- Email: [email protected]
Dispersal of the skin fluke Benedenia seriolae (Monogenea: Capsalidae) by tidal currents and implications for sea-cage farming of Seriola spp.
Aquaculture 250 (2005) 60 – 69 www.elsevier.com/locate/aqua-online
Dispersal of the skin fluke Benedenia seriolae (Monogenea: Capsalidae) by tidal currents and implications for sea-cage farming of Seriola spp. C.B. Chambers*, I. Ernst Environmental Biology, DP418, School of Earth and Environmental Sciences, The University of Adelaide, Adelaide, SA 5005, Australia Received 8 November 2004; received in revised form 15 April 2005; accepted 24 April 2005
Abstract Sea-cage aquaculture of Seriola lalandi (kingfish) is an emerging industry in Australia with production estimated at 2000 tonnes for 2004/2005. Infections with the monogenean Benedenia seriolae are a major barrier to efficient production and industry growth. Strategic positioning of farms and cages has been identified as a possible husbandry technique to limit parasite population growth, however little information is available on the infection dynamics of this parasite. This study investigated the effect of tidal currents on the dispersal of B. seriolae eggs and on the infection rates of B. seriolae on sentinel fish positioned near a kingfish farm. Two experiments were conducted over intra- and inter-farm scales. In the intra-farm scale experiment, egg density and infection rates at 0, 250, 500 and 1000 m across and inline with tidal current direction from a source were determined by the use of plankton tows (for egg density) and sentinel fish (for infection rates). The density of B. seriolae eggs in the plankton and infection rates on sentinel fish was lower at sites across rather than inline with current direction (no eggs were recovered at sites across tidal current). In the inter-farm scale experiment, the effect of fish farms on infection rates in surrounding waters was determined using sentinel fish placed up to 18 km from the nearest source farm. Results suggest that within the hydrographic conditions studied, dispersal of B. seriolae is considerable and distances greater than 8 km may be required for effective parasite management using independent management units. D 2005 Elsevier B.V. All rights reserved. Keywords: Infection rates; Parasite management; Monogenea; Re-infection; Parasite dispersal
1. Introduction
* Corresponding author. Fax: +61 8 8303 4364. E-mail address: [email protected] (C.B. Chambers). 0044-8486/$ - see front matter D 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.aquaculture.2005.04.061
Benedenia seriolae is an economically important monogenean parasite of kingfish (Seriola lalandi) aquaculture in Australia and Japanese yellowtail (Seriola quinqueradiata), amberjack (Seriola dumerili)
C.B. Chambers, I. Ernst / Aquaculture 250 (2005) 60–69
and kingfish aquaculture in Japan (Egusa, 1983; Whittington et al., 2001). Kingfish aquaculture in Australia is an emerging industry with current production estimated at more than 2000 tonnes for 2004/2005 (personal communication, Martin Hernen). Monogenean infections are a major concern for this industry. B. seriolae inhabits the skin and fins of Seriola spp. and feeds on mucus and epithelia cells. Without regular intervention, fluke populations can impact negatively through loss of fish growth, decreased market value due to parasite-induced damage on fish and fish mortality (Egusa, 1983; Ernst et al., 2002). In Australia, B. seriolae populations are currently managed by bathing fish in hydrogen peroxide. Bathing fish is expensive because extra personnel and infrastructure are required, feeding days are lost, fish stress is increased and the size and design of sea-cages may be limited. When a cage of fish is treated for B. seriolae infections, by far the greatest source of re-infection comes from fluke populations on surrounding stocked sea-cages; the wild kingfish population within the Spencer Gulf is considered to be small (McGlennon, 1997) and no other hosts of B. seriolae are known to occur in the upper Spencer Gulf. However, dispersal dynamics of B. seriolae within and from a farm lease are not understood. Dispersal of B. seriolae relies on egg and free-swimming larval stages. Eggs are laid freely into the water column and drift with currents until becoming entangled in structure or settling to the sea floor. Monogenean larvae are slow swimming compared to tidal currents or their hosts and are able to swim at speeds of 14.4–40 m/h (Paling, 1969; Ernst, unpublished data), depending on water temperatures (Gannicott and Tinsley, 1998). Dispersal of B. seriolae eggs and larvae to other cages of fish could therefore be limited by the strength and direction of water currents, the distance between cages and the orientation of cages with respect to current direction. Løland (1993) modelled the movement of water currents through and around floating fish farms and suggested that neutrally buoyant contaminants stay concentrated in the wake of cages over large distances. Therefore, dispersal of B. seriolae between distant cages or those orientated across prevailing currents, is likely to be less than between nearby cages or those orientated inline with prevailing currents. Understanding the influence of tidal currents on the dispersal of B. seriolae may reveal opportunities
61
to strategically position cages to decrease the re-infection of farmed fish following treatment. In addition, knowledge of dispersal dynamics for given hydrographic conditions may reveal the distance at which B. seriolae dispersal is negligible for parasite management purposes. This distance defines the extent of an independent management unit (IMU), within which cage-specific populations of worms will interact by means of egg or larval dispersal. Knowledge of IMUs is critically important for implementation of parasite and pathogen control strategies such as fallowing (Grant and Treasurer, 1994; Jackson et al., 1997; St-Hilaire et al., 2001; Rae, 2002).
2. Materials and methods Three separate experiments were conducted to determine the infection dynamics of B. seriolae within and around a kingfish farm in the upper Spencer Gulf, Australia. Initially, an experiment was conducted to determine the most appropriate sampling technique for infection rates. The second experiment aimed to determine fluke infection dynamics within the scale of a farm lease (intra-farm), and a third experiment aimed to determine the extent of an independent management unit by measuring infection rates up to 18 km from a farm lease (inter-farm). The design for each experiment is outlined below. 2.1. Study site All experiments were conducted at Fitzgerald Bay in the upper Spencer Gulf, South Australia. Two separately owned farms are located in Fitzgerald Bay with cages distributed between 5 lease sites (Fig. 1). The number of fish stocked within the Bay fluctuates seasonally but was approximately 450,000 fish at the time of experiments; infection intensity with B. seriolae was approximately 40 worms per fish. The population of wild kingfish within the Spencer Gulf is considered to be small (McGlennon, 1997) and no other hosts of B. seriolae are known to occur in the upper Spencer Gulf. Therefore the sea-caged fish within Fitzgerald Bay can be considered the primary source of infection within and around the bay and other sources of infection (e.g. wild fish) are likely to be negligible by comparison.
62
C.B. Chambers, I. Ernst / Aquaculture 250 (2005) 60–69
seriolae individuals, which turn opaque and detach immediately or within a few hours (unpublished results). Fish were then placed in sentinel cages, unfed, for 5 days. After this period, fish were removed from cages and B. seriolae removed by bathing fish individually in freshwater for 5 min. Any worms that did not immediately detach from fish were dislodged by rubbing fish surfaces with bare hands. Worms were recovered from bath water by filtering through 75 Am mesh. Worms were collected in specimen bottles, fixed with formalin and counted using a stereomicroscope. Infection rates between cages were analysed for dcageT and dfish densityT effects. 2.3. Intra-farm infection dynamics
Fig. 1. Map of the farm leases and study sites in Fitzgerald Bay and Spencer Gulf, South Australia.
2.2. Preliminary infection rate experiment Infection rates were determined in all experiments using uninfected sentinel fish (mean size 343 mm length caudal fork) placed in small experimental cages (1.5 1.5 1.8 m). Experimental cages were placed at sampling sites for several days before fish were removed and infections determined. Fish were not fed during experiments. A preliminary experiment was performed to determine the most optimal configuration for this sampling technique. Six cages (3 with 10 fish and 3 with 20 fish) were placed within 10 m of each other and suspended at a depth of 5 m. Fish were treated to remove B. seriolae in a 5-min freshwater bath. Bathing fish in freshwater for 5 min kills all B.
