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On a cold and bitter winter night, in a field of boulders beneath a thick layer of snow, a mountain pygmy possum sleeps safe and snug. Strange though it may seem, it is the snow that’s keeping the possum warm; fluffed up by countless pockets of air, the uncompacted snow insulates the ground and prevents the warmth from escaping into the night. Under this white blanket, the mountain pygmy possum can hibernate the winter away.

The pygmy possum might be snug, but those of us concerned for its future can’t afford to be complacent. This is just one example of an Australian species that stands to lose its habitat in the face of climate change. The biodiversity that underpins Australia’s unique ecosystems is under threat from increasing land and ocean temperatures and changing weather patterns.

Climate change

The world is heating up. The increasing concentrations of greenhouse gases, such as CO2, in the Earth’s atmosphere are causing the planet’s climate system to retain more energy. The average temperature of the Earth's surface increased by an estimated 0.7°C since the beginning of the 20th century and, according to the most recent projections of the Intergovernmental Panel on Climate Change, could rise by 1.6–4.3°C compared to a 1850–1900 baseline by 2100.


Note that the figures above use a compilation of both instrumental and proxy data.

The effects of increased CO2 in the atmosphere and changing climatic conditions are expected to include:

  • more frequent extreme high maximum temperatures and less frequent extreme low minimum temperatures, and warmer winter conditions
  • decreased snow cover: satellite observations suggest that the area of the planet covered by snow has already declined by 10 per cent since the 1960s
  • increased climate variability, with changes in both the frequency and severity of extreme weather events
  • altered distributions of certain infectious diseases
  • increased sea levels
  • increased ocean acidification

In Australia the climate is expected to become significantly warmer. CSIRO scientists predict that by 2030 average temperatures will rise above 1990 levels by around 0.7–0.9°C in coastal areas, and around 1–1.2°C in inland regions. On a continent already as warm as Australia, such an increase could have major ecological impacts. The number of extreme rainfall events—such as those leading to flooding—is also expected to increase, even though overall, most of the country is expected to become drier in the 21st century.

Shifts in climatic envelopes

To estimate the effect of climate change on species, scientists use what they call a climatic envelope (sometimes also referred to as a bioclimatic envelope), which is the range of temperatures, rainfall and other climate-related parameters in which a species currently exists.

As the climate warms, the geographic location of climatic envelopes will shift significantly, possibly even to the extent that species can no longer survive in their current locations. Such species will need to follow their climatic envelopes by migrating to cooler and moister environments, usually uphill or southwards in the southern hemisphere. Marine species will also need to adapt to warmer ocean temperatures. There are several well documented cases of climate-induced shifts in the distribution of plants and animals in the northern hemisphere, but less information is available for southern hemisphere species.

In many cases, however, such migration might not be possible because of unfavourable environmental parameters, geographical or human-made barriers and competition from species already in an area. The mountain pygmy possum is particularly vulnerable to a loss of habitat linked to climate change.

While there is evidence that suggests the distribution of some animals like flying foxes and birds are responding to warmer temperatures in Australia, it is often difficult to separate the effects of climate from other influences upon habitats.

As human activities, particularly agriculture but also settlement and industrial development, have expanded over the last few centuries, natural vegetation—such as forests, grasslands and heathlands—has been cleared in large swathes. Once-extensive plant communities have been reduced in size and broken into smaller patches. This habitat reduction and fragmentation poses a problem because it limits the ability of many species to migrate to areas with favourable conditions. Species on mountain-tops, islands and peninsulas will have a similar problem.

In general, those species with restricted climatic envelopes, small populations and limited ability to migrate are most likely to suffer in the face of rapid climate change. An estimated 25 per cent of Australian eucalypts, for example, have distributions spanning areas where average annual temperature varies less than 1°C. Even a relatively small increase in average temperature will shift the climatic envelopes of such species outside their current distribution. Modelling suggests that by 2070, the majority of species in our protected nature reserves and national parks will encounter novel climatic conditions that they have not experienced in their historical past.

Threats to biodiversity

Temperature spikes

A number of species will be affected physiologically by climate change. There is evidence that some species are physiologically vulnerable to temperature spikes. For example, the green ringtail possum, an endemic species of Queensland’s tropical rainforests, cannot control its body temperature when the ambient temperature rises above 30°C. An extended heatwave in north Queensland could kill off a large part of its population.

Coral bleaching

Warmer sea surface temperatures are blamed for an increase in a phenomenon called coral bleaching. This is a whitening of coral caused when the coral expels their zooxanthellae, a symbiotic photosynthesising algae that lives within the coral tissues and provides it with essential nutrients. The zooxanthellae also give corals their spectacular range of colours. Zooxanthellae are expelled when the coral is under stress from environmental factors such as abnormally high water temperatures and/or pollution. Since the zooxanthellae help coral in nutrient production, their loss can affect coral growth and make coral more vulnerable to disease. Major bleaching events took place on the Great Barrier Reef in 1998, 2002 and 2006, causing a significant die-off of corals in some locations. Ocean acidification poses yet another challenge for corals because it makes it harder for corals to build their skeletons.

