Applying landscape ecology to conservation biology: Spatially explicit analysis reveals dispersal limits on threatened wetland gastropods

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available at www.sciencedirect.com

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Applying landscape ecology to conservation biology: Spatially explicit analysis reveals dispersal limits on threatened wetland gastropods Karla Niggebruggea,b, Isabelle Durancea, Alisa M. Watsona, Rob S.E.W. Leuvenb, S.J. Ormeroda,* a

Catchment Research Group, School of Biosciences, Cardiff University, Cardiff CF10 3US, United Kingdom Department of Environmental Science, Institute for Wetland and Water Research, Radboud University, Nijmegen, P.O. Box 9010, 6500 GL Nijmegen, The Netherlands

b

A R T I C L E I N F O

A B S T R A C T

Article history:

Three gastropods in the UK red data book (RDB) occupy drainage ditches on threatened graz-

Received 21 September 2006

ing marshes. Segmentina nitida, Anisus vorticulus and Valvata macrostoma are affected by hab-

Received in revised form

itat loss, ditch management and eutrophication, but dispersal and fragmentation effects

27 June 2007

have also been postulated. We used landscape ecological approaches to examine such effects

Accepted 11 July 2007

on these and 17 other gastropods on four English marshes, specifically combining ordination

Available online 5 September 2007

to identify suitable habitat with spatially-explicit analysis of occupancy. Among all gastropods, the occupancy of suitable habitat declined significantly as the distance to the nearest

Keywords:

occupied site increased. S. nitida and A. vorticulus were among the species most affected, with

Eutrophication

median nearest distances from occupied to unoccupied suitable sites significantly greater by

Fragmentation

3  4X than distances between occupied sites. V. macrostoma was not limited locally by dis-

GIS

persal, but was absent from three out of four marshes with suitable habitat. Eutrophication

Grazing marshes

(elevated N) had no effects on distances between occupied and unoccupied sites and did

Habitat suitability

not contribute to fragmentation. Although four non-threatened species were apparently also

Invertebrates

limited by dispersal, only two (Armiger crista; Gyraulus albus) showed some combination of the

Niche

dispersal effects, low occupancy of suitable habitat (<50%) and small niche extent that char-

Ordination

acterized RDB species. While dispersal alone cannot explain unfavourable conservation status in these wetland snails, our data support the hypothesis that limited dispersal between (all species) and within marshes (S. nitida and A. vorticulus) affect all three RDB snails in their remaining UK range. Action is required to better understand the population and genetic consequences; to better understand dispersal mechanisms; and to evaluate re-introduction and reinforcement as aids to recovery. The latter could double the existing site occupancy. Ó 2007 Elsevier Ltd. All rights reserved.

1.

Introduction

British grazing marshes are threatened lowland wetlands that typically comprise periodically inundated pastures inter-

spersed with fresh- or brackish-water ditches to regulate water levels (HMSO, 1995a). Many are of high conservation interest and have national or international status, for example under the EU Habitats Directive (92/43/EEC) or the Ramsar

* Corresponding author: Tel.: +44 029 20 875 871; fax: +44 029 20 874 305. E-mail addresses: [email protected] (K. Niggebrugge), [email protected] (I. Durance), [email protected] (A.M. Watson), [email protected] (R.S.E.W. Leuven), [email protected] (S.J. Ormerod). 0006-3207/$ - see front matter Ó 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.biocon.2007.07.003

