Does reproductive plasticity in Lumbricus rubellus improve the recovery

of populations in frequently inundated river floodplains?

Chris Kloka,*, Mathilde Zornb, Josee E. Koolhaasb, Herman J.P. Eijsackersb,

Cornelis A.M. van Gestelb

aALTERRA, Department of Ecology and Environment, Droevendaalsesteeg 3, P.O. Box 47, 6700 AA Wageningen, The NetherlandsbVrije Universiteit Amsterdam, Institute of Ecological Science, De Boelelaan 1085, 1081 HV Amsterdam, The Netherlands

Received 19 October 2004; received in revised form 10 June 2005; accepted 14 June 2005

Available online 20 July 2005

Abstract

Flooding events often eradicate all of the individuals of the earthworm species Lumbricus rubellus living in river floodplains, although

earthworm cocoons usually survive immersion, permitting populations to recover after the flood waters recede. Yet, if the area is flooded

again before earthworms hatching from cocoons or migrating from adjacent areas reach reproductive maturity, it is unlikely that their

populations will recover. The objective of this study is to determine the importance of the length of the dry period for population recovery in

L. rubellus. Earthworms were collected at three floodplain sites along the Rhine River that were frequently, moderately or seldom flooded.

Reproductively mature L. rubellus from the frequent flooded site were half the weight and probably younger than those from the other sites. A

mechanistic population model was used to estimate the time for earthworm development from hatching to reproductive maturity, and to

calculate the probability of population recovery after flooding. The model results show that the probability of extinction increases when the

dry period is not long enough for individuals to reach reproductive maturity. When this condition is met population extinction is virtually

absent resulting from the high lifetime reproductive output of L. rubellus. Parameterization of the model with site-specific data indicate that

population survival on the site with the shortest dry period drastically decreases if worms mature at the weight measured at the other sites.

The results therefore strongly suggest that the dry period is critical for population recovery in river floodplains and that earthworm

populations have adapted to local (site-specific) conditions.

q 2005 Elsevier Ltd. All rights reserved.

Keywords: L. rubellus; Population model; River floodplain; Flooding; Recovery; Adaptation

1. Introduction

As a result of frequent inundation, river floodplains form

one of the most fertile soils of the earth. Soil invertebrates,

such as earthworms, can reach high densities in these soils

(Lavelle and Spain, 2001). However, to maintain viable

population levels in river floodplains, earthworms must

cope with the stress induced by frequent flooding. Zorn et al.

(2005) found a reduction in the biomass of the most

abundant species, Aporrectodea caliginosa and Lumbricus

rubellus, after an inundation period. This decline was

greatest for the epigeic species L. rubellus, which inhabits

0038-0717/$ - see front matter q 2005 Elsevier Ltd. All rights reserved.

doi:10.1016/j.soilbio.2005.06.013

* Corresponding author. Fax: C31 3117 477871.

E-mail address: chris.klok@wur.nl (C. Klok).

the top 10 cm soil profile. In L. rubellus virtually all life

stages, with the exception of cocoons, were absent when

floods subsided (Zorn et al., 2005). Consequently L. rubellus

populations have to recover after an inundation period,

either by immigration from non-flooded areas, or from

cocoons. Migration rates for L. rubellus range from 8 to

11 m yK1 (Hoogerkamp et al., 1983; Curry and Boyle,

1987; Marinissen and Van den Bosch, 1992), but the

distance between non-flooded areas and the center of

flooded sites is often more than 100 m, suggesting that

immigration does not contribute much to population

recovery after the flood waters recede. Population recovery

from surviving cocoons seems more likely, and has been

suggested for epigeic species by Pizl (1999). Moreover,

cocoons are not harmed by immersion, and under laboratory

conditions can even hatch under water (Roots, 1956).

If soil temperature and moisture content are suitable,

cocoons can be produced throughout the year (Edwards and

Soil Biology & Biochemistry 38 (2006) 611–618

www.elsevier.com/locate/soilbio

C. Klok et al. / Soil Biology & Biochemistry 38 (2006) 611–618612

Lofty, 1977). However, seasonal fluctuation in these soil

factors can cause strong variation in cocoon production

(Gerard, 1967). In northern Europe and America, cocoon

production in Allolobophora chlorotica and A. caliginosa is

mainly restricted to the first 6 months of the year and peaks

in late spring and early summer (Gerard, 1967), whereas in

Lumbricus terrestris, L. rubellus and Aporrectodea tuber-

culata cocoon production peaks in mid summer and

recruitment of juveniles occurs primarily in autumn

(Whalen et al., 1998). In L. rubellus cocoons can develop

in 36–112 days (Gerard, 1960 cited in Lee, 1985).

