69The parasite Lernaeocera branchialis on caged cod :infection pattern is caused by diﬀerences in hostsusceptibilityD. A. L Y S N E "* and A. S K O R P I N G #" Finnmark University College, Follumsvei 31, N-9509 Alta, Norway# Department of Zoology, University of Bergen, Realfagbygget, AlleT gaten 41, 5007 Bergen, Norway(Received 23 January 2001 ; revised 5 May 2001 and 1 August 2001 ; accepted 1 August 2001)Variation in host susceptibility causes signiﬁcant diﬀerences in infection rates between hosts living in a semi-naturalsituation. Such knowledge has implications for population dynamics and evolutionary models of host–parasite interactionsas well as for estimations of parasite abundance. Infection rates by Lernaeocera branchialis (L.) were measured throughtime and space on caged Atlantic cod (Gadus morhua L.). One group of hosts, identiﬁed by their infection history,developed signiﬁcantly higher infection rates than the others. These were ﬁsh which had been infected previously, but hadlost their infection. Diﬀerences between groups were consistent through both time and space. Two types of cod seem tohave been present in the caged population ; a small group of inherently susceptible ﬁsh, which were infected, and reinfectedif the parasite was lost, and another group of resistant hosts with a small chance of becoming infected.Key words : Atlantic cod, Gadus morhua, Lernaeocera branchialis, susceptibility. studies where the eﬀect of heterogeneities in ex- posure rate to infective stages can be separated fromMost macroparasites show a non-random distri- heterogeneities in host susceptibility. As pointed outbution across their host population (Shaw, Grenfell by Clayton, Pruett-Jones & Lande (1992), a major& Dobson, 1998). The level of parasite aggregation shortcoming in many studies has been that workershas consequences for population regulation have been using variation in parasite numbers as a(Anderson & May, 1978 ; May & Anderson, 1978), as measure of variation in susceptibility. Experimentalwell as for epidemiological studies since, at in- studies in the laboratory, where individuals arecreasing levels of aggregation, a larger number of exposed to a known number of infective stages, havehosts must be sampled in order to estimate parasite repeatedly shown that host susceptibility variesabundance. Furthermore, several evolutionary between individuals (Chevassus & Dorson, 1990 ;models hypothesize that parasites can be important Bakke et al. 1992 ; Wakelin, 1994). These are notselective agents on their hosts (Barbehenn, 1969 ; easily extrapolated to natural situations becauseHamilton & Zuk, 1982 ; Freeland, 1983 ; Hamilton, exposure rates may diﬀer widely from those in theAxelrod & Tanese, 1990). A necessary requirement ﬁeld (Quinnell & Keymer, 1990), and also becausefor such parasite-mediated selection is that the trait host susceptibility may be aﬀected by conditions into be selected must covary with parasite numbers the laboratory (Lloyd, 1995). An alternative is to run(Goater & Holmes, 1997 ; Skorping, 1998). For ﬁeld experiments where hosts can be exposed toexample, in the hypothesis proposed by Hamilton & naturally occurring transmission stages under en-Zuk (1982) on sexual selection, it is assumed that vironmental conditions more similar to those ex-diﬀerences in male heritable susceptibility will be perienced in the wild. By using ectoparasites onreﬂected in the distribution of parasites. The im- individually marked hosts, it should be possible toportance of parasites as selective agents is likely to compare infection rates between host individuals,increase when parasite distribution becomes less and examine if diﬀerences in rates are consistentaggregated because more hosts harbour a higher through time.number of parasites. This paper describes ﬂuctuations in the population In order to understand why wild-living parasites of Lernaeocera branchialis (L.) on caged cod (Gadusaggregate within their host populations we need morhua L.) for 598 days. L. branchialis uses mainly diﬀerent species of ﬂatﬁsh as intermediate hosts (Kabata, 1979), but can also develop on other ﬁsh* Corresponding author : Finnmark University College,N-9509 Alta, Norway, Tel : j 47 78 45 03 56. Fax : j47 species (Lester & Roubal, 1995). After mating, the78 43 44 38. E-mail : daga!hifm.no pregnant female has a short free-living periodParasitology (2002), 124, 69–76. " 2002 Cambridge University PressDOI : 10.1017S0031182001008848 Printed in the United Kingdom
