REVIEWS

Extinctionfilters and currentresilience:

the significanceof past selection
pressuresfor conservationbiology

ccording to the latest and There is now little reasonable doubt about
New work suggests that palaeonthe scale of the present extinction crisis:
tology may provide us with some
most exhaustive survey
recent and ongoing rates of species loss
of the status of the worlds
clues.
birds, more than 11%are
exceed background levels by two to three
threatened with extinction in the
orders of magnitude. Nevertheless,
Climatic extinction filters
species differ widely in their vulnerability
near future. In some regions, reWith the onset of northern
to current threats. Growing evidence from
cent losses may be even greater.
hemisphere glaciation at the end
both paiaeontoiogy and conservation
Archaeological finds of new speof the Pliocene, sea temperatures
biology suggests that past events
dropped dramatically. Even in
cies on tropical Pacific islands
may help to explain this variation.
indicate that human activity has
the tropics, marine species underalready resulted in the extinction
Communities appear far more resilient to
went substantial turnover. In the
of very large numbers of land birds
particular threats if they have faced
Caribbean, an estimated 36% of
similar challenges in the past. This
(Fig. 1). Extrapolation from a figPliocene molluscan genera and
intuitive but poorly reported phenomenon
ure of l-4 fossil species just of ensubgenera went extinct by the early
has potentially far-reaching implications
demic rails (Rallidae) from every
Pleistocene; synchronous turnover
well-studied island of the tropical
for attempts to focus conservation
occurred in western Atlantic corals
efforts on those areas most at risk from
Pacific suggests that prehistoric
and ForaminiferaG. However, sub
humans caused the extinction of
contemporary human activity.
sequent and equally severe Pleistoas many as 2000 endemic landbird
cene cycles of warming and cooling
species across the Pacific as a
and associated sea-level changes
Andrew Balmford is at the Dept of Animal and Plant
whole2.3.Comparison of such extinchave had little impact on surviving
Sciences, University of Sheffield, Sheffield,
tions and of current threat levels
Caribbean molluscs or corals6J.
UK SIO 2TN (a.balmford@sheffield.ac.uk).
with turnover in the fossil record
Moreover, the biological conseconfirms that humans are responquences of Pliocene-Pleistocene
sible for an extinction crisis in
refrigeration were less extensive in
the eastern Pacific, where cooling was preceded by the onwhich species are being lost 100-1000 times faster than
set of upwelling and pronounced seasonal temperature flucbackground rates4J. The scale of this problem means that
tuation. One explanation for both patterns is that the initial
conservation action must increasingly be directed towards
exposure to climatic changes purged marine faunas of therwhole communities rather than species - but how can we
mally sensitive taxa, leaving behind a core of species that
identify key sites where such efforts might be most rewarding?
were relatively resilient to further temperature fluctuations@.
A recent and elegant review of ice-age insect faunas provides evidence of similar filtering on landg. In spite of frequent, rapid and intense climatic changes during glacials and
interglacials, very few Quaternary insect fossils from western Europe are extinct. Of more than 2000 species recorded
from Quaternary Britain, for example, over 99% have been
matched to extant counterpart@. It appears that ranges of
nearly all species have shifted so that, instead of succumbing
to dramatic climatic change, the species have paradoxically
continued to live in effectively constant environmental conditions. In contrast, assemblages from the Upper Tertiary
contain some species that failed to survive the onset of the
Pleistocene climatic oscillations. The analogy that Coopeg
draws to explain these results is that of a hurdle race, in which
certain species, perhaps because of their ecology, physiology or biogeography, fail to move out of trouble during
the first major climatic challenge. These go extinct, whereas
other species that can clear the initial hurdle could in turn
most
likely leap all succeeding ones.
Time Fig. 1. Long-termchanges in the number of forest birds on Eua, Tonga.
In the 3000 years since human arrival, recorded species richness has
declined by at least two-thirds. Redrawn from Ref. 2.

