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Prey selection and daily food consumption by a cleaner fish, Ctenolabrus rupestris (L.), on farmed Atlantic salmon, Salmo salar L.
Aquaculture ELSEVIER
Aquaculture 122 ( 1994) 269-277
Prey selection and daily food consumption by a cleaner fish, Ctenolabrus rupestris (L. ) , on farmed Atlantic salmon, Salmo salar L. James Treasurer Marine Harvest,Lochailort,Inverness-shire,UK (Accepted 20 December 1993)
Abstract Feeding electivity and daily food consumption by a cleaner fish goldsinny wrasse, Ctenolabrus rupestris (L.) on sea lice, Lepeophtheirus salmonis Kroyer, on farmed Alantic salmon, Salmo salar L., was assessed by comparison of lice numbers and developmental stages on salmon in pens with and without wrasse. Mobile stages of L. salmonis in the pen with wrasse remained low ( l-8 per fish) with no requirement for chemical treatment compared with a heavy infestation (up to 50) on the control pen. Wrasse selectively preyed on the larger lice stages, mainly adults and female pre-adult Stage II, and this was measured and statistically tested using Pearre’s selection index. The mean number of mobile L. salmonis consumed daily by an individual wrasse varied from 26-46 at water temperatures of lo- 12” C and daily food consumption was 1.18-2.72% of body weight.
1. Introduction
Wrasse have been used as cleaner fish to remove sea lice (Copepoda: Caligidae ) from Atlantic salmon, Sulrno sulur L., on farms in Norway (Bjordal, 199 1 ), Ireland (Darwall et al., 199 1) and Scotland (Treasurer, 1993). Sea lice, principally Lepeophtheirus salmonis Kroyer and to a lesser extent Caligus elongatus Nordmann, are major pathogens of farmed salmon. Use of wrasse as an alternative biological method of control has environmental advantages over traditional chemotherapeutant treatments. Stress and adverse effects on salmon growth are also reduced (Costello, 1993 ) . Initial trials with wrasse were in aquaria (Bjordal, 199 1 ), but such results were not applicable to the farm setting as wrasse and salmon were in unusually close physical contact, high stocking ratios of wrasse were used, no alternative food source was provided, and in a tank setting swim0044~8486/94/$07.00 0 1994 Elsevier Science B.V. AU rights reserved SsDI0044-8486(93)E0319-5
270
J. Treasurer/Aquaculture 122 (1994) 269-277
ming speed of salmon may be reduced. Bjordal ( 1990) extended this work to include trials in experimental and commercial farm cages. A subsequent independent study (Treasurer, 1993) also verified cleaning activity by comparison of the population dynamics of sea lice in cages with and without wrasse. However, the detailed predator-prey relationship of wrasse and sea lice has not been examined. The present study examines daily food consumption (Ct ) and the nature of prey selection in the goldsinny wrasse, Ctendabrus rupestris (L. ), by comparison of lice numbers and developmental stages on salmon in adjacent cages, one stocked with wrasse and the other without wrasse. Various measures of food selection (“electivity”) in fish have been tested by comparison of the relative abundance of prey in the environment with abundance of that species in the diet, e.g. Ivlev’s index (Ivlev, 196 1)) but few enable a means of significance testing. However, Pearre’s index (Pearre, 1982) uses chi-square analysis to provide levels of significance and is used in the present study.
