Download Conservation paleobiology: putting the dead to work

Survey
yes no Was this document useful for you?
   Thank you for your participation!

* Your assessment is very important for improving the workof artificial intelligence, which forms the content of this project

Document related concepts

Climate change in Saskatchewan wikipedia , lookup

Transcript
Review
Conservation paleobiology: putting
the dead to work
Gregory P. Dietl1 and Karl W. Flessa2
1
2
Paleontological Research Institution, 1259 Trumansburg Road, Ithaca, NY 14850, USA
Department of Geosciences, University of Arizona, Tucson, AZ 85721, USA
Geohistorical data and analyses are playing an increasingly important role in conservation biology practice and
policy. In this review, we discuss examples of how the
near-time and deep-time fossil record can be used to
understand the ecological and evolutionary responses of
species to changes in their environment. We show that
beyond providing crucial baseline data, the conservation
paleobiology perspective helps us to identify which
species will be most vulnerable and what kinds of
responses will be most common. We stress that inclusion of geohistorical data in our decision-making process provides a more scientifically robust basis for
conservation policies than those dependent on shortterm observations alone.
What is conservation paleobiology?
Conservation paleobiology is a relatively new, synthetic
field of research that applies the theories and analytical
tools of paleontology to the solution of problems concerning
the conservation of biodiversity [1]. The primary sources of
data are geohistorical in nature: the organic remains,
geochemical signals and associated sediments of the fossil
record [2]. The conservation paleobiology perspective has
the unique advantage of being able to identify phenomena
beyond timescales of direct human experience. Such data
are crucial for acquiring a long-term perspective on modern
systems, which is needed in order to develop more effective
conservation policies in the face of an uncertain future.
Conservation paleobiology involves two complementary
approaches. The first (near-time) approach uses the relatively recent past (the last few million years) as a dynamic
context for present-day conditions. The second (deep-time)
approach, ‘equally valuable but less systematically pursued’ [2], takes advantage of the entire history of life as a
natural ecological and evolutionary laboratory. This latter
approach sets the field apart from historical ecology, its
sister discipline (Box 1).
Here, we review examples illustrating how the neartime and deep-time fossil record can be used to understand
ecological and evolutionary dynamics. We build on previous studies where geohistorical data have proven valuable
to conservation research. Although the near-time fossil
record of ecological dynamics has attracted the most attention to date from conservation paleobiologists, we also
discuss how knowledge of the deep-time fossil record of
evolutionary dynamics can contribute to the conservation
of biodiversity. Our message is that the perspective
provided by geohistorical data is essential for the development of successful conservation strategies in the midst of a
constantly changing environment.
The nature and value of geohistorical data
In 2005, the U.S. National Research Council (Committee
on the Geologic Record of Biosphere Dynamics) acknowledged the key role that geohistorical data have to play in
addressing current biodiversity problems (Figure 1). And
yet, conservation-related research rarely employs such
data [3]; the majority of studies within the conservation
biology literature still focus on very short timescales ranging from years to decades [4].
Limited use of geohistorical data by many conservation
biologists might reflect both a lack of knowledge about the
availability of geohistorical records, reluctance to use (or
trust) data that do not come from well-controlled and replicated experiments [5] and uncertainties about the adequacy
of such information. These uncertainties commonly center
on precision and accuracy in inferring past environmental
conditions and on temporal resolution [2]. However, although the fossil record is incomplete, valuable insights
can be gained even from isolated samples that are well
positioned before and after significant biotic or abiotic
events. For instance, a study on the frequency of insect
damage to fossil angiosperm leaves from the Bighorn Basin
of Wyoming, dating from before, during and after the Paleocene-Eocene Thermal Maximum (PETM, 55.8 Ma), one of
the best deep-time analogs for our current global climate
change problems [6], suggests that insect herbivory intensified during that episode of global warming. This finding
provides insight into how the ongoing human-induced rise in
atmospheric CO2 is likely to affect insect–plant interactions
Glossary
Conservation paleobiology: the application of theories and analytical tools of
paleontology to biodiversity conservation.
Ecological legacies: ecological properties attributable to past events.
Environmental proxy: indicators based on physical, chemical, or biological
features of the geologic record that capture environmental information in
indirect form.
Geohistorical data: the individual stratigraphic sections, sediment or ice cores,
tree ring series, fossil collections or specimens that provide temporal,
environmental, and ecological information [2].
Historical baselines: reference conditions against which current changes can
be assessed.
Natural range of variability: the variation of ecological and evolutionary
patterns and processes over time and space.
Time-averaging: accumulation of fossil material over a span of time.
Corresponding author: Dietl, G.P. ([email protected]).
30
0169-5347/$ – see front matter ß 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2010.09.010 Trends in Ecology and Evolution, January 2011, Vol. 26, No. 1
Review
[()TD$FIG]
Trends in Ecology and Evolution
Box 1. Relationship between conservation paleobiology
and historical ecology
Conservation paleobiology shares its philosophical foundations
with historical ecology, which Swetnam et al. [85] defined as ‘the
use of historical knowledge in the management of ecosystems’.
Data sources in historical ecology are derived from written records,
long-term ecological monitoring, archaeology and paleoecology.
