Biological Conservation 144 (2011) 821829

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Biological Conservation
journal homepage: www.elsevier.com/locate/biocon

Applying species distribution modelling to identify areas of high conservation value for endangered species: A case study using Margaritifera margaritifera (L.)
Conor D. Wilson , Dai Roberts, Neil Reid
Quercus, School of Biological Sciences, Queens University Belfast BT9 7BL, UK

a r t i c l e

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a b s t r a c t
The development and implementation of a population supplementation and restoration plan for any endangered species should involve an understanding of the species habitat requirements prior to the release of any captive bred individuals. The freshwater pearl mussel, Margaritifera margaritifera, has undergone dramatic declines over the last century and is now globally endangered. In Northern Ireland, the release of captive bred individuals is being used to support wild populations and repatriate the species in areas where it once existed. We employed a combination of maximum entropy modelling (MAXENT) and Generalized Linear Mixed Models (GLMM) to identify ecological parameters necessary to support wild populations using GIS-based landscape scale and ground-truthed habitat scale environmental parameters. The GIS-based landscape scale model suggested that mussel occurrence was associated with altitude and soil characteristics including the carbon, clay, sand, and silt content. Notably, mussels were associated with a relatively narrow band of variance indicating that M. margaritifera has a highly specic landscape niche. The ground-truthed habitat scale model suggested that mussel occurrence was associated with stable consolidated substrates, the extent of bankside trees, presence of indicative macrophyte species and fast owing water. We propose a three phase conservation strategy for M. margaritifera identifying suitable areas within rivers that (i) have a high conservation value yet needing habitat restoration at a local level, (ii) sites for population supplementation of existing populations and (iii) sites for species reintroduction to rivers where the mussel historically occurred but is now locally extinct. A combined analytical approach including GIS-based landscape scale and ground-truthed habitat scale models provides a robust method by which suitable release sites can be identied for the population supplementation and restoration of an endangered species. Our results will be highly inuential in the future management of M. margaritifera in Northern Ireland. 2010 Elsevier Ltd. All rights reserved.

Article history: Received 1 June 2010 Received in revised form 8 November 2010 Accepted 18 November 2010 Available online 13 December 2010 Keywords: Captive breeding Endangered species management Generalized Linear Mixed Model Geographic Information System (GIS) MAXENT Reintroduction Supplementation

1. Introduction Subtle variation within the natural environment of an organisms range is considered to be one of the most inuential determinants of its distribution (Strayer, 2008; Reid et al., 2010). However, dening a species habitat niche is often difcult (Hastie et al., 2000). Using a tool that gives an understanding of the variation of the quality of an organisms habitat enables the prioritization of areas for conservation (Farren et al., 2010) and is important in reducing effort and cost required to manage rare or threatened species (Olsson and Rogers, 2009). Habitat suitability mapping is frequently used to identify areas in need of restoration or preservation (Gibson et al., 2004), or identify candidate areas for species reintroduction (Olsson and Rogers,
Corresponding author. Address: Quercus, School of Biological Sciences, Queens University Belfast, MBC, 97 Lisburn Road, Belfast BT9 7BL, UK. Tel.: +44 (0) 2890972066; fax: +44 (0) 28 9097 5877. E-mail address: cwilson20@qub.ac.uk (C.D. Wilson).
0006-3207/$ - see front matter 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.biocon.2010.11.014

2009). Predictive species-specic landscape favourability models, based on Geographic Information Systems (GIS), have become the favoured method in dening species habitat requirements (Guisan and Zimmerman, 2000). However, remotely-sensed satellite data frequently used in GIS-based models generally only represent coarse proxies for those variables exerting true inuence (Guisan and Zimmerman, 2000). GIS-based models are, therefore, likely to benet from the inclusion of local environmental parameters that have been ground-truthed (Brambilla et al., 2009) but this is rarely employed (Gibson et al., 2004). Endangered species conservation increasingly involves breeding animals in captivity and releasing them into areas where they historically existed (Wilson et al., 2010). Although seen as the method of last resort, captive breeding and release has had some notable successes; for example, the American bison Bison bison (Fitter, 1986) and black-footed ferret Mustela nigripes (Russell et al., 1994). However, reintroduction programmes generally have limited monitoring whilst research is ad hoc and in need of experimental and empirical approaches to evaluate their efcacy

