Reference to Gyrodactylus Salaris (Platyhelminthes, Monogenea)

Home , Dactylogyrus, Gyrodactylidae, Gyrodactylidea, Gyrodactylus, Gyrodactylus salaris, Gyrodactylus turnbulli

DISEASES OF AQUATIC ORGANISMS 1 Published June 18 Dis. aquat. Org. I

REVIEW

Host specificity and dispersal strategy in gyr odactylid monogeneans, with particular reference to Gyrodactylus salaris (Platyhelminthes, Monogenea)

Tor A. Bakkel, Phil. D. Harris2, Peder A. Jansenl, Lars P. Hansen3

'Zoological Museum. University of Oslo. Sars gate 1, N-0562 Oslo 5, Norway 2Department of Biochemistry, 4W. University of Bath, Claverton Down, Bath BA2 7AY, UK 3Norwegian Institute for Nature Research, Tungasletta 2, N-7004 Trondheim. Norway

ABSTRACT: Gyrodactylus salaris Malmberg, 1957 is an important pathogen in Norwegian populations of Atlantic salmon Salmo salar. It can infect a wide range of salmonid host species, but on most the infections are probably ultimately lim~tedby a host response. Generally, on Norwegian salmon stocks, infections grow unchecked until the host dies. On a Baltic salmon stock, originally from the Neva River, a host reaction is mounted, limltlng parasite population growth on those fishes initially susceptible. Among rainbow trouts Oncorhynchus mykiss from the sam.e stock and among full sib anadromous arctic char Salvelinus alpjnus, both naturally resistant and susceptible individuals later mounting a host response can be observed. This is in contrast to an anadromous stock of brown trout Salmo trutta where only innately resistant individuals were found. A general feature of salmonid infections is the considerable variation of susceptibility between individual fish of the same stock, which appears genetic in origin. The parasite seems to be generally unable to reproduce on non-salmonids, and on cyprinids, individual behavioural mechanisms of the parasite may prevent infection. Transmission occurs directly through host contact, and by detached gyrodactylids and also from dead fishes. Relative importance of these routes and of different host species in the epidemiology of the disease is discussed with reference to laboratory experiments and existing knowledge concerning the host-parasite ecology.

INTRODUCTION 1986, 1988) and this has been held responsible for declines of up to 520 t 120 % of the total catch; see Dol- Monogeneans of the genus Gyrodactylus are com- men (1987) and MO (1989)l per year in catches of adult mon parasites of freshwater and marine fishes. Al- salmon returning to the rivers to spawn. The ecological though well known as pathogens of farmed fishes impact of the parasite, and of measures aimed at its (Malmberg 1957, 1989a, b, Bauer 1958, 1988, Cone et control, is considerable (Johnsen & Jensen 1991); at al. 1983, Musselius 1988, Solomatova & Luzin 1988), present salmon from a number of Norwegian rivers are they are believed to do little direct harm in natural in- being eradicated using rotenone prior to restocking fections. The present epidemic of G. salaris Malmberg, with disease-free stock (Johnsen et al. 1989). 1957 on wild Atlantic salmon Salmo salar L. along the Little is known of the epidemiology of Gyrodactylus Atlantic seaboard of Norway is therefore quite excep- salaris in Norway (see Johnsen & Jensen 1991). Gyro- tional (Anonymous 1990). Over the past 15 yr severe dactylids are unusual in being viviparous (Harris 1988a) mortality of young salmon due to G. salaris has been and can transfer freely between hosts as adults. The reported from many rivers (Johnsen & Jensen 1985, population dynamics of gyrodactylids are therefore

