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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 OIKOS 100:1 (2003) 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. 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