Balée [86] later offered a more narrowly focused definition of
historical ecology as a ‘research program concerned with comprehending temporal and spatial dimensions in the relationships of
human societies to local environments and the cumulative global
effects of these relationships’(for a similar view, see [87]). Time
scales in historical ecology studies are typically limited to relatively
recent time intervals, geologically speaking (i.e., the Pleistocene). In
addition, historical ecology concentrates on ecological dynamics
(e.g., changes in species distribution and abundance). Two perspectives that distinguish between the fields are: (1) the temporal
scope of conservation paleobiology also extends to the prePleistocene record; and (2) conservation paleobiology, in addition
to ecological dynamics, concentrates on evolutionary dynamics
(e.g., adaptive responses of species to changing climates or
ecological interactions).
in the long run, which is difficult to predict from short-term
studies that have shown highly species-specific responses
[7]. In addition, time-averaged information, as typically
captured by the geological record, has been shown to be
extremely useful in disentangling natural changes from
those induced by human activities. For instance, the frequent mismatch between the composition of time-averaged
death assemblages of mollusks and local living communities
has been shown repeatedly to be reliable evidence for
human-induced ecological change in marine habitats worldwide [8,9]. A growing list of indicators, based on physical,
chemical or biological features of the geological record
(Figure 2), also captures environmental information in indirect or proxy form. For example, the shells of mollusks
typically carry several kinds of proxy information: taxonomic identity, body size, growth patterns (e.g., growth
rings), ecological interactions (e.g., predation trace fossils),
geochronological estimates and geochemical signals (e.g.,
stable isotopes of oxygen and carbon; see examples in [10]).
Multiproxy methods are increasingly used, thus exploiting
the complementary strengths of each proxy [11].
The absolute age dating of geologic materials and time
series has also improved greatly over the last 25 years [12].
In particular, the high-resolution data available in the
most recent 100,000 years have proven to be an excellent
source of historical baseline information on species and
ecosystems [13]. High-resolution radiocarbon and amino
acid racemization dates are now routinely available at
modest costs while tree-rings, sclerochronology and varved
sediments often provide annual or sub-annual resolution
([14–16]).
Baselines and natural range of variability
Baselines, or reference conditions that show no discernable
human influence against which current changes can be
compared, are a fundamental concept in conservation paleobiology. How deep (in other words, how far back in time)
a baseline reference needs to be depends on the question.
For instance, van Leeuwen et al. applied geohistorical data
to identify invasive alien species [17]. The fossil pollen and
January 2011, Vol. 26, No. 1
Modeling
Information
integration
Geohistorical
data
Experimental/
observational data
TRENDS in Ecology & Evolution
Figure 1. Tripartite data integration. Approaches to conservation based on
geohistorical data are certainly not a substitute for modern-day observational
and experimental data or modeling. Instead, each source of information benefits
from the other’s strengths. Therefore, the ideal relationship is one of reciprocal
interaction (arrows) to increase our ability to predict (or develop scenarios of)
possible biotic responses to global environmental changes in an uncertain future.
The position of the inner circle within the ternary diagram reflects the relative
dominance of each approach. The current relationship is heavily biased toward
models being parameterized from modern-day observational and experimental
data (i.e., the inner circle is positioned closer to the side of the ternary diagram
opposite the geohistorical data apex). For instance, attempts to forecast the impact
of global climate change on species have often relied on bioclimate envelope
models, in which modern-day observed patterns of species distribution are
combined with environmental variables (typically climatic and other physical
variables) to predict distributions of species under future climate scenarios [90].
The critical assumptions in these models is that climate exerts a dominant role in
governing species distributions and that the occurrence–climate association
(ecological niche) of individual species does not change. The validity of these
assumptions is currently hotly debated (e.g., see [90–92]). A more integrated
approach (i.e., a centrally positioned inner circle) would also consider past
distributions of species across a broad range of environmental conditions outside
modern experience. When this type of integration has been attempted, the latter
assumption that ecological niche characteristics are conserved has had mixed
results. For instance, Martı́nez-Meyer and Peterson in a study of 23 extant North
American mammals and their Pleistocene fossil records, showed that for nine
species the model was able to predict the Pleistocene species distributions from the
modern-day data [93]. The distributions of the remaining species, however, were not
predicted accurately by the model. These results highlight aspects of a species’
relationship with its environment that are not apparent from modern observations
alone, underscoring the value of an integrated approach in conservation.
plant record of the Galápagos Islands shows that at least
six putative non-native or doubtfully native species were in
fact present before the first arrival of humans. This baseline information is crucial because a current conservation
priority in the Galápagos Islands is the removal of invasive
species [17]. Van Leeuwen et al.’s results thus highlight the
importance of baseline data as well as the risk involved in
applying management practices that use inappropriate
baselines.
The idea of using baselines is also the cornerstone of the
field of restoration ecology (and historical ecology; Box 1),
with baselines typically defined as conditions found before
European colonization or before industrial humans [4]. It is
often not appreciated, however, that even a few hundred
years ago the human footprint on the planet was widespread [18,19]. In other words, we often base our conservation efforts on data derived from already degraded
ecosystems. As Jackson reminds us, we need to be cautious
31
()TD$FIG][ Review
Trends in Ecology and Evolution January 2011, Vol. 26, No. 1
[34] and Avila-Serrano et al. [35] were able to compare
present-day benthic productivity conditions in the Colorado River estuary with the range of variation in the system
over the past 1000 years. Their geohistorical analysis
demonstrated a dramatic decrease in benthic productivity
(as estimated by the abundance of bivalve mollusks) in the
estuarine ecosystem after the diversion of the Colorado
River for human uses (Box 2). Carrasco et al. also showed
that shortly after humans arrived in North America, mammalian diversity dropped drastically relative to the normal
diversity baseline that had existed for millions of years
[36]. These examples (and many others like them) highlight how the use of geohistorical data can distinguish
human impact from natural variation (or noise) in the
system.