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(Seddon et al., 2007). A clear understanding of species-specic habitat niche allows the identication of potential release sites with the maximum chance of post-release survival often demonstrating a need for habitat restoration prior to reintroduction. Consequently conservationists are increasingly emphasizing the integration of distribution models with reintroduction and population augmentation programmes (Seddon et al., 2007; Sergio et al., 2007). A rule of thumb in biogeography is that a species is most abundant at the centre of the range of environmental gradients along which it occurs (Hochberg and Ives, 1999); this is the abundant centre distribution model (Sagarin and Gaines, 2002). Chronic changes in environmental conditions are likely to have greater impact on those individuals at the edges of a species range than those at the centre. Consequently, although it could be argued that habitat suitability models might be biased if they are developed when a species is no longer found throughout its historic range, they should indicate key elements of its niche that can be used to inform conservation strategies during reintroductions (Gibson et al., 2004). Populations of the freshwater pearl mussel Margaritifera margaritifera (Linnaeus, 1758) declined substantially during the 20th century throughout most of its holarctic range (Bauer, 1988; Wilson and Roberts, 2010). The principal causes were pearl shing, declining water quality, lack of sh hosts and siltation (Beasley et al., 1998; Hastie and Young, 2003; Skinner et al., 2003; Preston et al., 2007). Consequently, the species is now listed as endangered by the IUCN (Mollusc Specialist Group, 1996). M. margaritifera has a complex life cycle; it has glochidial larvae that are parasitic on the gills of young salmonids, which remain on the gills of the host overwinter after which they excyst and fall to the riverbed (Young and Williams, 1984; Bauer, 1987; Skinner et al., 2003). Excysted mussels require oxygen rich interstitial spaces in the hyporheic zone of gravel substrate where they remain for up to 4 years (Skinner et al., 2003; sterling et al., 2008). Modern agricultural practices and deforestation increases river silt loads blocking interstitial spaces and generally degrades habitat quality for mussel recruitment (sterling et al., 2008; Geist and Auerswald, 2007). Moreover, ooding events increase environmental stress on mussels, most notably

juveniles, which are at increased risk of being dislodged from the riverbed (Hastie et al., 2001) and translocated downstream into unsuitable habitat (sterling et al., 2008). Conservation strategies aimed at slowing or halting the decline of M. margaritifera throughout Europe recommend supplementing remnant populations and extending the species current range to sites were it existed historically but is now locally extinct (Araujo and Ramos, 2001; Anonymous, 2005). Consequently, there has been much interest in captive breeding of M. margaritifera to generate stocks for population restoration (Buddensiek, 1995; Preston et al., 2007; McIvor and Aldridge, 2008). The inuence of environmental parameters on M. margaritifera distribution has been examined at varying spatial scales (Beasley and Roberts, 1999; Hastie et al., 2000, 2003; Morale et al., 2004). However, most historic and contemporary attempts to characterise freshwater pearl mussel habitat have gone untested (Strayer, 2008). In Northern Ireland, the species declined dramatically in the last century and remains extant in only six rivers restricted to the west of the country in Counties Fermanagh and Tyrone (Fig. 1). Estimates that M. margaritifera may be extinct in Northern Ireland within 80 years (Beasley et al., 1998) prompted the initiation of an ex situ captive breeding programme in 1998 (Preston et al., 2007). This programme came to fruition during 2009 when approximately 350, 810 year old captive-bred juvenile mussels were released into the wild to supplement an existing population in the Ballinderry River, Co., Tyrone (Wilson et al., 2010). Because the release of captive-bred animals is a measure of last resort, it is important that release sites are selected carefully. Initial release sites in Northern Ireland were chosen primarily because they supported living mussels. Further releases of captive-bred mussels rely on identifying suitable reintroduction rather than population supplementation sites, contingent with the Species Action Plan for the freshwater pearl mussel in Northern Ireland. However, the landscape and habitat requirements of the species are evidently complex and poorly understood. The present study aimed to develop GIS-based landscape and ground-truthed habitat models that explain the current distribution of M. margaritifera in Northern Ireland. These models will

