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Journal of Fish Biology (1996) 48, 1256–1265
Parasites as indicators of individual feeding specialization inArctic charr during winter in northern Norway
R. K, A. K F. S
Department of Aquatic Biology, Norwegian College of Fishery Science,University of Tromsø, N-9037 Tromsø, Norway
(Received 17 November 1994, Accepted 26 November 1995)
The relationship between infection with the food-transmitted parasites Diphyllobothriumdendriticum, D. ditremum (Cestoda) and Cystidicola farionis (Nematoda) and prey selectionwas studied in individual Arctic charr from Lake Takvatn, northern Norway. There was nocorrelation between parasites transmitted throughout prey organisms from benthic habitats(amphipods) and pelagic habitats (copepods). A strong relationship between infection with aparasite species and the corresponding intermediate host from the stomach content of individualcharr, indicated an individual feeding specialization. Independent of size, charr specialized onthe intermediate hosts of all three parasite species. Some charr maintained this specialization onspecific prey items throughout the winter period. These parasite species are considered to beuseful indicators of past prey selection. ? 1996 The Fisheries Society of the British Isles
Key words: Arctic charr; feeding specialization; food-transmitted parasites; Cystidicolafarionis; Diphyllobothrium spp.
INTRODUCTION
Parasites have often been used as biological indicators to provide information onfish ecology, including feeding behaviour (MacKenzie, 1983; Konovalov &Butorina, 1985; Moser, 1991; Williams et al., 1992). Individual feeding special-ization is known for several species of invertebrates and vertebrates (Partridge &Green, 1985), including salmonids (Bryan & Larkin, 1972; Amundsen, 1994,1995; Amundsen et al., 1995). The stability of individual feeding specializationsis difficult to measure under natural conditions (Partridge & Green, 1985).Infection of food-transmitted parasites may to some extent reflect past preyselection (Curtis, 1985; Bérubé & Curtis, 1986; Knudsen, 1995).In Lake Takvatn, northern Norway, the Arctic charr Salvelinus alpinus (L.)
population is heavily infected with both Diphyllobothrium dendriticum(Nitzsch) and D. ditremum (Creplin), and with the nematode Cystidicola farionisFisher (Giæver et al., 1991; Kristoffersen, 1993; Knudsen & Klemetsen, 1994).C. farionis has charr as its final host, and the amphipod, Gammarus lacustrisSars, as its only intermediate host in this lake. D. ditremum and D. dendriticummature in fish-eating birds, use copepods as their first intermediate hosts(procercoid-larvae) and fish as their second intermediate host (plerocercoid-larvae). Plerocercoids from small fish are able to re-establish in piscivorous charr(Halvorsen & Wissler, 1973; Curtis, 1984). The intermediate hosts of these threeparasites represent three different feeding strategies for charr: pelagic (oncopepods), benthic (on amphipods) and piscivorous feeding.Tel.: +47-776-46037; fax: +47-776-46020; email: [email protected].
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0022–1112/96/061256+10 $18.00/0 ? 1996 The Fisheries Society of the British Isles
If individual fish specialize on particular types of food, they may be expectedto acquire different parasite loads transmitted by prey items from benthichabitats as opposed to those from pelagic habitats. A relationship betweenparasite infection and the occurrence of the corresponding intermediate hostsfrom the stomach contents of individual fish would then be expected. These twohypotheses are tested by analysing the parasite infections and prey selection ofindividual Arctic charr.