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Convention (HMSO, 1995c; Ramsar Convention Bureau, 2006). The drainage ditches support a particularly high diversity of native macrophytes and invertebrates (RSBP et al., 1997; Watson and Ormerod, 2004a). Constructed centuries ago for land drainage to allow summer grazing, these ditches are remnants of formerly extensive wetlands that are now the sole habitats for some relict species (Sutherland and Hill, 1995). Over the last 70 years, the area of grazing marshes in the UK has declined substantially due to arable conversion, nutrient enrichment, increased flood control and adverse ditch management (Cook and Moorby, 1993; HMSO, 1995a; RSBP et al., 1997; Jefferson and Grice, 1998; Watson and Ormerod, 2004a). Only 3% of the current 300,000 ha is considered of good conservation quality (HMSO, 1995a). At least 70% of freshwater molluscs in the United Kingdom occur in marshland drainage systems (Kerney, 1999; Killeen et al., 2004). Among them are three species listed in UK’s Red Data Book (RDB) (Bratton, 1991): Segmentina nitida (Muller 1774), Anisus vorticulus (Troschel, 1834) and Valvata macrostoma (Mo¨rch, 1864). S. nitida has declined by about 80% of its range during the 20th century (Kerney, 1999). All three have unfavourable conservation status across Europe in general (Wells and Chatfield, 1992; HMSO, 1995b), and A. vorticulus was added recently to Annex II of the EU Habitats Directive (92/ 43/EEC). Although influences on their distribution are incompletely understood, on traditional British grazing marsh each has specific requirements for different stages of ditch hydroseral succession while requiring also relatively calcareous, clean water. Eutrophication and adverse ditch management, with over-frequent dredging and vegetation clearance, are potentially detrimental (Watson and Ormerod, 2004a,b). However, increasing fragmentation, lack of connectivity between ditches and dispersal problems have been suggested as addition limits on their population viability (Watson and Ormerod, 2004a). So far, this hypothesis has not been examined. Species dispersal is determined both by specific dispersal traits and landscape characteristics (Ozinga et al., 2005). Dispersal limitation can lead to differences in species composition between sites if poor dispersers are excluded from otherwise suitable locations (Matlack and Monde, 2004; Ozinga et al., 2005). In aquatic habitats, loss of connectivity can exacerbate such effects and increase the risks of local extinction (Willing and Killeen, 1999; Kallimanis et al., 2005). In these systems, loss of connectivity might reflect not only physical barriers, but also habitat degradation caused by inappropriate water quality, decline among dispersal vectors or altered flood frequency. Consequences for the threatened gastropods considered here have never been evaluated and their dispersal strategies are poorly known. While they might be expected to disperse passively over medium distances using animal vectors, water flow or attachment to mobile debris (Bilton et al., 2001), flooding might also mediate transport at least within floodplains. The number of ditches occupied by A. vorticulus is linked to prolonged flooding, but the effects have never been quantified (Willing and Killeen, 1999). Here, we use landscape ecological approaches to test the hypothesis that restricted dispersal might affect the distribution of both common and scarce freshwater gastropods in drainage ditches with special attention to S. nitida, A. vorticulus and V. macrostoma. As dispersal could not be measured

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directly, we used spatially explicit analysis to infer dispersal effects from the distribution of species relative to the distribution of suitable habitat. We postulated that evidence for limited dispersal would arise if species occupied a limited proportion of suitable sites, and if distances between occupied and suitable but unoccupied sites were relatively large. The steps involved (i) quantifying habitat suitability and niche extent for each gastropod species using ordination; (ii) quantifying habitat occupancy for each species relative to habitat suitability; (iii) using GIS to assess the spatial arrangement of occupied locations, suitable but unoccupied locations, and patterns of connectivity; (iv) comparing habitat suitability with patterns of occurrence across species and (v) classifying all species using combined measures of niche extent, habitat occupancy and limited dispersal. Because eutrophication probably excludes S. nitida and V. macrostoma from some ditches (Watson and Ormerod, 2004a), we used an additional analysis to assess explicitly whether eutrophication added to fragmentation effects. This situation would arise if adverse water quality substantially reduced occupancy at sites that were otherwise suitable and thereby increased gaps between occupied locations. The possibility that pollution can contribute to fragmentation in this way is a particular problem in aquatic ecosystems that has seldom been evaluated.

2.

Study area and methods

2.1.

Sampling locations

The data were derived from four large grazing marshes in south-east England described previously (Watson and Ormerod, 2004a): the Arun Valley in West Sussex (National Grid Reference TQ 03 14), Pevensey Levels in East Sussex (TQ 64 09), the Stour Valley in Kent (TR 26 63) and Lewes Brooks in East Sussex (TQ 42 08) (Fig. 1). All four marshes are periodically inundated by river flooding during autumn and winter and are grazed during spring and early summer mainly by cattle. Large parts are notified as Sites of Special Scientific Interest (SSSI) while the floodplain of the Arun, Pevensey Levels and part of the Stour Valley (Stodmarsh) are wetlands of international importance (Ramsar Convention Bureau, 2006). The Arun Valley and Stodmarsh are Special Protection Areas (SPA) under the EC Birds Directive (79/409/EEC) and Stodmarsh is a Special Areas of Conservation under the EC Habitat Directive (92/43/EEC). Stodmarsh and the south east of the Pevensey Levels are National Nature Reserves.

2.2.

Sampling procedure

Totals of 34, 35, 31 and 6 ditches were sampled for molluscs in the summer of 1999 respectively in the Arun Valley, Pevensey Levels, the Stour Valley, and the smaller Lewes Brooks. The overall total (n = 106) comprised 81 ditches selected randomly and 25 chosen since they had previous records of either S. nitida or A. vorticulus. This partial departure from an entirely random sample was defensible because (i) ditches holding each species were necessary to address the hypotheses under test; (ii) known locations were drawn from previous exhaustive surveys and reflected the true spatial distribution

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Fig. 1 – Location of the four grazing marshes surveyed for gastropods in south-east England.