The most easterly (gulf-ward) kingfish lease in Fitzgerald Bay was used as the study site for this experiment and at the time of the experiment, contained several cages of infected fish that provided a source of B. seriolae infection (Fig. 1). The density of fluke eggs in the water column and the infection rates on sentinel fish at distances from the farm site were determined. Seven sampling sites were chosen including the source of infection (farm site) and sites 250 m, 500 m and 1000 m from the source of infection in directions inline with (southward) and across (eastward) tidal current (Fig. 1). Current direction was determined from a model of tidal movement in Fitzgerald Bay provided by the National Tidal Centre (Bureau of Meteorology, Australia). Densities of B. seriolae eggs in the water column were determined by performing vertical tows with a 75 Am nylon mesh plankton net. The net was 2.4 m long, had a mouth diameter of 0.33 m and a cod end weighed down with a 2 kg lead weight. Vertical tows were performed by lowering the net, cod end first, to the sea floor and then retrieving the net at a rate of approximately 0.25 m/s. The depth of each plankton tow was measured using 1 m increments marked on the tow rope. Three replicate plankton samples were taken at each site. The number of fluke larvae infecting fish at sampling sites was determined by placing 10 uninfected fish (mean size 403 mm length caudal fork) in small (1.5 1.5 1.8 m) cages. Cages were tied to floats moored at the sampling sites and suspended at a depth of 5 m. Fish were held in the cages for 10 days, unfed,
C.B. Chambers, I. Ernst / Aquaculture 250 (2005) 60–69
whereupon they were removed and processed to recover specimens of B. seriolae as described for the preliminary experiment. 2.4. Inter-farm infection dynamics The infection pressure of B. seriolae was determined at the most northeastern kingfish lease in the bay and at sites 1, 2, 4, 8, and 16 km northwards (Fig. 1). Distances were not calculated in straight lines from the source (0 km) but followed the path of water movement from the source during an incoming tide that was predicted using model outputs provided by the National Tidal Centre. Ten uninfected fish (mean size 395 mm length caudal fork) were placed in sentinel cages for a period of 7 days and were handled as described above.
63
data were transformed (log10(x + 1)) and analysed using a one-way ANOVA. Pairwise comparisons between study sites were conducted using Tukey’s Test. All analyses were performed using Genstat (v. 7, VSN International, UK).
3. Results 3.1. Preliminary experiment Prevalence of infection with B. seriolae was 100% in all cages. Infection rates did not differ significantly between cages containing similar numbers of fish, nor did infection rates differ between cages containing 10 and 20 fish (mean 11.43, S.E.M. 0.553). 3.2. Intra-farm infection dynamics
2.5. Analysis For the preliminary experiment, cages with similar numbers of fish were analysed using a one-way ANOVA. For comparisons between cages with different numbers of fish, the Kruskal–Wallis H test was utilised. For intra- and inter-farm infection dynamics
Two types of fluke eggs were recovered in the vertical plankton tows. One belonged to an unidentified monogenean, which does not infect kingfish and is not considered here further. The second egg type belonged to B. seriolae. B. seriolae eggs were recovered from the water column at the source, and 250 m, across
1.8
inline
Mean eggs m-3 (log10(y+1))
1.6 1.4 1.2 1 0.8 0.6 0.4 0.2 0 0
0.25
0.5
1
Distance (km) Fig. 2. Density of Benedenia seriolae eggs in the water column at distances both across and inline with direction of tidal current from a source of infection (error bars indicate pooled S.E.M.).
64
C.B. Chambers, I. Ernst / Aquaculture 250 (2005) 60–69
Table 1 Infection rates for Benedenia seriolae for distances both inline with and across tidal current from a source of infection in Spencer Gulf, Australia (data is log10(x + 1) transformed and pooled standard error of the mean (S.E.M.) given) Distance from source
Mean abundance log10(x + 1) (FS.E.M.)
Source 1.738 Inline with current 250 m l 1.705 500 m 1.620 1000 m 1.584 Across current 250 m 1.449 500 m 1.390 1000 m 1.163
(F 0.035)
% of source infection pressure 100
Infection rate (1 worm per fish per unit time) 4.4 h
(F 0.035) (F 0.035) (F 0.035)
94.1 77.2 70.8
4.7 h 5.7 h 6.2 h
(F 0.035) (F 0.035) (F 0.035)
51.5 44.1 26.1
8.6 h 10.0 h 16.9 h
500 m and 1000 m from the source inline with tidal current. However, no eggs were recovered at sites across tidal current (Fig. 2). B. seriolae infections were recorded on sentinel fish at all sampling sites (prevalence 100% within each site). All B. seriolae individuals were less than 1.5 mm in length, indicating that they were 10 days old or less for the water temperatures experienced (unpub-
lished data). Infection rates were highest at the source (within the lease site) and decreased with increasing distance in both directions inline with and across tidal current (Table 1) (Fig. 3). Infection rates at sites across tidal current were significantly lower than those at corresponding distances inline ( P b 0.05). This difference was marked and infection rates at the 250 m across site were comparable (not significantly different) to infection rates at the 1000 m inline site. 3.3. Inter-farm infection dynamics The sentinel cage placed at the 16 km site dragged moorings to 18 km within the first 24 h of the experiment. Due to strong currents and unsuitable substrate for moorings at 16 km, it was decided to leave this cage at 18 km. Infection with B. seriolae was recorded at all study sites. Prevalence of infection within sites was 100% for 0, 1, 2, and 4 km and 60% and 20% for 8 and 18 km sites respectively. All B. seriolae individuals were less than 0.7 mm in length, indicating that they were 7 days old or less for the water temperatures encountered (unpublished data). Infection rates ranged from 1.470 worms/fish/day (log10(x + 1)
1.9
Mean B. seriolae abundance (log10(y+1))
across inline
1.8 1.7 1.6 1.5 1.4 1.3 1.2 1.1 1 0
0.25
0.5
1
Distance (km) Fig. 3. The mean abundance of Benedenia seriolae per fish over 10 days at distances both across and inline with the direction of tidal current from a source of infection (error bars indicate pooled S.E.M.).
C.B. Chambers, I. Ernst / Aquaculture 250 (2005) 60–69 Table 2 Infection rates for B. seriolae for distances inline with tidal current from a source of infection in Spencer Gulf, Australia (data is log10(x + 1) transformed and pooled standard error of the mean (S.E.M.) given) Distance inline with current from source (km)
Mean abundance log10(x + 1) (F S.E.M.)
