Download Explaining density-dependent regulation in earthworm populations

OIKOS 100: 89–95, 2003
Explaining density-dependent regulation in earthworm populations
using life-history analysis
Jan E. Kammenga, David J. Spurgeon, Claus Svendsen and Jason M. Weeks
Kammenga, J. E., Spurgeon, D. J., Svendsen, C. and Weeks, J. M. 2003. Explaining
density-dependent regulation in earthworm populations using life-history analysis. –
Oikos 100: 89 – 95.
At present there is little knowledge about how density regulates population growth
rate and to what extent this is determined by life-history patterns. We compared
density dependent population consequences in the Nicholsonian sense based on
experimental observations and life-history modeling for the earthworms Lumbricus
terrestris and Eisenia fetida. Both species differ in their life-histories, L. terrestris
being a relatively long-lived species with slow reproduction and occurring at low
densities compared to E. fetida which has a more opportunistic strategy with a high
reproductive output. E. fetida is able to colonise new habitats rapidly and may occur
at relatively high population densities. Density dependency of population growth rate
was estimated by incorporating density dependent effects on reproduction and
growth using a modified Euler equation. The results point out that E. fetida was not
as strongly impacted by density as compared to L. terrestris. Population growth rate
in E. fetida was hardly affected at low and moderate density, being reduced only at
high level, this compares to L. terrestris where even relatively small density effects
resulted in a strong negative effect on population growth rate. Our findings indicate
that density-dependent regulation in earthworms can be quantified using life-history
analysis. The outcomes are in agreement with empirical field observations for
populations (i.e. L. terrestris occurs ar low density, E. fetida at high density).
Consideration of the potential importance of Nicholsonian density dependence for
field populations of these two species in light of their known biology however
produces counterintuitive conclusions. In E. fetida, although density tolerant, rapid
population growth may mean this species may be subject to density dependent
regulation. In L. terrestris, although density sensitive, complex behavioural ecology
(surface activity, territoriality) may limit of feedback influence on population size.
J. E. Kammenga, Lab. of Nematology, Wageningen Uni6., PO Box 8123, Binnenha6en
5, NL-6709 PD Wageningen, The Netherlands ([email protected]). – D. J.
Spurgeon and C. S6endsen, Inst. of Terrestrial Ecology, Monks Wood, Abbotts Ripton,
Huntingdon, Cambridgeshire, PE17 2LS, UK. – J. M. Weeks, WRc-NSF, Henley
Road, Medmenham, Marlow, Buckinghamshire, SL2 2HD, UK.
It is well known that density-dependence acts on most
plant and animal populations but obtaining insight into
how natural populations are regulated still poses a
great challenge for ecologists (Hellriegel 2000). In the
classical Nicholsonian interpretation density dependence implies a change in demographic rates based on a
biological feed back. Through changes to birth, growth
or survival rates, the controlling factor influences population growth rate r which depends on population size
N. This interpretation as well as various other forms of
density dependence are still the centre of a hot debate
(Sale and Tolimieri 2000). Yet, as pointed out by
Tanner (1999), this debate has grossly surpassed the
potential for experimental manipulations and modeling
approaches for obtaining insight into the mechanisms
underlying observed phenomena.
Most analyses of density dependence have focused on
insects (Hassell et al. 1989, Hopper et al. 1996) follow-
Accepted 12 June 2002
Copyright © OIKOS 2003
ISSN 0030-1299
OIKOS 100:1 (2003)
89
ing early work by Nicholson (1933) and Andrewatha
and Birch (1954), but many other species have also
been investigated (Condit et al. 1994, Ferrer and Donazar 1996, Wilkens and Exo 1998). However within
these, surprisingly, few studies have been carried out on
density dependency in soil organisms. This is despite
the fact that they play an important role in food web
dynamics and contribute to nutrient cycling and decomposition processes (DeRuiter et al. 1995). Amongst
the few studies that have been conducted, Bengtsson et
al. (1994) reported on the density-dependent dispersal
of springtails and Klironomos and Ursic (1998) concluded that microarthropod population densities were
influenced by the fungi species upon which they fed.