j b k f e i c a g

Fig. 1. Rivers in Northern Ireland with extant mussel populations: (a) Ballinderry, (b) Owenkillew, (c) Owenreagh, (d) Swanlinbar, (e) Tempo, (f) Waterfoot and historic mussel populations: (g) Upper Bann, (h) Bush, (i) Colebrooke, (j) Moyola, (k) Mourne/Strule.

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provide objective criteria to identify areas within rivers that: (a) have a high conservation value yet need habitat restoration at a local level, (b) sites for population supplementation of existing populations and (c) sites for species reintroduction to rivers where the species historically occurred but is now locally extinct. These methods are widely applicable to other species of conservation concern and are likely to be highly useful for other reintroduction programmes, especially where individuals being released are from an endangered species.

2. Materials and methods 2.1. Species records The entire distribution of M. margaritifera in Northern Ireland was surveyed during 2009. On each of the six rivers where the species remains extant, point transect surveys for species presence were conducted every 500 m between the most upstream and downstream points from which the species was known. Mussel presence was determined using a bathyscope and a zig-zag survey design across the width of the river 10 m above and below each survey point. All surveys were conducted during low water. 2.2. Landscape parameterization ArcGIS v9.3 (ESRI, California, USA) was used to extract habitat variables on a landscape scale resampled to a common pixel size of 250 m throughout Northern Ireland. Altitude and the range of slope (in degrees) were taken as topographic descriptors, soil type was characterised by percentage carbon, clay, sand, and silt whilst habitat variables were chosen intuitively; broad-leaved woodland and coniferous plantations were deemed likely to alter the water cycle and affect ground runoff, sedimentation and water acidication whilst urban areas were considered likely sources of water contaminant pollution (Table 1).

Water quality was excluded from the current study for a number of reasons. Firstly, there are many measures of quality including physical (pH), chemical (N2, P, DO, etc.) and biological (for example, invertebrate scores such as BMWP) metrics. Secondly, whilst water quality is monitored throughout Northern Ireland sampling points frequently focus on areas such as commercially important shing rivers or areas designated for some aspect of their biodiversity. Some stretches of river have not been surveyed and it is impossible to interpolate values across the landscape for the purposes of species modelling as metrics vary not only between-catchments but within-catchments; unidirectionally downstream from any source of pollutant. Moreover, pollution events can be stochastic resulting in a temporal reduction in water quality before rapidly returning to background levels, Consequently, resampling water quality metrics at a common pixel size of 250 m may well have been meaningless. Thirdly, M. Margaritifera is long-lived and the effect of variance in water quality may have differential effects on adults and juveniles as well as the sh populations on which they depend. Availability of suitable densities of sh hosts for the parasitic larvae of M. margaritifera is also likely to be a limiting factor in their distribution but electroshing data did not cover all potential sites and suffered from similar problems to that of water quality and has also been excluded from analyses. Whilst we acknowledge the importance of water quality and sh densities it would be difcult to incorporate any metric at a useful scale into a species favourability model. Consequently, we focus here exclusively on landscape and habitat metrics, some of which may, themselves, be proxies for water quality or sh density. As a result we explicitly deal with any shortcomings in our model in Section 4. 2.3. Habitat parameterization Point transect surveys were used to ground-truth local habitat features. A modied River Habitat Survey (RHS, 2003) was used to collect data on the presence and absence of habitat features

