancy’s
California pop-up wetland initiative, which involves seasonalland ‘rentals’, in which farmers agree to flood their fields
to facilitate water bird migration (McColl et al., 2016).
Predictive habitat modelling of bird migration is used toearmark different land parcels, and landholders submit bids
to participate in each year’s habitat creation program. As
in this example, local and regional conservation planningfor multiple uses requires good-quality data, plus resources
for monitoring and implementation. Researchers also needto understand what information land-owners, planners andpolicy makers actually need to aid decision-making, which
requires considerable engagement and knowledge exchange(Cvitanovic et al., 2015).
As part of this engagement, structured decision-making
processes can inject both values and scientific data into thedevelopment of management strategies for ecosystem-basedmarine management, as proposed for development ofhigh seas protected areas (Maxwell, Ban & Morgan,2014). Options for managers and policy makers can beevaluated with quantitative modelling tools, such as models
of intermediate complexity (Plagányi et al., 2014), while
management strategy evaluation (Bunnefeld, Hoshino &Milner-Gulland, 2016) can be used to test climate-smart
management strategies that include socio-ecological criteria.
In addition to novel dynamic management approaches,existing tools in development and conservation law, such11
as biodiversity offsets, will need to be modified to promote
adaptive conservation planning for species redistribution(McDonald, McCormack & Foerster, 2016b) and to allow
management responses on appropriate timescales (Hobday
et al., 2014).
(4) Managed relocation
Given numerous decision frameworks for managed
relocation, the science required to inform any decision to
relocate a species is defined by knowledge gaps in local
species ecology and management (e.g. Richardson et al.,2009; McDonald-Madden et al., 2011; Rout et al., 2013 andsee Article 9 in Glowka et al., 1994). Trial introductions of
the critically endangered western swamp turtle (Pseudemydura
umbrina) to the south-western corner of Australia (300 km
south of its native range), in 2016, serve as a useful example.
For the turtle, persistence in the wild is constrained bysevere habitat loss and fragmentation and by a rapid
reduction in winter rainfall. Correlative SDMs based oncoarse-grained climatic data have created a challenge fortranslocation planning, as the turtle historically occupies
just two wetlands 5 km apart (Mitchell et al., 2013). The
solution has been to build mechanistic SDMs that are
based on detailed knowledge of the turtle’s physiologicallimits, behaviour, and the ecohydrology of their ephemeral
wetland habitats (Mitchell et al., 2013, 2016). Forcing theseprocess-based SDMs with future drier and warmer climates
has illustrated where suitable habitat might exist into the
future, and when complemented with spatially explicit
multiple criteria analysis (Dade, Pauli & Mitchell, 2014) has
identified candidate wetlands for future attempts to establish
outside-of-range populations.
The primary challenge for practicing managed relocation
is identifying ways to overcome any social barriers to
relocation. Relocating species for conservation can challenge
deeply held values and beliefs about human intervention
in nature, and what constitutes appropriate and desirable
environmental stewardship. Particular challenges may arise
for Indigenous peoples, for whom connection to landscapesand historically, culturally and spiritually significant species isof great importance. Formal mechanisms for engaging withlocal communities and stakeholders, including considerationof the cultural effects and drivers of proactive conservation
management under climate change, will be critical. Issues
include cultural nuances, such as the terminology used inmanagement proposals and policy. For example the term‘assisted colonisation’, adopted in the guidelines of theInternational Union for Conservation of Nature (IUCN) for
species introductions outside of the known range to prevent
extinction, has historical and colonial connotations with theword ‘colonisation’ that may create barriers to participation.
In this case, an alternative, culturally considerate phrase toencourage broader inclusion might be ‘managed relocation’(see Schwartz et al., 2012).
The IUCN guidelines for conservation translocations(IUCN/SSC, 2013) provide a complete framework toassess the need for managed relocation, including the risks
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12
associated with translocations for the species of interest andfor the ecosystem that receives the new species. Potential
damage to the ecosystem from managed relocation is theworst-case scenario, and this issue forces decision-makers
to ask themselves what they value most. Is the survival ofa particular species that is threatened by human actions
sometimes worth the risk of profound change to therecipient ecosystem? If we aim for a species to thrive,
when does it become invasive? These are questions thatwill need to be answered as managed relocation forconservation becomes more frequent. Legislative reform
is also required to change the regional and domestic
laws and policies that guide practical implementation ofmanaged relocations. Many jurisdictions around the world
have no explicit legal mechanisms for relocating species
across jurisdictional borders, a regulatory gap that is likely
to become more problematic under rapid climate change(Schwartz et al., 2012). Law and policy should incorporate
collaborative mechanisms for cross-tenure, local, regional
and international species relocations, and should facilitate
species relocation to support broader ecological processes,
not just to preserve charismatic threatened species.

