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Habitat features important for the conservation of the native crayfish Austropotamobius pallipes in Britain
ELSEVIER
0006-3207(95)00073-9
Biological Conservation 75 (1996) 239-246 Copyright © 1996 Elsevier Science Limited Printed in Great Britain. All rights reserved 0006-3207/96/$15.00+.00
HABITAT FEATURES IMPORTANT FOR THE CONSERVATION OF THE NATIVE CRAYFISH Austropotamobiuspallipes IN BRITAIN G. R. T. Smith, M. A. Learner, F. M. Slater & J. Foster* School of Pure and Applied Biology, University of Wales College of Cardiff, PO Box 915, Cardiff CF1 3TL, UK
(Received 27 January 1995; accepted 15 May 1995) larger predators such as trout Salmo trutta, chub Leuciscus cephalus and otter Lutra lutra (Foster & Slater, in press). Predation by fish is mainly on young crayfish (Stein, 1977), but crayfish of all sizes form a significant proportion of the diet of otters (McFadden & Fairley, 1984; Chanin, 1985; Slater & Rayner, 1993). Austropotamobius pallipes has been given protected status in Britain by the Wildlife and Countryside Act since 1986 (Holdich & Reeve, 1991) and it is now listed in Annex II of the European Union Habitats and Species Directive (1992) which requires Special Areas of Conservation to be set up to protect it. Consequently, the Joint Nature Conservation Committee has drawn up an action plan that includes the designation and management of protected areas (Palmer, 1994). Implicit in such designation is the need for a thorough understanding of the habitat requirements of A. pallipes so that suitable areas can be defined. The principal objective of the present study was to identify key habitat features that determine the success of A. pallipes populations in the upper catchments of the rivers Wye and Severn. These rivers were known to support good populations, are largely unaffected by crayfish plague, and are the largest relatively unpolluted and unmodified rivers in southern Britain (Ratcliffe, 1977). Additionally, the upper catchment of the Wye supports one of the highest densities of otters in southern Britain. A subsidiary objective was to obtain more up-to-date information about the status of crayfish populations in these catchments.
Abstract
The survival of Austropotamobius pallipes in Britain is threatened by habitat modification, pollution, exotic crayfish species, and crayfish plague. The status of A. pallipes in the catchments of the relatively unpolluted Upper Wye and Upper Severn were surveyed in July~August 1988. Sixty-two sites were visited and A. paUipes was found at 48% of them. The Llynfi and Teme sub-catchments were particularly well populated A large number of environmental variables was measured at each site and multiple regression techniques used to determine which of the variables most influenced crayfish abundance. It was concluded that, provided the water chemistry ensured crayfish survival the size of the crayfish populations was determined principally by the steepness of the channel banks, the presence of riparian shrubs and trees, and the extension of their roots into the water. The channel margins seemed to be especially important as nursery areas for the young crayfish. It is essential where A. pallipes is to be protected or re-established, that these bankside features are retained, enhanced or restored. Keywords." Austropotamobius pallipes, Malacostraca, crayfish conservation, River Wye, River Severn. INTRODUCTION
Austropotamobius pallipes (Lereboullet) is the only species of crayfish indigenous to the British Isles (Goddard & Hogger, 1986), and was until recently widely distributed in alkaline waters. However, a combination of habitat modification, such as river channelization (Hogger & Lowery, 1982), pollution, particularly from farms, competition from introduced alien crayfish (Holdich & Reeve, 1991), and the introduction in the early 1980s of crayfish plague Aphanomyces astaci (Alderman et al., 1984; Holdich & Reeve, 1991), seriously threatens its survival in Britain. The crayfish has an important functional role in freshwater ecosystems. It is a generalist feeder (Lorman & Magnuson, 1978) converting detritus, periphyton and macrophytes into a form readily exploited by
METHODS Study areas
The survey was carried out during July and August 1988 when 62 sites were visited. These sites, mainly in Powys, Wales, were spread amongst six sub-catchments with the addition of a few small tributaries associated directly with the River Wye (Table 1). The sub-catchments were chosen to reflect geological variation across the catchments of the Upper Wye and Severn. Thus, the most northerly sites (Banwy sub-catchment) were dominated by Silurian rocks, mainly of the Wenlock series (essentially limey shales). The Upper Severn sub-catchment is also influenced by the Wenlock series but it is most affected by the Llandovery series (also
Correspondence to M. A. Learner. Tel: 01222 874000; Fax: 01222 874305. *Present address: National Rivers Authority, Guildbourne House, Chatsworth Road, Worthing, Sussex, BN11 1LD, UK 239
G. R. T. Smith, M. A. Learner, F. M. Slater, J. Foster
240
Table 1. SampUng locations
Catchment
Sub-catchment
Severn
Banwy
1. SJ127097 (Cefnllwyd) 3. SJ098065 (Tributary) 5. SJ012097 (Gain) 7. SH962124 (Banwy)
Severn
Teme
9. SO395768 (Clun) 11. SO335729 (Teme) 13. SO206763 (Lawn) 15. SO277869 (Unk) 17. SO404738 (Teme) 41. SO357739 (Redlake) 43. SO420722 (Teme) 58. SO397777 (Tributary)
10. SO389748 (Redlake) 12. SO212783 (Teme) 14. SO300808 (Clun) 16. SO288827 (Unk) 18. SO407729 (Tributary) 42. SO398727 (Tributary) 44. SO393787 (Clun)
Severn
Upper Severn
19. SN883923 (Clewedog) 21. SN918864 (Clewedog) 23. SO009938 (Garno) 25. SO162947 (Mule)
20. SN917863 (Tributary) 22. SN026886 (Severn) 24. SO058931 (Tributary)
Wye
Lugg
26. SO287570 (Arrow) 31. SO426637 (Lugg) 33. SO316646 (Lugg) 35. SO213610 (Tributary)
27. SO391585 (Arrow) 32. SO368673 (Tributary) 34. SO345634 (Hindwell) 36. SO281607 (Hindwell)
Wye
Frome
29. SO613427 (Frome)
30. SO624433 (Loddon)
Wye
Llynfi
37. SO150344 (Llynfi) 39. SO148344 (Dulas) 45. SO127343 (Trwffrwd) 47. SO174378 (Three Cocks) 54. SO171374 (Velindre) 56. SO163365 (Llynfi) 59. SO133305 (Llynfi) 62. SO248135 (Cwy)
38. SO153338 (Ennig) 40. SO152344 (Ennig) 46. SO118358 (Trwffrwd)
28. SO167397 (Glasbury) 49. SO231427 (Dulas) 51. SO229451 (Clyro) 53. SO192418 (Moelfre)
48. SO202406 (Digedi) 50. SO252444 (Hardwick) 52. SO183411 (Cilkenni) 61. SO042551 (Dulas)
Wye
Small tributaries
Site number, National Grid Reference (River)
Silurian). The rivers draining these relatively basic strata are ionically richer than most rivers draining the Cambrian Mountains. The upper part of the Teme subcatchment is dominated by rocks of the Ludlow series (Silurian) which give way to Old Red Sandstone (Devonian) in the lower part of the sub-catchment. The Wye sub-catchments sampled south of the main river are all dominated by Old Red Sandstone. These rocks weather more easily than the Silurian formations and the rivers draining them have greater calcium concentrations and higher conductivities. They also carry more silt, which was especially noticeable in the Llynfi sub-catchment where the channel gradients were low. At each site a 15 m length of river was selected and various habitat features noted (Table 2). The choice of features was influenced by the habitat evaluation parameters used by Milner et al. (1985). Crayfish census Two methods were used at each site to assess crayfish abundance. In the mid-channel regions, where larger
2. SJ131099 (Banwy) 4. SJ076084 (Einion) 6. SH987133(Twrch) 8. SJ114076 (Banwy)
55. SO164366 (Pontithel) 57. SO136249 (Llynfi) 60. SO132305 (Glandwr)