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Resilience to present-day threats

These palaeontological observations suggest that variation in past history may explain hitherto poorly understood
differences in the vulnerability of biotas to modern-day
Science

Ltd

PII: SO169-5347(96)100X-4

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REVIEWS

Fig. 2. The impact of cattle grazing on native plants and animals in the western
and Great Plains regions of the USA, in relation to the historical range of Bison
bison. The shaded area shows states where two or more studies (cited in Ref. 10)
have revealed deleterious effects of cattle: filled circles indicate records of Bison
bison from 5000s~ to the present (from Ref. 11). Most instances of negative
impacts are from states at or beyond the limits of bison distribution.

challenges. An illustration of this comes from a vigorous

debate on the impact of grazing on the rangelands of North
America (Fig. 2). A major new assessment10 concluded that
the conservation impact of cattle in the arid and semi-arid
western USAhas been almost universally negative. Several
authors have challenged this assertioni2~13,citing a number
of examples of benign or even beneficial effects of grazing
on native plant and animal communities. However, these
counterexamples come from the more mesic Midwest and
Great Plains regionsl4315.Unlike most of the western states,
these areas lie well within the Holocene range of the bison
(Bison bison)ii and thus support species that have evolved
counteradaptations against grazing by large ungulates.
Differences in historical selection pressures thus appear to
explain geographical variation in the resilience of native
plants to modern grazing regimes.
Two other examples are more speculative. One of the
greatest single anthropogenic causes of extinction of island birds is predation by introduced rats (Rattus ~pp.)~,l6,~7,
yet island avifaunas differ widely in their vulnerability to
alien species. On a few islands, rats have brought about
catastrophic levels of bird extinction, but in many (perhaps
most) cases, introductions have been followed by coexistence of rats and native birds. A possible solution to this
puzzle might lie in the presence or absence of endemic
predators. For instance, islands that historically have supported native rodents (such as Christmas Island in the Indian
Ocean, and the Galapagos Islands) appear to have avifaunas
that are now relatively resilient to introduced ratsi*.
Likewise, the generally lower vulnerability of birds on tropical, as opposed to temperate, islands may be linked to the
historical distribution of land crabs - potentially important
predators of chicks*. In both cases, continued selection for
194