In soils, earthworms play a crucial role in nutrient
cycling, maintenance of structure and decomposition
processes and there is increased evidence that populations are regulated by density dependent mechanisms.
This assumption is based on results from a number of
both field and laboratory-based studies. Baveco and
DeRoos (1996) identified a number of plausible density
dependent mechanisms operating within earthworm
populations, including predation, food-limitation and
crowding effects. More detailed information was given
by Neuhauser et al. (1980) on the relationship between
growth and density in Eisenia fetida Linné
(Oligochaeta: Annelida) and Hartenstein and Amico
(1983) for Lumbricus terrestris Linneaus (Oligochaeta:
Annelida). However despite these few studies, there is
limited knowledge about how density regulates population growth rate and to what extent this is determined
by the life-history of the earthworm species. In this
paper we focus on this aspect by comparing density
dependent population consequences in the Nicholsonian sense for the two earthworm species based on
experimental observations and life-history modeling.
These two species, E. fetida and L. terrestris differ
widely in their life-histories. E. fetida is a rapidly developing species with high rates of reproduction that inhabits organic matter rich locations such as animal
manure or compost heaps often at high population
densities. L. terrestris has a relatively slow reproduction. It lives at lower densities in deep vertical burrows
within the soil.
In conducting this study of density dependence, an
important aspect to consider is the taxonomic background in which the study was set. Earthworm taxonomy is far from being well developed and because
earthworms have few morphological characteristics,
confusion exists concerning the taxonomic purity of
some species (Bouché 1992). For our study we focused
on L. terrestris and worms belonging to the ‘E. fetida’
complex. Within the latter, two closely related sub-species have been identified (Bouché et al. 1988). These
are: E. fetida fetida, which is characterised by the
presence of pigmentless bands extending from the furrows between segments and E. fetida andrei, which is
90
totally pigmented (Sims and Gerard 1985). Comparative studies of the two Eisenia species have indicated
that although life-cycle, habits and temperature preferences are broadly similar, some subtle behavioural differences do occur (Haimi 1990, Elvira et al. 1996).
However for the purposes of this paper, we have considered studies from both species as this increases the
volume of data available from which to model the
density responses of the complex. In the remainder of
the paper we refer to the complex merely as E. fetida.
Life-history model and data collection
The density dependent effect on population growth rate
of L. terrestris and E. fetida was estimated by incorporating density dependency on reproduction and growth.
The model was based on the classic Euler-Lotka equation where the intrinsic rate of population increase r
was defined as the root of:
t = tm
1= % e − r · tLt · nt
(1)
t=0
where t is age, tm is time to death, Lt is survivorship
during time t and nt is the number of offspring per time
unit at age t. To determine the consequence of densitydependent life-cycle changes on particular traits, the life
cycle for both species was divided into three discrete
stages (cf. Kammenga et al. 1997). A juvenile stage (tj )
which includes the egg stage, an adult reproductive
stage (ta ) during which offspring are produced at a
given rate (nt ) and a senescent stage which continues
until death. Based on a three-stage life cycle eq. (1) can
be rewritten as:
t = tj
t = tj + t a − 1
t=0
t = tj + 1
1= % e − rt · Lt · nt +
%
e − rt · Lt · nt
t = tm
+
%
e − rt · Lt · nt
(2)
t = tj + t a
Because nt = 0 for 0 B t Btj and for t \ (tj + ta ) only
the second term of the equation is important. Therefore
it follows that:
t = tj + t a − 1
1=
%
e − r · t · Lt · nt
(3)
t = tj + 1
For earthworms, as for many species, adult mortality
is time dependent and the survival curve can be described by a Weibull distribution function Lt =
c
p · e − q · (t) where p, q and c are constants. In addition it
is assumed that: L(tj ) =sj and L(tj + ta ) =sj · sa hence:
Lt = sj · e − q · (t − tj )
c
(4)
OIKOS 100:1 (2003)
and
c
c
sj · sa =sj · e − q · (tj + ta − tj ) “sa =e − q · (ta ) “ln sa
= −q · (ta )c “q= −(ln sa )/(ta )c
(5)
Substituting eq. (5) into eq. (4) gives Lt = sj ·
c
c
e − (ln sa /ta) · (t − tj ) , which can be rewritten as: Lt = sj ·
[(t − tj )/ta ]c
sa
. Now the modified Lotka equation (eq. (2))
becomes:
tj + ta − 1
1=
%
c
− tj )/ta ]
e − r · t · nt · sj · s [((t
a
(6)
t = tj + 1
Using eq. (6), r can be estimated by means of iteration when parameters sj, tj, ta, nt, sa and c are estimated
from earthworm life-cycle studies. For describing relationships between life-cycle traits, density and time
algorithms were constructed using PROC NLIN in SAS
(Anonymous 1990). For the calculation of nt, it was
necessary to consider a number of reproductive
parameters. In earthworms, production of juveniles occurs via cocoons formed at the clitellum and shed from
the front end of the worm (Edwards and Bohlen 1996).
