Download Extinction, Colonization, and Metapopulations: Environmental

Extinction, Colonization, and
Metapopulations: Environmental
Tracking by Rare Species
C. D. THOMAS
School of Biological Sciences
The University of Birmingham
Edghaston, Birmingham
B15 2TT, England
Abstract: Extinction and metapopulation theories emphasize that stochastic fluctuations in local populations cause
extinction and that local extinctions generate empty habitat
patches that are then available f o r recolonizatiorL Metapopulation persistence depends on the balance o f extinction and
colonization in a static environment For many rare and
declining specie~ I argue (1) that extinction is usually the
deterministic consequence o f the local environment becoming unsuitable (through habitat loss or modification, introduction o f a predator, eta); (2) that the local environment
usually remains unsuitable following local extinction, so
extinctions only rarely generate empty patches o f suitable
habitat; and (3) that colonization usually follows improvement o f the local environment f o r a particular species (or
long-distance transfer by humans). Thus, persistence depends predominantly on whether organisms are able to
track the shifting spatial mosaic o f suitable environmental
conditions or on maintainance o f good conditions locally.
Extinction
Over the past 20 years, extinction models have b e e n
applied increasingly to populations of endangered species. Typically, an estimate is made of the median ( o r
m a x i m u m ) population size that could be sustained in a
Paper submitted July 17, 1993; revised manuscript accepted October
13, 199~
Extinci6n, colonizaci6n y metapoblaciones: adecuaci6n
ambiental de especies raras
Resumen: Las teorias sobre exttnci6n y metapoblaciones
enfatizan que ftuctuaciones estocdsttcas en poblaciones locales causan la extinci6n y que la extinci6n total genera
parches de hdbitat vacios que estdn entonces disponthles
para la recolonizaci6rL En un ambiente estdtico, la persistencla de la metapoblaci6n depende del balance entre extinclones y colonizacionex Yo sostengo que para muchas especies raras y e n declinaci6n, (t) usualmente la extinci6n es
una consecuencia deterministica de un ambiente local que
se hace inadecuado (e.g., pddtda o modificaci6n del hdbita~
introducci6n de un predador, eta); (ii) usualment¢ el ambiente local permanece inadecuado It,ego de la extinct6n
local p o r consiguient¢ s61o rarament¢ extinciones locales
generan parches vacios de habitats adecuados; y (ii 0 usualmente la colonizacion viene despu~s de la mejora de las
condiciones ambientales para una especie en particular (o
la transferencla a larga dtstancla p o r humanos). Por consiguiente, la persistencia depende predominantemente de
que los organismos puedan adaptarse al mosaico espacial
cambiante de las condiciones ambientales o de que se mantengan buenas condiciones localex
reserve, and the probability of persistence is calculated
by adding stochastic variation to birth and death, either
separately or combined. Variation is usefully divided
into demographic stochasticity that affects the chance
birth and death events of individuals independently, environmental stochasticity that affects average birth and
death rates in each generation, and environmental catastrophe that can result in extinction regardless of initial population size (May 1973; Shaffer 1981). Genetic
stochasticity and feedback into the population parameters may also be important. The combination of relatively small population size and stochastic variability un373
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F~vironmenmlTracing by Rare Species
Thomas
derpinned almost all extinction models of the 1970s and
1980s (see Richter-Dyn & Goel 1972; Leigh 1981; Shaffer & Samson 1985; Strebel 1985).
In most of these extinction models, mean birth and
death rates w e r e assumed to be equal in the long term,
even if stochasticity varied the rates from generation to
generation. The models generated a decreasing probability of extinction with increasing population size, so
the object of conservation was to prevent stochastic
local extinction by achieving a minimum viable population size. Estimates of m i n i m u m viable population size
w e r e often so large that few if any remnant populations
w e r e considered large enough to be viable, at least for
large terrestrial vertebrates. The objective of a new approach to extinction models is to balance stochastic
local extinctions by recolonization, usually through
multiple reserves and corridors (see Boyce 1992; Nunn e y & Campbell 1993).