the retention of anti-predator traits may have ensured that

native birds were less susceptible to introduced rats than
were birds from islands lacking predators.
Lastly, the idea of long-term evolutionary pressures
underpinning current resilience has been put forward to
account for the apparently anomalous lack of recent extinctions in Brazils Atlantic forestslg. According to predictions
based on the classic species-area relationshipzo, the clearance of around 90% of the regions forests should have committed 25-50% of its endemic species to global extinction,
but so far no species has been proven extinct. This striking
discrepancy has been cited as a major criticism of attempts
to apply the species-area technique in order to estimate extinction rates worldwide21.One proposed explanation is that
the complex topography and high rates of natural disturb
ante characteristic of the Atlantic forests have selected for
traits conferring resistance to the habitat fragmentation and
microclimatic changes that accompany forest clearanceig;
thus, deforestation may have less impact in the Atlantic forests than elsewhere.
However, in this case, the evidence for disproportionate resilience is equivocal. Species-area relationships do
not predict immediate disappearance, but rather the eventual loss of species as communities adjust (potentially over
lengthy period+24) to reductions in habitat area2Q6. A detailed analysis of threatened (as opposed to extinct) Atlantic
forest birds in relation to deforestation patterns shows that,
in practice, the species-area relationship predicts quite
accurately the number and distribution of endemic species
already in serious danger of extinction through habitat
10s~~The
.
apparent mismatch between theory and the real
world is therefore illusory - Atlantic forest species may be
no more resilient than those elsewhere.
as an extinction filter
Homo sapiens
Our growing awareness of the scale of extinctions caused
by prehistoric humans raises the possibility that, as well as
climatic and biotic factors, humans themselves may have SC
lectively purged naive biotas of particularly vulnerable species. A likely example comes from the long-settled island of
Java, where, in contrast to other parts of the Greater Sundass,
predictions of species loss based on the extent of deforestation overestimate the number of forest endemics threatened with extinction42. One answer for this is simply that the
list of threatened birds is incomplete27. However, Java is also
unusual in possessing a markedly depauperate avifauna at
altitudes of 300-1500m (Ref. 28), suggesting that its apparent shortage of currently threatened birds may instead arise
because historical forest clearance purged the island of many
of its more vulnerable species long ago.
Fresh quantitative support for the notion that intensive
human activity acts as a major extinction filter is provided
by a new analysis of plant extinctions across four Mediterranean regions29. This reveals that the extent of recent extinctions (measured as a proportion of the known flora) is
lowest in the longest-settled, most disturbed area (the Mediterranean proper), higher in the Cape region of South Africa
and in California, and highest in Western Australia (Fig. 3a).
The obvious solution to this apparent paradox again lies in
the idea of unrecorded, human-induced loss. If most anthropogenic extinctions occur relatively soon after the onset of
intensive human settlement, then this initial wave of species
loss would have gone largely unnoticed around the Mediterranean and, to a lesser extent, in the Cape and California;
only relatively resilient species would have been left to be
recorded by science, and to face present-day challenges. In
contrast, in Western Australia, visits by botanists generally
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preceded permanent European settlement, so that science
has been able to document large numbers of human-caused
extinctions. A corollary of this interpretation, of course, is
that in long-settled areas, cryptic losses that occurred before
species were recorded are likely to have been disturbingly
high.
But for the most convincing evidence of the purging of
vulnerable species by early human settlement, one must return to the islands of the Pacific. There, the proportion of recent bird species that are extinct or endangered decreases
as time since colonization increases30 (Fig. 3b). As in Mediterranean regions, the impact of people thus appears superficially greatest in the most recently occupied areas. The
implication once again is that places with long histories of
human settlement have already lost most of their humansensitive species. In the Pacific, however, this cryptic loss
hypothesis is buttressed by additional arguments30. On the
one hand, the distribution of described species (including
those known only from fossils) contradicts simple biogeographic principles, with more birds recorded from small isolated islands than from larger islands nearer to potential
sources of colonists. This anomaly could of course be explained if unrecorded losses occurred predominantly on
earlier-settled, more-accessible islands. Second, clever reworking of the familiar mark-recapture method provides
quantitative evidence that many Holocene birds must have
gone extinct without leaving skins or fossils. Indeed, Pimm
and colleagues suggest that on certain islands of the western
Pacific, cryptic losses of vulnerable species may even exceed
the number of species already known from fossils and living
birds. All three lines of evidence provide independent support for current archaeological estimates of the magnitude
and timing of human-induced extinctions in the PacificzJ.
Conservation implications
The idea that climatic, ecological or anthropogenic challenges have already filtered out many of the species that
would be most susceptible to todays threats has several
important implications for conservation biologists.
First, if the evidence from the Pacific, the Mediterranean
and the Greater Sundas on the magnitude of cryptic, humancaused loss is correct, then currently-cited figures for overall levels of anthropogenic extinction are clearly gross
underestimates (see also Ref. 31). It seems likely that longterm human-induced filtering of vulnerable taxa has gone on
elsewhere as well. Indeed, this may provide an additional
explanation (alongside the importance of large species
ranges) for the apparent lack of extinctions following extensive habitat clearance in Europe and North ArnericasJ2.
A second, related point deals with the unresolved yet
crucial question of what species do in ecosystems33J4. Evidence that some areas may have already lost as many as
half their recent species highlights the scope for palaeoecological studies into the effects (if any) that these dramatic reductions in biodiversity have had on ecosystem
stability and function.
Third, the concept of filtering and resulting variation in
the susceptibility of biotas to current ,threats raises an important issue for conservation practice. Initial exposure to
novel anthropogenic challenges can evidently cause the
geologically and even ecologically rapid extinction of large
numbers of species2JJr (for instance, see Fig. 1). This adds
to the controversial suggestion that the current emphasis on
fire-fighting in areas where threats are already extensive
should be reviewed, and that efforts should be partly redirected towards potentially more-rewarding pre-emptive
conservation action in relatively untouched and therefore
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vulnerable areas (see Box 1). For island birds, attempts are
already under way to catalogue priority sites that are still
free from introduced rodentss. The identification of other
biologically rich assemblages that have been exposed to
only moderate levels of habitat loss or other threats may be
equally valuable.
Fourth, even where current threats are broadly similar
to those of the recent past, there are no grounds for complacency. Contemporary challenges may often be subtly but
critically different from historical ones. Perhaps more worryingly, even where threats are identical, humans may have
radically altered the capacity of previously resilient species
to cope with future challengessr. For instance, although temperate insects survived climatic upheavals during the
Quaternary by shifting their ranges, modern-day fragmentation of remaining habitats may preclude similar range
shifts during future climatic change@.
Finally, as well as the sorts of historical pressures considered here, many other past selective agents have doubtless had effects on patterns of contemporary vulnerability.
For instance, there is growing evidence that species with
naturally scarce, fluctuating or isolated populations are less
susceptible than other taxa to the demographic and genetic
problems of reduced population size38-40.Awareness of