Figure 2. Examples of proxy indicators. Environmental proxies may be based on
physical (lithological), chemical (geochemical) and individual fossil and fossil
assemblage (biological) features of the geologic record. Some proxies have utility
throughout much of the geological past (e.g., oxygen isotopes), while others are
limited to relatively recent time intervals and conditions of exceptional
preservation, such as ancient DNA (see Table 2.1 in [2] for a more complete list
of proxies and their interpretations).
‘when we make strong statements based on ecological
calculations and insights derived from degraded, remnant
ecosystems. . .’ [20]. The most striking example concerns
the extinctions of the Pleistocene vertebrate megafauna
(animals greater than 44 kg (100 pounds) [21,22]) in North
America and other regions of the world; an event that
coincides with the first appearance of humans across the
landscape. While a human cause for extinction remains
debatable [21], undoubtedly the loss of these large, strongly interactive species has had lasting ecological and evolutionary consequences [23,24]. There is also overwhelming
evidence that today many top consumers, such as whales
[25,26] and sharks [27], have either been eliminated or
depressed in their numbers to the point where these
animals no longer fulfill their earlier ecological roles in
structuring ecosystems [28,29]. Predicting ecological consequences of these declines in abundance remains a challenge [30], which is made even more difficult because ‘many
ecologists fail to appreciate the prior existence of strong,
stabilizing interactions’ in the systems that they study
[31]. Insights gained from geohistorical baselines provide
a needed but largely untapped context of what is possible
in setting conservation or restoration goals for these ecologically important species.
It is typically acknowledged that the reference to baselines should take into account the dynamic nature of
ecological systems. Thus, another important concept in
conservation paleobiology is the natural range of variability [32,33], which is often estimated so as to better understand the bounds or envelope around temporally dynamic
patterns and processes. For instance, Kowalewski et al.
32
The geologic record as a natural ecological and
evolutionary laboratory
Another fundamentally important role of geohistorical
data is to provide access to a wider range of past environmental conditions (alternative worlds of every imaginable
circumstance) to address the ecological and evolutionary
dynamics of species. In other words, the geohistorical
record is a natural laboratory from which we can address
the responses of species to environmental changes, helping
us to understand which species will be most sensitive and
what kinds of responses will be most common.
There are three main ways in which species respond to
changes in their environment: (1) they can move, tracking
environmental changes; (2) they can stay put and adapt to
the changing environment; and (3) they can fail to track
habitats or to adapt, thus becoming extinct. In this section,
we review select examples of how geohistorical information
(derived from a variety of proxies; Figure 2) can inform
current trends and predict the responses of species to a
changing global environment in an uncertain future. These
examples are meant to be illustrative (but not exhaustive)
of the potential applications of conservation paleobiology
(for additional examples, see [1]).
Geographic range shifts
Shifts in species ranges are a predicted and inevitable
consequence of global climate change [37,38]. The underlying assumption is that climate change causes organisms
to migrate to (or track) habitats to which they are already
adapted. Predicting changes in species distributions under
different scenarios of global climate change is thus a major
agenda for many conservation organizations. We need to
know whether and where species will move in response to
future climate change [3].
Our understanding of what happens to species distributions as climate changes is greatly informed by geohistorical data [39,40]. Only geohistorical data can indicate
where species occurred in the past outside their present
range limits. There are now several examples of geographic
range shift in response to the contraction and expansion of
glaciers during the Pleistocene. For instance, Greenstein
and Pandolfi detailed how reef-building coral species from
Western Australia have responded to climate change since
the Late Pleistocene [41]. They found that many coral
species (particularly acroporids) contracted their ranges
Review
Trends in Ecology and Evolution
January 2011, Vol. 26, No. 1
Box 2. Historical baseline for the Colorado River Delta
The Colorado River no longer reaches the sea. Since 1960, its water
has been diverted to cities and farms in the U.S.A. and Mexico. There
is no scientific survey of the area before human impact. The upstream
dams and aqueducts that divert the river from the wetlands, floodplains and estuary the river once supported were completed well
before the implementation of laws requiring consideration of
environmental impact or endangered species. Old photographs,
maps and travelers’ accounts (e.g., [88]) provide a qualitative measure
of the natural ecosystems that have been lost, but the shells and fish
otoliths in natural accumulations, middens and museum collections
provide a quantitative record of the delta’s decreased productivity,
altered composition, changes in trophic structure and depressed
growth rates. High-precision radiocarbon and amino acid dating,
analysis of growth increments in shells and otoliths, and stable
isotope analysis of biogenic carbonates enable a remarkably detailed
look at the Colorado River’s estuarine ecosystem in the era before
upstream dams.
Studies summarized by Calderon and Flessa [89] document the
ecological impacts of upstream water diversions. Shell accumulations (Figure I) dating from before the upstream diversions were
made, show the following. Population densities of shelly mollusks
were up to ten times greater than those of today. A now rare,
endemic mollusk once flourished in the brackish waters of the
estuary and was an important trophic resource for snails and crabs.
