Download Interspecific competition in metapopulations

Biological Journal of the Linnean Sociev (1991), 42: 219-237. With 2 figures
Interspecific competition in metapopulations
JAN BENGTSSON
Department of Ecolosy and Environmental Research, Swedish University of Agricultural
Sciences, Box 7072, S-750 07 Uppsala, Sweden
The assumptions and predictions of metapopulation models for competing species are discussed in
relation to empirical studies of colonization and extinction in metapopulations. I n three species of
Daphnia in rockpools, interspecific competition increased local extinction rates, while no effects on
colonization rates were detected. Distributional patterns were consistent with several predictions of
the competition model; for example, the number of species on an island increased with the number
of pools and the proportion of pools occupied by each species decreased with increasing species
number. I t is concluded that interspecific cornpetition is important for the distributional dynamics of
Dophnia species in rockpools, but the question whether the coexistence of these species depends on
metapopulation dynamics is still unresolved. Other studies on the effects of interspecific competition
on colonization and extinction rates are discussed.
KEY WORDS-Metapopulations
Daphnia - rockpools.
- interspecific competition - extinction - colonization - dispersal
-
CONTENTS
Introduction . . . . . . . . . . . . . . .
Assumptions and predictions ofcompetition models.
. . . . .
A case study: Daphnia in rockpools . . . . . . . . . .
The assumptions . . . . . . . . . . . . .
EKects of interspecific competition on colonization and extinction rates
Dispersal and competitive abilities . . . . . . . . .
Estimating model parameters for rockpool Daphnia . . . . .
Testing the predictions
. . . . . . . . . . .
Conclusions . . . . . . . . . . . . . .
Studies of interspecific competition in metapopulations . . . . .
Effects of competition on colonization rate . . . . . . .
Effects of competition on extinction rate . . . . . . .
No effects of interspecific competition . . . . . . . .
Is metapopulation strurture essential for coexistence? . . . .
Acknowledgements
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References
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INTRODUCTION
The single-species metapopulation model formulated by Levins ( 1969) was
soon extended to two or more competing species to investigate the effects of
spatial heterogeneity on the coexistence of similar competitors (e.g. Levins &
Culver, 1971; Horn & MacArthur, 1972; Levin, 1974; Slatkin, 1974; Armstrong,
1976; Hanski, 1983). In contrast to most Lotka-Volterra-based models, which
predict that similar competitors cannot coexist, these models suggested that
patchiness allowed coexistence of similar or even identical species. One
00244066/91/010219+ 19 $03.00/0
219
0 1991 The Linnean
Society of London
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J. BENGTSSON
mechanism permitting the coexistence of species with similar niches was a tradeoff between good dispersal and good competitive abilities, a notion involved
already in the concept of ‘fugitive species’ (e.g. Hutchinson, 1951; Skellam,
1951).
These metapopulation models of interspecific competition have rarely been
related to empirical observations of species’ distributions and regional dynamics.
Levins et al. (1973) discussed competition and the distribution of ant species on
islands around Puerto Rico in terms of a single-species model. Keddy (1976)
used a single-species model derived from MacArthur & Wilson (1967) to analyse
the distributions of two Lemna species in ponds. The distribution of Duphnia
waterfleas in rockpools (Hanski & Ranta, 1983) and seabirds on islands (Caraco
& Whittam, 1984) have been discussed using metapopulation models for
competing species, but most field studies of interspecific competition have been
conducted without regard to the regional dynamics of the species. In the present
paper the assumptions, predictions and existing empirical data on the effects of
interspecific competition in metapopulations will be reviewed. A case study,
three species of Daphniu living in rockpools, will be discussed in some detail, and
it will be argued that the key theoretical question, i.e. whether a metapopulation
structure allows similar competitors to coexist, remains unresolved.
ASSUMPTIONS AND PREDICTIONS OF COMPETITION MODELS
In the metapopulation models for two or more species (e.g. Levins & Culver,
1971; Slatkin, 1974; Armstrong, 1976; Hanski, 1983; Hanski & Ranta, 1983),
the proportions of habitat patches inhabited by each species are modelled in
relation to migration and extinction rates, which both may be affected by
interspecific competition. In the single-species version, the change in the
proportion of occupied patches is
where p = NIT, the proportion of patches occupied, N is the number of
inhabited patches, 7is the total number of suitable patches in the region, and m
and e are migration and extinction parameters respectively. Interspecific
competition is introduced into this model by assuming that the colonization
parameter of a species decreases with an amount p when patches contain
another species, and that the extinction parameter increases with an amount E in
patches where both species are present (Slatkin, 1974; Hanski, 1983).
The basic two-species model of Slatkin (1974) models changes in the
proportions of patches occupied by neither of the species, Po: by species 1 alone,
PI,by species 2 alone, P2, and by both species, P,. For simplicity, the proportion
of patches with species 1 is defined as TI = P I +p3, and in the same way
K2 = p 2 + p 3 . The rates of extinction of species 1 are eg, in patches where it is
alone, and (e,+E,,)p, in patches where both species are together. The rate of
colonization of empty patches of species 1 is proportional to the proportion of
patches occupied by the species, TI, and its ability to disperse and colonize,
measured by the colonization parameter m,, i.e. m,T,po. Similarly, its rate of
colonization of patches with species 2 is ( m ,-p12)Yg,.Thus E , , and p,, measure
IN'I'ERSPECIFIC COMPETITION
22 1
the competitive effect of species 2 on species 1. The parameters e2, gpl, m2 and pZl
are defined in the same way. If stochasticity is ignored, the equations for this
system are:
Since po+p, +p2+p3 = 1, only three of the equations are independent of each
other.