V. SOCIAL AND ECONOMIC IMPACTS OF
SPECIES REDISTRIBUTION
Changing distributions of economically and socially
important species under climate change are affecting awide range of peoples and communities. Understanding
the ecology of species on the move and the development ofconservation tools for species redistribution responses will,
together, contribute to an integrated approach to managing
social impacts (Table 1). Consequences will likely include
exacerbated food security issues; challenges for Indigenous
and local livelihoods, governance and cultures; and humanhealth problems. Facing these challenges will require aninterdisciplinary, participatory approach (O’Brien, Marzano& White, 2013) that will include not only scientists
and professionals from different fields but also managers,
governments and communities.
(1) Food security
Since the spike in food prices in 2008, much thought hasgone into how to feed nine billion people by 2050 (World
Bank, 2008; Evans, 2009; Royal Society of London, 2009).
A key to producing 70–100% more food by 2050 will befilling the yield gap for agriculture (Godfray et al., 2010),
i.e. the difference between potential and actual yields. For
fisheries and aquaculture, the challenge is to provide an
additional 75 Mt of fish by 2050 to supply 20% of the dietary
protein needed by the human population (Rice & Garcia,2011). Given that yields from capture fisheries have alreadyplateaued, most of the additional fish will need to come fromaquaculture (FAO, 2014).
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Timothy C. Bonebrake and others
The challenges of enhancing agricultural and fisheries
productivity to meet global food demand (Godfray et al.,2010; FAO, 2014) are exacerbated by species redistribution.
Increased agricultural productivity will depend in part on
keeping weeds, diseases and pests in check where they
increase in abundance and disperse to new areas. As fish
species migrate in search of optimal thermal conditions, thelocations of productive fisheries will change (Cheung et al.,2010), resulting in gains for some communities and losses
for others (Bell et al., 2013). Changes in the distributions
and relative abundances of harmful marine algae, pathogens
and pests, will also create new hurdles for fisheries andaquaculture (Bell et al., 2016).
A key short-term priority for food-security research is thedevelopment of new global models of fishery productionthat account for climate change. Several models are now
being used to inform large-scale policy on global change inmarine fishery production (e.g. Cheung et al., 2010; Barange
et al., 2014). However, a single approach (Cheung et al., 2010)
has been dominant in representing species redistributions.
While this model has been repeatedly updated (Cheung& Reygondeau, 2016; Cheung et al., 2016), considerable
structural uncertainty remains in our ability to predictchange in fishery production, as production depends criticallyon uncertain future fishery-management arrangements(Brander, 2015). The extent to which structural uncertainty
afflicts global production estimates needs to be evaluatedwith alternative modelling approaches. These issues are
beginning to be addressed by model ensemble initiatives
such as through the Inter-sectoral Model Intercomparison
Project (https://www.isimip.org/) and through the inclusionof more detailed bio-economic processes (Galbraith, Carozza& Bianchi, 2017).
(2) Indigenous livelihoods, governance and cultures
The distributions and relative abundances of species within
their historic ranges have been central to the knowledge
of Indigenous peoples, including not only sedentarycommunities, but also mobile communities such as nomads,
pastoralists, shifting agriculturalists and hunter-gatherers(Kawagley, 2006; Sheridan & Longboat, 2006; Arctic
Council, 2013; Mustonen & Lehtinen, 2013). Maintaining
relatively intact ecosystems is crucial to the preservationof livelihoods, cosmologies, cultures and languages of thesegroups, and many have developed governance systems fortheir biological resources based on holistic observations andchecks-and-balances to prevent overharvesting (Huntington,
2011; Mustonen, 2015; Mustonen & Mustonen, 2016).
Alterations in species ranges and relative abundances due toclimate change will have profound consequences for thesegovernance systems.
Leaders of these societies also recognise that changes inrelative abundances of species are caused by other drivers,
such as extraction of natural resources and development of
infrastructure (Arctic Council, 2013), and have called fora paradigm shift in governance to address the profoundchanges underway (Kawagley, 2006; Huntington, 2011).

