Special Section
Vulnerability and Resilience of Tropical Forest
Species to Land-Use Change
NIGEL E. STORK,? JONATHAN A. CODDINGTON,? ROBERT K. COLWELL,?
ROBIN L. CHAZDON,? CHRISTOPHER W. DICK,??? CARLOS A. PERES,??
SEAN SLOAN,? AND KATHY WILLIS??
?Department of Resource Management and Geography, University of Melbourne, 500 Yarra Boulevard, Richmond, Victoria VIC
3121, Australia, email nstork@unimelb.edu.au
?Department of Entomology, NHB 105, National Museum of Natural History, Smithsonian Institution, Washington, D.C.
20013-7012, U.S.A.
?Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, CT 06269-3043, U.S.A.
?Department of Ecology and Evolutionary Biology and University Herbarium, University of Michigan, 830 North University Avenue,
Ann Arbor, MI 48109-1048, U.S.A.
??Smithsonian Tropical Research Institute, P.O. Box 0843-03092, Balboa Anco?n, Republic of Panama?
??School of Environmental Sciences, University of East Anglia, Norwich NR4 7TJ, United Kingdom
??Oxford University Centre for the Environment, South Parks Road, Oxford OX2 7LE, United Kingdom
Abstract: We provide a cross-taxon and historical analysis of what makes tropical forest species vulnerable
to extinction. Several traits have been important for species survival in the recent and distant geological
past, including seed dormancy and vegetative growth in plants, small body size in mammals, and vagility
in insects. For major past catastrophes, such as the five mass extinction events, large range size and vagility
or dispersal were key to species survival. Traits that make some species more vulnerable to extinction are
consistent across time scales. Terrestrial organisms, particularly animals, are more extinction prone than
marine organisms. Plants that persist through dramatic changes often reproduce vegetatively and possess
mechanisms of die back. Synergistic interactions between current anthropogenic threats, such as logging, fire,
hunting, pests and diseases, and climate change are frequent. Rising temperatures threaten all organisms,
perhaps particularly tropical organisms adapted to small temperature ranges and isolated by distance from
suitable future climates. Mutualist species and trophic specialists may also be more threatened because of
such range-shift gaps. Phylogenetically specialized groups may be collectively more prone to extinction than
generalists. Characterization of tropical forest species? vulnerability to anthropogenic change is constrained
by complex interactions among threats and by both taxonomic and ecological impediments, including gross
undersampling of biotas and poor understanding of the spatial patterns of taxa at all scales.
Keywords: extinction vulnerability, range shifts, species traits, tropical forest species
Vulnerabilidad y Resiliencia de Especies de Bosques Tropicales al Cambio de Uso de Suelo
Resumen. Aportamos un ana?lisis trans-taxo?n e histo?rico de lo que hace que las especies de bosques
tropicales sean vulnerables a la extincio?n. Varios atributos han sido importantes para la supervivencia de
especies en el pasado reciente y geolo?gico, incluyendo la latencia de semillas y el crecimiento vegetativo en
plantas, el taman?o corporal pequen?o de mam??feros y la vagilidad en insectos. Para las mayores cata?strofes del
pasado, como los cinco eventos de extincio?n masiva, la extensio?n del rango y la vagilidad o dispersio?n fueron
claves para la supervivencia de especies. Los atributos que hacen que algunas especies sean ma?s vulnerables
a la extincio?n son consistentes a trave?s de las escalas de tiempo. Los organismos terrestres, particularmente
1438
Conservation Biology, Volume 23, No. 6, 1438?1447
C?2009 Society for Conservation Biology
DOI: 10.1111/j.1523-1739.2009.01335.x
Stork et al. 1439
animales, son ma?s propensos a la extincio?n que los organismos marinos. Las plantas que persisten a trave?s
de cambios drama?ticos a menudo se reproducen vegetativamente y poseen mecanismos de muerte regresiva.
Las interacciones sine?rgicas entre amenazas antropoge?nicas actuales, como explotacio?n de madera, fuego,
cacer??a, plagas y enfermedades y cambio clima?tico son frecuentes. Las temperaturas crecientes amenazan a
todos los organismos, quiza?s particularmente a organismos tropicales adaptados a rangos de temperatura
pequen?os y aislados por distancia de climas futuros adecuados. Las especies mutualistas y los especialistas
tro?ficos pueden estar ma?s amenazados debidos a tales discontinuidades en los cambios de rango. Los grupos
filogene?ticamente especializados colectivamente pueden ser ma?s propensos a la extincio?n que los generalistas.
