THE ABUNDANCE AND DISTRIBUTION OF LEPEOPHTHEIRUS

SALMONIS(COPEPODA: CALIGIDAE) ON PINK (ONCORHYNCHUS

GORBUSCHA) ANDCHUM (O. KETA) SALMON IN COASTAL BRITISH
COLUMBIA
Author(s): Simon R. M. Jones and N. Brent Hargreaves
Source: Journal of Parasitology, 93(6):1324-1331. 2007.
Published By: American Society of Parasitologists
DOI: http://dx.doi.org/10.1645/GE-1252.1
URL: http://www.bioone.org/doi/full/10.1645/GE-1252.1

BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and
environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published
by nonprofit societies, associations, museums, institutions, and presses.
Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of
BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use.
Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries
or rights and permissions requests should be directed to the individual publisher as copyright holder.

BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research
libraries, and research funders in the common goal of maximizing access to critical research.
 J. Parasitol., 93(6), 2007, pp. 1324–1331
䉷 American Society of Parasitologists 2007

THE ABUNDANCE AND DISTRIBUTION OF LEPEOPHTHEIRUS SALMONIS

(COPEPODA: CALIGIDAE) ON PINK (ONCORHYNCHUS GORBUSCHA) AND
CHUM (O. KETA) SALMON IN COASTAL BRITISH COLUMBIA
Simon R. M. Jones and N. Brent Hargreaves
Pacific Biological Station, 3190 Hammond Bay Road, Nanaimo, British Columbia, V9T 6N7, Canada. e-mail: joness@pac.dfo-mpo.gc.ca

ABSTRACT: In total, 23,750 specimens of the salmon louse, Lepeophtheirus salmonis, were collected from 3,907 juvenile pink
and 3,941 chum salmon caught within the Broughton Archipelago during a 2-yr survey. The prevalence on pink salmon was
significantly higher than on chum salmon in 2004 (62.3% and 58.6%, respectively) and in 2005 (26.4% and 23.1%, respectively).
The mean abundance on chum salmon was significantly higher than on pink salmon in 2004 (7.0 ⫾ 0.3 and 2.8 ⫾ 0.2, respec-
tively), whereas in 2005 the mean abundance did not differ between species (0.6 ⫾ 0.1 and 0.5 ⫾ 0.0, respectively). The mean
intensity on chum salmon was significantly higher than on pink salmon in 2004 (12.0 ⫾ 0.4 and 4.5 ⫾ 0.2, respectively) and in
2005 (2.5 ⫾ 0.2 and 1.7 ⫾ 0.1, respectively). The prevalence, intensity, and abundance of L. salmonis were significantly higher
on salmon belonging to both host species in 2004 compared with 2005. In both years, a majority of pink and chum salmon had
2 or fewer lice. In general, a decline in abundance of L. salmonis over the 3 collection periods in each year coincided with an
increased percentage of motile developmental stages. The abundance was lowest on fish collected from zones in which the
seawater surface salinity was also lowest. Seawater surface temperature was higher and salinity was lower in 2004 compared
with 2005. The spatial and temporal trends in the abundance of L. salmonis in relation to host size, infestation rates, and seawater
salinity and temperature, evident in both years, must be considered in future studies assessing the role of farmed salmon in the
epizootiology of this parasite on juvenile salmon in this area.