2. Methods Trial group The trial was conducted from August 199 1 to January 1992 on an experimental group of 32 cages (called “pens” in the salmon farming industry), dimensions 5 x 5 x 4 m deep with net mesh 12 mm2 located on a farm at Loch Eil, west Scotland. Water temperature measured at 4 m depth varied from 13 ‘C in August to 8 a C in January and salinity over this period was 2 l-30 ppt. In April 199 1,20 000 smolts of the 199 1 year class (in marine salmon farming, “year class” refers to the year in which fish are put to sea) were stocked on the trial unit. Settlement of copepodites, mainly L. salmonis (Caligus comprised less than 5% of lice numbers on any date), was immediate and four treatments with Aquagard (CibaGeigy) were required by 20 August to remove mobile stages. On 28 August goldsinny wrasse at a ratio of 1: 25 salmon post-smolts were stocked in 18 pens. An additional 4 pens with no wrasse were randomly assigned as controls in the block of 32 pens using statistical tables. Three adjacent pens were used for the present trial, pen 13 stocked with wrasse and pens 14 and 15 with no wrasse (two of the 4 pens indicated above ) . On 20 October wrasse were added to pen 15 for 10 days to control lice numbers to avoid treatment of lice with a chemotherapeutant. 250 salmon, range 150-250 g and 2 1-23 cm length, were stocked in each pen giving a biomass of l-l.6 kg.mm3. Each week 5 salmon were removed from each pen, anaesthetised in 15 ppm benzocaine, and lice identified to sessile chalimus and mobile stages, and fish then returned. Mobile lice dislodged in this process were counted in the holding bin. Five additional fish were removed and killed with a blow to the head every 2 weeks. Lice were identified to larval chalimus Stages I-IV and the mobile lice, sexed and identified to preadult Stages I and II and adults (Johnson and Albright, 199 1). A low-power ( x 10) binocular microscope was used to check for the presence of chalimus on the body surface, branchial chamber and gills. Length, ex-
J. Treasurer /Aquaculture 122 (1994) 269-277
271
eluding egg sacs, and breadth (mm) of mobile L. salmonis were measured, and also wet weights from a sample of each developmental stage. Dry weight was determined after drying the lice in an oven at 60’ C for 24 h. An attempt was made to extrude copepod remains in the faeces of anaesthetised wrasse by gently massaging the belly. Statistical analyses
Numbers of chalimi and mobile lice followed an overdispersed distribution with a high variance to mean ratio. Data were therefore transformed to log(x+ 1) and presented as geometric means with 95% confidence limits, and comparison made by Student’s t-test. Prey selection was measured using Pearre’s index (Pearre, 1982) ranging from + 1 to - 1 for complete selection for and against an item and a value of 0 representing no selection. A 2x2 contingency table was constructed to permit statistical comparison with randomness. The proportion of free-living prey in the environment (notation in Pearre=ae) is represented in the present study as the percentage number of mobile lice of each developmental stage on hosts in the control pen. Pearre’s dietary component (ad) is given here as the difference in the representation of each developmental stage in the pen with wrasse compared with the proportion on the control fish. As the alimentary tracts of wrasse were not examined and other food items may have been eaten, the term “daily estimated lice consumption” (Ct ) of individual wrasse is used rather than daily food consumption. This was calculated from: Ct=~{[(YxS)/T,-T,]/N)x~
(1)
where Y= mean reduction in mobile lice numbers per fish from commencement of the trial (TO) to completion ( T,)in days, S=number of salmon, N=number of stocked wrasse, and W= wet weight of each developmental stage. Two further estimates of Ct were obtained following the introduction of wrasse to the control pen on 20 October for 10 days and the additional control pen 14. 3. Results Lice population dynamics
Numbers of mobile lice increased rapidly in pens with and without wrasse following treatment of lice with dichlorvos on 28 August (Fig. 1) . However, 3 weeks after stocking wrasse, mobile lice numbers on fish in the experimental pen declined to 4.7 ? 1.7 95% CL ( 1 October) and numbers remained low, varying from 1.4 2 1.2 to 8.4 t 1.3 per fish to 3 1 December, with no requirement for chemical treatments. In contrast, mobile L. salmonis increased to a maximum of 49.7 5 1.2 per fish on 14 October in the control pen. After 10 wrasse were added for 10 days to avoid treating salmon with Aquagard, lice numbers declined to 0.9 5 0.6 on average by 30 October and, when wrasse were retrieved by handnet after raising the net (no wrasse escaped during the trial period), rose to 46.9 +-1.2 by 26 November. Apart from September, numbers of mobile lice were significantly greater
J. Treasurer /Aquaculture 122 (1994) 269-277
212 al
Mean no. mobile L. salmonis
,
26 Aw
7
1
Sept
14
act -pen13
5
Date
19 NW
3
16 D&?C
6 Jail
+,, Pen 15
Fig. 1. Mean numbers (geometric) of mobile Lepeophtheirus salmonis on salmon in the pen with wrasse compared with the control. Bars indicate 95% confidence limits.
-pal3
+
Pen15
Fig. 2. Mean numbers (geometric) ofchahmus of L. salmonis in the pen with wrasse compared with the control. Bars represent 95% confidence limits.
