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Effect of flooding by fresh and brackish water on earthworm communities along Matsalu Bay and the Kasari River
European Journal of Soil Biology 53 (2012) 11e15
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European Journal of Soil Biology journal homepage: http://www.elsevier.com/locate/ejsobi
Original article
Effect of flooding by fresh and brackish water on earthworm communities along Matsalu Bay and the Kasari River Mari Ivask*, Mart Meriste, Annely Kuu, Sander Kutti, Eduard Sizov Tartu College of Tallinn University of Technology, Puiestee 78, 51008 Tartu, Estonia
a r t i c l e i n f o
a b s t r a c t
Article history: Received 20 March 2012 Received in revised form 2 August 2012 Accepted 10 August 2012 Available online 27 August 2012 Handling editor: Stefan Schrader
The continuum of Matsalu Bay and the Kasari River located on the east coast of the Baltic Sea represents a complex mosaic of marine, coastal and inland wetlands (shallow sea waters, estuarine waters, coastal lagoons, an inland delta and flooded meadows). Earthworm communities were studied at five sites on the southern shore of Matsalu Bay and the banks of the Kasari River under different salt water regimes (brackish or fresh water). Sample sites were located along a flooding gradient (distance from the sea). Flooding duration appears to have the strongest negative impact on the abundance of earthworm communities, which largely depends on species’ tolerance of high moisture content and low soil aeration. The brackish conditions of the Baltic Sea create special habitat conditions; the sea water salinity and periodic flooding have a significant negative impact on earthworm communities. Ó 2012 Elsevier Masson SAS. All rights reserved.
Keywords: Earthworms Diversity Flooded grasslands Brackish conditions
1. Introduction The continuum of Matsalu Bay and the Kasari River in the eastern Baltic Sea represents a complex mosaic of marine, coastal and inland wetlands (shallow sea waters, estuarine waters, coastal lagoons, an inland delta and flooded meadows) characteristic of the boreal biogeographical region. The brackish conditions of the Baltic Sea create special habitats in the coastal grassland soils surrounding Matsalu Bay. Equally, the floodplains of the Kasari River are periodically flooded by fresh water. In the eastern part of Matsalu Bay and in the delta of the river, brackish and fresh water can be mixed due to strong winds from the west or due to exceptionally large amounts of fresh water flowing from the river in the spring [1,2]. Flooding significantly alters the habitat of earthworm communities because of high moisture and poor aeration. It has long been known that in coastal areas earthworms are vulnerable to saline substrates, expelled from the soil by the salt solution and killed by immersion in sea water, and are therefore scarce or absent in saline soils [3,4]. The spatial distribution and abundance of earthworms are affected by sea water salinity, periodical flooding, habitat dry-off and unfavorable soil texture [5e7]. A reduction in the abundance and biomass of earthworm communities on European floodplains was concluded by several * Corresponding author. Tel.: þ372 6204809; fax: þ372 6204801. E-mail address: [email protected] (M. Ivask). 1164-5563/$ e see front matter Ó 2012 Elsevier Masson SAS. All rights reserved. http://dx.doi.org/10.1016/j.ejsobi.2012.08.001
authors [8e13]. Few studies are available on the earthworm communities of flooded areas on the eastern coast of the Baltic Sea and its river floodplains. Eitminaviciute et al. [14] collected 60e180 individuals m2, belonging to nine species (the dominant species being Aporrectodea caliginosa, Lumbricus rubellus and Dendrodrilus rubidus in the soil of drier coastal meadows); only one species (Eiseniella tetraedra, 57e336 individuals m2) was found in soil with a very high moisture content. Earlier studies of earthworms on the coastal and floodplain grasslands around Matsalu Bay and in the delta of the Kasari River [15] concluded that the communities are low in both numbers and species due to periodic anaerobic conditions and the negative impact of sea water in coastal meadows. The aims of the study were to evaluate which earthworm species are able to live under the extreme environmental conditions of the soil in the coastal grasslands of the Baltic Sea or under flooding conditions; and to determine how flooding by saline or fresh water influences the composition and diversity of communities. 2. Materials and methods 2.1. Site description Matsalu Bay is shallow, brackish and rich in nutrients; it is 18 km long (west to east) and 6 km wide (north to south). The average depth of the bay is 1.5 m, with a maximum depth of 3.5 m. The mean water salinity is approx. 7&. The shoreline length of the bay is
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M. Ivask et al. / European Journal of Soil Biology 53 (2012) 11e15
165 km, lacking high banks, with mostly shingle shores and muddy flats with extensive reed stands in the innermost sheltered part. Fluctuations of water at a level above 2 m are mostly due to winds, as there are no significant tidal variations. The Kasari River is the largest of several rivers that enter the bay, and the alluvial meadow of its delta is one of the largest (4000 ha) open wet meadows in Europe, 2500 ha of which is mown once per year. Annual inflow into Matsalu Bay exceeds the volume of the bay itself by approx. eight times, and the average seasonal variation of the water level in the Kasari River exceeds 1.7 m. Rivers carry large quantities of nutrient-rich sediments into the bay from its 3500 km2 drainage basin. These sediments (about 6300 tonnes per annum) [16] are deposited in river estuaries, allowing reed beds to expand. The bedrock is formed of Silurian and Ordovician limestone and the relief is mostly flat. Loamy till and fluviolacustrine (laminated clay) plains dominate. The climate is characterized by mean temperatures of 5 C in February and 16.5 C in July. The average annual precipitation is 700 mm and the number of days with snow cover ranges from 100 to 105. Spring floods last one to two months; the floodplain meadow is often also flooded in summer and autumn during heavy rains and westerly storms [17,18]. As a result of longterm observations, the highest water level (1.74 m) in the Kasari River was observed in spring (April); the highest water levels in the delta (1.91 m) and Matsalu Bay (1.57 m) were observed in October during strong westerly winds [16]. 2.2. Sampling design Earthworm communities were evaluated in August and September 2008 and 2010 in five areas located on the southern shore of Matsalu Bay and on the banks of the Kasari River under variable flooding conditions (either brackish or fresh water) (Fig. 1). In August and September 2009 the sampling of earthworms was not possible because of high water level on shore and in the delta. The locations of the sample areas were arranged on the basis of a gradient distance from the sea which indicates the influence of salt water during floods (Table 1). Areas 1 and 2 were flooded coastal meadows close to the sea, area 3 was coastal meadows more affected by fresh water from the river, area 4 was meadows of the delta frequently flooded with fresh water from the river but affected by rising seawater in the event of strong westerly winds and area 5 was floodplains unlikely to be subject to any seawater influence. In each area, a transect with three study points in different zones was determined (1 e subsaline, 2 e saline and 3 e suprasaline zones in the coastal area or at three different altitudes on the river banks numerated as 1, 2 and 3 from nearest to farthest).