MATERIAL AND METHODS
Lake Takvatn (69)07* N, 19)05* E, 214 m a.s.l.) is an oligotrophic lake in northernNorway. The surface area is 14·2 km2 and the lake has two main basins, each with amaximum depth of 70–80 m. Fish species in the lake are Arctic charr, three-spinedstickleback Gasterosteus aculeatus L., and a small population of brown trout Salmo truttaL. Knudsen & Klemetsen (1994) give information about abiotic conditions during thewinter period, and methods for fish sampling.The charr (n=505) were sampled monthly from November 1987 to June 1988 by
gillnetting. The fish were weighed and measured (FL), and age was determined by thesurface reading of otoliths placed in glycerol. The charr were divided into small(100–149 mm), mid-sized (150–199 mm) and large (§200 mm) size classes followingKnudsen & Klemetsen (1994). Stomach contents were preserved in 70% ethanol. Thefood items were identified and their relative contribution to stomach fullness estimatedaccording to Amundsen (1989). Potential intermediate hosts from the stomachs areexpressed as frequency of occurrence (%) and percentage contribution to stomach content(volume %). Charr were divided into four groups, three feeding groups based on thepresence of prey items which may serve as intermediate hosts (amphipods, copepods andfish), while the remaining fish were placed in a separate group (others). The few fish thatate both copepods and amphipods and those with empty stomachs were excluded fromthe food–parasite analyses. The food–parasite associations were tested by Mann–Whitney U-tests using SYSTAT 5.0 (Systat, Inc., 1992). The least digested G. lacustris(n=985) from stomachs of charr were examined for all larval parasites.The swimbladders were preserved in 70% ethanol and later opened. The nematodes
were classified into three groups according to Giæver et al. (1991): L3, L4 (pre-adult) andadults. The L3-larvae are the recruitment stage. The stomach wall, visceral organs andall cysts in the flesh were placed in digestive fluid (2 ml HCl, 5 g pepsin, 9 g NaCl, in 1 lwater). The excysted Diphyllobothrium plerocercoids were preserved in 4% bufferedformalin, and later species identified according to Andersen & Gibson (1989). Theplerocercoids were measured and placed in 1 mm length classes for D. ditremum, startingat <2 mm, and every 2 mm for D. dendriticum starting at <4 mm. The minimum lengthclasses are regarded as the youngest plerocercoids (see Knudsen & Klemetsen, 1994 fordetails). The terms prevalence and relative density are used according to Margolis et al.(1982).
RESULTS
Individual Arctic charr which were heavily infected with the plerocercoids ofDiphyllobothrium spp. had relatively low numbers of C. farionis and vice versa(Fig. 1). No fish were heavily infected with both copepod- and amphipod-transmitted parasites. The correlation between D. ditremum and C. farionis(r2=0·005, d.f.=1/504) and between D. dendriticum and C. farionis (r2=0·003) inthe total charr sample, were both rejected (P>0·05). The correlation between thetwo Diphyllobothrium species was weak (r2=0·307) but could not be rejected(P<0·001).
1257
There were close relationships between the relative density of parasites and theoccurrence of the corresponding intermediate host in the stomach content of allsize classes of charr (Table I). This included the total relative density, anddensity of the youngest parasite stages. Feeding groups with less than five charrwithin a size class are not shown. Large or mid-sized Arctic charr feeding onfish (sticklebacks and charr) or copepods, had significantly greater levels ofD. dendriticum and D. ditremum infection than did Arctic charr which had eatenamphipods or other prey items (Mann–Whitney U-tests P<0·05). Conversely,piscivorous charr, copepod feeders or charr with other food items had signifi-cantly lower infections of C. farionis than amphipod-feeding charr. The infec-tion pattern of small charr showed the same tendency both in prevalence anddensity. Results of Mann–Whitney U-tests of parasite infection in differentfeeding groups of charr are presented in Table II. Throughout the samplingperiod 40% of the charr had empty stomachs.
8000
1000
00
No. of C. farionis
No.
of
D. d
end
riti
cum 750
500
250
2000 4000 6000
(b)
1000
0
No.
of
D. d
itre
mu
m
750
500
250
(a)
F. 1. Number of C. farionis plotted against (a) D. ditremum and (b) D. dendriticum in individual Arcticcharr (n=505).
1258 . .
T
I.Relativedensity(RD),variancetomeanratio(s2/x)andprevalence(Prev.)ofC.farionis,D
.ditremum
andD.dendriticuminthree
sizeclassesofArcticcharr,dividedaccordingtodi
fferencesinstom
achcontent
Fishsize
(mm)
Feeding
groups
nC.farionis
D.ditremum
D.dendriticum
Age
(&1
..)
RD(x)
s2/x
Prev.
RD(x)
s2/x
Prev.
RD(x)
s2/x
Prev.
§200
Amphipod
321831·7
757·1
100
45·2
24·0
100
3·6
16·9
698·4&0·4
612·6
304·9
972·5
6·7
430·1
1·3
11Fish
10120·8
89·9
100
160·7
141·8
100
30·7
38·9
100
7·4&0·5
8·8
12·1
807·5
4·9
8010·7
22·1
80Other
24799·9
1949·9
9753·8
117·3
975·6
56·9
618·3&0·5
231·8
674·8
652·0
11·5
290·9
17·3
10150–199
Amphipod
35152·9
236·4
100
27·1
21·0
940·9
4·2
314·4&0·2
100·4
175·9
974·7
4·8
830·3
4·3
11Copepod
2835·3
105·3
9673·2
104·0
100
5·1
18·1
714·5&0·2
13·1
58·4
6811·7
5·8
932·2
6·9
62Fish
624·5
16·7
100
42·2
4·0
100
3·2
3·9
100
4·2&0·2
7·7
10·0
839·8
1·9
100
1·5
5·3
50Other
9642·0
126·0
9830·3
28·2
100
1·0
7·6
314·2&0·1
22·5
114·9
846·9
5·8
930·5
6·2
22100–149
Amphipod
1426·3
51·6
926·9
4·8
100
00
03·0&0·1
17·2
34·6
854·3
3·1
93Copepod
812·5
26·2
6318·9
116·8
630
00
3·1&0·2
7·6
13·0
639·6
68·5
50Other
5512·8
33·8
895·4
4·5
840·1
1·0
73·0&0·1
6·7
26·6
712·5
2·6
670·02
1·0
2
Upperlinerepresentthetotalparasitesample,thelowerline(italics)representstheyoungestparasiteindividuals(n=numberoffish).