The marine ecosystem of the Broughton Archipelago in settlement of L. salmonis (Pike and Wadsworth, 1999; Boxas-
coastal British Columbia, Canada (Fig. 1), is hydrographically pen, 2006; Bricknell et al., 2006). Thus, the relative roles of
and biologically complex. The area supports numerous popu- oceanographic processes and the availability of nonsalmonid
lations of Pacific salmon (Oncorhynchus spp.), and there are 28 and salmonid (farmed and nonfarmed) hosts in influencing the
sites for the production of farmed Atlantic salmon (Salmo sa- epizootiology of L. salmonis in the Broughton Archipelago re-
lar), of which 15 to 18 are typically active at any time. There main unclear. The objective of this study was to describe pat-
are few studies of the relationships among the physical and terns of L. salmonis infestation, salmon size, water temperature,
biological components of this region (e.g., see Brooks, 2005; and salinity over 2 yr in the Broughton Archipelago.
Foreman et al., 2006). The Broughton Archipelago has been the
focus of recent scientific debate because of concerns that ju- MATERIALS AND METHODS
venile pink (O. gorbuscha) and chum (O. keta) salmon migrat- The study area, including its stratification into 11 zones, and the
ing from natal streams in the area toward the open ocean are methods by which salmon were collected using beach and purse seine
vulnerable to infestations with the salmon louse, Lepeophthei- gear were described previously (Jones, Prosperi-Porta et al., 2006). Data
rus salmonis (Morton et al., 2004; Krkošek et al., 2005, 2006). were collected during 6 periods, 3 in each of 2004 and 2005 (see Table
I for the corresponding dates). Fish were collected from approximately
These studies concluded that the spatial and temporal patterns 10 sites per zone in all periods. Fish were confined into a small volume
of mixed infestations with L. salmonis and a related parasite, of water within the net, individually bagged directly from the net, la-
Caligus clemensi, are consistent with proximity of the pink and belled, and immediately frozen. The first 30 specimens of each salmon
chum salmon to salmon farms. Furthermore, the studies con- species to be bagged were selected for examination. The frozen speci-
mens were transported to the laboratory for species confirmation and
cluded that the farmed salmon serve as reservoirs of the salmon microscopic examination. Wet weight and fork length were determined
louse. However, despite the presence of salmon farms and in- for each fish, and all lice, including those free in the bag, were counted,
festations with L. salmonis, measurements made in 2003 and and identified to species and to developmental stage according to pub-
2004 indicated that pink salmon in this area experienced high lished criteria (Kabata, 1988; Johnson and Albright, 1991). After iden-
marine survival (Beamish et al., 2006). tification, lice were stored in 70% ethanol for future reference. Salinity
and temperature data were obtained from samples of surface seawater
Lepeophtheirus salmonis is a common parasite of salmonids collected from most sites in each period. Salinity was estimated from
in seawater in the Northern Hemisphere. The parasite undergoes conductivity using a salinometer as described previously (Jones et al.,
direct development, which includes planktonic (2 nauplii), in- 2006), and temperature was measured using a hand-held thermometer.
fective (1 copepodid), and parasitic (4 chalimus, 2 preadult, 1 Prevalence, mean intensity, and mean abundance of L. salmonis were
defined according to Bush et al. (1997). The significance of differences
adult) stages (Johnson and Albright, 1991). In the Broughton in these parameters was tested using the chi-square and Kruskal–Wallis
Archipelago, L. salmonis and C. clemensi were found to infest tests. The significance of log-transformed weights was tested using Bon-
a high proportion of three-spine stickleback (Gasterosteus acu- ferroni-adjusted 2-sample t-tests. The significance of differences in
leatus) (Jones, Prosperi-Porta et al., 2006), which was a pre- mean salinity and mean temperature was tested using the Kruskal–Wal-
viously unrecognized host species for L. salmonis. Furthermore, lis test. In all cases, differences were considered significant when P ⱕ
0.05.
the abundance of these parasites was lower on sticklebacks col-
lected from zones in which the seawater salinity was also low
RESULTS
(Jones, Prosperi-Porta et al., 2006). This observation is consis-
tent with the adverse effect of low salinity on the survival and Over 2 yr, 3,907 pink and 3,941 chum salmon were exam-
ined, and 23,750 L. salmonis in total were collected. Approxi-
mately 80% of all fish samples were obtained from 6 of the 11
Received 9 March 2007; revised 4 May 2007; accepted 23 May 2007. zones surveyed, i.e., D, E, F, G, H, and K (see Fig. 1; Tables

1324
 JONES AND HARGREAVES—SALMON LICE ON JUVENILE PACIFIC SALMON 1325

FIGURE 1. Map of study area showing major water bodies and zone designations. bi, Broughton Island; gi, Gilford Island. Reproduced from
Jones et al. (2006). Journal of Parasitology 92: 473–480 (with permission).