It has been found difficult to solve these equations analytically for internal
equilibria, and therefore only the conditions allowing the invasion of a second
species have been studied (Slatkin, 1974; Hanski, 1983; Hanski & Ranta, 1983).
The two-species model has been extended to more than two species (Hanski &
Ranta, 1983; Caraco & Whittam, 1984).
Although details may differ between particular multi-species models, they
usually make a number of similar assumptions:
Al. The regional distribution of the species can be modelled as a
metapopulation process, i.e. extinctions and colonizations occur with measurable
frequencies.
A2. The rates of extinction and colonization are affected by interspecific
competition.
A3. Local (within-patch) dynamics are usually assumed to occur at a faster
time scale than regional dynamics (for a discussion see Hanski, 1983).
A4. Related to assumptions A3 and A6 (below) extinction probabilities are,
apart from competitive effects, assumed to be constant for each population of a
species, regardless of, for example, population sizes and dispersal, and extinction
events are assumed to be uncorrelated between patches. The effects of relaxing
the assumptions A3 and A4 have been discussed by Hanski (1983, 1985).
A5. Colonization of empty patches is usually considered to occur randomly via
a propagule pool, i.e. the spatial locations of the patches are ignored.
A6. All patches are considered to be equal.
Assumptions A3 to A6 are not crucial for applying a metapopulation model to
a system, but they make the model more tractable mathematically.
Given that a metapopulation model for two or more competing species is
applicable to a system, the theoretical models yield a number of predictions
which can be tested.
PI. For given colonization and extinction rates, there is a threshold number of
patches below which a species cannot persist (since p * T must be 3 1). Since
these rates may be influenced by interspecific competition, the number of species
is expected to increase with the number of patches in the region if competition is
important (e.g. Hanski & Ranta, 1983). However, this is a poor test of
interspecific competition, since it may also be caused by the species having
222
J. BENGTSSON
different numbers of suitable patches, or different colonization abilities and
extinction propensities leading to different pre-competitive thresholds.
P2. As the number of competing species increases, each species should occupy a
decreasing proportion of the patches (e.g. Slatkin, 1974; Hanski, 1983; Hanski &
Ranta, 1983).
P3. Species with similar or identical colonization and extinction rates may
coexist regionally, even though prolonged coexistence in the same patch is
unlikely (e.g. Slatkin, 1974; Hanski, 1983, 1987; Hanski & Ranta, 1983).
P4. Regional priority effects (in this case when an initially more widespread
species can prevent invasion by another species) are possible for certain
parameter values (Hanski, 1983; Hanski & Ranta, 1983; contrary to Slatkin,
1974).
P5. Hanski (1983) showed that increased movements may homogenize the
system, make local and regional timescales similar, and lead to exclusion of one
of the species. If, however, the local timescale is slower than the regional one,
higher migration rates slows down the rate of competitive exclusion and leads to
coexistence.
P6. A species which would be competitively excluded in a homogeneous
environment may coexist with a superior competitor in a patchy environment,
especially if it has a better dispersal ability (e.g. Levin, 1974; Armstrong, 1976;
Hanski & Ranta, 1983; cf. Hutchinson, 1951; Skellam, 1951). Thus, coexistence
of competitors in metapopulation systems can be a result of either a trade-off
between dispersal and competitive ability, or similar or identical niches
(prediction P3).
These predictions are all derived from deterministic models. If stochasticity is
introduced, species are less likely to persist in systems with few than many
patches (cf. P l ) , and may in the long term ‘drift’ (sensu e.g. Hubbell & Foster,
1986) to regional extinction (cf. P3) (see e.g. Nisbet & Gurney, 1982; Hanski,
1987; immigration-extinction stochasticity in Hanski, 1991) .
A CASE STUDY: DAPHNIA IN ROCKPOOLS
There are only a few studies in which the effects of interspecific competition on
metapopulation dynamics and species distributions have been evaluated. As far
as I know, the best studied system is the three waterflea (Daphnia) species in
rockpools in Fennoscandia.
Rockpools are small, waterfilled depressions in the bedrock containing fresh or
brackish water. The habitat is common in coastal areas all around Fennoscandia
(e.g. Ranta, 1979, 1982; Bengtsson, 1988), in parts of the Soviet Union
(Ghilarov, 1967) and in Canada (e.g. Good, 1981; Weider & Hebert, 1987). The
most abundant crustacean zooplankton in rockpools are the three species
Duphnia magna (Straus), D . pufex (de Geer) and D . longispina (0.F. Muller)
(henceforth abbreviated M, P and L, respectively), which coexist regionally
along the coasts of Finland and Sweden (e.g. Ranta, 1979; Pajunen, 1986;
Bengtsson, 1988). The niches of the species overlap widely along several niche
dimensions, including the food axis (Ranta, 1979; Bengtsson, 1988). Ghilarov
(1967) and Ranta (1979) used this finding to suggest that interspecific
competition influenced the distribution of Duphnia in rockpools. Dispersal
between rockpools takes place by means of drought-resistant resting eggs
INTERSPECIFIC COMPETITION
223
(ephippia) which, it has been suggested, are carried by aquatic insects, birds,
overflowing water and wind (e.g. Proctor & Malone, 1965; Hanski & Ranta,
1983; Pajunen, 1986). Unfortunately, data on dispersal and dispersal abilities of
Duphniu are largely lacking. As rockpools usually freeze solid every winter and
often dry up during summer droughts, the main function of the resting eggs is to
allow survival during such unfavourable periods.