La caracterizacio?n de la vulnerabilidad de las especies de bosques tropicales al cambio antropoge?nico esta?
limitada por las complejas interacciones entre amenazas y tanto por impedimentos taxono?micos y ecolo?gicos,
incluyendo el muestreo incompletos de biotas y el pobre entendimiento de los patrones espaciales de taxa a
todas las escalas.
Palabras Clave: atributos de las especies, cambios de rango, especies de bosque tropical, vulnerabilidad de
extincio?n
Introduction
Arguably 65?75% of all terrestrial species may be re-
stricted to tropical forests. Approximately 50% of all
plants and vertebrates are believed to be endemic to 34
identified global biodiversity hotspots (Myers et al. 2000;
Mittermeier et al. 2004). Most are in tropical forests. More
than 50% of these forests have been severely degraded or
converted for agriculture (FAO 2007), and this may have
resulted in the loss of many species. The 2008 Interna-
tional Union for Conservation of Nature Red List consid-
ers roughly one-quarter to one-third of species in the best
known groups (e.g., amphibians, birds, mammals, and
gymnosperms) threatened with extinction in the near fu-
ture (Fig. 1). Climate change poses additional threats to
tropical forest species (Thomas et al. 2004; Laurance &
Peres 2006; Colwell et al. 2008), which potentially could
be far more severe than in higher-latitude regions (Wright
et al. 2009 [this issue]).
Since the early 1980s many have warned of the po-
tential loss of species through tropical forest loss and
conversion (Myers 1979; Ehrlich & Ehrlich 1981). Lack of
evidence for the predicted mass extinctions (Brooks et al.
1999) may be due to our limited ability to detect extinc-
tions, time lags before species become extinct (Diamond
1972), and the ability of secondary forests to retain high
levels of primary forest biodiversity (Meijaard et al. 2005;
Chazdon et al. 2009 [this issue]; but see Barlow et al.
2007). Singapore, for example, has lost many species
(Turner et al. 1997; Brook et al. 2003; Sodhi & Brook
2008) and may presage coming events in other tropical
forests. We examined the traits that make tropical forest
taxa prone to extinctions from anthropogenic causes and
considered similarities and differences in such responses
across taxa. We examined first the vulnerability of taxa
in the geological past and then the possible synergistic
effects of diverse extinction drivers acting on species
(Peres 2001; Laurance 2006; Brook et al. 2008). We also
considered current constraints to the understanding of
vulnerability.
Learning from the Past about Species Vulnerability
and Resilience
The fossil record shows that marine species with broad
geographical ranges or widespread larval dispersal were
especially likely to survive mass extinction events like
the ?big five? and smaller events (Jablonski 1995; Jack-
son 1995). Modern marine and terrestrial species are
predicted to respond similarly (May et al. 1995). Nev-
ertheless, perhaps 90?96% of all extinctions occurred
outside such extinction events, presumably due to less
understood and less globally catastrophic factors (May
et al. 1995). Species longevity also varies among major
0 10 20 30 40 50 60 70 80 90 100
Mammals
Birds
Reptiles
Amphibians
Species (%)
extinct
threatened
low risk
data deficient
Figure 1. Proportions of species by threat category for
four comprehensively assessed groups: amphibians,
birds, mammals, and gymnosperms. Threat categories
are extinct (EW, extinct in the wild; EX, extinct),
threatened (VU, vulnerable; EN, endangered; CR,
critically endangered); low risk (LC, least concern; NT,
near threatened), and data deficient (DD) (data from
IUCN (2009).
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Volume 23, No. 6, 2009
1440 Land-Use Change and Tropical Forest Species
groups (Raup 1978; May et al. 1995): marine taxa en-
dure longer (6?25 million years) than terrestrial taxa
(1?4 million years) (McKinney 1997). McKinney (1997)
also showed there is a high correlation between modern
and fossil extinction rates; modern terrestrial taxa are
more prone to extinction as in the past. Perhaps marine
species have wider geographical ranges than terrestrial
species (Norse 1993; McKinney 1997). Animals may also
be much more prone to mass extinction than plants?the
plant fossil record suggests fewer comparable extinction
events than does the animal record (Willis & McElwain
2002). Traits of persistent plant species include seed dor-
mancy, underground vegetative reproduction, and die-
back mechanisms (Knoll 1984; Willis & Bennett 1995).