stones occurred, the operator moved slowly upstream lifting stones carefully and placing any exposed crayfish into a bucket (Thomas & Ingle, 1971; Lilley et al., 1979). To be effective, this method requires relatively shallow, clear water. The maximum average water depth sampled in the present study was 64.8 cm. At three sites the mid-channel census had to be abandoned because a combination of silty conditions and depth of water was believed to be compromising sampling efficiency. In the marginal regions, where stones were generally smaller, kick sampling, a method widely used for sampling benthic macro-invertebrates, was employed. The operator gradually worked upstream along the margins of both banks kicking the substratum vigorously just ahead of a 10 mm mesh pond net. The same operator sampled the crayfish throughout the survey. The time taken to sample the 15 m reach at each site was noted for each method and converted to catch-per-unit-effort (CPUE), the unit of effort being 1 h. Each crayfish caught was sexed, the length of the
Conservation of the native crayfish in Britain
241
Table 2. Habitat evaluation variables
General features 1. Altitude 3. Stream order 5. Adjacent land use 7. Downstream physical barriers
2. Gradient 4. Aspect 6. Geology 8. Other barriers
Flow type 1. Torrent/cascade 3. Riffle/pool 5. Deep pool (>3 m)
2. Turbulent/broken riffle 4. Glide/run 6. Shallow pool (<3 m)
Bankside vegetation (proportion of bank length; dominant species; diversity) 1. Rushes/sedge 3. Shrubs (<2 m tall) 5. Evergreen trees
2. Grass 4. Deciduous trees 6. Other
Bank structure (proportion of bank length) 1. Tree roots 3. Overhang 5. Eroding 7. Other 9. Canopy cover (>0.5 m)
2. Undercut (>10 cm) 4. Vertical 6. Beach 8. Canopy cover (<0.5 m above water surface)
Aquatic vegetation (proportion of bed covered; species) 1. Angiosperms 3. Filamentous algae
2. Mosses
Channel substratum (proportion of bed) 1. Bedrock 3. Cobble 5. Fine gravel 7. Organic debris
2. Boulder 4. Coarse gravel 6. Sand/silt 8. Other
Channel dimensions (based on four transects) 1. Bank width Water quality 1. Temperature 5. Alkalinity 9. Potassium 13. Sulphate
2. Oxygen 6. Calcium 10. Aluminium 14. Chloride
2. Water depth (at three equidistant points) 3. pH 7. Magnesium 11. Nitrate 15. Ammonia
carapace measured, and claw regeneration, stage of moult, and any disease were noted. The carapace length from the tip of the rostrum (Rhodes & Holdich, 1979) was measured to the nearest 0-1 mm by means of a vernier calliper. Claw regeneration was evident from the presence of a smaller than normal cheliped. The absence of a claw was also recorded. The moult stage was based on four categories (Table 3) derived from a Table 3. Stage-of-moult classification
Stage
Characteristics
Intermoult Full rigidity of carapace. Pre-moult
Animal generally darker than in post-moult. Separation of epidermis from exoskeleton noticeable.
Moult
Animal feels like gelatin; only lasts a few hours.
Post-moult Animal lighter in colour. Postorbital ridge and cervical groove easily bent. Carapace often feels leathery.
4. Conductivity 8. Sodium 12. Phosphate
more complex system described by Stevenson (1975); our simplified version was easier to use in the field. Chemical samples At the completion of the survey (24/25 August) samples of water were collected in plastic bottles from every site. Samples for metal analysis were fixed with nitric acid and the other samples were kept in a refrigerator overnight before being analysed using standard methods at the Welsh Water Authority laboratory in Llanelli. Metal concentrations were measured using an Inductively Coupled Plasma Emission Spectrophotometer Model 200 (Thermo Electron Ltd, Warrington, Cheshire, UK) which reduces spectral interference compared with atomic absorption spectrophotometric techniques. Conductivity and pH were measured on site, the former by means of a Philips PW 9527 digital conductivity meter (accuracy +1 /~S cm ~) (Philips, Eindhoven, The Netherlands), and the latter by means of a Mettler DL 40RC Memotitrator Electrode (accuracy + 0-05 pH units) (Mettler Instruments, Greifensee, Switzerland). This electrode was also used to determine alkalinity.
G. R. T. Smith, M. A. Learner, F. M. Slater, J. Foster
242
Table 4. Frequency and abundance of crayfish
Catchment
Sub-catchment
Severn Severn Severn Wye Wye Wye Wye
Number of sites
Proportion with crayfish (%)
Average abundance at crayfish sites (Catch per Unit Effort)
8 15 7 8 2 14 8
25 53 0 62 0 71 62
7.9 30-8 -16"9 -30.6 14.8
Banwy Teme Upper Severn Lugg/Arrow Frome Llynfi Small tributaries
Statistical analysis Chi-square and Student-t tests were used in the analysis of discontinuous and continuous data respectively (Sokal & Rohlf, 1981). Multiple regression techniques were applied to the data obtained for sites where crayfish were present to produce a tentative model enabling crayfish abundance to be predicted from known habitat characteristics. 'Best sets' of predictor variables were selected using the STEPWISE facility for multiple regression. Forward selection, backward elimination, and conventional stepwise procedures were all used in the early stages of model building. The early methods were refined using a combination of knowledge and intuition to give models that were explicable and which could be applied and tested without undue difficulty. Multicollinearity was adjusted when detected by the Minitab program. Autocorrelation was checked by measuring the Durbin-Watson statistic. It was never a problem (DW statistic >2). Residuals were examined
30 (a)
u • (b) 15
nil. 1
9
17 25 33 Carapace length (ram)
41
49
Fig. 1. Comparison of carapace-length frequency distributions obtained from (a) stone-turning and (b) kick-sampling.
via a time-series plot: none of the predictor variables used in the models required transformation. RESULTS General features Crayfish were found at 30 of the 62 sites sampled (Table 4). No crayfish was found at the sites visited in the Upper Severn sub-catchment or in the Frome subcatchment. However, only two sites were sampled in the latter. The highest frequency of occurrence was obtained for the Llynfi sub-catchment, which also had a relatively high average abundance (Table 4). The results obtained for the stone-turning and kick-sampling techniques were averaged for each site before the average abundance per sub-catchment was calculated. The Teme sub-catchment had a similar average abundance of crayfish to the Llynfi sub-catchment but the frequency of occurrence was lower. All of the 616 individuals caught were Austropotamobius pallipes. The average CPUE for kick-sampling was 3.2 times that for stone-turning. Also, much higher numbers of smaller individuals were caught by kicksampling (Fig. 1). As these sampling methods were used in different parts of the channel, it is likely that these differences largely reflect crayfish distributional patterns, smaller (younger) individuals occurring more abundantly in the channel margins. However, these differences may also partly reflect differential selectivity between the methods; small crayfish are difficult to see and catch when stone-turning. Of the 616 individuals, 596 were sexed, the remainder being too young. Females significantly outnumbered males 1.2:l (Chi2 = 6.04; p < 0-05). Figure 2 shows that females predominated in almost all size classes. However, a comparison of the M:F sex ratio of immatures (0.9, n = 280) with that of adults (0.75, n = 316) shows that there was a disproportionate number of adult females. Individuals were classed as adult if the carapace length exceeded 24 mm. Previous work had shown A. pallipes to become sexually mature at 23-26 mm (Thomas & Ingle, 1971; Brown & Bowler, 1977; Woodlock & Reynolds, 1988). Application of Pratten's 0980) results to the carapace length-frequency data (Fig. l) obtained in the present
Conservation of the native crayfish in Britain
,--,, I
so I--
,4
?7
100[ 1M /
Sex ratio
.
.
.
.
.
.
(60-390) 6.4
L8
pH o
.
,3
Conductivity
114
70
243
(6.8 -8.5)
Alkalinity as CaCO3 2.
.
Ca I .
0
1-7
~
II
Fig. 2. Variation in sex ratio (M:F) with size (age).
.
.
(6.1-66.8) 21.7 ] (1.8-12.3) 26.7 ] (7.0-12.1) 6.5 ] (0.8-3.9) 0.37
.5
4
Mg 4.25.7
13
2
Na
0
12-15 20-23 2 8 - 3 1 36-3940+ Size class (carapace length (nun))
.