O Inter-Research 1992 64 Dis. aquat. Org. 13: 63-74, 1992

more characteristic of bacterial and protozoan micro- Table 1. Gyrodactylusspp. Number of hosts infected by Gyro- parasites than of metazoan pathogens (Anderson & May dactylus species, derived from survcy data. (A) Based upon 1978, Scott & Anderson 1984). High fish mortality and total data set of 319 specles descriptions, excluding obv~ous synonyms and misidentifications; (B)based upon 76 species high parasite abundance is seen in salmon parr before which have featured in more than 1 faunistic survey or have they migrate to the sea, but other stages in the life cycle been used in experimental work (smolts, precocious males, returning adults) and other fish species ran support the parasite and may play a part in its transmission. Fish vary, both between and within species, in their susceptibility and response to Gyro- dactylus infection. An understanding of the processes (A) 319 23 27 13 9 involved, in such variability will contribute to our knowledge of the factors underlying disease epidemics. Fur- thermore, knowledge of the transmission and dispersal 1970, 1972, 1973, Malmberg & Malmberg 1970, Ergens of Gyrodactylus species in space and time within the 1983a). To date such detailed analysis has only been host community is essential for a proper understanding applied to G. safaris. of the etiology of gyrodactylosis and ultimately for the Although Bychowsky (1957) considered gyrodactyl- best management practices for the Atlantic salmon ids the least specific of monogeneans, subsequent against G. salaris. Much relevant literature on the host authors (e.g. Malmberg 1970) have regarded them as specificity and transmission of gyrodactylids is found in narrowly host-specific. This is superlicially conlirmed unpublished theses, research reports and foreign jour- by published host records; after eliminating obvious nals of restricted accessibility. Nevertheless, here we synonymies and misidentifications, 74 % of the 319 attempt to review and identify processes which may be valid Gyrodactylus spp. are recorded from a single important in the transmission of G. salaris between com- host species (Table 1A). However, by restricting analy- ponents of the natural ecosystem. sis to those gyrodactylids which have featured in 2 or more field studies, or have been used experimentally, the proportion declines to 30 % of 76 species (Table HOST SPECIFICITY OF GYRODACTYLIDS 1B). This suggests that gyrodactylids are less host- specific than commonly thought, and that narrow Most parasites infect a range of host species which specificity is an artifact based on numerous species form a continuum from those which are infected but descriptions of gyrodactylids collected from only a cannot support the parasite, through those on which single host. The prominent difference in susceptibility/ some reproduction is possible, to hosts on which repro- resistance between stocks of the same fish species (see ductive output is maximised (Holmes 1979). For gyro- Fig. 1) (Bakke et al. 1990b) and between individuals of dactylids, even hosts which cannot support the parasite the same stock (see Fig. 2) (Bakke et al. 1991a) exam- may transport it, facilitating transfer to more suitable i,ned experimentally further stresses the uncertainty in hosts (Bakke et al. 1991b). Unfortunately, accounts of estimating host utilisation of gyrodactylids based on gyrodactylid specificity often fail to consider this spec- few observations. trum and deal only with host range. Furthermore, many Many gyrodactylids have been recorded on single descriptions implicitly or explicitly utilise host identity occasions from hosts other than those normally in- as a character for specific diagnosis (Ergens 1965, Prud- fected; these transient infections are probably a result hoe & Bray 1982), which may overestimate the diversity of inter-specific contact between fishes. An example and underestimate the host range of gyrodactylids. is Gyrodactylus errabundus Malmberg, 1970 which These problems, and the taxonomic complexity of the could invade many other species from the true host genus, make it difficult to analyse patterns of specificity. Zoarces viviparus (L.)but could not live or feed on For example, Cone & Dechtiar (1986) showed that them (Malmberg 1970). Some gyrodactylids, however, Gyrodactylus katharineri Malmberg, 1964, a parasite exploit a range of fish species, reproducing on each. of Cyprinus carpio L., and G. mizellei Kritskyet Leiby, For example G. macrochin Hoffman & Putz. 1964 is re- 1971, a Eurasian parasite of percid fishes in North ported from 8 species and 3 genera of centrarchid America, are morphologically indistinguishable, despite fishes (H0ffma.n & Putz 1964, Hanek & Fernando 1971, the divergence in host and geographical distribution. Rawson & Rogers 1973, Barnhardt et al. 1976, Nicola & Detailed laboratory study is needed for each species Cone 1987). Itinfects different hosts in different locali- to determine the pattern of host utilisation. However, ties and it is not clear which is the principal host. The crowding of hosts in aquaria can break down barriers to species G. macrochin reported by Hanek & Fernando cross-infections, allowing gyrodactylids to infect atypi- (1971) is an additional difficulty, suspected by Nicola & cal hosts (Hargis 1953, Putz & Hoffman 1963, Malmberg Cone (1987) to be misidentified. Bakke et al.. Host specificity and dispel-sal strategy in Gyrodactylus spp. 65

Four salmonid gyrodactylids, Gyrodactylus salaris, G. Salvelinus, according to Cone et al. 1983); G. salmonis salrnonis Yin et Sproston, 1948, G. colenlanensis Mizelle (6 host species in the genera Salmo, Salvelinus and et Kritsky, 1967 and G. derjaviniMikailov, 1975, are re- Oncorhynchus, according to Cone et al. 1983, Cone & ported from more than 4 hosts. G. salaris has a particu- Cusack 1988); G. avalonia Hanek & Threlfall, 1960 and larly broad range, as shown in Tables 2 & 3. This broad specificity for attachment and reproduction does .not ap- Table 2, Gyrodactylus salaris Mal,nberg, 1957, Review of Pear to be Present amongst the gyrodactylids of other records on freshwater fish in the Western Palaearctic. N: in fish groups; for example, the majority of Gyrodactylus nature; H: present in hatcheries or used in experiments species infect cyprinids and yet only 1 infects more than 4 hosts. The pattern of specificity of G. salaris cannot be Host records Sources related to the evolutionary relationships of the hosts, as Salmo trutta L. is less susceptible than e.g. Salvelinus Salmo salar" N: Ergens 1983b, MO 1983, 1987, 1988, Tanurn 1983, Johnsen & Jensen fontinalis (Mitchell), S. alpinus (L.), Thymallus thymal- 1985, 1986, 1988, Malmberg 1988, lus (L.) or Oncorhynchus mykiss (Walbaum) in labora- Eken & Garnas 1989, Malrnberg & tory experiments (see Fig. 3) (Tanum 1983, Malmberg Malmberg 1991 1988, Bakke & Jansen 1991a, b, Bakke et al. 1991a). The H: Malmberg 1957, 1973, 1987a, b, host range of G. salaris outside the Salmonidae needs Malrnberg & Malmberg 1970, 1991, Tanum 1983, MO 1987, 1988, Bakke further investigation but the parasite does not appear to et al. 1990b infect cyprinids [Phoxinus phoxinus (L.) and Rutilus Oncorhyncl~usN: Lucky 1963', Zitnan & Cankovjc rutilus (L.)],percids (Perca fluviatilis L.)or the lamprey m ykiss" 1970C,MO 1988 Lampetra planeri (Bloch) (see Bakke & Sharp 1990, H: Zitnan & Cankovic 1970C,Rehulka Bakke et al. 1990a), and it can infect and survive for up 1973C,Tanum1983, Malmberg 198713, to 8 d but not feed upon the eel Anguilla anguilla 1988, MO 1988, Lux 1990, Bakke et al. (Bakke et al. 1991~).Malmberg (1987b) thought that G. 1991a, Maln~berg& Malmberg 1991 salaris was most closely related to G, thymalli Zitnan, Salrno trutta" N: Ergens 1961C,Zitnan & Cankovic 1960, which infects another riverine salmonid, the 197OC,Tanum 1983, Malmberg 1988, Malmberg & Malmberg 1991 grayling T. thymallus. Our preliminary experiments in- H: Rehulka 1973', Tanunl 1983, MO 1987, dicate that G. salaris can reproduce on T, thymallus (see 1988, Malmberg 1988, Lux 1990, Bakke Bakke & Jansen 1991b),and further work will examine & Jansen unpubl.., present results the host range of G, thymalli (see Lux 1990, Malmberg SaJr/elinus N: MO 1988 & Malmberg 1991). alpinus H: Tanum 1983, MO 1988, Eken & GarnAs 1989, Bakke & Jansen 1991a Salvelinus H:Reh~lka1973~,Mo1987,Eken& ETHOLOGICAL AND PHYSIOLOGICAL fontinalis " GarnAs 1989, Bakke et al. 1992a MECHANISMS OF HOST SPECIFICITY Salvelinus H: Bakke et al. 1992b namaycush We have found by a scrutiny of earlier observations Thymallus H: Bakke & Jansen 1991b that certain Gyrodactylus species vary from narrowly thymallus a specific species which can utilise only a single host to Salmothymus N: Zitnan & Cankovic 1970 those which can successfully attach for dispersal or obtusirostris establish and reproduce on several host genera. This Platichthys N: MO 1987 includes G. pungitii Malmberg, 1964 (several host flesus species during the colder periods of the year when Anguilla H: Bakke et al. 1991b fishes shoal), G, pharyngicus Malmberg, 1964 (2 host angujlla species), G. arcuatus (a number of temporary hosts) and Platjchthys H: Sharp & Bakke 1990 G, errabundus Malmberg, 1970 (a pronounced abhty to phoxinus spread from its normal host to other fish species) (all Lampetra H: Bakke et al. 1990a according to Malmberg 1970); G. unicopula Gluchowa, planeri 1955 (4 host species, according to MacKenzie 1970); G, gasterostei Glaser, 1974 (6 possible hosts, especially Rutilus rutilusb H: Bakke et al. 1990a during the fish breeding season, according to Glaser Perca H: Bakke et al. 1990a 1974); G. katharineri (occurs on several fish genera, fluviatilis termed temporary substratum, especially at higher aSee text; bunsuitable host; 'misidentification, according populations levels, according to Ergens 1983a); G. cole- to Tanum (1983) and Ergens (1983b) manensis (4 host species in the genera Salmo and 66 Dis. aquat. Org 13 63-74, 1992 -- -