D. A. Lysne and A. Skorping 70Fig. 1. Chart of Kvalfjorden with cage locations marked by dots. Four net bags were placed in cage A, while cages Band C had 1 net bag each.searching for the deﬁnitive host, a gadoid ﬁsh. If successful, she will settle at the base of the gill archeson the ventral side, and undergo a metamorphosis Six hundred cod were caught by ﬂoating trawl oﬀ thewhere the head penetrates into the heart region of the coast of Finnmark County, Norway, and caged inﬁsh (Grabda, 1991). The parasite is known to Kvalfjorden (70m 42h N and 23m 48h E). The ﬁsh wereinﬂuence both growth and level of liver fat, and may allowed to recover from capture and acclimatized forbe lethal, especially to young ﬁsh (Khan, Lee & 2 weeks while fed several times a day with artiﬁcialBarker, 1990). The parasite may live up to 18 months food. Thereafter, the ﬁsh were caged in 6 net bags(Lester & Roubal, 1995) and can not move between (height 4 m, volume 40 m$ each) at 3 diﬀerenthosts. locations in the fjord. One hundred cod were placed In the present study a ﬁeld experimental approach in each of 4 net bags in cage A (see Fig. 1). Thesewas used to address the following question. Do were all free from infection by L. branchialis, with 3infection rates vary between hosts due to inherent accidental exceptions. The depth at low tide was 8 mdiﬀerences in susceptibility? Exposure can be at this cage. This paper is part of a larger study, andassumed to be random within each of the host ﬁsh from another 2 cages, which were placed in thelocations used in this experimental set-up. If then study area for other reasons (labelled B and C in Fig.the pattern of infection is caused mainly by factors 1), were also included in the present data. At cagingunrelated to host susceptibility, infection rates 100 cod were placed at random, with respect toshould show random variations between host indi- infection, in one net bag in each of cage B and Cviduals. (Table 1). The cages were placed 200 m and 50 m
Variation in susceptibility to L. branchialis 71 Table 1. Infection levels of Lernaeocera branchialis on the caged cod at the start of the experiment are given separately for the 3 cages in the experiment together with the mean and range of both body mass and length of the ﬁsh at caging, as well as increase in body mass and length through the study period (Cage-labelling refers to Fig. 1) Cage A Cage B Cage C Infection Abundance 0n01 0n85 0n71 Prevalence 1n1 % 38n5 % 40n9 % Mass (g) Mean 1876n4 1855n2 2013n2 Range 1025n0–2905n0 1110n0–2525n0 1110n0–4300n0 Increase, mean 2454n6 2408n6 2248n7 Increase, range 410n0–4170n0 705n0–4490n0 310n0–5070n0 Length (cm) Mean 60n6 60n5 61n2 Range 47n5–71n0 48n0–66n0 50n0–79n5 Increase, mean 10n6 10n3 9n5 Increase, range 3n5–21n0 2n0–18n5 1n0–20n5from the shore respectively. Depths at low tide were (i) included ﬁsh where numbers of parasites in-31n5 m at cage B and 18n5 m at cage C. In the fjord creased during a time-period, and group (ii) includedthe average water level change is 1n8 m (Statens ﬁsh where numbers of parasites did not increase.Kartverk, 2001) between high to low tide. Strong The data were used in a logistic regression modeltidal currents, which are especially pronounced close with binomial errors in Glim4 (Crawley, 1993).to the shores (Fig. 1), continuously replaced the Groups of cod, identiﬁed by infection history, werewater within the cages. tested for diﬀerences in age distributions using Before the separation into diﬀerent cages ﬁsh were contingency tables (GLM with Poisson errors andinspected for L. branchialis, and length and mass log