(P-z 0.05) on control fish. Numbers of chalimus (Fig. 2) were not significantly different (P> 0.05 ) between fish in pens 13 and 15 in October but were significantly higher on controls in pen 15 in November. Chalimus on salmon in both pens declined gradually from 19 November. Selectivity Apart from one sample, all mobile and chalimus stageswere less in the pen with wrasse (Fig. 3): the line represents a ratio of 1: 1, i.e. identical numbers in each pen. Selection was strongest for male and female adults, female pre-adult Stage
J. Treasurer /Aquaculture 122 (1994) 269-277 Table 1 Pearre electivity indices for ( + ) and against ( - ) the developmental by goldsinny wrasse Date (1991)
I Ott 23 Ott 5 Nov 19Nov 3 Dee 18 Dee
L. salmonis developmental
Pearre index/ &i-square
Index x2 Index X2 Index x2 Index X2 Index X2 Index X2
273
stages of L. salmonis consumed
stage
MPAI
MPAII
MAD
FPAI
FPAII
FAD
+ 0.002 (0.001) - 1.ooo
-0.028 (0.156) +0.055 (0.605) 0.000
+0.027 (0.041) +0.070 (0.977) +0.003 (0.002) $0.021 (0.844) +0.054 (0.602) +0.032 (0.205)
- 0.092 (1.681) -0.080 (1.264) +0.008 (0.013) - 0.004 (0.003) -0.094 (1.751) -0.083 (1.370)
+ 0.042 (0.352) + 0.046 (0.430) -0.007 (0.010) -0.001 (0.0003) +0.019 (0.070) - 0.224 (10.004)**
+0.047 (0.438) + 0.079 (0.125) 0.000
-0.006 (0.007) -0.013 (0.036) - 0.075 (1.134) + 0.024 (0.114)
-0.012 (0.028) -0.017 (0.058) - 0.042 (0.358)
+0.013 (0.034) + 0.054 (0.586) +0.121 (2.936)
The values were tested for significance by chi-square test; chi-square values are shown in parentheses. M = male; F= female; PA = pre-adult stage; AD = adult. Note: none of chi-square values significant at the 0.05 level with the exception of ** = significant at 0.01 level.
0
10
20
30
40
50
60
70
80
No. lice/fish in control -
MPAI
+
MPAII
*
Macha
x
FPAII
0
Fadult
A
Chdimus
M = male
F = female
0
FPA,
PA = preadult
Fig. 3. A plot of the number of each developmental stage of Lepeophtheirus salmonis on salmon in the pen with wrasse compared with fish in the control pen. The line at the 45 ’ angle indicates a 1: 1 ratio. Data shown for four sampling dates: 7 and 23 October, and 5 and 19 November.
274
.T. Treasurer /Aquaculture 122 (1994) 269-277
h
h
h
J. Treasurer / Aquaculture 122 (I 994) 269-2 77 Table 3 Lengths (range)
215
(n= 10 each stage) and wet and dry weights (N shown) of L. salmonis
Developmental stage
Nlice weighed
Total length
Breadth
Mean wet
Mean dry
(TL
(mm)
W (mg)
W (mg)
MPAI MPAII MAD FPAI FPAII FAD
16 9 63 25 25 95
3.2-3.6 4.4-4.9 5.2-5.9 3.1-4.1 5.0-5.7 8.5-l 1.8
1.5-1.9 2.23-2.3 2.6-3.0 1.8-2.0 2.8-3.0 3.9-4.2
5.13 8.33 15.11 6.08 11.80 39.92
0.25 0.61 1.08 0.28 0.84 3.11
mm)
II, followed by male pre-adult II and male and female pre-adult I. For example, in the pen with wrasse, adults of both sexes combined on 7 October comprised 3.9% of all lice stages compared with 20.3% in the control pen, 6.3% vs. 48.4% on 23 October, and 0% vs. 22.7% on 19 November. Comparison was not possible on 5 November as most lice had been removed in the control pen by the temporary stocking of wrasse and the lice on control fish were mainly pre-adult Stages I and II. The Pearre selection index indicated selection for and against particular developmental stages (Table 1). This was statistically significant on only one date, 18 December, with selection against female PA Stage II (P=O.Ol ) because stages of lice consumed were almost equal to those present on control fish. Daily lice consumption
Numbers of lice consumed daily per wrasse were similar in pens 13, 14 and 15 (25.9, 46.2 and 39.2 mobiles respectively) at a water temperature range of lo12 ‘C (Table 2 ) . This was converted to wet and dry weight consumed from data presented in Table 3 and daily lice consumption calculated as a percentage of mean body weight = 29.66 g ( t 3.19, 95% CL) (n = 53 goldsinny wrasse) . The average range of daily lice consumption was 1.18-2.72% of body weight.