At the same date in each zone, the following soil characteristics were measured: conductivity, salinity and pH (5 study points per zone, Multi 340i WTW, Germany), organic matter content (composite sample, muffle furnace at 360 ) and volumetric water content (10 study points per zone, Fieldscout TDR300, Spectrum Technologies Inc.). Earthworms were collected in three 50 50 cm areas using a 15% mustard powder solution [19,20] as a handsorting method was too complicated because of the high groundwater table (0e30 cm) and inappropriate soil texture. The earthworms were identified and the composition of the community was calculated by ecological group (epigeic, endogeic and anecic by Ref. [21] and the common habitat of species by Ref. [22]) (semiaquatic e E. tetraedra and Octolasion lacteum, terrestrial e all other species) as well as Simpson’s diversity index (1-D) to characterize species diversity in a community. 2.3. Statistical analysis Data analysis was performed using Microsoft Excel (mean values and standard deviation) and STATISTICA 8.0 (nonparametric methods: Spearman’s correlation, KruskalleWallis one-way analysis of variance and the ManneWhitney U-test). Canonical Correspondence Analysis (CCA) was used to analyze the data on earthworm communities with regard to environmental variables using the CANOCO 4.52 programme [23]; the forward selection method with the Monte Carlo test (999 permutations) available in the CANOCO software was used. 3. Results Soil conductivity was higher in the soils flooded by sea water (mean value 1.96 1.8 mS cm2) and lower in the soil of the delta and floodplain of the Kasari River (mean value 0.52 0.12 mS cm2); the difference between the mean conductivity in areas 1e5 was not statistically significant. The conductivity was positively correlated (P < 0.05) with the salinity of soil, moisture and organic matter content. Negative correlations (P < 0.05) were found between soil conductivity, number of earthworm species and total abundance of community. The decrease in abundance was the highest for the endogeic species A. caliginosa and Aporrectodea rosea. Most of the soil parameters (conductivity, salinity, moisture and organic matter content) had the highest values in the zone closest to the shoreline or river bank and values decreased with distance from the body of water (Table 1). Earthworm community density had a negative correlation (P < 0.05) with conductivity and salinity
Fig. 1. Map of Matsalu Bay and Kasari River. Sample areas are marked with numbers 1e5.
M. Ivask et al. / European Journal of Soil Biology 53 (2012) 11e15
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Table 1 General and soil characteristics of sites along Matsalu Bay and the Kasari River. Sample area code
Location (lat., long.)
Altitude (m)
Water salinity (&)
Soil pH
Soil electrical conductivity, (mS cm1)
1e1 1e2 1e3 2e1 2e2 2e3 3e1 3e2 3e3 4e1 4e2 4e3 5e1 5e2 5e3
58 58 58 58 58 58 58 58 58 58 58 58 58 58 58
0 0 1 0 0 1.5 0 0.5 1.5 1 1 1 2.5 4 4.5
5e6 5e6 5e6 4e6 4e6 4e6 3e4 3e4 3e4 0 0 0 0 0 0
7.23 0.13 6.94 0,06 7.1 0.12 6.96 0.09 6.73 0.04 7.03 0.05 7.36 0.14 7.1 0.13 7 0.06 6.61 0.02 6.61 0.04 6.54 0.02 7.33 0.07 7.18 0.02 6.91 0.02
3.170 1.559 0.086 4.960 1.331 0.644 1.176 0.605 0.252 0.707 0.618 0.468 0.439 0.478 0.413
430 3900 , 430 3900 , 430 3800 , 440 0500 , 440 0200 , 440 0500 , 440 3800 , 440 3700 , 440 3100 , 450 1900 , 450 2100 , 450 2300 , 440 0600 , 440 0400 , 440 0100 ,
23 23 23 23 23 23 23 23 23 23 23 23 23 23 23
340 4900 340 4900 340 4800 390 3300 390 5900 400 1100 400 1000 400 1300 400 0300 500 4300 500 4200 500 3500 590 1500 590 0900 590 0500
of soil, and a positive correlation with the number of species. The number of species had a negative correlation with conductivity, salinity and organic matter content in the soil, and a positive correlation with the number of individuals and earthworm diversity (P < 0.05). The diversity of the earthworm community (Simpson’s diversity index 1-D) had a positive correlation (P < 0.05) with the number of species (Table 2). Community parameters (number of individuals, number of species and diversity) were lowest in the zone closest to the shoreline or river bank and increased with distance from the body of water, except for sample area 4 in the delta. The endogeic species A. caliginosa, A. rosea and O. lacteum were negatively (P < 0.05) affected by soil conductivity and salinity. Soil moisture content was negatively correlated with the number of A. caliginosa, A. rosea and L. rubellus and positively (P < 0.05) correlated with E. tetraedra abundance (Table 3). Soil factors had an impact on earthworms (Fig. 2). The first CCA axis on Fig. 2 seems to represent variances in zone soil conditions. The second CCA axis appears to represent the sequence of sample areas starting from the east (sample area 5, floodplain). Zone number (distance from the sealine) was inversely related to soil moisture, conductivity and salinity, and positively to soil pH. Moisture content, conductivity and salinity influenced the number of E. tetraedra and Dendrobaena octaedra, and the difference between sample areas was greater in those flooded by fresh water