Table 3. Gyrodactylus spp. Review of gyrodactylid species (bold) associated with salmonids in the Western Pal~ledrctic. K,in nature; H present in hatcheries or used in experiments

Host records Sources -- -p Gyrodaclylus lrullae Glaser, 1974. Fig. 6a' Salmo trutta N: Ergens 1961, 1981, Glaser 1974. MO 1983~,Lux 1990' Salrno salar N. MO 1983~ 11: 110 1987~ Oncorhynchus N: Ergens 1983b, Mo 1988~,Eken & m ykiss GarnAs 1989" H: Lux 1990' Salveljnus N: Ergens 1983b, Eken & GarnAs fontinalis 1989~ Gyrodactylus derjavini Mikailov, 1975 Salmo Lrulta N: Campbell 19749. Glaser 1974, Mikailov 1975, Ergens 1983b, Malmberg 1987a, b, 1989b, Malnl- berg & blalmberg 1991 H: Malmberg 1989b Salmo salar N: Malmberg 198913. Malmberg & Malmberg 1991 H: Malmberg & Malmberg 1991 Salvelinus H: Malmberg & Malmberg 1991 alpinus Salvelinus H: Malmberg & Malmberg 1991 0 10 20 3 0 A 0 fon tinalis TIME (OAYSI Oncorl~ynchus N: Glaser 1974, Malmberg 1989b m ykiss H: Malmberg 1987b. 1989b. Malm- berg & Malmberg 1991 Fig. 1. Gy-rodaclylus salaris, Salrno salaris. Influence of Chondrostorna N: Ergens 1983b intraspecific stock differences in salmonids for infrapopu- cyria lation growlh of G. salaris. Hosts: individually isolated Cyprinus carpio" N: Ergens 1983b Atlantic salmon. Temperalure: ca 12 "C; infection started with Gyrodaclylus birmani Konovalov, 1967 I gravid parasite; dashed lines- Baltic Neva stock (n = 10); Salvelinus N: Konovalov 1967, MO pers, comm continuous Ilnes: Norwegian Lone stock (n = 10).(After Bakke alpin us et al. 1990b) Gyrodaclylus lavareti Malmberg, 1957 Coregon us N: Malmberg 1957, Ergens 1983b. lavaretus hlalmberg & Malmberg 1991 G. canadensis Hanek & Threlfall, 1969 (show only a Coregonus nasus N: Ergens 1983b weak specificity for salmonid fishes, according to Cone Gyrodactylus thymalli Zitnan, 1960 Thymallus N: Zitnan 1960, Ergens 1983b, Malrn- & Wiles 1985), G. stellatus Crane & Mizelle, 1967 (3 host thyrnallus berg & Malrnberg 1991 species, of different genera, according to Kamiso & Thymallus N: Ergens 1983b Olson 1986); G. bullatar~rdisTurnbull, 1956 (found on arcticus distinctly related hosts, according to Marris 1986); and Gyrodaclylus aphyae Malmberg, 1957 G. goerani Hanek & Fernando, 197 1 (4 host species, ac- Salmo salarh N: MO 1983 cording to Nicola & Cone 1987). According to the results Gyrodactylus phoxini Malmberg. 1957 of Wood & Mizelle (1957), 22 % of a total of 28 Gyro- Salrno salar" N: MO 1988 dactylus spp. may occur on more than 1 host species Gyrodaclylus arcualus Bychowsky, 1933 ~alrnosalar" N: Tanurn 1983 and based on the data of 33 Gyrodactylus spp. listed by Gyrodactylus gobii Schulmann. 1953 Margolis & Arthur (1979),58 ':Lcould be characterized Oncorhynchus H: Lux 1990 as being host specific, 39 5" as narrow in host specific~ty m ykiss " and 3 % as having a broad host specificity. At least 3 Gyrodactylus macronychus Malmberg, 1957 mechanisms maintain these patterns. Salrno truttah N: MO 1983 Firstly, behavioural mechanisms may maintain the "Occas~ondlhost according to Ergens (1983h], "unsu~t- parasite on the normal host. For example Gyrodactyl- able host. ' accord~nqto Malmberg (1987b1, dprobably G us gasterostej Glaser, 1974 transmits freelv to unin- deqavanr, 'sensu Ergens (1983). 'srnsu Glascr (19711, fected Gasterosteus aculeatus (L.),up to 10 ' .>per day Ymlsldent~flcat~on,accord~ng to Tanum (1983) and Erqens (1983b) transferring in laboratory experiments (Harris 1982, section 4.1). Under identical conditions, transmission Bakke et al.: Host specificity and dlispersal strategy in Gyrodactylus spp. 67