Increases in extreme events

Predicted changes in the intensity, frequency and extent of disturbances such as fire, cyclone, drought and flood will place existing vegetation under stress and favour species able to rapidly colonise denuded areas. In many cases this will mean the spread of alien ‘weed’ species and major changes in the distribution and abundance of many indigenous species. Heatwaves may affect the biodiversity of marine ecosystems, as seen in the summer of 2010–11 in south western West Australia. Extended periods of warmer sea temperatures resulted in the shut-down of the abalone industry, and the migration of whale sharks and manta rays further south and east than usual.

Changes in rainfall

Australia is a dry continent. Its plants and animals are mostly well adapted to drought and have developed a wide range of strategies for coping with the country’s climatic extremes. The marginal nature of the environment, however, means that even minor changes in rainfall patterns could have major impacts on wildlife. The Murray-Darling Basin (Australia’s largest water catchment) and southwest Western Australia are already threatened by salinity and other environmental problems. Predicted decreased rainfall and consequent lower river flows in both regions would have a major impact on aquatic biota. Freshwater wetlands such as the Macquarie Marshes in the central west of New South Wales—and the frogs, waterbirds, turtles and other aquatic life dependent on them—are also at risk because of a change in water quality and quantity.

Increased CO2 and plant growth

The basic ingredients for photosynthesis include carbon dioxide and water. Increased carbon dioxide in the atmosphere causes increased growth rates in many plant species. This is good news for farmers, but only if this carbon dioxide ‘fertilisation’ effect is matched by adequate soil moisture and other nutrients. Leaf-eating animals like koalas may not be so lucky: increased concentrations of carbon dioxide could diminish the nutritional value of foliage.

A lot of CO2 that has been emitted into the atmosphere has been absorbed by the oceans. This has resulted in a decrease in the ocean’s pH, which in turn affects the rate at which many marine organisms build skeletons, meaning that reefs damaged by bleaching or other agents would recover more slowly.

Sea-level rise

According to the most recent IPCC report, sea level is predicted to rise by 26–98 centimetres by 2100, due to the thermal expansion of the oceans and the melting of polar ice-caps and ice sheets. Coupled with the effects of storm surges, which are expected to be of a greater magnitude in a warmer world, this increase in sea level could threaten many coastal ecosystems. Also at risk are mangrove forests and low-lying freshwater wetlands in Kakadu National Park.

What would rapid species extinction mean for Australia?

Climate change is predicted to take place faster in the next century than at any time for at least the last 10,000 years. Coupled with other factors, such as continued land-clearing, this could mean the extinction of species at a rate even greater than when the dinosaurs disappeared around 65 million years ago. Some species not under immediate threat of extinction might nonetheless suffer decreases in population size, diminishing intra-species’ genetic diversity (and therefore face increased vulnerability).

Does it really matter if many species go extinct? The world would certainly be a less interesting place with less biodiversity, but would it affect us?

A diversity of species increases the ability of ecosystems to do things like hold soils together, maintain soil fertility, deliver clean water to streams and rivers, cycle nutrients, pollinate plants (including crops), and buffer against pests and diseases—these are sometimes called ‘ecosystem functions’ or ‘ecosystem services’. A loss of species could reduce this ability, particularly if environmental conditions are changing rapidly at the same time. It is possible that as the climate changes and as species are eliminated from an area we will see a change in some ecosystem functions; this could mean more land degradation, changes in agricultural productivity and a reduction in the quality of water delivered to human populations.

Source: CSIRO on YouTube. View video details and transcript.

Adapting to change

The Earth will continue to warm for some time even if greenhouse gas emissions are somehow instantly curbed. Some species, primarily microorganisms and invertebrates with short generation times, might be able to adapt to changing conditions or evolve in response to climate change. But for many, especially those that are already rare and inhabit limited climatic envelopes, global warming could pose an insurmountable challenge.

  • How some species have already responsed to climate change

    Adaptation strategies will not be limited to the efforts of human societies; some species may already be adapting—and evolving—in response to climate change. Climate change has probably always played a role in evolution, although scientists debate the nature of that role. At least some of the data are inconclusive: for example, studies of beetles during the Quaternary Period (the past 2 million years or so) show that beetles survived climate change in the past mainly by dispersing to new environments—that is, by following their climatic envelopes.

    Evolutionary responses

    Australian scientists have detected what they think is an evolutionary response to rapid climate change amongst the fruitfly Drosophila—a species that often used in genetic experiments. This insect carries a gene called Adh; a variation of this gene, called Adhs, is thought to help the insect survive arid conditions. Usually Adhs is more common in northern Australia, which is hotter and drier, but scientists have discovered that the distribution of the gene has moved 400 km to the south—presumably in response to rising temperatures and decreasing rainfall.

    Behavioural responses

    Scientists who study the relationship between the seasons and biological phenomena have looked at long-term records of the indicators of change from one season to another, such as temperature, rainfall and the number of hours of sunlight. They found that climate change has changed the timing of the seasons—spring arrives earlier and autumn lasts longer—and that wildlife is adapting to the change by altering its behaviour. A number of plants are consistently forming buds and flowering earlier in spring, and the migration and breeding times of birds has also changed.

In Australia, action plans have been prepared for a number of endangered species that try to address the possible impacts of global warming. For example, the recovery plan for the mountain pygmy possum prepared by the NSW National Parks and Wildlife Service includes the development of a model to illustrate habitat suitability under current snow conditions and to identify key refugia for the possum under the predicted impacts of climate change. The action plan prepared by the government of the Australian Capital Territory for the northern corroboree frog includes a commitment to a coordinated research program on the actual and potential effects of global warming on the species.