Research directions in species redistribution
This paradigm shift requires partnership approaches with
non-Indigenous institutions to respond to the scale andsignificance of impacts on livelihoods (Huntington, 2011).
Culturally safe and respectful language spoken by scientists,
and teaching of science for Indigenous, traditional andmobile peoples are an essential part of this approach.
Otherwise, opportunities to effectively integrate the often
deep and diverse knowledge of these people into strategies tocope with change will be lost (Lee et al., 2016).
(3) Human health
The risk of increases in infectious diseases due to species
redistributions, potentially exacerbated by food insecurity
crises, is also a significant concern (Altizer et al., 2013) anda key research challenge. History is full of examples ofclimate-driven species movements and human distribution
shifts, resulting in infectious disease outbreaks (McMichael,2012). For example, bubonic plague outbreaks caused by
the bacterium Yersinia pestis during the Black Death – thegreat pandemic originating in Asia and spreading throughout
Europe between 1347 and 1353 – have been shown to occur
roughly 15 years after a warmer and wetter period (Schmid
et al., 2015). Even the contemporary dynamics of bubonic
plague, which still occurs in Central Asia, have been clearly
linked to climate change (Stenseth et al., 2006).
In the Arctic, many interconnected factors such as climate,
wildlife populations, and health have triggered infectious
disease outbreaks. Although the health of Indigenous peoplesof the circumpolar region has improved over the last 50 years,
certain zoonotic and parasitic infections remain higher
in Arctic Indigenous populations compared to respective
national population rates (Parkinson & Evengård, 2009).
Evidence for associations between climate and infectious
disease in the Arctic is clear, but the relationship between
climate change and vector-borne disease rates is poorly
explored, owing to the small number of studies on the subject(Hedlund, Blomstedt & Schumann, 2014). However, the caseof increasing incidence of tick-borne encephalitis in Sweden
since the 1980s is instructive: mild winters have increasedtick population densities in the country, leading to increased
disease incidence (Lindgren & Gustafson, 2001). A key
component of prevention and control of climate-mediatedinfectious diseases is surveillance.
(4) Need for monitoring
More modelling is needed to understand the cascading effects
of climatic changes on the species that we rely on for foodand livelihoods and those whose spread can adversely affecthuman health. Such modelling will help identify practicaladaptations and the policies needed to support them.
Collection of the information needed to validate thesemodels can be enhanced by community-based monitoring
and citizen science, engaging the agriculture, fishing
and aquaculture industries and Indigenous and local
communities (Mayer, 2010; Johnson et al., 2015; Robinson
et al., 2015). These groups are well placed to monitor