0.20.8
2.5
K 0.( AI
2
( - _ _
1
8
NO3
study indicates that some animals were at least 6 years old and that maturity was attained in the third year. Of the 616 crayfish examined, 24% had regenerated claws and 7% had missing claws. A higher proportion had regenerated/missing left claws (18%) than right claws (14%) but the difference was not significant at the 5% level. Regenerated claws were more prevalent amongst adults (28%) than amongst immatures (20%) (Chi 2 = 4.6; p < 0.05). The majority (c. 70%) of individuals at the nine sites where sample size exceeded 30 were in the pre-moult stage in August and about 10% were in the post-moult stage. About 2% of individuals were in the moult stage, but this jelly-like stage lasts for only a few hours. The sites with high numbers of crayfish were essentially in the sub-catchments Teme, Lugg and Llynfi. The proportions of individuals in the various moult stages were similar for these sites, indicating a cross-catchment synchronization of this process.
Disease Almost half (44%) of the sites which had crayfish populations were affected by porcelain disease Thelohania contejeani (Unestam, 1973). Although widespread, the incidence of the disease was low with only 2.9% of crayfish affected overall. The highest incidence was recorded at Site 56 (River Llynfi, 7.25%). Males were affected more often (4.1%) than females (2.1%) but the difference was not significant at the 5% level. The youngest crayfish with detectable symptoms of the disease was a male in its second year. A second disease widespread in the catchments investigated was rust, which is caused by a number of hostspecific fungi. This also affected 44% of the sites which had crayfish populations but, as with porcelain disease, the incidence was low with 2.6% of individuals affected overall. The incidence was higher amongst males (3%) than females (2.4%) but the difference was not significant (p > 0.05). There was no evidence that crayfish plague Aphanomyces astaci occurred at any of the sites, but as this disease can eliminate a population quickly its occurrence may be missed.
PO4 SO 4
0.001 ~ 5.2 8.4
0.59
0.22
23.6
44.9
~
0.01 0.05 NH4 l l " - " - 5 8 CI 7]
1
2 5
1 ]
0.32 4 23
31
Fig. 3. The ranges of concentration over which crayfish were found (black) compared with the range for all sites. Values within the bars denote the number of sites with concentrations that were more or less than the crayfish range. Sixty-two sites were sampled. The values in parentheses are the ranges over which crayfish were recorded by Lilley et al. (1979). Units are mg litre 1 except for conductivity (/xS cm-I at 20°C) and pH.
Habitat-abundance relationships The range of chemical values over which crayfish populations were recorded in comparison with the range of values for all the sites sampled is given in Fig. 3. The relatively high number of sites without crayfish at the lower concentrations of calcium, magnesium, sodium and potassium suggests that A. pallipes may be unable to survive in habitats where these ions are in low concentration. In the Upper Wye and Severn catchments these sites also generally had a low conductivity and an acid pH. Product-moment regression analysis gave a poor linear relationship between the above-mentioned chemical variables and crayfish abundance (CPUE), the highest R 2 value obtained (3.2%) being that for conductivity. Amongst the remaining chemical variables, higher R 2 values were obtained for phosphate and chloride concentrations but these were still low (7%). It seems that once a threshold concentration is exceeded the chemistry of the water within the Upper Wye and Severn catchments had relatively little influence on crayfish abundance. Other factors are clearly much more important. Of those measured in the present study, three showed strong positive relationships (p < 0.01) with crayfish abundance: the proportion of vertical bank present (R 2 = 53%), the proportion of the channel width overhung by a plant canopy that was more than 0.5 m above the water surface (R 2 = 43.9%), and the proportion of bank length with tree root systems projecting into the water (R 2 = 38.2), all within
244
G. R. T. Smith, M. A. Learner, F. M. Slater, ,1. Foster
a 15 m length of channel. Multiple regression analysis showed that the combined effect of these three variables accounted for 71% of the variability in crayfish abundance. The relationship obtained was stronger using the kick-sampling data so only these data are presented. CPUE = 2.02 + 0.96 (Tree Roots) + 0.478 (Canopy) + 0.385 (Vertical Bank); (R 2 = 71%; F (3,15) = 12.26; p < 0.001). As all the variables are positive, any increase in their proportion should stimulate an increase in crayfish population. The addition of altitude and the proportion of grass in the bankside vegetation as predictive variables increased the R 2 value to 78%. CPUE = 27.2 + 0.358 (Canopy) + 0.324 (Vertical Bank) + 0-244 (Grass) + 0.234 (Tree Roots) + 0-147 (Altitude); (R 2 = 78%; F (5,12) -- 8.53; p < 0.01). DISCUSSION Lilley et al. (1979) surveyed 103 sites on 57 streams and rivers draining the Upper Wye catchment in 1977/78 using the stone-turning technique. They found A. pallipes to be distributed widely in the Llynfi (50% of sites had crayfish), Lugg/Arrow (29%) and Irfon (31%) sub-catchments, but it was recorded from two sites only on the main river and was absent from the Ithon sub-catchment. The present study concentrated on the Llynfi and Lugg/Arrow sub-catchments and, in many cases, different sites were used so a direct comparison is not possible. Nevertheless, the present study suggests that the crayfish populations in the Llynfi system remained strong and also demonstrated the presence of crayfish in the River Lugg system upstream of the Lugg/Arrow confluence; Lilley et aL (1979) did not record them at any of the nine sites they sampled. The present study also showed that good populations of A. pallipes existed in the River Teme system in the Upper Severn catchment. There was a preponderance of female A. pallipes in the Upper Severn and Wye catchments. A similar observation had been made for the Wye about 10 years earlier (Lilley et al., 1979). Although other investigators working in different catchments have also recorded a preponderance of females (Brown & Brewis, 1979), this is not always the case (Brown & Bowler, 1977). The present data suggest that the M : F ratio is influenced by the age structure of the population (Fig. 2), so that in the Severn and Wye catchments the better survival of females than males following sexual maturity results in an overall sex ratio less than one. About 30% of the crayfish examined in the present study had either regenerating or missing chelipeds. The claw is very important in interspecific and intraspecific interactions. Stein (1976) has shown that chela size is the dominant factor determining the outcome of attacks by predators, aggressive encounters and attempts to copulate. The high incidence of individuals in the present study that had lost a claw indicates that it is a frequent occurrence.
The moulting of A. pallipes was synchronous within and amongst sites in the Upper Wye and Upper Severn catchments. This phenomenon is well known and reduces mortality from cannibalism. That synchrony occurred not only within sites but also amongst them suggests that A. pallipes moulting pattern is affected less by local conditions than by one or more environmental factors that operate on a broader geographical scale. This accords with Quackenbush (1986), who suggested that photoperiod is probably the principal variable that controls moulting synchronicity. Porcelain disease is the principal disease of A. pallipes, apart from plague, and causes death within several months to 2 years of infection (Vey et al., 1975; Bowler & Brown, 1977). This disease was widespread in the Upper Wye and Upper Severn catchments but at a low level of incidence (2.9%, n = 616). This value is close to the 3.4% incidence reported by Lilley et aL (1979) for the Upper Wye catchment in 1977, and indicates a fairly constant level of infection. Higher incidences than this have been reported from other areas of Britain (Pixell-Goodrich, 1956; Holdich et al., 1978) but comparison is confounded by marked differences in the extent and intensity of the studies. In the present study, the highest incidence recorded at a site was 7.25%. This is more than twice the overall incidence recorded. This site on the River Llynfi also had the highest crayfish abundance, which accords with Bowler and Brown's (1977) observations that the incidence of porcelain disease increases with increasing crayfish density. The present study relied on visual inspection of crayfish in the field to detect symptoms of porcelain disease and may therefore have underestimated the true incidence. O'Keefe and Reynolds (1983) used visual inspection in the field as well as microscopic examination and concluded that the actual incidence of the disease in the populations they studied was about twice that indicated by field inspection alone. The smallest individual with clear symptoms of porcelain disease observed in the present study was a male (carapace length 15-6 mm), probably in its second year (Pratten, 1980). In contrast, the youngest individual with the disease observed by O'Keefe and Reynolds (1983) was in its fifth year. Too few data are available to determine whether the earlier infection of crayfish observed in the present study is exceptional. Rust disease was also widespread in the Upper Wye and Upper Severn catchments but as with porcelain disease the incidence was low (2-6%). Lilley et aL (1979) in their study of crayfish in the Upper Wye catchment do not appear to have looked for rust disease so it is not possible to comment on possible temporal changes. O'Keefe and Reynolds (1983) recorded a significantly higher incidence (p < 0.05) amongst males than amongst females in a lake population of A. pallipes. We also found a higher incidence of rust disease amongst males (3%) than amongst females (2.4%) but the difference was not statistically significant. Our study also indicated a higher incidence of porcelain disease amongst males, though again not statistically significant.