Over the last 1.8 million years temperature oscillations
caused massive changes to the distribution of ecosystems
and vegetation types, with many species becoming lo-
cally and some globally extinct. For this period Willis
et al. (2004) concluded extinction exceeded speciation
inmany temperate groups. Although some therefore infer
that the Ice Ages saw little net diversification (Zink et al.
2004), others infer major adaptive change, for example
a modern temperate mammalian fauna rich in rapidly re-
producing and generalist species (Lister 2004). On the ba-
sis of evidence from Southeast Asia, Meijaard et al. (2007)
argue that geologically older vertebrate species are more
vulnerable to climate fluctuations. These species tended
to have smaller ranges and occupied fewer, smaller out-
lying islands than modern species.
Drought sensitivity strongly limits the distributions of
tropical forest trees and other taxa (Engelbrecht et al.
2006). Lowland evergreen tropical forests contracted and
tropical dry forests expanded during glacial periods in
South and Central America, Africa, Australia, and South-
east Asia (Pennington et al. 2000; Morley 2000; Hugall
et al. 2002). Increased warmth and rainfall due to con-
temporary climate change may further fragment highly
threatened dry forests. Cover of Neotropical, wet, low-
land forest was maintained through the Last Glacial Max-
imum in spite of globally reduced rainfall, reduced atmo-
spheric CO2 concentrations, and cooling. Species com-
position, however, changed as upper-elevation taxa in-
vaded the lowlands to create Ice Age tree communities
with no modern analogs in Central and South America
(e.g., Colinvaux et al. 1996; Piperno & Jones 2003).
Severe historical forest fragmentation is best docu-
mented in Africa and Central America (Morley 2000).
Africa has less forest than Amazonia (in part because the
rainforests lack a protective montane rain shadow like
the Andes) and has experienced severe extinctions of tree
taxa. According toMorley (2000), African tree extinctions
in the rainforest pulsed during the Eocene-Oligocene
transition as savanna biomes became established and
more recently and abruptly during the late Pliocene as
forests contracted with Ice Age cooling and drying. Africa
has notably low palm diversity compared with Asia and
the Americas, probably due to the late Eocene and late
Pliocene extinctions. In general, the smaller area over
geological time of African tropical forests explains their
relatively low regional species diversity compared with
Asia and the Neotropics (Fine & Ree 2006).
To comprehend one potential future of rain forests,
consider the thermal maxima of the Miocene and Eocene,
when atmospheric CO2 exceeded today?s levels (1000
ppm) and those predicted over the next century (IPCC
2001; Hansen et al. 2008). Pollen cores show that trop-
ical forests were more diverse (Morley 2000) and cov-
ered most of the world?s landmasses, including Eu-
rope (?boreotropical forests?) (Willis & McElwain 2002).
These rich, ancient forests may be a poor model for
the future because extinctions could easily spike dur-
ing the extraordinarily rapid climatic transition currently
underway. Nevertheless, some populations of Neotrop-
ical, lowland, rainforest trees share common Miocene
ancestors (Dick & Heuertz, 2008); hence, tree popula-
tions can endure both warmth and climatic transitions.
If such species retain their thermal tolerances to warmer
climates, it will have been in spite of the generally cooler
past several million years. Poleward range shifts of equa-
torial species due to globalwarming are unlikely given the
prevailing narrow tropical temperature gradient today
(Wright et al. 2009). Upslope elevational range shifts in
the tropics are perhaps more likely (Colwell et al. 2008).
But neither poleward nor elevational shifts of contem-
porary tropical species toward newly suitable areas can
be expected if seed-dispersing animals decline through
either anthropogenic habitat fragmentation or overhunt-
ing. As cloud levels rise on tropical mountains and cli-
mate zones shift upslope, human land-use patterns may
well follow, further fragmenting the forest corridors es-
sential for elevational range shifts for many species (Bush
2002).