Following a study of the distribution and habitat niches of the species in the
Tvarminne archipelago in south-western Finland (Ranta, 1979), Hanski &
Ranta (1983) suggested that the distributions of Duphnia in rockpools could be
explained in terms of a metapopulation model for three competing species. This
proposition has been subsequently examined by Bengtsson (1986, 1987a, b,
1988, 1989) using laboratory studies, field experiments, and studies of
distributional dynamics during 5 years in three areas in Sweden, and
independently by Pajunen (1986) in a 3-year field study in the Tvarminne area
(Fig. 1).
The assumptions
Hanski & Ranta (1983) suggested that extinctions and colonizations of empty
rockpools were frequent events (Al). The subsequent studies have
unambiguously shown that this is the case. In Tvarminne (Pajunen, 1986) as
well as on the Swedish coast (Bengtsson, 1989), 10-20% of the populations
became extinct each year, and colonizations of empty pools occurred at a similar
rate. Although resting eggs of freshwater crustaceans can survive more than 1
year in the bottom sediment (e.g. Moritz, 1987; De Stasio, 1989), there is
evidence that most of the population turnover observed in rockpools consists of
real extinctions and colonizations, not of dormancy. For example, in artificial
rockpools with gravel and detritus as bottom sediment, no populations scored as
extinct after 4 years reappeared in later years (J.Bengtsson, unpublished data).
The distribution of colonization distances (Pajunen, 1986, see below) is
consistent with real extinctions, but not with the view that populations survive in
the dormant stage in the sediment. Figure 1 shows the distributional dynamics of
rockpool Duphniu on two islands in the Angskar archipelago during 1982 to 1986.
Assumption A2, whether interspecific competition affects colonization and
extinction rates, will be dealt with in the following section. Regarding
assumptions A3 and A4, it can quite convincingly be argued that local dynamics
in single rockpools occur at a faster time scale than regional dynamics (Hanski &
Ranta, 1983). Duphniu have several generations each year, and the rate of
population growth ( r ) in late spring and summer can be as high as 0.3 day-'
(Bengtsson, 1986). The colonization and extinction rates in rockpools are about
0.1 to 0.2 events pool-' year-' (above). Although extinction probabilities may
depend on population sizes (Bengtsson, 1988, 1989) and dispersal (rescue effect,
Brown & Kodric-Brown, 1977), A3 and A4 may be regarded as acceptable for
rockpool Duphniu.
It is uncertain to what extent colonizations of empty rockpools can be assumed
to occur randomly via a propagule pool (A5). Pajunen (1986) showed that the
distribution of distances between invaded pools and closest possible source pools
was highly skewed towards short distances, casting doubt on this assumption. O n
224
J. BENGTSSON
Island N
I
be\
\
N
Island R
100 rn
Figure I . The distributional dynamics of three Daphnia species in rockpools on two adjacent islands
in the Angskar archipelago on the east coast of Sweden during 1982 to 1986; Angskar (island N ) and
Noorskaret (island R). The inserted map shows Fennoscandia with the four study areas indicated: I .
Flatholmen (F), 2. Monster ( M ) , 3. Angskar archipelago (A) (see Bengtsson 1988 for details). 4.
Tvarminne archipelago (Ranta 1979; Hanski 81 Ranta, 1983; Pajunen, 1986). 0 ,Empty rockpool;
0 , D. magna population; A,D.pulex population; @, D. longispina population; @@, rockpool with
two species (in this case D.magna and D . longispina);\, extinct population (e.g. \). ‘, colonizing
population (e.g. 0‘).
the other hand, long-distance dispersal of resting eggs up to a distance of a few
kilometres is clearly possible (e.g. Pajunen, 1986). Although the assumption is
not likely to be quantitatively correct, it can hopefully be used as a first
approximation in the absence of better data.
It is clear that the assumption that all patches are equal (A6) cannot be
expected to hold for any natural system. There are pronounced differences
between rockpools in factors such as salinity, probability of desiccation,
INTERSPECIFIC COMPETITION
225
productivity and predator fauna. Pajunen (1986) argued that regional
populations of Duphniu consist of populations in favourable rockpools with low
turnover, and of ephemeral populations in marginal rockpools with high
turnover. Bengtsson ( 1988) found some differences in the abiotic environmental
factors between pools with persisting populations and pools with population
turnover, but the differences were not great. The available data suggest that the
Duphniu metapopulations studied are somewhere between the mainland-island
and the Levins types (sensu Harrison, 1991). The exact positions along this
gradient have yet to be determined, and may differ between areas depending on
environmental conditions. I have chosen to ignore differences between pools in
the following, except when it is appropriate for interpreting the data.
Efects of interspecijc competition on colonization and extinction rates
Does interspecific competition influence colonization and extinction rates in
rockpool Duphniu, as conjectured by Hanski & Ranta (1983)? Neither Pajunen
(1986) nor Bengtsson (1988) found that colonization rates differed between
empty pools and pools occupied by another species. This suggests that
colonization rates are not affected by interspecific competition. However, the
possible effects of interspecific competition on colonization rates should be
evaluated experimentally before any firm conclusions are drawn.