But do stochastic causes of extinction really merit the
attention they have b e e n given? If direct or indirect
modification of the environment by humans results in a
mean birth rate that is persistently lower than the mean
death rate, on average individuals do not replace themselves. In such cases organisms are on an inevitable,
deterministic slide to extinction, the time taken to extinction depending on the initial population size and the
extent to which the death rate is greater than the birth
rate. Although deterministic causes of extinction have
b e e n widely recognized (see Shaffer 1981; Gilpin &
Soul6 1986; Simberloff 1988), particularly in empirical
work, the clear emphasis of theory and reviews has b e e n
on the importance of different types of stochasticity. It
can be argued that simple models are not applied to real
endangered populations and metapopulations, but the
conceptual basis of these models pervades conservation
thinking (see reviews by Boyce 1992; Nunney & Campbell 1993).
The evidence from real population and species extinctions is that extinction is normally deterministic. A
m a j o r r e v i e w of species extinctions ( G r o o m b r i d g e
1992) has revealed that m o s t animal extinctions are
caused by direct hunting by humans, introductions of
species with which the extinct species could not coexist, and loss of habitat (Table 1). "Habitat alteration"
plus "natural" extinctions place a ceiling on the proportion of species extinctions in which stochastic processes
could have played a significant part. This p r o p o r t i o n is
about half for invertebrates and aquatic vertebrates and
a quarter for terrestrial vertebrates (Table 1). In fact,
stochasticity is important to far fewer species: in m a n y
cases virtually the entire habitat was lost or modified,
causing 100% mortality. Stochastic extinction from surviving habitat fragments is minor b.y comparison.
The story is similar for population extinctions. Most
extinctions of any but the smallest populations are determined by persistent changes in the local environm e n t (Harrison 1991; C.D. Thomas 1993, 1994), and
large populations are not i m m u n e to these changes (J. A.
Thomas 1991). For British butterflies, almost all local
extinctions can be attributed to c o m p l e t e habitat loss
(through, for example, agricultural conversion) or to
m o r e subtle changes in the vegetation (such as short
grass to slightly longer grass, resulting in the elimination
of short-grass species). The latter could mistakenly be
classifed as "stochastic extinction" in the absence of
detailed knowledge of the precise habitat requirements
of individual species. D o c u m e n t e d extinctions of local
butterfly populations from nature reserves are almost
always associated with clear, albeit subtle, changes in
the habitat that r e m o v e conditions required by a particular species (J.A. Thomas 1991; W a r r e n 1993). Although unusual weather (temporal environmental stochasticity) has been responsible for several well-cited
examples of local butterfly extinctions (see Ehrlich et al.
1980), most local extinctions appear to be deterministic
responses to persistent changes in the local environm e n t (C. D. Thomas 1993, 1994). Typically, population
stochasticity is important only in the last generations,
w h e n the fate of a population has already b e e n sealed.
With a stochastic approach based on m e a n birth and
death rates being equal to one another, there is little a
conservation manager can do other than ensure that the
original population size is large. This may be good advice, but it does little to help managers p r e v e n t declines
in the short term or establish recovery programs. With
a m o r e deterministic approach, models can be used to
explore ways of maximizing birth rates and minimizing
death rates.
A shift is n o w taking place in this d i r e c t i o n m t o w a r d
models that concentrate on factors that determine population trends yet recognize that stochastic variability
will be superimposed on the trend ( H o c h b e r g et al.
Table 1. Causes of species extinctions (% a) (after Groombridge 1992).
Invertebrates (n = 72)
Aquatic Vertebrates (n = 28)
Terrestrial Vertebrates (n = 111 )
Human
Predation b
Introduced
Species
Indirect
Effects
Habitat
Alteration
"Natural"
Causes
16
8
30
33
37
46
1
4
1
49
50
22
1
1
0
a Percentages given have been rounded to the nearest whole number.
Includes species consumed as food, exploited for other biological products, and deliberately eliminated as pests.
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Thomas
EnvirograentalTrackingby Rare Species
375
1992; Burgman et al. 1993). Starting population size
needs to b e known, m e a n birth and death rates measured ( o r the net effect calculated from past changes in
population size), and, if possible, the strength and type
of density-dependence estimated. As with stochastic extinctions, deterministic extinctions are m o r e likely to
take place in small rather than large populations because
( 1 ) for a given decline, small populations are likely to
b e c o m e extinct sooner than large ones, and ( 2 ) large
populations usually inhabit relatively large areas, such
that local habitat deterioration will probably not affect
the entire area simultaneously (C. D. Thomas 1991,
1994). Stochasticity in birth and d e a t h w i l l still play an
important role and can be included, but the m e a n rates
are crucial ( m e a n birth = mean death is just a special
case). W h e n particular habitat components, such as predation by humans or distributions' of other species, affect m e a n birth and death rates (and also immigration
and emigration), the implications of specific habitat
conditions and m a n a g e m e n t can be predicted (Hochberg et al. 1992; Burgman et al. 1993).