link function). The variables were included in thewere recorded (Table 1). All ﬁsh were also in- models in a forward stepwise manner. Signiﬁcancedividually tagged with external anchor tags (T-tags). of eﬀects in the models were tested by comparing theBefore handling, each ﬁsh was anaesthetized in change in deviance by the removal of a term from the0n15 % chlorobutanol (C H Cl O). During the ex- model with the values of Chi-square tables in % ( $perimental period the ﬁsh were anaesthetized, L. accordance with Crawley (1993).branchialis counted and length and mass recorded 6times ; on days 0, 74, 327, 431, 522 and 598 after caging. The large gap in collection times between thesecond and third sample was caused by bad weather A total of 495 cod survived the experimental period.conditions which made it impossible to transport the Of the survivors, 339 ﬁsh could be identiﬁedﬁsh between the cages and the location where they throughout the study, while the remaining indi-were anaesthetized and inspected. On day 598 all viduals had lost their tags and were subsequently re-surviving ﬁsh were killed and sexed. The otoliths tagged. Of the 339 cod, which were identiﬁedwere removed for age determination. During the throughout the study, 79 % remained uninfected,experiment cod were fed cuttings from the codﬁllet while the rest of the ﬁsh harboured the parasite atindustry and herring meal mixed with commercial one or more sampling points. During the studyﬁsh food (‘ Salmomix 45 % ’). Food was added to the period there was a decline in numbers of hostscages twice a week, and what was not eaten, sank out harbouring more than 1 L. branchialis (Fig. 2 ; χ# lof the cage within a period of less than 30 sec. 9n29 ; P l 0n0023 at 1 ..). The death of 22 ﬁsh was Only ﬁsh which survived longer than day 327, caused by predation by the otter, Lutra lutra, whichwere included in the analyses. All statistical tests in most cases made the ﬁsh impossible to inspect forwere run using generalized linear models (GLMs) in parasites. These killings took place during the darkthe Glim4 computer package (Crawley, 1993). period each year, between late November and earlyChanges in frequency distribution of parasites February. The otter entered the cages through self-through time were tested using a contingency table made holes in the net. However, among the dead ﬁsh(Poisson errors and log link function). Changes in which could be inspected, intensity and prevalencerates of infection were treated as binary data : group were within the levels measured among the survivors
D. A. Lysne and A. Skorping 72 40 30Number of fish 20 10 0 0 74 327 431 522 598 June August April August November January 1993 1993 1994 1994 1994 1995 Days after caging and month and year of samplingFig. 2. Numbers of cod harbouring diﬀerent numbers of Lernaeocera branchialis during the period of caging. Onlyﬁsh which appeared in all samples (n l 339) were included. Number of L. branchialis per ﬁsh 1; 2; 3; 8 4;: 5 ; 5 6.Fig. 3. Infection rates, with standard errors, by Lernaeocera branchialis for ﬁsh which were free from infection at thestart of a time-period (open columns), compared to rates for ﬁsh which harboured the parasite (ﬁlled columns). ‘ 0 ’ lNo ﬁsh acquired new infections.(intensity l 1.78, prevalence l 0n36, n l 22). Data the changes in infection rates were not apparent fromon the surviving ﬁsh therefore seem not to have been the analyses. Inclusion of a second order and thirdbiased by parasite-related deaths. order parameter of the ‘ time ’ variable did not exert The rate at which L. branchialis established within signiﬁcant inﬂuence on infection rates (χ# l 0n30 ; Pthe caged population was high during the ﬁrst time l 0n58 at 1 ., and χ# l 2n56 ; P l 0n11 at 1 ..,period (Fig. 3), but then dropped to a lower level ( χ# respectively).l 50n5 ; P 0n001 at 1. ..). Seasonal ﬂuctuations in Infection rates were compared between groups of
