Hydrobiologia 234: 1-6, 1992. O 1992 Kluwer Academic Publishers. Printed in Belgium.

Ecological impact of crayfish plague in Ireland

Milton Matthews & Julian D. Reynolds Department of Zoology, University of Dublin, Trinity College, Dublin 2, Ireland

Received 1 August 1989; in revised form 19 June 1991; accepted 7 July 1991

Key words: Crayfish, Austropotamobius, Chara, grazing, vegetation

Abstract

Freshwater crayfish are key members of aquatic communities due to their large size and abundance. Although most commonly regarded as herbivores and detritivores, they are also selective predators. The crayfish plague fungus Aphanomyces astaci (Schikora) led to the elimination of a stock of white-clawed crayfish, Austropotamobius pallipes (Lereboullet) from Lough Lene, Co. Westmeath, in 1987. Samples taken of the flora and benthic communities of two Irish lakes, one (Lough Bane) formerly containing crayfish and the other (Lough Lene) immediately following a plague outbreak, were compared to sim- ilar samples taken a year later and ecological shifts were noted and compared to laboratory feeding results. Over time, Chara strands increased in mean length, and molluscs became more abundant.

Introduction

Freshwater crayfish by their size and population structure are important trophic components of freshwater ecosystems (Momot, 1984; Goddard, 1988). Lorman & Magnuson (1978) and Momot et al. (1978) suggest that crayfish may be ecolog- ically important at three different levels: As detritivores they hasten the transformation of allochthonous energy sources into biomass of consumers; as herbivores, they are important converters of plant tissue into animal; and as adaptable predators, they may maintain commu- nity stability and structure by selectively preda- ting upon particular species as they become abun- dant.

Nonetheless, there is little published informa- tion on carnivory (Goddard, 1988) and crayfish tend to be regarded primarily as herbivores/ detritivores (Abrahamsson, 1966; Magnuson et al., 1975). Several American crayfish species

are known to reduce aquatic macrophyte biomass in lakes through grazing (Dean, 1969; Saiki & Tash, 1979). Lodge & Lorman (1987) have demonstrated that macrophyte abundance and species richness was reduced through selective grazing by Orconectes rusticus (Girard), and macrophyte-associated snails also decreased in abundance. At densities greater than five crayfish per square metre all macrophytes were eventually eliminated, although about one third of the vegetation destroyed was not consumed. Pacfas- tacus leniusculus (Dana) at mean densities of 1.4 per m2 in Lake Tahoe (Abrahamsson & Gold- man, 1970) also checked increases in benthic pri- mary productivity by grazing on periphyton and macrophyte vegetation (Flint & Goldman, 1975). Enclosed Procambarus clarkii (Girard) reduced Potamogeton pectinatus (L.) in Californian marshes in proportion to their density, while ex- closures allowed plant regrowth to occur (Femi- nella & Resh, 1989). In Europe, the importance

ofAstacus astacus L. in controlling aquatic macro- phytes was demonstrated by Abrahamsson (1966) and Unestam (1973) who noted over- growth of many Swedish lakes by vegetation fol- lowing the elimination of crayfish populations by crayfish plague. The ecological impact of Austro- potamobius pallipes (Lereboullet) on lake vegeta- tion is undocumented, but both invertebrates and aquatic plants are taken in captivity (Reynolds, 1978) and are important food categories in lake populations of this crayfish species in Ireland (O'Keeffe, 1986).

Although A. pallipes is still widespread in Ire- land (Lucey & McGarrigle, 1987), several mid- lands lake populations have recently disappeared. In July 1987 no crayfish could be found in Lough Bane or in several neighbouring lakes, all reported to hold crayfish in the recent past (Reynolds, 1982; Woodlock & Reynolds, 1988). In early October 1987 crayfish mortalities were noted in Lough Lene (P. Ashe, pers. comm.) and within three weeks no living crayfish could be found in that lake. Crayfish fungal plague, caused by the oomycete, Aphanomyces astaci Schikora, was subsequently diagnosed (Matthews & Reynolds, 1990), and was the suggested cause of crayfish mortality in this group of midland lakes (Rey- nolds, 1988).

Although the detailed ecological consequences of a loss of an Austropotamobius pallipes stock have yet to be interpreted, changes occurring in the littoral-benthic macrophytic and invertebrate community should give some indication of the ecological role of A. pallipes in Irish lakes and rivers. We here present information on lake benthic flora and fauna observed at different pe- riods after the loss of crayfish from two Irish midlands lakes.

Materials and methods

The environment and biota of Lough Lene (Nat. Grid Ref. N 5169) and Lough Bane (N 5371) were surveyed in October 1987. These rather similar lakes lie on glacial gravels overlying Carbo- niferous limestone. Lough Lene is a transparent

(Secchi disc transparency 4.5-6.0 m), moderately hard (105-125 mg 1- ' CaCO,), markedly alka- line lake (pH 8.2-8.5), 430 ha in extent, tending towards natural eutrophy (Flanagan & Toner, 1975) which drains both underground westward to the River Inny (Shannon system) and eastward into the River Deel (Boyne system). Lough Bane, which drains into the River Deel about 3 km above Lough Lene, is smaller (100 ha) but com- parable in water quality and clarity. The shores of both lakes are mainly stony, with extensive patches of Chara extending to 5 m depth; below this, Lough Bane is floored with fine marly mud while Lough Lene is more stony.