different ontogenetical life cycle stages, are unknown for gyrodactylids. A second physiological mechanism may limit Gyro- dactylus salarjs infections on eels. G. salaris infects thls host more readily than it does Phoxinus phoxinus, Rutilus rutilus, Perca fluviatilis or Lampetra planeri, and persists for longer, but parasites cannot reproduce, and die after some days (Bakke & Sharp 1990, Bakke et al. 1990a, Bakke et al. 1991b).The short duration of infection (ca 8 d at 13 "C) compared to the normally longer lifespan of G. salaris at this temperature (see Jansen & Bakke 1991) suggests that the parasite is unable to feed on the eel. G. salaris attached to the skin of this host although Buchmann (1988) has pointed out that no monogenean successfully infects eel skin, while several species infect the gills. This suggests the presence of a non-specific mechanism, either mechan- ical barriers to feeding, such as the thickness of the mucus layer (Jakubowski 1960), or inhibitory or toxic component of eel skin or mucus, which could affect G. salaris in several ways, e.g. through inhibition of en- 0 10 20 3 0 4 0 50 zymes secreted from the pharyngeal glands and used TIME [OAYSI for extracorporeal feeding. The third mechanism maintaining specificity has Fig. 2. Gyrodactylus salaris, Oncorhynchus mykiss. Influence only been noted in Gyrodactylus salaris infecting of intraspecific differences within 1 salmonld host stock for in- salrnonids. The parasite appears to transmit to almost frapopulation growth of G. salaris. Hosts: individually (n = 11) all salmonids tested (see Bakke 1991), although the isolated rainbow trout. Temperature: 12 to 13'C; relative number: no. of parasites in relation to start infection at time 0. species, stocks and individuals differ in their responses (After Bakke et al. 1991a) to the parasite. In experiments with Norwegian stocks of Salmo salar the parasite population generally in- creased without check until the hosts died. On a Baltic to Pungitius pungitius (L.) and Phoxinus phoxinus stock of this fish, however, and on e.g. Oncorhynchus was, however, only 1 %. Gyrodactylus salaris also mykiss (see Bakke et al. 1991a) and Salvelinus fonti- shows a similar mechanism reducing the probability nalis (see Bakke et al. 1992a), parasite populations of attachment to Phoxinus phoxinus, Rutilus rutilus were limited on initially susceptible host individuals by and Perca fluviatilis in relation to salmon (see Bakke a host response 8 to 20 d after infection (Fig. 1).Even & Sharp 1990, Bakke et al. 1990a), and also to bottom amongst individual rainbow trout considerable hetero- dwellers as the eel and lamprey. However, for such geneity of innate resistance and response is observed fish species with frequent bottom contact, the differ- (Fig. 2), although all specimens eventually mobilised ences are less prominent (Bakke & Sharp 1990, Bakke an effective immune response (Bakke et al. 1991a; et al. 1991b, authors' unpubl. data). Gyrodactylus while on Salmo trutta, Coregonus lavaretus (L.)and salaris, detached or attached to a dead host, seems to Salvelinus namaycush (Walbaum) the parasite popula- change its behaviour. The characteristic 'searching tion failed to grow significantly (Fig. 3) (Bakke et al. activity' after a new host and transmission rate in- 199213, authors' unpubl. data), although attachment oc- creases and the selective host-preference decreases. curred, but in these cases apparently at a reduced rate This seems to be a dispersal strategy as it increases (see Bakke 1991). Variation is also seen, from highly the chance of incorporation of transport hosts (Harris susceptible to resistant, amongst the full sib progeny of 1980, Bakke et al. 1991b, authors' unpubl. data). Nev- arctic char Salvelinus alpinus (see Bakke & Jansen ertheless, there seem to be mechanisms not linked to 1991a),which was found, however, not to influence the host behaviour, which generally prevent transfer to attachment rate (Bakke, Jansen & Sterud unpubl.). innapropriate hosts for reproduction and may allow These differences in innate resistance and timing and narrowly specific gyrodactylids to coexist without efficacy of the host reaction are probably genetic, as competition (Harris 1985). The specific mechanisms has been shown in the case of the host response of and behavioural triggers involved in such trans- guppies to G. bullatarudis (see Madhavi & Anderson mission, both for attached and detached parasites of 1985, Jansen et al. 1991). 68 Dis. aquat. Org. 13: 63-74, 1992

and then being picked up by the fish from the substrate. Harris (1982) estimated that up to 10 % of transmission could occur by this indirect route in G. gasterostei. Host-host contact must be most important for gyrodactylids of pelagic hosts as dead hosts and detached parasites would rapidly be swept out of contact with living hosts. Llewellyn (1984) studied transmission of Isancistrum subulatae, a gyrodactylid infecting the pelagic squid Alloteuthis subulata, and demonstrated that transmission occurred when squid made contact with arms cut from infected squid. As the host never rests on the sea floor, and avoids contact with other squid, transmission probably occurs during agonistic behaviour or copulation, a hypothesis supported by the observation that prevalence increases in larger, sexually mature squid (Llewellyn 1984).