1 0.9 0.8

Probability/sample

of these two species; (iii) ditches selected for A. vorticulus were random with respect to S. nitida and vice versa; both were random with respect to V. macrostoma; (iv) the frequencies of occurrence of S. nitida, A. vorticulus and V. macrostoma were not significantly different between the random and pre-selected ditches (v21d:f: ¼ 0:14  2:29, NS at p < 0.1). Molluscs in each ditch were sampled by surveying a 20 m stretch from which collections were bulked from four random points along one bank. At each point, a sweep was made over 1 m of sediment, vegetation and water surface using a sieve net with 0.18 m diameter and 1 mm mesh (Watson and Ormerod, 2004a). This method was subject to a quality assurance assessment involving 20 sweep samples drawn at random points from each of 20 ditches known to hold either A. vorticulus (n = 10) or S. nitida (n = 11), some of which also contained V. macrostoma (n = 12) (see Watson and Ormerod, 2004b). The average probability of detecting S. nitida, A. vorticulus and V. macrostoma in any one sample from ditches where they occurred was 0.418, 0.415 and 0.625; probabilities of capture increased with abundance (Fig. 2). Our chosen method with four replicate samples should thus give, on average, a 69–100% chance of detecting each of the RDB species where they occurred, with representation highly accurate for V. macrostoma. The chances of detecting S. nitida and A. vorticulus were effectively 100% at over two thirds of their occupied sites, but detection was more difficult at around one-third of occupied sites where abundances were low and probabilities of capture in four samples were around 15%. On this evidence, a small but quantifiable number of false negatives are likely in our data set, as is often the case for rare species (Wintle et al., 2004). Although the resulting samples contained 39 species of gastropods and bivalves, we selected only aquatic gastropods

0.7 0.6 0.5 0.4 0.3

Segmentina nitida Anisus vorticulus Valvata macrostoma

0.2 0.1 0 0.01

0.1

1

10

100

Abundance (Log)

Fig. 2 – The probability of detecting each of Segmentina nitida, Anisus vorticulus and Valvata macrostoma in individual sweep samples in relation to their mean abundance per sample across 20 drainage ditches of four grazing marshes in SE England. Twenty samples were drawn from each ditch at random locations (see Section 2).

present in >10% of the ditches (20 species). Abundance data were transformed (log(n + 1)) prior to all subsequent statistical analysis to homogenize variances. Two samples from the Arun Valley were also removed from the dataset since they contained no gastropods, leaving a total of 104 ditches in the dataset.

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Environmental measurements were made contemporaneously with mollusc collections (see Watson and Ormerod, 2004a). Briefly, ditch dimensions were recorded while water samples were collected at each site and analysed within 24 h for a range of determinand using standard methods (total oxidized nitrogen, ammonia, orthophosphate, nitrate, nitrite, chloride, alkalinity, calcium, pH, conductivity, chlorophyll a). For all except pH, concentrations were log(n+1) transformed prior to further data analysis. Vegetation character in each ditch was assessed by measuring the percentage cover by all vegetation, and by submerged, floating, emergent and amphibious plant groups (see Watson and Ormerod, 2004a). All ditches have very low current velocities, and no hydraulic variables were included in the analysis.

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conditions were within the ellipse boundaries. By comparing these to the sites that were actually occupied, sites were categorised as: (1) suitable and occupied: sites that fell within the tolerance ellipse and were occupied by the species; (2) suitable and unoccupied: sites within the tolerance ellipse that were not occupied; (3) classification errors: occupied sites that were not within the tolerance ellipse; (4) Unsuitable and unoccupied: sites that were outside of the tolerance ellipse and were not occupied.

2.5. Spatial pattern of occupancy and effects of connectivity

Assessments of habitat suitability were derived using Canonical Correspondence Analysis (CCA). This is a direct gradient ordination that relates the co-occurrence of species directly to environmental variables (Ter Braak, 1986). Ordination axes are derived such that each explains as much variability in species occurrence as possible while being independent of previous axes (Sˇmilauer and Lepsˇ, 2003). Axes are constrained to be a linear combination of the environmental variables included in the analysis. Species are assumed to have an unimodal response surface to the ordination axes (Ter Braak, 1986). We conducted CCA on the 20 gastropod species and 15 environmental variables, observed in 104 ditches using CANOCO 4.0 (Ter Braak and Sˇmilauer, 1998). A Monte Carlo permutation test of 499 permutations was used to determine whether variation in community composition was significantly related to variation in environmental data (Sˇmilauer and Lepsˇ, 2003). CCA can describe statistically the habitat amplitude over which each contributing species could occur, i.e. the proportion of available habitat that is suitable (Prentice and Cramer, 1990; Ruckelshaus et al., 1997). This is because the species’ positions on each ordination axis estimate their optimum habitat requirements. In turn, the standard deviation from this optimum reflects each species’ tolerance to changing conditions and can be considered a parameterisation of niche extent (Green, 1971). Since the tolerance parameter in CCA is sensitive to species’ prevalence, we applied a correction recommended by Ter Braak and Verdonschot (1995) and Ter Braak and Sˇmilauer (1998) in which the tolerance was divided by (1  1/N2)1/2, where N2 is the effective number of occurrences. When any two ordination axes are plotted, the niche extent of individual species can be described by ellipses of length proportional to the tolerance (Thioulouse and Chessel, 1992; Pappas and Stoermer, 1997). These ellipses were derived by multiplying the corrected tolerance on the first two ordination axes by 1.96 to calculate 95% confidence intervals (Dytham, 2003).