At the national level, climate change has also become central to Australia’s Biodiversity Conservation Strategy 2010–2030. This new plan is focussed on removing threats and building resilience in Australia’s ecosystems to help them adapt to climate change and other threats. The plan attempts to engage all Australians in biodiversity and proposes concrete and measurable steps in developing resilience in a cost effective way. Unfortunately, the threats associated with climate change continue to increase with the failure of governments worldwide to reach a consensus around decreasing emissions of CO2 and other greenhouse gases to levels that limit impacts upon biodiversity.

Some of the impacts of climate change may be sudden, but in many cases societies will have some years to adapt their management of biodiversity as conditions change. Increasing our understanding of the effects of climate change on biodiversity, and developing practical ways of mitigating such effects, are critical to limit the damage. Even so, the dangers are great—for humans as well as our native plants and animals. Not only mountain pygmy possums stand to lose their security blanket.

opener

The corroboree frog lives in a small area of New South Wales and Victoria. Further research is planned to assess how global warming may impact on this threatened species. Image credit: Australian Alps on Flickr.

Hot topics in biodiversity and climate change research

Barry W. Brooka,1 and Damien A. Fordham2

1School of Biological Sciences, Private Bag 55, University of Tasmania, Hobart, 7001, Australia

2The Environment Institute and School of Earth and Environmental Sciences, University of Adelaide, Adelaide, SA, 5005, Australia

aEmail: ua.ude.satu@koorb.yrrab

Competing interests: The authors declare that they have no disclosures or conflicts of interest.

Author information ►Article notes ►Copyright and License information ►

Accepted 2015 Sep 28.

Copyright : © 2015 Brook BW and Fordham DA

This is an open access article distributed under the terms of the Creative Commons Attribution Licence, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

With scientific and societal interest in biodiversity impacts of climate change growing enormously over the last decade, we analysed directions and biases in the recent most highly cited data papers in this field of research (from 2012 to 2014). The majority of this work relied on leveraging large databases of already collected historical information (but not paleo- or genetic data), and coupled these to new methodologies for making forward projections of shifts in species’ geographical ranges, with a focus on temperate and montane plants. A consistent finding was that the pace of climate-driven habitat change, along with increased frequency of extreme events, is outpacing the capacity of species or ecological communities to respond and adapt.

Keywords: biodiversity, climate change, global change, conservation

Introduction

It is now halfway through the second decade of the 21 st century, and climate change impact has emerged as a “hot topic” in biodiversity research. In the early decades of the discipline of conservation biology (1970s and 1980s), effort was focused on studying and mitigating the four principal drivers of extinction risk since the turn of the 16 th century, colourfully framed by Diamond 1 as the “evil quartet”: habitat destruction, overhunting (or overexploitation of resources), introduced species, and chains of extinctions (including trophic cascades and co-extinctions). Recent work has also emphasised the importance of synergies among drivers of endangerment 2. But the momentum to understand how other aspects of global change (such as a disrupted climate system and pollution) add to, and reinforce, these threats has built since the Intergovernmental Panel on Climate Change reports 3 of 2001 and 2007 and the Millennium Ecosystem Assessment 4 in 2005.

Scientific studies on the effects of climate change on biodiversity have proliferated in recent decades. A Web of Science ( webofscience.com) query on the term “biodiversity AND (climate change)”, covering the 14 complete years of the 21 st century, shows the peer-reviewed literature matching this search term has grown from just 87 papers in 2001 to 1,377 in 2014. Figure 1 illustrates that recent scientific interest in climate change-related aspects of biodiversity research has outpaced—in relative terms—the baseline trend of interest in other areas of biodiversity research (i.e., matching the query “biodiversity NOT (climate change)”), with climate-related research rising from 5.5% of biodiversity papers in 2001 to 16.8% in 2014.

Figure 1.

Relative growth of refereed studies on climate change and biodiversity, compared to non-climate-related biodiversity research.

Interest in this field of research seems to have been driven by a number of concerns. First, there is an increasing societal and scientific consensus on the need to measure, predict (and, ultimately, mitigate) the impact of anthropogenic climate change 5, linked to the rise of industrial fossil-fuel combustion and land-use change 6. Biodiversity loss and ecosystem transformations, in particular, have been highlighted as possibly being amongst the most sensitive of Earth’s systems to global change 7, 8. Second, there is increasing attention given to quantifying the reinforcing (or occasionally stabilising) feedbacks between climate change and other impacts of human development, such as agricultural activities and land clearing, invasive species, exploitation of natural resources, and biotic interactions 2, 9. Third, there has been a trend towards increased accessibility of climate change data and predictions at finer spatio-temporal resolutions, making it more feasible to do biodiversity climate research 10, 11.

What are the major directions being taken by the field of climate change and biodiversity research in recent years? Are there particular focal topics, or methods, that have drawn most attention? Here we summarise major trends in the recent highly cited literature of this field.