4. Discussion
The reduction in chalimi numbers in both experimental and control pens from 19 November was perhaps due to reduced larval recruitment following harvesting of most production fish and to reduced salinity and temperature with the onset of winter. There was a definite pattern of prey selection for larger developmental stages of lice (Fig. 3 ) , although there was an indication that chalimi were also consumed (Fig. 2), similar to findings in Ireland (Costello, personal communication). Other fish species show similar selection for larger food items, e.g. Percafluviatilis (Guma’a, 1978 ). Several assumptions are made here in calculating daily lice consumption, because the extent of cleaning activity is measured indirectly by the comparison of
276
J. Treasurer /Aquaculture 122 (1994) 269-277
lice population dynamics in pens with and without wrasse. Direct measurement would have been possible by killing wrasse and examination of contents of the alimentary tract, but this would have interfered with the trial. Extrusion of copepod remains in the faeces of anaesthetised wrasse was unsuccessful. A stomach pump based on two linked syringes was also unsuccessful, with only small fragments of lice being retrieved from two fish. The calculations of daily food consumption are based on wrasse eating only sea lice. It is probable that wrasse, once acclimatised to the cage environment, would prey mainly on sea lice and would only switch to other food items when lice were scarce. The rate of transfer of lice between fish in different pens was not assessed and is likely to occur (Bruno and Stone, 1990). It is assumed that the immigration rate from adjacent pens to the trial pens was constant (Jaworski and Holm, 1992). The number of L. saZmon2.s(26-46) consumed per wrasse per day at Loch Eil was similar to cleaning rates reported in aquaria for goldsinny, 28.3 and 45 lice respectively in separate trials, and up to 20 in a sea cage (Bjordal, 199 1). The rates of daily food consumption quoted here ( 1.2-2.7% body weight) are comparable with freshwater and marine fish of similar body weight, e.g. 2-5% in Eurasian perch, PercajluviatiZis (L.) (Thorpe, 1977), 2.4 and 3.7% in juvenile coho salmon, Oncorhynchus kisutch (Walbaum) at water temperatures of 11.4 and 13.7 “C respectively (Brodeur and Pearcy, 1987), 6% in haddock, Melanogrammus aeglifinus (L.) and 4.1% in dab, Limanda Zimanda (L.) (Hall, 1987), 510% for small ( 15-20 cm) plaice, Pleuronectes platessa L. (Basimi and Grove, 1985 ), and 7% in common sole, SoZeavulgaris Quensel (Lagardere, 1987). Some of these examples for marine fish are higher than in wrasse and, as wrasse are known to browse on nets and eat benthic organisms (Hillden, 1978; Costello, 199 1)) the data presented here are likely to be minimum estimates of daily food consumption.
Acknowledgements I am grateful to Mark Costello for helpful comments on the manuscript staff at Loch Eil fish farm for assistance during the trial.
and to
References Basimi, R.A. and Grove, D.J., 1985. Estimates of daily food intake by an inshore population of Pleuronectesplatessa L. off eastern Anglesey, North Wales. J. Fish Biol., 27: 505-520. Bjordal, A., 1990. Sea lice infestation on farmed salmon: possible use of cleaner-fish as an alternative method for de-lousing. Can. Tech. Rep. Fish. Aquat. Sci., 1761: 85-89. Bjordal, A., 199 1. Wrasse as cleaner-fish for farmed salmon. Prog. Underwater Sci., 16: 17-28. Brodeur, R.D. and Pearcy, W.G., 1987. Die1 feeding chronology, gastric evacuation and estimated daily ration of juvenile coho salmon, Oncorhynchus kisutch (Walbaum), in the coastal marine environment. J. Fish Biol., 3 1: 465-477.