Stochastic models are likely to be important only
w h e r e deterministic pressures have o c c u r r e d and have
then b e e n alleviated. Conservation efforts should concentrate first on ensuring that birth exceeds or equals
death and should w o r r y about stochasticity second. Provided that birth exceeds death at low population dens i t y m t h a t t h e r e is s o m e d e n s i t y - d e p e n d e n c e - - - e v e n
quite small populations may survive well.
unavailable for recolonization. For example, this w o u l d
be the case if a species is eliminated from a patch of
habitat because of vegetation succession, or if a species
is eliminated from an island after the arrival of rats. The
local e n v i r o n m e n t may or may not b e c o m e suitable
again, depending on future events. Thus, the major process that creates e m p t y habitat in metapopulation models does not operate widely in nature. This is crucial. In
m o s t metapopulation models, stable equilibria o c c u r because a stochastic increase in extinction generates an
increased n u m b e r of habitat patches available for colonization, so there is a corresponding increase in colonization. If the link b e t w e e n extinction and subsequent
colonization is broken, so is the basis for equilibrium.
It is important, therefore, to recognize the events that
p r e c e d e colonization in nature. Working with British
butterflies, I have identified six general ( n o t entirely
distinct) contexts in which natural colonizations are observed (Thomas 1993).
Colonization and Metapopulations
2. Creation of New "Permanent" Habitat Close to
Existing Populations
Notwithstanding the above arguments, models and empirical observations suggest that very small populations
are relatively likely to b e c o m e extinct (see Soul~ 1986;
Lande 1988; Simberloff 1988; Thomas 1990; Kindvall &
Ahl6n 1992), and, alas, m a n y local populations in remnant habitat fragments are and will remain small. If habitat remains suitable following local extinction, recolonization of the n o w - e m p t y habitat may replace at least
some of these losses. The pessimistic view of continuing, inevitable extinctions has given way in the past five
years to some degree of optimism that a balance may be
reached b e t w e e n local extinctions and colonization.
Metapopulation dynamics provide the theoretical basis
for this optimism, and the approach is fast b e c o m i n g the
n e w vogue in conservation biology (Gilpin & Hanski
1991; Harrison 1994).
Harrison (1991, 1994) and Thomas ( 1 9 9 3 ) question
w h e t h e r there is likely to be a balance b e t w e e n extinction and colonizations in m o s t natural systems, particularly w h e r e endangered species are concerned. If the
cause of extinction is a deterministic population response to unsuitable conditions, the local habitat is
likely to remain unsuitable after extinction and so be
Freshly created habitats on road verges, railway embankments, and wide forest tracks (associated w i t h
mechanized timber extraction) have b e e n colonized by
many species of butterfly (Warren 1984; Munguira &
T h o m a s 1992). Changes in the c o n d i t i o n of longestablished habitats have also b e e n exploited by butterflies. Rabbit grazing was virtually eliminated from calcareous grasslands in Britain following the introduction
of the disease myxomatosis in the 1950s. Due to the
resultant increase in long-turf habitat, one skipper butterfly, Thymelicus acteo~ colonized many n e w localities that subsequently b e c a m e dominated by its host
plant (J. A. Thomas 1983). Over the same period, populations of a short-grass skipper, Hesperia c o m m ~ declined. Recovery of rabbit populations in the last 15
years has resulted in H. c o m m a colonizing at least 29
patches of grassland as new areas of short-turf habitat
have b e c o m e available ( T h o m a s & Jones 1993).
1. Disturbance and Succession
Following natural disturbance or h u m a n management,
species colonize specific seral stages of a particular vegetation. Some generations later, they are eliminated b y
succession. Examples include Mellicta athalia~ w h i c h
colonizes fresh woodland clearings (Warren 1991 ), and
Melitaea cinxig which colonizes crumbling cliffs (Sirecox & Thomas 1979). The dynamics of the endangered
plant Pedicularisfurbishiae on river banks appear to be
similar (Menges 1990).