Conservation of the native crayfish in Britain The greater susceptibility of males to disease, if confinned, would partly account for the low male:female sex ratio observed for the Wye/Severn populations. Curiously, no individual was found infected by both porcelain and rust disease but whether this is because infection by one disease modifies the animal's behaviour or physiology, so reducing the likelihood of infection by the other disease, is not known. Although crayfish plague was not evident during the 1988 survey, it has been recorded since in the Lugg/Arrow system (Holdich & Reeve, 1991) and in the Upper Severn (D. M. Holdich, pers. comm.).
Habitat-abundance relationships Our results indicate that the architecture of the channel banks, the presence of bankside shrubs and trees, and the extension of their roots into the water, had a major influence on the abundance of A. pallipes. The importance of these riparian features is not entirely unexpected. The study area is largely one of high rainfall coupled with a relatively impermeable geology. This combination produces rapid fluctuations in flow. The highly ramified, fibrous nature of the tree roots provides excellent protection in times of high flow. Alder Alnus glutinosa roots and to a lesser extent those of willow Salix spp. and hazel Corylus avellana appeared to be particularly suitable. The structural complexity of the roots also provides crayfish with protection from predators. In conjunction with vertical or near-vertical banks, roots help produce undercuts favoured by the shade-seeking crayfish. Roots also act as debris-traps that retain leaf litter. Allochthonous leaves are a primary source of food for crayfish in many lotic systems (Momot, 1984) and are an important source of calcium. Thus, the combination of riparian vegetation, its roots and a vertical bank provides protection and food for crayfish. The present study indicates that these marginal regions provide important nursery areas for the younger crayfish. It is therefore essential in the management of river corridors where A. pallipes is to be protected or re-established that these bankside features are retained, enhanced or restored. A thorough understanding of the habitat requirements of A. pallipes is an essential component of any conservation strategy that is advocated by the Joint Nature Conservation Committee (Palmer, 1994). This ensures that effort is not wasted in attempting to introduce or reintroduce crayfish into unsuitable localities. Our model allows crayfish abundance to be predicted from measurements of a few easily assessed habitat features, and thus provides a clear basis for active conservation measures within our study area. However, further studies are needed to assess its wider applicability. ACKNOWLEDGEMENTS We are grateful to the then Welsh Water Authority laboratory at Llanelli for analysing the chemical sampies, and to Dr D. M. Holdich, University of Nottingham, for information on crayfish plague.
245
REFERENCES Alderman, D. J., Polglase, J., Frayling, M. & Hogger, J. B. (1984). Crayfish plague in Britain. £ Fish Diseases, 7, 401-5. Bowler, K. & Brown, D. J. (1977). Some aspects of the growth in the British freshwater crayfish, Austropotamobius pallipes (Lereboullet). Freshwater Crayfish, III, 295-308. Brown, D. J. & Bowler, K. (1977). A population study of the British freshwater crayfish Austropotamobius pallipes (Lereboullet). Freshwater Crayfish, III, 33-50. Brown, D. J. & Brewis, J. M. (1979). A critical look at trapping as a method of sampling a population of Austropotamobius pallipes (Lereboullet) in a mark and recapture study. Freshwater Crayfish, IV, 159-64. Chanin, P. (1985). The natural history of otters. Croom Helm, London. Foster, J. & Slater, F. M. (in press). A global review of crayfish predation with particular reference to Austropotamobius pallipes in the Welsh Wye in relation to plague. Freshwater Crayfish. Goddard, J. S. & Hogger, J. B. (1986). The current status and distribution of freshwater crayfish in Britain. Fld Stud., 6, 383-96. Hogger, J. B. & Lowery, R. S. (1982). The encouragement of freshwater crayfish populations by attention to the construction and maintenance of waterways. J. Inst. Water Engnrs & Scient., 36, 214--20. Holdich, D. M. & Reeve, I. D. (1991). Distribution of freshwater crayfish in the British Isles, with particular reference to crayfish plague, alien introductions and water quality. Aquat. Conserv.: Mar. & Freshwat. Ecosyst., 1, 139-58. Holdich, D. M., Jay, D. & Goddard, J. S. (1978). Crayfish in the British Isles. Aquaculture, 15, 91-7. Lilley, A. J., Brooker, M. P. & Edwards, R. W. (1979). The distribution of the crayfish, Austropotamobius pallipes (Lereboullet), in the upper Wye catchment, Wales. Nature in Wales, 16, 195-200. Lorman, J. G. & Magnuson, J. J. (1978). The role of crayfish in aquatic ecosystems. Fisheries, 3, 8-10. McFadden, Y, M. T. & Fairley, J. S. (1984). Food of otters (Lutra lutra L.) in an Irish limestone river system with special reference to the crayfish Austropotamobius pallipes. J. Life ScL, R. Dublin Soc., 5, 65-78. Milner, N. J., Hemsworth, R. J. & Jones, B. E. (1985). Habitat evaluation as a fisheries management tool. J. Fish Biol., 27, 85-108. Momot, W. T. (1984). Crayfish production: a reflection of community energetics. J. Crustac. Biol., 4, 35-53. O'Keefe, C. & Reynolds, J. D. (1983). The occurrence of crayfish diseases and their significance in Ireland. Freshwater Crayfish, V, 299-306. Palmer, M. (1994). Action plan for the conservation of the native freshwater crayfish Austropotamobius pallipes in the United Kingdom. JNCC Rep., No. 193. Peterborough. Pixell-Goodrich, H. P. (1956) Crayfish epidemics. Parasitology, 46, 480-3. Pratten, D. J. (1980). Growth in the crayfish Austropotamobius pallipes (Lereb.). Freshwat. Biol., 10, 401-12. Quackenbush, D. J. (1986). Crustacean endocrinology - - a review. Can. J. Fish. Aquat. ScL, 43, 2271-82. Ratcliffe, D. (1977). A nature conservation review, Vol 2. Site accounts. Cambridge University Press, Cambridge, Rhodes, C. P. & Holdich, D. M. (1979). On size and sexual dimorphism in Austropotamobius pallipes (Lereboullet). A step in assessing the commercial exploitation potential of the native British freshwater crayfish. Aquaculture, 17, 345-58. Slater, F. M. & Rayner, G. (1993). Austropotamobius pallipes in otter diet in the mid-Wye catchment of central Wales. Freshwater Crayfish, 9, 365-7. Sokal, R. R. & Rohlf, F. J. (1981). Biometry, 2nd edn. W. H. Freeman, New York.
246
G. R. T. Smith, M. A. Learner, F M. Slater, J. Foster
Stein, R. A. (1976). Sexual dimorphism in crayfish chelae, functional significance linked to reproductive activities. Can. J. Zool., 54, 220-7. Stein, R. A. (1977). Selective predation, optimal foraging, and the predator-prey interaction between fish and crayfish. Ecology, 58, 1237-53. Stevenson, J. R. (1975). The moulting cycle in crayfish: recognising the moulting stages, effects of ecxlysone, and changes during the cycle. Freshwater Crayfish, II, 255-69. Thomas, W. & Ingle, R. (1971). The nomenclature, bionomics and distribution of the crayfish, Austropotamobius
pailipes (Lereboullet) (Crustacea, Astacidae) in the British Isles. Essex Nat., 32, 349-60. Unestam, T. (1973). Significance of diseases on freshwater crayfish. Freshwater Crayfish, I, 135-50. Vey, A., Boemare, N. & Vago, C. (1975). Recherche sur les maladies bacteriennes de r6crevisse Austropotamobius pallipes. Freshwater Crayfish, II, 287-98. Woodlock, B. & Reynolds, J. D. (1988). Reproduction in an Irish lake population of the crayfish Austropotamobius pallipes (Lereboullet). Freshwat. Biol., 19, 79-86.