Development time strongly depends on soil temperature

(Holmstrup et al., 1991) and may be delayed when soil

moisture conditions are unfavorable (Lee, 1985; Sims and

Gerard, 1985).

Under the assumption that population recovery in

L. rubellus after a flood results primarily from cocoons

which can be produced throughout the year, may develop

under water, and hatch within the year, viability of local

populations will be constrained by the site-specific

inundation regime: the duration of inundation and the

length of the dry period (time span between subsequent

floods). If flooding takes place repetitively in a year and

none of the dry periods is long enough for individuals to

grow from hatched cocoons to maturity, population

recovery will certainly be disrupted.

The objective of this study is to determine the importance

of the length of the dry period for population recovery in

L. rubellus. Three sites with different inundation regimes

were selected based on specific geographical data and water

levels over a 15 year reference period. The critical dry

period for population survival was assessed with

Table 1a

Field characteristics of the frequently F, moderately M and seldom S inundated s

Code Name Location Height (level

above NAPa)

F Afferdensche en

Deestsche Waarden

51854 0N,5839 0E 765 cm

M Lage Hof 51845 0N,4845 0E 100 cm

S Petrusplaat Oost 51845 0N,4847 0E 140 cm

a NAP (Nieuw Amsterdams Peil).

Table 1b

Soil characteristics and heavy metal levels of the frequently F, moderately M and

Code pH Organic matter Clay (!2 mm)

n % n % n

F 7.3

(0.17)

20 14.7

(3.22)

8 20.2

(2.14)

30

Ma 7.1

(0.03)

10 18.8

(2.0)

3 35.1

(1.1)

3

Sa 7.1

(0.09)

5 11.4

(0.6)

5 20.5

(2.6)

5

a Data from Hobbelen et al. (2004).

a deterministic population model. A stochastic version of

this model was used to assess the population survival

probability, as influenced by the length of the dry period,

and validated with data from earthworm populations living

in the three study sites.

2. Material and methods

2.1. Field sites and flooding intensity

Three sites with different inundation regimes were

selected: the Afferdensche and Deestsche Waarden, a

frequently (F) inundated site, Lage Hof, a moderately

(M) inundated site, and Petrusplaat Oost a seldom (S)

inundated site. Field and soil characteristics are given in

Tables 1a and 1b.

Water levels have been monitored along the Rhine River

and its tributaries by ‘Rijkswaterstaat’, a department of the

Dutch Ministry of Transport, Public Works and Water

Management. These monitoring data are available to the

public (www.waterbase.nl). The monitoring point Dode-

waard (longitude 51854 0N, latitude 5839 0E) is about 200 m

upstream from site F, and Deenenplaat (longitude 51845 0N,

latitude 4847 0E) is the nearest monitoring point to the sites

M and S. We used water levels at the monitoring points

recorded from 1974 to 1989 as a reference and assumed that

the average values and variation in river water levels during

the reference period would be representative of current

levels. We described the inundation regime at each site by

the frequency of flooding during the year, the time that

ites

Grazing Vegetation

Horses Elitrigia repens, Agrostis stolonifera, Cirsium

arvense, Potentilla reptans, Potentilla anserina

No grazing Phragmites australis, Urtica dioica, Symphytum

officinale, Valeriana officinalis

No grazing Phragmites australis, Urtica dioica, Anthriscus

sylvestris

seldom S inundated site. Standard deviations are given in parentheses

Zinc Copper Cadmium

mg/kg n mg/kg n mg/kg n

514

(203)

43 67

(25)

43 3.78

(1.52)

43

2333

(404)

3 387

(31)

3 19.3

(0.6)

3

1140

(114)

5 142

(18)

5 11.7

(1.7)

5

C. Klok et al. / Soil Biology & Biochemistry 38 (2006) 611–618 613

the site remains inundated and the duration of the longest

dry period in the year.

2.2. Earthworm collection

At all sites earthworms were collected by hand-sorting in

spring in 2002 and 2004 from six quadrants (0.25!0.25!0.25 m) distributed randomly over the part of the site which

had been flooded. The weight of individuals in juvenile,

sub-adult and adult development classes was determined.

Earthworms were considered sub-adult if they had a full

tubercula pubertatis but no clitellum and adult if they were

clittellate (Sims and Gerard, 1999).