The effect of interspecific competition on extinction rates was subjected to an
experimental test using artificial rockpools of different volumes and containing
established populations of each of the three two-species combinations, the threespecies combination, and a number of single-species controls (Bengtsson, 1989).
The vessels were filled with freshwater, inoculated with a natural phytoplankton
assemblage, covered with insect nets to exclude predators, and never allowed to
dry up (see Bengtsson, 1988 for details). In this 4-year experiment, extinction
rates per population and year were zero in single-species controls, usually higher
in two-species experiments, and always highest in the three-species experiments
(Table 1; Bengtsson, 1989). Detailed studies of population dynamics and
reproduction showed that the three species used the same food resources, and
that food levels as well as reproductive rates were severely depressed during
prolonged periods in each year (Bengtsson, 1988). Thus, the three species
competed with each other.
In natural rockpools, extinction rates were higher in two-species pools than in
single-species pools in all the four areas studied (Table 1; Bengtsson, 1989). O n
average, 1 1 % of the populations in single-species pools, and 18% of the
population in two-species pools became extinct each year. No three-species pools
were observed, either by Pajunen (1986) or by me (Bengtsson, 1988).
To conclude, extinction rates are clearly influenced by interspecific
competition in the rockpool Daphniu. Combining the results from natural and
experimental rockpools, it is possible to get a rough estimate of the increase in
extinction rate due to interspecific competitions in these species. T h e increase in
extinction probability per year due to one competing species is about 0.06
(Tables 1, 2). The experimental data suggest that the presence of two
competitors increases the extinction probability by about 0.15.
J. BENGTSSON
226
TABLE
1. Extinction
rates in artificial rockpools (4,12, 50 a n d 300
litres) and in natural rockpools in four areas in Fennoscandia.
n = Number of possible extinction events. After Bengtsson (1989)
Extinction rate
(probability of extinction population-'
year-') ( n )
Volume or study area
1 species
present
4 litres
12 litres
50 litres
300 litres
Flatholmen*
Monster*
Angskar.
Tvarminne'
0 (6)
0 (16)
0 (12)
~
0.13 (82)
0.12 (74)
0.097 (143)
0.11 (123)
2 species
present
3 species
0.21 (28)
0.029 (68)
0 (80)
0 (8)
0.15 (58)
0.42 (12)
0.17 (54)
0.16 (50)
0.28 (18)
0.20 (15)
0.10 (39)
0.030 (33)
present
-
*On Flatholmen, Monster and hgskar, an extinction was considered to
have occurred if a previously recorded species was absent in the samples
from the pool in two successive years. Rates for Tvarminne were calculated
from Pajunen (1986).
The number of extinctions differ significantly between two-species and
three-species experiments (one-tailed P < 0.005) and between natural
rockpools with one and two species (Fisher's combined probability test:
one-tailed P < 0.02); see Bengtsson (1989) for details.
Dispersal and Competitive abilities
Hanski & Ranta (1983), following many others (e.g. Hutchinson, 1951;
MacArthur & Wilson, 1967; Armstrong, 1976), suggested that the dispersal and
competitive abilities of the three Daphnia species might be inversely related to
each other. In particular, they suggested the following orders of the species: in
dispersal ability: M > P > L, and in competitive ability: L > P > M. However,
recent data on colonization rates are not consistent with this hypothesis. The
rates of colonization of empty pools did not differ in any consistent way between
the three species, in either Sweden (Bengtsson, 1988) or Tvarminne (Pajunen,
1986), and hence the dispersal abilities of the species can be regarded to be
approximately equal.
The competitive abilities of the species have been examined in detail by
Bengtsson (1986, 1987a, b, 1988). In laboratory experiments, the relative
competitive abilities of the species varied with environmental conditions. The
large D . mugna was the best competitor at higher food levels and at lower
temperatures, whereas the smaller species D. pulex and D . longispina were
superior competitors at low food densities and higher temperatures (Bengtsson,
1986, 1987a). Several other studies of competition between cladoceran species
have reached similar results (e.g. Romanovsky & Feniova, 1985; see Bengtsson,
1987a). Of the two smaller results D . pulex and D . longispinu, the former appears
to be superior in the laboratory (Bengtsson, 1986).
Of the total of 2 1 extinctions observed in the experiment in artificial rockpools,
the large D. magna became extinct fewer times than the other two species (M: 2,
P: 9, L: 10 extinctions; Bengtsson, 1988, 1989). In natural rockpools with two
227
INTERSPECIFIC COMPETITION
TABLE
2. Estimates of model parameters using empirical d a t a from rockpools in four areas of Fennoscandia (S), individual areas in Sweden (Flat, F;
Monster, M; Angholmenskar, A) and artificial rockpools (AR) (data from
Bengtsson 1988, 1989, a n d unpublished). m, and p,, = Colonization parameters (Levins, 1969), e,, ,&,, &,, and g, = extinction parameters, p , =
proportion of pools occupied,
total number of suitable pools in the
region (excluding islands in area A where the species did not occur).
M = D. magna, P = D . pulex, L = D . longispina
$=
Parameter
Estimate
0.19 (F, M, A)
z 0 (S, AR)
0.11 ( S ) *
0.064 ( S ) * , 0.06 (AR)
0.15 (AR)
0.03 (AR)
0.47 (113) (F)
(F)
0.41 (101) (F)
~
0.61 (111) (M)
0.43 (68) (M)
~
(M)
0.27 (179) (A)
0.49 (184) (A)
0.34 (62) (A)
*Extinction rates for individual areas are given in Table I.