13changes in the relative abundance and distribution of
species that they rely on or regularly interact with. For
many Indigenous and local communities, monitoring iscentral to the preservation of their sea- and land-use
patterns and sustainable development (Sheridan & Longboat,
2006; Mustonen, 2015). Moreover, rapidly developing tools
and networks in citizen science may enhance large-scalemonitoring (Chandler et al., 2016). For example, citizen
science has already contributed approximately half of what
we know about migratory birds and climate change (Cooper,
Shirk & Zuckerberg, 2014). Broad stakeholder engagement
has the added benefit of increasing awareness of the effects
of climate change on human well-being, while empoweringcommunities to effect changes in environmental behaviour
and policies.
Involving local stakeholders in monitoring also enhancesmanagement responses at the local spatial scale, and increases
the speed of decision-making to tackle environmental
challenges at operational levels of resource management(Danielsen et al., 2010). The promptness of decision-making
in community-based monitoring and the focus of
the decisions at the operational level of species andresource management make community-based monitoring
approaches particularly suitable when species are rapidly
shifting ranges. Community-based monitoring is also likely toprovide information about crucial new interactions between
species (Alexander et al., 2011; Huntington, 2011). One
potential challenge to community-based monitoring is that,in situations in which constraints or demands on resources
may condition quotas or financial payments to communities,
the local stakeholders might have an incentive to report false
positive trends in those natural resources so they can continue
to harvest the resources or continue to be paid, even though
the resources may actually be declining (Danielsen et al.,2014). Systems ensuring triangulation and periodic reviewof the community-based monitoring results will therefore
be required, whether the monitoring is implemented bycommunities, governments or the private sector.
Increased monitoring may also increase understandingof the spatial and temporal impacts on human societies
posed by changes in the distribution and abundance ofspecies. The effects of climate change on species needs tobe mainstreamed into routine food-production assessments
so that society is prepared and can adapt to predictedchanges. Technological improvements have increased thepotential for citizen scientists to engage in the necessary
monitoring (Brammer et al., 2016) and for industries tocapture essential data as part of routine field operations(Ewing & Frusher, 2015). On a broader scale, co-ordinationof monitoring to obtain data that can be compared acrossdiverse regions is needed. Identification of hotspots, whererange changes and impacts are expected to be seen earlier(Hobday & Pecl, 2014; Pecl et al., 2014), can aid in the early
development of broad-based practical adaptive strategies.
Moreover, technological advances are making it possible to
not just monitor the location of organisms, but understandthe physiological and behavioural processes underlying their
Biological Reviews (2017) 000–000 © 2017 Cambridge Philosophical Society

14
movement patterns (Block et al., 2001; Clark et al., 2008,2010). An integrated understanding of the drivers of species
movement will greatly strengthen our capacity to plan for
species redistributions in the future.

VI. INTERDISCIPLINARY APPROACHES TOADDRESS SPECIES REDISTRIBUTION
CHALLENGES
Species redistribution is a complex phenomenon dependent
upon multiple and interacting multiscale climatic variation,
as well as social and ecological/evolutionary processes(Fig. 3). The formation of novel species assemblages asa consequence of this redistribution brings significant new
challenges for governments, resource users and communities,
particularly when dependence on natural resources is highor where present or future species ranges cross jurisdictionalboundaries (Pecl et al., 2011). Identifying the mechanisms andprocesses driving species redistributions is critically importantfor improving our capacity to predict future biologicalchange, managing proactively for changes in resource-based
human livelihoods and addressing conservation objectives(Pinsky & Fogarty, 2012).
In recent years, the scientific study of climate-driven
species redistribution has matured significantly (Fig. 1).
Although research continues to focus on modellingand prediction of distribution shifts, researchers haveincreasingly incorporated management and socio-economic
considerations explicitly (Fig. 2). As this review has
highlighted, biological studies and management and social
science research on species redistribution have provided a
wealth of insights into global change, and have supported
several innovative management responses (i.e. managed
relocation, real-time management systems). Nevertheless,many challenges and key questions require answers (Table 1).
Further integrated development will require working acrossdisciplines to find innovative solutions (Bjurström & Polk,
2011).
Long-term interdisciplinary research programs that
integrate the natural and social sciences are needed to study,
understand and model the impact of climate-driven species
redistribution on ecosystem functioning. More specifically,
interdisciplinary research is needed on changes to multiple
ecosystem services (e.g. food) and disservices (e.g. diseases)delivered to society, as climate changes, particularly asinterdisciplinary approaches are not well represented inclimate research (Bjurström & Polk, 2011). Simultaneous
socio-ecological time series often reveal that people respondto ecosystem change in surprising ways. For example, aclimate regime shift around 1960–1990 drove declines
of a cod fishery, but opened up opportunities for a
new shrimp fishery off Greenland (Hamilton et al., 2003).
However, only communities with sufficient capital to invest
in new fishing gear, and entrepreneurial individuals who
were willing to invest in a new fishery were able toadapt to the ecosystem change. Thus, societal responses
Biological Reviews (2017) 000–000 © 2017 Cambridge Philosophical Society