In some earthworm species, more than one (up to 20)
juvenile may emerge from each cocoon (Evans and
Guild 1948), furthermore, some cocoons may contain
no or unviable ova. Thus when estimating age specific
reproduction the average number of juveniles per fertile
cocoon was used which was calculated from the cocoon
production rate, cocoon viability and the mean number
of juvenile emerging per cocoon.
To compare density effects for each species, parameter estimates for life-cycle traits of L. terrestris were
collected from field data or data obtained from laboratory populations which were kept at realistic field temperatures and moisture levels. For E. fetida, laboratory
and bioassay data were used for 20°C which is an
optimal temperature for this species (Reinecke and
Kriel 1981, Reinecke et al. 1992, Van Gestel et al.
1992).
L. terrestris data
Butt et al. (1994b) showed that age specific reproduction nt in L. terrestris was 0.05 juveniles per worm per
day. The only study in which tj was measured was
conducted by Lofs-Holmin (1983), who reported a
value of 90 days. For juvenile survival sj a value of 0.9
was given by Lakhani and Satchell (1970). For this
paper ta =1095 days was taken from the study by Butt
et al. (1994b).
According to Butt (1993), a relatively high survival of
80% over the adult period sa was found. In order to
estimate the shape of the adult survival curve c,
longevity data from Butt and Nuutinen (1998), who
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monitored survival of adult L. terrestris, were used to
estimate survival curves using the SAS algorithm
PROC LIFETEST. Subsequent survival values were
used in a least-square method with the non-linear regression procedure SAS algorithm PROC NLIN
(Anonymous 1990) to estimate c in the Weibull distribution curve according to:
Lt = e ( − ln 2 · (t/LT50))
c
E. fetida data
Venter and Reinecke (1988) showed that age specific
reproduction in E. fetida was time invariant and nt =
0.34 and the average length of the juvenile period, tj,
was 50 days. Only slight mortality was observed in the
juvenile stage (Watanabe and Tsukamoto 1976); thus a
value for juvenile survival of 95% was taken as appropriate. The length of the reproductive period was 800
days (Venter and Reinecke 1988). Tsukamoto and
Watanabe (1977) found a survivorship of 90% for
adults after 200 days. To our knowledge, no long-term
survival studies have been published for E. fetida.
Therefore we decided to use the estimation of the slope
of the Weibull survival curve c from the only data
available for worms by Butt and Nuutinen (1998) in L.
terrestris. Using this data was considered valid because
a sensitivity analysis of eq. (6) indicated that r was not
greatly influenced by changes in c.
Because no data existed on the direct relationship
between density and reproduction we decided to combine the results of two different data sets. The first set
was taken from Domı́nguez and Edwards (1997) who
investigated the influence of worm density on body size
and growth rate. Mean individual biomass was clearly
density dependent and the data could be fitted with a
logistic growth equation to obtain growth rates (Fig.