Given projected global warming and anthropogenic
land-use patterns, we suggest traits of species that make
them particularly vulnerable to extinction. The nar-
row thermal tolerances characteristic of tropical species
(Janzen 1967; Deutsch et al. 2008; Chen et al. 2009)
should translate into narrow elevational ranges (McCain
2009). As climate change drives upslope range shifts,
the lower elevational limit of narrow-ranged species may
soon be forced beyond their current upper elevational
limits. Colwell et al. (2008) project that over the next cen-
tury half the plants and insects they studied on an eleva-
tional transect in Costa Rica are likely to experience such
?range shift gaps,? at least locally. Evidence from past cli-
matic changes (e.g., Davis & Shaw 2001; Bush & Flenley
2007) make it clear that range shifts are routinely discor-
dant and idiosyncratic, despite net shifts that tend to track
climate zones (Wilson et al. 2007;Moritz et al. 2008; Chen
et al. 2009). Species dependent on mutualisms (e.g., pol-
lination, seed or fruit dispersal) and trophic specialists
(e.g., insects requiring specific host plants) are therefore
Conservation Biology
Volume 23, No. 6, 2009
Stork et al. 1441
particularly likely to encounter obstacles in the case of
range-shift gaps. Taxa with low physiological tolerances
for higher temperatures or low genetic plasticity are simi-
larly vulnerable (Hoffman et al 2003; Deutsch et al. 2008),
as discussed by Wright et al. (2009). In the last 50,000
years, Homo sapiens and possibly other Homo species
probably caused numerous extinctions, particularly by
hunting large tropical vertebrates (Barnosky 2008), forest
conversion, and wildfires (Piperno 2007). South America
lost 50 megafauna genera, (reviewed in Koch & Barnosky
2006) between 12,000 and 8,000 years ago (Barnosky
2008), mainly large and often slow-breeding mammals
(Hubbe et al. 2007). All mammals larger than 320 kg and
many between 320 and 100 kg went extinct. More recent
human-induced extinctions are also common on tropical
islands (Pimm et al. 2006).
Vulnerability to Extinction and Depletion
Many authors have attempted to identify extinction-
prone traits (e.g., Lawton&May 1995; Koh et al. 2004a,b;
Brook et al. 2008; Sodhi et al. 2008a,b; Supporting In-
formation), some from local or regional studies (e.g.,
Laurance 1991) and some from global analyses (e.g.,
Gaston & Blackburn 1997; Cardillo et al. 2005). Most
studies focus on birds or large mammals, rather than
plants, invertebrates, or other organisms, and fewer at-
tempt cross-taxon analyses of tropical forest taxon re-
sponse to anthropogenic perturbation such as land-use
change, hunting, or their synergies. McKinney (1997)
showed that extinction is rarely random. Specialization
results in nested extinction-prone traits in certain clades.
Isolating simple ecological correlates of overall risk can
be difficult because multiple mechanisms underlie ex-
tinction patterns (Owens & Bennett 2000). In general,
low population densities and fecundity, small ranges, low
vagility, narrow niches, mature-forest habitat specificity,
large body size, high species dependency for food or dis-
persal, and high trophic guild presage risk. These traits
predominate among larger vertebrates, which are there-
fore more vulnerable. But vertebrate and other higher
taxa vary widely within and between groups so that par-
ticular species respond quite divergently to threats. Life-
history patterns, for example, vary dramatically across
tropical forest vertebrates, plants, arthropods, fungi, and
parasitic groups. Extinction vulnerability traits for plants
and arthropods are little known (Supporting Informa-
tion).
Extinction vulnerability increases if a species partially
or entirely depends on another vulnerable organism
(Stork & Lyall 1993; Dunn 2005; Koh et al. 2004c). Ob-
vious examples are parasites or host-specific herbivores.
Whether herbivorous insects of tropical forests are more
host specific (and therefore more vulnerable) than tem-
perate taxa is hotly debated (Novotny et al. 2007; Dyer
et al. 2007). Taxa with complex life histories or more
than one host species would be even more vulnerable
(Koh et al. 2004c). We considered one key complex
set of threats, deforestation and fragmentation and wild-
fires, and their synergies with others such as climate
change and invasive organisms. Hunting has been ex-
tensively covered elsewhere (e.g., Robinson & Bennett
2000; Milner-Gulland et al. 2003) and is not addressed in
detail here.