Using digitised Ordnance Survey data and data supplied (under licence) by the Environment Agency, we mapped all ditches in the four grazing marshes using ArcGIS 9.0 (ESRI, 2004). For all 20 gastropod species, both a Network-weighted and Euclidean nearest-neighbour distance were calculated from every suitable but unoccupied site to its nearest occupied neighbour within the same marsh. We also calculated the nearest-neighbour distances between occupied sites. Network-weighted distance was defined as the shortest possible distance through connected drainage ditches – representing the least-cost path between sources and potential new habitats for snails assumed to disperse through the ditch network. Euclidean distances reflected the straight-line movement between ditches that would have to be made by dispersing individuals either (i) during floods that inundated the entire marsh or (ii) when vectored by other organisms moving independently on the ditch network. Both these distance measures assume that dispersers could move freely between two specified points in sufficient numbers to result in colonisation (Lockwood et al., 2005). We used Kolmogorov–Smirnov tests in SPSS to compare the frequency distributions of the nearest-neighbour Euclidian distances between occupied sites with those from unoccupied suitable sites to occupied sites (i.e. potential sources). This difference, as indicated by the Kolmogorov–Smirnov Z, was taken as an index of limited dispersal. For each species, we calculated a classical fragmentation index as the median distance between all sites at which habitat was suitable irrespective of whether or not they were occupied (McGarigal and Marks, 1995). For the three marshes with sufficient data (i.e. excluding Lewes Brooks), we regressed the percentage of suitable but unoccupied sites for each species against the mean shortest distance between suitable unoccupied sites and occupied sites. These regressions were repeated using both networkweighted distances and Euclidean distances. Our intention was to assess whether these distance measures could explain patterns of occupancy among species and to appraise which species might be most affected. In order to produce a typology of species based on three conservation traits, we used Ward’s method to classify all gastropod species on three attributes of distribution: (i) percentage of suitable habitat occupied; (ii) niche extent and (iii) Kolmogorov–Smirnov Z.

2.4.

2.6.

2.3.

Assessing habitat suitability using ordination

Habitat occupancy relative to habitat suitability

From the ordinations, we derived tolerance ellipses for all 20 gastropod species and recorded the number of sites at which

Effect of eutrophication

Watson and Ormerod (2004a) showed using our data-set that both S. nitida and V. macrostoma were absent from otherwise

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were sometimes absent. For example, S. nitida occurred in all marshes except the Arun Valley, A. vorticulus was only present in the Arun Valley and the Pevensey Levels, and V. macrostoma only occurred in the Pevensey Levels. However, RDB species tended to have to some of the smallest niche extents of all gastropod species. They also occupied less than half (21.7–48.6%) of suitable habitats available, although the latter was true also in some non-RDB species such as Gyraulus albus, Valvata piscinalis (Table 2). This reflected the extreme position of all these species on ordination axes, and hence their apparently specific habitat requirements.

suitable sites that had elevated nitrate or nitrite concentrations. We wished to quantify whether these eutrophication effects might contribute to spatial patterns of occurrence, and to any limits on dispersal. Ordination analyses were repeated either excluding or including the water quality variables that indicated eutrophication (total oxidized nitrogen, ammonium, phosphate, chlorophyll a). This allowed an assessment of which sites were unsuitable explicitly because of water quality. We next repeated the analysis of spatial patterns in habitat suitability and habitat occupancy to assess the extent to which eutrophication affected distances between occupied and unoccupied sites.

3.3. Spatial pattern of occupancy and effects of connectivity

3.

Results

3.1.

