Nordic Society Oikos

Determining Minimum Habitat Requirements in Theory and Practice

Author(s): C. Patrick Doncaster, Thierry Micol and Susanne Plesner Jensen
Source: Oikos, Vol. 75, No. 2 (Mar., 1996), pp. 335-339
Published by: Wiley on behalf of Nordic Society Oikos
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FORUM FORUM is intended for new ideas or new ways of interpreting existing information. It
provides a chance for suggesting hypotheses and for challenging current thinking on
F(JRUl ecological issues. A lighter prose, designed to attract readers, will be permitted. Formal
research reports, albeit short, will not be accepted, and all contributions should be concise
FORJM with a relatively short list of references. A summary is not required.

Determining minimum habitat requirements in theory and practice

C. Patrick Doncaster, Dept of Biology, University of Southampton, Bassett Crescent East, Southampton, U.K. S016
7PX - Thierry Micol, Centre d'Etudes Biologiques de Chize, Centre National de la Recherche Scientifique, F-79360
Villiers-en-Bois, France - Susanne Plesner Jensen, Large Animal Research Group, Dept of Zoology, Univ. of
Cambridge, Downing Street, Cambridge, U.K. CB2 3EJ

A central problem in conservation biology is how to
determine the amount of suitable habitat required for a
population to persist. The critical minimum is what
Lande (1987) terms the 'extinction threshold'. Lawton
et al. (1994) and Nee (1994) have pointed out the
fundamental equivalence of this quantity to the 'eradi-
cation threshold' used in epidemiology (Anderson and
May 1991). The eradication threshold defines the maxi-
mum fraction of a susceptible population that an im-
munisation programme can afford to miss, while still
succeeding in eradicating the disease. This has been
shown to equal in magnitude the uninfected fraction of
the susceptible population; in other words, it takes the
same value as the unused amount of the disease's
limiting resource (Anderson and May 1991).
For a conservation biologist, the eradication
threshold would define the smallest amount of suitable
habitat or limiting resource that can sustain a popula-
tion of animals. Lawton et al. (1994) give the example
of a metapopulation consisting of local populations
distributed among discrete patches. The metapopula-
tion is at equilibrium when a local population colonises
just one other patch before going extinct. Not all
patches are occupied at equilibrium. This scenario par-
allels the epidemiological case of a human population
of which some fraction are not immune to the disease
and are either carrying it or susceptible to it. Some
fraction, h, of the patches are habitable, and a fraction
x* among these are unoccupied at equilibrium though
susceptible to colonisation. By the simple device of
presenting the equilibrium fraction of occupied patches
as h - x*, it follows that this reaches zero (extinction of
the metapopulation) when h equals x*. In other words,
the minimum fraction of patches required to avoid
extinction, h, is simply x*, the unoccupied but suscep-
tible fraction at equilibrium. Nee (1994) likewise
demonstrates how the eradication threshold of a preda-
tor is equal in magnitude to the uneaten fraction of
limiting prey.
A population well buffered against extinction is thus
one that occupies the majority of habitable patches; or
it is one that maintains the equilibrium density of
limiting prey well below what it would be in the ab-
sence of predation. Conversely, a population that is at
risk of extinction in the event of a small reduction in
habitable patches or prey is one whose members occupy
few of the habitable patches at equilibrium, or make
little impact on the density of their prey. Such situa-
tions can arise if the habitat is highly fragmented and
dispersal incurs a substantial mortality risk. Equally a
predator might make little impact on prey density if the
prey have effective defences against predation (they are
present in numbers, but difficult to catch). It is interest-
ing to note that highly disturbed environments are
likely to be inhabited by species that use the majority of
suitable habitat, whereas historically undisturbed envi-
ronments will support species that are less efficient in
this respect. Knowledge of the unused fraction thus
provides a way of indexing environmental disturbance.
Most of the species-specific details that are com-
monly sought in conservation studies, such as migra-
tion rates between patches, foraging efficiency for
limiting prey, birth rates, death rates, etc. are superflu-
ous to this estimate of minimum habitat requirements
(Nee 1994). This conclusion has obvious consequences
for field research on rare species: the essential priority
in conservation studies is to determine accurately what
constitutes the limiting resource or the suitable habitat.
Unfortunately, this is often the most difficult objective
to realise in practice (see Caughley and Sinclair 1994
for examples). Several factors may combine to regulate
population size (Sinclair 1989). Even if their combined
influence points towards certain types of habitat as
being more suitable than others, defining exactly what