% of source infection pressure
Infection rate (1 worm per fish per unit time)
0 1 2 4 8 18
1.470 1.159 1.062 0.640 0.276 0.067
100 48.3 37.4 13.9 3.7 0.7
5.7 h 11.8 h 15.3 h 40.7 h 6.3 days 33.3 days
(F0.056) (F0.056) (F0.056) (F0.056) (F0.056) (F0.056)
65
4. Discussion The present study investigated the effects of tidal currents on egg dispersal and infection rates of B. seriolae. Two experiments were conducted on different scales. The first experiment investigated dispersal dynamics on an intra-farm scale (up to 1km). The second experiment investigated infection dynamics on a larger, inter-farm scale (up to 18 km) with the aim of determining the appropriate size of independent management units (IMUs) for B. seriolae. At the intra-farm scale, dispersal of B. seriolae was strongly influenced by the direction of tidal currents. Eggs of B. seriolae were recovered from the water column only at sites inline with the tidal current, and infection rates on sentinel fish were higher at sites inline with rather than across current direction. At the inter-farm scale, infection rates on sentinel fish decreased with increasing distance from the source. At 8 and 18 km from the source, infection rates were 3.7 and 0.7% of those at the source.
transformed) at the source to 0.067 worms/fish/day (log10(x + 1) transformed) at the 18 km site (Table 2). Infection rates decreased significantly with increasing distance from the source of infection. The relationship between distance and infection rates was linear when distance was log transformed (infection rate = 1.5288– 1.1992*distance; R 2 = 0.974; P b 0.001) (Fig. 4). 1.8
Mean B. seriolae abundance (log10(y+1))
1.6
1.4
1.2
1
0.8
0.6
0.4
0.2
0 0
0.2
0.4
0.6
0.8
1
1.2
1.4
Distance (log10(km+1)) Fig. 4. The mean abundance of Benedenia seriolae per fish over 7 days at distances in line with tidal current from a source of infection. Trend line indicates linear regression ( y = 1.5288–1.1992x; R 2 = 0.974; P b 0.001). Error bars indicate pooled S.E.M.
66
C.B. Chambers, I. Ernst / Aquaculture 250 (2005) 60–69
Sea cages are often organised in rows inline with current direction because this arrangement allows operational efficiencies, efficient mooring systems and aids in maintaining net-pen shape. However this arrangement can be disadvantageous because water flow through cages may be slowed and dissolved oxygen levels reduced (Løland, 1993). This layout is also likely to enhance transmission of pathogens and parasites between cages. Løland (1993) demonstrated that neutrally buoyant particles are likely to accumulate in the wake of sea cages and our results indicate a similar dispersal pattern for eggs of B. seriolae. We found no eggs in plankton samples at sites across current direction but eggs were found at all sampling sites inline with current direction up to 1 km from the source. This pattern of egg dispersal was reflected in infection rates recorded from sentinel fish at the same sampling sites. However the distribution of infection rates was more uniform among sites across and inline with current direction when compared to planktonic egg density. This result could be expected for 2 reasons: 1) it is conceivable that egg dispersal continues across the sea floor for several days while eggs embryonate and 2) B. seriolae larvae are free-swimming and may disperse in tidal currents for the duration of their life, which was estimated by Hoshina (1968) to be 24 h. Infection rates at sites across current direction were however lower than those at sites inline with current direction and this pattern of infection may provide an opportunity to manage infection by strategic arrangement of cages. The infection pressure that we measured at each sampling site, expressed as a percentage of infection at the source (Table 1 and 2), may provide a suitable estimate of parasite population interaction between 2 sites orientated either across or inline with current direction. In our experiment, fish at sites 250 m from the source in directions across and inline with current direction had infection rates that were 52% and 94% of those at the source. It is plausible that these infection rates represent the level of interaction between B. seriolae populations on separate, similarly orientated sea-cages containing kingfish. At the intrafarm scale, these levels of interaction (range 26% to 94%; see Table 1) would prevent independent, longterm parasite management of individual sea-cages because re-infection following treatment would be rapid and proportional to that of adjacent, untreated
cages. However, population growth could be slower for cages arranged across current direction because interaction between cage-specific parasite populations would be reduced, resulting in lower cumulative infection rates among all cages. Slower population growth is clearly advantageous because intervals between parasite treatments, which are both stressful to fish and costly, may be extended. Effective, long-term management of parasite populations in sea-cage aquaculture requires coordinated management of all interacting parasite populations within an IMU. Spatially coordinated approaches to parasite management have been particularly successful for the control of sea-lice infections on sea-caged salmon where treatments, stocking and fallowing are coordinated temporally within an IMU (Grant and Treasurer, 1994; Jackson et al., 1997; Rae, 2002). In the case of salmonid aquaculture, farming sites are often located within bays, fjords, lochs or estuaries that provide a logical basis for designation of IMUs. Such designation is supported by studies on planktonic dispersal of sea lice (Lepeophtheirus salmonis Kroyer) larvae (Costelloe et al., 1996; Costelloe et al., 1998). Although single year class stocking of sites and fallowing have been important strategies for managing sea lice infections on salmonids these same strategies have not been used for the control of B. seriolae infections of kingfish in Australia or of Japanese yellowtail (S. quinqueradiata), amberjack (S. dumerili) or kingfish in Japan. In Australia, B. seriolae infections on kingfish are managed using coordinated treatments that are timed to interrupt the parasite’s life cycle. These coordinated treatments rely on precise timing to ensure that all reinfecting parasites are killed following an initial round of treatments. Although temporal coordination must be precise, spatial coordination of these treatments has required little consideration because most kingfish farms in Spencer Gulf are isolated (may be more than 100 km from the nearest neighbouring farm) and, as a result, each can be treated as an IMU. However with the predicted growth of the kingfish industry in South Australia, and the practical limitations of coordinated treatments (all cages within a farm must be treated within a short period of time), other management strategies such as fallowing may be required. For fallowing strategies to be effective it is important that separate year class sites are chosen that
C.B. Chambers, I. Ernst / Aquaculture 250 (2005) 60–69
are separated by distances that allow minimal or almost no interaction of parasite populations; i.e. each year class site must be within a separate IMU. In this study, we found infection rates at 4, 8 and 18 km to be equivalent to infection by a single B. seriolae per fish every 1.4, 6.3 and 33.3 days. At 4 km from the source, the infection rate was clearly above that required for independent management of populations because uninfected fish exposed to this rate of infection (1 worm/fish/1.4 days) would quickly develop their own self sustaining parasite populations. At 8 km from the source, the infection rate was lower (1 worm/fish/6.3 days) and parasite populations could be expected to grow more slowly. However in this case, significant populations of mature parasites would be expected within a period of several months. At 18 km from the source, the infection rate was equivalent to 1 worm/fish every 33 days. This infection rate is clearly low and would result in very slow parasite population growth, even if survival for recruiting parasites were high or if warm temperatures allowed rapid maturity of recruiting parasites. It is possible that some component of the infection rates measured in this study are due to background infection from parasites infecting wild populations of kingfish that are not associated with kingfish farms. However any background infection of B. seriolae is likely to be inconsequential in comparison to the magnitude of infection within sea-cages for 2 reasons. First, wild kingfish populations within Spencer Gulf are small (McGlennon, 1997) and kingfish are thought to migrate into the gulf seasonally. Second, the maximum possible background infection indicated by our study was 0.03 worms/fish/day recorded at the 18 km site. We propose that under the hydrographic conditions of this study a distance of greater than 8 km may be required to designate separate IMUs that are positioned inline with current direction. This study has demonstrated that IMUs required for B. seriolae in the upper Spencer Gulf are large (N 8 km), however it should be noted that this study was designed to detect maximum parasite dispersal. The study was performed at a time when large populations of B. seriolae were present on sea-caged fish (immediately prior to a round of treatments), and during a 7day period of the tidal cycle with the greatest tidal movement (2.4 m vertically). Furthermore, Fitzgerald Bay has the highest tidal current velocities of all
67
kingfish farming areas in Spencer Gulf and our sampling sites were chosen carefully to ensure all sites were inline with the tidal currents flowing from the source farm. The distance between designated IMUs could be much smaller in other locations in Spencer Gulf where tidal currents are slower or where IMUs are positioned across current direction. We have studied the infection dynamics of B. seriolae, but Zeuxapta seriolae is another important monogenean parasite of S. lalandi that requires concurrent management with B. seriolae. Z. seriolae is a gill-dwelling blood-feeder with biological characteristics that differ substantially from B. seriolae. These different biological characteristics could result in different dispersal capabilities and consequently different requirements for designating IMUs. For both parasite species, dispersal could be affected by egg sedimentation rates, egg morphology, egg developmental periods, larval longevity, larval swimming speed and larval behaviour. The morphology of monogenean eggs is known to vary widely and is likely to affect dispersal of eggs after they are laid into the water column (Kearn, 1986). Eggs of B. seriolae are laid individually and possess a single filament that is approximately 2 mm long (Kearn et al., 1992), whereas those of Z. seriolae are laid in groups of several hundred eggs connected together by their filaments (Mooney et al., in press). The begg stringsQ of Z. seriolae are more likely to entangle on structures than the individual eggs of B. seriolae, and Z. seriolae eggs are also known to have faster sedimentation rates (Ernst, unpublished data). These factors combined could contribute to more limited dispersal of Z. seriolae eggs from sea-caged fish compared to eggs of B. seriolae. Seasonal factors could also contribute to dispersal of monogenean eggs because temperature is known to affect embryonation period strongly (Kearn, 1986; Ernst et al., 2005). At low temperatures, eggs take longer to develop before hatching, would be exposed to more tidal cycles, and could be dispersed further along the seafloor. The longevity and behaviour of monogenean larvae are likely to have considerable impact on the ability of larvae to disperse. The larvae of B. seriolae and Z. seriolae are free-swimming, allowing them to adjust their orientation in water currents and potentially maximise dispersal. Hoshina (1968) reported
68
C.B. Chambers, I. Ernst / Aquaculture 250 (2005) 60–69
that larvae of B. seriolae survive for approximately 1 day (temperature not stated), which would allow dispersal throughout few tidal cycles. Larval longevity for Z. seriolae is unknown but larvae of the related parasite Heterobothrium okamotoi, which infects seacaged tiger puffer (Takifugu rubripes), have been studied. Larval longevity for H. okamotoi is much longer (9.1 days at 15 8C; 4.7 days at 25 8C; Ogawa, 1998) than for B. seriolae and could result in far greater larval dispersal over distances inline with and across tidal currents.