3. Introductions Outside of Range
Releasing butterflies in n e w areas, beyond their normal
dispersal capacity, sometimes results in a w h o l e series of
fresh colonizations. Thomas and Harrison ( 1 9 9 2 ) give
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an example. Introductions of m a n y species around the
w o r l d fall into this category.
4. Increases in Range
Following changes in climate or widespread changes in
habitat, several sp.ecies have expanded their ranges. Ladoga camilla expanded its range in the relatively w a r m
weather of the 1930s and 1940s, w h e n British woodlands b e c a m e m o r e shaded and h e n c e m o r e suitable for
this species (Pollard 1979); Pyronia tithonus has expanded its range over the last 30 years (Pollard 1991).
5. Turnover-Prone Peripheral Patches
In the absence of deterioration in the local environment, most extinctions are confined to the smallest habitat patches (Schoener & Spiller 1987; Harrison 1991;
Schoener 1991). These patches then b e c o m e available
for recolonization. Following recolonization, very small
patches of habitat support short-lived local populations
that are unimportant to overall persistence. A similar
argument can be made for population "sinks" in p o o r
habitat.
6. Seasonal Spread
In fairly mobile species, a mixture of contexts four and
five may be seen. Some species may survive inhospitable
periods (winter, dry season) in favorable refuges (warm,
mesic) and spread m o r e widely in favorable seasons
(Shapiro 1979; DeVries 1987; J o r d a n o et al. 1991).
Metapopulation theory is not appropriate for such mobile species. True migration is an extension of the phenomenon.
These contexts share the vital condition that a species
has recently c o m e into contact with favorable but unexploited environmental conditions. In most cases, previously uninhabitable localities have only recently bec o m e suitable. I am n o t a w a r e of any c o n v i n c i n g
example of a local extinction that left vacant habitat that
was immediately suitable for a new, viable, persistent
population. Following contact, colonization is distancedependent; it is probabilistic but predictable (Thomas
et al. 1992; Thomas 1993, 1994; Thomas &Jones 1993).
Although the observed events preceding colonizations necessitate modification of most existing metapopulation models, there is a positive message for conservation managers. If real colonizations follow an imp r o v e m e n t in habitat quality or transfers of organisms
over long distances, as they seem to, a manager can
attempt to increase rates of colonization by creating
n e w habitats and restoring connectivity. This is vital.
Many British butterflies are declining because the creation of n e w habitats has decreased rather than because
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Volume8, No. 2,June 1994
Thomas
local extinction rates from existing habitats have increased (Thomas. 1993).
Mosaics and Metapopulations
I argued that habitat dynamics rather than stochastic
factors are the key to the persistence of m a n y real populations and metapopulations. Most extinctions are the
result of deterministic population responses to a deterioration of conditions; m o s t observed colonizations follow an i m p r o v e m e n t in conditions near an existing local
population or the transfer of organisms across some barrier to dispersal. Species track suitable environmental
conditions, becoming locally extinct w h e r e conditions
are no longer suitable for them and colonizing w h e r e
conditions improve ( o v e r limited distances). Species
persist in regions w h e r e they are able to track the environment, and they b e c o m e extinct if they fail to keep
up with the shifting habitat mosaic. For many island
species, the loss of suitable e n v i r o n m e n t conditions
throughout their limited range has resulted in species
extinction.
The d e v e l o p m e n t of m e t a p o p u l a t i o n t h e o r y has
played a crucial role in expanding our perspective on
local to regional persistence, but existing models need
to be superimposed on an environmental mosaic which
in many cases will itself be spatially dynamic (see Southw o o d ' s [1977] habitat templet theory). This approach
has advantages over existing metapopulation theory.
Emphasis on the deterministic factors that cause species
declines and population extinctions will focus attention
on those factors that must be manipulated if a decline is
to be checked. Emphasis on changes in the environment
that p r e c e d e colonization will focus attention on factors
that could result in species recovery.
Can n e w m a n a g e m e n t a p p r o a c h e s create suitable
habitat within colonization distance? If not, can sufficiently large areas of suitable habitat be created elsew h e r e that would support separate, viable populations,
or can networks of habitat be created and p r o t e c t e d
elsewhere that would support n e w viable metapopulations following introduction? The environmental mosaic
approach also shifts the emphasis away from discrete
patches. Population declines in large patches may b e as
worrying as local extinctions in small patches, and expansion of patches may be as valuable as colonization of
small additional patches. Decreases and increases in
patch areas may be as amenable to m a n a g e m e n t as
losses and gains of whole patches. Patch enlargement
and i m p r o v e m e n t of the quality of existing patches are
important conservation options.