Table 2 Selected characteristics of earthworm communities on sites along Matsalu Bay and the Kasari River. Dominance of ecological groups in community Area N Mean number of Species Diversity Epigeic Endogeic Anecic Semicode individuals SE number index aquatic 1e1 6 20 1e2 6 32 1e3 6 92 2e1 6 4 2e2 6 12 2e3 6 34 3e1 9 36 3e2 9 38 3e3 9 39 4e1 12 108 4e2 12 84 4e3 12 32 5e1 9 52 5e2 9 121 5e3 9 124
4 9 6 1 2 6 4 6 8 14 6 4 4 8 7
3 5 5 1 1 3 4 3 6 3 5 3 5 6 6
0.589 0.849 0.608 0 0 0.653 0.74 0.713 0.646 0.598 0.747 0.669 0.794 0.752 0.732
0.8 0.94 0.15 1 0 0.33 0.5 1 0.46 1 0.63 0.56 0.29 0.37 0.26
0.2 0.06 0.83 0 1 0.67 0.5 0 0.54 0 0.37 0.44 0.71 0.63 0.74
0 0 0.2 0 0 0 0 0 0 0 0 0 0 0 0
0.8 0.75 0.13 0 1 0.2 0.31 0 0.23 0.29 0.63 0.75 0.19 0.36 0.42
0.101 0.229 0.054 0.519 0.195 0.109 0.186 0.113 0.079 0.07 0.043 0.018 0.013 0.076 0.025
Soil salinity (mS cm1) 1.53 0.67 0 2.56 0.52 0.07 0.40 0.08 0 0.08 0.03 0 0 0 0
0.06 0.21
0.54 0.15 0.13 0.11 0.05
0.03 0.02
Soil volumetric moisture content
Soil organic matter (%)
115.7 4.7 102.2 8.5 42.6 2.9 109.9 2.1 84.2 4.2 63.3 7.5 97.9 8.2 68.2 9.3 73.4 5.7 84.6 3.6 92.1 4.3 107.6 1.8 66.6 10.1 64.1 7.4 49 7.6
17.2 12.4 6.9 28.9 18.6 14.2 16.7 8.01 4.76 14.8 28.2 26 12.4 14.8 13.1
(areas 4 and 5). The impact of environmental factors on single species abundance was stronger than the impact on total community parameters (number of individuals, number of species and diversity). 4. Discussion Flooding conditions differ between sample areas. On the coast of the bay (sample areas 1 and 2) floods are shorter with potential temporary dry-off periods in between. This creates variable unstable soil conditions for earthworms. Flooding in the delta and on the floodplain lasts longer (normally >1 month) and is more stable. As mentioned by Keplin and Broll [10], the soil moisture regime seems to be the key factor that regulates most soil processes and controls the earthworm population in wet grasslands. The strong influence of flooding on population density and biomass of earthworms was also demonstrated by Simonsen and Klok [11]. Earthworms are able to survive under flooded conditions, but survival rates vary between species [24]. Plum [25] describes the following five mechanisms for flooding survival strategies: horizontal migration; vertical migration; physiological adaptation; phenology; and reproduction. Lumbricidae were considered to employ all five strategies [25]. Endogeic species burrow through and feed on mineral soils, while epigeic species are active surface crawlers, feeding on organic litter [26,27]. With flooding, endogeic species can survive in the soil, but in years with excessive flooding (two months or more) they fail to survive. Anecic species are seldom present in flooded soils because of sandy coastal soil [28] or the high groundwater table, which limits vertical burrowing [25]. The salinity of flood water has an additional negative effect on earthworms. Piearce and Piearce [3] studied the earthworm populations in northewest England that had recently been inundated by the sea and showed a decline in the density, biomass and species spectrum in proportion to the severity of inundation; all six species tested under experimental conditions avoided 14& salinity, whereas sea water with 29& salinity was lethal to the earthworms. The salinity of water in the Baltic Sea is relatively low, with a maximum concentration of salt ions of 6e8& in Matsalu Bay. The salinity in the water comprises chloride ions in the bay and mostly hydrocarbonate ions in the delta [17]. Low salinity did not cause total avoidance by earthworms in the flooded soils, but it decreased the abundance and diversity of communities. So far, 13 earthworm species are known in Estonia, all peregrine cosmopolitan [22]. In the flooded areas studied in Matsalu, 10 earthworm species were found. The number of earthworms ranged from 4 to 92 individuals m2 on the shore and 32 to 124 individuals
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M. Ivask et al. / European Journal of Soil Biology 53 (2012) 11e15
Table 3 The mean abundance (SE) of earthworm species in communities. Area code
N
ACAL
AROS
ACHL
ALON
LRUB
LCAS
DOCT
DRUB
OLAC
ETET
1-1 1e2 1e3 2e1 2e2 2e3 3e1 3e2 3e3 4e1 4e2 4e3 5e1 5e2 5e3
6 6 6 6 6 6 9 9 9 12 12 12 9 9 9
0 0 54 8 0 0 14 5 0 0 64 0 42 0 81 41 82
0 0 12 4 0 0 0 73 0 15 4 0 0 0 14 1 16 3 28 3
0 0 0 0 0 0 0 0 0 0 0 0 0 12 2 41
0 0 21 0 0 0 0 0 0 0 0 0 0 0 0
0 41 14 2 41 0 10 3 13 5 12 4 15 6 24 6 82 0 62 36 4 81
0 21 0 0 0 0 0 0 21 0 16 6 0 0 94 24 3
41 21 0 0 0 0 52 20 6 11 60 12 0 81 61 0 0
0 0 0 0 0 0 0 41 0 0 0 0 0 0 0
42 22 12 3 0 12 2 63 11 3 0 93 0 28 6 14 4 86 44 12 52 4
12 22 0 0 0 0 0 0 0 24 20 10 0 0 0
4 5
12 3 2
Abbreviations: N e number of samples; ACAL e Aporrectodea caliginosa; AROS e Aporrectodea rosea; ACHL e Allolobophora chlorotica; ALON e Aporrectodea longa; LRUB e Lumbricus rubellus; LCAS e Lumbricus castaneus; DOCT e Dendrobaena octaedra; DRUB e Dendrodrilus rubidus; OLAC e Octolasion lacteum; ETET e Eiseniella tetraedra.
