Journal of Biogeography (J. Biogeogr.

) (2014) 41, 421–428

GUEST Can biodiversity hotspots protect

EDITORIAL more than tropical forest plants
and vertebrates?
Nigel E. Stork1* and Jan Christian Habel2

1
Environmental Futures Centre, Griffith
School of Environment, Griffith University,
Nathan, QLD 4111, Australia, 2Department
of Ecology and Ecosystem Management,
Technische Universit€at M€
unchen, D-85350,
Freising-Weihenstephan, Germany
*Correspondence: Nigel E. Stork,
Environmental Futures Centre, Griffith School
of Environment, Griffith University, 170
Kessels Rd, Nathan, QLD 4111, Australia.
E-mail: nigel.stork@griffith.edu.au
ABSTRACT
Conservation International’s biodiversity hotspots are areas of high vascular
plant endemism combined with high levels of habitat destruction and land use
change. Although such hotspots have also been shown to be centres for terres-
trial vertebrate endemism, much less is known about how well these areas
function as hotspots for other less well-studied groups, including the hyperdi-
verse arthropods, other invertebrates and fungi. Because there is a close evolu-
tionary and ecological relationship between insects and plants, we suggest that
the potential role of plants as umbrella species for herbivorous insects, poten-
tially herbivorous fungi and nematodes, and parasitic insects should be
explored. Finally, we reflect on the increasing social, economic, human conflict
and governance issues and the impacts of increasing land use change and glo-
bal climate change that threaten the biodiversity hotspot system.
Keywords
Conservation biogeography, Conservation International’s hotspots, endemic
species, global change, invertebrate diversity, plant diversity, species richness,
strategic conservation planning, umbrella species.

THE CONCEPT
Why biodiversity is not homogenously distributed across the
globe, but is concentrated in specific geographical areas, has
fascinated biologists for centuries and has been the inspira-
tion for key ecological and evolutionary theories (Darwin,
1859; Wallace, 1860; Briggs, 1987; Gaston, 2000). In the early
1980s attention was drawn to the loss of biodiversity result-
ing from increasing deforestation of tropical forests (Lovejoy,
1980; Ehrlich & Ehrlich, 1981; Myers, 1988a; Wilson & Peter,
1988). The importance of such losses was heightened first by
the recognition that some of the main centres for deforesta-
tion were also centres for high plant and animal species rich-
ness and endemism (Davies et al., 1986), and second by new
estimates of global species richness which suggested that
there were many more undescribed species than had previ-
ously been considered (Erwin, 1982). Myers (1988b), in first
defining the hotspot concept, identified 10 tropical forest
areas as key hotspots with high diversity, endemism and
threat from deforestation. He suggested that concentrating
resources to protect these areas would lead to the greatest
benefit in conserving biodiversity. Myers et al. (2000) later
refined the concept, defining a biodiversity hotspot as a
restricted area that must contain 1500 endemic plant species
and has already lost at least 70% of its former natural vegeta-
tion cover through land use change. The hotspot list has
now increased to 35, with these areas recognized as including
77% of all endemic plant species, 43% of vertebrates (includ-
ing 60% of threatened mammals and birds), and 80% of all
threatened amphibians (Mittermeier et al., 2004, 2007, 2011;
Williams et al., 2011).
The conservation of biodiversity hotspots sensu Mitterme-
ier et al. (2004), also called ‘CI biodiversity hotspots’, is a
key element of the baseline conservation strategy for Conser-
vation International. Because it focuses on endemic species it
inherently incorporates the key concept of complementarity
(Ladle & Whittaker, 2011) and has also become a key con-
servation strategy for many other organizations (e.g. the
MacArthur Foundation, the Gordon and Betty Moore Foun-
dation, the Global Environmental Facility, and the World
Bank), with more than US$1 billion being invested to sup-
port it.
Some have warned that the biodiversity hotspots approach
is not a cure-all strategy for the conservation of biodiversity
(Jepson & Canney, 2001) and have placed it in the context
of several other global strategies (Brooks et al., 2006; Jepson
et al., 2011; Rodrigues, 2013). In this review we question
how applicable the biodiversity hotspot concept may be for

ª 2013 John Wiley & Sons Ltd http://wileyonlinelibrary.com/journal/jbi 421

doi:10.1111/jbi.12223
N. E. Stork and J. C. Habel
protecting global biodiversity in its widest sense when plants
and vertebrates comprise only a small proportion of all spe-
cies. We provide ideas on how this global conservation strat-
egy may be an umbrella for a large part of the greater variety
of life. We focus particularly on insects but suggest that the
principles we use might apply to other terrestrial inverte-
brates and fungi. Finally, we examine how a range of anthro-
pogenic factors are threatening the survival of biodiversity
hotspots.
TAXON BIAS
The taxonomy of plants is comparatively well explored and
therefore sensibly used as a basis for delineating biodiversity
hotspots. However, they, along with vertebrates, comprise
less than 6–8% of global diversity (Hamilton et al., 2010,
2011; Mora et al., 2011). Arguably, there are some 5  3
million species on Earth (Costello & Wilson, 2011; Hamilton
et al., 2011, 2012; Costello et al., 2013), with arthropods
comprising the majority of species. Other invertebrates, such
as nematodes, and fungi also contribute an additional large
proportion of the total but they, along with arthropods, are
ignored in many comparative conservation analyses, largely
because 80–95% of species are unknown to science or are
taxonomically intractable.