Table 1 Description of variables extracted at two spatial scales (a) landscape parameters extracted from 250 m raster pixels and (b) habitat parameters recorded during point transect surveys every 500 m along rivers used in the biogeographical modelling of M. margaritifera occurrence. Spatial scale Variable name Unit Metres % % Index % % % % % Categorical Categorical Categorical Categorical Categorical Description Mean elevation above sea level derived from a Digital Elevation Model for Northern Ireland Percentage coverage of broad-leaved woodland derived using the Land Cover Map 2000 Percentage coverage of coniferous forest derived using the Land Cover Map 2000 The difference between the steepest and gentlest slope in degrees in each 250 m raster pixel derived from a Digital Elevation Model for Northern Ireland The mean percentage content of soil within that was classied organic (carbon) using the Northern Ireland Soil Survey data The mean percentage content of soil that was classied clay using the Northern Ireland Soil Survey data The mean percentage content of soil that was classied sand using the Northern Ireland Soil Survey data The mean percentage content of soil that was classied silt using the Northern Ireland Soil Survey data Percentage coverage of urban and suburban plus rural development derived using the Land Cover Map 2000 Presence or absence of (a) broken standing waves, (b) unbroken standing waves, (c) rippled ow or (d) smooth ow Presence or absence of (a) submerged ne leaved, (b) submerged linear leaved, (c) submerged broadleaved, (d) liverworts/mosses/lichens, (e) emergent reeds/sedges/rushes/grasses/horsetails or (f) lamentous algae Presence or absence of (a) bankside tree cover, (b) exposed bankside roots, (c) underwater tree roots, (d) fallen trees, (e) large woody debris, (f) shading of channel or (g) overhanging boughs Classed as either consolidated or mobile substrate Classed as (a) bedrock, (b) boulder, (c) cobble, (d) earth/peat, (e) gravel/pebble, (f) sand or and (g) silt

(a) Landscape parameters 250 m Raster Altitude pixels Broad-leaved woodland Coniferous plantations Slope range Soil carbon content Soil clay content Soil sand content Soil silt content Urban (b) Habitat parameters Survey points Flow regime every 500 m Macrophytes Riparian trees Substrate mobility Substrate type

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10 m above and below each survey point. These included characterisation of ow regime, description of macrophyte communities, extent of riparian trees, substrate type, and mobility (Table 1).

3. Results A total of 50 out of 120 point transects were positive for M. margaritifera (41.7% occurrence). Overall mean mussel density was 0.12 mussels m2 0.33 SD. Whilst mussels occurred most frequently and at highest density in the Owenkillew river, Co. Tyrone and least frequently and at lowest density in the Ballinderry river, Co. Tyrone variability was large with little differences between sites (Fig. 2). At the landscape scale, M. margaritifera occurrence was most strongly associated with altitude and soil clay content but also inuenced by broad-leaved woodland, soil sand, carbon and silt content (Fig. 3). Whilst largely negatively associated with broadleaved woodland and positively associated with soil sand content, the species-landscape associations displayed a relatively narrow band of tolerance for most explanatory variables (Fig. 4). For example, probability of occurrence was markedly greater between 0% and 20% soil silt content (almost reaching probability 1.0 at 10% silt) yet showed little differentiation (probability % 0.4) throughout the rest of the variables natural range (2080% silt). Model performance, dened as the area under the curve, was highly discriminative with AUC = 0.970, indicating that M. margaritifera occupied a highly specic landscape niche. Landscape favourability for M. margaritifera was generally biased towards the eastern slopes of the Sperrin Mountains, south County Tyrone and the Fermanagh lakelands (Fig. 5a).