10 20 3 0 Transmission by detached parasites TIME (DAYS) This route is probably most important for gyrodactylids of benthic hosts which have opportunities for Fig. 3. Gyrodactylus salaris, Salmo trutta. Influence of a resistant salmonid host stock on the infrapopulation growth of contact with the substrate. Detached gyrodactylids G. salaris. Hosts: individually (n = 10) isolated brown trout. readily attach to, and can move over, wet glass and Temperature. ca 12 "C. (Original results) plastic surfaces, making infections from landing nets which have previously contained infected hosts a pos- sibility (MO1987). Gyrodactylus macrochiri achieved higher infections TRANSMISSION when wire cages containing the hosts were placed in contact with the substrate rather than suspended Gyrodactylids cannot swim and are transmitted by 4 in the water column (Hoffman & Putz 1964, see also routes: (1) direct transfer during contacts between Parker 1965), implying that transmission by detached fishes; (2) contact between fishes and detached para- parasites was occurring, although it is possible that sites on the substrate; (3) contact between fishes and host behaviour differed in the 2 experiments, affect- detached parasites in the drift; (4) contact between ing parasite transmission. Detached free-living G. living fishes and infected dead fishes. salaris have been found in the outlet filters of infected salmon hatcheries in Norway and MO (1987) found large numbers of G. salaris on the bottom Direct transfer of aquaria which had contained infected salmon for 20 h. Parker (1965), Harris (1982), Eken & GarnAs Gyrodactylid transmission is reduced when infected (1989) and Bakke et al. (1991b, authors' unpubl. and uninfected hosts are separated by a barrier data) also report transmission of detached gyro- through which the parasites can pass (Parker 1965, dactylids. Malmberg 1970, Harris 1982), demonstrating the im- Gyrodactylids may become detached from their portance of host contact for transmission. Bychowsky hosts through accident, active migration or as a result (1957) felt this to be the most important route for trans- of a host response (Lester 1972, Scott & Anderson mission and Kamiso & Olson (1986) found that Gyro- 1984). Because detached parasites are not killed but dactylus stellafus transferred most efficiently when are able to reinfect the same or a different host, the there was unrestricted contact between fishes. Al- host response does not necessarily stabilize the para- though host-host contact accounts for a large propor- site population behaviour (May & Anderson 1978), and tlon of transmission, nevertheless a small proportion of at high host densities sufficient flukes may reattach to parasites do succeed in transferring in the presence of significantly reduce the impact of the host response on a barrier, presumably by crawling through the mesh the parasite suprapopulation. Bakke et al.: Host specificity and dispersal strategy in Gyrodactylus spp. 69

Transmission by detached parasites in the drift Transmission between host species

The ability of detached parasites within the plank- Gyrodactylids lack a specific transmission stage and tonic drift to reinfect fishes may have been under- as the mobility of detached parasites is limited, intra- estimated, at least under lotic conditions. Both Parker specific transmission relies on host aggregation and (1965) and Eken & Garnas (1989) reported trans- contact during shoaling, agonistic or reproductive mission of detached, drifting gyrodactylids to fishes. encounters. However, opportunities for interspecific We have observed a mean parasite intensity of 6.6 transfer are more restricted. Glaser (1974) noted Gyrodactylus salaris per fish in 35 previously unin- the importance of multispecies shoals of fishes for fected salmon parr (Age l+) isolated in a cage in an inter-specific transmission, and predator-prey and infected river for 20 d, indicating that several G. salaris scavenger-dead fish interactions may also be impor- probably drifted into contact with the parr (Jansen & tant routes. Predator-prey interactions may have been Bakke unpubl.). important in the speciation of gyrodactylids, as predators are often infected with gyrodactylids closely related to those infecting their prey. For example the Transmission from dead fishes Gyrodactylus wageneri species complex (see Malm- berg 1970) are principally found on cyprinids, but re- When an infected fish dies the behaviour of its gyro- lated species are found on predators sharing the same dactylids changes. Although some species continue to habitat. Furthermore, gyrodactylids from prey species feed (Kulemina 1979) others may abandon the host are occasionally found on predators. Malmberg (1974) (Malmberg 1970) and their activity may increase recorded a species normally found on cottids on Salmo (Harris 1980), increasing the chance of transmission to trutta, and G. macronychus Malmberg, 1957 as well as living fishes. Both transport and natural hosts were G. aphyae Malmberg, 1957 and G. phoxini Malmberg, more heavily infected with Gyrodactylus salaris when 1957, 2 species normally restricted to the minnow exposed to dead salmon than when exposed to a living Phoxinus phoxinus, have been found on salmonids in host (Bakke et al. 1991b), indicating the possible im- the same river system (MO 1983, 1988, Tanum 1983). portance of dead fishes in gyrodactylid transmission. G. arcuatus Bychowsky, 1933, a species which nor- Scott & Anderson (1984) also found transmission from mally infects the stickleback Gasterosteus aculeatus, dead fishes as even more important than from living has also been found on salmon (Tanum 1983). In hosts in their studies of G. bullatarudis on guppies, Nearctic freshwaters, G. brevis Crane et Mizelle, 1967, possibly because dead fishes attract the attention of normally a parasite of a cyprinid (Hesperoleucas living guppies (Scott 1982). Although transmission navarroensis), was originally described by Crane & from dead fishes is clearly efficient, the importance of Mizelle (1967) from the predatory trout Salmo gaird- this route in gyrodactylid epidemiology is limited by neri (= Oncorhynchus mykiss) (see Cone et al. 1983). parasite survival after host death and by the speed at This process may also occur in reverse. Scavenging which parasites leave a dead fish. Up to 50 % of G. on dead fishes may also form an important route of in- gasterostei left the dead host within 18 h at 15 "C terspecific transmission, and the record of G. salaris (Harris 1980), and their subsequent chance of trans- from flatfish may be an example of this (see MO 1987; mission, without the focus of the fish carcass to attract Table 2). other potential hosts, is presumably the same as that for detached parasites. The importance of dead fishes is also limited by the number of infected hosts dying. In Parasite behaviour and transmission many gyrodactylid-host interactions this number is probably very small, but Scott & Anderson (1984) Although gyrodactylid transmission has generally found parasite-induced host mortality to be important been regarded as a function of host behaviour only, for parasite dispersion in G. bullatarudis. The same parasite behaviour may also be very important, at least might be expected in Norwegian river systems for G. during host-host contact. Gyrodactylids inhabiting the salaris, which generally is reported to grow exponen- gill chamber and other cryptic sites (e.g. Gyrodactylus tially until host death (Johnsen & Jensen 1986, 1991). cryptarum Malmberg, 1970 in the acoustico-lateralis In fact, the high abundance of G. salaris reported by canals) must presumably migrate onto the surface of Heggberget & Johnsen (1982) at low salmon densities the fish skin before transmission can occur during host- due to parasite-induced fish mortality may be ex- host contact. Even the action of the host response may plained by such mechanisms, as the salmon parr involve a component of modified parasite behaviour also rest and have frequent contact with the bottom when the gyrodactylids become detached from the substrate. host. For example Gyrdicotylus gallieni Vercammen- 70 Dis. aquat. Org. 13:63-74. 1992