On 19 October 1987 equivalent 100 m stretches of shoreline were surveyed at Loughs Lene and Bane for evidence of crayfish. In each lake simi- lar areas of stony substrate in water 10-40 cm deep were also examined by dip-netting and stone-turning for juvenile crayfish. SCUBA dives were undertaken in both lakes on 4 January 1988 to further check that no crayfish were present. Pairs of healthy crayfish were then enclosed in mesh cages and introduced into each lake to de- termine the continued suitability of these waters for crayfish. Cages were retrieved after 18 days and the crayfish placed in sterilized laboratory aquaria for further observation.

On 19 October 1987 the relative abundance of littoral invertebrate species in each lake was estimated by pooling six standard sweeps of a 1 mm mesh hand-net taken through strands of Chara; for each sweep the net was moved forward and back at one m sec-' over a 1 m trajectory. This sampling was repeated on 24 October 1988. Samples were sorted live by eye, invertebrates preserved in 90% alcohol and identified under x 10 microscopy.

On both dates four samples of Chara were pulled up at the base by hand in each lake at a depth of 0.5-1 m using a Surber sampler of area 225 cm2 to quantify and enclose the vegetation. These were identified as Chara desmacantha (H. and J. Groves), a dominant charophyte forming pure stands in the littoral of these lakes (J. King, pers. comm.). Wet and dry weights were obtained for each sample, and the ten longest strands of

Chara in each sample were measured. In the labo- ratory, two groups of two ovigerous females and four adult male crayfish were held in 20 x 30 cm perspex tanks for seven days at ambient temper- atures (14 to 20 "C), each tank provided with 10 weighed and measured strands of Chara desmacantha. These short-term experiments re- presented a density of 33 to 67 individuals per square metre. In this way we hoped to obtain preliminary information on the influence of A. pallipes on lake vegetation and invertebrates in Ireland.

Results and discussion

No wild living crayfish were seen in either lake during the study. Crayfish remains were found only at Lough Lene in October 1987. Two months after the plague outbreak no wild crayfish or their remains could be found at Lene, indicating the speed at which all physical traces of a substantial population can disappear. SCUBA observations confirmed the absence of crayfish from Loughs Lene and Bane in 1988, although the habitat of each appeared suitable to support crayfish, with clear, apparently unpolluted water, a stony bot- tom providing much shelter, extensive Chara cover and a rich benthic invertebrate community. The caged crayfish from Loughs Lene and Bane remained alive in the laboratory for over 40 days. The survival of encaged crayfish in Lough Lene three months after a confirmed plague outbreak is in agreement with the known short-term persis- tence of Aphanomyces zoospores after the total elimination of crayfish (Matthews & Reynolds, 1990).

Although Laurent (1988) reviews many studies on stream crayfish population estimates, there is little information on population densities for Austropotamobius pallipes in lakes. Mees (1983) records up to 10 per square metre in a water-filled quarry in central England. The population of adult crayfish in While Lake (Grid ref. N 51 72, adja- cent to Bane and Lene), has been assessed at

between 35 000 and 45000 (Moriarty, 1971; O'Keeffe, 1986), with mean adult densities of 0.25 and 1.74 per m2 in Chara and among stones re- spectively (O'Keeffe, 1986). Unpublished obser- vations by divers and from trapping in 1987 sug- gest a comparable density for Lene crayfish, and given the extent of suitable habitat Lough Lene may have held around 1 million crayfish. Such crayfish densities must have exercised a consid- erable impact on the benthic community.

Benthic invertebrates

In the 1988 benthic samples, oligochaetes and chironomid larvae made up 34 % of individuals in L. Lene samples and 25% in L. Bane. As these forms were excluded from the 1987 count they are not considered further here. Total abundance of other invertebrates in samples increased from 1987 to 1988 in both lakes. Results are therefore given in relative terms (Table 1).

Gammarus, Asellus and Caenis dominated 1987 samples. In both lakes, the dominant remaining macro-crustaceans (Gammarus in L. Lene, Asel-

Table 1. Percentage composition of benthic invertebrates (ex- cluding chironomid larvae and oligochaetes) in sweep samples from two lakes in County Westmeath, Ireland.

L. Bane L. Lene

Sampling year 1987 1988 1987 1988

Taxon: Hirudinea 0 0 6.5 5.3 Tricladida 2.4 1.4 0 0 Bithynia 0 8.9 4.3 0.9 Planorbidae 0 2.0 1.1 5.3 Other snails* 0 0.3 1.1 1.3 Pisidium 0 2.0 0 3.5 Gammarus 21.1 9.2 34.4 39.9 Asellus 33.1 55.6 9.7 7.9 Caenis 41.0 10.4 38.7 22.8 Trichoptera 2.4 9.5 4.3 11.4 Other insects** 0 0.6 0 1.8

Total numbers 166 347 93 228

* Lymnea, Ancylus, Potamopyrgus spp. ** Tipulidae, Dytiscidae

lus in L. Bane) increased in relative abundance over the two sampling years. There was also a relative decrease in Caenis but a rise in trichopte- rans and other insects. Total snail numbers changed little between 1987 and 1988, but a de- crease in Bithynia was balanced by a strong in- crease in planorbids.