OIKOS 75:2 (1996) 335

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constitutes suitable habitat will always be problematic
for a rare species, precisely because many of its habitats
are likely to be unoccupied. Here we demonstrate the
utility of Principal Components Analysis both to define
what constitutes suitable habitat and to determine the
eradication threshold from the unoccupied fraction.
Our illustration uses empirical data on a common
species, the hedgehog (Erinaceus europaeus). Model as-
sumptions are then explored with the aid of simula-
tions.
Empirical example
Hedgehog populations show marked gradients in abun-
dance across the patchwork of farmland in rural Ox-
fordshire, UK. Within the space of about 6 km, and
within the same broad land-use category, their numbers
can range between complete absence to as many as 12
adults ha-1. Some local populations are clearly sepa-
rated from their neighbours by stretches of arable land,
or rivers and trunk roads. Those comprising just a few
individuals, occupying a rural farmhouse garden for
example, are subject to extinction and to later recoloni-
sation from neighbouring populations as far as 4 km
away. How robust is the whole metapopulation to
extinction in the event of habitat removal? We esti-
mated the correlates of hedgehog abundance within a
region of 30 x 30 km by surveying pasture fields, one of
the hedgehog's preferred foraging habitats (Micol
et al. 1994). Of the 18 environmental variables used
to characterize each of 58 independent fields, seven
were revealed by a Discriminant Function Analysis to
best separate those fields inhabited by foraging hedge-
hogs from those not used by them. These seven vari-
ables were therefore chosen for Principal Components
Analysis.
Fig. 1 shows the distribution of pasture fields in the
first two dimensions of Principal Component space.
Fields in which hedgehogs were present are all grouped
around the upper right-hand quartile of positive scores
for both factors 1 and 2. Pasture fields in which hedge-
hogs were not recorded are mainly distributed through-
out the other three quartiles.
The environmental variables contributing most
strongly to defining the first axis are found to be food
related. Fields with positive values on this axis are
associated with a high availability of earthworms, the
principal item in the diet of hedgehogs. This variable
makes no contribution to the second axis, where posi-
tive values are associated with a greater distance from
the nearest sign of badger activity (given by setts,
latrines or badgers seen). Predation by badgers is
known to influence hedgehog distribution and abun-
dance (Doncaster 1992, 1994). For both axes, negative
values are associated with greater distances from the
nearest urban settlement. These urban areas are all
336 OIKOS
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largely inaccessible to badgers but rich in food and
occupied by large numbers of hedgehogs, possibly act-
ing as 'mainland' populations (i.e. invulnerable to ex-
tinction). The occupancy of pasture fields is thus
associated with several factors, including food availabil-
ity and predation threat, both of which are interacting
with distance from the nearest mainland.
The polygon in Fig. 1 delineates h, the region of
biological space encompassing suitable areas of pasture
for foraging hedgehogs. Assuming that this habitat is
limiting, we can readily estimate how much of it is
required to ensure persistence of the hedgehog popula-
tion. The eradication threshold, h., is simply the num-
ber of empty fields within the polygon, as a fraction of
all surveyed fields. Here we have 2 out of 58, or 3%. As
the species occupies 23 of 25 suitable patches of forag-
ing pasture, it would therefore be very resistant to
eradication. Some 92% of this habitat, or 97% of all
pasture, would have to be removed to cause their
extinction.
Methodological considerations
Such a technique seems particularly well suited to stud-
ies of rare species, for which it is otherwise difficult to
distinguish between suitable and unsuitable habitat
among the unoccupied fraction. Clearly the more
patches that are surveyed, the lower will be the risk of
counting suitable but empty patches in the class of
unsuitable patches. If few patches have been surveyed
relative to the number of environmental variables, then
the sensitivity of the data to slight variations in the
2- 0
1- AE
0 - C -_ C__b
- 0-2 -1 0 1 2 3
FACTOR 1
Fig. 1. Scores for factors 1 and 2 of the Principal Components
Analysis of 58 pasture fields in Oxfordshire. Fields inhabited
by nocturnally foraging hedgehogs (filled circles) are distin-
guished from those not frequented by hedgehogs (open cir-
cles). The convex polygon surrounds all occupied fields, and
delineates the region of Principal Component space containing
suitable pasture habitat for foraging hedgehogs. Adapted from
Micol et al. (1994).
75:2 (1996)
variable values can be examined with bootstrap tech-
niques (Efron and Tibshirani 1993). The Principal
Components Analysis, nevertheless, has the same limi-
tation as any descriptive statistic, insofar as the analysis
cannot distinguish causal factors that regulate popula-
tion size from those that merely correlate with varia-
tions in size. For example, it required field
manipulations of hedgehog population sizes to demon-
strate a regulatory influence of badgers on hedgehog