Grandjean, 1960 lives in the mouth of Xenopus laevis, has been extensively modified by man, with large- and accidental dislodgement would result in swallow- scale changes in salmon population density and ing. The age structure of the parasite population sug- genetic structure (Anonymous 1990). As gyrodactylid gests that this occurs rarely. However, Harris & Tinsley population dynamics probably are unstable (May & (1987) noted the synchronous appearance of living G. Anderson 1978, Scott & Anderson 1984), host density gallieni outside of the hosts 1 to 2 mo after infection, and genetics may have a major effect on parasite implying a migration of parasites out of the mouth, population behaviour; it is therefore necessary to con- possibly for the purpose of transmission. Srivastava sider human influences on the host in relation to par- & James (1967) recorded Gyrodactylus medius asite translocation, transmission and parasite popula- Kathariner, sensu Srivastava et James, 1967, normally tion growth. G. salaris can coexist on wild, restocked a gill parasite of the rockling Onos mustela, as occur- and farmed salmonids in the same watershed (Eken ring on the skin in heavy infections, which may also & Garnds 1989) and transmission between these hosts suggest migration by the parasite, and Cone & Cusack must be considered in assessing the epidemiology of (1989) describe migrations of Gyrodactylus colema- the disease. nensis on the host skin after infection. Finally Harris Gyrodactylus salaris principally affects salmon parr (1986, 1988b, 1989) recorded complex changes in par- of O+to 3 yr in age. In suitable areas of river these fishes asite distribution and crowding during infections of form large populations, within which individuals may Gyrodactylus turnbulli Harris, 1986 on guppies, which be territorial (Kalleberg 1958, Saunders & Gee 1964, were probably due to migrations upon the host. Syrnons 1976). Individuals do not move far from their The parasites can discriminate between host species territories (Saunders & Gee 1964) but intraspecific during transmission (Harris 1982, Bakke & Sharp 1990, agonistic interactions would provide opportunities for Bakke et al. 1991b), probably using multiciliate 'spike' host-host transmission of G. salaris during physical sensilla (Lyons 1969a, b) found only in gyrodactylids contact when nipping. However, most interactions (Harris 1983) and which may be chemosensory (Lyons between territorial parr would involve threat display 1969b). Chemoreception forms an important part of rather than contact (J. Heggenes pers. comm.), indi- monogenean transmission biology (Lyons 1969b, cating the importance of indirect transmission in Llewellyn 1984) allowing gyrodactylids to recognise the Salmo salar-Gyrodactylus salaris associations. In suitable hosts before transfer (Cone & Cusack 1989). Norway during spring and summer, these infections Small diffusible molecules (e.g. urea) activate the increase, but in winter, when water temperature in swimming larvae of oviparous monogeneans (Kearn Norwegian rivers are close to 0 OC and fish activity is 1967, 1986), but are too generally distributed to allow reduced to a minimum, parasite populations decline host discrimination. However, the chemical composi- although the parasite still can reproduce at this tion of fish skin appears to be species-specific (Barry & temperature (Jansen & Bakke 1991a). O'Rourke 1959, O'Rourke 1961, Lubbock 1979) and The spatial and temporal patterns of parasite disper- contains sufficient chemical information to allow sal between populations and age-classes of salmon recognition of individuals by conspecifics (Bardach & parr are uncertain. Adult salmon re-entering fresh- Todd 1970). It could therefore produce chemoattrac- water are initially uninfected but contract Gyrodacty- tive cues suitable for use by the gyrodactylids. Jus salaris as they swim through populations of infected parr. Infections may be contracted from detached parasites adhering to gravel and weeds in TRANSMISSION. HOSTSPECIFICITY AND THE areas where epidemics on parr are occurring; alter- EPIDEMIOLOGY OF GYRODACTYLUS SALARIS natively, infected precocious males may transmit the INFECTIONS parasite to adults during spawning (see Malmberg & Malmberg 1991).Adults swim rapidly and can cover 30 In Norway, Gyrodactylus salaris was first noted as a km in 2 d (L.P. Hansen unpubl.), so the potential of pathogen of Salmo salar during the mid-1970's these fishes to spread infection is considerable. Smolts, (Johnsen 1978) and was thought to be an opportunist passing through populations of parr on their way to the infecting already weakened fishes. Subsequently the sea, are probably similarly important (Malmberg & parasite was thought to have been introduced with Malmberg 1991).Pure transport hosts may also spread Baltic salmon stocks (Johnsen & Jensen 1986, Malm- G. salaris between populations of parr within water- berg 1988). This origin for the parasite is disputed sheds. Eels can sustain infections for several days (Halvorsen & Hartvigsen 1989), although supported (Bakke et al. 1991b) and could therefore transport the by differences in susceptibility between Baltic and parasite considerable distances. This is probably also Norwegian salmon (Bakke et al. 1990b, see Johnsen valid for G. salarisinfections of the flounder Platichthys & Jensen 1991). The ecology of the Atlantic salmon flesus (see MO 1987). In these ways G. salaris, which Bakke et al.: Host specificity and dispersal strategy in Gyrodactylus spp. 7 1