0006-3207(95)00073-9
Biological Conservation 75 (1996) 239-246 Copyright © 1996 Elsevier Science Limited Printed in Great Britain. All rights reserved 0006-3207/96/$15.00+.00
HABITAT FEATURES IMPORTANT FOR THE CONSERVATION OF THE NATIVE CRAYFISH Austropotamobiuspallipes IN BRITAIN G. R. T. Smith, M. A. Learner, F. M. Slater & J. Foster* School of Pure and Applied Biology, University of Wales College of Cardiff, PO Box 915, Cardiff CF1 3TL, UK
(Received 27 January 1995; accepted 15 May 1995) larger predators such as trout Salmo trutta, chub Leuciscus cephalus and otter Lutra lutra (Foster & Slater, in press). Predation by fish is mainly on young crayfish (Stein, 1977), but crayfish of all sizes form a significant proportion of the diet of otters (McFadden & Fairley, 1984; Chanin, 1985; Slater & Rayner, 1993). Austropotamobius pallipes has been given protected status in Britain by the Wildlife and Countryside Act since 1986 (Holdich & Reeve, 1991) and it is now listed in Annex II of the European Union Habitats and Species Directive (1992) which requires Special Areas of Conservation to be set up to protect it. Consequently, the Joint Nature Conservation Committee has drawn up an action plan that includes the designation and management of protected areas (Palmer, 1994). Implicit in such designation is the need for a thorough understanding of the habitat requirements of A. pallipes so that suitable areas can be defined. The principal objective of the present study was to identify key habitat features that determine the success of A. pallipes populations in the upper catchments of the rivers Wye and Severn. These rivers were known to support good populations, are largely unaffected by crayfish plague, and are the largest relatively unpolluted and unmodified rivers in southern Britain (Ratcliffe, 1977). Additionally, the upper catchment of the Wye supports one of the highest densities of otters in southern Britain. A subsidiary objective was to obtain more up-to-date information about the status of crayfish populations in these catchments.
Abstract
The survival of Austropotamobius pallipes in Britain is threatened by habitat modification, pollution, exotic crayfish species, and crayfish plague. The status of A. pallipes in the catchments of the relatively unpolluted Upper Wye and Upper Severn were surveyed in July~August 1988. Sixty-two sites were visited and A. paUipes was found at 48% of them. The Llynfi and Teme sub-catchments were particularly well populated A large number of environmental variables was measured at each site and multiple regression techniques used to determine which of the variables most influenced crayfish abundance. It was concluded that, provided the water chemistry ensured crayfish survival the size of the crayfish populations was determined principally by the steepness of the channel banks, the presence of riparian shrubs and trees, and the extension of their roots into the water. The channel margins seemed to be especially important as nursery areas for the young crayfish. It is essential where A. pallipes is to be protected or re-established, that these bankside features are retained, enhanced or restored. Keywords." Austropotamobius pallipes, Malacostraca, crayfish conservation, River Wye, River Severn. INTRODUCTION
Austropotamobius pallipes (Lereboullet) is the only species of crayfish indigenous to the British Isles (Goddard & Hogger, 1986), and was until recently widely distributed in alkaline waters. However, a combination of habitat modification, such as river channelization (Hogger & Lowery, 1982), pollution, particularly from farms, competition from introduced alien crayfish (Holdich & Reeve, 1991), and the introduction in the early 1980s of crayfish plague Aphanomyces astaci (Alderman et al., 1984; Holdich & Reeve, 1991), seriously threatens its survival in Britain. The crayfish has an important functional role in freshwater ecosystems. It is a generalist feeder (Lorman & Magnuson, 1978) converting detritus, periphyton and macrophytes into a form readily exploited by
METHODS Study areas
The survey was carried out during July and August 1988 when 62 sites were visited. These sites, mainly in Powys, Wales, were spread amongst six sub-catchments with the addition of a few small tributaries associated directly with the River Wye (Table 1). The sub-catchments were chosen to reflect geological variation across the catchments of the Upper Wye and Severn. Thus, the most northerly sites (Banwy sub-catchment) were dominated by Silurian rocks, mainly of the Wenlock series (essentially limey shales). The Upper Severn sub-catchment is also influenced by the Wenlock series but it is most affected by the Llandovery series (also
Correspondence to M. A. Learner. Tel: 01222 874000; Fax: 01222 874305. *Present address: National Rivers Authority, Guildbourne House, Chatsworth Road, Worthing, Sussex, BN11 1LD, UK 239
G. R. T. Smith, M. A. Learner, F. M. Slater, J. Foster
240
Table 1. SampUng locations
Catchment
Sub-catchment
Severn
Banwy
1. SJ127097 (Cefnllwyd) 3. SJ098065 (Tributary) 5. SJ012097 (Gain) 7. SH962124 (Banwy)
Severn
Teme
9. SO395768 (Clun) 11. SO335729 (Teme) 13. SO206763 (Lawn) 15. SO277869 (Unk) 17. SO404738 (Teme) 41. SO357739 (Redlake) 43. SO420722 (Teme) 58. SO397777 (Tributary)
10. SO389748 (Redlake) 12. SO212783 (Teme) 14. SO300808 (Clun) 16. SO288827 (Unk) 18. SO407729 (Tributary) 42. SO398727 (Tributary) 44. SO393787 (Clun)
Severn
Upper Severn
19. SN883923 (Clewedog) 21. SN918864 (Clewedog) 23. SO009938 (Garno) 25. SO162947 (Mule)
20. SN917863 (Tributary) 22. SN026886 (Severn) 24. SO058931 (Tributary)
Wye
Lugg
26. SO287570 (Arrow) 31. SO426637 (Lugg) 33. SO316646 (Lugg) 35. SO213610 (Tributary)
27. SO391585 (Arrow) 32. SO368673 (Tributary) 34. SO345634 (Hindwell) 36. SO281607 (Hindwell)
Wye
Frome
29. SO613427 (Frome)
30. SO624433 (Loddon)
Wye
Llynfi
37. SO150344 (Llynfi) 39. SO148344 (Dulas) 45. SO127343 (Trwffrwd) 47. SO174378 (Three Cocks) 54. SO171374 (Velindre) 56. SO163365 (Llynfi) 59. SO133305 (Llynfi) 62. SO248135 (Cwy)
38. SO153338 (Ennig) 40. SO152344 (Ennig) 46. SO118358 (Trwffrwd)
28. SO167397 (Glasbury) 49. SO231427 (Dulas) 51. SO229451 (Clyro) 53. SO192418 (Moelfre)
48. SO202406 (Digedi) 50. SO252444 (Hardwick) 52. SO183411 (Cilkenni) 61. SO042551 (Dulas)
Wye
Small tributaries
Site number, National Grid Reference (River)
Silurian). The rivers draining these relatively basic strata are ionically richer than most rivers draining the Cambrian Mountains. The upper part of the Teme subcatchment is dominated by rocks of the Ludlow series (Silurian) which give way to Old Red Sandstone (Devonian) in the lower part of the sub-catchment. The Wye sub-catchments sampled south of the main river are all dominated by Old Red Sandstone. These rocks weather more easily than the Silurian formations and the rivers draining them have greater calcium concentrations and higher conductivities. They also carry more silt, which was especially noticeable in the Llynfi sub-catchment where the channel gradients were low. At each site a 15 m length of river was selected and various habitat features noted (Table 2). The choice of features was influenced by the habitat evaluation parameters used by Milner et al. (1985). Crayfish census Two methods were used at each site to assess crayfish abundance. In the mid-channel regions, where larger
2. SJ131099 (Banwy) 4. SJ076084 (Einion) 6. SH987133(Twrch) 8. SJ114076 (Banwy)
55. SO164366 (Pontithel) 57. SO136249 (Llynfi) 60. SO132305 (Glandwr)