Plants have been used as the focal taxa for hotspots because
their distribution is relatively easily measurable by comparison
to many other taxa and not necessarily because they deserve
protection and conservation more than other taxa. Here we
ask whether a strategy based on a minority of taxa might also
serve to conserve and protect the majority of the world’s bio-
diversity. We are not the first to pose this question. For exam-
ple, Prendergast et al. (1993, p. 336) commented: ‘a strategy
based … on a limited number of taxa, may fail to provide ade-
quate protection for many other organisms’. Insects, other
invertebrates and fungi form the majority of species on Earth
and we argue that these deserve consideration and protection
as much as other more charismatic taxa because of the unique
contributions they make to the functioning of ecosystems, rep-
resentation of the evolutionary past, and the future evolution-
ary potential of the world’s biota. Insects and other
arthropods play essential roles in key processes such as herbiv-
ory, pollination, seed dispersal, predation and decomposition
(e.g. Weisser & Siemann, 2007). Since the Cretaceous, the
extraordinary co-evolution of insects and flowering plants has
given rise to a large part of today’s biodiversity and the sur-
vival of many vascular plants depends on their pollinators and
seed dispersers. Herbivory is suggested as one of the key mech-
anisms promoting plant coexistence and diversity, especially
in tropical forests (Lubchenko, 1978; Viola et al., 2010), and
the vast majority of tropical trees are pollinated by insects
(Bawa, 1990). Despite their small size, many arthropods and
fungi are recognized as ecosystem engineers and keystone spe-
cies, and play key roles in communities (Smith et al., 1991; Lill
& Marquis, 2003; Buse et al., 2008; Collier & Bidartondo,
2009).
422
These facts highlight the irreplaceability of these poorly
studied taxa, but are these organisms as threatened with
extinction as plants and vertebrates and therefore of concern
for conservationists? The answer is that we are not sure. For
the best-known biota in the world, that of the UK, the evi-
dence is equivocal, with some suggesting that the decline of
insects may be greater than or equal to that of vascular
plants or birds (Thomas et al., 2004; Hambler et al., 2011)
and others suggesting that birds and mammals are on aver-
age seven times more likely to be threatened with extinction
than invertebrates (Mawdsley & Stork, 1995). McKinney
(1999) concluded that in the USA some, but not all, insects
and other invertebrates are more threatened than many ver-
tebrates and plants. Of direct relevance to this essay, Fonseca
(2009) estimated that roughly a third of insect species in bio-
diversity hotspots may be committed to extinction because
of past reductions in the geographical range size of their
endemic host plants. Fonseca argued that if the 150,371
endemic plant species in CI’s biodiversity hotspots had an
average of roughly 5.3–10.6 monophagous insect species per
plant species, this would mean that there were 795,971–
1,602,423 monophagous insect species in these biodiversity
hotspots. In light of these studies, we should assume that at
least some invertebrate groups, and probably some fungi, are
as threatened as some vertebrates and plants. It would also
be prudent to consider how well the biodiversity hotspots
strategy protects them.
ARE PLANTS SUITABLE SURROGATES
FOR INSECTS AND OTHER BIODIVERSITY?
Because CI’s biodiversity hotspots are in large part defined
by endemic plant species richness, we should question
whether endemic plants are good surrogates for endemic
insects and other biodiversity and whether their protection
will provide protection for other biodiversity. There is an
extensive literature examining the close relationship between
herbivorous insects and plants (e.g. Southwood, 1961; Ehr-
lich & Raven, 1964; Lewinsohn et al., 2005). Most species of
herbivorous insects show a strong association with a group
of closely related host plant species or single host plant spe-
cies and these are reflected in close co-evolutionary phyloge-
nies for the plants and insects (Novotny et al., 2002). For
example, recent phylogenetic analysis of Australian chryso-
melid beetles shows general conservation of host association
with Australian plants, with host shifts between distant plant
lineages occurring only rarely (Jurado-Rivera et al., 2009).
This close co-evolutionary link between many insects and
plants has led to the suggestion that the loss of some plant
species will lead to the co-extinction of their host-dependent
insect species (Stork & Lyal, 1993; Fonseca, 2009; Moir et al.,
2010; Colwell et al., 2012).
Implicit in Erwin’s (1982) estimation of 30 million species
of insects on Earth was his assumption that 84% of all
insects are host-specific herbivores. Recent recalculations of
global species richness suggest much lower numbers of insect
Journal of Biogeography 41, 421–428
ª 2013 John Wiley & Sons Ltd

species specific to trees and other plants and hence a lower
proportion of perhaps 25–40% of all insects being herbivores
(e.g. Hamilton et al., 2010, 2011). In addition, a large pro-
portion of both nematodes and fungi are plant-feeding and
tied closely to plant species but as yet their host-specificity is
still largely unknown. As many parasitic insects are tightly
bound to host insect species then this might also be generally
true for a large component of this trophic group (Smith
et al., 2008). If parasitic insects comprise perhaps 15–30% of
global insects (LaSalle & Gauld, 1992) then, when combined
with herbivores, this would suggest that roughly 40–70% of
insect species are linked to particular plant species. The spe-
cies richness of other trophic levels has been shown to be
influenced by plant species richness, with this influence
declining with increasing trophic level (Scherber et al., 2010).
Hence, one would predict less tenuous links with plants for
groups such as predators and for those organisms involved
in decomposition. Current evidence would suggest that such
links between plants and below-ground microbial diversity
are more tenuous (De Deyn & Van der Putten, 2005).
If such a large proportion of invertebrates and possibly
fungi is linked to particular plant species how well might
plants or even other taxa act as surrogates for these groups?