Filtering and categorising the publications

To select papers, we used the Web of Science indexing service maintained by Thomson Reuters, using the term “biodiversity AND (climate change)” to search within article titles, abstracts, and keywords. This revealed 3,691 matching papers spanning the 3-year period 2012 to 2014. Of these, 116 were categorised by Essential Science Indicators ( esi.incites.thomsonreuters.com) as being “Highly Cited Papers” (definition: “As of November/December 2014, this highly cited paper received enough citations to place it in the top 1% of [its] academic field based on a highly cited threshold for the field and publication year”), with five also being classed as “Hot Papers” (definition: “Published in the past two years and received enough citations in November/December 2014 to place it in the top 0.1% of papers in [its] academic field”). The two academic fields most commonly associated with these selected papers were “Plant & Animal Science” and “Environment/Ecology”.

Next we ranked each highly cited paper by year, according to its total accumulated citations through to April 1 2015, and then selected the top ten papers from each year (2012, 2013 and 2014) for detailed assessment. We wished to focus on data-oriented research papers, so only those labelled “Article” (Document Type) were considered, with “Review”, “Editorial”, or other non-research papers being excluded from our final list. Systematic reviews that included a formal meta-analysis were, however, included. We then further vetted each potential paper based on a detailed examination of its content, and rejected those articles for which the topics of biodiversity or climate change constituted only a minor component, or where these were only mentioned in passing (despite appearing in the abstract or key words).

The final list of 30 qualifying highly cited papers is shown in Table 1, ordered by year and first author. The full bibliographic details are given, along with a short description of the key message of the research (a subjective summary, based on our interpretation of the paper). Each paper was categorised by methodological type, the aspect of climate change that was the principal focus, the spatial and biodiversity scale of the study units, the realm, biome and taxa under study, the main ecological focus, and the research type and application (the first row of Table 1 lists possible choices that might be allocated within a given categorisation). Note that our choice of categories for the selected papers was unavoidably idiosyncratic, in this case being dictated largely by the most common topics that appeared in the reviewed papers. Other emphases, such as non-temperature-related drivers of global change, evolutionary responses, and so on, might have been more suitable for other bodies of literature. We also did not attempt to undertake any rigorous quantification of effect sizes in reported responses of biodiversity to climate change; such an approach would have required a systematic review and meta-analysis, which was beyond the scope of this overview of highly cited papers.

Table 1.

Summary information on the 30 most highly cited papers related to climate change effects on biodiversity, for the period 2012–2014.

Summary of the ten most highly cited research papers based on the search term: “biodiversity AND (climate change)”, for each of 2012 9, 13, 14, 23, 26, 32, 34, 36, 40, 45, 2013 15– 17, 21, 27, 30, 31, 33, 37, 39 and 2014 18– 20, 22, 24, 25, 28, 29, 35, 38, as determined in the ISI Web of Science database. Filters: Reviews, commentaries, and opinion pieces were excluded, as were papers for which climate change was not among the focal topics of the research. The first row of the Table is a key that shows the possible categorisations that were open to selection (more than one description might be selected for a given paper); n is the number of times a category term was allocated.

AuthorsYearTitleJournal/Vol/PgDOIMain MessageTypenClimate ChangenSpatial
Scale
nBiodiversity
Scale
nRealmnBiomenTaxonnUsenEcological
Focus
N
Author 1
Author 2
Author 3
…then et al.
2012
2013
2014
Article titlePublication details
Journal, volume
Page range
Digital Object IdentifierKey findings of
the paper
Methods
development
Meta-analysis
New model
Experiment
New field data
Database
Statistical

9
3
5
5
6
14
8
Observed
Retrospective
validation
Reconstruction
Future forecast
Experimental
9

2
1
19
2
Local
Regional
Global
Multiscale
7
14
7
2
Population
Species
Community
Ecosystem
7
14
8
6
Terrestrial
Marine
Other
24
8
1
Montane
Polar
Boreal
Temperate
Subtropical
Tropical
Desert
Island
Riverine
Lacustrine
Pelagic
Benthic
Abyssal
Global
Any
9
3
4
11
6
4
2
0
1
0
3
5
1
4
2
Plant
Invertebrate
Amphibian
Reptile
Fish
Bird
Mammal
All
16
4
4
4
4
2
3
5
Theoretical-
Fundamental
Applied-
Management
Strategic-
Policy

13

17

7
Trait
Population
dynamics
Biogeography
Physiology
Behaviour
Distribution
Genetic
Migration-
dispersal
Networks
Threatened
species
Community
dynamics
Biotic
interactions
Global change
5