Variation in susceptibility to L. branchialis 73 Table 2. The inﬂuence of infection history and location on infection rates of Lernaeocera branchialis on cod during successive time-periods (‘ Infection history ’ identiﬁes 2 groups among the cod. Fish which were un- infected at the start of the time-period are compared to ﬁsh which harboured the parasite (see also Fig. 3). ‘ Location ’ refers to the 3 locations in the fjord where the cod were caged. In the analysis ‘ infection rate ’ was treated as a binary response variable, and included in models (GLMs) with binomial errors.) Inf. history Location Inf. history i Days after caging (.. l 1) (.. l 2) loc. (.. l 2) 0–74 χ# l 1n93 χ# l 4n94 χ# l 0n31 P l 0n16 P l 0n09 P l 0n86 74–327 χ# l 1n37 χ# l 2n44 χ# l 0n38 P l 0n24 P l 0n30 P l 0n83 327–431 χ# l 0n28 χ# l 0n92 χ# l 0n002 P l 0n60 P l 0n63 P l 0n999 431–522 χ# l 1n76 χ# l 1n64 χ# l 0n001 P l 0n19 P l 0n44 P l 0n999 522–598 χ# l 0n13 χ# l 0n30 χ# l 3n099 P l 0n72 P l 0n86 P l 0n21Fig. 4. Infection rates, with standard errors, by Lernaeocera branchialis for 2 subgroups of the ﬁsh classiﬁed as‘ uninfected ’ in Fig. 3. Fish which had lost the infection, and therefore were free from the parasite at the start of thetime-period (open columns), are compared to ﬁsh which were not recorded as infected prior to the start of the time-period (ﬁlled columns). ‘ 0 ’ l No ﬁsh acquired new infections.cod identiﬁed by their infection history. Rates did of the 4 time-periods, these cod were more likely tonot diﬀer between ﬁsh which were uninfected at the be infected than the cod which had never harbouredstart of a time-period, compared to infected ﬁsh (Fig. the parasite at any of the previous sampling points3). This was shown statistically by the lack of (the statistics are given in Table 3). In the seconddiﬀerence within all of the 5 time-periods which interval in Fig. 4, where infection rate is zero in thewere compared (the statistics are given in Table 2). group of previously infected cod, only 11 of theHowever, 1 subgroup among the uninfected ﬁsh individuals which were free from infection after 327showed signiﬁcantly higher rates of infection than days in the cage, had been recorded as infectedthe others. These were the ﬁsh which had been earlier in the study. None of these were recorded asinfected, but had lost their infection prior to the start infected after 431 days in the cage. Furthermore,of the time-period under investigation (Fig. 4). This when compared to the group of cod which harbouredloss of infection was identiﬁed among individuals the parasite at the start of a time-period, the group ofwhich had harboured the parasite at one or more of cod which had lost all their parasites, showedthe previous samplings but were free from infection signiﬁcantly higher infection rates in 2 of the 4 time-at the start of the time-period in question. Within 3 periods (the statistics are given in Table 4). This
D. A. Lysne and A. Skorping 74 Table 3. Fish which had been infected by Lernaeocera branchialis, but had lost their infection prior to the start of the time-period, are compared to ﬁsh which were not recorded as infected (see Fig. 4) (These are subgroups of the ‘ uninfected ’ ﬁsh in Fig. 3. In the analyses ‘ infection rate ’ was treated as a binary response variable, and included in models (GLMs) with binomial errors.) Inf. history Location Inf. history Days after caging (.. l 1) (.. l 2) i location 74–327 χ# l 7n92 χ# l 2n14 χ# l 3n06 P l 0n005 P l 0n34 P l 0n08 (1 ..) 327–431 χ# l 0n11 χ# l 0n61 χ# l 0n0002 P l 0n74 P l 0n74 P l 0n999 (2 ..) 431–522 χ# l 13n60 χ# l 3n58 χ# l 0n24 P l 0n001 P l 0n17 P l 0n89 (2 ..) 522–598 χ# l 7n03 χ# l 1n66 χ# l 0n118 P l 0n008 P l 0n44 P l 0n94 (2 ..) Table 4. Fish which had been infected by Lernaeocera branchialis previous to the time-period in question, but had lost the infection (a subgroup of the ‘ uninfected ’ in Fig. 3), are compared to ﬁsh which harboured the parasite at the start of the period (the ‘ infected ’ ﬁsh in Fig. 3) (In the analyses ‘ infection rate ’ was treated as a binary response variable, and included in models (GLMs) with binomial errors.) Inf. history Location Inf. history Days after caging (.. l 1) (.. l 2) i location 74–327 χ# l 7n31 χ# l 4n64 χ# l 0n0008 P l 0n007 P l 0n10 P l 0n977 (1 ..) 