In addition, growth banding and stable isotopes in otoliths of a
once commercially important but now endangered fish indicate that
first-year growth was faster when fresh water reached the river’s
estuary, leading to larger populations in the past and that species
recovery depends on river management as well as fisheries
management.
north towards the tropics in response to a drop in sea
surface temperatures of at least 2 8C since the last interglacial (about 120 ka).
Species are not always able to track suitable habitats,
however. For instance, Dalén et al. used ancient DNA to
show that the arctic fox (Alopex lagopus) in Europe was not
able to track shifting climates as its range contracted,
eventually becoming extinct at the end of the Pleistocene[42]. However, the species persisted in refugia in
northeastern Siberia. Geohistorical records are thus critical in identifying where species survived periods of changing climates (i.e., refugia [43]). For instance, during the
glacial intervals of the Pleistocene in Europe, the Balkans,
Iberia and Italy served as refugia for many temperate
plants, insects and vertebrates [43]. Such information
can significantly enhance our ability to understand and
predict future effects of global climate change on species
distributions, because most ecological models are parameterized from modern-day observations alone (Figure 1)
[44]; and so might fail to accurately predict range shifts
in response to changing climates in the future.
Geohistorical analysis can help locate and assess the
persistence of source regions by documenting the patterns
of spread of species. Source regions are important conservation priorities because populations from these areas
provide recruits for other populations and adaptations that
characterize the species as a whole largely originate within
them [45]. For example, geohistorical data indicate that
the northeastern Atlantic has served as a source region
since the Pliocene for many cool-temperate marine species
that are found on both sides of the Atlantic [46].
Given the ecological similarities between range shifts
and introductions of species [47], it is insightful to look to
The environmental impacts of water diversions on the Colorado
River’s estuary can no longer be ignored simply because they are
undocumented. Abundant, high-resolution geohistorical data have
provided crucial documentation and the next step is restoration.
Analysis of oxygen isotopes in shells and otoliths suggests that
dedicating 5–10% of the river’s annual flow, managed to include an
annual pulse flow, could restore the core of this vanished
ecosystem.
[()TD$FIG]
Figure I. Beaches along the Baja California shore of the Colorado River Delta
are estimated to contain two trillion shells, evidence of the estuary’s high
productivity in the past. (Photo credit: Karl Flessa)
the geohistorical record of invasion (basically a history of
range expansion) for insights into the likely effects of global
climate change on species distributions. For instance,
there is growing concern that warming climates will increase the rate of introduction and establishment (whether
through human-assisted introduction or natural range
shifts) of invasive marine species, particularly predatory
species, into the Antarctic [48]. The endemic, shallowwater bottom fauna of Antarctica is functionally unique
in the world’s oceans [48,49]. In particular, in terms of
structure and function, the Antarctic bottom fauna: (1)
lacks fast-moving, shell-crushing predators, such as sharks
and crabs; and (2) soft-sediment habitats are dominated by
organisms that live on the surface and feed on the plankton
[48,49]. This unique food-web structure was established
about 41 million years ago in the Eocene as temperatures
started to cool and shell-crushing predators were excluded
from Antarctic waters [48]. As global climate change continues, the re-invasion of shell-crushing predators, which
has already begun [50], will have drastic effects, modernizing the shallow-water bottom fauna and profoundly
altering the character of marine life in Antarctica [48].
This deep-time perspective is beyond the reach of modern
ecology.
Analysis of geohistorical records also suggests that
present-day global climate change might lead to processes
of large-scale biotic interchange, the spread of many species from one geographic area to another [51]. This process
has been a common form of invasion in the history of life
and is almost always a highly asymmetrical process, with
one of the geographic areas typically serving as the donor
biota and the other serving as the recipient biota [52]. Well
studied examples include the Great American interchange,
33
Review
the spread of species (especially mammals) between North
and South America [53] and the Trans-Arctic interchange
(the spread of species between the North Pacific and North
Atlantic Oceans [54]). Most episodes of biotic interchange
coincide with warm climates [51]. Thus, as the world
warms, we might enter a new era of biotic interchange,
especially at high latitudes [55]. Insights gained from
geohistorical analysis of past episodes of biotic interchange
provide predictive power for the long-term effects of invasion [56].
Adaptive phenotypic responses
Many species today are failing to track global climate
changes by shifting their geographic ranges [38,57]. For
these species, their potential for adaptive response to new
environmental conditions is crucial to their long-term
persistence. Those species that are tracking local changes
in their environment might also undergo adaptive changes
[57–59]. This realization suggests that there is an urgent
need to develop practical approaches to managing adaptation (i.e., eco-evolutionary dynamics or contemporary evolution [60–65]). Unfortunately, whereas geographic range
shifts in response to global climate change are increasingly
well documented [38], adaptive responses are far less well
understood. Our understanding of how local adaptive
responses influence species’ persistence is hindered by a
lack of basic data on which ecologically important traits are
most likely to evolve and keep species in the ecological
game [66] and whether species will be able to adapt fast
enough to keep up with their changing environment
[67,68].