abundance (Doncaster 1992, 1994), and thereby to
name this factor among other covariates as identifying
a predator axis. Where such manipulations are not
practical for rarer species, the Principal Component
axes can only be given a provisional interpretation.
Related to this is the problem of how to differentiate
unoccupied but suitable habitat from unoccupied and
inaccessible habitat. An unoccupied habitat patch lying
within the 'suitable' region of Principal Component
space should count towards the unused fraction of
suitable habitat if it is potentially accessible (for hedge-
hogs, a field surrounded by arable land with low earth-
worm abundance). But it should not be counted in this
way if it is so difficult to access that it will never be
occupied (a field surrounded by an impenetrable fence).
If isolation is a potentially limiting factor, then the
environmental variables influencing isolation should be
included in the design of the Principal Components
Analysis.
Defining what is the unused part of this area, more-
over, requires careful selection of the time-scale over
which surveying is accomplished. An animal's mini-
mum habitat requirements will be underestimated if the
unused part of its resource or habitat is underestimated,
either by surveying over too long a period or too short
a period. The survey should approximate a snap-shot of
the currently occupied fraction of suitable habitat. The
attraction of compiling a survey from repeated census
data is that it reduces the risk of failing to record
individuals that are actually present. But the associated
risk will be to include among the occupied fraction of
suitable habitat all areas colonised during the course of
the survey (while ignoring simultaneous extinctions
from other areas). This is particularly a problem for
non-territorial animals, or those with drifting home
ranges (Doncaster and Macdonald 1991, Gautestad and
Mysterud 1995), but applies also to fixed territories that
are colonised by dispersal. In the case of our hedgehog
example, occupancy of fields was evaluated from the
cumulative results of three censuses (during the same
breeding season). Hedgehogs are essentially non-territo-
rial and their ranges will drift during a season. The
proportion of unmarked animals in the surveyed popu-
lation, however, fell dramatically from the second to
the third census, giving us reason to believe that the
surveyed fields were frequented by individuals from a
stable population living in the vicinity.
OIKOS 75:2
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For animals that occupy different home ranges in
different seasons, the habitat or resource requirements
of each season must be treated separately to avoid
greatly underestimating the eradication threshold. The
hedgehogs left unoccupied 8% of suitable foraging
habitat in summer, but it is quite possible that their
habitat for winter hibernation is defined by different
constraints. Supposing the unoccupied fraction of win-
ter habitat to be 20%/0, for the population to persist it
requires at least 8%YO of existing summer habitat and at
least 20%/0 of the winter habitat.
The assumption of homogeneous mixing
The model h. = x* assumes the patches are weakly
connected by homogeneous mixing (Lawton et al.
1994), such that x* remains a constant fraction of all
patches for decreasing h; in other words, the number of
suitable but unoccupied patches does not change with
patch removal. Diminishing the quantity of suitable
habitat thereby entails an increasing unoccupied frac-
tion of h, which reaches 1 at h.. Most metapopulation
models from Levins (1969, 1970) onwards have as-
sumed the existence of an isolation effect, which in-
creases the number (as well as the fraction) of suitable
but unoccupied patches with increasing fragmentation
(reviewed in Andren 1994). This can result from re-
duced colonisation rate between patches that are still
assumed to be equally connected, so they interact ho-
mogeneously. Alternatively it can result from spatial
constraints on mixing, such as 'stepping-stone' disper-
sal. In the hedgehog example, destruction of some
surveyed patches is likely to further fragment the re-
maining suitable habitat, leaving some patches so iso-
lated as to be inaccessible to colonists at times when the
nearest other suitable habitat is also unoccupied. Their
colonisation must await the recolonisation of neigh-
bouring patches, thus increasing the number of unoccu-
pied patches. The effect of such constraints on dispersal
as these would be further exacerbated by a preferential
destruction of occupied patches. Lawton et al. (1994)
point out that the occupied fraction at the new equi-
librium following destruction is then h less the x *
susceptible fraction, less the y* transiently uninhabit-
able fraction (analogous in epidemiology to immunity
following infection). Failure to separate y* from the
equilibrium occupied fraction therefore leads to an
estimate of the eradication threshold that is smaller (by
the value of y*) than the true minimum requirement of
habitable patches.
The effect of habitat removal on persistence under
these conditions of non-homogeneous mixing can use-
fully be explored by simulations. Hanski's (1994) model
for the probability of occupancy of a set of habitat
patches provides a realistic framework for simulating
patch destruction across a spectrum of connectivity
(1996) 337
 100 (a) 100-