Assessing habitat suitability using ordination

As an index of habitat fragmentation, the median distance between all suitable sites performed poorly, and explained no significant variation among species either in habitat occupancy (r2 = 0.06, NS) or distance between occupied and unoccupied suitable sites (r2 = 0.10, NS; Table 2). By contrast, across all gastropod species, percentage habitat occupancy declined significantly with increasing distances between unoccupied and occupied sites (Tables 2 and 3; e.g. Fig. 5). Occupancy patterns were equally well explained by Euclidean and Networkweighted distances between locations. These effects differed slightly across marshes, with distance effects apparently stronger in the Pevensey Levels than in the Arun or Stour Valley. Connectivity effects also varied across marshes: networkweighted distances (i.e. through drainage ditches) between occupied and unoccupied suitable sites were on average 2.3X greater (±0.7SD, n = 20 species) than Euclidean distances for gastropods on Pevensey Levels in comparison to 1.7X on the Arun (±0.7, n = 17) or 1.5X on the Stour (1.5 ± 0.2, n = 17; F2,51 = 13.93, p < 0.001). In other words, dispersal independently of the ditch network could be particularly effective in reaching unoccupied habitat on all marshes, but particularly on Pevensey Levels. Species most affected by distance effects and least likely to occupy all suitable habitats (i.e. those with high x and y positions in Fig. 5) were Planorbis carinatus, V. piscinalis, A. vorticulus,

In CCA, the first two axes explained over 15% of the variance in the species data and over 57% of the variance in species- environment relationship (Table 1). Axis 1 reflected a gradient from calcareous shallower ditches to deeper ditches with more open water while axis 2 graded ditches with nitrogen compounds to wider ditches richer in phosphate and chlorophyll a. Species scores and environmental vectors in ordination revealed the habitat preferences of the 20 gastropod species (Fig. 3). S. nitida (found at 18 sites) typified shallow, calcareous ditches covered with vegetation; A. vorticulus (13 sites) characterized deeper ditches with more open water, a high plant diversity and relatively low calcium concentrations; V. macrostoma (19 sites) characterized wide ditches with relatively high phosphate and chlorophyll a concentrations but low ammonium and oxidized nitrogen. Their tolerance ellipses also differed in both extent and position (Fig. 4). S. nitida and A. vorticulus overlapped only marginally but V. macrostoma overlapped with both these species.

3.2.

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Habitat occupancy relative to habitat suitability

Based on their tolerance ellipses, all 20 gastropod species had suitable habitat in all four grazing mashes even though species

Table 1 – Eigenvalues and statistics from CCA on 20 gastropod species from 104 ditches on four English grazing marshes Axes

(i) Including eutrophication variables Eigenvalues Species–environment correlations Cumulative percentage variance Species data Species–environment relation (ii) Excluding eutrophication variables Eigenvalues Species–environment correlations Cumulative percentage variance Species data Species–environment relation

Total inertia

1

2

3

4

0.164 0.807

0.070 0.722

0.045 0.677

0.035 0.545

11.1 40.2

0.154 0.784 10.4 46.1

15.8 57.2

0.054 0.666 14.1 62.4

All canonical axes significant in Monte Carlo test (499 permutations, p = 0.002) Separate analyses either included or excluded variables describing eutrophication.

18.8 68.1

0.038 0.621 16.6 73.7

1.483

21.1 76.6

0.031 0.506 18.7 82.9

1.483

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Emergent plant cover

TON

Ammonia Calcium

Amphibious plant cover Open water

CCA 2

Depth Plant diversity pH Width Phosphate Chlorophyl a

Submerged plant cover

Chloride Floating plant cover

Planorbis carinatus Lymnaea palustris sl

Valvata piscinalis

Planorbis planorbis

Bithynia tentaculata L. peregra L. stagnalis A. vortex Physa fontinalis Bathyomphalus Planorbarius corneus V. cristata contortus

Anisus vorticulus

Segmentina nitida

Armiger crista

Hippeutis complanatus

Bithynia leachii Acroloxus lacustris

Valvata macrostoma

Gyraulus albus

CCA 1

CCA 2

Fig. 3 – The first two axes from a CCA relating 20 gastropod species to 15 environmental variables in 104 drainage ditches in four English grazing marshes. The Red Data Book species are in bold.

CCA 1

Fig. 4 – Confidence tolerance ellipses (95%) describing habitat suitability for three Red Data Book gastropods on southern English grazing marsh. Segmentina nitida: grey; Valvata macrostoma: thick outline; Anisus vorticulus: dotted outline. Filled symbols are the species scores and unfilled symbols represent the site scores.

Armiger crista and S. nitida (Table 4). Bithynia tentaculata and Limnaea peregra were least affected. Species rankings were consistent across all three marshes (rs = 0.48-0.82, all p < 0.05), with only minor exceptions. For S. nitida and A. vorticulus (but not V. macrostoma), median Euclidean distances from occupied to unoccupied but suitable sites were significantly greater than distances between occupied sites by 3  4X (Kolmogorov– Smirnov tests, P < 0.05). However, these effects were also apparent in four non-RDB species, in particular Planorbis carinatus and Acroloxus lacustris (Table 2). When all gastropod species were classified using combined measures of apparent dispersal effects (Kolomogorov–Smirnov Z), niche extent and habitat occupancy, three contrasting groups were clearly apparent (Table 2). At one extreme, Group A species had wide niches, occupied much

of their available habitat and in no case were characterized by variations in distance between occupied-occupied and occupied-suitable sites. By contrast, Group C species had the smallest niche extents coupled with some combination of low habitat occupancy (e.g. V. macrostoma) and/or significantly greater distances between occupied-suitable sites than between occupied sites (A. vorticulus and S. nitida). Other species apparently affected by dispersal were not additionally affected by reduced niche extents (i.e. Group B species).