7
3
10
1
16
0

8
1

3

4

2
3
Dullinger, S.,
Gattringer, A.,
Thuiller, W.,
et al.
2012Extinction
debt of high-
mountain
plants under
twenty-first-
century
climate
change
Nature Climate Change/
2/619–622
10.1038/nclimate1514European Alps
plants will
suffer average
21stC range
contractions
of 50% but
population
dynamics will
lag, causing
extinction debt
New model,
Database
Future forecastRegionalCommunity,
Species
TerrestrialMontanePlantStrategic-PolicyPopulation
dynamics,
Distribution
Elmendorf, S.C.,
Henry, G.H.R.,
Hollister, R.D.,
et al.
2012Global
assessment of
experimental
climate
warming
on tundra
vegetation:
heterogeneity
over space
and time
Ecology Letters/
15/164–175
10.1111/j.1461-
0248.2011.01716.x
Response of
tundra plants
to experimental
warming was
linear/
cumulative,
with no obvious
saturating
or threshold
impacts
(indicating lack
of feedbacks)
but strong
regional
heterogeneity
Meta-analysisExperimentalMultiscaleCommunity,
Ecosystem
TerrestrialPolar, BorealPlantTheoretical-
Fundamental
Population
dynamics,
Community
dynamics
Fordham, D.A.,
Akçakaya, H.R.,
Araújo, M.B.,
et al.
2012Plant
extinction risk
under climate
change:
are forecast
range shifts
alone a good
indicator
of species
vulnerability
to global
warming?
Global Change Biology/
18/1357–1371
10.1111/j.1365-
2486.2011.02614.x
It is important
to consider
direct
measures
of extinction
risk, as well
as measures
of change
in habitat
area, when
assessing
climate change
impacts on
biodiversity
Methods
development,
Database
Future forecastRegionalSpeciesTerrestrialTemperatePlantApplied-
Management
Population
dynamics,
Distribution, Trait
Gottfried, M.,
Pauli, H.,
Futschik, A.,
et al.
2012Continent-
wide
response
of mountain
vegetation
to climate
change
Nature Climate Change/
2/111–115
10.1038/nclimate1329Based on
60 mountain
peaks in
Europe plant
communities
are being
transformed
by gradual
warming, with
thermophillic
species
displacing
competitors
at a
geographically
variable pace
DatabaseObservedRegionalCommunityTerrestrialMontanePlantTheoretical-
Fundamental
Trait, Physiology,
Community
dynamics
Hickler, T.,
Vohland, K.,
Feehan, J.,
et al.
2012Projecting
the future
distribution
of European
potential
natural
vegetation
zones with a
generalised,
tree species-
based
dynamic
vegetation
model
Global Ecology and
Biogeography/
21/50–63
10.1111/j.1466-
8238.2010.00613.x
A new dynamic
vegetation
model shows
that climate
change is
likely to cause
significant
shifts in
vegetation
types in
Europe
New modelFuture forecastRegionalCommunityTerrestrialMontane,
Boreal,
Temperate
PlantTheoretical-
Fundamental,
Applied-
Management
Biogeography,
Distribution
Mantyka-
Pringle, C.S.,
Martin, T.G.,
Rhodes, J.R.
2012Interactions
between
climate and
habitat loss
effects on
biodiversity:
a systematic
review and
meta-analysis
Global Change Biology/
18/1239–1252
10.1111/j.1365-
2486.2011.02593.x
In synergy with
other threats,
maximum
temperature
was most
closely
associated
with habitat
loss, followed
by mean
precipitation
decrease
Meta-analysis,
Database
ObservedGlobalPopulation,
Community
TerrestrialGlobalAllStrategic-PolicyGlobal change,
Distribution
Schloss C.A.,
Nunez, T.A.,
Lawler, J.J.
2012Dispersal will
limit ability of
mammals to
track climate
change in
the Western
Hemisphere
Proceedings of the
National Academy of
Sciences of the United
States of America/
109/8606–8611
10.1073/
pnas.1116791109
Many
mammals in
the Western
Hemisphere
will be unable
to migrate
fast enough
to keep pace
with climate
change
Database,
Statistical
Future forecastRegional -
Western
Hemisphere
SpeciesTerrestrialMontane,
Polar, Boreal,
Temperate,
Subtropical,
Tropical, Desert
MammalApplied-
Management
Distribution,
Migration-dispersal
Sunday J.M.,
Bates, A.E.,
Dulvy, N.K.
2012Thermal
tolerance and
the global
redistribution
of animals
Nature Climate Change/
2/686–690
10.1038/nclimate1539Thermal
tolerance
determines
the ranges of
marine, but
not terrestrial,
ectotherms
Database,
Statistical
ObservedGlobalSpeciesTerrestrial,
Marine
GlobalInvertebrate,
Amphibian,
Reptile, Fish
Theoretical-
Fundamental,
Applied-
Management
Biogeography,
Physiology,
Distribution
Urban, M.C.,
Tewksbury, J.J.,
Sheldon, K.S.
2012On a collision
course:
competition
and dispersal
differences
create
no-analogue
communities
and cause
extinctions
during
climate
change
Proceedings of the
Royal Society
B-Biological Sciences/
279/2072–2080
Interspecific
competition
and dispersal
differences
between
species will
elevate future
climate-driven
extinctions
Methods
development
Future forecastLocalCommunityTerrestrialMontaneAllTheoretical-
Fundamental
Community
dynamics, Biotic
interactions,
Migration-dispersal
Zhu, K.,
Woodall, C.W.,
Clark, J.S.
2012Failure to
migrate: lack
of tree range
expansion
in response
to climate
change
Global Change Biology/
18/1042–1052
10.1111/j.1365-
2486.2011.02571.x
Tree species in
the US showed
a pattern of
climate-related
contraction
in range, or
a northwards
shift, with <5%