Geohistorical records have the unique advantage of
providing evidence for how species adapt under a wide
range of environmental conditions, unlike those of the
present day. For instance, Bruzgul et al. used the late
Holocene fossil record of the tiger salamander (Ambystoma
tigrinum) from Lamar Cave in Yellowstone National Park,
Wyoming, to assess responses in morphology and life
history to changes in climate [69]. This species is able to
exploit alternative life histories in response to environmental changes by either metamorphosing into a terrestrial
adult, or remaining aquatic and retaining a larval (i.e.,
paedomorphic) morphology [69]. Bruzgul et al. found that
A. tigrinum responded to the largest climatic shift in the
Yellowstone region over the last 3000 years, the Medieval
Warm Period (1150 – 650 ybp), which is characterized by a
warm and dry climate, by increasing body size. There was
also a consistent ratio of paedomorphic to metamorphic
individuals over the duration of the time interval studied,
demonstrating that climate changes did not have an effect
on all life history characteristics. This study provides
timely information for managers on how this sensitive
indicator amphibian species will respond ecologically
and evolutionarily to predicted future climatic warming
in the Yellowstone region. This example also highlights the
utility of geohistorical records in helping to outline scenarios [70] of possible complex and uncertain futures.
Extinction selectivity
The need for long-term geohistorical perspectives on species is especially critical in understanding extinction risks.
34
Trends in Ecology and Evolution January 2011, Vol. 26, No. 1
Applying geohistorical data to modern extinction problems
is desirable because habitat loss was also the cause of many
species extinctions in the geological past [71]. By using the
geological record to examine the filtering effects of extinction, we can better understand what types of species have
more favorable odds of surviving under future environmental conditions.
As with species invasions and despite the great difference in the scale of observation, geohistorical and ecological evidence largely agree on which traits increase
extinction risk [72], such as slow growth rate and restricted
geographic distribution. For instance, analysis of bird
extinctions from islands across the Pacific Ocean over
the past 3500 years shows that complexes of interacting
traits, which characterize species ecology (e.g., endemism,
body size, diet), are the best predictors of extinction risk
through time [73].
It is also increasingly evident that past extinctions act
as important filters on current vulnerability [74]. For
instance, fossil evidence suggests that birds of the Hawaiian Islands suffered a large-scale extinction event around
the time of Polynesian arrival [75]. In a comparison of the
ecological characteristics of bird species before and after
this extinction interval, Boyer showed a strong extinction
bias against larger bodied and flightless, ground-nesting
species [76]. This pattern supported a role for direct human
hunting in the extinction event. By the time of first European contact in the 18th century (which also led to a second
wave of extinction with its own selectivity pattern), most
large-bodied species had already disappeared; those that
survived had traits that helped them survive both extinction waves.
A similar story can be told for other places and species.
For instance, rapid and intense Pleistocene climatic
change led to few extinctions of western European insect
species [77]. Instead, species shifted their ranges, tracking
acceptable habitats. As Coope described it: ‘Those species
that could not make such an adjustment would have
become extinct at the beginning of glacier/interglacial
cycles... The species that cleared the first fence of the
climatic hurdle race could similarly clear all the rest.’
[77]. This idea of extinction filters suggests that we should
expect some species to respond to current climatic changes
in the same way as they did to past environmental changes.
Geohistorical data thus tell us that we have inherited a
world in which there is considerable variation in the
vulnerability of species to extinction due to historical
contingencies (e.g., ecological legacies from past selective
agents [78]).
Moving from promise to application
Mitigating environmental damage requires that we know
what has been damaged; adapting to environmental
change requires that we know what to expect. In both
cases, geohistorical data are essential to formulating both
a general policy and a specific response. But changes in
conservation policy rarely occur because of the inclusion of
a new set of data. Expecting geohistorical data to make
such a difference is thus unreasonable. Instead, moving
from promise to application requires the data of conservation paleobiology and the means to translate those data
Review
into a useful form. In other words, there is an increasing
need, shared with other environmental sciences, to demonstrate knowledge transfer between science and policy
[79,80].
This task is easier said than done. A widely acknowledged impediment to conservation action is the inability to
translate research results into effective policies and management due, in large part, to differences in scales, methodology, treatment of uncertainty and goals and/or values
between different communities [81–83]. However, progress
can be made. Conservation biologists have learned to work
with both agencies and environmental non-governmental
organizations in order for their data to have an impact
(although evaluating the success of conservation efforts
and identifying the most effective approaches remain important challenges [84]). Conservation paleobiologists
need to do the same. Genuine outreach, putting the dead
to work, requires real effort. Conservation paleobiologists
first need to learn from agencies and non-governmental
organizations what new data are needed and then need to
translate their results to address real-world problems in
conservation.
Concluding statement
Mounting evidence indicates that when conditions are
right and paleobiologists are clever, data and insights
useful in the practice of conservation biology will result.
We have argued, through selected examples, that beyond
baselines and the range of natural variability, understanding of the range of ecological and evolutionary responses of
species to past environmental changes can be greatly
informed by geohistorical data. A crucial challenge for
the immediate future is making conservation paleobiology
results policy-relevant. As the approaches of conservation
paleobiology move from their academic development to
their application by agencies and non-governmental organizations, this new discipline will be putting the dead to
work to benefit the future.
Acknowledgments
We thank David Jablonski for coining the catchphrase ‘‘putting the dead
to work’’ and two anonymous reviewers for their helpful comments.
References
1 Dietl, G.P. and Flessa, K.W., eds (2009) Conservation Paleobiology:
Using the Past to Manage for the Future, The Paleontological Society
Papers, vol. 15, Paleontological Society.