Cl) 75 ( 75-

n) 50 15 501
LU LU

D 22

T-~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~T

25- 25-

0 II0 1+
0 50 100 150 200 0 50 100 150 200
YEARS YEARS

100- (b) Fig. 2. Simulation of metapopulation dynamics in the 100 yr

preceding and following random patch removal. In the hypotheti-
cal example, incidence probabilities were calculated yearly using
Hanski's (1994) discrete time model incorporating the rescue
,I,0 75- e effect. The model started with 75 occupied patches out of 100
habitable patches, varying in size at random between 2 and 20 ha,
H W yand distributed at random within a 123-km2 area. The constants
in the model were set at y' = 10, a = 0.26, e = 2.74, x = 2 (see
o 50- Hanski 1994 for symbol definitions). Variation in the number of
occupied patches before and after patch removal in year 100 is
32 plotted for 10 metapopulation runs. Those runs that ended in
C)
0 extinction are shown stippled in the figures. (a) Removal of the
of 25- mean fraction concurrently occupied over the first 100 yr, leaving
intact the equilibrium unoccupied fraction (26 patches on average
for the 10 runs); 4 runs persist for 100 yr following removal, while
6 go to extinction. (b) As for (a) but leaving intact 5 patches more
0 than the mean unoccupied fraction; 8 runs persist for > 80 yr, and
0 50 100 150 200 6 for 100 yr following removal. (c) As for (a) but leaving intact 5
patches less than the mean unoccupied fraction; 9 of the 10 runs
YEARS go to extinction within 50 yr of removal.