Timothy C. Bonebrake and others
to species redistributions can be highly dependent on a
few individuals, and human responses and natural changes
must be considered in combination (Pinsky & Fogarty,2012).
Many challenges must be overcome to execute a successful
long-term interdisciplinary research program. Even withinfields such as ecology, disciplinary barriers threaten to limit
advances in species redistribution research. For example,
communication and collaboration between marine andterrestrial researchers (Webb, 2012) has the potential tospark key developments. Unfortunately, research proposals
with the highest degree of interdisciplinarity currently
have the lowest probability of being funded (Bromham,
Dinnage & Hua, 2016). Although long-term monitoring
programs provide the essential foundation for tracking
and understanding the causes and consequences of species
redistributions, they also encounter funding difficulties dueto the long time span of funding required and a bias in grantagencies away from studies perceived as simply observational
research and towards hypothesis-driven research (Lovett
et al., 2007). Institutional change in funding agencies andan emphasis on prioritising interdisciplinary and long-term
projects could lead to important, high-impact climate change
research (Green et al., 2017). In the meantime, global change
scientists also need to explore multiple options to support
long-term and interdisciplinary studies, such as harnessing
citizen science and engaging in large-scale collaborative
efforts.
In fact, citizen science may help to fill the knowledge gap
in long-term and spatially extensive studies (Breed, Stichter& Crone, 2013). Citizen science approaches typically involve
recruiting observers to be part of a formal program, amethod for recording meaningful data, and a means ofmaking those data accessible and discoverable for later use.
In addition, successful programs often include data-vetting
and data-management practices to ensure the integrity andlong-term availability of data, providing data products tocontributors and other interested parties, and interpreting
the results of these efforts to tell a story of environmental
functioning or change to larger audiences. Further work isneeded, however, to find suitable ways to connect citizen
science and community-based monitoring programs withinternational biodiversity data repositories (Chandler et al.,2016).
Growing recognition of the important role of Indigenous,
traditional and mobile peoples in protected area
management is one positive change in recent years. The
creation of a fourth type of governance (in addition
to government, shared and private governance) in the
IUCN’s Protected Area Guidelines specifically addresses
IPAs and Indigenous peoples’ and Community-Conserved
territories and Areas (ICCAs). In this case, the nature–culturebinary is being dismantled to incorporate a rangeof worldviews that promote sustainable development,
governance vitality and management devolution (delegationof power) (Borrini-Feyerabend et al., 2013; Lee, 2016).
Acknowledging the legitimacy of traditional knowledge

Research directions in species redistribution

15

Fig. 3. Ophiocordyceps sinensis, a caterpillar-feeding fungus of the Tibetan plateau, presents a useful case study for the importance ofan integrated and interdisciplinary approach to species redistribution. The species is widely consumed throughout China, largely
for medicinal purposes. Distribution shifts of the species in recent decades have been observed, but models under future climateshave yielded divergent outcomes (both range expansion and reduction) based on different sets of data and approaches (Shrestha& Bawa (2014); Yan et al., 2017). Open questions remain about the physiology of the species and, particularly critical in this case,
how interactions with the host caterpillar species might change under warming. O. sinensis is a critical part of the Tibetan economy(Winkler, 2008) but is also vulnerable to extinction given intensive collecting pressure and possible climate change impacts (Yanet al., 2017). Greater understanding of the ecology of the species will assist in addressing economic and conservation challenges. But,
equally importantly, the Indigenous populations that depend upon O. sinensis for income can also provide invaluable insights into
complex ecological systems and how climate change might be changing these systems (Klein et al., 2014).