J. Treasurer /Aquaculture 122 (1994) 269-277
217
Bruno, D.W. and Stone, J., 1990. The role of saithe, Pollachius virens L., as a host for sea lice, Lepeophtheirus salmonis Kroyer and Cal&-uselongatus Nordmann. Aquaculture, 89: 201-207. Costello, M., 199 1. Review of the biology of wrasse (Labridae:Pisces ) in northern Europe. Prog. Underwater Sci., 16: 29-5 1. Costello, M., 1993. Controlling sea-lice infestations on farmed salmon in Northern Europe: options and the use of cleaner fish. World Aquacult., 24-91: 49-56. Darwall, W., Costello, M.J. and Lysaght, S., 1991. Wrasse: how well do they work? Aquacult. Irel., 5: 26-29. Guma’a, S.A., 1978. The food and feeding habits of young perch, Perca fluviatilis, in Windermere. Freshwater Biol., 8: 177-187. Hall, S.J., 1987. Maximum daily ration and the pattern of food consumption in haddock, Melanogrammus aeglefinus (L. ), and dab, Limanda limanda (L. ). J. Fish Biol., 3 1: 479-49 1. Hillden, N.-O., 1978. On the feeding of the gold&my, Ctenolabrus rupestris L. (Pisces, Labridae). Ophelia, 17: 195-198. Ivlev, V.S., 196 1. Experimental Ecology of the Feeding of Fishes. Yale University Press, New Haven, CT, 302 pp. Jaworski, A and Hahn, J.C., 1992. The distribution and structure of the population of sea lice (Lepeophtheirus salmonis Kroyer) on Atlantic salmon (Salmo salar L. ) under typical rearing conditions. Aquacult. Fish. Manag., 23: 577-589. Johnson, S.C. and Albright, L.J., 199 1. Development, growth and survival of Lepeophtheirus salmonis (Copepodaz Caligidae) under laboratory conditions. J. Mar. Biol. Assoc. U.K., 7 1: 425-436. Lagardere, J.P., 1987. Feeding ecology and daily food consumption of common sole, Solea vulgaris Quensel, juveniles on the French Atlantic coast. J. Fish Biol., 30: 91-104. Pearre, S., 1982. Estimating prey preference by predators: uses of various indices, and a proposal of another based on 2. Can. J. Fish. Aquat. Sci., 39: 9 14-923. Thorpe, J.E., 1977. Daily ration of adult perch, Percafluviatilis L., during summer in Loch Leven, Kinross, Scotland. J. Fish Biol., 11: 55-68. Treasurer, J.W., 1993. Management of sea lice (Caligidae) with wrasse (Labridae) on Atlantic salmon (Salmo salar) farms. In: Boxshall, G.A. and Defaye, D. (Editors), Pathogens of Wild and Farmed Salmonids: Sea Lice. Ellis Horwood, Chichester, pp. 335-345.
Aquaculture 122 ( 1994) 269-277
Prey selection and daily food consumption by a cleaner fish, Ctenolabrus rupestris (L. ) , on farmed Atlantic salmon, Salmo salar L. James Treasurer Marine Harvest,Lochailort,Inverness-shire,UK (Accepted 20 December 1993)
Abstract Feeding electivity and daily food consumption by a cleaner fish goldsinny wrasse, Ctenolabrus rupestris (L.) on sea lice, Lepeophtheirus salmonis Kroyer, on farmed Alantic salmon, Salmo salar L., was assessed by comparison of lice numbers and developmental stages on salmon in pens with and without wrasse. Mobile stages of L. salmonis in the pen with wrasse remained low ( l-8 per fish) with no requirement for chemical treatment compared with a heavy infestation (up to 50) on the control pen. Wrasse selectively preyed on the larger lice stages, mainly adults and female pre-adult Stage II, and this was measured and statistically tested using Pearre’s selection index. The mean number of mobile L. salmonis consumed daily by an individual wrasse varied from 26-46 at water temperatures of lo- 12” C and daily food consumption was 1.18-2.72% of body weight.
1. Introduction
Wrasse have been used as cleaner fish to remove sea lice (Copepoda: Caligidae ) from Atlantic salmon, Sulrno sulur L., on farms in Norway (Bjordal, 199 1 ), Ireland (Darwall et al., 199 1) and Scotland (Treasurer, 1993). Sea lice, principally Lepeophtheirus salmonis Kroyer and to a lesser extent Caligus elongatus Nordmann, are major pathogens of farmed salmon. Use of wrasse as an alternative biological method of control has environmental advantages over traditional chemotherapeutant treatments. Stress and adverse effects on salmon growth are also reduced (Costello, 1993 ) . Initial trials with wrasse were in aquaria (Bjordal, 199 1 ), but such results were not applicable to the farm setting as wrasse and salmon were in unusually close physical contact, high stocking ratios of wrasse were used, no alternative food source was provided, and in a tank setting swim0044~8486/94/$07.00 0 1994 Elsevier Science B.V. AU rights reserved SsDI0044-8486(93)E0319-5
270
J. Treasurer/Aquaculture 122 (1994) 269-277
ming speed of salmon may be reduced. Bjordal ( 1990) extended this work to include trials in experimental and commercial farm cages. A subsequent independent study (Treasurer, 1993) also verified cleaning activity by comparison of the population dynamics of sea lice in cages with and without wrasse. However, the detailed predator-prey relationship of wrasse and sea lice has not been examined. The present study examines daily food consumption (Ct ) and the nature of prey selection in the goldsinny wrasse, Ctendabrus rupestris (L. ), by comparison of lice numbers and developmental stages on salmon in adjacent cages, one stocked with wrasse and the other without wrasse. Various measures of food selection (“electivity”) in fish have been tested by comparison of the relative abundance of prey in the environment with abundance of that species in the diet, e.g. Ivlev’s index (Ivlev, 196 1)) but few enable a means of significance testing. However, Pearre’s index (Pearre, 1982) uses chi-square analysis to provide levels of significance and is used in the present study.