2.4. Statistical analyses Ninety-ve percentage condence intervals were calculated for the percentage occurrence of mussels within each site using 1000 iteration re-sampling bootstrapping conducted by the Resampling Stats for Excel RSXL add-in v.4.0. Whilst every effort was made to survey the entire range of M. margaritifera, it remained possible that the species occurred on other tributaries or river basins not surveyed. Therefore, a presence-only modelling approach was used to predict landscape favourability for the species throughout Northern Ireland. Emerging literature suggests that maximum entropy modelling has greater predictive success than more traditional presenceabsence modelling techniques such as general linear modelling (GLM), general additive modelling (GAM) or boosted regression trees, most notably using small sample sizes (Hernandez et al., 2006). k, 2008) was Maxent 3.2.1 (Phillips et al., 2006; Phillips and Dudl used to predict the probability of species occurrence at a pixel size of 250 m, ensuring the spatial exclusivity of each 500 m point transect. Due to the restricted range of M. margaritifera it was hypothesised that the species habitat associations would occupy a narrow band of tolerance and, therefore, not display linear relationships. Consequently, model exibility was by maximised by considering quadratic, product, threshold, hinged and discrete functions for k, 2008). Jackknife reall landscape parameters (Phillips and Dudl sampling analysis was used to determine a heuristic estimate of the relative contribution of each variable based on the performance of the global model (known as test gain) without the variable of interest compared to the inuence of that variable in isolation (derived from a univariate model only). Global model performance was judged using the area under the receiver operating characteristic (ROC) curve (Liu et al., 2005). Marginal response curves of the predicted probability of species occurrence were graphed for each explanatory variable that contributed substantially to the global model. A map of landscape favourability for M. margaritifera was generated to reect the predicted probability of species occurrence using ArcGIS 9.3. The proximate determinants of species occurrence at the local scale were examined using a true presenceabsence approach. Type II errors (false negatives) were minimised by the fact the entire range of the species was surveyed within each river. Consequently, a Generalized Linear Mixed Model (GLMM) assuming a binomial error distribution and a logit link function was used to examine species occurrence in relation to ground-truthed habitat features. Principal Components Analysis (PCA) was used to reduce presenceabsence data for aspects of ow regime, macrophyte communities and riparian trees into independent, intuitively appealing and biologically relevant variables. The latter were tted as covariates; substrate type and mobility were tted as xed factors and river ID was tted as a random factor. Model selection followed an information-theoretic approach (Burnham and Anderson, 2002). The Akaike Information Criterion (AIC; Akaike, 1983) was used to rank all possible model combinations. The Akaike weight (wi) of each model is the relative likelihood of that model being the best within a set of n models, and was determined within those models with a DAIC(Di) 6 2 (Burnham and Anderson, 2002). Multimodel inference was used to determine the averaged effect size (b coefcient) of each variable across the top set of models (Burnham and Anderson, 2002). GLMM analysis was performed using procedure lmer from the lme4 library in the open-source statistical package R (www.cran.r-project.org).

100
Mussel density % occurrence

1.0 0.8 0.6 0.4 0.2 0.0

po h ba ag rry ot fo m lin re de er Te lin an en en at ki lle w r

80

60 40 20 0

Ba l

Sw

Fig. 2. Percentage occurrence and density of M. margaritifera across six rivers in Northern Ireland bootstrapped 95 condence intervals.

Altitude Soil clay content Broad-leaved woodland Soil sand content Soil carbon content Soil silt content Coniferous plantations Slope Urban 0.0 0.5 1.0 1.5

(21.6) (21.6) (13.9) (13.2) (10.5) (9.1) (4.7) (3.8) (1.5)

2.0

% test gain
Fig. 3. Jackknife analyses of the importance of environmental variables in maximum entropy modelling of M. margaritifera occurrence. A heuristic estimate of the relative contribution of each variable to the global model is given in parentheses whilst variables are listed in descending order of importance. Grey bars show the performance of the global model (known as test gain) without each variable and black bars show the inuence of each variable in isolation (derived from a univariate model only).

Mussel density (m )

% occurrence

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1.0

1.0 0.8 0.6 0.4 0.2 0.0 0 200 400 600 0 10 20 30 40 50 60

1.0 0.8 0.6 0.4 0.2 0.0 0 20 40 60 80 100

Probability

0.8 0.6 0.4 0.2 0.0

Altitude (m)

Soil clay content (%)

% Broad-leaved woodland

1.0

1.0 0.8 0.6 0.4 0.2 0.0

1.0 0.8 0.6 0.4 0.2 0.0

Probability

0.8 0.6 0.4 0.2 0.0 0 20 40 60 80 100

10

20

30

40

50

20

40

60

80

Soil sand content (%)

Soil carbon content (%)

Soil silt content (%)

Fig. 4. Marginal response curves of the predicted probability of M. margaritifera occurrence for explanatory variables that contributed substantially to the global maximum entropy model.