Deforestation and Forest Degradation
Primary forest habitat specificity or, conversely, tolerance
to the open-habitat matrix strongly determines the prob-
ability of local extinction in tropical forest landscapes
undergoing forest fragmentation and recurrent wildfires
(Thomas 2004; Prugh et al 2008; Lees & Peres 2009).
Survival of old-growth species in secondary forest seems
increasingly important as forests throughout theworld re-
generate (Chazdon et al. 2009). Many animals fare poorly
in tropical forest fragments (Laurance 2008) and will
not cross open clearings (e.g., some large mammals, Eu-
glossine bees, Nymphalid butterflies, and birds: Dressler
1982; Herrera 1987; Barlow et al. 2007), although the
latter is crucial to persistence in fragmented landscapes
(Lees & Peres 2009).
Singapore (699.4 km2) has lost 99.6% of its primary,
lowland, evergreen rainforest to deforestation and frag-
mentation (Turner et al. 1997; Koh et al. 2004a; Sodhi
et al. 2008a). Only secondary forest remains, covering
10?15% of the island. Sodhi et al. (2008a) evaluated 454
locally extinct versus 1430 extant terrestrial angiosperms
for geographic distribution, pollination system, breed-
ing system, growth form, habitat, height, fruit- or seed
-dispersalmechanism and resprouting capacity, and other
traits. These factors explained relatively little variation
in extinction probability. Epiphytic, monoecious and
hermaphroditic, inland forest specialists, and mammal-
pollinated species had higher probabilities of extinction.
Dispersal traits, particularly small seed size and rapid
seed production, correlate highlywith establishment dur-
ing post-disturbance succession. Animals disperse over
70% of tropical plant seeds (Howe & Smallwood 1982).
Scarcity of large frugivores in fragmented or overhunted
forests favors wind-dispersed and small-seeded plants
(Peres & Palacios 2007; Cramer et al. 2007; Turner et al.
1997; Wright et al. 2007). Shade-tolerant, old-growth
species with large seeds dispersed by large arboreal ver-
tebrates are particularly vulnerable (Parry et al. 2007).
Slow growth rates, low population densities, and low re-
production rates also increase risk following large-scale
disturbances (see also Slik 2005 for further reference).
Species able to persist in edge-dominated and secondary
habitats exhibit fewer pollination systems, greater use
of generalist diurnal vectors, and more hermaphroditism
(Chazdon et al. 2003; Lopes et al. 2009).
Conservation Biology
Volume 23, No. 6, 2009
1442 Land-Use Change and Tropical Forest Species
Recurrent surface wildfires are now one of the most
important threats to seasonally dry tropical forests
(Cochrane 2003), often acting synergistically with se-
vere droughts. Wet tropical forest woody plants are typ-
ically thin barked and therefore vulnerable to even low
?creeping? fires set by shifting cultivators (Barlow&Peres
2004). Mast fruiting species such as Dipterocarpaceae in
Southeast Asia are particularly susceptible because fires
following recent recruitment events have drastic effects
(van Nieuwstadt & Sheil 2005). In Kalimantan even larger
stemmed dipterocarp treeswith bark thick enough to sur-
vive fire are still vulnerable to drought. Indeed, much of
the plant mortality ascribed to fire is due to the severe
droughts required before a forest can burn. Both larger
and smaller species were vulnerable in different con-
texts, presumably depending on soil moisture and root-
ing depths. Small seedlings and nondeciduous canopy
trees suffer if they cannot drop their leaves. Drought
and fire together strongly affect the maintenance or re-
covery of forests and their role as carbon stores (van
Nieuwstadt et al. 2001). Recurrent fires have changed
forest structure and composition so that pioneers domi-
nate the understory in some central-eastern Amazonia re-
gions (Cochrane & Schulze 1999; Barlow & Peres 2008).
Most guilds of birds decline after recurrent fires but ar-
boreal granivores, frugivores, and nectarivores show uni-
modal responses, whereas arboreal gleaning insectivores
increase (Barlow & Peres 2004). For forest vertebrates,
fire poses the greatest risk to primary forest specialists
characterized by lowmobility, poor climbing ability, poor
flight capacity, small home ranges, or that rely heavily on
woody shelters, such as cavity nests within hollow tree
trunks (Peres et al. 2003).