T
II.ResultsofMann–WhitneyU-testsofdistributionsofC.farionis,D.ditremum
andD.dendriticum,inthreesizeclassesofArctic
charrdividedaccordingtodi
fferencesinstom
achcontent
Feeding
groups
Parasite
species
Charr100–149mm
Charr150–199mm
Charr
§200mm
Copepod
Other
Copepod
Fish
Other
Fish
Other
TOT
YOU
TOT
YOU
TOT
YOU
TOT
YOU
TOT
YOU
TOT
YOU
TOT
YOU
Amphipod
C.farionis
N.S.
N.S.
N.S.
****
***
**
***
***
***
***
***
***
D.ditremum
N.S.
*N.S.
N.S.
***
***
***
N.S.
****
**N.S.
N.S.
D.dendriticum
N.S.
N.S.
N.S.
N.S.
***
***
**N.S.
N.S.
N.S.
***
***
N.S.
N.S.
Other
C.farionis
N.S.
N.S.
——
N.S.
N.S.
N.S.
N.S.
——
N.S.
N.S.
——
D.ditremum
N.S.
N.S.
——
***
***
*—
—**
**—
—D.dendriticum
N.S.
N.S.
——
***
***
***
N.S.
——
*****
——
Fish
C.farionis
——
——
***
***
——
——
——
——
D.ditremum
——
——
***
***
——
——
——
——
D.dendriticum
——
——
***
***
——
——
——
——
TOTrepresentsthetotalparasitenumbersandYOUrepresentsnumberofyoungparasitestages.
Significance:N.S.,notsignificant;*P
¦0·05;**P
¦0·01;***P
¦0·001(—,nottested).SeeTableIfornumberofcharrineachforaging
group.
In the mid-sized charr (150–199 mm), both occurrence of intermediate hosts(copepods and amphipods) from stomachs and prevalence of young D. ditremumand C. farionis were high (Table I). There was an inverse relationship betweenyoung D. ditremum and L3-larvae of C. farionis in charr, as high parasite loadsof one species were associated with low burdens of the other species (Fig. 2). Theprey selection reflects this infection pattern of parasites. A high proportion ofcharr which were heavily infected with young D. ditremum had eaten copepodsbut few fed on amphipods, as compared to charr with low levels of D. ditremum,which had fed on amphipods rather than copepods.All sizes of charr ate G. lacustris frequently. In all size classes, charr which
were most heavily infected with L3-larvae [Fig. 3(a)] and preadult/adults[Fig. 3(b)] of C. farionis, were those individuals that fed quantitatively (frequencyof occurrence %) and qualitatively (volume %) most on G. lacustris. Theserelationships increased with increasing size of charr. G. lacustris from thestomachs of charr had a prevalence of 2·3% larval C. farionis.
DISCUSSION
The negative relationship between parasites transmitted by copepods andthose transmitted by amphipods, as demonstrated between C. farionis and
60
Numerical classes of D. ditremum
Am
phip
ods
10
30
0
30
0 2 4 6 15 20 21>
0
Rel
ativ
e de
nsi
ty o
fL
3-la
rvae
60 7525n=16 23 31 33 20 14 13
50
25Cop
epod
s
Fre
quen
cy o
f oc
curr
ence
(%
)
F. 2. Records (frequency of occurrence) of copepods ( ) and amphipods ( ) against increasing numberof young D. ditremum in middle-sized (150–199 mm) Arctic charr. Relative density of L3-larvae(&1 ..) of C. farionis (-—–-) in identical numerical classes of D. ditremum are shown. Notedifference scaling on x-axes. n=Number of fish in each group.