2A). The second data set was taken from a study by
Van Gestel et al. (1992) on the relationship between
body growth rate and reproduction (Fig. 2B). They
found a significant correlation between growth rate (g)
and cocoon production n and a linear curve could be
fitted according to n = −0.069× g+1.337 with correlation coefficient R2 = 0.46. The growth rate data of
Domı́nguez and Edwards (1997) were substituted in this
equation and the age-specific reproduction was calculated at each density.
Results
Analysis of the Nicholsonian effects of density on reproduction of L. terrestris was made by considering the
results of Butt et al. (1994a). This study which measured reproduction at a range of worm densities indi91
The results for E. fetida are displayed in Fig. 2C
showing that reproduction was density-dependent when
density was higher than approx. 7.5 worms per l manure. When Figs. 1 and 2C are compared it is shown
that population growth rate in E. fetida is not as
strongly impacted by the investigated densities as compared to L. terrestris. The significance of these effects
for the regulation of natural populations is discussed
below.
Fig. 1. Relationship between density, age specific reproduction, and population growth rate for L. terrestris. The level of
maximum field density is also shown (see text for explanation).
cated that reproduction was density-dependent (Fig. 1).
Using these reproduction values, the impact on population growth rate was calculated by eq. (6) which is also
shown in Fig. 1.
Discussion
In this paper we suggest that populations of L. terrestris and E. fetida can be regulated by classical Nicholsonian density dependence. Here the controlling process
modifies population growth rate r by changing vital
rates, and is dependent on N, the population density
through negative feedback. In earthworm species, den-
Fig. 2. Body size growth
curves in E. fetida at different
densities (worms/l manure,
data from Domı́nguez and
Edwards (1997)) (A); the
relationship between age
specific reproduction and
body weight change (B) (data
from Van Gestel et al. 1992)
and (C) (left hand figure) the
combination of A and B,
reproduction vs density (see
text for explanation). The
grey triangle connects the
different scales of the vertical
axes for reproduction. The
right hand figure shows the
relationship between age
specific reproduction and
population growth rate
calculated using eq. (6).
92
OIKOS 100:1 (2003)
sity dependence of r was regulated by the impact on
reproduction and growth. The results imply that density-dependent regulation of population growth rate in
earthworms can be quantified using life-history analysis
and it appears that the outcomes of this analysis are in
agreement with empirical observations under field conditions. Although the data used for the model were
taken from different sources, they were comparable to
realistic field conditions with regards to temperature
and soil moisture conditions. The projections calculated
from the modified Euler–Lotka equation, which basically applies to exponential growing populations, agree
with field observations of population abundance.
Density values of L. terrestris in the field have shown
to be very variable among different habitats with densities being relatively higher in grass meadows than forest
soils. In a study on the field population dynamics of L.
terrestris, Daniel (1992) found densities ranging from
0.2 to a maximum of 4 worms per l (a patch of 0.25 m2
was sampled at 5 cm depth) in a grassland meadow.
Our model analyses suggest that above these levels (Fig.
1) density would influence population growth rate substantially. Abundance in the field of adults appeared to
remain fairly constant throughout the year. The high
density patches consisted mostly of juveniles and subadults, but there were also a fair number of adults
recorded. Bernier and Ponge (1998) reported densities
ranging from 1 to 3 worms per l in a mountain spruce
stand. Also Bengtsson et al. (1983) studied the density
of L. terrestris in forest soils. They reported a mean
density of 2 individuals per l soil. The field observed
densities by Daniel (1992) correlate well with the values
used in the studies by Butt et al. (1994a) and indicate
that the related impact of fecundity effects that translate to density dependent effects on r are comparable to
the field situation (Fig. 1).
For E. fetida information concerning field population
densities are not well documented. No formal field
density studies have been reported in the literature and
results under experimental conditions seem inconsistent
because of variations due to small differences in substrates (Domı́nguez et al. 1997). On a less formal level,
the fact that, in northern Europe, E. fetida primarily
inhabits discrete organic rich locations such as manure
and compost heaps has meant that this species has
become widely used in the vermicomposting and bait
industries. Under such conditions, and when in pure
culture, very high densities of 15 worms per l can be
reached as reported by Domı́nguez and Edwards
(1997). At these conditions, reproduction was impaired
although our life-history analyses showed that population growth rate was hardly influenced.