Synergistic Effects of Threats
Increasing evidence suggests that different threats (such
as fire and drought) act additively or synergistically and
exacerbate species declines (Laurance 2006; Peres &
Michalski 2006; Brook et al. 2008). Brook et al. (2008) de-
fine synergistic as positive or multiplicative interactions
that occur due to simultaneous action of separate pro-
cesses (extrinsic threats or intrinsic biological traits). Syn-
ergies occur between almost all anthropogenic threats
(Supporting Information). The lack of observed extinc-
tions in tropical forests over the last 50 years may belie
future exponential increases. For example, hunting often
acts synergistically with other threats such as fragmenta-
tion and disease to cause local extinction (Peres 2001;
Walsh et al. 2003). Climate change will likely power
disease diffusion by altering host-pathogen interactions
(Aguirre & Tabor 2008). Logging increases forest fires and
fragmentation and thus accentuates ecoclimatic stresses,
species invasions, and edge-related change, which are
often followed by hunting, trophic cascades (Spiller &
Schoener 1990; Pace et al. 1999), invasions of agricultural
pests, and sometimes complete deforestation as colonists
follow loggers into the forest frontier. Invasive organisms
including those transported by humans or accentuated by
climate change, can severely affect faunas naive to these
new species or invasions. Predation by exotic species on
islands has caused the extinctions ofmany native animals.
In contrast, exotic plant invasions appear to have caused
few island native plant extinctions (Sax & Gaines 2008).
The impact of chytrid fungus on amphibians (Pounds
et al. 2006) is a particularly apt example of synergistic
threats on a global basis.
The complexity of synergies complicates the identifi-
cation of individual species traits that contribute to vul-
nerability or persistence. Sodhi et al. (2008b), however,
showed that amphibians with small geographic ranges in
areas with pronounced seasonality in temperature and
precipitation are most likely to be on International Union
for Conservation of Nature?s Red List. Habitat loss and hu-
man densities also correlated with risk. In a similar study,
Bradshaw et al. (2008) found that plant species that are
more- ?invasive? (e.g., climbing, herbaceous, and those
that span multiple habitats and bioregions) are less threat-
ened, whereas species that are tall, have tree-like forms,
are range restricted, or inhabit lowland closed forest are
more threatened. In some instances, different threats may
affect different suites of species within a taxon but do not
act synergistically. Owens and Bennett (2000) found that
extinction risk in birds from hunting and persecution is
associated with large body size and long generation time,
but is not associated with habitat specialization, whereas
extinction risk from habitat loss is associated with habi-
tat specialization and small body size, but not genera-
tion time. In contrast, numerous examples show how
different threats on the same landscape exhibit strong
synergies (Supporting Information); presumably as yet
unrecognized synergies await discovery.
Constraints to Understanding the Extent of
Vulnerability to Extinction in Tropical Forests
Both taxonomic and ecological factors, including a
paucity of tools for species identification, and severe
undersampling, limit understanding of extinction-prone
traits. For example, in western Amazonian forest plots,
about 20% of midstory and canopy trees species are not
identifiable to species; understory trees, woody lianas,
epiphytes, and hemiepiphytes are ignored in most sur-
veys (Ruokolainen et al. 2005). Consequently, research
on regional forest dynamics is typically limited to large
trees identified only to genus. One intensively stud-
ied 1-ha forest plot in Amazonian Ecuador contains
900 vascular plant species (Balslev et al. 1998), yet
only 4000 plant species have been reported for the sur-
rounding 7 million ha of Amazonian forest in Ecuador
Conservation Biology
Volume 23, No. 6, 2009
Stork et al. 1443
(J?rgensen & Leo?n-Ya?nez 1999; Ruokolainen et al. 2005).
Sampled floristic similarity across 122 sites in the same
region ranged from zero overlap to more than 70% of
species in common (Tuomisto et al. 2003). For many
other groups the taxonomic impediment is even greater.
Lawton et al. (1998), for example, showed that there is
at least a 100-fold increase in the amount of taxonomic
effort in measuring species richness of the smallest of
nine taxonomic groups examined, the nematodes, com-
pared with birds (see also Gardner et al. 2008 for further
reference), yet nematodes, along with arthropods, mi-
croorganisms, and fungi, comprise the majority of global
terrestrial species.