1261
Diphyllobothrium spp. in individual Arctic charr, is most easily explained bydifferent habitat choice or food habits of the fish host. From other lake systems,infection patterns of helminth species have been shown to correspond withdifferences in habitat and diet of Arctic charr, both in allopatric populations(Knudsen, 1995) and between sympatric morphs (Frandsen et al., 1989). Themonomorphic Arctic charr population in Lake Takvatn segregate in habitat andfood choice during the ice-free season (Amundsen, 1989; Klemetsen et al., 1989,1992; Amundsen et al., 1993; Dahl-Hansen et al., 1994). However, in the presentwinter study almost all fish were caught littorally (Knudsen & Klemetsen, 1994),and the charr within each size-group are assumed to be equally able to utilize theavailable prey items. If the diet was chosen randomly or a result of short-termopportunistic feeding activity, a strong correlation between infection of aparasite species and the corresponding intermediate host from the stomachcontent in individual fishes would not be expected. However, we found a closerelationship in the present study during the winter season indicating thatindividual feeding specialization had occurred. Other studies have shown similarresults during the ice-free season where fish were feeding on copepods or fish(Bérubé & Curtis, 1986) and on amphipods (Knudsen, 1995).Our results indicate that charr may specialize on all known intermediate
hosts of the three present parasite species: amphipods, copepods and fish. Most
0
No. of pre-adults/adults of C. farionis
Fre
quen
cy o
f oc
curr
ence
(%
)
40
0 5 10 11>0
Vol
um
e (%
)
80 80n=20 23 26 18
40
<5 15 40 41>
49 59 48 38
<100 500 1500 1501>
23 22 18 14(b)
0
No. of L3-larvae of C. farionis
40
0 5 15 16>0
80 80n=25 28 21 13
40
0 5 40 41>
29 64 56 45
0 50 500 501>
15 19 20 23(a) Small charr Mid-sized charr Large charr
F. 3. Records of amphipods in stomach content against increasing number of (a) L3-larvae and(b) pre-adults/adults of C. farionis in three size classes of Arctic charr. , frequency of occurrence(%) and , represent volume (%) of amphipods. Note different scaling on x-axes. n=Numberof fish.
1262 . .
of the mid-sized charr, which ingested copepods, were heavily infected withD. ditremum. This indicates a preference for a planktonic diet although moreprofitable benthic prey items were available. This selective feeding behaviourwas seen more clearly in the parasites which were transmitted by amphipods.The strong relationship between increased ingestion of amphipods with increas-ing infection of C. farionis among all size classes of charr, suggests an individualfeeding specialization which is independent of fish size. Closer relationships byincreasing size (and age) of charr imply that experience and learning may bebasic for this kind of individual foraging behaviour (Magurran, 1986).During the winter, Arctic charr stomach contents are assumed to represent the
food selection for the past few days. The close relationship between the presenceof young stages of parasites, and the occurrence of the corresponding intermedi-ate hosts in the stomach contents of individual fish, indicates that some charrhave specialized on specific prey items for several months. The strong relation-ship between the high infection levels with pre-adults/adults of C. farionis and thehigh percentage of ingested amphipods, indicates that this dietary specializationis maintained throughout the winter period, perhaps over several years, as thedevelopment time of C. farionis from L3-larvae to adults takes from 1 to 2 years(Black & Lankester, 1980). If the prevalence of C. farionis found in G. lacustrisreported in the present study reflects the infection level throughout the year, thenthe most heavily infected charr must have eaten very high numbers of amphipodsover a long period of time.In general, some individuals in salmonid populations have often been reported
to be heavily infected with Diphyllobothrium spp. (Vik, 1957; Halvorsen, 1970;Curtis, 1984; Bérubé & Curtis, 1986; Kristoffersen, 1993; Knudsen & Klemetsen,1994) or Cystidicola spp. (Black & Lankester, 1981, 1984; Black, 1985; Giæveret al., 1991; Knudsen & Klemetsen, 1994). A stable selective feeding behaviouron potential intermediate hosts as indicated by our results, may contribute tothe great variance in infection rates in charr of similar size and age, for all of thepresent parasites species.Strong competition is suggested to be one important mechanism causing
dietary specialization (Holbrook & Schmitt, 1992). Interactive behaviour insalmonid populations decreases during the winter (Hindar & Jonsson, 1982;Rembel & Northcote, 1989). Zoobenthic biomass is at a maximum during thewinter period (Nilsson, 1955; Brittain & Lillehammer, 1978), and winter foodresources may be in excess as the charr have low metabolic needs (Rembel &Northcote, 1989). If this is so, then we have demonstrated that individualfeeding specialization may also occur during periods of low competition.
We thank Hanna and Arne Haugli for help at Lake Takvatn and Jessica Marksfor correcting the English. The work was funded by the Research Council of Norway(No. 100610/410).
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