Invertebrate numbers increased less strongly between 1987 and 1988 in L. Bane than in L. Lene samples (Table 1). Snails were absent from 1987 L. Bane samples, but plentiful in 1988 (particu- larly Planorbidae) and Trichoptera and some other insects increased in relative abundance in both lakes in 1988 compared with 1987, while numbers of Caenis in L. Bane declined. Leech and flatworm numbers were relatively unaffected.

Our results suggest a change in the benthic community with time in a lake which had recently lost crayfish populations, in particular an increase in total invertebrates and in crustaceans, planor- bids and most other snails. Lodge et al. (1987) state that planorbids and other thin-shelled pul- monates are more susceptible to crayfish preda- tion than are prosobranchs such as Bithynia. Mol- luscs are known to have formed a significant part of the crayfish diet in White Lake (O'Keeffe, 1986).

Macrophytic vegetation

In northern Europe overgrowth of lake vegetation (including Chara) may be the most conspicuous

consequence of noble crayfish (A. astacus) re- moval (Abrahamsson, 1966; Unestam, 1973) but there are no published data for Austropotamobius. Chara formed an important component of the diet of adult lake A. pallipes (O'Keeffe, 1986). In lab- oratory tests crayfish fed on Chara desmacantha significantly reduced strand lengths (p < 0.000 1) over a seven day period (Table 2), the reduction being greater at higher crayfish density. We there- fore hypothesised that in the absence of wild cray- fish populations, uncropped Chara should have longer strands of new growth with relatively lower dry to wet weight ratios than the older coarser vegetation resulting from frequent cropping.

Lough Lene Chara strand length increased ap- proximately 14.5% between 1987 and 1988 (Ta- ble 3), which was a highly significant increase (one way ANOVA, F = 11.52, df = 1,17, p = 0.0035). In contrast, little change was recorded in Lough Bane (F= 1.55, df = 1,18, p = 0.23). Comparisons of Chara length between the two lakes in 1987 showed a difference at the 10% level, however, the following year this difference was much higher (p < 0.0001) reflecting the change in Lough Lene over this time. Chara samples from Lough Lene also had a lower mean wet weight than those from Lough Bane in both years. The Chara dry to wet weight ratio of Lough Lene fell markedly in 1988, while that in Lough Bane rose (Table 3). The fluc- tuations recorded in Lough Bane may reflect an earlier date of crayfish removal (Reynolds, 1988). Overall the greatest changes in Chara occurred in

Table 2 . Grazing impact of adult crayfish on measured strands of Chara desmacantha over a seven day period under laboratory conditions.

Tank 1: Control (no crayfish)

Tank 2: Two females

Tank 3: Four males

Chara: Starting length (cm): mean 23.7 22.6 23.5

Standard deviation 6.28 4.33 4.85 Final length (cm): mean 23.7 5.36 2.83

Standard deviation 6.28 1.84 1.36

Paired t-tests: (i) Tank 2 11.39, p < 0.0001 @)Tank 3 12.99,ptO.OOOl

Initial length of Chara (males vs females) t = 0.54, p < 0.603 Final length of Chara (males vs females) t = 3.69, p<0.005

Table 3. Comparison of Chara samples taken from Loughs Bane and Lene in 1987 and 1988.

Parameter L. Bane L. Lene

Mean Std. dev. Mean Std. dev.

1987 Lengths (cm) Wet weights (g) Dry weights (g) Dry to wet weight ratio

1988 Lengths (cm) Wet weights (g) Dry weights (g) Dry to wet weight ratio

Lough Lene where sampling had begun immedi- ately after crayfish elimination.

The laboratory experiments thus agree with our field study findings which indicate that a loss of lake stocks of the crayfish A . pallipes is associated with a measurable increase in new growth of a dominant aquatic macrophyte. This must have influenced invertebrate diversity and species composition, apart from changes due to any re- laxation of direct predation by crayfish. Lodge & Lorman (1987) obtained reductions in macro- phytes by manipulating densities of Orconectes rusticus (Girard), concluding that both direct her- bivory by crayfish, and indirect effects through the destruction of epiphyte-feeding snails, were im- plicated. However, Feminella & Resh (1989) de- tected no significant relationships between snails and crayfish (Procambarus clarkii) densities, con- cluding that the effect on macrophytes was direct. Further work is required to quantify the effect of lake populations of Austropotamobius on inverte- brate relative abundance (notably gastropod mol- luscs) and community structure.

Acknowledgements

We would like to thank Jimmy King and Sylvia Reynolds for identifying the Chara, Patrick Ashe and Ray Billington for sampling the study lakes for crayfish in 1987, Michael Keatinge for help-

ful comments on the manuscript and the staff of the Zoology Department, TCD for facilities and assistance.

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