expanding. No
relationship
between
climate velocity
and rate of
seedling
spread
DatabaseObservedRegionalPopulationTerrestrialMontane,
Temperate,
Subtropical
PlantTheoretical-
Fundamental
Distribution,
Migration-dispersal
Anderegg, W.R.L.,
Plavcova, L.,
Anderegg, L.D.,
et al.
2013Drought’s
legacy:
multiyear
hydraulic
deterioration
underlies
widespread
aspen forest
die-off and
portends
increased
future risk
Global Change Biology/
19/1188–1196
10.1111/gcb.12100Accumulation
of drought-
induced
hydraulic
damage to
trees over
multiple
years leads
to increased
forest mortality
rates and
increased
vulnerability
to extreme
events
New field data,
Experiment
Observed,
Experimental
LocalPopulationTerrestrialTemperatePlantTheoretical-
Fundamental
Physiology,
Population
dynamics
Boetius, A.,
Albrecht, S.,
Bakker, K.,
et al.
2013Export of
algal biomass
from the
melting Arctic
sea ice
Science/339/1430–143210.1126/
science.1231346
Anomalous
melting of
summer
Arctic sea-ice
enhanced the
export of algal
biomass to
the deep-sea,
leading to
increased
sequestering
of carbon
to oceanic
sediments
New field dataObservedRegionalEcosystemMarinePolar, Pelagic,
Benthic
PlantTheoretical-
Fundamental
Global change
Foden W.B.,
Butchart, S.H.M.,
Stuart, S.N.,
et al.
2013 Identifying
the World's
Most Climate
Change
Vulnerable
Species: A
Systematic
Trait-Based
Assessment
of all Birds,
Amphibians
and Corals
PLoS ONE/8/e6542710.1371/journal.
pone.0065427
Species’ traits
associated with
heightened
sensitivity and
low adaptive
capacity to
climate change
can be used
to identify
the most
vulnerable
species and
regions
Database,
Methods
development
Future forecastGlobalSpeciesTerrestrial,
Marine
AnyAmphibian,
Invertebrate,
Bird
Applied-
Management,
Strategic-Policy
Threatened
species,
Distribution, Trait
Franklin, J.,
David, F.W.,
Ikeami, M.,
et al.
2013Modeling
plant species
distributions
under future
climates: how
fine scale
do climate
projections
need to be?
Global Change Biology/
19/473–483
10.1111/gcb.12051The spatial
resolution
of models
influences
the location
and amount
of forecast
suitable habitat
under climate
change
Methods
development,
Database,
Statistical
Future forecastRegionalSpeciesTerrestrialTemperate,
Montane
PlantApplied-
Management
Distribution
Hannah, L.,
Roehrdanz, P.
Ikegami, M.,
et al.
2013Climate
change,
wine, and
conservation
Proceedings of the
National Academy of
Sciences of the United
States of America/
110/6907–6912
10.1073/
pnas.1210127110
Climate
change
will have a
substantial
impact on
suitable habitat
for viticulture,
potentially
causing
conservation
conflicts
Statistical,
Database
Future forecastGlobalSpeciesTerrestrialTemperatePlantApplied-
Management
Distribution
Harvey B.P.,
Gwynn-Jones, D.,
Moore, P.J
2013Meta-analysis
reveals
complex
marine
biological
responses to
the interactive
effects
of ocean
acidification
and warming
Ecology and Evolution/
3/1016–1030
10.1002/ece3.516Biological
responses
of marine
organisms are
affected by
synergisms
between ocean
acidification
and warming
Meta-analysis,
Experiment
Future forecastMultiscalePopulationMarinePelagic,
Benthic,
Abyssal
Plant,
Invertebrate,
Fish
Theoretical-
Fundamental,
Applied-
Management
Physiology,
Population
dynamics
Hazen, E.L.,
Jorgensen, S.,
Rykaczewski, R.,
et al.
2013Predicted
habitat shifts
of Pacific top
predators in
a changing
climate
Nature Climate Change/
3/234–238
10.1038/nclimate1686For a forecast
rise of 1–6C
in sea-surface
temperature,
predicts up
to a +/-35%
change in
core habitat
of top marine
predators
New model, New
field data
Future forecastRegionalEcosystemMarineTemperate,
Pelagic
Bird, Fish,
Mammal, Reptile
Theoretical-
Fundamental,
Strategic-Policy
Distribution,
Migration-dispersal
Scheiter, S.,
Langan, L.
Higgins, S.I.
2013Next-
generation
dynamic
global
vegetation
models:
learning from
community
ecology
New Phytologist/
198/957–969
10.1111/nph.12210Describes
features
of next-
generation
dynamic global
vegetation
models,
illustrates
how current
limits could
be addressed
by integrating
community
assembly
rules
New model,
Methods
development
Retrospective
validation, Future
forecast
GlobalPopulation,
Ecosystem
TerrestrialBoreal,
Temperate,
Subtropical,
Tropical
PlantTheoretical-
Fundamental,
Applied-
Management
Trait, Physiology,
Biogeography
Smale, D.A.,
Wernberg, T.
2013Extreme
climatic event
drives range
contraction
of a habitat-
forming
species
Proceedings of the
Royal Society
B-Biological Sciences/
280/20122829
10.1098/
rspb.2012.2829
Extreme
warming
events
can cause
population
extirpation
leading to
distribution
shifts
New field data,
Experiment
ObservedRegionalSpeciesMarineBenthicPlantApplied-
Management
Distribution,
Physiology
Warren, R.,
VanDerWal, J.,
Price, J., et al.
2013Quantifying
the benefit of
early climate
change
mitigation
in avoiding
biodiversity
loss
Nature Climate Change/
3/678–682
10.1038/nclimate1887Analysis of a
range of future
climate change
scenarios
shows that
over 1/2 plant
species and