1.0
m2 in the delta and on the river bank. Epigeic species were more tolerant to the limiting effect of flooding and salinity. Endogeic species were more sensitive to submersion and the unfavorable texture of the coastal soil. Only the semi-aquatic species O. lacteum
2-1
Sample area
4-3
OM
5-3 5-2 ACHL LCAS
Axis 2
AROS
Zone
Moisture
4-2
Conductivity
OLAC
1-1
EPI TERR SEMIAQ Species Number ENDO Diversity 3-3 LRUB 5-1
Salinity ETET
3-1
pH
2-2 2-3
DOCT DRUB
4-1
3-2 1-2
ACAL
-1.0
1-3
ALON AN
-0.8 SPECIES
Axis 1 ENV. VARIABLES
1.0
SAMPLES
Fig. 2. Ordination triplots with environmental variables based on Canonical Correspondence Analyses (CCA) of species, displaying 33% of variance on axis 1 and 17% on axis 2. Abbreviations for environmental variables: pH e acidity of soil (KCl), OM e organic matter (%), moisture e volumetric water content of soil and zone e zone by salinity or by distance from river. Abbreviations for earthworm community: epi e dominance of epigeic individuals in community, endo e dominance of endogeic earthworms in community, an e dominance of anecic earthworms in community, TERR e dominance of terrestrial individuals in community, SEMI e dominance of semiaquatic earthworms in community, number e number of earthworm individuals per m2, species e number of earthworm species in sample area, samples e codes of sample areas. Eigenvalues of first two axes: 0.257 and 0.130; sum of all canonical eigenvalues: 0.524. The abbreviations of species names see Table 3.
was able to inhabit the coastline subsaline area flooded by seawater and also dominated in the soil of the delta and floodplain. Flooded areas appear to be unacceptable habitats for anecic species because of the high groundwater table; only a few individuals of Aporrectodea longa were found in sample area 1 in the zone farthest from the shoreline. There are inconsistent data on the presence [8,29] or non-presence [10] of anecic species in inundated soil, it seems that some are able to inhabit shortly flooded soils. L. rubellus was dominant in the subsaline zone of the coast and abundant in areas flooded by fresh water (areas 4 and 5). Different conclusions have been published about the tolerance of L. rubellus in floodplains. According to Ausden et al. [30] and Zorn et al. [8] this species is abundant in flooded grasslands belonging to the dominant species in floodplains with changing moisture content and flooding regimes. Keplin and Broll [10] have mentioned large fluctuations in the abundance of this species during periodical flooding and drying on floodplains. Epigeic D. octaedra, E. tetraedra, D. rubidus and Lumbricus castaneus were present in subsaline and saline coastal zones, wherein the numbers of E. tetraedra and L. castaneus were greater in the high moisture soils of the delta and floodplain (areas 4 and 5). Small numbers of A. caliginosa and A. rosea were present in the suprasaline zone in areas where the soil horizon was better developed. A. caliginosa did not tolerate soil with high soil moisture and lack of aeration; this result coincides with published data [10,30]. We have previously published that A. caliginosa was the most abundant species in flooded areas in Matsalu: this study was performed after years with very short or no flooding [15] and the flooding conditions were different from the conditions of this study. A. rosea was numerous in floodplain soil, where the flooding was shorter. Keplin and Broll [10] and Bullinger-Weber et al. [12] have concluded that this species is dependent on humus or organic carbon content in soil habitat. Three peregrine species present in Estonia (Lumbricus terrestris, Octolasion cyaneum and Eisenia fetida) were not found in flooded soils, while two species (Allolobophora chlorotica and D. rubidus) were not found in soils affected by sea water. According to Ref. [8], total A. chlorotica numbers showed no response to flooding; this species is clearly moisture tolerant but not tolerant to salinity. In conclusion, the brackish conditions of the Baltic Sea create special habitats for earthworms, and the duration and character of flooding affect earthworm species and communities. Sea water salinity and periodical flooding have a strong negative impact on earthworm communities. The duration of flooding seems to be the strongest factor with a negative impact on the abundance of earthworm communities; this depends greatly on species’ tolerance to high moisture content and low soil aeration. In spite of this,
M. Ivask et al. / European Journal of Soil Biology 53 (2012) 11e15
most of Estonia’s earthworm species inhabited the flooded areas on the coast of the Baltic Sea and the delta and floodplains of Kasari River. Acknowledgments The authors would like to thank the Estonian Science Foundation for its support (grants no. 6739 and 9145). We are very grateful to Mrs. Nele Nutt for helping with the map of sample areas and to Mrs. Karin Muoni for editing the text.