2. Methods Trial group The trial was conducted from August 199 1 to January 1992 on an experimental group of 32 cages (called “pens” in the salmon farming industry), dimensions 5 x 5 x 4 m deep with net mesh 12 mm2 located on a farm at Loch Eil, west Scotland. Water temperature measured at 4 m depth varied from 13 ‘C in August to 8 a C in January and salinity over this period was 2 l-30 ppt. In April 199 1,20 000 smolts of the 199 1 year class (in marine salmon farming, “year class” refers to the year in which fish are put to sea) were stocked on the trial unit. Settlement of copepodites, mainly L. salmonis (Caligus comprised less than 5% of lice numbers on any date), was immediate and four treatments with Aquagard (CibaGeigy) were required by 20 August to remove mobile stages. On 28 August goldsinny wrasse at a ratio of 1: 25 salmon post-smolts were stocked in 18 pens. An additional 4 pens with no wrasse were randomly assigned as controls in the block of 32 pens using statistical tables. Three adjacent pens were used for the present trial, pen 13 stocked with wrasse and pens 14 and 15 with no wrasse (two of the 4 pens indicated above ) . On 20 October wrasse were added to pen 15 for 10 days to control lice numbers to avoid treatment of lice with a chemotherapeutant. 250 salmon, range 150-250 g and 2 1-23 cm length, were stocked in each pen giving a biomass of l-l.6 kg.mm3. Each week 5 salmon were removed from each pen, anaesthetised in 15 ppm benzocaine, and lice identified to sessile chalimus and mobile stages, and fish then returned. Mobile lice dislodged in this process were counted in the holding bin. Five additional fish were removed and killed with a blow to the head every 2 weeks. Lice were identified to larval chalimus Stages I-IV and the mobile lice, sexed and identified to preadult Stages I and II and adults (Johnson and Albright, 199 1). A low-power ( x 10) binocular microscope was used to check for the presence of chalimus on the body surface, branchial chamber and gills. Length, ex-
J. Treasurer /Aquaculture 122 (1994) 269-277
271
eluding egg sacs, and breadth (mm) of mobile L. salmonis were measured, and also wet weights from a sample of each developmental stage. Dry weight was determined after drying the lice in an oven at 60’ C for 24 h. An attempt was made to extrude copepod remains in the faeces of anaesthetised wrasse by gently massaging the belly. Statistical analyses
Numbers of chalimi and mobile lice followed an overdispersed distribution with a high variance to mean ratio. Data were therefore transformed to log(x+ 1) and presented as geometric means with 95% confidence limits, and comparison made by Student’s t-test. Prey selection was measured using Pearre’s index (Pearre, 1982) ranging from + 1 to - 1 for complete selection for and against an item and a value of 0 representing no selection. A 2x2 contingency table was constructed to permit statistical comparison with randomness. The proportion of free-living prey in the environment (notation in Pearre=ae) is represented in the present study as the percentage number of mobile lice of each developmental stage on hosts in the control pen. Pearre’s dietary component (ad) is given here as the difference in the representation of each developmental stage in the pen with wrasse compared with the proportion on the control fish. As the alimentary tracts of wrasse were not examined and other food items may have been eaten, the term “daily estimated lice consumption” (Ct ) of individual wrasse is used rather than daily food consumption. This was calculated from: Ct=~{[(YxS)/T,-T,]/N)x~
(1)
where Y= mean reduction in mobile lice numbers per fish from commencement of the trial (TO) to completion ( T,)in days, S=number of salmon, N=number of stocked wrasse, and W= wet weight of each developmental stage. Two further estimates of Ct were obtained following the introduction of wrasse to the control pen on 20 October for 10 days and the additional control pen 14. 3. Results Lice population dynamics
Numbers of mobile lice increased rapidly in pens with and without wrasse following treatment of lice with dichlorvos on 28 August (Fig. 1) . However, 3 weeks after stocking wrasse, mobile lice numbers on fish in the experimental pen declined to 4.7 ? 1.7 95% CL ( 1 October) and numbers remained low, varying from 1.4 2 1.2 to 8.4 t 1.3 per fish to 3 1 December, with no requirement for chemical treatments. In contrast, mobile L. salmonis increased to a maximum of 49.7 5 1.2 per fish on 14 October in the control pen. After 10 wrasse were added for 10 days to avoid treating salmon with Aquagard, lice numbers declined to 0.9 5 0.6 on average by 30 October and, when wrasse were retrieved by handnet after raising the net (no wrasse escaped during the trial period), rose to 46.9 +-1.2 by 26 November. Apart from September, numbers of mobile lice were significantly greater
J. Treasurer /Aquaculture 122 (1994) 269-277
212 al
Mean no. mobile L. salmonis
,
26 Aw
7
1
Sept
14
act -pen13
5
Date
19 NW
3
16 D&?C
6 Jail
+,, Pen 15
Fig. 1. Mean numbers (geometric) of mobile Lepeophtheirus salmonis on salmon in the pen with wrasse compared with the control. Bars indicate 95% confidence limits.