I, II). Similarly, 45.9% of samples were collected in period 1,

whereas 18.7% were collected in period 3 (Table III). The
TABLE I. Infestations with Lepeophtheirus salmonis on pink salmon weight of pink and chum salmon increased significantly during
(Oncorhynchus gorbuscha) collected from the Broughton Archipelago, the surveys in both years (Table III), and this trend was evident
British Columbia. in most zones, although the salmon tended to be smallest in
zones A, B, C, and J.
2004 2005 In both years, the overall prevalence of L. salmonis on pink
Zone* 1† 2 3 1 2 3 salmon was significantly higher than on chum salmon (62.3%
vs. 58.6% in 2004; 26.4% vs. 23.1% in 2005; P ⫽ 0.02 both
A 0/1‡ 0/8 0/0 0/10 0/3 0/0
years). A significantly higher overall prevalence was observed
B 1/1 0/2 0/0 0/3 0/2 0/0
on both species in 2004 (P ⬍ 0.01). In contrast, the overall
C 0/0 0/0 0/0 1/13 0/0 0/0
D 33/85 35/64 0/0 7/101 15/58 1/55 mean abundance of L. salmonis on chum salmon in 2004 (7.0
E 49/98 64/107 1/2 21/120 20/109 5/67 ⫾ 0.3) was significantly higher than on pink salmon (2.8 ⫾ 0.2)
F 222/285 63/112 36/56 11/59 47/124 15/103 (P ⬍ 0.01), whereas in 2005, there was no significant difference
G 61/111 24/37 5/8 82/234 14/48 5/57 in overall mean abundance between the host species (0.6 ⫾ 0.1
H 142/214 133/208 34/44 95/188 50/175 10/115 and 0.5 ⫾ 0.0, respectively) (P ⫽ 0.10). The overall abundance
I 1/4 9/9 0/0 19/71 6/23 5/32 on both species was significantly higher in 2004 (P ⬍ 0.01). In
J 0/1 0/3 0/0 0/3 1/1 0/0
both years, the overall mean intensity on chum salmon was
K 10/18 15/24 0/0 72/183 98/315 34/133
significantly higher than on pink salmon (12.0 ⫾ 0.4 vs. 4.5 ⫾
* See Figure 1 for locations of zones. 0.2 in 2004; 2.5 ⫾ 0.2 vs. 1.7 ⫾ 0.1 in 2005) (P ⬍ 0.01 both
† Collection period (2004): 1 ⫽ 25 May–1 June, 2 ⫽ 22–29 June, 3 ⫽ 20–26
July; (2005): 1 ⫽ 23 May–1 June, 2 ⫽ 20–29 June, 3 ⫽ 18–27 July. years). The overall mean intensity on both species was signif-
‡ Number infested/number examined. icantly higher in 2004 (P ⬍ 0.01).
1326 THE JOURNAL OF PARASITOLOGY, VOL. 93, NO. 6, DECEMBER 2007

TABLE III. Temporal changes in Lepeophtheirus salmonis infestations on juvenile pink (Oncorhynchus gorbuscha) and chum (O. keta) salmon from the Broughton Archipelago, British

Cop* (%) Motile (%)

TABLE II. Infestations with Lepeophtheirus salmonis on chum salmon

70.6†‡
(Oncorhynchus keta) collected from the Broughton Archipelago, British

34.0†

44.9†
15.8

29.1

37.1
Columbia.

2004 2005

5.4†‡
23.7†

8.2†
Zone* 1† 2 3 1 2 3

30.5

14.4

11.4
A 0/39‡ 0/5 0/0 0/34 0/4 0/0
B 6/26 0/6 0/0 2/95 0/25 0/3

Prev* (%)
C 2/2 0/0 0/0 2/23 1/6 0/2

23.6†‡

8.0†‡
61.0†

23.7†
D 98/127 56/104 0/5 15/123 1/20 5/40

71.8

29.7
E 32/36 57/134 6/60 11/47 7/51 0/5
F 212/218 48/64 25/61 17/64 5/19 2/23
G 81/94 36/46 31/124 21/29 2/3 0/9

Chum

0.2†‡
H 169/180 157/218 27/68 50/59 39/121 14/58

0.5†

0.0†
0.5

0.1
0.1
Abund*
I 39/72 26/62 13/98 36/63 1/3 1/100

⫾
⫾
⫾
⫾
⫾
⫾
J 11/140 6/70 2/47 16/83 0/42 0/2

9.8
6.8
1.0
0.8
0.5
0.1
K 166/202 156/181 10/21 26/40 53/165 3/70

* See Figure 1 for locations of zones.

† Collection period (see Table I for dates).

0.6†‡

0.8†‡
‡ Number infested/number examined.

0.2†

0.3†
Weight (g)

0.1

0.1
⫾
⫾
⫾
⫾
⫾
⫾
In 2004, the maximum number of L. salmonis observed was

3.8
9.6
28.7
5.0
14.2
27.6
175 on a chum and 79 on a pink salmon, whereas in 2005 the
maxima were 30 and 17, respectively. In 2004, 2, or fewer, lice
were observed on 69.4% of pink and 53.2% of chum salmon,

No. fish

1,136
890
484
660
459
312
whereas in 2005, these values were 95.8% and 93.8% (Fig. 2).
A category of ⬎10 lice per fish was notable in 2004 (5.7% of
pink and 19.9% of chum salmon) but not in 2005 (0.04% and

* P, collection period (see Table I for dates); Abund, mean abundance (⫾ SE); Prev, prevalence; Cop, copepodid.
Prev* (%) Cop* (%) Motile (%)
0.6%, respectively) (Fig. 2). In 2004, copepodids predominated

94.9†‡

95.0†‡
82.3†

87.5†
on pink and chum salmon, whereas in 2005 the predominant

26.0

47.4
stages were preadults on chum and adults on pink salmon (Fig.
2). In both years, all 4 chalimus stages were more abundant on
chum salmon than on pink salmon.
3.3†‡
13.6†

4.6†
1.0†
43.7

21.9
Significant declines in the mean abundance of L. salmonis
over the 3 collection periods occurred on chum salmon in both
years and on pink salmon in 2005 (Table III). The mean abun-
dance on pink salmon increased between periods 2 and 3 such
13.3†‡
69.1‡
63.4
59.2