3.4.

Effect of eutrophication

Variations explained by CCA decreased marginally when eutrophication variables were excluded (Table 1). Eutrophication

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Table 2 – Niche extent, percentage occupancy of suitable habitat, and median distances (m) between occupied–occupied sites and occupied–unoccupied but suitable sites for 20 gastropod species on southern English grazing marsh

An index of fragmentation is also shown for each species derived as the median distance between all suitable sites. Differences between the frequency distributions of occupied–occupied and occupied–unoccupied but suitable sites are shown according to Kolomogorov–Smirnov tests. Species classifications on occupancy, niche extent and dispersal limits are shown according to Ward’s method.

Table 3 – Regressions relating the percentage unoccupied suitable habitat among 20 gastropod species to either the average functional or Euclidean distance between the suitable empty sites and their nearest suitable occupied ditch Marsh

Equation

SE constant

SE slope

p-Value slope

R2

(i) Functional distance Arun Valley (n = 17) Pevensey Levels (n = 20) Stour Valley (n = 17)

0.0047x + 42.4 0.0156x + 5.27 0.0122x + 20.0

6.3 6.6 7.8

0.0017 0.0023 0.0035

0.017 <0.0001 0.004

32.6% 71.3% 43.9%

(ii) Euclidean distance Arun Valley Pevensey Levels Stour Valley

0.0085x + 42.1 0.0242x + 14.9 0.0123x + 26.7

6.3 5.1 7.5

0.0031 0.0034 0.0046

0.015 <0.0001 0.017

33.7% 73.5% 32.4%

Standard Errors (SE), p values and R2 are given for each equation (see Fig. 5).

reduced the percentage of suitable sites that were unoccupied for S. nitida and V. macrostoma so that water quality could explain respectively 7.2% and 17.1% of their absences (data not illustrated). However, distances between occupied and suitable unoccupied sites were effectively unchanged after accounting for eutrophication (e.g. S. nitida median 1483 m; V. macrostoma median 794 m; cf. Table 2) because eutrophic ditches were not spatially aggregated on any marsh. There were no eutrophication effects on A. vorticulus.

4.

Discussion

Previous research indicated that habitat loss and quality affect the distribution of S. nitida, A. vorticulus and V. macrostoma in the UK (Watson and Ormerod, 2004a,b). The analyses here confirm their habitat requirements and also illustrate how they can be quantified using ordination (see Section 3.1). However, three results support the hypothesis that dispersal is an additional limit. First, each species occupied only 1–3

% suitable ditches unoccupied

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100

80

60

Planorbis carinatus Anisus vorticulus Valvata piscinalis Acroloxus lacustris Armiger crista Segmentina nitida

Lymnaea stagnalis

Valvata cristata

40

Lymnaea palustris sl Hippeutis complanatus

20

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Gyraulus albus

Planorbarius corneus

Physa fontinalis Valvata macrostoma Bathyomphalus contortus

Bithynia leachii

Anisus vortex Planorbis planorbis Bithynia tentaculata Lymnaea peregra

Euclidean distance (m)

0 0

500

1000

1500

2000

2500

3000

3500

4000

Fig. 5 – The percentage of suitable habitat that was unoccupied for each of the 20 gastropods in the Pevensey Levels in relation to the average nearest distance between occupied and suitable but unoccupied habitat. The Red Data Book species are in bold (see Table 3).

Table 4 – Gastropod species ranked according to apparent effects of distance between occupied and suitable habitat on habitat occupancy in three English grazing marshes (1 = least affected) Species Lymnaea peregra Bithynia tentaculata Planorbis planorbis Hippeutis complanatus Bithynia leachii Lymnaea palustris sl Anisus vortex Valvata cristata Bathyomphalus contortus Lymnaea stagnalis Physa fontinalis Valvata macrostoma Planorbarius corneus Gyraulus albus Acroloxus lacustris Segmentina nitida Armiger crista Anisus vorticulus Planorbis carinatus Valvata piscinalis

Pevensey Levels 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20

Arun Valley 4 1 7 9 6 2 3 15 13 5 12 16 14 17 10 11 8

Stour Valley 5 1 4 10 7 9 6 3 2 11 12 8 14 13 15 16 17

See Fig. 5 for an example of how species were ranked.

