Biological Conservation 151 (2012) 32–34

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Biological Conservation
journal homepage: www.elsevier.com/locate/biocon

Special Issue Article: Advancing Environmental Conservation: Essays In Honor Of Navjot Sodhi

Improving estimates of biodiversity loss

Chase D. Mendenhall ⇑, Gretchen C. Daily, Paul R. Ehrlich
Center for Conservation Biology, Department of Biology, Stanford University, Stanford, CA 94305-5020, USA

a r t i c l e i n f o a b s t r a c t

Article history: Quantifying the magnitude of human-induced biodiversity loss is a critical yet daunting challenge.
Received 26 August 2011 Recently, species extinction rate estimates using island biogeography theory have once again been called
Received in revised form 29 January 2012 into question. Here we highlight two of the many factors making the traditional application of this
Accepted 31 January 2012
approach problematic for measuring biodiversity loss: first, the extreme assumption that native habitats
Available online 13 March 2012
are surrounded by a sea of human enterprise largely incapable of sustaining native biodiversity and, sec-
ond, the sole use of species-level extinction estimates, which always underestimates the loss of biodiver-
Keywords:
sity. Here we show that a wide array of taxa make human-dominated, farming countryside their home
Agriculture
Countryside biogeography
beyond the borders of native habitats. With data on native tropical birds, we show how simple species
Endemics-area relationship numeration masks dramatic differences between habitat types in community composition (e.g. species
Extinction rates diversity or functional diversity). Overlooking the countryside biota, coupled with a scientific paradigm
Species-area relationship that underestimates biodiversity loss by equating it with species extinction, will only exacerbate the
Population diversity ongoing crisis. This is especially true given the rapid expansion and intensification of agriculture threat-
ening countryside biotas, and a persistent limited understanding of how population extinctions and
changes in community composition alter ecosystem functioning and services that support human life
and wellbeing.
Ó 2012 Elsevier Ltd. All rights reserved.

Contents

Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 34
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 34

Navjot S. Sodhi dedicated his life to understanding and reversing diversity were to be found in remnants of native habitat – Noah’s
the biodiversity loss now sweeping the planet. Ecologists recognize Arks floating in a hostile flood of human enterprise. The logic
Earth’s biota is now already experiencing the sixth great extinction was that most organisms are highly adapted to their native habi-
wave, but nonetheless quantifying its pace mid-stride remains tats and that few would be able to exploit areas heavily modified
difficult. Problems of estimating biodiversity loss persist, partly be- by human activities. In general, those few species would not
cause of the limitations and continued interpretation of species- require or merit protection and efforts should concentrate on
area relationships (SAR) for estimating species extinction. The use preserving ecosystems in their pristine forms removed from areas
of the SAR as the sole method for estimating biodiversity loss per- of high human activity.
petuates the idea that only pristine habitats matter for conservation A great deal of work has now reported that, to the contrary, hu-
and dramatically underestimates biodiversity loss by ignoring pop- man-dominated ecosystems (currently constituting 75% of the glo-
ulation and community changes. We examine the conventional bal land surface; Ellis et al., 2010) collectively host substantial
assumptions that human-dominated habitats and landscapes are biodiversity, and that this reservoir of biodiversity is under threat
largely incapable of sustaining native biodiversity and that the bio- from rapid intensification of agricultural production systems and
diversity crisis is best viewed by evaluating species extinction. other factors associated with human population growth and con-
Thirty years ago, extinction rates were estimated using the clas- sumption (Bignal and McCracken, 1996; Fischer et al., 2008;
sical framework of island biogeography (MacArthur and Wilson, Haslem and Bennett, 2008; Hughes et al., 2002; Perfecto et al.,
1967). The prevailing view was that the clues to the future of bio- 2009). New theory (Koh et al., 2010; Nelson et al. 2011; Pereira
et al. 2004; Pereira and Daily 2006;) and empirical study (Menden-
⇑ Corresponding author. Tel.: +1 650 723 3171; fax: +1 650 723 5920. hall et al., 2011) show how, for instance, many ‘‘tropical forest ani-
E-mail address: cdm@stanford.edu (C.D. Mendenhall). mals’’ can make their homes outside of native habitats, and their