Methods of calculation: Since p,, z 0 (see text), m,= o l , , . Ti(T,-JV,)JV,,where
Col,,, = the observed number of colonizations, (T,-JV,) = the number ofsuitable but
unoccupied pools, JV, = the observed number of populations and I, = the number of
pools suitable for species i.
e, = Probability of a local population of species i becoming extinct in single-species
pools; 8, = probability of a local population of species i becoming extinct in twospecies pools -e,. E,,~ = &y+&4+g,,kwhere gvt is the interactive effect of the two species
j and k on the extinction parameter of species i (cf. Caraco & Whittam, 1984).
The extinction parameters were calculated as the total number of observed
extinctions during the study period divided by the number of possible extinction
events (see Bengtsson, 1989), and m,was calculated in a similar way. ?-,,the number
of suitable pools in each area, was determined by performing a principal components
analysis of seven environmental variables in all rockpools (mean salinity, variation in
salinity, pH (Angskar only), maximum volume, maximum depth, macrophyte coverage and water colour), and then comparing the scores along the first three principal
component axes for pools with and without each species with ANOVAs. If significant
(P< 0.05) differences were found, pools outside the range of the species in question
were considered unsuitable. If no difference was found, pools outside the range of all
Duphniu species were considered unsuitable (see Bengtsson, 1988 for details).
species, no clear differences between the species in extinction rates have been
found (Pajunen, 1986; Bengtsson, 1988, 1989).
Thus none of the available experimental or observational data support the
hypothesis of Hanski & Ranta (1983) that D . longispinu is the best and D. magna
the weakest competitor. Fluctuations in the factors affecting the relative
competitive abilities of the three species, for example food levels, temperature,
salinity and predation intensity, are common in rockpools (e.g. Ganning, 1971;
Ranta, 1979, 1982). The average competitive abilities of the three species appear
to be similar, even though conditions in particular pools may favour one or the
other.
Estimating model parameters for rockpool Daphnia
The metapopulation models described above are quite abstract, and when
applying them to empirical data several things have to be considered. Different
J. BENGTSSON
228
0
No. pools
B
0 . 0
3-
.-t0
2-
n
0
z
I-
0
10
20
30
40
50
60
No. pools
Figure 2. The number of species in relation to the number of pools suitable for Daphnia: A, on islands
in the Angskar archipelago 0. Bengtsson, unpublished data) and B, .on islands in the Tvarminne
area (from Hanski & Ranta, 1983). Spearman rank correlations: Angskar: r, = 0.57, P = 0.05,
n = 13. Tvarminne: r, = 0.71, P = 0.01, n = 14.
versions of the basic model exist, and the choice of model may affect the
definition and calculation of the parameters (e.g. Hanski, 1987). The
terminology and definitions of parameters differ between models (compare e.g.
Levins, 1969; Levin, 1974; Slatkin, 1974; Armstrong, 1976; Hanski, 1983, 1991;
Hanski & Ranta, 1983). The choice of time interval between measurements of
patch occupancy is important. Moreover, estimation of the model parameters
may be difficult. The easiest parameters to estimate are the number of occupied
patches, N,, and the extinction parameters, e, and E~ (the subscripts for species 1
and 2 in equation (2) have been changed to the general i, j,.. .used in
multispecies models), provided that the system of habitat patches can be
delimited regionally and that real extinctions have taken place (for problems of
distinguishing between true extinctions and sampling errors or dormancy, see
e.g. Lynch & Johnson, 1974; Simberloff, 1976a; Nilsson & Nilsson, 1983;
Pajunen, 1986; Bengtsson, 1988). The colonization parameters, mi and pi, and
q,the total number of suitable patches in the region, are more difficult to
estimate. In practice, the easiest (but not only) way to measure mi is to monitor
INTERSPECIFIC COMPETITION
229
the rate of colonization to suitable but empty patches. T o do this, a criterion to
distinguish between empty suitable patches and empty but unsuitable patches is
needed; such information is rarely known to the accuracy required.
In spite of these problems, estimates of the model parameters for rockpool
Daphnia are instructive. Measuring patch occupancy in 1-year intervals seems
reasonable for rockpool Daphnia. All Daphnia populations are refounded from
resting eggs each spring and, given the estimates of extinction and colonization
rates (Table 1; Bengtsson, 1988), this interval appears to capture most important
events happening on the regional time scale. Having chosen 1 year as the time
unit, the extinction parameters e, and E, were calculated as the probability of a
local population going extinct in single-species pools, and the increase in
extinction probability in two-species pools, respectively (cf. Levins, 1969;
Slatkin, 1974; Armstrong, 1976). Using the basic two-species model in equation
(2), and the fact that colonization rates did not differ between empty pools and
pools occupied by another species, the colonization parameter m, could be
calculated as the probability that a pool unoccupied by a species was colonized
divided by the proportion of pools occupied. Calculated in this way, the
colonization parameter measures the number of other patches receiving colonists
from one particular patch in a given time unit (cf. Armstrong, 1976). It may be
noted that this colonization parameter, which is derived from Levins (1969),
does not depend on the number of patches in the region, in contrast to the one in
equation (1) in Hanski (1987: 157). It is therefore the most appropriate when
comparing between species or regions.