marshes even though all four marshes provided suitable habitat. Dispersal between marshlands or drainage basins can thus be considered a potential barrier to occupancy for all three species. As S. nitida and V. macrostoma have been lost from whole marshes in their former range (e.g. V. macrostoma from Lewes Brooks), we are not erroneously ascribing fragmentation effects to the species’ primary distribution. Secondly, among all 20 gastropods examined, the occupancy of suitable habitat declined significantly as the distance to the nearest occupied sites increased. S. nitida and A. vorticulus were among the species most affected. This supports previous evidence for dispersal limits on these two species which

are slower than more common snails to recolonise dredged ditches (Hingley, 1979). Thirdly, distance effects on each species were replicated across marshes, suggesting that general attributes of the species (e.g. dispersal ability) or marshes (e.g. ditch management, ditch connectivity or flood frequency) must be involved. Notwithstanding these results, one aspect of our data illustrates that limited dispersal alone cannot explain the unfavourable conservation status of freshwater gastropods in that four non-RDB species were also affected by distance and dispersal effects. However, only Armiger crista and Gyraulus albus had some combination of limited dispersal, low habitat occupancy (<50%) and small

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niche extent of the type that characterized the RDB species. The overall implication is that these factors combine in various ways to affect the distribution of S. nitida, A. vorticulus and V. macrostoma even where habitats are suitable. Interpretation of our data requires three assumptions: that samples drawn from each site effectively detect the species present; that the scale at which sites were sampled adequately reflects distribution; and that ordination captures all key influences on habitat suitability. Sampling is particularly problematic for rare species (Wintle et al., 2004), but our methods were carefully calibrated in replicate ditches (see Fig. 2 and Watson and Ormerod, 2004b). Detection using four replicate samples was highly effective for V. macrostoma, but the average probabilities of detecting A. vorticulus or S. nitida were smaller (p = 0.69), particularly at low abundance. Some false negative results – i.e. absence ascribed to sites that were actually occupied – might therefore exist in our data. At this probability of capture, the true number of occupied sites is likely to have been around 45% greater than that recorded (n = 13–18 sites) for both species, adding probably 6 and 8 sites, respectively for A. vorticulus and S. nitida. This represents just 13% and 36% of the 22 and 44 sites identified by ordination as suitable for these species but unoccupied. Gaps in distribution were thus 2.8  7.7X more numerous than could be explained by sampling error. Moreover, random errors in detection would be unlikely to explain apparent distance effects (see Fig. 5). As with sampling, issues of scale-dependence often affect distributional studies. At broader scales (ditch-to-ditch or marsh-to-marsh), variations in ditch chemistry and vegetation influence the three RDB species (Watson and Ormerod, 2004a). Dispersal effects are most likely at these scales, where water bodies are not directly connected. Errors in determining spatial patterns might have arisen if occupied or suitable sites were more adjacent than were recorded at our sampling resolution. However, three arguments support our conclusions about dispersal effects. First, gaps in distribution were apparent at both ditch-to-ditch and marsh-to-marsh scales, and so cannot depend on sampling density within marshes. Secondly, site-selection was quasi-random, and allows the conclusion that explicit spatial pattern (i.e. aggregation of occupied sites but increased distance to suitable but unoccupied sites) is a real attribute of current distribution. Finally, randomly sampling more ditches at finer resolution might reduce the magnitude of the distances involved in Table 2 and Fig. 5, but not the relative effects of distance or occupancy. The third assumption – that habitat suitability was adequately parameterised using ordination and reciprocal averaging – depends on whether the measured environmental variables represent major causal influences on distribution. Species–environment correlations were strong, explaining 57% of the variance in mollusc assemblage composition. Errors might arise, nevertheless, if some key influence on distribution were overlooked. Biotic factors, such as predation, parasitism, disease, competition or food availability, are poorly understood in the RDB species and none was included. A more technical assumption was that simple, variancebased ellipses adequately represented each species’ n-dimensional niche (Doledec et al., 2000). Our experience comparing actual and expected occurrence indicated that this niche

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measure is probably slightly conservative for generalist taxa while overly optimistic about the range of rarer taxa. The use of 95% ellipses corrected the latter effect when applied to the three RDB species.

4.1.