0006-3207/$ - see front matter Ó 2012 Elsevier Ltd. All rights reserved.
doi:10.1016/j.biocon.2012.01.069
 C.D. Mendenhall et al. / Biological Conservation 151 (2012) 32–34 33

Fig. 1. Proportion of population inhabiting different countryside habitats for 148

native bird species censused using constant-effort mistnet sampling in the canton
of Coto Brus, Costa Rica. Species’ forest dependency rank ranges from complete
forest dependendency (rank 1) to complete forest avoidance (rank 148) and was
determined by comparing relative abundance in natural forest (a 260 ha reserve;
green) versus agricultural plots (deforested farm plots; yellow). The proportion of
each species’ population in intermediate habitats (grey) is also shown. These Fig. 2. Mean species richness values (with minimum and maximum values, from
habitats include 10–20 yr-old secondary forest fragments (50–75 ha), primary three locations) in six common habitat types in Coto Brus, Costa Rica. Species
forest in small fragments (1–20 ha), and primary forest in thin riparian strips (10– richness was estimated through constant-effort mist net sampling from 2007–2009.
100 m wide). Proportion of population was calculated by summing the individuals Data are shown for 148 native bird species represented by P5 individuals captured
encountered during mist net sampling from 2007–2009 and controlling for at 18 sampling locations. Species accumulation curves for all sites have reached
sampling effort among habitat types. Data are depicted for 16,168 individual birds asymptote. Each habitat type is represented by three sampling locations. Habitat
of commonly captured species (species represented by 65 captures are not shown). descriptions match those in Fig. 1, except agricultural plots were split into low
(For interpretation of the references to colour in this figure legend, the reader is intensity (25% tree cover on farms) and high intensity (5% tree cover on farms)
referred to the web version of this article.) categories. Species richness was distributed among habitat types equally (one-way
analysis of variance, F5,227 = 2.19, P = 0.12). When community composition was
compared using Sørensen similarity coefficients, two distinct communities were
observed: in agricultural plots (both low and high intensity) and all countryside
ability to do so varies with a range of species traits (Daily, 2001; forest elements (natural forest and intermediate habitats; one-way analysis of
Daily et al., 2001, 2003; Horner-Devine et al., 2003; Ricketts, similarity, R = 0.756, P < 0.001)(Mendenhall et al., 2011).
2001; Sekercioglu et al., 2007). Moreover, different individuals
within a population may use combinations of habitat that do not
fit within the confines of the island paradigm (Fig. 1). Only a small
fraction of the planet can be considered either pristine or com- tributed among habitat types (agricultural plots, semi-native hab-
pletely inhospitable, with the vast majority of biodiversity existing itats, and native forest) (Fig. 2). From a species extinction
in habitats located somewhere in between (Ellis et al., 2010). perspective, very little biodiversity change has occurred.
Understanding how to sustain biodiversity and ecosystem pro- Considerable differences between habitat types arise from
cesses and services in these habitats requires much more attention. changes in species community composition, however, at a fine
There is tremendous opportunity to harmonize the conserva- scale along a gradient from native to more human-impacted
tion of biodiversity with human activities in biomes worldwide. habitats. A dramatic shift in species community composition oc-
For example, in ancient human-modified landscapes, certain agri- curs within 70 m of small forest elements scattered throughout
cultural practices have sustained high biodiversity, as in the case the countryside (Mendenhall et al., 2011). It remains an open
of arecanut palm production in the biodiversity-rich Western question if these differences in species community composition
Ghats of India. Despite continuous cultivation for over two millen- reflect changes in functional diversity, biological filtering be-
nia, the landscape has retained populations of some 95% of the bird tween habitats, and/or population losses. Moreover, we have lit-
species associated with native forest (Ranganathan et al., 2008). tle knowledge of how such changes in community composition
The scientific community continues to lack a clear understanding are affecting ecosystem functioning or the provisioning of biodi-
of how different types and intensities of human activity affect versity-driven services to society, nor at what spatial or time
the components of biodiversity that drive ecosystem functioning, scales (Balvanera et al., 2006; Cardinale, 2011). Considering the
in part because of narrow concentration on species counts and complexity of the issues, there obviously remains much work
species-level extinction. to understanding how ecosystems respond to human-induced
Like Navjot S. Sodhi, we urge ecologists to broaden their con- environmental change at levels deeper than species richness
ceptualization and quantification of biodiversity loss by including (Tscharntke et al., this issue).
within it population extinctions and changes in community com- Currently the biodiversity crisis measured in units of species
position (e.g. species diversity and functional diversity) (Ceballos extinction only accounts for a cusp of biodiversity loss. The extinc-
and Ehrlich, 2002; Hughes et al., 1997; Sekercioglu et al., 2004; tion of a species is the culmination of many populations perishing
Sodhi et al., 2004). Our research has shown the shortcomings of and indicative of immense disruption, reorganization, and restruc-
the sole use of species richness, the fundamental unit of the SAR, turing of biological communities, often over huge areas. Our cur-
to measure biodiversity’s response to human impacts. For example, rent understanding of the size and gravity of biodiversity loss is
after extensive deforestation (about 70% of original forest cover) in crippled by overlooking habitats beyond the island paradigm of
the 1960s and 70s in the canton of Coto Brus, Costa Rica (ca. 950 hospitable and inhospitable, and the loss is dramatically underes-
km2), only four bird species (1.4%) underwent local extinction timated because we ignore population extinctions and community
(none of which are globally extinct; Daily et al., 2001, Appendix change over such large areas. To gain a better sense of the ongoing
A and B). Additionally, the number of bird species is equally dis- biodiversity crisis, we must direct our attention toward research
34 C.D. Mendenhall et al. / Biological Conservation 151 (2012) 32–34