31.3
29.3

that the significantly lower mean abundance of L. salmonis on

pink compared with chum salmon described above for 2004
was only evident in periods 1 and 2. The prevalence on chum
0.2†‡

0.0†‡

salmon decreased significantly over the 3 periods in both years

0.1†
Pink

0.3

0.0
0.0
Abund*

and on pink salmon in 2005 (Table III). Parasite development

⫾
⫾
⫾
⫾
⫾
⫾

was estimated by calculating the percentage of motile (preadult

3.8
1.6
2.0
0.6
0.5
0.2

and adult) stages. Percentage of motile stages on pink salmon

increased to 95% in both years. On chum salmon, percentage
of motiles only increased significantly by period 3 in 2004 (Ta-
† Significantly different from collection period 1.
‡ Significantly different from collection period 2.

ble III). Significant reductions in the proportion of copepodids

0.5†‡

0.2†‡
0.1†

0.1†
Weight (g)

0.1

0.0

were observed on pink salmon in both years and on chum salm-

on in 2004.
⫾
⫾
⫾
⫾
⫾
⫾

Similar spatial patterns in the abundance of L. salmonis were

3.3
6.8
14.6
2.5
7.0
13.2

observed for both host species and in both years. Mean abun-
dance tended to be greatest in those zones within Tribune Chan-
No. fish

nel (F, G, and H), lower Knight Inlet (E), and Well’s Passage
818
574
110
985
858
562

(K) (Fig. 3). Conversely, mean abundance was consistently

lowest in the zones furthest inland (A, B, and J), and these
patterns were most pronounced in periods 1 and 2. A decline
P*

1
2
3
1
2
3

in mean abundance was evident in most zones, resulting in a

Columbia.

spatial pattern of mean abundance in period 3 that was less

2004

2005
Year

conspicuous than in earlier periods. Nevertheless, in period 3,

differences in mean abundance among zones in which lice were
 JONES AND HARGREAVES—SALMON LICE ON JUVENILE PACIFIC SALMON 1327

FIGURE 2. Distribution and developmental stages of Lepeophtheirus salmonis on juvenile pink and chum salmon in the Broughton Archipelago.
Percentage of salmon with salmon lice in 2004 (A) and 2005 (B). Percent of developmental stages in 2004 (C) and 2005 (D). Co, copepodid;
C1–C4, chalimus I to IV; PAd, preadult (both stages and sexes); Ad, adult (both sexes).

detected were still significant (P ⬍ 0.01) on chum salmon in DISCUSSION

both years and on pink salmon in 2005. The prevalence on both
salmon species also varied among zones and followed a trend Infestations with L. salmonis were observed on 2.5- to
similar to that described for abundance (Tables I, II). 28.7-g pink and chum salmon from the Broughton Archipelago
The mean surface salinity was 15.1 parts per thousand (ppt) in British Columbia, Canada, collected over 2 yr. All measures
(range, 0.02–30.5) in 2004 and 20.2 ppt (range, 0.05–30.9) in of L. salmonis infestation in 2005 were significantly lower than
2005. Salinity decreased significantly between the first and third in 2004, and in neither year were infestations uniform through-
periods in both years (Table IV). In all periods, salinity was out the study area. In addition, distinct patterns of infestation
significantly lower in 2004 compared with 2005 (P ⬍ 0.01). were observed on pink and chum salmon in both years. The
Significant variation in salinity was observed among zones in present study confirmed earlier work documenting year-to-year
both years (Fig. 4). Salinity was greatest in zones closest to the differences in the abundance of L. salmonis on juvenile salmon
open ocean (E, H, and K) and least in zones furthest inland (A, in the Broughton Archipelago. Significantly higher abundances
B, and J). The significant decline in salinity among periods of L. salmonis were reported on juvenile pink and chum salmon
described above was most evident in those zones furthest from in 2004 compared with 2002 and 2003 (Morton et al., 2005).
the open ocean (zones A, B, C, I, and J) (Fig. 4). The latter study reported an overall abundance of 9.75 for 2004,
The mean surface temperature was 14.6 C (range, 6.8–23.2 but it did not report infestations on pink and chum salmon sep-
C) in 2004 and 12.8 C (range, 8.5–19.8 C) in 2005. In both arately. Relatively low abundances were also reported for 2003,
years, temperatures increased significantly between the first and and in that year, C. clemensi was approximately 3 times more
second periods (Table IV), and a trend of increasing tempera- abundant than L. salmonis on both salmon species (Jones and
ture was evident in most zones (Fig. 4). In all periods, the Nemec, 2004). The abundance of L. salmonis on juvenile pink
temperature was significantly higher in 2004 compared with and chum salmon in the study area in 2006 was similar to that
2005 (P ⬍ 0.01) (Table IV). Significant differences in temper- observed in 2003 (S. Jones, unpubl. obs.). Together, these stud-
ature were evident among zones, and these differences were ies support a significantly higher abundance of L. salmonis in
most pronounced in period 3 (Fig. 4). With the exception of 2004 compared with the adjacent years. This pattern of inter-
zones A and B, temperatures were higher throughout the study annual variability with peak abundance occurring in 2004 was
area in 2004 compared with 2005. The warmest water occurred also evident on three-spine sticklebacks collected from the same
in Kingcome Inlet (zones I and J) in both years. The water was area (Jones and Nemec, 2004; Jones, Prosperi-Porta et al., 2006;
coolest in upper Knight Inlet (zone A) in 2004 and in lower S. Jones, unpubl. obs.). Interannual differences in the abun-
Knight Inlet (zone E) in 2005. dance of L. salmonis on wild migrating salmon smolts have
1328 THE JOURNAL OF PARASITOLOGY, VOL. 93, NO. 6, DECEMBER 2007