There are few studies that directly examine the potential sur-
rogacy of plants for insects, but recently Basset et al. (2012)
found that models based on plant diversity fitted the accu-
mulated species richness of both herbivore and non-herbi-
vore insects in Panama tropical rain forest exceptionally well.
Given that this study reported one of the most extensive
insect surveys ever carried out, this finding is important.
Elsewhere a weak but positive power of surrogacy was
observed in a review of the effectiveness of cross-taxon sur-
rogacy based on complementarity using data for a wide
range of taxa from 27 studies from across the world (Rodri-
gues & Brooks, 2007).
Two further studies, one from a tropical forest hotspot
and one from Europe, are discussed here to demonstrate
some of the confounding issues in examining surrogacy and
in particular the use of non-herbivorous insect groups in
preference to herbivores. Both studies also show the impor-
tance of past history in determining current distribution pat-
terns. First, Moritz et al. (2001) found that endemism and
species richness varies significantly between amphibians,
birds, mammals and selected groups of invertebrates across
the Wet Tropic rain forests in North Queensland, Australia,
suggesting that these groups do not necessarily act as a sur-
rogate for the others (Williams et al., 1996; Moritz et al.,
2001). However, plants were not examined and the relatively
small groups of insects they selected (330 endemic species,
mostly flightless) included no herbivores, comprising mostly
flightless predatory Carabidae, dung-feeding Scarabaeidae
and fungus feeding aradid bugs. The distribution of the taxa
studied, including vertebrates, appears to be the result of past
Pleistocene climates with many of the endemic vertebrates
and invertebrates being cool-adapted species trapped on the
tops of isolated mountain blocks (Moritz et al., 2001).
Journal of Biogeography 41, 421–428
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Biodiversity hotspots under review
Second, a much larger-scale study compared species rich-
ness and endemism of a wide range of invertebrate (spiders,
springtails, mayflies, dragonflies, stoneflies, aphids, ants, caddis-
flies, butterflies, mosquitoes, ground-beetles, longhorn beetles),
with those for vertebrates and plants in Europe (Schuldt &
Assmann, 2010). Unlike the Wet Tropics study, the European
data show a strong latitudinal gradient in species richness for
all groups, with centres of high diversity and endemism for
plants, vertebrates and many of the insect taxa, reflecting
strong temperature gradients. The distributions of species in
Europe have been greatly affected by Pleistocene glacia-
tions and the hotspots are recognized as major glacial refugia
(Hewitt, 1999; Taberlet & Cheddadi, 2002). Once again, the
selection of taxa determines the patterns observed with only
three of twelve invertebrates groups selected being herbivores.
Patterns of endemism for butterflies are very similar to those
for plants, and those for longhorn beetles slightly less so, lend-
ing support for our arguments. Aphids, the third group, is
one of the few groups of herbivores that are most rich in cool
temperate parts of the world and hence patterns of endemism
for this group do not coincide so well with that for plants. For
some invertebrate groups that are less obviously tied to plant
diversity, their species richness is often influenced more by
ecosystem structure and their low vagility than by the total
number of plant species (e.g. ants, ground beetles and tiger
beetles; Pearson & Carroll, 1998; Baselga, 2008; Hortal et al.,
2008; Schuldt et al., 2009; Schuldt & Assmann, 2010).
Selecting the right taxa for comparisons of patterns of spe-
cies richness, endemism and surrogacy is therefore crucial.
Both the Australian and European studies show the impor-
tance of past climates for understanding the current distribu-
tions of species and how this may impact on species that are
closely tied to each other, such as herbivorous insects and
plants (cf. Wiens & Donoghue, 2004). A further potential
issue is in comparative studies in which groups of trophically
different organisms are lumped together in analyses. For
example, in a study comparing the species richness of differ-
ent taxa in forest treatments from primary forest through to
complete clearance, it was shown that the species richness of
very few taxa were correlated (Lawton et al., 1998). In large
part this is because some of the taxa studied, such as beetles
sampled from the canopy or from the ground and soil-dwelling
nematodes, each represent a range of trophically different
species. No one would lump all vertebrates together (includ-
ing fish) and expect the species richness of this group to cor-
relate with all plants! A further issue still is the spatial scale
of observation. Reid (1998) showed that at larger geographi-
cal or taxonomic scales (globally rather than locally, and
family based rather than species based) there is greater
congruency for hotspots than on a regional scale where the
environment is much more heterogeneous. However, conser-
vation action takes place locally and congruence at the global
level may be less relevant if there are strong discongruencies
at the landscape level.
We conclude that it is reasonable to suggest that the con-
servation and protection of more than half of the world’s
423
N. E. Stork and J. C. Habel
endemic plants within hotspots might also provide an
umbrella for the protection of a large proportion of the
world’s herbivorous insects, nematodes and fungi plus a large
proportion of their parasites. We suggest that this might be
worthwhile testing for those groups of herbivorous insects
where there are good empirical biogeographical data. These
groups might include butterflies, cicadas, sphingid moths,
psyllid bugs and possibly some groups of parasitic Hyme-
noptera and Diptera. Botanists lead the world in establishing
study plots that can be compared for taxonomic composition
as well as studies of changing structure and biomass, and
many of these large-scale plots (20–50 hectares) are in some
of CI’s biodiversity hotspots (Condit, 1995). In a new initia-
tive that might serve as an example of what needs to be
done, Basset and colleagues, building on their successful
study of a single location in Panama (Basset et al., 2012), are
now establishing comparative in-depth inventories of insects
in many of these plots. They have provided a preliminary
example of how this might work in a comparison of the but-
terfly fauna of sites in three different biogeographical regions
(Basset et al., 2011).