stones occurred, the operator moved slowly upstream lifting stones carefully and placing any exposed crayfish into a bucket (Thomas & Ingle, 1971; Lilley et al., 1979). To be effective, this method requires relatively shallow, clear water. The maximum average water depth sampled in the present study was 64.8 cm. At three sites the mid-channel census had to be abandoned because a combination of silty conditions and depth of water was believed to be compromising sampling efficiency. In the marginal regions, where stones were generally smaller, kick sampling, a method widely used for sampling benthic macro-invertebrates, was employed. The operator gradually worked upstream along the margins of both banks kicking the substratum vigorously just ahead of a 10 mm mesh pond net. The same operator sampled the crayfish throughout the survey. The time taken to sample the 15 m reach at each site was noted for each method and converted to catch-per-unit-effort (CPUE), the unit of effort being 1 h. Each crayfish caught was sexed, the length of the
Conservation of the native crayfish in Britain
241
Table 2. Habitat evaluation variables
General features 1. Altitude 3. Stream order 5. Adjacent land use 7. Downstream physical barriers
2. Gradient 4. Aspect 6. Geology 8. Other barriers
Flow type 1. Torrent/cascade 3. Riffle/pool 5. Deep pool (>3 m)
2. Turbulent/broken riffle 4. Glide/run 6. Shallow pool (<3 m)
Bankside vegetation (proportion of bank length; dominant species; diversity) 1. Rushes/sedge 3. Shrubs (<2 m tall) 5. Evergreen trees
2. Grass 4. Deciduous trees 6. Other
Bank structure (proportion of bank length) 1. Tree roots 3. Overhang 5. Eroding 7. Other 9. Canopy cover (>0.5 m)
2. Undercut (>10 cm) 4. Vertical 6. Beach 8. Canopy cover (<0.5 m above water surface)
Aquatic vegetation (proportion of bed covered; species) 1. Angiosperms 3. Filamentous algae
2. Mosses
Channel substratum (proportion of bed) 1. Bedrock 3. Cobble 5. Fine gravel 7. Organic debris
2. Boulder 4. Coarse gravel 6. Sand/silt 8. Other
Channel dimensions (based on four transects) 1. Bank width Water quality 1. Temperature 5. Alkalinity 9. Potassium 13. Sulphate
2. Oxygen 6. Calcium 10. Aluminium 14. Chloride
2. Water depth (at three equidistant points) 3. pH 7. Magnesium 11. Nitrate 15. Ammonia
carapace measured, and claw regeneration, stage of moult, and any disease were noted. The carapace length from the tip of the rostrum (Rhodes & Holdich, 1979) was measured to the nearest 0-1 mm by means of a vernier calliper. Claw regeneration was evident from the presence of a smaller than normal cheliped. The absence of a claw was also recorded. The moult stage was based on four categories (Table 3) derived from a Table 3. Stage-of-moult classification
Stage
Characteristics
Intermoult Full rigidity of carapace. Pre-moult
Animal generally darker than in post-moult. Separation of epidermis from exoskeleton noticeable.
Moult
Animal feels like gelatin; only lasts a few hours.
Post-moult Animal lighter in colour. Postorbital ridge and cervical groove easily bent. Carapace often feels leathery.
4. Conductivity 8. Sodium 12. Phosphate
more complex system described by Stevenson (1975); our simplified version was easier to use in the field. Chemical samples At the completion of the survey (24/25 August) samples of water were collected in plastic bottles from every site. Samples for metal analysis were fixed with nitric acid and the other samples were kept in a refrigerator overnight before being analysed using standard methods at the Welsh Water Authority laboratory in Llanelli. Metal concentrations were measured using an Inductively Coupled Plasma Emission Spectrophotometer Model 200 (Thermo Electron Ltd, Warrington, Cheshire, UK) which reduces spectral interference compared with atomic absorption spectrophotometric techniques. Conductivity and pH were measured on site, the former by means of a Philips PW 9527 digital conductivity meter (accuracy +1 /~S cm ~) (Philips, Eindhoven, The Netherlands), and the latter by means of a Mettler DL 40RC Memotitrator Electrode (accuracy + 0-05 pH units) (Mettler Instruments, Greifensee, Switzerland). This electrode was also used to determine alkalinity.
G. R. T. Smith, M. A. Learner, F. M. Slater, J. Foster
242
Table 4. Frequency and abundance of crayfish
Catchment
Sub-catchment
Severn Severn Severn Wye Wye Wye Wye
Number of sites
Proportion with crayfish (%)
Average abundance at crayfish sites (Catch per Unit Effort)
8 15 7 8 2 14 8
25 53 0 62 0 71 62
7.9 30-8 -16"9 -30.6 14.8
Banwy Teme Upper Severn Lugg/Arrow Frome Llynfi Small tributaries
Statistical analysis Chi-square and Student-t tests were used in the analysis of discontinuous and continuous data respectively (Sokal & Rohlf, 1981). Multiple regression techniques were applied to the data obtained for sites where crayfish were present to produce a tentative model enabling crayfish abundance to be predicted from known habitat characteristics. 'Best sets' of predictor variables were selected using the STEPWISE facility for multiple regression. Forward selection, backward elimination, and conventional stepwise procedures were all used in the early stages of model building. The early methods were refined using a combination of knowledge and intuition to give models that were explicable and which could be applied and tested without undue difficulty. Multicollinearity was adjusted when detected by the Minitab program. Autocorrelation was checked by measuring the Durbin-Watson statistic. It was never a problem (DW statistic >2). Residuals were examined
30 (a)
u • (b) 15
nil. 1
9
17 25 33 Carapace length (ram)
41
49
Fig. 1. Comparison of carapace-length frequency distributions obtained from (a) stone-turning and (b) kick-sampling.
via a time-series plot: none of the predictor variables used in the models required transformation. RESULTS General features Crayfish were found at 30 of the 62 sites sampled (Table 4). No crayfish was found at the sites visited in the Upper Severn sub-catchment or in the Frome subcatchment. However, only two sites were sampled in the latter. The highest frequency of occurrence was obtained for the Llynfi sub-catchment, which also had a relatively high average abundance (Table 4). The results obtained for the stone-turning and kick-sampling techniques were averaged for each site before the average abundance per sub-catchment was calculated. The Teme sub-catchment had a similar average abundance of crayfish to the Llynfi sub-catchment but the frequency of occurrence was lower. All of the 616 individuals caught were Austropotamobius pallipes. The average CPUE for kick-sampling was 3.2 times that for stone-turning. Also, much higher numbers of smaller individuals were caught by kicksampling (Fig. 1). As these sampling methods were used in different parts of the channel, it is likely that these differences largely reflect crayfish distributional patterns, smaller (younger) individuals occurring more abundantly in the channel margins. However, these differences may also partly reflect differential selectivity between the methods; small crayfish are difficult to see and catch when stone-turning. Of the 616 individuals, 596 were sexed, the remainder being too young. Females significantly outnumbered males 1.2:l (Chi2 = 6.04; p < 0-05). Figure 2 shows that females predominated in almost all size classes. However, a comparison of the M:F sex ratio of immatures (0.9, n = 280) with that of adults (0.75, n = 316) shows that there was a disproportionate number of adult females. Individuals were classed as adult if the carapace length exceeded 24 mm. Previous work had shown A. pallipes to become sexually mature at 23-26 mm (Thomas & Ingle, 1971; Brown & Bowler, 1977; Woodlock & Reynolds, 1988). Application of Pratten's 0980) results to the carapace length-frequency data (Fig. l) obtained in the present
Conservation of the native crayfish in Britain
,--,, I
so I--
,4
?7
100[ 1M /
Sex ratio
.
.
.
.
.
.
(60-390) 6.4
L8
pH o
.
,3
Conductivity
114
70
243
(6.8 -8.5)
Alkalinity as CaCO3 2.
.
Ca I .
0
1-7
~
II
Fig. 2. Variation in sex ratio (M:F) with size (age).
.
.
(6.1-66.8) 21.7 ] (1.8-12.3) 26.7 ] (7.0-12.1) 6.5 ] (0.8-3.9) 0.37
.5
4
Mg 4.25.7
13
2
Na
0
12-15 20-23 2 8 - 3 1 36-3940+ Size class (carapace length (nun))
.