The estimates of the parameters in the basic multispecies model and the
methods of calculation are given in Table 2. The estimates of e, and e are quite
1
accurate (Bengtsson, 1989), while errors in eYk,grlk,m,, p,, and
are likely to be
larger, but of unknown magnitude (Bengtsson, 1988). Since no clear differences
between the species in extinction and colonization rates have been found
(Bengtsson, 1988, 1989; Pajunen, 1986), the species have been regarded as
similar in these respects. Therefore, the values in Table 2 are for all three species.
Testing the predictions
If interspecific competition is important in determining the distributions of
species, it has often been assumed to result in negative associations between the
competing species (e.g. Diamond, 1975; Giller, 1984; but see Strong et al., 1984;
Caraco & Whittam, 1984; Hastings, 1987). Having excluded pools that were not
suitable for both species, a negative association was only found for the species
pair D . pulex and D . longispina on the Angskar islands (G-test: G = 7.74, P <
0.01, n = 62; Bengtsson, 1988). Of the other species pairs, D . magna and
D. longispina co-occurred more often than expected by chance, whereas D . magna
and D-.pulex did not show any positive or negative associations at all (Bengtsson,
1988).
In’the Angskar archipelago, where 13 islands have been studied, the number
of species on an island increased with the number of pools (Fig. 2). A similar
pattern was found in the Tvarminne area (Fig. 2; Hanski & Ranta, 1983). This
result is consistent with the hypothesis that interspecific competition influences
the metapopulation dynamics of the species ( P l ) , but it could also be due to
J. BENGTSSON
230
TABLE
3. The number of suitable pools and .!he proportion of occupied pools on
islands with different numbers ofspecies in the Angskar area. Means ( +SD) are given,
n is the number of islands. M = D. magna, P = D . pulex, L = D. longispina
No. suitable pools*
No.
species ( n )
1 (2)
2 (8)
3 (3)
Proportion of pools occupied
M&P
L
M
P
L
7.5 (0.71)
19.9 (11.4)
30.0 (14.7)
6.5 (0.71)
13.0 (8.0)
24.0 (13.0)
0 (-)
0.40 (0.31)
0.13 (0.017)
0.46 (0.24)
0.36 (0.23)
0.25 (0.10)
0 (-)
0 (--)
0.25 (0.082)
*The number of suitable pools on different islands was calculated as in Table 2, except for
three islands sampled in 1984 only, where the observed values of the environmental variables in
each pool were compared with the values in the main material. Pools with values outside the
species’ range were considered unsuitable.
other factors, for example interspecific differences in the number of suitable pools
(cf. above).
The two single-species islands in the Angskar area had only D . pulex, while the
two-species islands were invariably inhabited by D . pulex and D. mugnu. This
situation differs from Tvarminne, where D. mugnu was the only species on singlespecies islands. I n both Angskar and Tvarminne, D . longispinu was found only on
three-species islands. Hanski & Ranta (1983) suggested that the restricted
distribution of D. longispinu was due to its poor dispersal ability, but since no
clear differences have been found in the colonization rates between the species
(above), another explanation for the absence of D . longispinu on many of the
smaller islands can be proposed. As is evident from Table 3, the number of
suitable pools seems to be smaller for this species than for the other two species,
apparently this species has a narrower habitat niche than the others (cf. Ranta,
1979), which together with the effect of interspecific competition on extinction
rates may account for the many absences of D . longispinu on islands with less than
20 pools, on which usually less than 15 were suitable for this species.
If interspecific competition affects the distribution of the species, the
proportion of pools occupied by each species should decrease with increasing
number of species on an island (P2).This is the case in D. pulex and D . mugnu on
the Angskar islands (Table 3), although the differences are not significant at the
0.05 probability level (Mann-Whitney U-tests). Hanski & Ranta (1983)
obtained the same result on islands in the Tvarminne archipelago. Another effect
of interspecific competition could be a negative relationship between the
proportion of pools inhabited by one species and the proportion of pools
inhabited by other species on an island. In the Angskar area, all three Spearman
rank correlations between these variables had negative signs, but none of them
was significant.
In the single-species Levins model, the equilibrium proportion of occupied
pools is d = 1 -e/m. Using the values of e and m given in Table 2, 6 = 0.42. The
mean proportion of occupied pools on the single-species islands was 0.46
(Table 3). Thus, the agreement between the prediction from the model and
observations is very good. The equilibrium proportions of occupied pools in twoand three-species models have not been given in closed form in the theoretical
papers (e.g. Slatkin, 1974; Hanski, 1983; Hanski & Ranta, 1983), and therefore
I have not attempted an analysis of these cases. However, it may be noted that
INTERSPECIFIC COMPETITION
23 I
the parameter estimates in Table 2 are consistent with the observation that two
species coexist regionally (equations 5, 6 and 8 in Hanski, 1983 are untrue).
A final reservation is appropriate. This discussion has almost exclusively been
concerned with interspecific competition. There exists ample evidence that
several other factors influence the distribution of Daphnia in rockpools.
Environmental factors such as salinity and desiccation are clearly important (e.g.
Lagerspetz, 1955; Bengtsson, 1988). For example, turnover of D.longispinu
populations appeared to be affected by high and variable salinities (Bengtsson,
1988). The different kinds of predators that occur in rockpools can also influence
species composition, for example, newts, fish (Ranta & Nuutinen, 1984, 1985;
Ranta et al., 1987) and backswimmers (J. Bengtsson, unpublished data; cf.