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European Journal of Soil Biology journal homepage: http://www.elsevier.com/locate/ejsobi
Original article
Effect of flooding by fresh and brackish water on earthworm communities along Matsalu Bay and the Kasari River Mari Ivask*, Mart Meriste, Annely Kuu, Sander Kutti, Eduard Sizov Tartu College of Tallinn University of Technology, Puiestee 78, 51008 Tartu, Estonia
a r t i c l e i n f o
a b s t r a c t
Article history: Received 20 March 2012 Received in revised form 2 August 2012 Accepted 10 August 2012 Available online 27 August 2012 Handling editor: Stefan Schrader
The continuum of Matsalu Bay and the Kasari River located on the east coast of the Baltic Sea represents a complex mosaic of marine, coastal and inland wetlands (shallow sea waters, estuarine waters, coastal lagoons, an inland delta and flooded meadows). Earthworm communities were studied at five sites on the southern shore of Matsalu Bay and the banks of the Kasari River under different salt water regimes (brackish or fresh water). Sample sites were located along a flooding gradient (distance from the sea). Flooding duration appears to have the strongest negative impact on the abundance of earthworm communities, which largely depends on species’ tolerance of high moisture content and low soil aeration. The brackish conditions of the Baltic Sea create special habitat conditions; the sea water salinity and periodic flooding have a significant negative impact on earthworm communities. Ó 2012 Elsevier Masson SAS. All rights reserved.
Keywords: Earthworms Diversity Flooded grasslands Brackish conditions
1. Introduction The continuum of Matsalu Bay and the Kasari River in the eastern Baltic Sea represents a complex mosaic of marine, coastal and inland wetlands (shallow sea waters, estuarine waters, coastal lagoons, an inland delta and flooded meadows) characteristic of the boreal biogeographical region. The brackish conditions of the Baltic Sea create special habitats in the coastal grassland soils surrounding Matsalu Bay. Equally, the floodplains of the Kasari River are periodically flooded by fresh water. In the eastern part of Matsalu Bay and in the delta of the river, brackish and fresh water can be mixed due to strong winds from the west or due to exceptionally large amounts of fresh water flowing from the river in the spring [1,2]. Flooding significantly alters the habitat of earthworm communities because of high moisture and poor aeration. It has long been known that in coastal areas earthworms are vulnerable to saline substrates, expelled from the soil by the salt solution and killed by immersion in sea water, and are therefore scarce or absent in saline soils [3,4]. The spatial distribution and abundance of earthworms are affected by sea water salinity, periodical flooding, habitat dry-off and unfavorable soil texture [5e7]. A reduction in the abundance and biomass of earthworm communities on European floodplains was concluded by several * Corresponding author. Tel.: þ372 6204809; fax: þ372 6204801. E-mail address: [email protected] (M. Ivask). 1164-5563/$ e see front matter Ó 2012 Elsevier Masson SAS. All rights reserved. http://dx.doi.org/10.1016/j.ejsobi.2012.08.001
authors [8e13]. Few studies are available on the earthworm communities of flooded areas on the eastern coast of the Baltic Sea and its river floodplains. Eitminaviciute et al. [14] collected 60e180 individuals m2, belonging to nine species (the dominant species being Aporrectodea caliginosa, Lumbricus rubellus and Dendrodrilus rubidus in the soil of drier coastal meadows); only one species (Eiseniella tetraedra, 57e336 individuals m2) was found in soil with a very high moisture content. Earlier studies of earthworms on the coastal and floodplain grasslands around Matsalu Bay and in the delta of the Kasari River [15] concluded that the communities are low in both numbers and species due to periodic anaerobic conditions and the negative impact of sea water in coastal meadows. The aims of the study were to evaluate which earthworm species are able to live under the extreme environmental conditions of the soil in the coastal grasslands of the Baltic Sea or under flooding conditions; and to determine how flooding by saline or fresh water influences the composition and diversity of communities. 2. Materials and methods 2.1. Site description Matsalu Bay is shallow, brackish and rich in nutrients; it is 18 km long (west to east) and 6 km wide (north to south). The average depth of the bay is 1.5 m, with a maximum depth of 3.5 m. The mean water salinity is approx. 7&. The shoreline length of the bay is
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M. Ivask et al. / European Journal of Soil Biology 53 (2012) 11e15
165 km, lacking high banks, with mostly shingle shores and muddy flats with extensive reed stands in the innermost sheltered part. Fluctuations of water at a level above 2 m are mostly due to winds, as there are no significant tidal variations. The Kasari River is the largest of several rivers that enter the bay, and the alluvial meadow of its delta is one of the largest (4000 ha) open wet meadows in Europe, 2500 ha of which is mown once per year. Annual inflow into Matsalu Bay exceeds the volume of the bay itself by approx. eight times, and the average seasonal variation of the water level in the Kasari River exceeds 1.7 m. Rivers carry large quantities of nutrient-rich sediments into the bay from its 3500 km2 drainage basin. These sediments (about 6300 tonnes per annum) [16] are deposited in river estuaries, allowing reed beds to expand. The bedrock is formed of Silurian and Ordovician limestone and the relief is mostly flat. Loamy till and fluviolacustrine (laminated clay) plains dominate. The climate is characterized by mean temperatures of 5 C in February and 16.5 C in July. The average annual precipitation is 700 mm and the number of days with snow cover ranges from 100 to 105. Spring floods last one to two months; the floodplain meadow is often also flooded in summer and autumn during heavy rains and westerly storms [17,18]. As a result of longterm observations, the highest water level (1.74 m) in the Kasari River was observed in spring (April); the highest water levels in the delta (1.91 m) and Matsalu Bay (1.57 m) were observed in October during strong westerly winds [16]. 2.2. Sampling design Earthworm communities were evaluated in August and September 2008 and 2010 in five areas located on the southern shore of Matsalu Bay and on the banks of the Kasari River under variable flooding conditions (either brackish or fresh water) (Fig. 1). In August and September 2009 the sampling of earthworms was not possible because of high water level on shore and in the delta. The locations of the sample areas were arranged on the basis of a gradient distance from the sea which indicates the influence of salt water during floods (Table 1). Areas 1 and 2 were flooded coastal meadows close to the sea, area 3 was coastal meadows more affected by fresh water from the river, area 4 was meadows of the delta frequently flooded with fresh water from the river but affected by rising seawater in the event of strong westerly winds and area 5 was floodplains unlikely to be subject to any seawater influence. In each area, a transect with three study points in different zones was determined (1 e subsaline, 2 e saline and 3 e suprasaline zones in the coastal area or at three different altitudes on the river banks numerated as 1, 2 and 3 from nearest to farthest).