BIODIVERSITY HOTSPOTS UNDER GLOBAL
CHANGE
Whilst biodiversity hotspots are important for the protection
of biodiversity, these areas are also under extreme threat
from anthropogenic pressures. Human population density
and growth rates are exceptionally high in hotspots and
hence the biodiversity of these areas is likely to be more
threatened than in other areas (Cincotta et al., 2000).
Approximately 20% of the world’s human population lives
within biodiversity hotspots and mean human population
growth rate is higher in these areas (1.8%) than for develop-
ing countries (1.6%) or industrial countries (1.3%) (Cincotta
et al., 2000). In addition, high population density in biodi-
versity hotspots has invariably led to rising poverty (Fisher &
Christopher, 2007) and increased conflicts (Balmford et al.,
2001; Hanson et al., 2009). Around 90% of all armed con-
flicts between 1950 and 2000 have taken place in countries
with biodiversity hotspots, and two-thirds of the hotspot
ecosystems have suffered severely from problems arising from
these (armed) conflicts such as managing refugees or an
increase in the bush-meat trade due to lack of food (Hanson
et al., 2009). In most hotspots factors such as human popu-
lation size, rural population density, population growth rate
and government debt are highly problematic. As a conse-
quence, poverty and conservation cannot be considered as if
they are two separate policy realms (O’Connor et al., 2003;
Veech, 2003). In addition, species-rich countries with prior-
ity areas for conservation have lower governance scores than
other nations, and higher levels of corruption that may nega-
tively impact conservation activities (Smith et al., 2003). To
link the level of governance (e.g. corruption) with the deteri-
oration of natural resources (e.g. biodiversity) seems to sim-
plify the socio-political complexity, as highlighted by Barrett
424
et al. (2006), who point out two major problems in postulat-
ing such congruencies: corruption comes in many forms, at
multiple levels, and may or may not affect resources, and it
is difficult to account for other important causes and control
variables pivotal to the relationship between humans and
natural resources. Nevertheless, a rising human development
index, which measures income, health and education, is fre-
quently accompanied by declining population growth and
reduced deforestation. Here, two drivers are of high impor-
tance: policy choices and human-development constraints.
Importantly, environmental education in biodiversity hotspot
areas has helped to develop communities at the same time as
protecting ecosystems of high value (Jha & Bawa, 2006).
Biodiversity hotspots are dynamic on historical biogeo-
graphical scales (Renema et al., 2008) as well as on shorter
temporal scales where anthropogenic activities accelerate the
rate of change (Brook et al., 2008; Beaumont et al., 2011). In
the geological past, climate change has caused major changes
in the distribution and diversity of some hotspots. For exam-
ple, the former marine Tethyan hotspot shifted due to
changing climatic conditions over the globe over millions of
years and can be found today in the so-called Coral Triangle
(Indonesia, Malaysia, the Philippines, Timor Leste, New Gui-
nea and the Solomon Islands) with the highest marine spe-
cies richness world-wide (Renema et al., 2008). However,
today biodiversity is affected by changes within very short
time periods. Hannah et al. (2002), for example, project that
by 2050 the Fynbos biome in the Cape Floristic Province
hotspot will decline by more than half and hence might lose
about 10% of endemic Proteaceae species from that area.
Other studies showed that global warming might cause the
extinctions of more than one out of ten of all endemic spe-
cies living in biodiversity hotspots (Malcolm et al., 2006)
and possibly much more (Colwell et al., 2008; Wright et al.,
2009). Malcolm et al. (2006) modelled climate change
impacts on major vegetation types within biomes and
showed that a doubling of atmospheric CO2 may result in
elevated extinction rates for endemic biota living in hotspots
of between < 1% and 43% (on average 11.6%) over the next
100 years. In their scenarios, extremely vulnerable hotspots
were the Cape Floristic Region, Mediterranean Basin, South-
west Australia and Tropical Andes, but also the Caribbean
and Indo-Burma, where projected plant extinctions per hot-
spot sometimes exceeded 2000 species.
Endemic species are often more strongly adapted to spe-
cific habitat conditions (Wiens & Donoghue, 2004) than are
more widespread species, which might have fatal conse-
quences if their habitat conditions change rapidly, as in cli-
mate change. Such fast changes in climatic conditions might
further have severe consequences for food-webs and can lead
to the reorganization of species communities and finally to a
complete loss of those taxa dependent on host animals and
plant species. Thus, the creation of geographically rather
restricted protected areas, covering only a proportion of the
core of a biodiversity hotspot may fail to conserve shifting
biota. Others have suggested that this conservation challenge
Journal of Biogeography 41, 421–428
ª 2013 John Wiley & Sons Ltd

might be addressed by the recognition of buffer and transi-
tion zones which may compensate such temporal dynamics,
as highlighted on a regional scale (Grant & Samways, 2011)
and as already partially realized by the PARCC (Protected
Areas Resilient to Climate Change) initiative and by UNEP
(United Nations Environmental Programme). Modelling dif-
ferent future scenarios and recent environmental require-
ments of species (e.g. Parviainen et al., 2009) may help to
identify future spatial shifts of biodiversity hotspots (e.g. Jen-
kins et al., 2010).
CONCLUSIONS
The CI biodiversity hotspot strategy focuses on the conserva-
tion of endemic vascular plant and terrestrial vertebrates in
areas of the world that are undergoing high levels of land use
change. Here we have highlighted the neglected role of inverte-
brates in decision making about global biodiversity hotspots,
but suggest that the co-evolution of plants and herbivorous
insects (and possibly herbivorous fungi and nematodes) might
lend support to the notion that conservation of plant species
may act as an umbrella for these herbivorous organisms. Fur-
ther, plants may act as surrogates for other trophic level groups
such as parasitic insects. We suggest that this be tested by look-
ing at whether centres of plant species richness and endemism
coincide with those for insects and other organisms.