An environment mosaic perspective shifts the emphasis onto transient dynamics and away from the equilibrium (balance) concept of metapopulation dynamics,
Thomas
for w h i c h there is little e v i d e n c e in nature (Harrison
1994). Rates o f e x t i n c t i o n and colonization are important to persistence, b u t t h e y can b e in balance only
w h e n the e n v i r o n m e n t is static o r w h e n the loss and
creation o f suitable e n v i r o n m e n t a l conditions are themselves in balance.
If m o s t major c h a n g e s in the distribution o f relatively
sedentary species are driven b y changes in the spatial
distribution o f suitable habitats, as I believe, conservation m u s t focus o n maintaining habitat continuity. For
species o c c u p y i n g persistent habitats, the emphasis is
o n habitat preservation. For species o c c u p y i n g shortlived or d y n a m i c habitats, the emphasis is o n ( 1 ) preservation and m a n a g e m e n t o f existing habitats, ( 2 ) preservation of sufficiently large areas or connected
n e t w o r k s o f reserves that natural d y n a m i c s can be relied
o n to p r o d u c e n e w habitats, and ( 3 ) creation of n e w
habitats w i t h i n colonization distance.
Acknowledgements
F~¢iromne~tal T ~ g
by Rare Species
377
Harrison, S. 1994. Metapopulations and conservation. Symposium of the British Ecological Society in press.
Hochberg, M. E., J. A. Thomas, and G. W. Elmes. 1992. A modelling study of the population dynamics of a large blue butterfly, Maculinea rebelg a parasite of red ant nests. Journal of
Animal Ecology 61:397-409.
Jordano, D., E.C. Retamosa, and J. Femfindez Haeger. 1991.
Factors facilitating the continued presence of Colotis evagore
(Klug, 1829) in southern Spain. Journal of Biogeography
18:637-646.
Kindvall, O., and I. Ahl6n. 1992. Geometrical factors and
metapopulation dynamics of the bush cricket, Metrioptera hicolor Philippi (Orthoptera: Tettigoniidae). Conservation Biology 6:520-529.
Lande, IL 1988. Genetics and demography in biological conservation. Science 241:1455-1460.
Leigh, E.G. 1981. The average lifetime of a population in a
varying environment. Journal of Theoretical Biology 90:21 3 239.
Thanks to Resit Akqakaya and Susan Harrison.
May, R.M. 1973. Complexity and stability in model ecosystems. Princeton University Press, Princeton, New Jersey.
Literature Cited
Menges, E.S. 1990. Population viability analysis for an endangered plant. Conservation Biology 4:52-62.
Boyce, M. S. 1992. Population viability analysis. Annual Review
of Ecology and Systematics 23:481-506.
Burgman, M.A., S. Ferson, and H.R. Ak~akaya~ 1993. Risk assessment in conservation biology. Chapman & Hall, London,
England.
DeVries, P.J. 1987. The butterflies of Costa Rica and their
natural history. Princeton University Press, Princeton, New
Jersey.
Ehrlich, P. R., D. D. Murphy, M. C. Singer, C. B. Sherwood, R. IL
White, and I. L. Brown. 1980. Extinction, reduction, stability
and increase: The response of checkerspot butterfly (Euphydryas editha) populations to the California drought. Oecologia 46:101-105.
Munguira, M. L., and J. A. Thomas. 1992. Use of road verges by
butterfly and burnet populations, and the effect of roads on
adult dispersal and mortality. Journal of Applied Ecology,
29:316-329.
Nunney, L., and K. L Campbell. 1993. Assessing minimum viable population size: Demography meets population genetics.
Trends in Ecology and Evolution 8:234-239.
Pollard, E. 1979. Population ecology and change in range of
the white admiral butterfly Ladoga camilla L. in England. Ecological Entomology 4:61-74.
Pollard, E. 1991. Changes in the flight period of the hedge
brown butterfly Pyronia tithonus during range expansion.
Journal of Animal Ecology 60:737-748.
Gilpin, M., and I, Hanski, editors. 1991. Metapopulation dynamics: Empirical and theoretical investigations. Academic
Press, London, England.