At the same date in each zone, the following soil characteristics were measured: conductivity, salinity and pH (5 study points per zone, Multi 340i WTW, Germany), organic matter content (composite sample, muffle furnace at 360 ) and volumetric water content (10 study points per zone, Fieldscout TDR300, Spectrum Technologies Inc.). Earthworms were collected in three 50 50 cm areas using a 15% mustard powder solution [19,20] as a handsorting method was too complicated because of the high groundwater table (0e30 cm) and inappropriate soil texture. The earthworms were identified and the composition of the community was calculated by ecological group (epigeic, endogeic and anecic by Ref. [21] and the common habitat of species by Ref. [22]) (semiaquatic e E. tetraedra and Octolasion lacteum, terrestrial e all other species) as well as Simpson’s diversity index (1-D) to characterize species diversity in a community. 2.3. Statistical analysis Data analysis was performed using Microsoft Excel (mean values and standard deviation) and STATISTICA 8.0 (nonparametric methods: Spearman’s correlation, KruskalleWallis one-way analysis of variance and the ManneWhitney U-test). Canonical Correspondence Analysis (CCA) was used to analyze the data on earthworm communities with regard to environmental variables using the CANOCO 4.52 programme [23]; the forward selection method with the Monte Carlo test (999 permutations) available in the CANOCO software was used. 3. Results Soil conductivity was higher in the soils flooded by sea water (mean value 1.96 1.8 mS cm2) and lower in the soil of the delta and floodplain of the Kasari River (mean value 0.52 0.12 mS cm2); the difference between the mean conductivity in areas 1e5 was not statistically significant. The conductivity was positively correlated (P < 0.05) with the salinity of soil, moisture and organic matter content. Negative correlations (P < 0.05) were found between soil conductivity, number of earthworm species and total abundance of community. The decrease in abundance was the highest for the endogeic species A. caliginosa and Aporrectodea rosea. Most of the soil parameters (conductivity, salinity, moisture and organic matter content) had the highest values in the zone closest to the shoreline or river bank and values decreased with distance from the body of water (Table 1). Earthworm community density had a negative correlation (P < 0.05) with conductivity and salinity
Fig. 1. Map of Matsalu Bay and Kasari River. Sample areas are marked with numbers 1e5.
M. Ivask et al. / European Journal of Soil Biology 53 (2012) 11e15
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Table 1 General and soil characteristics of sites along Matsalu Bay and the Kasari River. Sample area code
Location (lat., long.)
Altitude (m)
Water salinity (&)
Soil pH
Soil electrical conductivity, (mS cm1)
1e1 1e2 1e3 2e1 2e2 2e3 3e1 3e2 3e3 4e1 4e2 4e3 5e1 5e2 5e3
58 58 58 58 58 58 58 58 58 58 58 58 58 58 58
0 0 1 0 0 1.5 0 0.5 1.5 1 1 1 2.5 4 4.5
5e6 5e6 5e6 4e6 4e6 4e6 3e4 3e4 3e4 0 0 0 0 0 0
7.23 0.13 6.94 0,06 7.1 0.12 6.96 0.09 6.73 0.04 7.03 0.05 7.36 0.14 7.1 0.13 7 0.06 6.61 0.02 6.61 0.04 6.54 0.02 7.33 0.07 7.18 0.02 6.91 0.02
3.170 1.559 0.086 4.960 1.331 0.644 1.176 0.605 0.252 0.707 0.618 0.468 0.439 0.478 0.413
430 3900 , 430 3900 , 430 3800 , 440 0500 , 440 0200 , 440 0500 , 440 3800 , 440 3700 , 440 3100 , 450 1900 , 450 2100 , 450 2300 , 440 0600 , 440 0400 , 440 0100 ,
23 23 23 23 23 23 23 23 23 23 23 23 23 23 23
340 4900 340 4900 340 4800 390 3300 390 5900 400 1100 400 1000 400 1300 400 0300 500 4300 500 4200 500 3500 590 1500 590 0900 590 0500
of soil, and a positive correlation with the number of species. The number of species had a negative correlation with conductivity, salinity and organic matter content in the soil, and a positive correlation with the number of individuals and earthworm diversity (P < 0.05). The diversity of the earthworm community (Simpson’s diversity index 1-D) had a positive correlation (P < 0.05) with the number of species (Table 2). Community parameters (number of individuals, number of species and diversity) were lowest in the zone closest to the shoreline or river bank and increased with distance from the body of water, except for sample area 4 in the delta. The endogeic species A. caliginosa, A. rosea and O. lacteum were negatively (P < 0.05) affected by soil conductivity and salinity. Soil moisture content was negatively correlated with the number of A. caliginosa, A. rosea and L. rubellus and positively (P < 0.05) correlated with E. tetraedra abundance (Table 3). Soil factors had an impact on earthworms (Fig. 2). The first CCA axis on Fig. 2 seems to represent variances in zone soil conditions. The second CCA axis appears to represent the sequence of sample areas starting from the east (sample area 5, floodplain). Zone number (distance from the sealine) was inversely related to soil moisture, conductivity and salinity, and positively to soil pH. Moisture content, conductivity and salinity influenced the number of E. tetraedra and Dendrobaena octaedra, and the difference between sample areas was greater in those flooded by fresh water