5. Conclusion The kingfish industry in Australia is growing rapidly but faces the significant challenge of managing potentially damaging monogenean infections. We have presented results that indicate that strategic cage orientation could reduce interaction between cage-specific B. seriolae populations and therefore reduce population growth. This strategy is feasible in Australia because most farms have relatively few cages, with individual moorings, located on large leases. Careful consideration of improved management practices such as year class separation and fallowing will be required as the industry grows and treatment-orientated management becomes impractical. Our results suggest that IMUs for B. seriolae may need to be separated by more than 8 km (and possibly up to 18 km) if positioned inline with current direction.
Acknowledgements We would like to thank the South Australian Aquaculture Management for providing the facilities and fish to make this study possible, and Allan Mooney for assistance in the field. We thank the National Tidal Centre (Bureau of Meteorology) for providing tidal modelling of the Spencer Gulf. This work was supported by an Australian Research Council Grant LP0211375 (awarded to Ian Whittington and Ingo Ernst). Contributing industry partners include Yamaha Nutreco Aquatech, Skretting Australia and the South Australian Marine Finfish Farmers Association.
References Costelloe, M., Costelloe, J., Roche, N., 1996. Planktonic dispersion of larval salmon-lice, Lepeophtheirus salmonis, associated with cultured salmon, Salmo salar, in Western Ireland. J. Mar. Biol. Assoc. U.K. 76, 141 – 149. Costelloe, M., Costelloe, J., O’Donohoe, G., Coghlan, N.J., Oonk, M., Van der Heijden, Y., 1998. Planktonic distribution of sea lice larvae, Lepeophtheirus salmonis, in Killary Harbour, West Coast of Ireland. J. Mar. Biol. Assoc. U.K. 78, 853 – 874. Egusa, S., 1983. Disease problems in Japanese yellowtail, Seriola quinqueradiata, culture: a review. Rapp. P.-V. Reun.-Cons. Int. Explor. Mer 182, 10 – 18. Ernst, I., Whittington, I.D., Corneillie, S., Talbot, C., 2002. Monogenean parasites in sea-cage aquaculture. Austasia Aquac., 46 – 48 (February/March). Ernst, I., Whittington, I.D., Corneillie, S., Talbot, C., 2005. Effects of temperature, salinity, desication and chemical treatments on egg embryonation and hatching success of Benedenia seriolae (Monogenea: Capsalidae), a parasite of farmed Seriola spp. J. Fish Dis. 28, 157 – 164. Gannicott, A.M., Tinsley, R.C., 1998. Larval survival characteristics and behaviour of the gill monogenean Discocotyle sagittata. Parasitology 117, 491 – 498. Grant, A.N., Treasurer, J.W., 1994. The effects of fallowing on caligid infestations on farmed Atlantic salmon (Salmo salar L.) in Scotland. In: Boxshall, G.A., Defaye, D. (Eds.), Pathogens of Wild and Farmed Salmon. Ellis Horwood, New York, pp. 255 – 260. Hoshina, T., 1968. On the monogenetic trematode, Benedenia seriolae, parasitic on yellowtail, Seriola quinqueradiata. Bull.-Off. Int. E´pizoot. 69, 1179 – 1191. Jackson, D., Deady, S., Leahy, Y., Hassett, D., 1997. Variations in parasitic caligid infestations of farmed salmonids and implications for their management. ICES J. Mar. Sci. 54, 1104 – 1112. Kearn, G.C., 1986. The eggs of monogeneans. Adv. Parasitol. 25, 175 – 273. Kearn, G.C., Ogawa, K., Maeno, Y., 1992. Egg production, the oncomiracidium and larval development of Benedenia seriolae, a skin parasite of the yellowtail, Seriola quinqueradiata, in Japan. Publ. Seto Mar. Biol. Lab. 35, 351 – 362. Løland, G., 1993. Current forces on, and water flow through and around, floating fish farms. Aquac. Int. 1, 72 – 89. McGlennon, D., 1997. Report to the Scalefish Management Committee on Yellowtail Kingfish (Seriola lalandi). South Australian Research and Development Institute, Adelaide. Mooney, A.J., Ersnt, I., Whittington, I.D., in press. An egglaying rhythm in Zeuxapta seriolae (Monogenea: Heteraxinidae), a gill parasite of yellowtail kingfish (Seriola lalandi). Aquaculture. Ogawa, K., 1998. Egg hatching of the monogenean Heterobothrium okamotoi, a gill parasite of cultured tiger puffer (Takifugu rubripes), with a description of its oncomiracidium. Fish Pathol. 33, 25 – 30. Paling, J.E., 1969. The manner of infection of trout gills by the monogenean parasite Discocotyle sagittata. J. Zool. 159, 293 – 309.
C.B. Chambers, I. Ernst / Aquaculture 250 (2005) 60–69 Rae, G.H., 2002. Sea louse control in Scotland, past and present. Pest Manag. Sci. 58, 515 – 520. St-Hilaire, S., Stephen, C., Kent, M., Ribble, C., 2001. Sentinels in the bay: using farm fish to monitor for pathogens in the environment. ICES J. Mar. Sci. 58, 369 – 373.
69
Whittington, I.D., Corneillie, S., Talbot, C., Morgan, J.A.T., Adlard, R.D., 2001. Infections of Seriola quinqueradiata Temminck and Schlegel and S. dumerili (Risso) in Japan by Benedenia seriolae (Monogenea) confirmed by morphology and 28S ribosomal DNA analysis. J. Fish Dis. 24, 421 – 425.