Increasing

length of intensive

human

occupancy

??
0

0
0
0
I

2000

3000

Length of human

4000
occupancy

5000

(yr)

flg. 3. Indirect evidence that the early phases of intensive human settlement purge
biotas of vulnerable species. (a) Across Mediterranean regions, the percentage of
described species that have gone extinct decreases with the time since the arrival
of European agriculture. Data from Ref. 29. This suggests that in longer-settled
areas, large-scale extinction preceded scientific description. (b) The same pattern,
this time looking across Pacific islands at the percentage of recent bird species
that are known to be extinct or endangered. Redrawn, with permission, from Ref. 30.

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13 Haas, CA. and Fraser, J.D. (1995) Grazing and advocacy, Conserv.
Biol. 9, 234-235

Box 1. Fktinction filters and spatial priorities

for conservation

The scale of contemporary species loss underlines the need to direct conservation
efforts towards entire communities rather than single species. Key criteria for iden
tidying area-based priorities for action include both the biological importance of
a site, and its current level of threat (i.e. what will happen to it if it is not actively
conserved)35,36.

14 Fleischner, T.L. (1995)GrazJng and advocacy, Conserv.Biol. 9,233-234

15 Ness, R. (1995) Grazing and advocacy, Conserv. Biol. 9,235
16 Moors, P.J., Atkinson, I.A.E.and Sherley, G.H. (1992) Reducing the
rat threat to island birds, Bird Consetz. Int. 2,93-l 14
17 Milberg, P. and Tyrberg, T. (1993) Ntive birds and noble savages a review of man-caused prehistoric extinctions of island birds,
Ecography

Low

High

Biological importance of area

Highest priority is generally attached to those areas characterized by both high
value and high threat (sector I in the figure), but evidence that initial exposure to a
new challenge can cause rapid species loss suggests that emphasis should also be
placed on identifying and conserving sites that are characterized by high value but
currently low levels of threat (sector Ill). As well as perhaps being relatively cheap
to conserve at present (because they may not yet be subject to high levels of exploitation), such naive but rich areas may be the only sites where large numbers
of particularly sensitive species can be retained.

these and other potential determinants of present-day vulnerability could play a pivotal role in guiding conservation
efforts towards those species and communities most at risk
from ongoing human activity.
Acknowledgements
This review was inspired in large part by papers given at
the 1993 Royal Society Discussion Meeting on Estimating
Extinction Rates. I thank Steve Albon, Bas van Balen,
Mike Brooke, Tom Brooks, Nigel Collar, Josh Ginsberg,
Adrian Long and Georgina Mace for thought-provoking
discussions and helpful comments on the manuscript.

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