Table 2 Selected characteristics of earthworm communities on sites along Matsalu Bay and the Kasari River. Dominance of ecological groups in community Area N Mean number of Species Diversity Epigeic Endogeic Anecic Semicode individuals SE number index aquatic 1e1 6 20 1e2 6 32 1e3 6 92 2e1 6 4 2e2 6 12 2e3 6 34 3e1 9 36 3e2 9 38 3e3 9 39 4e1 12 108 4e2 12 84 4e3 12 32 5e1 9 52 5e2 9 121 5e3 9 124
4 9 6 1 2 6 4 6 8 14 6 4 4 8 7
3 5 5 1 1 3 4 3 6 3 5 3 5 6 6
0.589 0.849 0.608 0 0 0.653 0.74 0.713 0.646 0.598 0.747 0.669 0.794 0.752 0.732
0.8 0.94 0.15 1 0 0.33 0.5 1 0.46 1 0.63 0.56 0.29 0.37 0.26
0.2 0.06 0.83 0 1 0.67 0.5 0 0.54 0 0.37 0.44 0.71 0.63 0.74
0 0 0.2 0 0 0 0 0 0 0 0 0 0 0 0
0.8 0.75 0.13 0 1 0.2 0.31 0 0.23 0.29 0.63 0.75 0.19 0.36 0.42
0.101 0.229 0.054 0.519 0.195 0.109 0.186 0.113 0.079 0.07 0.043 0.018 0.013 0.076 0.025
Soil salinity (mS cm1) 1.53 0.67 0 2.56 0.52 0.07 0.40 0.08 0 0.08 0.03 0 0 0 0
0.06 0.21
0.54 0.15 0.13 0.11 0.05
0.03 0.02
Soil volumetric moisture content
Soil organic matter (%)
115.7 4.7 102.2 8.5 42.6 2.9 109.9 2.1 84.2 4.2 63.3 7.5 97.9 8.2 68.2 9.3 73.4 5.7 84.6 3.6 92.1 4.3 107.6 1.8 66.6 10.1 64.1 7.4 49 7.6
17.2 12.4 6.9 28.9 18.6 14.2 16.7 8.01 4.76 14.8 28.2 26 12.4 14.8 13.1
(areas 4 and 5). The impact of environmental factors on single species abundance was stronger than the impact on total community parameters (number of individuals, number of species and diversity). 4. Discussion Flooding conditions differ between sample areas. On the coast of the bay (sample areas 1 and 2) floods are shorter with potential temporary dry-off periods in between. This creates variable unstable soil conditions for earthworms. Flooding in the delta and on the floodplain lasts longer (normally >1 month) and is more stable. As mentioned by Keplin and Broll [10], the soil moisture regime seems to be the key factor that regulates most soil processes and controls the earthworm population in wet grasslands. The strong influence of flooding on population density and biomass of earthworms was also demonstrated by Simonsen and Klok [11]. Earthworms are able to survive under flooded conditions, but survival rates vary between species [24]. Plum [25] describes the following five mechanisms for flooding survival strategies: horizontal migration; vertical migration; physiological adaptation; phenology; and reproduction. Lumbricidae were considered to employ all five strategies [25]. Endogeic species burrow through and feed on mineral soils, while epigeic species are active surface crawlers, feeding on organic litter [26,27]. With flooding, endogeic species can survive in the soil, but in years with excessive flooding (two months or more) they fail to survive. Anecic species are seldom present in flooded soils because of sandy coastal soil [28] or the high groundwater table, which limits vertical burrowing [25]. The salinity of flood water has an additional negative effect on earthworms. Piearce and Piearce [3] studied the earthworm populations in northewest England that had recently been inundated by the sea and showed a decline in the density, biomass and species spectrum in proportion to the severity of inundation; all six species tested under experimental conditions avoided 14& salinity, whereas sea water with 29& salinity was lethal to the earthworms. The salinity of water in the Baltic Sea is relatively low, with a maximum concentration of salt ions of 6e8& in Matsalu Bay. The salinity in the water comprises chloride ions in the bay and mostly hydrocarbonate ions in the delta [17]. Low salinity did not cause total avoidance by earthworms in the flooded soils, but it decreased the abundance and diversity of communities. So far, 13 earthworm species are known in Estonia, all peregrine cosmopolitan [22]. In the flooded areas studied in Matsalu, 10 earthworm species were found. The number of earthworms ranged from 4 to 92 individuals m2 on the shore and 32 to 124 individuals
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M. Ivask et al. / European Journal of Soil Biology 53 (2012) 11e15
Table 3 The mean abundance (SE) of earthworm species in communities. Area code
N
ACAL
AROS
ACHL
ALON
LRUB
LCAS
DOCT
DRUB
OLAC
ETET
1-1 1e2 1e3 2e1 2e2 2e3 3e1 3e2 3e3 4e1 4e2 4e3 5e1 5e2 5e3
6 6 6 6 6 6 9 9 9 12 12 12 9 9 9
0 0 54 8 0 0 14 5 0 0 64 0 42 0 81 41 82
0 0 12 4 0 0 0 73 0 15 4 0 0 0 14 1 16 3 28 3
0 0 0 0 0 0 0 0 0 0 0 0 0 12 2 41
0 0 21 0 0 0 0 0 0 0 0 0 0 0 0
0 41 14 2 41 0 10 3 13 5 12 4 15 6 24 6 82 0 62 36 4 81
0 21 0 0 0 0 0 0 21 0 16 6 0 0 94 24 3
41 21 0 0 0 0 52 20 6 11 60 12 0 81 61 0 0
0 0 0 0 0 0 0 41 0 0 0 0 0 0 0
42 22 12 3 0 12 2 63 11 3 0 93 0 28 6 14 4 86 44 12 52 4
12 22 0 0 0 0 0 0 0 24 20 10 0 0 0
4 5
12 3 2
Abbreviations: N e number of samples; ACAL e Aporrectodea caliginosa; AROS e Aporrectodea rosea; ACHL e Allolobophora chlorotica; ALON e Aporrectodea longa; LRUB e Lumbricus rubellus; LCAS e Lumbricus castaneus; DOCT e Dendrobaena octaedra; DRUB e Dendrodrilus rubidus; OLAC e Octolasion lacteum; ETET e Eiseniella tetraedra.