In addition to the Nicholsonian mediated dependence
excerpted through non-specific effects such as crowding, Baveco and DeRoos (1996) highlighted a number
of other density-dependent control factors which modify r but independently of N, such as food limitation
OIKOS 100:1 (2003)
and differential predation. Clearly, effects on r could
result due to food limitation for worms. However, in
the studies used to generate density based relationships
within our modelling framework, worms in all treatments were supplied with excess food (Butt et al. 1994a,
Domı́nguez and Edwards 1997). Thus it appears that
food availability per se was not the primary density
dependent mechanism in these studies, although the
possibility of such effects cannot be eliminated under
field conditions. For density dependent predation,
Baveco and DeRoos (1996) concluded that, because
earthworms make up a substantial portion of the diet
of over 200 vertebrate species, many of which display
prey density mediated foraging, this mechanism could
be an important control for field populations of
earthworms.
The observation of Nicholsonian density dependence
in L. terrestris at densities representative for field populations (e.g. based on the data of Daniel 1992, Bernier
and Ponge 1998), does not necessarily mean that this is
an important population regulation mechanism. Instead, such effects should be considered in their biological context. L. terrestris while it is a soil dwelling
earthworm is frequently active on the surface for foraging, by pulling leaves into its burrow and mating, which
occurs between worms whose tails remain anchored in
their burrows, and front ends become conjoined on the
soil surface (Butt and Nuutinen 1998). Such surface
activity makes this worm particularly vulnerable to
predators, such as birds, shrews and badgers (McCay
and Storm 1997, Goszczynski et al. 2000, Green et al.
2000). As suggested by Baveco and DeRoos (1996),
such predation is likely to be heaviest when populations
are dense and thus have the greatest chance of detection. Thus for L. terrestris it can be postulated that, due
to high surface activity, density dependent predation is
likely to be a key mechanism mediating population size
in L. terrestris, with Nicholsonian density dependence
having an impact on regulating the upper abundance
level.
An additional factor that could limit population sizes
of L. terrestris in field situations is territorial behaviour.
L. terrestris occupies established burrows. From these,
individuals will both feed and mate, while keeping their
tail ends anchored in the burrow entrance (Butt and
Nuutinen 1998, Michiels et al. 2001). In anecique earthworms, there is experimental evidence of a reluctance to
enter the area around occupied burrows (Capowiez and
Belzunces 2001). This means effectively that each burrow represents the centre of a circular territory. Territorial based systems have the potential to buffer
populations population size from environmental
changes and also to decrease the influence of density
dependence. In cases where number of suitable territories are limited, suitable sites will be occupied, with any
losses replaced from a small floating population. This
can make the population resilient to environmental
93
changes. In earthworms, such a territorial scenario for
population regulation appears unlikely as floating individuals are not likely to surviving frequent surface
movements. Populations could however be site dependent population mediated (Rodenhouse et al. 1997).
Such regulation driven by movement of individuals to a
more suitable adjacent territory should this become
free. Such transfers increase population growth rate
when few sites are occupied, however as population size
increases, the mean suitability of occupied sites will fall
resulting in slowed population growth rate and ultimately population stabilisation. Territorial behaviour in
L. terrestris thus presents a further population regulation mechanism in this species in addition to Nicholsonian feedback.
Despite the obvious tolerance of E. fetida to live at
high densities, knowledge of the biology of this species
does suggests that Nicholsonian density dependence
could be an important regulatory factor for field populations. Under ideal conditions, E. fetida has a comparatively high population growth rate due to its high
reproduction and relatively short juvenile period. The
relatively high value for r allows the worm to rapidly
colonise discrete locations (Sims and Gerard 1985).