Dispersal of the skin fluke Benedenia seriolae (Monogenea: Capsalidae) by tidal currents and implications for sea-cage farming of Seriola spp. C.B. Chambers*, I. Ernst Environmental Biology, DP418, School of Earth and Environmental Sciences, The University of Adelaide, Adelaide, SA 5005, Australia Received 8 November 2004; received in revised form 15 April 2005; accepted 24 April 2005
Abstract Sea-cage aquaculture of Seriola lalandi (kingfish) is an emerging industry in Australia with production estimated at 2000 tonnes for 2004/2005. Infections with the monogenean Benedenia seriolae are a major barrier to efficient production and industry growth. Strategic positioning of farms and cages has been identified as a possible husbandry technique to limit parasite population growth, however little information is available on the infection dynamics of this parasite. This study investigated the effect of tidal currents on the dispersal of B. seriolae eggs and on the infection rates of B. seriolae on sentinel fish positioned near a kingfish farm. Two experiments were conducted over intra- and inter-farm scales. In the intra-farm scale experiment, egg density and infection rates at 0, 250, 500 and 1000 m across and inline with tidal current direction from a source were determined by the use of plankton tows (for egg density) and sentinel fish (for infection rates). The density of B. seriolae eggs in the plankton and infection rates on sentinel fish was lower at sites across rather than inline with current direction (no eggs were recovered at sites across tidal current). In the inter-farm scale experiment, the effect of fish farms on infection rates in surrounding waters was determined using sentinel fish placed up to 18 km from the nearest source farm. Results suggest that within the hydrographic conditions studied, dispersal of B. seriolae is considerable and distances greater than 8 km may be required for effective parasite management using independent management units. D 2005 Elsevier B.V. All rights reserved. Keywords: Infection rates; Parasite management; Monogenea; Re-infection; Parasite dispersal
1. Introduction
* Corresponding author. Fax: +61 8 8303 4364. E-mail address: [email protected] (C.B. Chambers). 0044-8486/$ - see front matter D 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.aquaculture.2005.04.061
Benedenia seriolae is an economically important monogenean parasite of kingfish (Seriola lalandi) aquaculture in Australia and Japanese yellowtail (Seriola quinqueradiata), amberjack (Seriola dumerili)
C.B. Chambers, I. Ernst / Aquaculture 250 (2005) 60–69
and kingfish aquaculture in Japan (Egusa, 1983; Whittington et al., 2001). Kingfish aquaculture in Australia is an emerging industry with current production estimated at more than 2000 tonnes for 2004/2005 (personal communication, Martin Hernen). Monogenean infections are a major concern for this industry. B. seriolae inhabits the skin and fins of Seriola spp. and feeds on mucus and epithelia cells. Without regular intervention, fluke populations can impact negatively through loss of fish growth, decreased market value due to parasite-induced damage on fish and fish mortality (Egusa, 1983; Ernst et al., 2002). In Australia, B. seriolae populations are currently managed by bathing fish in hydrogen peroxide. Bathing fish is expensive because extra personnel and infrastructure are required, feeding days are lost, fish stress is increased and the size and design of sea-cages may be limited. When a cage of fish is treated for B. seriolae infections, by far the greatest source of re-infection comes from fluke populations on surrounding stocked sea-cages; the wild kingfish population within the Spencer Gulf is considered to be small (McGlennon, 1997) and no other hosts of B. seriolae are known to occur in the upper Spencer Gulf. However, dispersal dynamics of B. seriolae within and from a farm lease are not understood. Dispersal of B. seriolae relies on egg and free-swimming larval stages. Eggs are laid freely into the water column and drift with currents until becoming entangled in structure or settling to the sea floor. Monogenean larvae are slow swimming compared to tidal currents or their hosts and are able to swim at speeds of 14.4–40 m/h (Paling, 1969; Ernst, unpublished data), depending on water temperatures (Gannicott and Tinsley, 1998). Dispersal of B. seriolae eggs and larvae to other cages of fish could therefore be limited by the strength and direction of water currents, the distance between cages and the orientation of cages with respect to current direction. Løland (1993) modelled the movement of water currents through and around floating fish farms and suggested that neutrally buoyant contaminants stay concentrated in the wake of cages over large distances. Therefore, dispersal of B. seriolae between distant cages or those orientated across prevailing currents, is likely to be less than between nearby cages or those orientated inline with prevailing currents. Understanding the influence of tidal currents on the dispersal of B. seriolae may reveal opportunities
61
to strategically position cages to decrease the re-infection of farmed fish following treatment. In addition, knowledge of dispersal dynamics for given hydrographic conditions may reveal the distance at which B. seriolae dispersal is negligible for parasite management purposes. This distance defines the extent of an independent management unit (IMU), within which cage-specific populations of worms will interact by means of egg or larval dispersal. Knowledge of IMUs is critically important for implementation of parasite and pathogen control strategies such as fallowing (Grant and Treasurer, 1994; Jackson et al., 1997; St-Hilaire et al., 2001; Rae, 2002).
2. Materials and methods Three separate experiments were conducted to determine the infection dynamics of B. seriolae within and around a kingfish farm in the upper Spencer Gulf, Australia. Initially, an experiment was conducted to determine the most appropriate sampling technique for infection rates. The second experiment aimed to determine fluke infection dynamics within the scale of a farm lease (intra-farm), and a third experiment aimed to determine the extent of an independent management unit by measuring infection rates up to 18 km from a farm lease (inter-farm). The design for each experiment is outlined below. 2.1. Study site All experiments were conducted at Fitzgerald Bay in the upper Spencer Gulf, South Australia. Two separately owned farms are located in Fitzgerald Bay with cages distributed between 5 lease sites (Fig. 1). The number of fish stocked within the Bay fluctuates seasonally but was approximately 450,000 fish at the time of experiments; infection intensity with B. seriolae was approximately 40 worms per fish. The population of wild kingfish within the Spencer Gulf is considered to be small (McGlennon, 1997) and no other hosts of B. seriolae are known to occur in the upper Spencer Gulf. Therefore the sea-caged fish within Fitzgerald Bay can be considered the primary source of infection within and around the bay and other sources of infection (e.g. wild fish) are likely to be negligible by comparison.
62
C.B. Chambers, I. Ernst / Aquaculture 250 (2005) 60–69
seriolae individuals, which turn opaque and detach immediately or within a few hours (unpublished results). Fish were then placed in sentinel cages, unfed, for 5 days. After this period, fish were removed from cages and B. seriolae removed by bathing fish individually in freshwater for 5 min. Any worms that did not immediately detach from fish were dislodged by rubbing fish surfaces with bare hands. Worms were recovered from bath water by filtering through 75 Am mesh. Worms were collected in specimen bottles, fixed with formalin and counted using a stereomicroscope. Infection rates between cages were analysed for dcageT and dfish densityT effects. 2.3. Intra-farm infection dynamics
Fig. 1. Map of the farm leases and study sites in Fitzgerald Bay and Spencer Gulf, South Australia.
2.2. Preliminary infection rate experiment Infection rates were determined in all experiments using uninfected sentinel fish (mean size 343 mm length caudal fork) placed in small experimental cages (1.5 1.5 1.8 m). Experimental cages were placed at sampling sites for several days before fish were removed and infections determined. Fish were not fed during experiments. A preliminary experiment was performed to determine the most optimal configuration for this sampling technique. Six cages (3 with 10 fish and 3 with 20 fish) were placed within 10 m of each other and suspended at a depth of 5 m. Fish were treated to remove B. seriolae in a 5-min freshwater bath. Bathing fish in freshwater for 5 min kills all B.