327–431 χ# l 0n21 – – P l 0n65 – – 431–522 χ# l 10n68 χ# l 3n22 χ# l 0n001 P l 0n001 P l 0n20 P l 0n999 (2 ..) 522–598 χ# l 2n41 χ# l 0n34 χ# l 2n82 P l 0n12 P l 0n84 P l 0n24 (2 ..)pattern may have been caused by age-related as uninfected. This diﬀerence was consistent throughdiﬀerences in infection rates. If so, age of the ﬁsh time and between locations. With respect to infectionshould diﬀer between groups identiﬁed by infective rates, 2 types of cod therefore appear to have beenhistory. This was not found to be the case within any present in the caged population ; one large groupof the time-periods (χ# 8n57 ; P 0n29 at 7 ..). with a relatively small chance of becoming infected Diﬀerences in infection rates between individuals and another smaller group with a much higher risk ofdid not depend on which location the ﬁsh were acquiring the parasite. The strong water currents inplaced in. This appeared from the fact that ‘ location ’ the caging area, which caused continuously re-neither aﬀected infection rate (Tables 2, 3 and 4), placement of the water within the cages, shouldnor inﬂuenced the eﬀect of ‘ infection history ’ within produce random variation in exposure to infectiveany of the time-periods (non-signiﬁcant eﬀects of the stages among ﬁsh within each cage. Furthermore,‘ infection historyilocation ’ interactions ; Tables 2, during the experimental period there were no3 and 4). signiﬁcant diﬀerences in infection rates between the cages. Therefore, the diﬀerences in rates between the 2 groups of cod, could not have been caused by diﬀerences in the rate of exposure, but must haveIn this study, infection rates did not vary randomly been related to phenotypic diﬀerences.between individual cod. Fish which had been An alternative explanation would be that theinfected previously with L. branchialis and had lost smaller group of hosts may have diﬀered in theirthe infection, had a signiﬁcantly higher rate of behaviour in a way that made them more frequentlyinfection than cod which previously were recorded exposed to transmission stages, for example, by
Variation in susceptibility to L. branchialis 75occupying the bottom of the net bags. Poulin, Rau Susceptibility can appear as a gradient from highlyCurtis (1991) showed that variation in behaviour susceptible to resistant hosts. This view does notinﬂuenced infection rates among laboratory reared change the argument that infection rates decreasedbrook trout fry (Salvelinus fontinalis) infected by the through time due to declining probability of encoun-crustacean ectoparasite Salmincola edwardsii. How- tering susceptible hosts because the highly sus-ever, if host behaviour were an important factor in ceptible individuals were infected during the ﬁrstthe present study the frequently exposed hosts part of the study and moved into the infected classshould show high levels of infection rates throughout with a low probability of reinfection.the study period, independent of their previous Other explanations for the observed decrease ininfection status. This was not observed. infection rate with time are possible, but less likely. The assumption that the caged cod population A decrease in rates of infection with time could beinitially consisted of a small group of inherently caused by stress during the caging process, whichsusceptible ﬁsh among a larger group of resistant may increase initial susceptibility to parasites (Lloyd,ones, would explain both the decrease in the infection 1995). However, ﬁsh seem to acclimatize to cagesrates within the whole group of cod, and the over a short time. Pickering (1987) argued thatﬂuctuating rate of infection among the ﬁsh which within 3 weeks most individuals of several species dohad carried the parasite earlier, but lost it. The not show signs of immune suppression. Seasonal orinfection rate within the whole group should decline annual changes in densities of transmission stagesbecause