The sensitivity of arthropods to species extinction, their
importance for species interactions and their roles in ecosys-
tem functioning lend weight to our argument that inverte-
brates need to be considered in future global conservation
strategies. Major challenges in achieving these goal, amongst
other things (see Cardoso et al., 2011) are the so-called Lin-
nean and Wallacean shortfalls (the lack of knowledge about
the major proportion of most taxa and their distribution,
respectively), which have resulted in our current focus largely
on vertebrates and plants. Costello et al. (2013) suggest that,
contrary to current thinking, there are now more taxono-
mists than in previous decades and that the goal of describ-
ing and naming most species on Earth is achievable. The
challenge for groups such as invertebrates and fungi, is to
collate and better use available data for conservation plan-
ning, at least for some of the better know taxa, and to fill
important knowledge gaps. New online tools are also helping
to overcome the Linnean/Wallacean shortfall (Guralnick
et al., 2007). We conclude with a warning that the future of
biodiversity hotspots is dependent on marrying conservation
goals with those of their human populations who are socially
and economically challenged. How well hotspots and the
unique biodiversity they contain can withstand these anthro-
pogenic threats is yet to be determined.
ACKNOWLEDGEMENTS
This paper resulted from a conference on biodiversity hot-
spots, held at the MNHN Luxembourg from 26 to 28
March 2009 (http://www.symposium.lu/hotspots) and
Journal of Biogeography 41, 421–428
ª 2013 John Wiley & Sons Ltd
Biodiversity hotspots under review
funded by the National Research Fund of Luxembourg
(FNR). J.C.H. acknowledges a postdoctoral grant by the
German Academic Exchange Service (DAAD). We thank
Thomas Brooks, Louise Ashton, Sarah Maunsell, Sean
Sloan, Aki Nakamura and three anonymous referees for
constructive comments on earlier draft version of this
article.
REFERENCES
Balmford, A., Moore, J.L., Brooks, T., Burgess, N., Hansen,
L.A., Williams, P. & Rahbek, C. (2001) Conservation con-
flicts across Africa. Science, 291, 2616–2619.
Barrett, C.B., Gibson, C.C., Hoffman, B. & McCubbins, M.D.
(2006) The complex links between governance and biodi-
versity. Conservation Biology, 20, 1358–1366.
Baselga, A. (2008) Determinants of species richness, ende-
mism and turnover in European longhorn beetles. Ecogra-
phy, 31, 263–271.
Basset, Y., Eastwood, R., Sam, L., Lohman, D., Novotny, V.,
Treuer, T., Miller, S., Weiblen, G., Pierce, N. & Bunyavej-
chewin, S. (2011) Comparison of rainforest butterfly
assemblages across three biogeographical regions using
standardized protocols. The Journal of Research on the Lep-
idoptera, 44, 17–28.
Basset, Y., Cizek, L., Cuenoud, P. et al. (2012) Arthropod
diversity in a tropical forest. Science, 338, 1481–1484.
Bawa, K.S. (1990) Plant-pollinator interactions in tropical
rain forests. Annual Review of Ecology and Systematics, 21,
399–422.
Beaumont, L.J., Pitman, A., Perkins, S., Zimmermann, N.E.,
Yoccoz, N.G. & Thuiller, W. (2011) Impacts of climate change
on the world’s most exceptional ecoregions. Proceedings of the
National Academy of Sciences USA, 108, 2306–2311.
Briggs, J.C. (1987) Biogeography and plate tectonics. Elsevier,
Amsterdam.
Brook, B.W., Sodhi, N.S. & Bradshaw, C.J.A. (2008) Syner-
gies among extinction drivers under global change. Trends
in Ecology and Evolution, 23, 453–460.
Brooks, T.M., Mittermeier, R.A., da Fonseca, G.A.B., Gerlach,
J., Hoffmann, M., Lamoreux, J.F., Mittermeier, C.G.,
Pilgrim, J.D. & Rodrigues, A.S.L. (2006) Global biodiversity
conservation priorities. Science, 313, 58–61.
Buse, J., Ranius, T. & Assmann, T. (2008) An endangered
longhorn beetle associated with old oaks and its possible
role as an ecosystem engineer. Conservation Biology, 22,
329–337.
Cardoso, P., Erwin, T.L., Borges, P.A.V. & New, T.R. (2011)
The seven impediments in invertebrate conservation and
how to overcome them. Biological Conservation, 144,
2647–2655.
Cincotta, R.P., Wisnewski, J. & Engelman, R. (2000) Human
population in the biodiversity hotspots. Nature, 404, 990–992.
Collier, F.A. & Bidartondo, M.I. (2009) Waiting for fungi:
the ectomycorrhizal invasion of lowland heathlands. Jour-
nal of Ecology, 97, 950–963.
425
N. E. Stork and J. C. Habel
Colwell, R.K., Brehm, G., Cardelus, C.L., Gilman, A.C. &
Longino, J.T. (2008) Global warming, elevational range
shifts, and lowland biotic attrition in the wet tropics. Sci-
ence, 322, 258–261.
Colwell, R.K., Dunn, R.R. & Harris, N.C. (2012) Coextinc-
tion and persistence of dependent species in a changing
world. Annual Review of Ecology, Evolution, and Systemat-
ics, 43, 183–203.
Condit, R. (1995) Research in large, long-term tropical forest
plots. Trends in Ecology and Evolution, 10, 18–22.