2.3. Data analysis

Normality of the data was analyzed with Kolomogorov–

Smirnov and Shapiro–Wilk tests. Sets of normal distributed

data were analyzed using analysis of variance (one-way

ANOVA) followed by a Tukey Post-Hoc test to analyze for

significant (P!0.05) differences between sites. Data that

were not normal distributed (also not when transformed)

where analyzed with non-parametrical Mann Whitney U

test. All statistics were performed using the statistical

software SPSS 10.1 for Windows.

2.4. Population model

The growth and reproduction of individual L. rubellus

were estimated using the mechanistic model described by

Klok and de Roos (1996). The growth of individuals is

estimated from the von Bertalanffy growth curve (Eq. (1))

and reproduction by Eq. (2).

lðaÞ Z lm Kðlm KlbÞeKg:a (1)

where l(a) equals the weight to the power of one third (W1/3)

of an individual of age a, lm the maximal attainable weight

(W1/3), lb the weight (W1/3) at hatching, g the von

Bertalanffy growth rate.

mðaÞ Z rm½lmKðlmKlbÞeKg:a�2 for lðaÞR lad (2)

where m(a) the reproduction rate of an individual of age a,

rm the maximum reproduction rate per unit of surface area,

and lad maturation weight (W1/3).

The lifetime reproductive output (R0) (Eq. (3))

of individuals is used as an indicator of population

survival.

R0 Z

ðtime

AðladÞ

mðaÞSðaÞda; (3)

with A(lad) the age of maturation in days (were

maturation weight is transposed to age by Eq. (1)),

time the dry period (the time span in days between two

floods), S(a) background mortality, and a age.

In an environment where the length of flooding and dry

periods is constant from year to year, an earthworm

population can persist if the lifetime reproductive output

is equal to or greater than one. Therefore, we can set R0 in

Eq. (3) to one and solve for time to determine the critical dry

period for population survival. In an environment where dry

period varies an earthworm population will persist only if

(a) at least one cocoon can grow to maturity each year, and

(b) population numbers (including cocoons) do not drop

below one over the years, and (c) the mean R0 over a long

time period is larger than or equal to one.

First, we assessed the probability of population extinc-

tion when the dry period was less than the critical value such

that cocoons hatching when flood waters receded did not

mature before the next flood. We assessed the percentage of

100 populations for which the variable time (a random draw

from a distribution of dry periods, assuming that the lengths

of these periods are independent over the years) is smaller

that the development time from hatched cocoon to adult

(A(lad)) in one of the simulated 100 years, and repeated this

procedure for a range of maturation weights (lad). Secondly,

for those populations that did not go extinct in the first step,

we calculated the development in number over 100 years

with Eq. (4) to assess the percentage of populations for

which numbers drop below one.

NtC1 Z R0$Nt (4)

with the initial condition 100 individuals, R0 a realization of

Eq. (3) and time a random draw from a distribution of dry

periods.

In the last step we calculated the mean R0 and 95%

confidence interval of the populations that survived the first

two steps.

2.5. Model parameterization and simulations with site

specific earthworm data

Parameter values for L. rubellus are given in Table 2.

Parameter values of lad vary from 300 to 1000 mg. We

based this range on the weights of adults measured at the

three sites which was never below 300 mg (see Table 3).

Under the assumption that population extinction only

occurs as a consequence of a too short dry period, such that

individuals do not mature, we assessed the number of

succeeding years out of a 100 for which time R(A(lad)). In

this calculation the variable time is a random value drawn

from the site specific distribution of dry periods and (A(lad))

the site-specific maturation age, based on the mean weight

of mature earthworms sampled in 2002.We repeated this

procedure for 10000 populations and assessed the percen-

tage of populations which survive the full simulation period

of 100 years and the frequency distribution of the number of

succeeding years populations survive.

Table 2

Parameter values for L. rubellus used for parameterization of the population model

Parameter Value Source

lad Adult weight (mg1/3) This study, see Table 3

lb 2.41 (mg1/3) Klok and de Roos, 1996a

lm 12.3 (mg1/3) Klok and de Roos, 1996a

g 0.014 (dK1) Klok and de Roos, 1996a

rm 0.001 ((mg1/3)K2 dK1 Klok and de Roos, 1996a

SðtÞZ ðð1KatÞ=ð1CbtÞÞk with aZ0.0014 bZ0.02 kZ0.369 Klok and de Roos, 1996a

a These data come from laboratory studies on L. rubellus and the survival data have been modified from laboratory studies on L. terrestris.

