Does reproductive plasticity in Lumbricus rubellus ...

Soil Biology & Biochemistry 38 (2006) 611–618 www.elsevier.com/locate/soilbio

Does reproductive plasticity in Lumbricus rubellus improve the recovery of populations in frequently inundated river floodplains? Chris Kloka,*, Mathilde Zornb, Jose´e E. Koolhaasb, Herman J.P. Eijsackersb, Cornelis A.M. van Gestelb a

ALTERRA, Department of Ecology and Environment, Droevendaalsesteeg 3, P.O. Box 47, 6700 AA Wageningen, The Netherlands b Vrije 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

* Corresponding author. Fax: C31 3117 477871. E-mail address: [email protected] (C. Klok).

0038-0717/$ - see front matter q 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.soilbio.2005.06.013

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

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

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 tuberculata 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

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 Dodewaard (longitude 51854 0 N, latitude 5839 0 E) is about 200 m upstream from site F, and Deenenplaat (longitude 51845 0 N, latitude 4847 0 E) 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

Table 1a Field characteristics of the frequently F, moderately M and seldom S inundated sites Code

Name

Location

Height (level above NAPa)

Grazing

Vegetation

F

51854 0 N,5839 0 E

765 cm

Horses

M

Afferdensche en Deestsche Waarden Lage Hof

51845 0 N,4845 0 E

100 cm

No grazing

S

Petrusplaat Oost

51845 0 N,4847 0 E

140 cm

No grazing

Elitrigia repens, Agrostis stolonifera, Cirsium arvense, Potentilla reptans, Potentilla anserina Phragmites australis, Urtica dioica, Symphytum officinale, Valeriana officinalis Phragmites australis, Urtica dioica, Anthriscus sylvestris

a

NAP (Nieuw Amsterdams Peil).

Table 1b Soil characteristics and heavy metal levels of the frequently F, moderately M and seldom S inundated site. Standard deviations are given in parentheses Code

pH n

F Ma Sa a

7.3 (0.17) 7.1 (0.03) 7.1 (0.09)

20 10 5

Organic matter % n

Clay (!2 mm) % n

Zinc mg/kg

14.7 (3.22) 18.8 (2.0) 11.4 (0.6)

20.2 (2.14) 35.1 (1.1) 20.5 (2.6)

514 (203) 2333 (404) 1140 (114)

Data from Hobbelen et al. (2004).

8 3 5

30 3 5

n 43 3 5

Copper mg/kg 67 (25) 387 (31) 142 (18)

n 43 3 5

Cadmium mg/kg n 3.78 (1.52) 19.3 (0.6) 11.7 (1.7)

43 3 5


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

lðaÞ Z lm Kðlm Klb ÞeKg: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 rm ½lm Kðlm Klb ÞeKg: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. time ð

R0 Z

mðaÞSðaÞda;

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 extinction 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

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).

(3)

Aðlad Þ

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.

613

(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 percentage of populations which survive the full simulation period of 100 years and the frequency distribution of the number of succeeding years populations survive.

614


Table 2 Parameter values for L. rubellus used for parameterization of the population model Parameter

Value Adult weight (mg ) 2.41 (mg1/3) 12.3 (mg1/3) 0.014 (dK1) 0.001 ((mg1/3)K2 dK1 with aZ0.0014 bZ0.02 kZ0.369

lad lb lm g rm SðtÞZ ðð1KatÞ=ð1C btÞÞk a

Source 1/3

This study, see Table 3 Klok and de Roos, 1996a Klok and de Roos, 1996a Klok and de Roos, 1996a Klok and de Roos, 1996a Klok and de Roos, 1996a

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

Mean

SD

n

(F) (M) (S) 2004 (F) (M) (S)

0.161a 0.281b 0.384c

0.084 0.169 0.193

13 31 24

0.320a 0.627b* 0.761c*

0.100 0.085 0.158

6 6 4

0.504a* 0.714b 0.972c

0.185 0.209 0.301

22 16 24

0.253a 0.384a 0.229a

0.051 0.113 0.091

4 59 39

0.328a 0.425a 0.565b*

0.058 0.131 0.186

6 23 20

0.404a* 0.719b 0.872c

0.169 0.169 0.344

16 50 39

n

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

3. Results

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.

3.1. Field data 3.2. Population effects

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

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.

flooding frequency (%)

100 80 60 40 20 0 Ja nu Fe ary br ua r M y ar ch Ap ril M ay Ju ne Ju Au ly Se gu pt st em b O er ct ob N ov er e D mb ec e em r be r

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 340G 25 d at site S.

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.

80 60 40 20 0 1

2

3

4 5 time (wks)

6

7

8

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.

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) 200 R0>1

dry period (d)

150

100

50 R0