the number of susceptibles rapidly became may cause a decrease in rate of infection throughinfected and moved into the infected class with a low time. If densities decreased through the ﬁrst autumnprobability of reinfection. Since this parasite may and winter, the rates of infection should havelive for 18 months (Lester Roubal, 1995), few of increased again over the second summer (from Aprilthese ﬁsh had lost their infection after 327 days in the to early November which would be from 327 to 522cage. This may explain the lack of new infections days in the cage). This did not happen. Neither is itamong the group of susceptibles during the second likely that annual ﬂuctuations in densities of trans-time-interval. mission stages caused the observed pattern, because Are cod with a previous record of carrying the changes in rates of infection with time diﬀeredparasite more vulnerable to reinfection due to between groups of cod. For example, infection ratesparasite-induced increase in susceptibility ? Such increased in the group of infected cod between thepatterns were observed in the laboratory on juvenile second-to-last and the last time-period. At the samesticklebacks (Gasterosteidae) infected by the crus- time the group of cod which had lost their infection,tacean ectoparasite Argulus canadensis (Wilson, 1916 ; showed a 40 % decrease in infection rates. It isPoulin FitzGerald, 1989), and on brook trout therefore reasonable to conclude that the decrease infry infected by another crustacean ectoparasite S. infection rates with time was caused by a decliningedwardsii (Poulin et al. 1991). However, the present number of susceptible hosts.data seem not to ﬁt this explanation. L. branchialis Are the present results comparable to the wilddid not induce higher infection rates among the ﬁsh situation ? It is not likely that factors tied to theharbouring the parasite, because the number of ﬁsh caging situation, for example stress, would aﬀect acarrying more than 1 parasite did not increase with fraction of the caged cod, i.e. the susceptible ﬁshtime, and ﬁsh infected by the parasite at the start of identiﬁed by their infection history, more seriouslya given time-period did not show higher infection than the rest of the population. However, therates than uninfected hosts. A supposed increase in availability of food may be more uniformly distri-susceptibility due to earlier infection may also take buted, and for part of the year more abundant,eﬀect only after the ﬁsh have lost the infection. between caged individuals than experienced by wild-However, if parasite-induced facilitation of re- living ﬁsh. As a consequence, diﬀerences in hostinfection were the most important factor causing resistance caused by ﬂuctuation in nutritional re-changes in infection rates, we would expect rates to source may be more pronounced among wild-livingbe low at the start of the study period, and thereafter hosts. The frequent availability of high quality foodincrease as parasites died and numbers of previously may explain why the numbers of multi-infectedinfected ﬁsh increased through time. This was not hosts decreased throughout the study period.observed. Since this is a relatively pathogenic parasite (Khan, The argument that the caged cod initially con- 1988 ; Khan et al. 1990), cod that are able to avoid itsisted of a small group of inherently susceptible ﬁsh should have a ﬁtness advantage relative to theamong a larger group of resistant ones, depends on susceptible group. Why then, does resistance notthe assumption that the observed temporal variations spread to the whole cod population ? We suggest 2in infection rate are caused by changes in availability possible mechanisms that may maintain such poly-of susceptibles. The distribution of the cod popu- morphism in susceptibility.lation in 2 distinct groups, susceptible or resistant Given that parasites show virulence speciﬁc tohosts, may, however, not be a realistic model. genotypes, Hamilton (1980) hypothesized that be-
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