During these periods of population growth, Nicholsonian mediated density dependence is absent, however,
as populations increase, these effects (coupled to denigration of the habitat) will impact increasingly more
strongly. At the highest densities (such as those known
to be reached in culture), population growth rate will
slow and it is in these circumstances that individuals
will begin to surface migrate in search of a new colonisation sites (Lee 1985). For density dependent predation, the fact that E. fetida is not surface active during
mating makes it less likely that density dependent predation has an influence on population dynamics in this
species. Further, territoriality is not known in this
species. Thus in this worm, Nicholsonian dependence
rather than predation or site dependent regulation may
be the key density mechanism regulating population
dynamics.
The life-history approach adopted in this paper has
identified that two earthworm species differ greatly in
the effect of density derived stress on r. Encouragingly,
the two scenarios generated from the model are entirely
consistent with the known biology of the two worms.
When the results are considered within context of their
importance for field population, the potential outcomes
for density for population regulation at first seem counter-intuitive. Thus while r in L. terrestris is strongly
impacted at increased densities, the fact that this worm
is rarely present in such abundance in the field suggests
that Nicholsonian density dependence may only be of
limited importance as regulatory mechanism at high
field densities. In other situations, density dependent
predation due to the high surface activity of this worm
and territoriality are likely to be the most important
94
controlling factors. E. fetida is tolerant to high densities, however, this worm can and does reach densities
that do impact heavily on r. The fact that this species is
not surface active and thus less likely to suffer density
dependent predation and is also not territorial, means
these regulatory mechanisms may be less important. In
this species Nicholsonian density dependence is thus
likely to be an important means of regulation for real
field populations. Such conclusions indicate the complex nature of potential density effects and their impact
in the field.
Acknowledgements – The work was conducted while DJS was
supported by a Natural Environment Research Council Advanced Fellowship (Ref. No. GT5/98/24/DAEC) held under
the DAEC scheme within the Environmental Diagnostic Thematic programme. Also we acknowledge the kind supply of
data by Kees van Gestel concerning Eisenia reproduction. We
also thank Chris Klok for comments on an earlier version of
the manuscript.
References
Andrewatha, R. V. and Birch, L. C. 1954. The distribution
and abundance of animals. – Univ. of Chicago Press.
Anonymous 1990. SAS Users Guide, Version 6, Fourth Edition, Vol. 2, Cary, NC, USA.
Baveco, J. M. and DeRoos, A. M. 1996. Assessing the impact
of pesticides on lumbricid populations: an individual-based
modelling approach. – J. Appl. Ecol. 33: 1451 – 1468.
Bengtsson, G., Nordström, S. and Rundgren, S. 1983. Population density and tissue metal concentration of lumbricids in
forest soils near a brass mill. – Environm. Poll. 30: 87 –
108.
Bengtsson, G., Hedlund, K. and Rundgren, S. 1994. Food-dependent and density-dependent dispersal-evidence from a
soil Collembolan. – J. Anim. Ecol. 63: 513 – 520.
Bernier, N. and Ponge, J. F. 1998. Lumbricus terrestris L.
distribution within an experimental humus mosaic in a
mountain spruce forest. – Biol. Fertil. Soils 28: 81 – 86.
Bouché, M. B. 1992. Earthworm species in ecotoxicological
studies. – In: Greig-Smith, P. W., Becker, H., Edwards, P.
J. and Heimbach, F. (eds), Ecotoxicology of earthworms.
Intercept Ltd, pp. 20 – 35.
Bouché, M. B., Haimi, J. and Huhta, V. 1988. Two earthworm
taxa (oligochaeta, Lumbricidae) new to Finland. – Fauna
Flora Fenn. 64: 65 – 67.
Butt, K. R. 1993. Reproduction and growth of three deep-burrowing earthworms (Lumbricidae) in laboratory culture in
order to assess production for soil restoration. – Biol.
Fertil. Soils 16: 135 – 138.
Butt, K. R. and Nuutinen, V. 1998. Reproduction of the
earthworm Lumbricus terrestris Linné after the first mating. – Can. J. Zool. 76: 104 – 109.