Principal Component Analysis successfully reduced aspects of ow regime, macrophyte communities and riparian trees to three highly structured components with 85.4%, 70.3% and 65.0% of cumulative variance explained in each respectively (Table 2). At the local habitat scale, the proximate determinants of M. margaritifera occurrence were substrate mobility, proximity of mature bankside trees (Tree PC1 and PC2), the presence of macrophytes such as liverworts mosses and lichens and the absence of lamentous algae (Macrophyte PC1) and rapid water ow (Flow PC1) (Fig. 6). Model performance was highly discriminative with AUC = 0.903; suggesting that within rivers M. margaritifera occupies a highly specic habitat. Whilst substrate type did not feature in the top set of models, exploration of the data suggested there was substantial variation in M. margaritifera occurrence between substrate types with cobble, gravel and pebble being most favourable (Fig. 7). The relatively small sample size (n = 50 positive occurrences) subdivided by a seven-level factor may be responsible for the inability to detect these relationships statistically.

4. Discussion This is the rst study to use both GIS-based landscape scale and ground-truthed habitat scale parameters that inuence the occurrence and distribution of the globally endangered bivalve M. margaritifera. We propose a three phase conservation strategy in line with the Species Action Plan (Anonymous, 2005); identifying areas within rivers that: (i) have a high conservation value yet needing habitat restoration at a local level, (ii) sites for population supplementation of existing populations and (iii) sites for species reintroduction to rivers where the species historically occurred but is now locally extinct.M. margaritifera distribution is highly restricted at both the landscape and local habitat scale with the probability of occurrence peaking within narrow bands of the spectrum of variability available within each environmental parameter. Species occurrence was greatest at altitudes in the region of 50100 m above sea level. Whilst the species might be expected to prefer shallow upland streams due to the higher dissolved oxygen

content, resulting from faster water ow, it may be that such streams are subject to extremes of variability in water level and ow resulting in an increased threat of mussels being washed out (Hastie et al., 2001). It may also be that the salmonid hosts necessary for mussel reproduction are also restricted to rivers at these altitudes. However, the relationship between the ability of sh hosts to distribute themselves within a river and the dynamic forces that inuence the distribution of mussels and their ability to infect sh is extremely complex and difcult to explain. Predicted probability of species occurrence peaked between 5 15% carbon content, 1525% clay content, 020% silt content and was generally positively associated (in a more or less linear fashion) with sand content. Soil clay and sand content can be taken as inverse proxies for soil permeability; clay soils are generally impermeable with decreased water inltration and elevated surface runoff resulting in an increased risk of river channel siltation. Although clay particles can bind to chemicals they are also a source of pollutants when saturated as contaminated surface water leaches into ground water (Cruickshank, 1997). Conversely, sandy soils are highly permeable and infertile due to their poor ability to retain nutrients (Cruickshank, 1997). Permeable soil permits water to inltrate into soil moisture and groundwater, delaying surface runoff and buffering rivers against ooding events (Cruickshank, 1997). Soil carbon is a measure of organic processes such as humus deposition (Cruickshank, 1997) and is therefore associated with vegetated landscapes. Soils with a high level of organic carbon are vulnerable to nutrient leaching and may be associated with water column nitrication and river eutrophication both of which are likely to negatively impact mussel presence. Mussel occurrence was therefore highly inuenced by soil composition being associated with low densities of clay and high densities of sand. Poor water quality, dened by high levels of siltation, is a major cause of M. margaritifera populations failing to recruit due to the smothering of post-parasitic juvenile mussels (sterling et al., 2008). Consequently, soil silt content is likely to have a direct impact on M. margaritifera occurrence. It is important to make the distinction between suitable landscapes and suitable habitats. Whilst this study has identied

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(a)

(b) Ballinderry River

(c) Moyola River

Fig. 5. (a) Biogeographical model of landscape favourability for M. margaritifera occurrence throughout Northern Ireland providing a means by which to select areas suitable for (b) population supplementation of existing populations e.g. the Ballinderry River, Co. Tyrone, and (c) reintroduction of populations to rivers where the species historically occurred but is now extinct e.g. the Moyola River, Co. Londonderry. The mouth of each river is shown as an asterisk to indicate the direction of waterow.