FIGURE 3. Mean abundance of Lepeophtheirus salmonis on juvenile pink salmon (Oncorhynchus gorbuscha) (A–B) and chum salmon (On-
corhynchus keta) (C–D), from zones within the Broughton Archipelago in 2004 and 2005. Error bars are SEM. See Figure 1 for locations of
zones and Table I for dates of collection periods.

also been reported from Norway (Heuch et al., 2005). Morton regardless of whether salmon farms were held fallow along this
et al. (2005) concluded that the relatively low abundance ob- watercourse (Jones and Nemec, 2004). It is possible that treat-
served in 2003 was the result of a coordinated fallow of several ment of farmed salmon for sea lice infestations may explain
salmon farms along Tribune Channel coincident with the mi- the patterns of variation in L. salmonis abundance on the ju-
gration of the juvenile salmon. The absence of coordinated fal- venile salmon. A fall in the abundance of caligid planktonic
lows in 2002 and 2004 was said to have resulted in the elevated stages was observed in Loch Shieldaig shortly after farmed
abundances observed in those years. However, the 4-fold re- salmon in the loch were treated for L. salmonis infestations
duction in abundance reported here for most zones and on both (Penston et al., 2004). However, there were no significant dif-
salmon species in 2005 also occurred in the absence of a co- ferences in annual sea lice treatment rates of farmed salmon in
ordinated fallow of farm sites in Tribune Channel (J. Constan- the Broughton Archipelago between 2003 and 2005 (Saksida et
tine and S. Saksida, pers. comm.). Furthermore, the abundance al., 2007), suggesting treatment alone does not explain the year-
of L. salmonis on juvenile salmon in Tribune Channel was to-year variation in abundance. Variation in the capacity of sea-
amongst the highest observed in each of 2003, 2004, and 2005, water to support the development, survival, and retention of the
planktonic nauplii in the study area requires consideration as an
alternative explanation. Temperature was significantly higher in
TABLE IV. Salinity and temperature of surface seawater within the 2004 compared with 2005. The seawater temperature reported
Broughton Archipelago, British Columbia, in 2004 and 2005. by Jones and Nemec (2004) for the equivalent of period 1 in
2003 was lower than that of 2004 and 2005. Similarly, Morton
Sample et al. (2005) reported cooler water temperatures in 2003 com-
Year Period size Salinity (‰) Temperature (⬚C) pared with 2002 and 2004. Laboratory studies support a role
2004 1* 144 15.0 ⫾ 0.7 13.1 ⫾ 0.1
of temperature in controlling developmental rates and promot-
2 147 17.2 ⫾ 0.8† 15.3 ⫾ 0.2† ing settlement success of larval L. salmonis (Tucker et al.,
3 144 13.2 ⫾ 0.7‡ 15.6 ⫾ 0.2† 2000). The apparent association of the abundance of L. sal-
2005 1 149 22.1 ⫾ 0.7 12.0 ⫾ 0.2 monis and seawater temperature over several years requires
2 151 19.8 ⫾ 0.8† 13.0 ⫾ 0.2† closer examination. Future research should also focus on salin-
3 149 18.8 ⫾ 0.9† 13.4 ⫾ 0.2† ity and temperature during the weeks preceding the juvenile
salmon migration, because these factors may be informative in
* See Table I for dates.
† Significantly different from collection period 1. understanding the occurrence of infective copepodids when the
‡ Significantly different from collection period 2. salmon first encounter seawater.
 JONES AND HARGREAVES—SALMON LICE ON JUVENILE PACIFIC SALMON 1329

FIGURE 4. Mean surface seawater temperatures and salinities collected within the Broughton Archipelago in 2004 and 2005. Error bars are
SEM. See Figure 1 for locations of zones and Table I for dates of collection periods.