0.20.8
2.5
K 0.( AI
2
( - _ _
1
8
NO3
study indicates that some animals were at least 6 years old and that maturity was attained in the third year. Of the 616 crayfish examined, 24% had regenerated claws and 7% had missing claws. A higher proportion had regenerated/missing left claws (18%) than right claws (14%) but the difference was not significant at the 5% level. Regenerated claws were more prevalent amongst adults (28%) than amongst immatures (20%) (Chi 2 = 4.6; p < 0.05). The majority (c. 70%) of individuals at the nine sites where sample size exceeded 30 were in the pre-moult stage in August and about 10% were in the post-moult stage. About 2% of individuals were in the moult stage, but this jelly-like stage lasts for only a few hours. The sites with high numbers of crayfish were essentially in the sub-catchments Teme, Lugg and Llynfi. The proportions of individuals in the various moult stages were similar for these sites, indicating a cross-catchment synchronization of this process.
Disease Almost half (44%) of the sites which had crayfish populations were affected by porcelain disease Thelohania contejeani (Unestam, 1973). Although widespread, the incidence of the disease was low with only 2.9% of crayfish affected overall. The highest incidence was recorded at Site 56 (River Llynfi, 7.25%). Males were affected more often (4.1%) than females (2.1%) but the difference was not significant at the 5% level. The youngest crayfish with detectable symptoms of the disease was a male in its second year. A second disease widespread in the catchments investigated was rust, which is caused by a number of hostspecific fungi. This also affected 44% of the sites which had crayfish populations but, as with porcelain disease, the incidence was low with 2.6% of individuals affected overall. The incidence was higher amongst males (3%) than females (2.4%) but the difference was not significant (p > 0.05). There was no evidence that crayfish plague Aphanomyces astaci occurred at any of the sites, but as this disease can eliminate a population quickly its occurrence may be missed.
PO4 SO 4
0.001 ~ 5.2 8.4
0.59
0.22
23.6
44.9
~
0.01 0.05 NH4 l l " - " - 5 8 CI 7]
1
2 5
1 ]
0.32 4 23
31
Fig. 3. The ranges of concentration over which crayfish were found (black) compared with the range for all sites. Values within the bars denote the number of sites with concentrations that were more or less than the crayfish range. Sixty-two sites were sampled. The values in parentheses are the ranges over which crayfish were recorded by Lilley et al. (1979). Units are mg litre 1 except for conductivity (/xS cm-I at 20°C) and pH.
Habitat-abundance relationships The range of chemical values over which crayfish populations were recorded in comparison with the range of values for all the sites sampled is given in Fig. 3. The relatively high number of sites without crayfish at the lower concentrations of calcium, magnesium, sodium and potassium suggests that A. pallipes may be unable to survive in habitats where these ions are in low concentration. In the Upper Wye and Severn catchments these sites also generally had a low conductivity and an acid pH. Product-moment regression analysis gave a poor linear relationship between the above-mentioned chemical variables and crayfish abundance (CPUE), the highest R 2 value obtained (3.2%) being that for conductivity. Amongst the remaining chemical variables, higher R 2 values were obtained for phosphate and chloride concentrations but these were still low (7%). It seems that once a threshold concentration is exceeded the chemistry of the water within the Upper Wye and Severn catchments had relatively little influence on crayfish abundance. Other factors are clearly much more important. Of those measured in the present study, three showed strong positive relationships (p < 0.01) with crayfish abundance: the proportion of vertical bank present (R 2 = 53%), the proportion of the channel width overhung by a plant canopy that was more than 0.5 m above the water surface (R 2 = 43.9%), and the proportion of bank length with tree root systems projecting into the water (R 2 = 38.2), all within
244
G. R. T. Smith, M. A. Learner, F. M. Slater, ,1. Foster
a 15 m length of channel. Multiple regression analysis showed that the combined effect of these three variables accounted for 71% of the variability in crayfish abundance. The relationship obtained was stronger using the kick-sampling data so only these data are presented. CPUE = 2.02 + 0.96 (Tree Roots) + 0.478 (Canopy) + 0.385 (Vertical Bank); (R 2 = 71%; F (3,15) = 12.26; p < 0.001). As all the variables are positive, any increase in their proportion should stimulate an increase in crayfish population. The addition of altitude and the proportion of grass in the bankside vegetation as predictive variables increased the R 2 value to 78%. CPUE = 27.2 + 0.358 (Canopy) + 0.324 (Vertical Bank) + 0-244 (Grass) + 0.234 (Tree Roots) + 0-147 (Altitude); (R 2 = 78%; F (5,12) -- 8.53; p < 0.01). DISCUSSION Lilley et al. (1979) surveyed 103 sites on 57 streams and rivers draining the Upper Wye catchment in 1977/78 using the stone-turning technique. They found A. pallipes to be distributed widely in the Llynfi (50% of sites had crayfish), Lugg/Arrow (29%) and Irfon (31%) sub-catchments, but it was recorded from two sites only on the main river and was absent from the Ithon sub-catchment. The present study concentrated on the Llynfi and Lugg/Arrow sub-catchments and, in many cases, different sites were used so a direct comparison is not possible. Nevertheless, the present study suggests that the crayfish populations in the Llynfi system remained strong and also demonstrated the presence of crayfish in the River Lugg system upstream of the Lugg/Arrow confluence; Lilley et aL (1979) did not record them at any of the nine sites they sampled. The present study also showed that good populations of A. pallipes existed in the River Teme system in the Upper Severn catchment. There was a preponderance of female A. pallipes in the Upper Severn and Wye catchments. A similar observation had been made for the Wye about 10 years earlier (Lilley et al., 1979). Although other investigators working in different catchments have also recorded a preponderance of females (Brown & Brewis, 1979), this is not always the case (Brown & Bowler, 1977). The present data suggest that the M : F ratio is influenced by the age structure of the population (Fig. 2), so that in the Severn and Wye catchments the better survival of females than males following sexual maturity results in an overall sex ratio less than one. About 30% of the crayfish examined in the present study had either regenerating or missing chelipeds. The claw is very important in interspecific and intraspecific interactions. Stein (1976) has shown that chela size is the dominant factor determining the outcome of attacks by predators, aggressive encounters and attempts to copulate. The high incidence of individuals in the present study that had lost a claw indicates that it is a frequent occurrence.
The moulting of A. pallipes was synchronous within and amongst sites in the Upper Wye and Upper Severn catchments. This phenomenon is well known and reduces mortality from cannibalism. That synchrony occurred not only within sites but also amongst them suggests that A. pallipes moulting pattern is affected less by local conditions than by one or more environmental factors that operate on a broader geographical scale. This accords with Quackenbush (1986), who suggested that photoperiod is probably the principal variable that controls moulting synchronicity. Porcelain disease is the principal disease of A. pallipes, apart from plague, and causes death within several months to 2 years of infection (Vey et al., 1975; Bowler & Brown, 1977). This disease was widespread in the Upper Wye and Upper Severn catchments but at a low level of incidence (2.9%, n = 616). This value is close to the 3.4% incidence reported by Lilley et aL (1979) for the Upper Wye catchment in 1977, and indicates a fairly constant level of infection. Higher incidences than this have been reported from other areas of Britain (Pixell-Goodrich, 1956; Holdich et al., 1978) but comparison is confounded by marked differences in the extent and intensity of the studies. In the present study, the highest incidence recorded at a site was 7.25%. This is more than twice the overall incidence recorded. This site on the River Llynfi also had the highest crayfish abundance, which accords with Bowler and Brown's (1977) observations that the incidence of porcelain disease increases with increasing crayfish density. The present study relied on visual inspection of crayfish in the field to detect symptoms of porcelain disease and may therefore have underestimated the true incidence. O'Keefe and Reynolds (1983) used visual inspection in the field as well as microscopic examination and concluded that the actual incidence of the disease in the populations they studied was about twice that indicated by field inspection alone. The smallest individual with clear symptoms of porcelain disease observed in the present study was a male (carapace length 15-6 mm), probably in its second year (Pratten, 1980). In contrast, the youngest individual with the disease observed by O'Keefe and Reynolds (1983) was in its fifth year. Too few data are available to determine whether the earlier infection of crayfish observed in the present study is exceptional. Rust disease was also widespread in the Upper Wye and Upper Severn catchments but as with porcelain disease the incidence was low (2-6%). Lilley et aL (1979) in their study of crayfish in the Upper Wye catchment do not appear to have looked for rust disease so it is not possible to comment on possible temporal changes. O'Keefe and Reynolds (1983) recorded a significantly higher incidence (p < 0.05) amongst males than amongst females in a lake population of A. pallipes. We also found a higher incidence of rust disease amongst males (3%) than amongst females (2.4%) but the difference was not statistically significant. Our study also indicated a higher incidence of porcelain disease amongst males, though again not statistically significant.