Inadequate sampling for almost all groups means the
ranges of species and hence the patterns and measure-
ment of beta-diversity are uncertain. Inadequate sam-
pling inevitably underestimates local species richness and
therefore range size, especially in richer biotas and poorly
known groups (Colwell & Hurtt 1994). The relatively re-
cent development andwidespread application of species-
richness estimators (Colwell 2006) has for the first time
allowed quantitative estimates of undersampling bias,
and, at least for most tropical arthropod surveys, the
bias seems considerable (Coddington et al. 2009). Local
undersampling biases the calculation of pairwise similar-
ity of species composition among samples (Chao et al.
2005, 2006), the basis of many measures of beta diversity
(Ruokolainen&Tuomisto 2002; Ruokolainen et al. 2002);
hence, undersampling underestimates alpha diversity and
overestimates beta diversity. Patterns of alpha and beta
diversity along elevational gradients are increasingly stud-
ied locally (e.g., Novotny et al. 2005; Brehm et al. 2007;
Cardelu?s et al. 2006) and in meta-analyses (Rahbek 1995,
2005; McCain 2005). Given the conservation importance
of elevational corridors as warming drives thermal zones
upslope (Wilson et al. 2007; Colwell et al. 2008; Moritz
et al. 2008; Raxworthy et al. 2008; Chen et al. 2009),
these patterns require urgent study.
Although alpha-diversity estimates exist for a few
groups, no ?all species inventory? (sensu D. H. Janzen,
see Yoon 1993) is available for any single tropical rain-
forest site, with the possible exception of Singapore
(e.g., Brook et al. 2003). Without such measures of al-
pha and beta diversity, gamma-diversity estimates remain
extremely imprecise. Determining the total range, varia-
tion, andmaintenance of species composition at different
locations (e.g., Tuomisto & Ruokolainen 2006) is crucial
to understanding extinction vulnerability. Relatively ac-
curate distributional data and beta diversity estimates are
available for terrestrial vertebrates in some regions (es-
pecially birds and mammals; e.g., Jetz & Rahbek 2002;
Rahbek et al. 2007; Rodriguez & Arita 2004, Willig &
Gannon 1997), but comparable data for arthropods and
other hyperdiverse groups are, at best, on much more
local scales (e.g., Novotny et al. 2007; Brehm et al. 2007;
Chen et al. 2009).
Ecological theory, largely based on vertebrates and
woody plants, suggests that species rangesmay be smaller
in tropical forests (Janzen 1967; Ghalambor et al. 2006;
Stevens 1989), at least on elevational gradients (Gaston &
Chown 1999; McCain 2009; R.K. C., unpublished). Yet, a
lack of comparative data for different parts of the tropical
world and for different taxa, particularly nonvertebrates
and other smaller organisms, means the predicted pattern
still awaits broad confirmation. In addition, how much
range sizes and patterns of range overlap differ for differ-
ent taxa, and hence whether species turnover rates dif-
fer, is largely unknown. Habitat fragmentation and other
land-use patterns could differentially affect species with
different range sizes (Lozada et al. 2008). Stochastic mod-
eling of species distributions on large spatial scales com-
bined with physical and climatic patterns (e.g., Storch
et al. 2006; Rahbek et al. 2007; Rangel et al. 2007) pro-
vides a new approach to studying the drivers of diversity
patterns that could be combined with human land-use
patterns and the vulnerability of different taxa to probe
the prospects for future extinctions.
Finally, recovering secondary forests may harbor many
old-growth species (Norden et al. 2009; Chazdon et al.
2009), which offers some hope that primary forest
species extinctions may not be as extensive as many fear.
Determining whether taxa differ in extinction-relaxation
times following forest conversion to other land uses will
be key.
Acknowledgments
We thank S.J. Wright and W.M. Laurance for their invi-
tation to participate in the Smithsonian Tropical Forest
Institute workshop on tropical forest extinctions that led
to the development of this paper. We thank T. Brooks
for access to Fig. 1 and D. Sheil and three anonymous
reviewers for valuable comments that improved this pub-
lication.
Supporting Information
Extinction vulnerability traits (Appendix S1) and effects
of threats to biodiversity (Appendix S2) are available as
part of the on-line article. The author is responsible for
the content and functionality of these materials. Queries
(other than absence of the material) should be directed
to the corresponding author.
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