suitable landscapes using broad-scale remotely-sensed GIS data it does not conclude that all stretches of river channel within favourable landscapes can support M. margaritifera populations. The ground-truthed local habitat model helps dene specic habitat niches within suitable landscapes that are likely to increase the success of any population supplementation and reintroduction programme. At the landscape scale, M. margaritifera was negatively associated with broad-leaved woodland and high carbon content soils but positively associated with the extent of mature riverbank broad-leaved trees at the local habitat scale indicating the impor-

tance of considering multiple spatial scales when assessing species occurrence. Riverbank trees shade the channel, reduce algal growth, stabilize the bank structure and provide cover for insects, which provide food for the sh hosts of M. margaritifera. The presence of mature trees also indicates that a section of river has not been disturbed or modied, for example, by bank re-sectioning or channel dredging. Many rivers have been heavily modied to prevent ooding of agricultural land (Cosgrove and Hastie, 2001), which is the predominant landuse type. M. margaritifera was also associated with liverworts/mosses/lichens and negatively associated with lamentous algae. These species indicate the extent to

C.D. Wilson et al. / Biological Conservation 144 (2011) 821829 Table 2 Principal components analyses describing (a) macrophytes, (b) riparian trees and (c) ow regime present at point transects surveyed for M. margaritifera. Principal component Variables Components PC1 (a) Macrophytes Liverworts, mosses and lichens Emergent reeds, sedges, rushes, grasses and horsetails Submerged linear leaved Submerged ne leaved Filamentous algae Cumulative% explained (b) Riparian trees Extent of riverbank trees Shading of bank Overhanging boughs Exposed bank side roots Underwater tree roots Fallen trees Large woody debris Cumulative% explained (c) Flow regime Broken standing waves Unbroken standing waves Rippled ow Smooth ow Cumulative% explained 0.738 0.165 0.010 0.014 0.807 24.5 0.375 0.834 0.758 0.865 0.775 0.306 0.090 40.0 0.906 0.907 0.161 0.220 43.0 PC2 0.020 0.629 0.051 0.879 0.065 48.0 0.368 0.081 0.146 0.107 0.034 0.880 0.891 65.0 0.194 0.187 0.910 0.982 85.4 PC3

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0.306 0.476 0.847 0.180 0.218 70.3

Consolidated Tree PC1 Macrophytes PC1 Trees PC2 Flow PC1 Macrophytes PC2 Macrophytes PC3 Flow PC2 Substrate 0.0 0.2 0.4 0.6 0.8

Independent variable

Factorial 0.889 0.297 -0.594 0.303 0.321 0.197 -0.234 0.169 0.031 0.071 0.009 0.032 -0.005 0.033 Factorial

1.0

Cumulative Akaike weight

Fig. 6. The relative importance of habitat parameters in explaining variance in M. margaritifera presence at point transect surveys. Variables were ranked in order of the sum of their Akaike weights (Rwi) within the top set of models, i.e. models with DAIC 6 2. Variables that were retained in the single best approximating model (i.e. that with the lowest AIC value) are in black and variables in grey are those that were included in all other models within the top set. The strength of the slopes for each covariate is indicated by the notation to the right and SE (mean b value and SE from top models).

35 30

% occurrence

25 20 15 10 5 0
bl e ck er e nd Si lt ob bl dr o ul d Sa eb rth /P Bo Be l/P C ea t

Fig. 7. Percentage occurrence bootstrapped 95% condence intervals of M. margaritifera in different substrate types.