Butt, K. R., Frederickson, J. and Morris, R. M. 1994a. Effect
of earthworm density on the growth and reproduction of
Lumbricus terrestris L. (Oligochaeta, Lumbricidae) in culture. – Pedobiologia 38: 254 – 261.
Butt, K. R., Frederickson, J. and Morris, R. M. 1994b. The
life-cycle of the earthworm Lumbricus terrestris L.
(Oligochaeta, Lumbricidae) in laboratory culture. – Eur. J.
Soil Biol. 30: 49 – 54.
Capowiez, Y. and Belzunces, L. 2001. Dynamic study of the
burrowing behaviour of Aporrectodea nocturna and Allolobophora chlorotica: interactions between earthworms
and spatial avoidance of burrows. – Biol. Fertil. Soils 33:
310 – 316.
OIKOS 100:1 (2003)
Condit, R., Hubbell, S. P. and Foster, R. B. 1994. Density-dependence in 2 understorey tree species in a neotropical
forest. – Ecology 75: 671 –680.
Daniel, O. 1992. Population dynamics of Lumbricus terrestris
L. (Oligochaeta, Lumbricidae) in a meadow. – Soil Biol.
Biochem. 24: 1425 –1431.
DeRuiter, P. C., Neutel, A. M. and Moore, J. C. 1995.
Energetics, patterns of interaction strength, and stability in
real ecosystems. – Science 269: 1257 –1260.
Domı́nguez, J. and Edwards, C. A. 1997. Effects of stocking
rate and moisture content on the growth and maturation of
Eisenia andrei (Oligochaeta) in pig manure. – Soil Biol.
Biochem. 29: 743 –746.
Domı́nguez, J., Briones, M. J. I. and Mato, S. 1997. Effect of
the diet on growth and reproduction of Eisenia andrei
(Oligochaeta, Lumbricidae). – Pedobiologia 41: 566 – 576.
Edwards, C. A. and Bohlen, P. J. 1996. The biology and
ecology of earthworms. – Chapman and Hall.
Elvira, C., Domı́nguez, J. and Briones, M. J. I. 1996. Growth
and reproduction of Eisenia andrei and E. fetida
(Oligochaeta, Lumbricidae) in different organic residues. –
Pedobiologia 40: 377 –384.
Evans, A. C. and Guild, W. J. M. 1948. Studies on the
relationship between earthworms and soil fertility. IV. On
the life-cycles of some British Lumbricidae. – Ann. Appl.
Biol. 35.
Ferrer, M. and Donazar, J. A. 1996. Density-dependent fecundity by habitat heterogeneity in an increasing population of
Spanish Imperial Eagles. – Ecology 77: 69 –74.
Goszczynski, J., Jedrzejewska, B. and Jedrzejewski, W. 2000.
Diet composition of badgers (Meles meles) in a pristine
forest and rural habitats of Poland compared to other
European populations. – J. Zool. 250: 495 –505.
Green, R. E., Tyler, G. A. and Bowden, C. G. R. 2000.
Habitat selection, ranging behaviour and diet of the stone
curlew (Burhinus oedicnemus) in southern England. – J.
Zool. 250: 161 –183.
Haimi, J. 1990. Growth and reproduction of the compost-living earthworms Eisenia andrei and E. fetida. – Revue De
Ecologie Et De Biologie Du Sol 27: 415 –421.
Hartenstein, R. and Amico, L. 1983. Production and carrying
capacity for the earthworm Lumbricus terrestris in culture.
– Soil. Biol. Biochem. 15: 51 –54.
Hassell, M. P., Latto, J. and May, R. M. 1989. Seeing the
wood for the trees-detecting density dependence from existing life-table studies. – J. Anim. Ecol. 58: 883 – 892.
Hellriegel, B. 2000. Single- or multistage regulation in complex
life cycles: does it make a difference? – Oikos 88: 239 – 249.
Hopper, K. R., Crowley, P. H. and Kielman, D. 1996. Density
dependence, hatching synchrony, and within-cohort cannibalism in young dragonfly larvae. – Ecology 77: 191 – 200.