Conservation of the native crayfish in Britain The greater susceptibility of males to disease, if confinned, would partly account for the low male:female sex ratio observed for the Wye/Severn populations. Curiously, no individual was found infected by both porcelain and rust disease but whether this is because infection by one disease modifies the animal's behaviour or physiology, so reducing the likelihood of infection by the other disease, is not known. Although crayfish plague was not evident during the 1988 survey, it has been recorded since in the Lugg/Arrow system (Holdich & Reeve, 1991) and in the Upper Severn (D. M. Holdich, pers. comm.).
Habitat-abundance relationships Our results indicate that the architecture of the channel banks, the presence of bankside shrubs and trees, and the extension of their roots into the water, had a major influence on the abundance of A. pallipes. The importance of these riparian features is not entirely unexpected. The study area is largely one of high rainfall coupled with a relatively impermeable geology. This combination produces rapid fluctuations in flow. The highly ramified, fibrous nature of the tree roots provides excellent protection in times of high flow. Alder Alnus glutinosa roots and to a lesser extent those of willow Salix spp. and hazel Corylus avellana appeared to be particularly suitable. The structural complexity of the roots also provides crayfish with protection from predators. In conjunction with vertical or near-vertical banks, roots help produce undercuts favoured by the shade-seeking crayfish. Roots also act as debris-traps that retain leaf litter. Allochthonous leaves are a primary source of food for crayfish in many lotic systems (Momot, 1984) and are an important source of calcium. Thus, the combination of riparian vegetation, its roots and a vertical bank provides protection and food for crayfish. The present study indicates that these marginal regions provide important nursery areas for the younger crayfish. It is therefore essential in the management of river corridors where A. pallipes is to be protected or re-established that these bankside features are retained, enhanced or restored. A thorough understanding of the habitat requirements of A. pallipes is an essential component of any conservation strategy that is advocated by the Joint Nature Conservation Committee (Palmer, 1994). This ensures that effort is not wasted in attempting to introduce or reintroduce crayfish into unsuitable localities. Our model allows crayfish abundance to be predicted from measurements of a few easily assessed habitat features, and thus provides a clear basis for active conservation measures within our study area. However, further studies are needed to assess its wider applicability. ACKNOWLEDGEMENTS We are grateful to the then Welsh Water Authority laboratory at Llanelli for analysing the chemical sampies, and to Dr D. M. Holdich, University of Nottingham, for information on crayfish plague.
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REFERENCES Alderman, D. J., Polglase, J., Frayling, M. & Hogger, J. B. (1984). Crayfish plague in Britain. £ Fish Diseases, 7, 401-5. Bowler, K. & Brown, D. J. (1977). Some aspects of the growth in the British freshwater crayfish, Austropotamobius pallipes (Lereboullet). Freshwater Crayfish, III, 295-308. Brown, D. J. & Bowler, K. (1977). A population study of the British freshwater crayfish Austropotamobius pallipes (Lereboullet). Freshwater Crayfish, III, 33-50. Brown, D. J. & Brewis, J. M. (1979). A critical look at trapping as a method of sampling a population of Austropotamobius pallipes (Lereboullet) in a mark and recapture study. Freshwater Crayfish, IV, 159-64. Chanin, P. (1985). The natural history of otters. Croom Helm, London. Foster, J. & Slater, F. M. (in press). A global review of crayfish predation with particular reference to Austropotamobius pallipes in the Welsh Wye in relation to plague. Freshwater Crayfish. Goddard, J. S. & Hogger, J. B. (1986). The current status and distribution of freshwater crayfish in Britain. Fld Stud., 6, 383-96. Hogger, J. B. & Lowery, R. S. (1982). The encouragement of freshwater crayfish populations by attention to the construction and maintenance of waterways. J. Inst. Water Engnrs & Scient., 36, 214--20. Holdich, D. M. & Reeve, I. D. (1991). Distribution of freshwater crayfish in the British Isles, with particular reference to crayfish plague, alien introductions and water quality. Aquat. Conserv.: Mar. & Freshwat. Ecosyst., 1, 139-58. Holdich, D. M., Jay, D. & Goddard, J. S. (1978). Crayfish in the British Isles. Aquaculture, 15, 91-7. Lilley, A. J., Brooker, M. P. & Edwards, R. W. (1979). The distribution of the crayfish, Austropotamobius pallipes (Lereboullet), in the upper Wye catchment, Wales. Nature in Wales, 16, 195-200. Lorman, J. G. & Magnuson, J. J. (1978). The role of crayfish in aquatic ecosystems. Fisheries, 3, 8-10. McFadden, Y, M. T. & Fairley, J. S. (1984). Food of otters (Lutra lutra L.) in an Irish limestone river system with special reference to the crayfish Austropotamobius pallipes. J. Life ScL, R. Dublin Soc., 5, 65-78. Milner, N. J., Hemsworth, R. J. & Jones, B. E. (1985). Habitat evaluation as a fisheries management tool. J. Fish Biol., 27, 85-108. Momot, W. T. (1984). Crayfish production: a reflection of community energetics. J. Crustac. Biol., 4, 35-53. O'Keefe, C. & Reynolds, J. D. (1983). The occurrence of crayfish diseases and their significance in Ireland. Freshwater Crayfish, V, 299-306. Palmer, M. (1994). Action plan for the conservation of the native freshwater crayfish Austropotamobius pallipes in the United Kingdom. JNCC Rep., No. 193. Peterborough. Pixell-Goodrich, H. P. (1956) Crayfish epidemics. Parasitology, 46, 480-3. Pratten, D. J. (1980). Growth in the crayfish Austropotamobius pallipes (Lereb.). Freshwat. Biol., 10, 401-12. Quackenbush, D. J. (1986). Crustacean endocrinology - - a review. Can. J. Fish. Aquat. ScL, 43, 2271-82. Ratcliffe, D. (1977). A nature conservation review, Vol 2. Site accounts. Cambridge University Press, Cambridge, Rhodes, C. P. & Holdich, D. M. (1979). On size and sexual dimorphism in Austropotamobius pallipes (Lereboullet). A step in assessing the commercial exploitation potential of the native British freshwater crayfish. Aquaculture, 17, 345-58. Slater, F. M. & Rayner, G. (1993). Austropotamobius pallipes in otter diet in the mid-Wye catchment of central Wales. Freshwater Crayfish, 9, 365-7. Sokal, R. R. & Rohlf, F. J. (1981). Biometry, 2nd edn. W. H. Freeman, New York.
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Stein, R. A. (1976). Sexual dimorphism in crayfish chelae, functional significance linked to reproductive activities. Can. J. Zool., 54, 220-7. Stein, R. A. (1977). Selective predation, optimal foraging, and the predator-prey interaction between fish and crayfish. Ecology, 58, 1237-53. Stevenson, J. R. (1975). The moulting cycle in crayfish: recognising the moulting stages, effects of ecxlysone, and changes during the cycle. Freshwater Crayfish, II, 255-69. Thomas, W. & Ingle, R. (1971). The nomenclature, bionomics and distribution of the crayfish, Austropotamobius
pailipes (Lereboullet) (Crustacea, Astacidae) in the British Isles. Essex Nat., 32, 349-60. Unestam, T. (1973). Significance of diseases on freshwater crayfish. Freshwater Crayfish, I, 135-50. Vey, A., Boemare, N. & Vago, C. (1975). Recherche sur les maladies bacteriennes de r6crevisse Austropotamobius pallipes. Freshwater Crayfish, II, 287-98. Woodlock, B. & Reynolds, J. D. (1988). Reproduction in an Irish lake population of the crayfish Austropotamobius pallipes (Lereboullet). Freshwat. Biol., 19, 79-86.