In neither 2004 nor 2005 were L. salmonis infestations uni- (Jones, Prosperi-Porta et al., 2006), raising the possibility that
formly distributed within the study area. Despite the differences the sticklebacks had migrated into this zone from areas of high-
in overall abundance between years, the parasite was most com- er salinity or that the L. salmonis in the study area are more
monly found on salmon from Tribune Channel (zones F, G, and tolerant of reduced salinity than expected (see Pike and Wads-
H), lower Knight Inlet (zone E), and Well’s Passage (zone K). worth, 1999). However, until salinity depth profiles are more
This is similar to the distribution of L. salmonis and C. clemensi adequately characterized within the study area, it is prudent to
observed on pink and chum salmon in 2003 (Jones and Nemec, use the surface salinity values reported here as indicators of
2004) and on sticklebacks in 2004 (Jones, Prosperi-Porta et al., spatial trends in the abundance of L. salmonis, rather than as
2006). Generally, juvenile salmon enter the sea from rivers predictors of its presence or absence. Other studies have con-
within the study area and migrate westerly toward the open cluded that local elevations in the abundance of L. salmonis
ocean. During this migration, they grow and move from areas and C. clemensi resulted from the proximity of the captured
of lower to higher salinity. The relatively low numbers of pink fish to salmon farms (Morton et al., 2004; Krkošek et al., 2005,
salmon collected from zones A, B, C, and J indicated that most 2006). Although the conclusions drawn in the latter studies re-
salmon from rivers in the headwaters of Knight and Kingcome main controversial (e.g., Brooks and Stucchi, 2006), it is well
Inlets had already migrated from these regions when collections established from coastal regions of Scotland, Norway, and Ire-
were made. In contrast, in period 1 of both years, chum salmon land that the local abundance of planktonic and parasitic stages
were still relatively abundant in these zones. Low abundances of L. salmonis is elevated when farmed salmon populations that
of L. salmonis were associated with zones in which the salmon occupy the same water body are known to be infested with egg-
were smallest and had the least opportunity for exposure to L. producing female L. salmonis (McKibben and Hay, 2004; Pen-
salmonis. In addition, the low salinities in these zones may have ston et al., 2004; Heuch et al., 2005). Thus, the present work
further impaired the viability and developmental potential of is consistent with earlier studies in identifying spatial patterns
planktonic stages of the parasite, consistent with laboratory ob- in the variation of L. salmonis. The variation was shown here
servations (Bricknell et al., 2006). A relatively low level of to occur on a population of rapidly growing juvenile salmon as
infestation in zones B and C was evident from the reduced they migrated through a coastal habitat of variable salinity and
proportions of copepodids on sticklebacks (6.7% and 2.6%, re- temperature. The significant spatial and temporal variations in
spectively) (Jones, Prosperi-Porta et al., 2006). Interestingly, abundance of L. salmonis on farmed salmon in this area (Sak-
copepodids accounted for 33.6% of developmental stages on sida et al., 2007) raises the possibility that common environ-
sticklebacks from another area of low salinity (zone J, ⬍10 ppt) mental processes play a role in regulating the abundance of the
1330 THE JOURNAL OF PARASITOLOGY, VOL. 93, NO. 6, DECEMBER 2007