Murdoch, Scott & Ebsworth, 1984). Patterns in species composition and
distributions are seldom, if ever, due to single factors (e.g. Hilborn & Stearns,
1982; Wilbur, 1987).
Conclusions
Taken together, the results presented here support the view that rockpool
Duphnia fit the assumptions as well as the qualitative predictions of the
metapopulation models to a fairly good approximation. At least extinction rates
have been shown to be influenced by interspecific competition in these species.
However, it is not clear whether regional coexistence of the species is crucially
dependent on colonization-extinction dynamics. There are other possible
explanations involving more or less subtle niche differences, for example, refuge
pools of various sorts and different centres of distribution (cf. Harrison, 1991) .
Although the niches of these species overlap greatly (Ranta, 1979; Bengtsson,
1988), there are differences in the sensitivities of the species to different kinds of
predators and abiotic factors such as salinity and drying up of the pool (see
above; Bengtsson, 1988). It is thus possible that different species have permanent
populations in different pools, and that the observed population turnover mainly
occurs in the remaining pools (cf. Pajunen, 1986; Harrison, 1991). This
hypothesis can be examined with long-term data on distributional dynamics and
environmental conditions. Critical experimental tests of the idea that
metapopulation dynamics allows coexistence would be to alter the number of
pools on an island and see whether the number of species changes accordingly; to
introduce species to pools and islands where they do not occur; and to manually
change the colonization and extinction rates of the species. Such long-term
experiments have yet to be performed.
STUDIES OF INTERSPECIFIC COMPETITION IN METAPOPULATIONS
The number of studies on the effects of interspecific competition on
metapopulation dynamics is surprisingly small. This may be partly due to the
general scarcity of long-term metapopulation studies, but in many cases this
particular question has not been thoroughly examined, even though relevant
data might exist, for example on mangrove insects (Simberloff, 1976a, b, and
other papers), insects on Spartina islands (Rey, 1981) , orb-weaving spiders on
small Bahamian islands (Toft & Schoener, 1983; Schoener & Spiller, 1987), and
Spence’s (1983) study of pond and lake water-striders. There are many good
232
J. BENGTSSON
studies of interspecific competition, but only in a few cases is it possible to judge
whether colonization-extinction dynamics are important in the studied system.
The studies discussed in the following have been selected according to two
criteria: ( 1 ) A metapopulation structure of one of the kinds discussed by
Harrison ( 1991 ) had to be shown or could be inferred to be highly likely, and (2)
the effects of interspecific competition on colonization or extinction rates had to
be discussed explicitly. Studies of species in patches suitable for one generation
only (e.g. Drosophila on fungi or rotting fruit, Shorrocks el al., 1979, 1984; or
carrion flies, Hanski, 1987) have not been included.
Efects of competition on colonization rate
Cole’s (1983) study of ants on small mangrove islands in Florida showed a
clear effect of the presence of one species on the colonization rate of another
species. In fact, no experimental introductions to islands with the two so-called
primary species were successful. Cole did not give any data concerning
metapopulation dynamics, but the data in Simberloff (1976a, b) show that
colonizations and extinctions do occur in this system. There are other studies
suggesting that ant species may often decrease the colonization probability of
later-arriving species (e.g. Levins, Pressick & Heatwole, 1973; Vepsalainen &
Pisarski, 1982). The mechanisms involved appear to be aggressive behavioural
interactions and avoidance. Thus competitive effects on ants’ metapopulation
dynamics can be great. Ants may also potentially influence the metapopulation
dynamics of other ground-living organisms in patchy habitats through
competition and/or predation.
Platt & Weis (1985) studied competition among five perennial, fugitive plant
species on badger disturbances in tall-grass prairie. They found that pre-emptive
competition prevented later arriving species from colonizing (in this case,
producing reproductive individuals), but only if colonizations were separated by
more than one growing season. The effects of competition on extinction rates
were not clear in this case. The authors suggested that coexistence in this guild of
fugitive species is maintained by an inverse relationship between colonization
and exploitative ability (cf. e.g. Levin, 1974; Hanski & Ranta, 1983).
Preemptive competition may often play a key role in the metapopulation
dynamics of plant species. In many studies of plant competition, the species
arriving first to an empty patch can exclude others from colonizing (e.g.
Schoener, 1983; Grubb, 1986).
The study by Paine (1988) of an intertidal brown alga, the sea palm,
suggested that species of small algae decreased the probability of colonization by
the former species. The mechanism was that immature sea palm individuals were
more likely to be swept away on algal substrate than on bare rocks. In addition,
the extinction rate of the sea palm was suggested to increase due to overgrowth
by the small algae. Regional persistence of the sea palm is dependent on mussels,
which outcompete small algae for space, and are later swept away, creating bare
rock patches which the species can colonize. It is likely that the spatial dynamics
of the sea palm can be modelled by a metapopulation model of the type
discussed in this paper.
Many of the instances of interspecific competition or competitive exclusion
reported in the literature (see e.g. Schoener, 1983; Connor & Bowers, 1987) may
INTERSPECIFIC COMPETITION
233
be examples of decreasing colonization rate due to competition, but in most cases
possible metapopulation structure and dynamics have not been investigated. For
example, in studies of South Pacific birds, Diamond (e.g. 1975) suggested that
distributional patterns as well as anecdotal observations of dispersal and
unsuccessful invasions were evidence of interspecific competition preventing
establishment, but the metapopulation dynamics of the presumed competitors
have not been analysed.