-pal3
+
Pen15
Fig. 2. Mean numbers (geometric) ofchahmus of L. salmonis in the pen with wrasse compared with the control. Bars represent 95% confidence limits.
(P-z 0.05) on control fish. Numbers of chalimus (Fig. 2) were not significantly different (P> 0.05 ) between fish in pens 13 and 15 in October but were significantly higher on controls in pen 15 in November. Chalimus on salmon in both pens declined gradually from 19 November. Selectivity Apart from one sample, all mobile and chalimus stageswere less in the pen with wrasse (Fig. 3): the line represents a ratio of 1: 1, i.e. identical numbers in each pen. Selection was strongest for male and female adults, female pre-adult Stage
J. Treasurer /Aquaculture 122 (1994) 269-277 Table 1 Pearre electivity indices for ( + ) and against ( - ) the developmental by goldsinny wrasse Date (1991)
I Ott 23 Ott 5 Nov 19Nov 3 Dee 18 Dee
L. salmonis developmental
Pearre index/ &i-square
Index x2 Index X2 Index x2 Index X2 Index X2 Index X2
273
stages of L. salmonis consumed
stage
MPAI
MPAII
MAD
FPAI
FPAII
FAD
+ 0.002 (0.001) - 1.ooo
-0.028 (0.156) +0.055 (0.605) 0.000
+0.027 (0.041) +0.070 (0.977) +0.003 (0.002) $0.021 (0.844) +0.054 (0.602) +0.032 (0.205)
- 0.092 (1.681) -0.080 (1.264) +0.008 (0.013) - 0.004 (0.003) -0.094 (1.751) -0.083 (1.370)
+ 0.042 (0.352) + 0.046 (0.430) -0.007 (0.010) -0.001 (0.0003) +0.019 (0.070) - 0.224 (10.004)**
+0.047 (0.438) + 0.079 (0.125) 0.000
-0.006 (0.007) -0.013 (0.036) - 0.075 (1.134) + 0.024 (0.114)
-0.012 (0.028) -0.017 (0.058) - 0.042 (0.358)
+0.013 (0.034) + 0.054 (0.586) +0.121 (2.936)
The values were tested for significance by chi-square test; chi-square values are shown in parentheses. M = male; F= female; PA = pre-adult stage; AD = adult. Note: none of chi-square values significant at the 0.05 level with the exception of ** = significant at 0.01 level.
0
10
20
30
40
50
60
70
80
No. lice/fish in control -
MPAI
+
MPAII
*
Macha
x
FPAII
0
Fadult
A
Chdimus
M = male
F = female
0
FPA,
PA = preadult
Fig. 3. A plot of the number of each developmental stage of Lepeophtheirus salmonis on salmon in the pen with wrasse compared with fish in the control pen. The line at the 45 ’ angle indicates a 1: 1 ratio. Data shown for four sampling dates: 7 and 23 October, and 5 and 19 November.
274
.T. Treasurer /Aquaculture 122 (1994) 269-277
h
h
h
J. Treasurer / Aquaculture 122 (I 994) 269-2 77 Table 3 Lengths (range)
215
(n= 10 each stage) and wet and dry weights (N shown) of L. salmonis
Developmental stage
Nlice weighed
Total length
Breadth
Mean wet
Mean dry
(TL
(mm)
W (mg)
W (mg)
MPAI MPAII MAD FPAI FPAII FAD
16 9 63 25 25 95
3.2-3.6 4.4-4.9 5.2-5.9 3.1-4.1 5.0-5.7 8.5-l 1.8
1.5-1.9 2.23-2.3 2.6-3.0 1.8-2.0 2.8-3.0 3.9-4.2
5.13 8.33 15.11 6.08 11.80 39.92
0.25 0.61 1.08 0.28 0.84 3.11
mm)
II, followed by male pre-adult II and male and female pre-adult I. For example, in the pen with wrasse, adults of both sexes combined on 7 October comprised 3.9% of all lice stages compared with 20.3% in the control pen, 6.3% vs. 48.4% on 23 October, and 0% vs. 22.7% on 19 November. Comparison was not possible on 5 November as most lice had been removed in the control pen by the temporary stocking of wrasse and the lice on control fish were mainly pre-adult Stages I and II. The Pearre selection index indicated selection for and against particular developmental stages (Table 1). This was statistically significant on only one date, 18 December, with selection against female PA Stage II (P=O.Ol ) because stages of lice consumed were almost equal to those present on control fish. Daily lice consumption
Numbers of lice consumed daily per wrasse were similar in pens 13, 14 and 15 (25.9, 46.2 and 39.2 mobiles respectively) at a water temperature range of lo12 ‘C (Table 2 ) . This was converted to wet and dry weight consumed from data presented in Table 3 and daily lice consumption calculated as a percentage of mean body weight = 29.66 g ( t 3.19, 95% CL) (n = 53 goldsinny wrasse) . The average range of daily lice consumption was 1.18-2.72% of body weight.