1.0
m2 in the delta and on the river bank. Epigeic species were more tolerant to the limiting effect of flooding and salinity. Endogeic species were more sensitive to submersion and the unfavorable texture of the coastal soil. Only the semi-aquatic species O. lacteum
2-1
Sample area
4-3
OM
5-3 5-2 ACHL LCAS
Axis 2
AROS
Zone
Moisture
4-2
Conductivity
OLAC
1-1
EPI TERR SEMIAQ Species Number ENDO Diversity 3-3 LRUB 5-1
Salinity ETET
3-1
pH
2-2 2-3
DOCT DRUB
4-1
3-2 1-2
ACAL
-1.0
1-3
ALON AN
-0.8 SPECIES
Axis 1 ENV. VARIABLES
1.0
SAMPLES
Fig. 2. Ordination triplots with environmental variables based on Canonical Correspondence Analyses (CCA) of species, displaying 33% of variance on axis 1 and 17% on axis 2. Abbreviations for environmental variables: pH e acidity of soil (KCl), OM e organic matter (%), moisture e volumetric water content of soil and zone e zone by salinity or by distance from river. Abbreviations for earthworm community: epi e dominance of epigeic individuals in community, endo e dominance of endogeic earthworms in community, an e dominance of anecic earthworms in community, TERR e dominance of terrestrial individuals in community, SEMI e dominance of semiaquatic earthworms in community, number e number of earthworm individuals per m2, species e number of earthworm species in sample area, samples e codes of sample areas. Eigenvalues of first two axes: 0.257 and 0.130; sum of all canonical eigenvalues: 0.524. The abbreviations of species names see Table 3.
was able to inhabit the coastline subsaline area flooded by seawater and also dominated in the soil of the delta and floodplain. Flooded areas appear to be unacceptable habitats for anecic species because of the high groundwater table; only a few individuals of Aporrectodea longa were found in sample area 1 in the zone farthest from the shoreline. There are inconsistent data on the presence [8,29] or non-presence [10] of anecic species in inundated soil, it seems that some are able to inhabit shortly flooded soils. L. rubellus was dominant in the subsaline zone of the coast and abundant in areas flooded by fresh water (areas 4 and 5). Different conclusions have been published about the tolerance of L. rubellus in floodplains. According to Ausden et al. [30] and Zorn et al. [8] this species is abundant in flooded grasslands belonging to the dominant species in floodplains with changing moisture content and flooding regimes. Keplin and Broll [10] have mentioned large fluctuations in the abundance of this species during periodical flooding and drying on floodplains. Epigeic D. octaedra, E. tetraedra, D. rubidus and Lumbricus castaneus were present in subsaline and saline coastal zones, wherein the numbers of E. tetraedra and L. castaneus were greater in the high moisture soils of the delta and floodplain (areas 4 and 5). Small numbers of A. caliginosa and A. rosea were present in the suprasaline zone in areas where the soil horizon was better developed. A. caliginosa did not tolerate soil with high soil moisture and lack of aeration; this result coincides with published data [10,30]. We have previously published that A. caliginosa was the most abundant species in flooded areas in Matsalu: this study was performed after years with very short or no flooding [15] and the flooding conditions were different from the conditions of this study. A. rosea was numerous in floodplain soil, where the flooding was shorter. Keplin and Broll [10] and Bullinger-Weber et al. [12] have concluded that this species is dependent on humus or organic carbon content in soil habitat. Three peregrine species present in Estonia (Lumbricus terrestris, Octolasion cyaneum and Eisenia fetida) were not found in flooded soils, while two species (Allolobophora chlorotica and D. rubidus) were not found in soils affected by sea water. According to Ref. [8], total A. chlorotica numbers showed no response to flooding; this species is clearly moisture tolerant but not tolerant to salinity. In conclusion, the brackish conditions of the Baltic Sea create special habitats for earthworms, and the duration and character of flooding affect earthworm species and communities. Sea water salinity and periodical flooding have a strong negative impact on earthworm communities. The duration of flooding seems to be the strongest factor with a negative impact on the abundance of earthworm communities; this depends greatly on species’ tolerance to high moisture content and low soil aeration. In spite of this,
M. Ivask et al. / European Journal of Soil Biology 53 (2012) 11e15
most of Estonia’s earthworm species inhabited the flooded areas on the coast of the Baltic Sea and the delta and floodplains of Kasari River. Acknowledgments The authors would like to thank the Estonian Science Foundation for its support (grants no. 6739 and 9145). We are very grateful to Mrs. Nele Nutt for helping with the map of sample areas and to Mrs. Karin Muoni for editing the text.
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