1/3 mammals
likely to lose
>50% of range
by 2080s;
mitigation
cuts this
substantially
Database,
Statistical
Future forecastGlobalSpeciesTerrestrialGlobalAllStrategic-PolicyDistribution
Bates, A.E.,
Barrett, N.S.,
Stuart-Smith, R.D.,
et al.
2014Resilience
and
signatures of
tropicalisation
in protected
reef fish
communities
Nature Climate Change/
4/62–67
10.1038/nclimate2062Protection from
fishing buffers
fluctuations
in reef fish
diversity and
provides
resistance
to climate
change
New field data,
Statistical
ObservedLocalCommunityMarineBenthicFishApplied-
Management
Global change
Burrows M.T.,
Schoeman, D.S.,
Richardson, A.J.,
et al.
2014Geographical
limits to
species-
range
shifts are
suggested
by climate
velocity
Nature/507/492–49510.1038/nature12976Global and
regional maps
of future
climate velocity
can be used
to infer shifts
in species
distributions
Methods
development
Reconstruction,
Future forecast
GlobalSpeciesTerrestrialGlobalAllApplied-
Management,
Strategic-Policy
Migration-
dispersal,
Distribution
Hennige, S.J.,
Wicks, L.C.,
Kamenos, N.A.,
et al.
2014Short-term
metabolic
and growth
responses
of the cold-
water coral
Lophelia
pertusa to ocean
acidification
Deep-Sea Research
Part II-Topical Studies in
Oceanography/
99/27–35
10.1016/
j.dsr2.2013.07.005
Increased
levels of
atmospheric
carbon dioxide
will negatively
influence the
respiration
rates, but not
calcification
rates, of cold-
water corals
ExperimentFuture forecastLocalPopulationMarineBenthicInvertebrateTheoretical-
Fundamental
Physiology
Jantz, P.,
Goetz, S.,
Laporte, N.
2014Carbon stock
corridors
to mitigate
climate
change and
promote
biodiversity in
the tropics
Nature Climate Change/
4/138–142
10.1038/nclimate2105If corridors
were
established to
strategically
connect
tropical forest
reserves,
would have
dual benefit
of facilitating
dispersal and
capturing 15%
of currently
unprotected
carbon stocks
StatisticalFuture forecastRegionalEcosystemTerrestrialTropicalPlantApplied-
Management
Networks,
Migration-dispersal
Pearson, R.G.,
Stanton, J.C.,
Shoemaker, K.,
et al.
2014Life history
and spatial
traits predict
extinction
risk due
to climate
change
Nature Climate Change/
4/217–221
10.1038/nclimate2113Extinction risk
from climate
change can
be predicted
using
spatial and
demographic
variables
already used
in species
conservation
assessments
Methods
development,
Database
Future forecastRegionalPopulation,
Species
TerrestrialMontane,
Temperate,
Subtropical,
Desert, Riverine
Amphibian,
Reptile
Applied-
Management
Trait, Population
dynamics,
Distribution,
Migration-
dispersal,
Threatened
species
Radosavljevic, A.,
Anderson, R.P.
2014Making better
MAXENT
models of
species
distributions:
complexity,
overfitting
and
evaluation
Journal of Biogeography/
41/629–643
10.1111/jbi.12227Application of
MAXENT to
a threatened
mouse species
to illustrate
how species-
specific tuning
can improve
model fit and
retrospective
validation
scores
Statistical,
Methods
development
Retrospective
validation
RegionalSpeciesTerrestrialTropicalMammalTheoretical-
Fundamental
Distribution,
Threatened
species
Scheffers, B.R.,
Edwards, D.P.,
Diesmos, A.,
et al.
2014Microhabitats
reduce
animal's
exposure
to climate
extremes
Global Change Biology/
20/495–503
10.1111/gcb.12439Microhabitats
decrease the
vulnerability of
species and
communities
to climate
change
New field data,
Experiment
Future forecastLocalSpeciesTerrestrialMontaneAmphibian,
Reptile
Applied-
Management
Physiology
Schmitz, O.J.,
Barton, B.T.
2014Climate
change
effects on
behavioral
and
physiological
ecology of
predator-prey
interactions:
Implications
for
conservation
biological
control
Biological Control/
75/87–96
10.1016/
j.biocontrol.2013.10.001
Develops
a "habitat
domain"
framework
to help to
forecast how
climate change
will alter
predator-prey
interactions
and biological
control
Methods
development
Future forecastLocalCommunityTerrestrialAnyAllApplied-
Management
Behaviour,
Physiology, Biotic
interactions
Shoo, L.P.,
O'Mara, J.,
Perhans, K.,
et al.
2014Moving
beyond the
conceptual:
specificity
in regional
climate
change
adaptation
actions for
biodiversity
in South East
Queensland,
Australia
Regional Environmental
Change/14/435–447
10.1007/s10113-012-
0385-3
Uses case
studies from
SE Queensland
biomes to
illustrate
the value
of context-
specific
approaches to
conservation
planning
under climate
change
DatabaseFuture forecastLocalEcosystemTerrestrial,
Other
SubtropicalPlantApplied-
Management
Community
dynamics,
Physiology
Zhu, K.,
Woodall, C.W.,
Ghosh, S.,
et al.
2014Dual impacts
of climate
change:
forest
migration
and turnover
through life
history
Global Change Biology/
20/251–264
10.1111/gcb.12382Tree species in
eastern US are
not migrating
sufficiently to
track climate
change, and
are instead
responding
with faster
turnover rates
in warm and
wet climates
Database, New
model
ObservedRegionalSpeciesTerrestrialTemperate,
Subtropical
PlantStrategic-
Policy
Migration-
dispersal,
Population
dynamics