Costello, M.J. & Wilson, S.P. (2011) Predicting the number
of known and unknown species in European seas using
rates of description. Global Ecology and Biogeography, 20,
319–330.
Costello, M.J., May, R.M. & Stork, N.E. (2013) Can we name
Earth’s species before they go extinct? Science, 339, 413–
416.
Darwin, C.S. (1859) On the origin of species by means of nat-
ural selection, or the preservation of favoured races in the
struggle for life. John Murray, London.
Davies, S., Droop, S., Gregerson, P., Henson, L., Leon, C.,
Villa-Lobos, J., Synge, H. & Zantovska, I. (1986) Plants in
danger. International Union of the Conservation of Nat-
ure, Gland, Switzerland.
De Deyn, G.B. & Van der Putten, W.H. (2005) Linking
aboveground and belowground diversity. Trends in Ecology
and Evolution, 20, 625–633.
Ehrlich, P.R. & Ehrlich, A.H. (1981) Extinction: the causes
and consequences of the disappearance of species. Random
House, New York.
Ehrlich, P.R. & Raven, P.H. (1964) Butterflies and plants: a
study in coevolution. Evolution, 18, 586–608.
Erwin, T.L. (1982) Tropical forests: their richness in Coleop-
tera and other arthropod species. The Coleopterists Bulletin,
36, 74–75.
Fisher, B. & Christopher, T. (2007) Poverty and biodiversity:
measuring the overlap of human poverty and the biodiver-
sity hotspots. Ecological Economics, 62, 93–101.
Fonseca, C.R. (2009) The silent mass extinction of insect her-
bivores in biodiversity hotspots. Conservation Biology, 23,
1507–1515.
Gaston, K.J. (2000) Global patterns in biodiversity. Nature,
405, 220–227.
Grant, P.B.C. & Samways, M.J. (2011) Micro-hotspot deter-
mination and buffer zone value for Odonata in a globally
significant biosphere reserve. Biological Conservation, 144,
772–781.
Guralnick, R.P., Hill, A.W. & Lane, M. (2007) Towards a
collaborative, global infrastructure for biodiversity assess-
ment. Ecology Letters, 10, 663–672.
Hambler, C., Henderson, P.A. & Speight, M.R. (2011)
Extinction rates, extinction-prone habitats, and indicator
groups in Britain and at larger scales. Biological Conserva-
tion, 144, 713–721.
Hamilton, A.J., Basset, Y., Benke, K.K., Grimbacher, P.S.,
Miller, S.E., Novotny, V., Samuelson, G.A., Stork, N.E.,
426
Weiblen, G.D. & Yen, J.D.L. (2010) Quantifying uncer-
tainty in estimation of tropical arthropod species richness.
The American Naturalist, 176, 90–95.
Hamilton, A.J., Basset, Y., Benke, K.K., Grimbacher, P.S.,
Miller, S.E., Novotny, V., Samuelson, G.A., Stork, N.E.,
Weiblen, G.D. & Yen, J.D.L. (2011) Correction. The Amer-
ican Naturalist, 177, 544–545.
Hamilton, A.J., Novotny , V., Waters, E.K., Basset, Y., Benke,
K.K., Grimbacher, P.S., Miller, S.E., Samuelson, G.A.,
Weiblen, G.D. & Yen, J.D.L. (2012) Estimating global
arthropod species richness: refining probabilistic models
using probability bounds analysis. Oecologia, 171, 357–365.
Hannah, L., Midgley, G.F., Lovejoy, T., Bond, W.J., Bush,
M., Lovett, J.C., Scott, D. & Woodward, F.I. (2002) Con-
servation of biodiversity in a changing climate. Conserva-
tion Biology, 16, 264–268.
Hanson, T., Brooks, T.M., da Fonseca, G.A., Hoffmann, M.,
Lamoreux, J.F., Machlis, G., Mittermeier, C.G., Mitterme-
ier, R.A. & Pilgrim, J.D. (2009) Warfare in biodiversity
hotspots. Conservation Biology, 23, 578–587.
Hewitt, G.M. (1999) Post-glacial re-colonization of European
biota. Biological Journal of the Linnean Society, 68, 87–112.
Hortal, J., Rodrıguez, J., Nieto-Dıaz, M. & Lobo, J.M. (2008)
Regional and environmental effects on the species richness
of mammal assemblages. Journal of Biogeography, 35,
1202–1214.
Jenkins, C.N., Alves, M.A.S. & Pimm, S.L. (2010) Avian con-
servation priorities in a top-ranked biodiversity hotspot.
Biological Conservation, 143, 992–998.
Jepson, P. & Canney, S. (2001) Biodiversity hotspots: hot for
what? Global Ecology and Biogeography, 10, 225–227.
Jepson, P., Whittaker, R.J. & Lourie, S.A. (2011) The shaping
of the global protected area estate. Conservation biogeogra-
phy (ed. by R.J. Ladle and R.J. Whittaker), pp. 93–135.
Wiley, Oxford.
Jha, S. & Bawa, K.S. (2006) Population growth, human
development, and deforestation in biodiversity hotspots.
Conservation Biology, 20, 906–912.
Jurado-Rivera, J.A., Vogler, A.P., Reid, C.A.M., Petitpierre,
E. & G omez-Zurita, J. (2009) DNA barcoding insect–host
plant associations. Proceedings of the Royal Society B: Bio-
logical Sciences, 276, 639–648.
Ladle, R.J. & Whittaker, R.J. (eds) (2011) Conservation bioge-
ography. Wiley, Oxford.