The most easterly (gulf-ward) kingfish lease in Fitzgerald Bay was used as the study site for this experiment and at the time of the experiment, contained several cages of infected fish that provided a source of B. seriolae infection (Fig. 1). The density of fluke eggs in the water column and the infection rates on sentinel fish at distances from the farm site were determined. Seven sampling sites were chosen including the source of infection (farm site) and sites 250 m, 500 m and 1000 m from the source of infection in directions inline with (southward) and across (eastward) tidal current (Fig. 1). Current direction was determined from a model of tidal movement in Fitzgerald Bay provided by the National Tidal Centre (Bureau of Meteorology, Australia). Densities of B. seriolae eggs in the water column were determined by performing vertical tows with a 75 Am nylon mesh plankton net. The net was 2.4 m long, had a mouth diameter of 0.33 m and a cod end weighed down with a 2 kg lead weight. Vertical tows were performed by lowering the net, cod end first, to the sea floor and then retrieving the net at a rate of approximately 0.25 m/s. The depth of each plankton tow was measured using 1 m increments marked on the tow rope. Three replicate plankton samples were taken at each site. The number of fluke larvae infecting fish at sampling sites was determined by placing 10 uninfected fish (mean size 403 mm length caudal fork) in small (1.5 1.5 1.8 m) cages. Cages were tied to floats moored at the sampling sites and suspended at a depth of 5 m. Fish were held in the cages for 10 days, unfed,
C.B. Chambers, I. Ernst / Aquaculture 250 (2005) 60–69
whereupon they were removed and processed to recover specimens of B. seriolae as described for the preliminary experiment. 2.4. Inter-farm infection dynamics The infection pressure of B. seriolae was determined at the most northeastern kingfish lease in the bay and at sites 1, 2, 4, 8, and 16 km northwards (Fig. 1). Distances were not calculated in straight lines from the source (0 km) but followed the path of water movement from the source during an incoming tide that was predicted using model outputs provided by the National Tidal Centre. Ten uninfected fish (mean size 395 mm length caudal fork) were placed in sentinel cages for a period of 7 days and were handled as described above.
63
data were transformed (log10(x + 1)) and analysed using a one-way ANOVA. Pairwise comparisons between study sites were conducted using Tukey’s Test. All analyses were performed using Genstat (v. 7, VSN International, UK).
3. Results 3.1. Preliminary experiment Prevalence of infection with B. seriolae was 100% in all cages. Infection rates did not differ significantly between cages containing similar numbers of fish, nor did infection rates differ between cages containing 10 and 20 fish (mean 11.43, S.E.M. 0.553). 3.2. Intra-farm infection dynamics
2.5. Analysis For the preliminary experiment, cages with similar numbers of fish were analysed using a one-way ANOVA. For comparisons between cages with different numbers of fish, the Kruskal–Wallis H test was utilised. For intra- and inter-farm infection dynamics
Two types of fluke eggs were recovered in the vertical plankton tows. One belonged to an unidentified monogenean, which does not infect kingfish and is not considered here further. The second egg type belonged to B. seriolae. B. seriolae eggs were recovered from the water column at the source, and 250 m, across
1.8
inline
Mean eggs m-3 (log10(y+1))
1.6 1.4 1.2 1 0.8 0.6 0.4 0.2 0 0
0.25
0.5
1
Distance (km) Fig. 2. Density of Benedenia seriolae eggs in the water column at distances both across and inline with direction of tidal current from a source of infection (error bars indicate pooled S.E.M.).
64
C.B. Chambers, I. Ernst / Aquaculture 250 (2005) 60–69
Table 1 Infection rates for Benedenia seriolae for distances both inline with and across tidal current from a source of infection in Spencer Gulf, Australia (data is log10(x + 1) transformed and pooled standard error of the mean (S.E.M.) given) Distance from source
Mean abundance log10(x + 1) (FS.E.M.)
Source 1.738 Inline with current 250 m l 1.705 500 m 1.620 1000 m 1.584 Across current 250 m 1.449 500 m 1.390 1000 m 1.163
(F 0.035)
% of source infection pressure 100
Infection rate (1 worm per fish per unit time) 4.4 h
(F 0.035) (F 0.035) (F 0.035)
94.1 77.2 70.8
4.7 h 5.7 h 6.2 h
(F 0.035) (F 0.035) (F 0.035)
51.5 44.1 26.1
8.6 h 10.0 h 16.9 h
500 m and 1000 m from the source inline with tidal current. However, no eggs were recovered at sites across tidal current (Fig. 2). B. seriolae infections were recorded on sentinel fish at all sampling sites (prevalence 100% within each site). All B. seriolae individuals were less than 1.5 mm in length, indicating that they were 10 days old or less for the water temperatures experienced (unpub-
lished data). Infection rates were highest at the source (within the lease site) and decreased with increasing distance in both directions inline with and across tidal current (Table 1) (Fig. 3). Infection rates at sites across tidal current were significantly lower than those at corresponding distances inline ( P b 0.05). This difference was marked and infection rates at the 250 m across site were comparable (not significantly different) to infection rates at the 1000 m inline site. 3.3. Inter-farm infection dynamics The sentinel cage placed at the 16 km site dragged moorings to 18 km within the first 24 h of the experiment. Due to strong currents and unsuitable substrate for moorings at 16 km, it was decided to leave this cage at 18 km. Infection with B. seriolae was recorded at all study sites. Prevalence of infection within sites was 100% for 0, 1, 2, and 4 km and 60% and 20% for 8 and 18 km sites respectively. All B. seriolae individuals were less than 0.7 mm in length, indicating that they were 7 days old or less for the water temperatures encountered (unpublished data). Infection rates ranged from 1.470 worms/fish/day (log10(x + 1)
1.9
Mean B. seriolae abundance (log10(y+1))
across inline
1.8 1.7 1.6 1.5 1.4 1.3 1.2 1.1 1 0
0.25
0.5
1
Distance (km) Fig. 3. The mean abundance of Benedenia seriolae per fish over 10 days at distances both across and inline with the direction of tidal current from a source of infection (error bars indicate pooled S.E.M.).
C.B. Chambers, I. Ernst / Aquaculture 250 (2005) 60–69 Table 2 Infection rates for B. seriolae for distances inline with tidal current from a source of infection in Spencer Gulf, Australia (data is log10(x + 1) transformed and pooled standard error of the mean (S.E.M.) given) Distance inline with current from source (km)
Mean abundance log10(x + 1) (F S.E.M.)