RIVER

Mature +

Fig. 4. Gyrodactylus salaris, Salmo salar. 1 HOST Circulation of G. salaris within the host COMMUNITYp community. Thick lines: life cycle of I anadromous Atlantic salmon; thin lines: I possible routes of circulation of G. salans w~thinthe salmon river ecosystem Epl- demiological data on relative importance of the different salmon cohorts and routes, and seasonal dynamics of the Maturing adult system under natural conditions are Ik-$l generally lacking

SEA cannot survive in sea water, may be also transferred LITERATURE CITED between rivers through regions of brackish water, as Anderson, R M., May, R. M (1978).Regulation and stability of they can endure up to 7.5 %O salt water for weeks host-parasite population interactions. I. Regulatory pro- (Soleng & Bakke 1991). cesses. J. Animal. Ecol. 47: 219-247 Possible transmission patterns of Gyrodactylus Anonymous (1990). Report on the Norwegian meeting on im- salaris within and between populations of salmon parr pacts of aquaculture on wild stocks. North Atlantic Salmon are summarised in Fig. 4. Rapid transmission within Conservation Organization, Councll Paper 28: 1-9 Bakke, T. A. (1991). A review of the inter- and intraspecific shoals of the new generation of parr in the spring, and var~abilityIn salmonid hosts to laboratory infections with the dissemination between parr populations of para- Gyrodactylus salaris Malmberg. Aquaculture 98: 303-310 sites by adult salmon, smolts and possibly eels and Bakke, T. A., Jansen, P. A. (1991a). Susceptibility of arctic flounders, appear to be the most important features char (Salvelinus alpinus) to Gyrodactylus salaris Malm- in Norway. The importance of other transmission berg (Monogenea). Bull. Scand. Soc. Par. 1: 60 Bakke. T A., Jansen. P. A. (1991b). Susceptibility of grayling routes remains unclear. We have no evidence of infec- (Thymallus thymallus) to Gyrodactylus salaris Malmberg tion of salmon eggs, only evidence for infections of (Monogenea) Bull. Scand. Soc. Par. 1 61 alevins, but the pathogenicity of G. salaris at this stage, Bakke, T. A., Jansen, P. A., Brabrand, A.(1990a). Susceptibil- and the importance of this age group as hosts of the ity and resistance of brook lamprey, Lampetra planen parasite, are unknown. In order to understand the epi- (Bloch), roach, Rutilus rutilus (L.)and perch, Perca fluviatilis L. to Gyrodactylus salaris Malmberg (Monogenea). demiology of G. salaris, and to develop rational control Fauna norv. (Ser A) 11: 23-26 strategies, the relative importance of all of these Bakke, T. A., ~ansen,P: A., Hansen, L. P. (1990b).D~fferences cohorts and ~ossibleroutes of transmission will need ~n the host resistance of Atlantic salmon (Salmo salar) to be investigated. stocks to the monogenean Gyrodactylus salaris Malm- bera.d. 1957. J. Fish Biol. 37: 577-587 Bakke, T. A., Harris, P. D., Jansen, P. A. (1992a). The susceptibility of Salvelinus fontinalis (Mitchell) of Gyrodactylus Acknowledgements. We appreciate the comments on the sal- salaris Malmberg (Platyhelminthes; Monogenea) under monid infection records in Western Palaearctic given by Tor experimental conditions. J. Fish Biol. (in press) A. MO. Veterinary Institute, Oslo. This study was supported Bakke, T. A., Jansen, P. A., Grande, M. (199213). The suscepti- by a grant from the Directorate for Nature Management, bility of Salvelinus namaycush (Walbaum) to Gyrodactylus Trondheim. salaris Malmberg (Platyhelrninthes; Monogenea) under 72 Dis. aquat. Org. 13: 63-74, 1992