LaSalle, J. & Gauld, I.D. (1992) Parasitic Hymenoptera and
the biodiversity crisis. Redia, 74, 315–334.
Lawton, J.H., Bignell, D.E., Bolton, B., Bloemers, G.F., Eggle-
ton, P., Hammond, P.M., Hodda, M., Holt, R.D., Larsen,
T.B., Mawdsley, N.A., Stork, N.E., Srivastava, D.S. & Watt,
A.D. (1998) Biodiversity inventories, indicator taxa and
effects of habitat modification in tropical forest. Nature,
391, 72–76.
Lewinsohn, T.M., Novotny, V. & Basset, Y. (2005) Insects
on plants: diversity of herbivore assemblages revisited.
Annual Review of Ecology, Evolution, and Systematics, 36,
597–620.
Journal of Biogeography 41, 421–428
ª 2013 John Wiley & Sons Ltd

Lill, J.T. & Marquis, R.J. (2003) Ecosystem engineering by
caterpillars increases insect herbivore diversity on white
oak. Ecology, 84, 682–690.
Lovejoy, T.E. (1980) A projection of species extinctions. The
global 2000 report to the President, pp. 328–331. Penguin,
Washington, DC.
Lubchenko, J. (1978) Plant species diversity in a marine
intertidal community: importance of herbivore food pref-
erence and algal competitive abilities. The American Natu-
ralist, 112, 23–39.
Malcolm, J.R., Liu, C.R., Neilson, R.P., Hansen, L. & Han-
nah, L. (2006) Global warming and extinctions of endemic
species from biodiversity hotspots. Conservation Biology,
20, 538–548.
Mawdsley, N.A. & Stork, N.E. (1995) Species extinction in
insects: ecological and biogeographical considerations.
Insects in a changing environment (ed. by R. Harrington
and N.E. Stork), pp. 321–369. Academic Press, London.
McKinney, M.L. (1999) High rates of extinction and threat
in poorly studied taxa. Conservation Biology, 13, 1273–
1281.
Mittermeier, R.A., Robles Gil, P., Hoffmann, M., Pilgrim, J.,
Brooks, T., Mittermeier, C.G., Lamoreux, J. & da Fonseca,
G.A.B. (2004) Hotspots revisited: Earth’s biologically richest and
most endangered terrestrial ecoregions. CEMEX, Mexico City.
Mittermeier, R.A., Gascon, C., Rajaobelina, L., Supriatna, J.,
da Silva, J.M.C., Rodriguez, C.M., Zhi, L. & Brandon, K.
(2007) Global and local conservation priorities. Science,
318, 1378–1379.
Mittermeier, R.A., Turner, W.R., Larsen, F.W., Brooks, T.M. &
Gascon, C. (2011) Global biodiversity conservation: the criti-
cal role of hotspots. Biodiversity hotspots (ed. by F.E. Zachos
and J.C. Habel), pp. 3–22. Springer, Heidelberg, Germany.
Moir, M.L., Vesk, P.A., Brennan, K.E.C., Keith, D.A.,
Hughes, L. & McCarthy, M.A. (2010) Current constraints
and future directions in estimating coextinction. Conserva-
tion Biology, 24, 682–690.
Mora, C., Tittensor, D.P., Adl, S., Simpson, A.G.B. & Worm,
B. (2011) How many species are there on Earth and in the
ocean? PLoS Biology, 9, e1001127.
Moritz, C., Richardson, K.S., Ferrier, S., Monteith, G., Stani-
sic, J., Williams, S.E. & Whiffin, T. (2001) Biogeographical
concordance and efficiency of taxon indicators for estab-
lishing conservation priority in a tropical rainforest biota.
Proceedings of the Royal Society B: Biological Sciences, 268,
1875–1881.
Myers, N. (1988a) Tropical-forest species: going, going,
going... Scientific American, 259, 132.
Myers, N. (1988b) Threatened biotas: “hot spots” in tropical
forests. Environmentalist, 8, 187–208.
Myers, N., Mittermeier, R.A., Mittermeier, C.G., da Fonseca,
G.A.B. & Kent, J. (2000) Biodiversity hotspots for conser-
vation priorities. Nature, 403, 853–858.
Novotny , V., Basset, Y., Miller, S.E., Weiblen, G.D., Bremer,
B., Cizek, L. & Drozd, P. (2002) Low host specificity of
Journal of Biogeography 41, 421–428
ª 2013 John Wiley & Sons Ltd
Biodiversity hotspots under review
herbivorous insects in a tropical forest. Nature, 416, 841–
844.
O’Connor, C., Marvier, M. & Kareiva, P. (2003) Biological
vs. social, economic and political priority-setting in con-
servation. Ecology Letters, 6, 706–711.
Parviainen, M., Marmion, M., Luoto, M., Thuiller, W. &
Heikkinen, R.K. (2009) Using summed individual species
models and state-of-the-art modelling techniques to iden-
tify threatened plant species hotspots. Biological Conserva-
tion, 142, 2501–2509.
Pearson, D.L. & Carroll, S.S. (1998) Global patterns of spe-
cies richness: spatial models for conservation planning
using bioindicator and precipitation data. Conservation
Biology, 12, 809–821.
Prendergast, J.R., Quinn, R.M., Lawton, J.H., Eversham, B.C.
& Gibbons, D.W. (1993) Rare species, the coincidence of
diversity hotspots and conservation strategies. Nature, 365,
335–337.
Reid, W.V. (1998) Biodiversity hotspots. Trends in Ecology
and Evolution, 13, 275–280.