2 National Research Council (2005) The Geological Record of Ecological
Dynamics: Understanding the Biotic Effects of Future Environmental
Change, National Academies Press
3 Willis, K.J. and Birks, H.J.B. (2006) What is natural? The need for a
long-term perspective in biodiversity conservation. Science 314, 1261–
1265
4 Froyd, C.A. and Willis, K.J. (2008) Emerging issues in biodiversity and
conservation management: the need for a palaeoecological perspective.
Quat. Sci. Rev. 27, 1723–1732
5 Sagarin, R. and Pauchard, A. (2010) Observational approaches in
ecology open new ground in a changing world. Front. Ecol. Environ.
20, 379–386
6 Currano, E.D. et al. (2008) Sharply increased insect herbivory during
the Paleocene-Eocene thermal maximum. Proc. Natl. Acad. Sci. U.S.A.
105, 1960–1964
7 Hamilton, J.G. et al. (2004) Insect herbivory in an intact forest
understory under experimental CO2 enrichment. Oecologia 138, 566–573
Trends in Ecology and Evolution
January 2011, Vol. 26, No. 1
8 Kidwell, S.M. (2007) Discordance between living and death
assemblages as evidence for anthropogenic ecological change. Proc.
Natl. Acad. Sci. U. S. A. 104, 17701–17706
9 Kidwell, S.M. (2009) Evaluating human modification of shallow marine
ecosystems: mismatch in composition of molluscan living and timeaveraged death assemblages. In Conservation Paleobiology: Using the
Past to Manage for the Future (Dietl, G.P. and Flessa, K.W., eds), The
Paleontological Society Papers, vol. 15, pp. 113–139, Paleontological
Society
10 Kowalewski, M. (2009) The youngest fossil record and conservation
biology: Holocene shells as eco-environmental recorders. In
Conservation Paleobiology: Using the Past to Manage for the Future
(Dietl, G.P. and Flessa, K.W., eds), The Paleontological Society Papers,
vol. 15, pp. 1–23, Paleontological Society
11 Mann, M. (2002) The value of multiple proxies. Science 297, 1481–1482
12 Erwin, D.H. (2006) Opportunities and challenges of a highly resolved
geological timescale. In Geochronology: Emerging Opportunities
(Olszewski, T.D., ed.), The Paleontological Society Papers, vol. 12,
pp. 171–180, Paleontological Society
13 Willis, K.J. et al. (2010) Biodiversity baselines, thresholds and
resilience:
testing
predictions
and
assumptions
using
palaeoecological data. Trends Ecol. Evol. 25, 583–591
14 Schöne, B.R. and Surge, D. (2005) Looking back over skeletal diaries:
high-resolution environmental reconstructions from accretionary hard
parts of aquatic organisms. Palaeogeogr. Palaeoclimatol. Palaeoecol.
228, 1–3
15 Swetnam, T.W. et al. (2009) Multi-millennial fire history of the
giant forest, Sequoia National Park, California, USA. Fire Ecol. 5,
120–
150
16 Tierney, J.E. et al. (2010) Late twentieth-century warming in Lake
Tanganyika unprecedented since AD 500. Nature Geosci. 3, 422–425
17 Van Leeuwen, J.F.N. et al. (2008) Fossil pollen as a guide to
conservation in the Galápagos. Science 322, 1206
18 Jackson, J.B.C. et al. (2001) Historical overfishing and the recent
collapse of coastal ecosystems. Science 293, 629–638
19 Delcourt, P.A. and Delcourt, H.R. (2004) Prehistoric Native Americans
and Ecological Change, Cambridge University Press
20 Jackson, J.B.C. (2006) When ecological pyramids were upside down. In
Whales, Whaling, and Ocean Ecosystems (Estes, J.A. et al., eds), pp. 27–
37, University of California Press
21 Barnosky, A.D. et al. (2004) Assessing the causes of Late Pleistocene
extinctions on the continents. Science 306, 70–75
22 Lyons, S.K. et al. (2004) Of mice, mastodons and men: human-mediated
extinctions on four continents. Evol. Ecol. Res. 6, 339–358
23 Donlan, C.J. et al. (2006) Pleistocene rewilding: an optimistic agenda
for twenty-first century conservation. Am. Nat. 168, 660–681
24 Vermeij, G.J. (2004) Nature: An Economic History, Princeton
University Press
25 Springer, A.M. et al. (2003) Sequential megafaunal collapse in the
North Pacific Ocean: an ongoing legacy of industrial whaling? Proc.