% of source infection pressure
Infection rate (1 worm per fish per unit time)
0 1 2 4 8 18
1.470 1.159 1.062 0.640 0.276 0.067
100 48.3 37.4 13.9 3.7 0.7
5.7 h 11.8 h 15.3 h 40.7 h 6.3 days 33.3 days
(F0.056) (F0.056) (F0.056) (F0.056) (F0.056) (F0.056)
65
4. Discussion The present study investigated the effects of tidal currents on egg dispersal and infection rates of B. seriolae. Two experiments were conducted on different scales. The first experiment investigated dispersal dynamics on an intra-farm scale (up to 1km). The second experiment investigated infection dynamics on a larger, inter-farm scale (up to 18 km) with the aim of determining the appropriate size of independent management units (IMUs) for B. seriolae. At the intra-farm scale, dispersal of B. seriolae was strongly influenced by the direction of tidal currents. Eggs of B. seriolae were recovered from the water column only at sites inline with the tidal current, and infection rates on sentinel fish were higher at sites inline with rather than across current direction. At the inter-farm scale, infection rates on sentinel fish decreased with increasing distance from the source. At 8 and 18 km from the source, infection rates were 3.7 and 0.7% of those at the source.
transformed) at the source to 0.067 worms/fish/day (log10(x + 1) transformed) at the 18 km site (Table 2). Infection rates decreased significantly with increasing distance from the source of infection. The relationship between distance and infection rates was linear when distance was log transformed (infection rate = 1.5288– 1.1992*distance; R 2 = 0.974; P b 0.001) (Fig. 4). 1.8
Mean B. seriolae abundance (log10(y+1))
1.6
1.4
1.2
1
0.8
0.6
0.4
0.2
0 0
0.2
0.4
0.6
0.8
1
1.2
1.4
Distance (log10(km+1)) Fig. 4. The mean abundance of Benedenia seriolae per fish over 7 days at distances in line with tidal current from a source of infection. Trend line indicates linear regression ( y = 1.5288–1.1992x; R 2 = 0.974; P b 0.001). Error bars indicate pooled S.E.M.
66
C.B. Chambers, I. Ernst / Aquaculture 250 (2005) 60–69
Sea cages are often organised in rows inline with current direction because this arrangement allows operational efficiencies, efficient mooring systems and aids in maintaining net-pen shape. However this arrangement can be disadvantageous because water flow through cages may be slowed and dissolved oxygen levels reduced (Løland, 1993). This layout is also likely to enhance transmission of pathogens and parasites between cages. Løland (1993) demonstrated that neutrally buoyant particles are likely to accumulate in the wake of sea cages and our results indicate a similar dispersal pattern for eggs of B. seriolae. We found no eggs in plankton samples at sites across current direction but eggs were found at all sampling sites inline with current direction up to 1 km from the source. This pattern of egg dispersal was reflected in infection rates recorded from sentinel fish at the same sampling sites. However the distribution of infection rates was more uniform among sites across and inline with current direction when compared to planktonic egg density. This result could be expected for 2 reasons: 1) it is conceivable that egg dispersal continues across the sea floor for several days while eggs embryonate and 2) B. seriolae larvae are free-swimming and may disperse in tidal currents for the duration of their life, which was estimated by Hoshina (1968) to be 24 h. Infection rates at sites across current direction were however lower than those at sites inline with current direction and this pattern of infection may provide an opportunity to manage infection by strategic arrangement of cages. The infection pressure that we measured at each sampling site, expressed as a percentage of infection at the source (Table 1 and 2), may provide a suitable estimate of parasite population interaction between 2 sites orientated either across or inline with current direction. In our experiment, fish at sites 250 m from the source in directions across and inline with current direction had infection rates that were 52% and 94% of those at the source. It is plausible that these infection rates represent the level of interaction between B. seriolae populations on separate, similarly orientated sea-cages containing kingfish. At the intrafarm scale, these levels of interaction (range 26% to 94%; see Table 1) would prevent independent, longterm parasite management of individual sea-cages because re-infection following treatment would be rapid and proportional to that of adjacent, untreated
cages. However, population growth could be slower for cages arranged across current direction because interaction between cage-specific parasite populations would be reduced, resulting in lower cumulative infection rates among all cages. Slower population growth is clearly advantageous because intervals between parasite treatments, which are both stressful to fish and costly, may be extended. Effective, long-term management of parasite populations in sea-cage aquaculture requires coordinated management of all interacting parasite populations within an IMU. Spatially coordinated approaches to parasite management have been particularly successful for the control of sea-lice infections on sea-caged salmon where treatments, stocking and fallowing are coordinated temporally within an IMU (Grant and Treasurer, 1994; Jackson et al., 1997; Rae, 2002). In the case of salmonid aquaculture, farming sites are often located within bays, fjords, lochs or estuaries that provide a logical basis for designation of IMUs. Such designation is supported by studies on planktonic dispersal of sea lice (Lepeophtheirus salmonis Kroyer) larvae (Costelloe et al., 1996; Costelloe et al., 1998). Although single year class stocking of sites and fallowing have been important strategies for managing sea lice infections on salmonids these same strategies have not been used for the control of B. seriolae infections of kingfish in Australia or of Japanese yellowtail (S. quinqueradiata), amberjack (S. dumerili) or kingfish in Japan. In Australia, B. seriolae infections on kingfish are managed using coordinated treatments that are timed to interrupt the parasite’s life cycle. These coordinated treatments rely on precise timing to ensure that all reinfecting parasites are killed following an initial round of treatments. Although temporal coordination must be precise, spatial coordination of these treatments has required little consideration because most kingfish farms in Spencer Gulf are isolated (may be more than 100 km from the nearest neighbouring farm) and, as a result, each can be treated as an IMU. However with the predicted growth of the kingfish industry in South Australia, and the practical limitations of coordinated treatments (all cages within a farm must be treated within a short period of time), other management strategies such as fallowing may be required. For fallowing strategies to be effective it is important that separate year class sites are chosen that
C.B. Chambers, I. Ernst / Aquaculture 250 (2005) 60–69
are separated by distances that allow minimal or almost no interaction of parasite populations; i.e. each year class site must be within a separate IMU. In this study, we found infection rates at 4, 8 and 18 km to be equivalent to infection by a single B. seriolae per fish every 1.4, 6.3 and 33.3 days. At 4 km from the source, the infection rate was clearly above that required for independent management of populations because uninfected fish exposed to this rate of infection (1 worm/fish/1.4 days) would quickly develop their own self sustaining parasite populations. At 8 km from the source, the infection rate was lower (1 worm/fish/6.3 days) and parasite populations could be expected to grow more slowly. However in this case, significant populations of mature parasites would be expected within a period of several months. At 18 km from the source, the infection rate was equivalent to 1 worm/fish every 33 days. This infection rate is clearly low and would result in very slow parasite population growth, even if survival for recruiting parasites were high or if warm temperatures allowed rapid maturity of recruiting parasites. It is possible that some component of the infection rates measured in this study are due to background infection from parasites infecting wild populations of kingfish that are not associated with kingfish farms. However any background infection of B. seriolae is likely to be inconsequential in comparison to the magnitude of infection within sea-cages for 2 reasons. First, wild kingfish populations within Spencer Gulf are small (McGlennon, 1997) and kingfish are thought to migrate into the gulf seasonally. Second, the maximum possible background infection indicated by our study was 0.03 worms/fish/day recorded at the 18 km site. We propose that under the hydrographic conditions of this study a distance of greater than 8 km may be required to designate separate IMUs that are positioned inline with current direction. This study has demonstrated that IMUs required for B. seriolae in the upper Spencer Gulf are large (N 8 km), however it should be noted that this study was designed to detect maximum parasite dispersal. The study was performed at a time when large populations of B. seriolae were present on sea-caged fish (immediately prior to a round of treatments), and during a 7day period of the tidal cycle with the greatest tidal movement (2.4 m vertically). Furthermore, Fitzgerald Bay has the highest tidal current velocities of all
67
kingfish farming areas in Spencer Gulf and our sampling sites were chosen carefully to ensure all sites were inline with the tidal currents flowing from the source farm. The distance between designated IMUs could be much smaller in other locations in Spencer Gulf where tidal currents are slower or where IMUs are positioned across current direction. We have studied the infection dynamics of B. seriolae, but Zeuxapta seriolae is another important monogenean parasite of S. lalandi that requires concurrent management with B. seriolae. Z. seriolae is a gill-dwelling blood-feeder with biological characteristics that differ substantially from B. seriolae. These different biological characteristics could result in different dispersal capabilities and consequently different requirements for designating IMUs. For both parasite species, dispersal could be affected by egg sedimentation rates, egg morphology, egg developmental periods, larval longevity, larval swimming speed and larval behaviour. The morphology of monogenean eggs is known to vary widely and is likely to affect dispersal of eggs after they are laid into the water column (Kearn, 1986). Eggs of B. seriolae are laid individually and possess a single filament that is approximately 2 mm long (Kearn et al., 1992), whereas those of Z. seriolae are laid in groups of several hundred eggs connected together by their filaments (Mooney et al., in press). The begg stringsQ of Z. seriolae are more likely to entangle on structures than the individual eggs of B. seriolae, and Z. seriolae eggs are also known to have faster sedimentation rates (Ernst, unpublished data). These factors combined could contribute to more limited dispersal of Z. seriolae eggs from sea-caged fish compared to eggs of B. seriolae. Seasonal factors could also contribute to dispersal of monogenean eggs because temperature is known to affect embryonation period strongly (Kearn, 1986; Ernst et al., 2005). At low temperatures, eggs take longer to develop before hatching, would be exposed to more tidal cycles, and could be dispersed further along the seafloor. The longevity and behaviour of monogenean larvae are likely to have considerable impact on the ability of larvae to disperse. The larvae of B. seriolae and Z. seriolae are free-swimming, allowing them to adjust their orientation in water currents and potentially maximise dispersal. Hoshina (1968) reported
68
C.B. Chambers, I. Ernst / Aquaculture 250 (2005) 60–69
that larvae of B. seriolae survive for approximately 1 day (temperature not stated), which would allow dispersal throughout few tidal cycles. Larval longevity for Z. seriolae is unknown but larvae of the related parasite Heterobothrium okamotoi, which infects seacaged tiger puffer (Takifugu rubripes), have been studied. Larval longevity for H. okamotoi is much longer (9.1 days at 15 8C; 4.7 days at 25 8C; Ogawa, 1998) than for B. seriolae and could result in far greater larval dispersal over distances inline with and across tidal currents.