which the river is shaded by adjacent trees and the levels of water eutrophication from agricultural runoff. Earlier studies have placed a great deal of emphasis on the importance of ow regime to M. margaritifera (Hastie et al., 2003), whereas results of the present study suggest that species presence was negatively related to stretches of river that were too fast, as determined by the presence of both broken and unbroken standing waves. Dynamism in ow regime may make river substrate unstable increasing the risk of mussels being washed out. The negative relationship with slope is similar to a nding by Arbuckle and Downing (2002) in relation to mussel density and species richness in the Mississippi River basin. Previous authors have suggested that one of the most important local features for M. margaritifera is the type and mobility of substratum (Beasley and Roberts, 1999; Cope et al., 2003; Hastie et al., 2003). Consolidated substrata enable mussels to remain burrowed during ooding events lessening the likelihood of becoming dislodged and washed into unsuitable habitat (Hastie et al., 2000). The importance of cobble substrata stabilised by ne sands and gravels to M. margaritifera has also been observed (Beasley and Roberts, 1999; Hastie et al., 2003). The present

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study also suggested that cobble and gravel/pebble substrata are preferred by M. margaritifera over other substratum types (Fig. 7). However, the substratum type was not identied in the habitat model as a signicant factor; this may be a statistical artefact of a small sample size subdivided by a seven-level factor. The IUCN (1998) recommends that the cause of a species decline be removed before any attempt at reintroduction is undertaken. Pearl shing was a major threat to M. margaritifera in Northern Ireland during the 19th and 20th centuries (Anonymous, 2005) but is now illegal and largely in decline or absent. The Northern Ireland Government must ensure that rivers meet European Water Framework Directive standards in terms of water quality being good or very good which has lead to a demonstrable increase in the conservation status of many rivers throughout the province (Anonymous, 2009). Economic benets from tourism have also increased the prevalence of salmonid aquaculture throughout Northern Ireland for game shing and angling, increasing the density of potential hosts for glochidial M. margaritifera. Consequently, the majority of direct causes of M. margaritifera are in the process of being mitigated. The Northern Ireland M. margaritifera Species Action Plan (Anonymous, 2005) aims to (i) maintain the range of existing populations, (ii) increase the size of each of the extant populations by 50% by 2010, (iii) re-establish a population in one former known locality for the species by 2015 and (iv) reestablish a population in a further suitable site by 2020. Our results highlight the importance of understanding the landscape and habitat niche of any species of conservation concern prior to translocation or reintroduction from captive breeding programmes. However, it must be remembered that species modelling is merely a tool for simplifying relationships with the highly complex environment of the wild. The current study excluded measures of water quality and host sh populations due to the difculty of incorporating explanatory measures at a suitable scale (both spatially and temporally). However, water quality must be of a high standard if M. margaritifera is to reproduce in the wild (Bauer, 1988; Skinner et al., 2003). Thus identifying reintroduction sites for this species is contingent on identifying high water quality, even within those areas identied as potentially suitable within our model. Moreover, sh host densities are integral in mussel recruitment (Ziuganov et al., 1994; Hastie and Young, 2003; Skinner et al., 2003; sterling et al., 2008). Although Geist et al. (2006) rarely observed a link between a lack of juvenile freshwater pearl mussels and a lack of suitable host sh, Ziuganov et al. (1994) suggests that long-term M. margaritifera maintenance depends upon a critical minimum salmonid host density of 0.2 sh per m2. Therefore, more work is required to verify suitable densities of host sh (via electroshing) at sites deemed suitable for reintroduction. Landscapes identied as favourable for M. margaritifera should be surveyed to ground-truth local suitability prior to any translocations or reintroductions. Local suitability, based on our ndings, should be based on the appropriate ow regime, tree lined banks and consolidated gravel or cobble substrata, while making sure to avoid sites where macrophytes indicative of eutrophication are present. Single species recovery is contingent on identifying, protecting or restoring areas of high conservation value. As a growing number of species restoration programmes involve captive breeding and release, a greater understanding of the landscape and habitat niche is required (Seddon et al., 2007). Moreover, restoration programmes are often contingent on re-establishing a species within its historic range (Anonymous, 2005), emphasizing the importance of the techniques used here in developing endangered species management.

Acknowledgements We thank Dr. Jane Preston and David McCann for assistance in the eld and Dr. Mathieu Lundy for advice on statistics and GIS. This project was funded by the Ballinderry Fish Hatchery (BFH) under a competitively-won tender from the Northern Ireland Environment Agency (NIEA). We would also like to thank two anonymous reviewers for comments on an earlier version of this manuscript. References
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