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Analysis of trends, biases and gaps

Based on the categorisation frequencies in Table 1 (counts are given in the n columns adjacent to each category), the “archetypal” highly cited paper in biodiversity and climate change research relies on a database of previously collated information, makes an assessment based on future forecasts of shifts in geographical distributions, is regional in scope, emphasises applied-management outcomes, and uses terrestrial plant species in temperate zones as the study unit.

Many papers also introduced new methodological developments, studied montane communities, took a theoretical-fundamental perspective, and considered physiological, population dynamics, and migration-dispersal aspects of ecological change. Plants were by far the dominant taxonomic group under investigation. By contrast, relatively few of the highly cited paper studies used experimental manipulations or network analysis; lake, river, island and marine systems were rarely treated; nor did they focus on behavioural or biotic interactions. Crucially, none of the highly cited papers relied on paleoclimate reconstructions or genetic information, despite the potential value of such data for model validation and contextualisation 12. Such data are crucial in providing evidence for species responses to past environmental changes, specifying possible limits of adaptation (rate and extent) and fundamental niches, and testing theories of biogeography and macroecology.

At the time of writing, 5 of the 30 highly cited papers listed in Table 1 (16%) also received article recommendations from Faculty of 1000 experts ( f1000.com/prime/recommendations) 9, 13– 16 with none of the most recent (2014) highly cited papers having yet received an F1000 Prime endorsement.

Key findings of the highly cited paper collection for 2012–2014

A broad conclusion of the highly cited papers for 2012–2014 (drawn from the “main message” summaries described in Table 1) is that the pace of climate change-forced habitat change, coupled with the increased frequency of extreme events 15, 17 and synergisms that arise with other threat drivers 9, 18 and physical barriers 19, is typically outpacing or constraining the capacity of species, communities, and ecosystems to respond and adapt 20, 21. The combination of these factors leads to accumulated physiological stresses 13, 15, 22, might have already induced an “extinction debt” in many apparently viable resident populations 14, 23– 25, and is leading to changing community compositions as thermophilic species displace their more climate-sensitive competitors 13, 26. In addition to atmospheric problems caused by anthropogenic greenhouse-gas emissions, there is mounting interest in the resilience of marine organisms to ocean acidification 27, 28 and altered nutrient flows 16.

Although models used to underpin the forecasts of climate-driven changes to biotic populations and communities have seen major advances in recent years, as a whole the field still draws from a limited suite of methods, such as ecological niche models, matrix population projections and simple measures of change in metrics of ecological diversity 7, 12, 29. However, new work is pushing the field in innovative directions, including a focus on advancements in dynamic habitat-vegetation models 30– 32, improved frameworks for projecting shifts in species distributions 29, 33, 34 and how this might be influenced by competition or predation 35, 36, and analyses that seek to identify ecological traits that can better predict the relative vulnerability of different taxa to climate change 37, 38.

In terms of application of the research to conservation and policy, some offer local or region-specific advice on ecosystem management and its integration with other human activities (e.g., agriculture, fisheries) under a changing climate 18, 24, 35, 39. However, the majority of the highly cited papers used some form of forecasting to predict the consequences of different climate-mitigation scenarios (or business-as-usual) on biodiversity responses and extinctions 20– 22, 33, 40, so as to illustrate the potentially dire consequences of inaction.

Future directions

The current emphasis on leveraging large databases for evidence of species responses to observed (recent) climate change is likely to wane as existing datasets are scrutinised repeatedly. This suggests to us that future research will be forced to move increasingly towards the logistically more challenging experimental manipulations (laboratory, mesocosm, and field-based). The likelihood of this shift in emphasis is reinforced by the recent trend towards mechanistic models in preference to correlative approaches 41. Such approaches arguably offer the greatest potential to yield highly novel insights, especially for predicting and managing the outcomes of future climate-ecosystem interactions that have no contemporary or historical analogue. Along with this work would come an increasing need for systematic reviews and associated meta-analysis, to summarise these individual studies quantitatively and use the body of experiments to test hypotheses.

Technological advances will also drive this field forward. This includes the development of open-source software and function libraries that facilitate and standardise routine tasks like validation and sensitivity analysis of projection or statistical models 42, 43, as well as improved access to data layers from large spatio-temporal datasets like ensemble climate forecasts 10 and palaeoclimatic hindcasts 44. An increasing emphasis on cloud-based storage and use of off-site high-performance parallel computing infrastructure will make it realistic for researchers to undertake computationally intensive tasks 31 from their desktop.

These approaches are beginning to emerge, and a few papers on these topics already appear in the highly cited paper list ( Table 1

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