parasite on captive and wild populations. Thus, we are presently that of farmed salmon, in influencing the epizootiology of L.
modeling the significance of environmental, host, and farm pa- salmonis.
rameters as sources of variation in L. salmonis infestations on
juvenile Pacific salmon. ACKNOWLEDGMENTS
Temporal trends evident during each of the 2 yr included a We acknowledge the skippers and crews of the seine vessels Clupea,
decrease in salinity, an increase in temperature, and an increase Lahaina Joye, Walker Rock, and Western Eagle. We also thank P. Cal-
in the weight of salmon in both species. The changes in salinity low of the Aquatic Animal Health Laboratory, Pacific Biological Sta-
and temperature are seasonal and related to the estuarine flow tion. Drs. S. Johnson and S. Saksida provided critical comments on an
early draft of this paper. This research was funded by Fisheries and
resulting from increased summer melting of snow and ice in Oceans Canada.
adjacent mountains (Foreman et al., 2006). Similarly, the rapid
growth of pink and chum salmon after entry into the ocean is LITERATURE CITED
well documented (Heard, 1991; Salo, 1991). Coincident with
BEAMISH, R. J., S. JONES, C. NEVILLE, R. SWEETING, G. KARREMAN, S.
these trends was a decreasing abundance of L. salmonis on both SAKSIDA, AND E. GORDON. 2006. Exceptional production of pink
species; however, trends in other measures of infestation were salmon in 2003/2004 indicates that farmed salmon and wild Pacific
not consistent between pink salmon and chum salmon. For ex- salmon can coexist successfully in a marine ecosystem on the Pa-
ample, the prevalence of L. salmonis increased on pink salmon cific coast of Canada. ICES Journal of Marine Science 63: 1326–
but decreased on chum salmon in 2004, whereas prevalence 1337.
———, C. M. NEVILLE, R. M SWEETING, S. R. M. JONES, N. AMBERS,
decreased on both species in 2005. The occurrence of new in- E. K. GORDON, K. L. HUNTER, AND T. E. MCDONALD. 2007. A
festations was estimated from the proportion of copepodids. As proposed life history strategy for the salmon louse, Lepeophtheirus
the percentage of copepodids decreased, motile stages became salmonis in the subarctic Pacific. Aquaculture 264: 428–440.
more abundant, increasing to approximately 95% on pink sal- BOXASPEN, K. 2006. A review of the biology and genetics of sea lice.
ICES Journal of Marine Science 63: 1304–1316.
mon in both years and to 71% on chum salmon in 2004. On BRICKNELL, I. R., S. J. DALESMAN, B. O’SHEA, C. C. PERT, AND A. J.
chum salmon in 2005, however, the percentage of neither co- MORDUE LUNTZ. 2006. Effect of environmental salinity on sea lice
pepodids nor motile stages changed over time. A smaller pro- Lepeophtheirus salmonis settlement success. Diseases of Aquatic
portion of motile L. salmonis was consistently observed on Organisms 71: 201–212.
chum compared with pink salmon throughout the study. The BROOKS, K. M. 2005. The effects of water temperature, salinity and
currents on the survival and distribution of the infective copepodid
distinct pattern of L. salmonis development, in addition to the stage of sea lice (Lepeophtheirus salmonis) originating on Atlantic
overall higher level of infestation on chum compared with pink salmon farms in the Broughton Archipelago of British Columbia,
salmon, was similar to laboratory studies. Infestations in these Canada. Reviews in Fishery Science 13: 177–204.
studies were lower on juvenile pink salmon as a result of a ———, AND D. J. STUCCHI. 2006. The effects of water temperature,
salinity and currents on the survival and distribution of the infective
more rapid rejection of L. salmonis from pink compared with copepodid stage of the salmon louse (Lepeophtheirus salmonis)
chum salmon after controlled exposures (Jones, Kim, and originating on Atlantic salmon farms in the Broughton Archipelago
Dawe, 2006; Jones et al., 2007). The trends suggested that, in of British Columbia, Canada (Brooks, 2005)—A response to the
general, infestations were acquired early during the seaward rebuttal of Krkošek et al. (2005a). Reviews in Fisheries Science
migration of pink salmon and that parasite development coin- 14: 13–23.
BUSH, A. O., K. D. LAFFERTY, J. M. LOTZ, AND A. W. SHOSTAK. 1997.
cided with salmon growth. This agrees with a life history strat- Parasitology meets ecology on its own terms: Margolis et al. re-
egy in which L. salmonis infestations on salmon that overwinter visited. Journal of Parasitology 83: 575–583.
in coastal habitats serve as a reservoir for infestations on ju- FOREMAN, M. G. G., D. J. STUCCHI, Y. ZHANG, AND A. M. BAPTISTA.
venile salmon that have recently entered the ocean (Beamish et 2006. Estuarine and tidal currents in the Broughton Archipelago.
Atmosphere Ocean 44: 47–63.
al., 2007). The possibility that sticklebacks serve as a reservoir HEARD, W. R. 1991. Life history of pink salmon (Oncorhynchus gor-
of L. salmonis infestations that establish on juvenile salmon by buscha). In Pacific salmon life histories, C. Groot and L. Margolis
the settlement of motile preadult stages requires further inves- (eds.). UBC Press, Vancouver, British Columbia, Canada, p. 121–
tigation. Prevalence on pink salmon remained between 60 and 230.
70% in 2004, indicating most infested fish remained in the pop- HEUCH, P. A., P. A. BJØRN, B. FINSTAD, J. C. HOLST, L. ASPLIN, AND F.
NILSEN. 2005. A review of the Norwegian ‘‘National Action Plan
ulation. In contrast, the declining prevalence on chum salmon Against Salmon Lice on Salmonids’’: the effect on wild salmonids.
in 2004 indicated a proportion of infested fish failed to remain Aquaculture 246: 79–92.
in the population. In 2005, declining prevalences on both spe- JOHNSON, S. C., AND L. J. ALBRIGHT. 1991. The developmental stages
cies suggested infested fish did not remain in the population or of Lepeophtheirus salmonis (Krøyer, 1837) (Copepoda: Caligidae).
Canadian Journal of Zoology 69: 929–950.
that L. salmonis was rejected from the salmon. Although there JONES, S. R. M., M. D. FAST, AND S. C. JOHNSON. 2007. Differential
are insufficient data to distinguish between these scenarios, the rejection of salmon lice by pink and chum salmon: Disease con-
laboratory studies cited above, in combination with the rela- sequences and expression of proinflammatory genes. Diseases of
tively low level of infestation observed in 2005, support the Aquatic Organisms 75: 229–238.
possibility that rejection by the host accounted for some of the ———, E. KIM, AND S. DAWE. 2006. Experimental infections with Le-
peophtheirus salmonis (Krøyer) on threespine sticklebacks, Gas-
reduced prevalence. terosteus aculeatus L. and juvenile Pacific salmon, Oncorhynchus
The present study has documented significant spatial and spp. Journal of Fish Diseases 29: 489–495.
temporal trends in L. salmonis infestation on juvenile pink ———, AND A. NEMEC. 2004. Pink salmon action plan: Sea lice on
salmon and chum salmon over 2 yr, coincident with trends in juvenile salmon and some non-salmonid species in the Broughton
Archipelago in 2003. Canadian Science Advisory Secretariat Re-
salmon size, and in the temperature and salinity of surface sea- search Document 2004/105. Fisheries and Oceans Canada, Ottawa,
water. Ongoing research seeks to establish the relative magni- Ontario, Canada, 87 p.
tude of these environmental and biological variables, relative to ———, G. PROSPERI-PORTA, E. KIM, P. CALLOW, AND N. B. HAR-
 JONES AND HARGREAVES—SALMON LICE ON JUVENILE PACIFIC SALMON 1331