Natl. Acad. Sci. U. S. A. 100, 12223–12228
26 Roman, J. and Palumbi, S.R. (2003) Whales before whaling in the
North Atlantic. Science 301, 508–510
27 Myers, R.A. et al. (2007) Cascading effects of the loss of apex predatory
sharks from coastal ocean. Science 315, 1846–1850
28 Lotze, H.K. and Worm, B. (2009) Historical baselines for large marine
animals. Trends Ecol. Evol. 24, 254–262
29 Humphries, P. and Winemiller, K.O. (2009) Historical impacts on river
fauna, shifting baselines, and challenges for restoration. BioSci. 59,
673–684
30 Heithaus, M.R. et al. (2008) Predicting ecological consequences of
marine top predator declines. Trends Ecol. Evol. 23, 202–210
31 Soule, M.E. (2010) Conservation relevance of ecological cascades. In
Trophic Cascades: Predators, Prey, and the Changing Dynamics of
Nature (Terborgh, J. and Estes, J.A., eds), pp. 337–351, Island Press
32 Keane, R.E. et al. (2009) The use of historical range and variability
(HRV) in landscape management. Forest Ecol. Management 258, 1025–
1037
33 Landres, P. et al. (1999) Overview of the use of natural variability in
managing ecological systems. Ecol. Applications 9, 1279–1288
34 Kowalewski, M. et al. (2000) Dead delta’s former productivity:
two trillion shells at the mouth of the Colorado River. Geology 28,
1059–1062
35
Review
35 Ávila-Serrano, G.E. et al. (2006) Distribution of the intertidal
macrofauna of the Colorado River Delta, northern Gulf of California,
Mexico. Ciencias Marinas 32, 649–661
36 Carrasco, M.A. et al. (2009) Quantifying the extent of North American
mammal extinction relative to the pre-anthropogenic baseline. PLoS
one 4, e8331
37 Graham, R.W. et al. (1996) Spatial response of mammals
to Late Quaternary environmental fluctuations. Science 272, 1601–
1606
38 Parmesan, C. (2006) Ecological and evolutionary response to recent
climate change. Annu. Rev. Ecol. Evol. Syst. 37, 637–669
39 Jackson, J.B.C. and Erwin, D.H. (2006) What can we learn about
ecology and evolution from the fossil record. Trends Ecol. Evol. 21,
322–328
40 Lyons, S. (2003) A quantitative assessment of the range shifts of
Pleistocene mammals. J. Mammal. 84, 385–402
41 Greenstein, B.J. and Pandolfi, J.M. (2008) Escaping the heat: range
shifts of reef coral taxa in coastal Western Australia. Global Change
Biol. 14, 513–528
42 Dalén, L. et al. (2007) Ancient DNA reveals lack of postglacial
habitat tracking in the arctic fox. Proc. Natl. Acad. Sci. U. S. A. 104,
6726–6729
43 Stewart, J.R. et al. (2010) Refugia revisited: individualistic
responses of species in space and time. Proc. Roy. Soc. B. 277,
661–671
44 Williams, J.W. and Jackson, S.T. (2007) Novel climates, no-analog
communities, and ecological surprises. Front. Ecol. Environ. 5,
475–482
45 Vermeij, G.J. and Dietl, G.P. (2006) Majority rule: adaptation and the
long-term dynamics of species. Paleobiology 32, 173–178
46 Vermeij, G.J. (2005) From Europe to America: Pliocene to recent transAtlantic expansion of cold-water North Atlantic mollusks. Proc. Roy.
Soc. B. 272, 2545–2550
47 Sorte, C.J.B. et al. (2010) Marine range shifts and species
introductions: comparative spread rates and community impacts.
Global Ecol. Biogeogr. 19, 303–316
48 Aronson, R.B. et al. (2007) Climate change and invasibility of the
Antarctic benthos. Annu. Rev. Ecol. Evol. Syst. 38, 129–154
49 Aronson, R.B. (2009) Metaphor, inference, and prediction in
paleoecology: climate change and the Antarctic bottom fauna. In
Conservation Paleobiology: Using the Past to Manage for the Future
(Dietl, G.P. and Flessa, K.W., eds), The Paleontological Society Papers,
vol. 15, pp. 177–194, Paleontological Society
50 Thatje, S. et al. (2005) Challenging the cold: crabs reconquer the
Antarctic. Ecology 86, 619–625
51 Vermeij, G.J. (2009) Seven variations on a recent theme of
conservation. In Conservation Paleobiology: Using the Past to
Manage for the Future (Dietl, G.P. and Flessa, K.W., eds), The
Paleontological Society Papers, vol. 15, pp. 167–175, Paleontological
Society
52 Vermeij, G.J. (2005) Invasion as expectation. In Species Invasions:
Insight into Ecology, Evolution, and Biology (Sax, D.F. et al., eds), pp.
315–339, Macmilliam Publishers Limited
53 Webb, S.D. (2006) The Great American Biotic Interchange: patterns
and processes. Ann. Mo, Bot. Gard. 93, 245–257
54 Vermeij, G.J. (1991) Anatomy of an invasion: the trans-Arctic
interchange. Paleobiology 17, 281–307
55 Vermeij, G.J. and Roopnarine, P.D. (2008) The coming Arctic invasion.
Science 321, 780–781
56 Strayer, D.L. et al. (2006) Understanding the long-term effects of
species invasions. Trends Ecol. Evol. 21, 645–651
57 Hill, J.K. et al. (2011) Climate change and evolutionary adaptations at
species’ range margins. Annu. Rev. Entomol. 56, 143–159
58 Jump, A.S. and Peñuelas, J. (2005) Running to stand still: adaptation
and the response of plants to rapid climate change. Ecol. Lett. 8, 1010–
1020
59 Davis, M.B. and Shaw, R.G. (2001) Range shifts and adaptive
responses to quaternary climate change. Science 292, 673–679
60 Smith, T.B. and Bernatchez, L. (2008) Evolutionary change in humanaltered environments. Mol. Ecol. 17, 1–8
61 Kinnison, M.T. and Hairston, N.G., Jr (2007) Eco-evolutionary
conservation biology: contemporary evolution and the dynamics of
persistence. Funct. Ecol. 21, 444–454
36
Trends in Ecology and Evolution January 2011, Vol. 26, No. 1
62 Stockwell, C.A. et al. (2003) Contemporary evolution meets
conservation biology. Trends Ecol. Evol. 18, 94–101
63 Carroll, S.P. (2008) Facing change: forms and foundations
of contemporary adaptation to biotic invasions. Mol. Ecol. 17,
361–372
64 Dietl, G.P. (2009) Paleobiology and the conservation of the evolving
web of life. In Conservation Paleobiology: Using the Past to
Manage for the Future (Dietl, G.P. and Flessa, K.W., eds), The
Paleontological Society Papers, vol. 15, pp. 221–244, Paleontological
Society
65 Rice, K.J. and Emery, N.C. (2003) Managing microevolution:
restoration in the face of global change. Front. Ecol. Environ. 1,
469–478
66 Thompson, J.N. (2009) Which ecologically important traits are most
likely to evolve rapidly? Oikos 118, 1281–1283
67 Visser, M.E. (2008) Keeping up with a warming world; assessing
the rate of adaptation to climate change. Proc. Royal. Soc. B. 275,
649–659
68 Atkins, K.E. and Travis, J.M.J. (2010) Local adaptation and the
evolution of species’ ranges under climate change. J. Theor. Biol.