efforts to forecast population diversity, community structure, eco- Should agricultural policies encourage land sparing or wildlife-friendly
farming? Frontiers in Ecology and the Environment 6, 380–385.
system functioning, and ecosystem services in concert with esti-
Haslem, A., Bennett, A.F., 2008. Countryside elements and the conservation of birds
mates of species extinctions. in agricultural environments. Agriculture, Ecosystems & Environment 125, 191–
203.
Horner-Devine, M.C., Daily, G.C., Ehrlich, P.R., Boggs, C.L., 2003. Countryside
biogeography of tropical butterflies. Conservation Biology 17, 168–177.
Acknowledgements Hughes, J.B., Ehrlich, P.R., Daily, G.C., 1997. Population diversity: its extent and
extinction. Science 278, 689–692.
We thank Melinda Belisle, Luke Frishkoff, Rachelle Gould, Mat- Hughes, J.B., Daily, G.C., Ehrlich, P.R., 2002. Conservation of tropical forest birds in
countryside habitats. Ecology Letters 5, 121–129.
thew Knope, John Harte, Daniel Karp, Guy Ziv, and two anonymous Koh, L.P., Lee, T.M., Sodhi, N.S., Ghazoul, J., 2010. An overhaul of the species-area
reviewers for helpful comments on the paper. We thank Federico approach for predicting biodiversity loss: Incorporating matrix and edge effects.
Oviedo Brenes and dozens of field assistants in the collection of Journal of Applied Ecology 47, 1063–1070.
MacArthur, R.H., Wilson, E.O., 1967. The Theory of Island Biogeography. Princeton
bird population data. Funding was provided by Peter and Helen
University Press.
Bing, Ralph and Louise Haberfeld, the Moore Family Foundation, Mendenhall, C.D., Sekercioglu, C.H., Oviedo Brenes, F., Ehrlich, P.R., Daily, G.C., 2011.
the Koret Foundation, the Mertz Gilmore Foundation, the Winslow Predictive model for sustaining biodiversity in the tropical countryside.
Proceedings of the National Academy of Sciences of the USA 108, 16313–16316.
Foundation, and a National Science Foundation graduate fellow-
Nelson, E., Cameron, R., Regetz, J., Polasky, S., Daily, G.C., 2011. Terrestrial
ship to C.D.M. biodiversity. In: Kareiva, P., Tallis, H., Ricketts, T.H., Daily, G.C., Polasky, S.
(Eds.), Natural Capital: Theory and Practice of Mapping Ecosystem Services.
Oxford University Press, Oxford, pp. 229–245.
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