under conditions of heterogeneous interaction. The
model describes the incidence function for the ith
patch, Ji = Ci/(Ci + E), where the colonisation proba-
bility (C1) is a function of patch isolation, and the
extinction probability (Ei) is a function of patch area.
A metapopulation with no constraints on colonisation
has all Ci = 1, and therefore Ji = 1/(1 + E). Regardless
of how many patches are removed, the number occu-
pied is a constant fraction of those remaining, and
dependent only on the patch size criteria defining E,.
The incidence function increases to unity for all patches
at Ci = 1, if the 'rescue effect' is taken into account.
Dispersal propensities that are selected to compensate
for extinctions, so that fragmented habitats are rescued
by this factor (Hanski 1991), are incorporated by mod-
ifying the incidence function to take the form Ji = Ci/
(C + E, - C1E,).
Persistence of the metapopulation is influenced by
patch removal in these models only with the introduc-
tion of constraints on connectivity between patches, so
that more isolated patches are less frequently colonised.
These constraints on dispersing ability (y' > 0 in Han-
ski's definition of C,) have the effect of increasing the
unoccupied fraction of remaining suitable habitat fol-
lowing patch removal. Reduced connectivity between
local populations resulting from distance-dependent
dispersal and the rescue effect, can then be made to
emulate the eradication threshold. This is shown by
Fig. 2(a) which illustrates persistence before and after
removal of all but the average unused fraction from 100
suitable patches. Removing just five patches less (b) or
more (c) than this makes the difference between persis-
tence and extinction. Where removal of the used frac-
tion does not result in imminent extinction, it leaves the
population occupying on average about 25% of the
remaining patches. The fraction of habitable patches
that are unoccupied therefore quadruples and, with
random variations in incidence, this is usually enough
to cause extinction. It is these random fluctuations that
cause the metapopulations to go extinct despite the
actual number of unoccupied habitable patches unreal-
istically decreasing with patch removal by up to 25%.
Without these fluctuations, rather stronger constraints
on dispersal would be required to simulate the eradica-
tion threshold by maintaining a constant number of
unoccupied habitable patches with patch removal.
This outcome can be explained in terms of transient
unavailability of patches, as defined above by y*. Be-

338 OIKOS 75:2 (1996)

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cause of the constraints on mixing, the unoccupied
fraction before patch removal includes some patches
that must await colonisation of their neighbours before
they in turn can be colonised. In Fig. 2 this is equiva-
lent to the number of habitable patches (h) in the first
100 years being less than 100 by this y** transiently
unavailable fraction. Or equivalently, the unoccupied
habitable fraction is x * - y**. When y** equals the
fraction y * that become transiently unavailable on re-
moval of patches, then the occupied fraction is
h-(x*-y**)-y*=h-x*. The prediction h, = x*
can therefore be reproduced by this level of spatial
constraints on mixing, if y** is included in the esti-
mated value of x*. We have assumed that it contributes
to the unoccupied fraction in the first 100 years of the
simulations in Fig. 2. It could also have been included
within the polygon in Fig. 1, if one of the two empty
patches is acting as a stepping stone to the colonisation
of the other, and this spatial constraint has not been
compensated by an additional Principal Component for
isolation. In the hedgehog example, however, the occu-
pied fraction is so high that the eradication threshold is
only approached with a large reduction in h, which is
likely to lead to y* taking a higher value than y**. This
would then reproduce the prediction of Moilanen and
Hanski (1995) that accounting for real-life ingredients
such as distance-dependent dispersal and the rescue
effect will tend to increase the number of unoccupied
habitable patches with decreasing h.
Conclusions
Conservation biology has much to gain from this cross-
fertilisation with epidemiology. Despite the apparent
simplicity of h, = x*, species specific details of popula-
tion dynamics remain an important element of deter-
mining minimum habitat requirements. They are
needed for estimating what constitutes suitable habitat,
and for testing the assumptions that the species is
present at equilibrium density and that the limiting
habitat or resource is homogeneously accessible. Suit-
able tools are available, however, for classifying the
biological information. Principal Components Analysis
has obvious attractions for determining the unoccupied
fraction of suitable habitat. Such techniques should be
complemented with additional modelling of resource
homogeneity and, ideally, experimental manipulation to
distinguish regulating from limiting factors.
OIKOS 75:2
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Acknowledgements - We would like to thank J. D. Goss-
Custard for suggesting the applicability of Principal Compo-
nents Analysis to the subject of eradication thresholds, E.
Danchin for creative insights, and S. Nee and an anonymous
reviewer for helping to clarify concepts. This study was sup-
ported by the Biotechnology and Biological Sciences Research
Council, and by grants from the European Community -
Human, Capital and Mobility (to CPD and SPJ), and the
British Council (to TM).
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