266, 449–457
69 Bruzgul, J.E. et al. (2005) Temporal response of the tiger salamander
(Ambystoma tigrinum) to 3,000 years of climatic variation. BMC Ecol.
5, 7
70 Peterson, G.D. et al. (2003) Scenario planning: a tool for conservation in
an uncertain world. Conserv. Biol. 17, 358–366
71 Jablonski, D. (2001) Lessons from the past: evolutionary impacts of
mass extinctions. Proc. Natl. Acad. Sci. U. S. A. 98, 5393–5398
72 McKinney, M.L. (1997) Extinction vulnerability and selectivity:
combining ecological and paleontological views. Annu. Rev. Ecol.
Syst. 28, 495–516
73 Boyer, A.G. (2009) Consistent ecological selectivity through time in
Pacific island avian extinctions. Conserv. Biol. 24, 511–519
74 Balmford, A. (1996) Extinction filters and current resilience: the
significance of past selection pressures for conservation biology.
Trends Ecol. Evol. 11, 193–196
75 Burney, D.A. et al. (2001) Fossil evidence for a diverse biota from
Kaua’i and its transformation since human arrival. Ecol. Monogr. 71,
615–641
76 Boyer, A.G. (2008) Extinction patterns in the avifauna of the Hawaiian
Islands. Divers. Distrib. 14, 509–517
77 Coope, G.R. (2004) Several million years of stability among insect
species because of, or in spite of, Ice Age climatic instability? Phil.
Trans. Roy. Soc. B. 359, 209–214
78 Jackson, S.T. et al. (2009) Ecology and the ratchet of events: climate
variability, niche dimensions, and species distributions. Proc. Natl.
Acad. Sci. U. S. A. 106, 19685–19692
79 Sutherland, W.J. et al. (2004) The need for evidence-based
conservation. Trends Ecol. Evol. 19, 305–308
80 Balmford, A. and Bond, W. (2005) Trends in the state of nature
and their implications for human well-being. Ecol. Lett. 8, 1218–
1234
81 Stevens, C.J. et al. (2007) Making ecological science policy-relevant:
issues of scale and disciplinary integration. Landscape Ecol. 22, 799–
809
82 Lawton, J.H. (2007) Ecology, politics and policy. J. Applied Ecol. 44,
465–474
83 Fox, H.E. et al. (2006) Perceived barriers to integrating social science
and conservation. Conser. Biol. 20, 1817–1820
84 Kapos, V. et al. (2008) Calibrating conservation: new tools for
measuring success. Conserv. Lett. 1, 155–164
85 Swetnam, T.W. et al. (1999) Applied historical ecology: using the past to
manage for the future. Ecol. Appl. 9, 1189–1206
86 Balée, W. (2006) The research program of historical ecology. Annu. Rev.
Anthropol. 35, 75–98
87 Egan, D. and Howell, E.A. (2001) The Historical Ecology Handbook: A
Restorationist’s Guide to Reference Ecosystems, Island Press
88 Leopold, A. (1949) The green lagoons. In A Sand County Almanac
(Leopold, A., ed.), pp. 150–158, Oxford University Press
89 Calderon-Aguilera, L.E. and Flessa, K.W. (2009) Just add water?
Transboundary Colorado River flow and ecosystem services in the
upper Gulf of California. In Conservation of Shared Environments:
Learning from the United States and Mexico (López-Hoffman, L.,
Review
McGovern, E.D., Varady, R.G. and Flessa, K.W., eds), pp. 154–169,
University of Arizona Press
90 Elith, J. and Leathwick, J.R. (2009) Species distribution models:
ecological explanation and prediction across space and time. Annu.
Rev. Ecol. Evol. Syst. 40, 677–697
91 Araájo, M.B. and Luoto, M. (2007) The importance of biotic interactions
for modeling species distributions under climate change. Global Ecol.
Biogeogr. 16, 743–753
Trends in Ecology and Evolution
January 2011, Vol. 26, No. 1
92 Chevin, L-M. et al. (2010) Adaptation, plasticity, and extinction in a
changing environment: towards a predictive theory. PLoS Biol. 8,
e1000357
93 Martı́nez-Meyer, E. et al. (2004) Ecological niches as stable
distributional constraints on mammal species, with implications for
Pleistocene extinctions and climate change projections for biodiversity.
Global Ecol. Biogeogr. 13, 305–314
37