Distance, dispersal and fragmentation effects

Dispersal affects population persistence, particularly in fluctuating environments or fragmented systems (Hanski, 1999). These effects may be widespread in freshwaters because (i) they are naturally isolated among otherwise terrestrial landscapes; (ii) many freshwater habitats are dynamic or transient; (iii) habitat loss, changing habitat quality and reduced hydrological connectance between water bodies exacerbate their natural patchiness (Pringle, 2001). Populations are impacted where water bodies become isolated at distances greater than can be covered by the colonists of any given species. However, because of their small body size, there are few examples where the dispersal of freshwater invertebrates has been measured directly (Briers et al., 2003). More often, dispersal and fragmentation are inferred by comparing species with contrasting dispersal traits (Rundle et al., 2002), from genetic pattern (Wilcock et al., 2001) or from distributional analysis like ours. In keeping with results from other studies, our data reveal the limitations of general ‘fragmentation indices’ (i.e. median distances among suitable sites) for the latter purpose (Tischendorf, 2001; Winfree et al., 2005). By contrast, spatially explicit analysis of occupancy relative to carefully quantified habitat suitability revealed distance effects, perhaps because this approaches gives a closer approximation of true source-sink dynamics and dispersal pattern (With and Crist, 1995). Drainage ditches in English grazing marsh are isolated not only by their location in different drainage systems (Fig. 1), but also by network distance within the same marsh. Here, the local occurrence of two RDB species was equally well explained by Euclidean distances and network distances through drainage ditches, implying that dispersal might involve either pathway. However, network distances exceeded Euclidean distances between occupied locations by 1.5  2.3X, so that straight-line dispersal using floods or other living vectors would be most efficient in reaching new habitat. Interestingly, not only RDB species were involved, suggesting that dispersal effects might be overlooked more generally in mollusc distributional studies. Potential fragmentation effects on grazing marsh that might exacerbate dispersal problems include increasing habitat loss, drainage, abstraction, flood control and eutrophication over the last 70 years. These phenomena are epitomized by Pevensey Levels (see Refs. in introduction), where major changes have occurred in three phases respectively following the creation of the Pevensey Levels Internal Drainage Board in the 1930s; MAFF-funded (Ministry of Agriculture, Fisheries and Food) drainage during the 1960s; and increased arable conversion between the late 1970–1990 under the Commons Agricultural Policy (Gasca-Tucker, 2005). One net effect would be the isolation of drainage ditches that are now less often connected by marsh-wide flooding. In addition, ditches are managed rotationally by vegetation clearance to allow unimpeded drainage, effectively altering

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the habitat conditions under which each of the RDB snails occurs (Watson and Ormerod, 2004a). Any such interventions at frequent intervals risk exacerbating fragmentation effects by increasing disturbance, reducing local populations and increasing distances between occupied patches. Patches of unsuitable habitat have also been extended by eutrophication in some ditches (Watson and Ormerod, 2004a), although in this case contributions to fragmentation are currently small: habitat loss due to eutrophication is apparently marginal (7% in S. nitida; 17% in V. macrostoma), while the affected ditches are not aggregated spatially.

4.2.

Conservation ramifications

Methods to assess dispersal and fragmentation effects on organisms are still scarce in conservation biology, and few examples quantify habitat suitability in conjunction with spatially explicit analysis. Our landscape ecological approach may be applicable more widely where similar problems arise, and we suggest that that some of the conservation ramifications of this work are generic. However, the results of most direct conservation value are specific to the species we examined. In particular, indications that dispersal in S. nitida, A. vorticulus and V. macrostoma might compound effects of small niche extent and limit distribution have three major corollaries: First, there is a need to understand better their dispersal mechanisms. Other than in parasite vectors, the traits and mechanisms in aquatic snails that favour effective dispersal, colonisation and persistence are poorly understood (Brown et al., 1998; Brown and Johnson, 2004; Reckendorfer et al., 2006). This is surprising given that freshwater gastropods are among the most numerous species on the IUCN red list (Seddon, 1998; Baillie et al., 2004). Secondly, the population effects of fragmentation and limited dispersal on each species require assessment. In other organisms, extinction risks increase in fluctuating environments where dispersal is disrupted (Stacey and Taper, 1992). Other consequences, such as reduced genetic diversity, can further reduce population viability and should be investigated (Cushman, 2006). Thirdly, re-inforcement and re-introduction should now be evaluated as means of maintaining and expanding the populations of the three RDB species. Given that they occupy less than half of their apparently suitable habitat, the implication is that artificial movement to suitable ditches could double existing populations. Habitat requirements can now be sufficiently quantified to identify candidate locations (see Figs. 3 and 4), while trial re-introductions would act as a means of validating habitat suitability assessments. For all three species, recovery is almost certain to require reintroduction – assuming that wider habitat restoration of lost or damaged grazing marsh can be achieved. In this case, experimental trials will be critical to success.

Acknowledgements The analytical part of this project was funded through the European Union Socrates programme through its support of

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295

KN. Data collection was funded by the Natural Environment Research Council and the Environment Agency, who also allowed access to GIS data layers that supported the spatial analysis. Kathy Friend and two anonymous reviewers provided insightful comments on the manuscript.

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