systems can be instrumental in understanding species
redistribution and provides a mechanism by which local
communities can monitor and manage impacts (Eicken et al.,2014; Tengö et al., 2017).
Examples of on-ground management responses to shifting
species are few, to date, and those that have been reported
are based on seasonal or short-term responses to changes
in species distribution (Hobday et al., 2011, 2014; McColl
et al., 2016). These few examples do illustrate how long-termchange might be accommodated, but such approaches may
not support management responses for the transformational
level of change that may be needed in some regions. In thesecases, development of long-term adaptive pathways (sensu
Wise et al., 2014) for species on the move is required. Thesepathways can include decision points at which switchingof strategies is required, for example defining at what
point a habitat-creation strategy should be changed to atranslocation strategy.

VII. CONCLUSIONS(1) Until recently, species redistribution was seen as
something that would happen in the future rather than an
immediate issue. However, it is happening now, with serious
ecological and societal implications and impacts alreadybeing observed.
(2) The cross-cutting nature of species redistribution
calls for the integration of multiple scientific disciplines,
from climate science to ecology, palaeoecology, physiology,
macroecology, and more. We further suggest that researchon contemporary species redistribution needs to span
process-based studies, observational networks by bothscientists and community members, historical data synthesis
and modelling over a variety of scales.
(3) Species redistribution defies conservation paradigms
that focus on restoring systems to a baseline and challenges
environmental management strategies, which are often static
Biological Reviews (2017) 000–000 © 2017 Cambridge Philosophical Society

16
and based on human-dictated boundaries drawn in thepast. Climate-driven species redistribution therefore presents
both fundamental philosophical questions and urgent issues
relevant to conservation and society.
(4) For species redistribution research to support
development of relevant adaptive strategies and policy
decisions adequately, studies need to take an interdisciplinary
approach and must recognise and value stakeholders.
Involving stakeholders in monitoring and collection of dataoffers an opportunity to help guide effective adaptation
actions across sectors.

VIII. ACKNOWLEDGEMENTS
We thank the many Species on the Move 2016conference participants who contributed to the intellectuallyengaging discussions, and particularly the key questionsin the field, that ultimately led to this paper. The
workshop and conference leading to this paper were
supported by the University of Tasmania, IMAS: ‘‘Institutefor Marine and Antarctic Studies’’, NOAA FisheriesService, CSIRO, National Climate Change Adaptation
Research Facility Natural Ecosystems Network, the Ian
Potter Foundation, the Antarctic Climate and Ecosystems
Cooperative Research Centre, and the ARC Centre of
Excellence for Environmental Decisions. An anonymous
reviewer, Jessica Blois and Tim Benton also provided helpfulcomments on the manuscript. T. C. B. was supported
by RGC-GRF (HKU778512). C. J. B. (DE160101207),
G. T. P. (FT140100596), E. W. (FT110100597) and
T. W. (FT110100174) were supported by the Australian
Research Council through DECRA and Future Fellowships,
respectively. R. K. C. was supported by the Universityof Connecticut (USA) and the Center for Macroecology,
Evolution, and Climate (University of Copenhagen, DK). B.
E. was supported by Nordforsk. R. A. G. was supportedby the South African National Research Foundation(KIC 98457 and Blue Skies 449888). M. A. J. was
supported by Yale Climate and Energy Institute. T. M.’s
participation has been made possible by the (WAPEAT)(Finnish Academy 263465) Project. J. M. S. and A. V.
were supported by ARC DP’s (150101491 and 170100023,
respectively).

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X. SUPPORTING INFORMATION
Additional supporting information may be found in the
online version of this article.
Appendix S1. Details of extraction and analysis of researchfoci in the field of species redistribution.
Table S1. List of 109 ‘trending’ terms defined as wordstems that significantly increased in annual frequency of
appearance in publications on species redistribution since
1995.
Table S2. List of 49 ‘high-impact’ terms defined as wordstems associated with higher than average citation rates,
accounting for publication year.