Renema, W., Bellwood, D.R., Braga, J.C., Bromfield, K., Hall,
R., Johnson, K.G., Lunt, P., Meyer, C.P., McMonagle, L.B.,
Morley, R.J., O’Dea, A., Todd, J.A., Wesselingh, F.P.,
Wilson, M.E.J. & Pandolfi, J.M. (2008) Hopping hotspots:
global shifts in marine biodiversity. Science, 321, 654–657.
Rodrigues, A.S.L. (2013) Hotspots. Encyclopedia of biodiver-
sity (ed. by S.A. Levin), pp. 127–136. Academic Press,
Waltham, MA.
Rodrigues, A.S.L. & Brooks, T.M. (2007) Shortcuts for biodi-
versity conservation planning: the effectiveness of surro-
gates. Annual Review of Ecology, Evolution, and Systematics,
38, 713–737.
Scherber, C., Eisenhauer, N., Weisser, W.W. et al. (2010)
Bottom-up effects of plant diversity on multitrophic inter-
actions in a biodiversity experiment. Nature, 468, 553–556.
Schuldt, A. & Assmann, T. (2010) Invertebrate diversity and
national responsibility for species conservation across Eur-
ope – A multi-taxon approach. Biological Conservation,
143, 2747–2756.
Schuldt, A., Wang, Z.H., Zhou, H.Z. & Assmann, T. (2009)
Integrating highly diverse invertebrates into broad-scale
analyses of cross-taxon congruence across the Palaearctic.
Ecography, 32, 1019–1030.
Smith, M.A., Rodriguez, J.J., Whitfield, J.B., Deans, A.R.,
Janzen, D.H., Hallwachs, W. & Hebert, P.D.N. (2008)
Extreme diversity of tropical parasitoid wasps exposed by
iterative integration of natural history, DNA barcoding,
morphology, and collections. Proceedings of the National
Academy of Sciences USA, 105, 12359–12364.
Smith, R., Muir, R., Walpole, M., Balmford, A. & Leader-
Williams, N. (2003) Governance and the loss of biodiver-
sity. Nature, 426, 67–70.
Smith, T.J., III, Boto, K.G., Frusher, S.D. & Giddins, R.L.
(1991) Keystone species and mangrove forest dynamics:
the influence of burrowing by crabs on soil nutrient status
427
N. E. Stork and J. C. Habel
and forest productivity. Estuarine, Coastal and Shelf Sci-
ence, 33, 419–432.
Southwood, T.R.E. (1961) The number of species of insect
associated with various trees. Journal of Animal Ecology,
30, 1–8.
Stork, N.E. & Lyal, C.H.C. (1993) Extinction or co-extinction
rates. Nature, 366, 307–307.
Taberlet, P. & Cheddadi, R. (2002) Quaternary refugia and
persistence of biodiversity. Science, 297, 2009–2010.
Thomas, J.A., Telfer, M.G., Roy, D.B., Preston, C.D., Green-
wood, J.J.D., Asher, J., Fox, R., Clarke, R.T. & Lawton,
J.H. (2004) Comparative losses of British butterflies, birds,
and plants and the global extinction crisis. Science, 303,
1879–1881.
Veech, J.A. (2003) Incorporating socioeconomic factors into
the analysis of biodiversity hotspots. Applied Geography,
23, 73–88.
Viola, D.V., Mordecai, E.A., Jaramillo, A.G., Sistla, S.A., Alb-
ertson, L.K., Gosnell, J.S., Cardinale, B.J. & Levine, J.M.
(2010) Competition-defense tradeoffs and the maintenance
of plant diversity. Proceedings of the National Academy of
Sciences USA, 107, 17217–17222.
Wallace, A.R. (1860) On the zoological geography of the
Malay Archipelago. Journal of the Proceedings of the Lin-
nean Society of London. Zoology, 4, 172–184.
Weisser, W.W. & Siemann, E. (2007) Insects and ecosystem
function. Springer, Berlin, Germany.
Wiens, J.J. & Donoghue, M.J. (2004) Historical biogeogra-
phy, ecology and species richness. Trends in Ecology and
Evolution, 19, 639–644.
428
Williams, K.J., Ford, A., Rosauer, D.F., De Silva, N., Mitter-
meier, R., Bruce, C., Larsen, F.W. & Margules, C. (2011)
Forests of East Australia: the 35th biodiversity hotspot.
Biodiversity hotspots (ed. by J.C. Habel and F. Zachos), pp.
295–310. Springer, Heidelberg.
Williams, S.E., Pearson, R.G. & Walsh, P.J. (1996) Distribu-
tion and biodiversity of the terrestrial vertebrates of Aus-
tralia’s Wet Tropics: a review of current knowledge. Pacific
Conservation Biology, 2, 327–362.
Wilson, E.O. & Peter, F.M. (eds) (1988) Biodiversity.
National Academy Press, Washington, DC.
Wright, S.J., Muller-Landau, H.C. & Schipper, J. (2009) The
future of tropical species on a warmer planet. Conservation
Biology, 23, 1418–1426.
BIOSKETCHES
Nigel E. Stork is Deputy Head of the Griffith School of
Environment, Australia. He is a past president of the Associ-
ation for Tropical Biology and Conservation and has
research interests in the magnitude and extinction of global
biodiversity as well as in tropical forest canopies.
Jan Christian Habel is an assistant professor at the Terres-
trial Ecology Group, Department of Ecology and Ecosystem
Management, Technische Universit€at M€ unchen, Germany.
His special interests are molecular ecology, biogeography and
conservation biology.
Editor: Richard Ladle
Journal of Biogeography 41, 421–428
ª 2013 John Wiley & Sons Ltd