Table 3

Mean weights of L. rubellus juvenile, sub-adults and adults collected from a frequently F, moderately M and seldom S inundated floodplain site along the Rhine

River in 2002 and 2004

2002 Juvenile (g fw) Subadult (g fw) Adult (g fw)

Site Mean SD n Mean SD n Mean SD n

(F) 0.161a 0.084 13 0.320a 0.100 6 0.504a* 0.185 22

(M) 0.281b 0.169 31 0.627b* 0.085 6 0.714b 0.209 16

(S) 0.384c 0.193 24 0.761c* 0.158 4 0.972c 0.301 24

2004

(F) 0.253a 0.051 4 0.328a 0.058 6 0.404a* 0.169 16

(M) 0.384a 0.113 59 0.425a 0.131 23 0.719b 0.169 50

(S) 0.229a 0.091 39 0.565b* 0.186 20 0.872c 0.344 39

Values within a column followed by a different letter and values between columns followed by a * are significantly different (P!0.05, Tukey test).

C. Klok et al. / Soil Biology & Biochemistry 38 (2006) 611–618614

3. Results

3.1. Field data

0

20

40

60

80

100

nuar

yru

ary

arch

April

May

June Ju

lyug

ust

mbe

rto

ber

mbe

rm

ber

flood

ing

freq

uenc

y (%

)

3.1.1. Inundation regime

Flooding in The Netherlands usually occurs in winter and

early spring. Site S is frequently flooded from October to

February, while flooding may occur at site M from

September to June and at site F in nearly all months of the

year (except September and November) (Fig. 1). Flood

waters tend to remain for one week at site S, one to two at

site M and up to 8 at site F (Fig. 2). The mean time site F

remained flooded over the reference period equaled 2.5

weeks with a maximum of 8 weeks, whereas sites M and S

usually were inundated for less than a week. Site S is seldom

inundated, such that the longest dry period in most years

equal 365 days, resulting in a right skewed distribution of

dry periods. Contrary to site S, the distribution at the other

two sites is normal (P!0.05) and not skewed. The mean

longest dry period in the year is significantly longer at site S

than at site F and M (non-parametrical Mann Whitney U test

P!0.001). On average, the longest dry period in the year

equals 269G76 d at site F, 283G51 d at site M and 340G25 d at site S.

Ja Feb M A

Septe Oc

Nove

Dece

Fig. 1. Frequency of monthly flooding events at floodplain sites along the

Rhine River during 15-year period (1974–1989). The floodplains were

classified as frequent (F) open bar, moderately (M) grey, and seldom (S)

dark bar.

3.1.2. Earthworm data

In both years the weight of adult L. rubellus sampled at

site F was significantly lower than at the other two sites

(Table 3). Moreover, the mean weight of adults at site F was

lower than the mean weight of sub-adults (P!0.05, Tukey

test) at site M and S in 2002 and at site S in 2004.

3.2. Population effects

3.2.1. Constant dry period

The parameter space of combinations of maturation

weights and length of dry periods where L. rubellus can

persist are shown in Fig. 3. The line in this graph indicates

the critical dry period, where R0 equals one, below this line

the modeled population goes extinct, and above the line the

population is viable. From the graph, it appears that the

critical dry period increases linearly with maturation weight.

0

20

40

60

80

100

1 2 3 4 5 6 7 8time (wks)

flood

dur

atio

n fr

eque

ncy

(%)

Fig. 2. Frequency of the duration of floods in weeks at floodplain sites along

the Rhine River during 15-year period (1974–1989). The floodplains were

classified as frequent (F) open bar, moderately (M) grey, and seldom (S)

dark bar.maturation weight (mg)

400 600 800 1000

pop

ulat

ion

extin

ctio

ns (

%)

0

20

40

60

80

100

Fig. 4. Proportion of population extinctions in L. rubellus, based on the

number of populations out of 100 which go extinct within 100 years.

Populations live in a variable environment with dry periods randomly

drawn from the F site distribution of dry periods, extinctions resulting from

a too short dry period such that individuals do not mature.

C. Klok et al. / Soil Biology & Biochemistry 38 (2006) 611–618 615

3.2.2. Variable dry period

The percentage of populations that go extinct resulting of

a too short dry period for populations living under

the inundation regime of the most frequent flooded site is

given in Fig. 4. This graph shows a strong increase in the

percentage of populations that go extinct with an increase in

maturation weight. Of the surviving populations, numbers

assessed with equation 4, increased and not one population

went extinct (results not shown). The mean life-time

reproductive output per year of these populations decreases

with maturation weight from about 14 for populations

maturing at 300 mg to 11 for populations that mature at

1000 mg (Fig. 5). However, these values are all much higher

than the critical value of R0 equal to one.