Kammenga, J. E., VanKoert, P. H. G., Koeman, J. H. and
Bakker, J. 1997. Fitness consequences of toxic stress evaluated within the context of phenotypic plasticity. – Ecol.
Appl. 7: 726 –734.
Klironomos, J. N. and Ursic, M. 1998. Density-dependent
grazing on the extraradical hyphal network of the arbuscular mycorrhizal fungus, Glomus intraradices, by the collembolan, Folsomia candida. – Biol. Fertil. Soils 26: 250 – 253.
OIKOS 100:1 (2003)
Lakhani, K. H. and Satchell, J. E. 1970. Production by
Lumbricus terrestris. – J. Anim. Ecol. 39: 472 – 492.
Lee, K. E. 1985. Earthworms: their ecology and relationships
with soils and land use. – Academic Press.
Lofs-Holmin, A. 1983. Reproduction and growth of common
arable land and pasture species of earthworms (Lumbricidae) in laboratory cultures. – Swed. J. Agric. Res. 13:
31 – 37.
McCay, T. S. and Storm, G. L. 1997. Masked shrew (Sorex
cinereus) abundance, diet and prey selection in an irrigated
forest. – Am. Midl. Nat. 138: 268 – 275.
Michiels, N. K., Hohner, A. and Vorndran, I. C. 2001. Precopulatory mate assessment in relation to body size in the
earthworm Lumbricus terrestris: avoidance of dangerous
liaisons? – Behav. Ecol. 12: 612 – 618.
Neuhauser, E. F., Kaplan, D. L. and Malecki, M. R. 1980.
Materials supporting weight gain by the earthworm E.
foetida in waste conversion systems. – Agric. Wastes 2:
89 – 97.
Nicholson, A. J. 1933. The balance of animal populations. – J.
Anim. Ecol. 2: 131 – 178.
Reinecke, A. J. and Kriel, J. R. 1981. Influence of temperature
on the reproduction of the earthworm Eisenia foetida
(Oligochaeta). – S. Afr. J. Zool. 16: 96 – 100.
Reinecke, A. J., Viljoen, S. A. and Saayman, R. J. 1992. The
suitability of Eudrilus eugeniae, Perionyx exca6atus and
Eisenia foetida (Oligochaeta) for vermicomposting in
Southern Africa in terms of their temperature requirements. – Soil Biol. Biochem. 24: 1295 – 1307.
Rodenhouse, N. L., Sherry, T. W. and Holmes, R. T. 1997.
Site-dependent regulation of population size: a new synthesis. – Ecology 78: 2025 – 2042.
Sale, P. F. and Tolimieri, N. 2000. Density dependence at
some time and place? – Oecologia 124.
Sims, R. W. and Gerard, B. M. 1985. Earthworms. – Linnean
Society and the Estuarine and Brackish-Water Sciences
Association.
Tanner, J. E. 1999. J. Anim. Ecol. 68: 390 – 399.
Tsukamoto, J. and Watanabe, H. 1977. Influence of temperature on hatching and growth of Eisenia foetida. – Pedobiologia 17.
Van Gestel, C. A. M., Dirven-Van Breemen, E. M. and
Baerselman, R. 1992. Influence of environmental conditions on the growth and reproduction of the earthworm
Eisenia andrei in an artificial soil substrate. – Pedobiologia
36: 109 – 120.
Venter, J. M. and Reinecke, A. J. 1988. The life-cycle of the
compost worm Eisenia fetida (Oligochaeta). – S. Afr. J.
Zool. 23: 161 – 165.
Watanabe, H. and Tsukamoto, J. 1976. Seasonal changes in
size, class and age structure of the lumbricid Eisenia foetida
population in a field compost and its practical application
as the decomposer of organic waste matter. – Rev. D’Ecol.
Biol. Sol 13: 141 – 146.
Wilkens, S. and Exo, K. M. 1998. Population size and density
dependant effects on breeding success in Herring Gulls
(Larus argentatus) on Mellum island. – J. Ornithol. 139:
21 – 36.
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