experimental conditions Fauna norv. (Ser. A) 12: (in press) Dolmen, D. (1987). Gyrodactylus salaris (Monogenea) in Bakke, T A., Jansen, P. A., Kennedy, C. R. (1991a). The host Norway; Infestations and management In: Stenmark, A, specificity of Gyrodactylus salaris Malmberg (Platy- Malmberg. G. (eds.) Parasites and diseases in natural helminthes, Monogenea): susceptibility of Oncorhynchus waters and aquaculture in Nordic countries. Proceedings myklss (Walbaum) under experimental conditions J. Fish Zoo-Tax-Symposium, Stockholm 1986. Naturhistoriska Biol. 39: 45-57 Rlksmuseet, Stockholm, p. 63-69 Bakke, T. A., Jansen. P. A.. Hansen, L. P. (1991b). Experimen- Eken, E., Garngs, E. (1989). Utbredelse og effekt av laksepar- tal transmission of Gyrodactylus salaris Malmberg (Platy- asitten Gyrodactylus salaris p& 0stlandet 1988. Fylkes- helminthes, Monogenea) from the Atlantlc salmon (Salmo mannen i Buskerud, Milj~vernavd.,Rapport nr. 1: 1-35 (In salar) to the European eel (Anguilla anguilla). Can. J. Norwegian) Zool. 69: 733-737 Ergens, R. (1961). Two further species of monogenetic trema- Bakke, T. A., Sharp, L. A. (1990).Susceptibility and resistance todes of the genus Gyrodactylus Nordmann, 1832, from of minnows, Phoxinus phoxinus (L.) to Gyrodactylus Czechoslovakia. Vestn. Cesk. Spol. Zool. 25 25-27 (In salaris Malmberg, 1957 (Monogenea) under laboratory German, Czechoslavakian summary) conditions. Fauna norv. (Ser. A) 11: 51-55 Ergens, R.(1965). Die Morphogenese der Chitinoidenteile des Bardach, J. E.,Todd, J. H. (1970).Chemical communication in Haptors bei Gyrodactylus decorus Malmberg, 1965 fishes. In: Johnston, J. W., Moultron. D. C.. Turk. A. (eds.) (~Monogeno~dea)und ihre Morphologisch-metrlsche Vari- Advances in chemoreception, Vol. 1. ~MeredithCorp.. New abilitat. 2. 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Sechs neue Arten der Gyrodactylus- Boyd Ltd, Edinburgh, p. 267-300 wageneri-Gruppe (Monogenea, Gyrodactylidae) nebst Bauer, 0. N. (1988). Ep~zootiologicalsignif~cance of monoge- Bemerkungen zur Praparation, Determination, Termin- neans. In: Skarlato, 0. A. (ed.) Investigations of mono- ologie und Wirtsspezifisitat. Zool. Anz., Jena 192: 56-76 geneans in the USSR, A. A. Balkema, Rotterdam, Halvorsen, 0.. Hartvigsen, R. (1989). A review of the bio- p. 137-142 (Russj.an translation series 62) geography and epidemiology of Gyrodactylus salaris. Buchmann, K. (1988). Pseudodactylogyrose i oppdrettet NlNA Utredning 2. 1-14 Al. Licentiatafhandling. Inst. Vet. Microbial. Hyg., Den Hanek, G., Fernando. C. H. (1971). Monogenet~ctrematodes Kgl. Vet.-Landbohcijskole, K~benhavn1988. (In English, from the Bay of Quinte area, Ontario, 11. Genus Gyro- Danish summary) dactylus Nordmann, 1832. Can. J. Zool. 49: 1331-1341 Bychowsky, B. E. (1957). Monogenetic trematodes. Their Hargls, W. J. Jr (1953). 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(1970). Gyrodactylus unicopula Glukhova, sitol. 1: 50 1955, from young plaice Pleuronectes platessa L. with Johnsen. B. 0. (1978). The effect of an attack by the parasite notes on the ecology of the parasite. J. Fish Biol. 2: 23-34 Gyrodactylus salaris on the population of salmon parr in Madhavi, R., Anderson, R. M. (1985). Variability in the sus- the river Lakselva, Misvaer in northern Norway. Astarte ceptibility of the fish host, Poecilia reticulata, to infection 11: 7-9 with Gyrodactylus bullatarudis (Monogenea). Parasi- Johnsen, B. O.,Jensen, A. J. (1985). Parasitten Gyrodactylus tology 91: 531-544 salaris pb lakseunger i norske vassdrag, statusrapport. Malmberg, G. (1957). Om forekomsten av Gyrodactylus pB Direktoratet for Vilt og Ferskvannsfisk, Reguleringsunder- svenska fiskar. Skr. sod. Sver. FiskFor. Arsskr. 1956: 19-76 sskelsene. Rapport nr. 2: 1-145 (In Norwegian) (In Swedish) Johnsen, B. O., Jensen, A. J. (1986).Infestations of Atlantlc Malmberg, G. (1970). 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Gyrodactylus-infections in Scandinavia. In: Parasites of Putz, R. E., Hoffman, G. L. (1963). Two new Gyrodactylus fresh-water fishes of North-west Europe. Inst. Biol. USSR (Trematoda: Monogenea) from cyprinid fishes with syn- Acad. Sci, Karelian Branch, Petrozavodsk 1989. p. 88-104 opsis of those found on North American fishes. J. Parasitol. Malmberg, G., Malmberg, M. (1970).Dactylogyrus och Gyro- 49: 559-566 dactylus - tvb vanliga parasiter pd svenska fiskar. Zool. Rawson, H. V. Jr. Rogers, W. A. (1973). Seasonal abundance of Revy 32: 9-18 (In Swedish, English Summary) Gyrodactylus macrochiri Hoffman & Putz, 1964 on bluegill Malmberg, G., Malmberg, M (1991). Undersokningar and largemouth bass. J Wildl. Dis. 9: 174-177 angaende Gyrodactylus pA laxfisk i fria vatten och odlin- Rehulka, J. (1973). Remarks on the occurrence of Gyro- gar under Aren 1951 - 72 och 1986 - maj 1991. Inf. 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Responsible Subject Editor: W Korting, Hannover, Germany Manuscript first received. July 20, 1991 Revised version accepted: February 14, 1992