3.2.3. Model support from field data

With variation in dry period of the frequently flooded

site and maturation based on site specific data of adult

weights, populations survive longer at site F as shown by

the frequency distribution of population persistence (the

number of succeeding years populations survive)

maturation weight (mg)

400 600 800 1000

dry

perio

d (d

)

0

50

100

150

200

R0<1

R0>1

Fig. 3. Parameter space of combinations of maturation weight and dry

period where L. rubellus populations can persists. Contour R0 equals 1

separates extinction (R0!1) from persistence (R0O1) region.

(Fig. 6a). The percentage of populations which survive

the full simulation period of 100 years decrease from

76% for weights measured at site F, to 59% for site M

and 26% for site S (read from Fig. 6a). The frequency

distribution is strongly right skewed for site F and M, but

more evenly distributed for site S. We applied the same

procedure for the distribution of dry periods of site M,

which resulted in strong increase in the number of years

populations survive (Fig. 6b). For maturation based on

weights measured at site F and M all populations survive

the full simulation period of 100 years whereas at site

S 98% of the populations survived. Given the fact that

with stochasticity in dry periods drawn randomly from

the M distribution all populations already survive

almost ceaselessly, investigation of the mean survival

time with the S distribution has not been further

explored.

maturation weight (mg)

400 600 800 1000

mea

n R

0 (y

–1)

8

10

12

14

16

Fig. 5. Lifetime reproductive output of L. rubellus populations (mean and

95% CI). Populations living in a variable environment with dry periods

randomly drawn from the F site distribution under the condition that the dry

period is long enough for individuals to mature.

0

20

40

60

80

100

10 20 30 40 50 60 70 80 90 100

persistence time (y)

num

ber

of p

opul

atio

ns (

%)

(a)

0

20

40

60

80

100

10 20 30 40 50 60 70 80 90 100

persistence time (y)

num

ber

of p

opul

atio

ns (

%)

(b)

Fig. 6. Frequency of the number of succeeding years L. rubellus populations survive if extinctions only result from a too short dry period such that individuals

do not mature. Maturation based on adult weights measured in 2002 at site F (open bar), M (grey bar) or S (dark bar). Populations live in a variable environment

with dry periods randomly drawn from: (a) the F site distribution of dry periods, (b) the M site distribution of dry periods.

C. Klok et al. / Soil Biology & Biochemistry 38 (2006) 611–618616

4. Discussion

4.1. Field data

Data collected from the floodplain sites show that

reproductive mature L. rubellus weight less at the frequently

inundated site than those that were moderately or seldom

inundated, suggesting that at the frequently inundated site

individuals mature at a lower weight and a younger age.

This change in life-history may be an adaptation to the site

specific flooding regime. Adaptation to flooding regimes

have been described for many species (Adis and Junk, 2002;

Lytle and Poff, 2004).

4.2. Model results

We hypothesized that the duration of the longest dry

period is critical for population recovery. Explorations with

the mechanistic model, which relate adult weights to

development time for L. rubellus, show a clear relation

between dry period and population survival and indicate that

the probability of population extinction mainly results from

not maturing as a consequence of a too short dry period.

When individuals can mature population extinction is

virtually absent resulting from the high R0 value of the

species. Our model result for R0, which ranges from 14 to 11

yK1, is near to the R0 value of 15.8 yK1 calculated by

Marinissen and Van den Bosch (1992).

The results of the model parameterized with site-specific

data on dry period and mean weight of sampled mature

earthworms, indicate that the relatively low weight of adults

at site F is important for survival of this population, whereas

the weights sampled at site M and S are not critical for the

viability of these populations. This result strongly suggest

that the population living at site F is adapted by plasticity in

maturation weight to the local inundation regime.

Possible effects of the duration of the inundation period

are not explored in this paper. We assumed that this

parameter has no negative influence on cocoon survival.

This seems reasonable given the relative insensitivity of

cocoon survival for inundation (Roots, 1956), and the

duration of inundation (mean at site F 2.5 weeks, and only

10% longer than 4 weeks), which is short compared to

cocoon development time (36 to 112 days (Gerard, 1960

cited in Lee, 1985).