Efects of competition on extinction rate
Apart from the rockpool Daphnia discussed above (Bengtsson, 1989), and
Paine’s (1988) sea palm study, few examples of increased local extinction rates in
metapopulations due to interspecific competition exist, although some of the
studies reviewed in, for example, Schoener (1983) and Connor & Bowers (1987)
may include such an effect.
Hoeck (1989) studied the distributional dynamics of two rock hyrax species
inhabiting rock outcrops in the Serengeti for 17 years. He found one probable
case of interspecific competition causing extinction. However, the overall
influence of competition in this system was unclear, partly because of the low
number of patches studied, but also because other factors such as interspecific
association and diseases were presumably operating in this system.
Jfo eJects of interspecijc competition
Some authors have looked for effects of interspecific competition on
metapopulation dynamics but have not found any. Simberloff (1976b) argued
that most of the turnover in mangrove insects could be attributed to
characteristics of individual species rather than species interactions, but did not
test for the influences of competition explicitly, and his results are contradicted
by those of Cole (1983).
Interspecific competition has been shown to operate among small mammals
(e.g. Shoener’s 1983 review). However, studies on the metapopulation dynamics
of small mammals have not been able to demonstrate any competitive effects on
colonization or extinction rates. Crowell (1973) and Crowell & Pimm (1976)
found no clear effects of competition on colonization probability or extinctions of
mice on islands off Maine, but sample size was very small in these studies.
Ebenhard (1987) introduced bank voles to islands off the Swedish east coast, and
found no effects of interspecific competition from field voles on colonization
probability. However, the experiment was not designed as a test of the influence
of interspecific Competition. Peltonen & Hanski (1991) studied three species of
shrew on 17 islands in a lake in Finland during 5 years, and found no evidence
for competition affecting colonization or extinction rates. Thus, the available
evidence suggest that although small mammal species may compete, the effects
of interspecific competition on their metapopulation dynamics are small.
Sillkn-Tullberg & Solbreck (1990) studied the local and metapopulation
dynamics of the seed feeding bug Lygaeus equestris on patches of its host plant
Vincetoxicum hirundinaria for 1 1 years, and could not detect any competitive effects
of a seed-eating fly on the bug’s dynamics.
There are some studies of regional dynamics of potential competitors where
234
J. BENGTSSON
the metapopulation structure and dynamics of the species are difficult to
determine, but which, nonetheless, are of interest in the present context. One
such example is the decline of the red squirrel and spread of the grey squirrel in
England, which was examined by Reynolds (1985). He concluded that local
extinctions of the red squirrel most probably were caused by a disease and not by
competition from the grey squirrel, as had been suggested earlier. However, this
conclusion was recently disputed by Lawton & Godfray (1990).
In the marine intertidal, pre-emptive competition for space has been shown in
many studies (e.g. Sousa, 1979; Schoener, 1983; Roughgarden, Gaines &
Possingham, 1988; and several others). It is clear that interspecific competition is
one of the factors affecting the probabilities of colonization and extinction of
patchily distributed organisms in this system (e.g. Sousa, 1979; Dethier, 1984;
Paine, 1988). However, many intertidal organisms have planktonic larvae that
may stay in the open water for days or months. Therefore, the importance of
local interactions in the adult stage may be of little importance for the large scale
dynamics of these organisms, and it is difficult to assess the effects of interspecific
competition between adults on the metapopulation dynamics of such species.
The dynamics of this kind of metapopulations have recently been discussed by
Roughgarden et al. (1988).
Is metapopulation structure essential for coexistence?
Multispecies metapopulation models have been constructed to investigate the
conditions under which spatial heterogeneity allows the coexistence of
competitors that would not coexist in a homogeneous environment (Levin, 1974;
Slatkin, 1974; Armstrong, 1976; Hanski, 1983). However, the empirical studies
on the effects of interspecific competition in metapopulations are not directly
relevant to this question. Even if interspecific competition influences colonization
and extinction rates in such systems, the explanation for regional coexistence
may still be niche differences. Many metapopulations may be of the ‘mainlandisland’ type (sensu Harrison, 1991), with different species having different
‘mainland patches’. As far as I know, critical experimental tests have not been
conducted in any field system to demonstrate that metapopulation structure per
se allows species to coexist. The kind of experiments outlined for rockpool
Daphnia above may be feasible in other metapopulation systems, and are needed
to properly examine this central theoretical question.
There are only a few studies examining the effects of interspecific competition
in metapopulations. While future studies are needed, I also urge those in
possession of data that can be used to examine these questions to explicitly look
for effects of interspecific interactions on metapopulation dynamics.
ACKNOWLEDGEMENTS
I thank Torbjorn Ebenhard, Mike Gilpin, Ilkka Hanski, Susan Harrison,
Tony Ives and Per Sjogren for clarifying discussions and for constructive
comments on the manuscript. The remaining errors are my own. My work on
rockpool Daphnia was stimulated by the model of Hanski & Ranta (1983) and
has been financed by grants from the Swedish Natural Science Research Council
to S. G. Nilsson, G. Milbrink, S. Ulfstrand and myself, and from Sven and Lilly
235
INTERSPECIFIC COMPETITION
Lawski's Foundation. The field work was carried out while I was at the
Department of Zoology, Uppsala University.
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