4. Discussion
The reduction in chalimi numbers in both experimental and control pens from 19 November was perhaps due to reduced larval recruitment following harvesting of most production fish and to reduced salinity and temperature with the onset of winter. There was a definite pattern of prey selection for larger developmental stages of lice (Fig. 3 ) , although there was an indication that chalimi were also consumed (Fig. 2), similar to findings in Ireland (Costello, personal communication). Other fish species show similar selection for larger food items, e.g. Percafluviatilis (Guma’a, 1978 ). Several assumptions are made here in calculating daily lice consumption, because the extent of cleaning activity is measured indirectly by the comparison of
276
J. Treasurer /Aquaculture 122 (1994) 269-277
lice population dynamics in pens with and without wrasse. Direct measurement would have been possible by killing wrasse and examination of contents of the alimentary tract, but this would have interfered with the trial. Extrusion of copepod remains in the faeces of anaesthetised wrasse was unsuccessful. A stomach pump based on two linked syringes was also unsuccessful, with only small fragments of lice being retrieved from two fish. The calculations of daily food consumption are based on wrasse eating only sea lice. It is probable that wrasse, once acclimatised to the cage environment, would prey mainly on sea lice and would only switch to other food items when lice were scarce. The rate of transfer of lice between fish in different pens was not assessed and is likely to occur (Bruno and Stone, 1990). It is assumed that the immigration rate from adjacent pens to the trial pens was constant (Jaworski and Holm, 1992). The number of L. saZmon2.s(26-46) consumed per wrasse per day at Loch Eil was similar to cleaning rates reported in aquaria for goldsinny, 28.3 and 45 lice respectively in separate trials, and up to 20 in a sea cage (Bjordal, 199 1). The rates of daily food consumption quoted here ( 1.2-2.7% body weight) are comparable with freshwater and marine fish of similar body weight, e.g. 2-5% in Eurasian perch, PercajluviatiZis (L.) (Thorpe, 1977), 2.4 and 3.7% in juvenile coho salmon, Oncorhynchus kisutch (Walbaum) at water temperatures of 11.4 and 13.7 “C respectively (Brodeur and Pearcy, 1987), 6% in haddock, Melanogrammus aeglifinus (L.) and 4.1% in dab, Limanda Zimanda (L.) (Hall, 1987), 510% for small ( 15-20 cm) plaice, Pleuronectes platessa L. (Basimi and Grove, 1985 ), and 7% in common sole, SoZeavulgaris Quensel (Lagardere, 1987). Some of these examples for marine fish are higher than in wrasse and, as wrasse are known to browse on nets and eat benthic organisms (Hillden, 1978; Costello, 199 1)) the data presented here are likely to be minimum estimates of daily food consumption.
Acknowledgements I am grateful to Mark Costello for helpful comments on the manuscript staff at Loch Eil fish farm for assistance during the trial.
and to
References Basimi, R.A. and Grove, D.J., 1985. Estimates of daily food intake by an inshore population of Pleuronectesplatessa L. off eastern Anglesey, North Wales. J. Fish Biol., 27: 505-520. Bjordal, A., 1990. Sea lice infestation on farmed salmon: possible use of cleaner-fish as an alternative method for de-lousing. Can. Tech. Rep. Fish. Aquat. Sci., 1761: 85-89. Bjordal, A., 199 1. Wrasse as cleaner-fish for farmed salmon. Prog. Underwater Sci., 16: 17-28. Brodeur, R.D. and Pearcy, W.G., 1987. Die1 feeding chronology, gastric evacuation and estimated daily ration of juvenile coho salmon, Oncorhynchus kisutch (Walbaum), in the coastal marine environment. J. Fish Biol., 3 1: 465-477.
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