5. Conclusion The kingfish industry in Australia is growing rapidly but faces the significant challenge of managing potentially damaging monogenean infections. We have presented results that indicate that strategic cage orientation could reduce interaction between cage-specific B. seriolae populations and therefore reduce population growth. This strategy is feasible in Australia because most farms have relatively few cages, with individual moorings, located on large leases. Careful consideration of improved management practices such as year class separation and fallowing will be required as the industry grows and treatment-orientated management becomes impractical. Our results suggest that IMUs for B. seriolae may need to be separated by more than 8 km (and possibly up to 18 km) if positioned inline with current direction.
Acknowledgements We would like to thank the South Australian Aquaculture Management for providing the facilities and fish to make this study possible, and Allan Mooney for assistance in the field. We thank the National Tidal Centre (Bureau of Meteorology) for providing tidal modelling of the Spencer Gulf. This work was supported by an Australian Research Council Grant LP0211375 (awarded to Ian Whittington and Ingo Ernst). Contributing industry partners include Yamaha Nutreco Aquatech, Skretting Australia and the South Australian Marine Finfish Farmers Association.
References Costelloe, M., Costelloe, J., Roche, N., 1996. Planktonic dispersion of larval salmon-lice, Lepeophtheirus salmonis, associated with cultured salmon, Salmo salar, in Western Ireland. J. Mar. Biol. Assoc. U.K. 76, 141 – 149. Costelloe, M., Costelloe, J., O’Donohoe, G., Coghlan, N.J., Oonk, M., Van der Heijden, Y., 1998. Planktonic distribution of sea lice larvae, Lepeophtheirus salmonis, in Killary Harbour, West Coast of Ireland. J. Mar. Biol. Assoc. U.K. 78, 853 – 874. Egusa, S., 1983. Disease problems in Japanese yellowtail, Seriola quinqueradiata, culture: a review. Rapp. P.-V. Reun.-Cons. Int. Explor. Mer 182, 10 – 18. Ernst, I., Whittington, I.D., Corneillie, S., Talbot, C., 2002. Monogenean parasites in sea-cage aquaculture. Austasia Aquac., 46 – 48 (February/March). Ernst, I., Whittington, I.D., Corneillie, S., Talbot, C., 2005. Effects of temperature, salinity, desication and chemical treatments on egg embryonation and hatching success of Benedenia seriolae (Monogenea: Capsalidae), a parasite of farmed Seriola spp. J. Fish Dis. 28, 157 – 164. Gannicott, A.M., Tinsley, R.C., 1998. Larval survival characteristics and behaviour of the gill monogenean Discocotyle sagittata. Parasitology 117, 491 – 498. Grant, A.N., Treasurer, J.W., 1994. The effects of fallowing on caligid infestations on farmed Atlantic salmon (Salmo salar L.) in Scotland. In: Boxshall, G.A., Defaye, D. (Eds.), Pathogens of Wild and Farmed Salmon. Ellis Horwood, New York, pp. 255 – 260. Hoshina, T., 1968. On the monogenetic trematode, Benedenia seriolae, parasitic on yellowtail, Seriola quinqueradiata. Bull.-Off. Int. E´pizoot. 69, 1179 – 1191. Jackson, D., Deady, S., Leahy, Y., Hassett, D., 1997. Variations in parasitic caligid infestations of farmed salmonids and implications for their management. ICES J. Mar. Sci. 54, 1104 – 1112. Kearn, G.C., 1986. The eggs of monogeneans. Adv. Parasitol. 25, 175 – 273. Kearn, G.C., Ogawa, K., Maeno, Y., 1992. Egg production, the oncomiracidium and larval development of Benedenia seriolae, a skin parasite of the yellowtail, Seriola quinqueradiata, in Japan. Publ. Seto Mar. Biol. Lab. 35, 351 – 362. Løland, G., 1993. Current forces on, and water flow through and around, floating fish farms. Aquac. Int. 1, 72 – 89. McGlennon, D., 1997. Report to the Scalefish Management Committee on Yellowtail Kingfish (Seriola lalandi). South Australian Research and Development Institute, Adelaide. Mooney, A.J., Ersnt, I., Whittington, I.D., in press. An egglaying rhythm in Zeuxapta seriolae (Monogenea: Heteraxinidae), a gill parasite of yellowtail kingfish (Seriola lalandi). Aquaculture. Ogawa, K., 1998. Egg hatching of the monogenean Heterobothrium okamotoi, a gill parasite of cultured tiger puffer (Takifugu rubripes), with a description of its oncomiracidium. Fish Pathol. 33, 25 – 30. Paling, J.E., 1969. The manner of infection of trout gills by the monogenean parasite Discocotyle sagittata. J. Zool. 159, 293 – 309.
C.B. Chambers, I. Ernst / Aquaculture 250 (2005) 60–69 Rae, G.H., 2002. Sea louse control in Scotland, past and present. Pest Manag. Sci. 58, 515 – 520. St-Hilaire, S., Stephen, C., Kent, M., Ribble, C., 2001. Sentinels in the bay: using farm fish to monitor for pathogens in the environment. ICES J. Mar. Sci. 58, 369 – 373.
69
Whittington, I.D., Corneillie, S., Talbot, C., Morgan, J.A.T., Adlard, R.D., 2001. Infections of Seriola quinqueradiata Temminck and Schlegel and S. dumerili (Risso) in Japan by Benedenia seriolae (Monogenea) confirmed by morphology and 28S ribosomal DNA analysis. J. Fish Dis. 24, 421 – 425.