Richter-Dyn, N., and N. S. Goel. 1972. On the extinction of a
colonizing species. Theoretical Population Biology 3:406433.
Gilpin, M., and M. E. Soul6. 1986. Minimum viable populations:
Processes of species extinctions. Pages 19-34 in M. E. Souh~.,
editor. Conservation biology: The science of scarcity and diversity. Sinaur Associate, Sunderland, Massachusetts.
Schoener, T.W. 1991. Extinction and the nature of the metapopulation: A case system. Acta Oecologia 12:53-75.
Schoener, T. W., and D. A. Spiller. 1987. High population persistence in a system with high turnover. Nature 330:47 ~. A.77.
Groombridge, B., editor. 1992. Global biodiversity. Status of
the Earth's living resources. Chapman & Hall, London, England.
Shaffer, M. L. 1981. Minimum population sizes for species conservation. BioScience 31:131-134.
Harrison, S. 1991. Local extinction in a metapopulation context: An empirical evaluation. Biological Journal of the Linnean
Society 42:73--88.
Shaffer, M. L., and F. B. Samson. 1985. Population size and extinction: A note on determining critical population size. American Naturalist 125:144-152.
Conservation Biology
Volume 8, No. 2, June 1994
378
EnvironmentalTrack~ by Rare Species
Shapiro, A. M. 1979. Weather and the lability of breeding populations of the checkered white butterfly, Pieris protodtce
Boisduval and LeConte. Journal of Research on the Lepidoptera 17:1-23.
Simberloff, D. 1988. The contribution of population and community biology to conservation science. Annual Review of
Ecology and Systematics 19:473-511.
Simcox, D.J., and J.A. Thomas. 1979. The Glanville fritillary.
Joint Committee for the Conservation of British Insects, Furzebrook, England.
Soul6, M. E., editor, 1986. Conservation biology: The science
of scarcity and diversity. Sinauer Associates, Sunderland, Massachusetts.
Southwood, T. 1L E. 1977. Habitat, templet for ecological strategies. Journal of Animal Ecology 46:337-365.
Strebel, D.E. 1985. Environmental fluctuations and extinction---single species. Theoretical Population Biology 27:1-26.
Thomas, C. D. 1990. What do real population dynamics tell us
about minimum viable population sizes? Conservation Biology
4:324-327.
Thomas, C. D. 1991. Spatial and temporal variability in a butterfly population. Oecologia 87:577-580.
Thomas, C.D. 1994. Local extinctions, colonizations and distributions: Habitat tracking by British butterflies. In press in
S. R. Leather, A. D. Watt, N.J. Mills, and K. F. A. Waiters, editors.
Individuals, populations, and patterns in ecology. Intercept
Ltd., Andover, England.
ConservationBiology
Volume 8, No. 2, June 1994
Thomas
Thomas, C.D. 1994. Essential ingredients of real metapopulations, exemplified by the butterfly Plebejus argug In press in
M. E. Hochberg J. Clobert, and IL Barbault, editors. Aspects of
the genesis and maintenance of biological diversity. Oxford
University Press.
Thomas, C.D., and S. Harrison. 1992. Spatial dynamics of a
patchily-distributed butterfly species. Journal of Animal Ecology 61:437-446.
Thomas, C.D., and T.M. Jones. 1993. Partial recovery of a
skipper butterfly (Hesperia comma) from population refuges:
Lessions for conservation in a fragmented landscape. Journal of
Animal Ecology 62:472-481.
Thomas, C. D., J. A. Thomas, and M. S. Warren. 1992. Distributions of occupied and vacant butterfly habitats in fragmented
landscapes. Oecologia 92:563-567.
Thomas, J.A. 1983. The ecology and status of Thymeltcus
acteon (Lepidoptera: Hesperiidae) in Britain. Ecological Entomology 8:427-435.
Thomas, J. A. 1991. Rare species conservation: Case studies of
European butterflies. Symposium of the British Ecological Society 31:149-197.
Warren, M. S. 1984. The biology and status of the w o o d white
butterfly. Entomologist's Gazette 35:207-223.
Warren, M. S. 1991. The successful conservation of an endangered species, the heath fritillary butterfly Melltcta athaltag in
Britain. Biological Conservation 55:37-56.
Warren, M. S. 1993. A review of butterfly conservation in central southern Britain. I. Protection, evaluation and extinction
on prime sites. Biological Conservation 64:25-35.