The model results depend heavily on the assumption that

there is little recolonization of the site by immigrating

earthworms. Recolonization may occur but is expected to be

low given the slow rate of migration in L. rubellus

(Hoogerkamp et al., 1983; Curry and Boyle, 1987;

Marinissen and Van den Bosch, 1992) and the distance

over which migration has to take place. In a study on the

effects of winter-flooding on earthworms in grasslands,

Ausden et al. (2001) also concluded that recolonization after

re-immersion was very slow. They found that the total

biomass of L. rubellus sampled in spring in fields that were

inundated in winter was reduced more than 10 fold

compared to non winter-flooded grasslands.

4.3. Model improvements and data requirements

We parameterized our model with parameter values from

growth curves of L. rubellus living under laboratory

conditions in sandy loam soil and with unlimited food

because growth curves for L. rubellus in river floodplain soil

do not currently exist. These laboratory based values may

give an underestimate of the maturation age and a

corresponding overestimate of the R0 values since limited

quantities of food may be present in the field. If it takes longer

for L. rubellus to reach reproductive maturity in floodplains

than we have assumed, the length of the dry period would

become even more critical for population survival.

C. Klok et al. / Soil Biology & Biochemistry 38 (2006) 611–618 617

4.4. Other factors

Differences in adult weight measured at the three sites

may result form other factors than flooding only. Sites

differ, next to flooding regime, in food conditions (resulting

from vegetation and grazing), soil characteristics, and

pollutant levels (Table 1). Food conditions have a strong

impact on weight gain and sexual development in earth-

worms (Edwards and Lofty, 1977). In particular, consuming

nitrogen rich food leads to faster earthworm growth and

more cocoon production than food with lower nitrogen

availability (Evans and Guild, 1948). Of the soil character-

istics clay contents negatively correlates with weight in

L. rubellus (Vandecasteele et al., 2004), and organic matter

contents of soil below 20% may negatively influence growth

since levels above 20% are considered optimal in earth-

worms (Curry et al., 2002). Also pollutants may have a

negative effect on weight development, at polluted sites

populations may be selected for faster growth, earlier

maturation and increased reproductive effort (Sibly and

Carlow, 1989; Charlesworth, 1994).

The grasses and animal dung available at the F site seem

a better food source than the organic substrates present at

the other two sites. Yet adult L. rubellus still weighted less

at site F than at the other sites. This lower weight at site F

can also not be explained by the soil characteristics or

pollutant levels of the sites, since soil characteristics of site

F are comparable with site S, and pollutant levels are higher

at site M and S (Table 1b).

4.5. Conclusion and implications for river management

The lower adult weight at the frequently inundated site

is probably a result of earthworm adaptation to the local

inundation regime. Adaptation in life-history character-

istics usually evolves slowly (Lytle and Poff, 2004), and so

human induced changes in flooding may have large effects

on the population viability of L. rubellus. Recent disastrous

floods in Europe encouraged the development of water-

related regulations (e.g. EU Water Framework Directive

(EU, 2000)), that are directed at reducing the risk of

flooding and focus on restoration or rehabilitation of river

landscapes (Jungwirth et al., 2002). Before rehabilitation,

the Rhine floodplain system was characterized by perma-

nent water and an aquatic-terrestrial transition zone, which

was dry for most of the year (Buijse et al., 2002) and most

cultivated. Restoration of floodplains in The Netherlands

aims to transform agricultural lands into new wetlands

(Nienhuis et al., 1998). This activity includes lowering and

widening of floodplains, which will result in an increase in

frequency and duration of inundation, and a subsequent

reduction of the duration of dry periods. The question

remains to what extent earthworms can maintain viable

populations in these river floodplains. Earthworms are an

important food source for many species (Lee, 1985). For

some of these predators, like the badger Meles meles and

the little owl Athene noctua vidalli, which have a

conservation status in The Netherlands, river-floodplains

form an important foraging habitat. River management

directed at increasing the area of flooded riverbanks, which

can be expected to decrease the area of habitat suitable for

earthworms, therefore may have unforeseen and adverse

effects on these protected species.

Acknowledgements

Professor R. Laskowski and Dr. J.C.Y Marinissen are

acknowledged for critically reviewing an earlier version of

the manuscript. We also thank an anonymous reviewer

whose comments have greatly increased the readability of

the manuscript. The Netherlands Science Foundation

(NWO) and the Department of Science and Knowledge

dissemination of the Ministry of Agriculture, Nature and

Nutrition quality of The Netherlands financially supported

this research which was performed within the framework of

the Stimulation Program System-oriented Ecotoxicological

Research (SSEO).

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