GREAVES. 2006. The occurrence of Lepeophtheirus salmonis and ———, ———, C. PEET, AND A. LADWIG. 2004. Sea lice (Lepeophthei-
Caligus clemensi (Copepoda: Caligidae) on threespine stickleback rus salmonis) infection rates on juvenile pink (Oncorhynchus gor-
Gasterosteus aculeatus in coastal British Columbia. Journal of Par- buscha) and chum (Oncorhynchus keta) salmon in the nearshore
asitology 92: 473–480. marine environment of British Columbia, Canada. Canadian Jour-
KABATA, Z. 1988. Copepoda and Branchiura. In Guide to the parasites nal of Fisheries and Aquatic Sciences 61: 147–157.
of fishes of Canada. Part II—Crustacea, L. Margolis and Z. Kabata PENSTON, M. J., M. A. MCKIBBEN, D. W. HAY, AND P. A. GILLIBRAND.
(eds.). Canada Special Publication in Fisheries and Aquatic Sci- 2004. Observations on open-water densities of sea lice larvae in
ences 101, Ottawa, Ontario, Canada, p. 3–127. Loch Shieldaig, Western Scotland. Aquaculture Research 35: 793–
KRKOŠEK, M., M. A. LEWIS, A. MORTON, L. N. FRAZER, AND J. P. VOLPE. 805.
2006. Epizootics of wild fish induced by farm fish. Proceedings of PIKE, A. W., AND S. L. WADSWORTH. 1999. Sea lice on salmonids: Their
the National Academy of Sciences USA 103: 15506–15510. biology and control. Advance in Parasitology 44: 233–330.
———, ———, AND J. P. VOLPE. 2005. Transmission dynamics of par- SAKSIDA, S., G. A. KARREMAN, J. CONSTANTINE, AND A. DONALD. 2007.
asitic sea lice from farm to wild salmon. Proceedings of the Royal Differences in Lepeophtheirus salmonis abundance levels on At-
Society B 272: 689–696. lantic salmon farms in the Broughton Archipelago, British Colum-
MCKIBBEN, M. A., AND D. W. HAY. 2004. Distributions of planktonic bia, Canada. Journal of Fish Diseases 30: 357–366.
sea lice larvae Lepeophtheirus salmonis in the inter-tidal zone in SALO, E. O. 1991. Life history of chum salmon (Oncorhynchus keta).
Loch Torridon, Western Scotland in relation to salmon farm pro- In Pacific salmon life histories, C. Groot and L. Margolis (eds.).
duction cycles. Aquaculture Research 35: 742–750. UBC Press, Vancouver, British Columbia, Canada, p. 231–309.
MORTON, A., R. ROUTLEDGE, AND R. WILLIAMS. 2005. Temporal patterns TUCKER, C. S., C. SOMMERVILLE, AND R. WOOTTEN. 2000. The effect of
of sea louse infestation on wild Pacific salmon in relation to the temperature and salinity on the settlement and survival of cope-
fallowing of Atlantic salmon farms. North American Journal of podids of Lepeophtheirus salmonis (Krøyer, 1837) on Atlantic
Fisheries Management 25: 811–821. salmon, Salmo salar L. Journal of Fish Diseases 23: 309–320.