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www.elsevier.com/locate/jembe

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Journal of Experimental Marine Biolog

Role of olfaction and vision in homing behaviour of black

rockfish Sebastes inermis

Hiromichi Mitamuraa,T, Nobuaki Araia, Wataru Sakamotob, Yasushi Mitsunagac,

Hideji Tanakad, Yukinori Mukaie, Kenji Nakamurae, Masato Sasakif, Yoshihiro Yonedaf

aGraduate School of Informatics, Kyoto University, 606-8501, JapanbFisheries Laboratory of Kinki University, 649-2211, JapancFaculty of Agriculture, Kinki University, 631-8505, Japan

dCOE for Neo-Science of Natural History, Graduate School of Fisheries Science, Hokkaido University, 041-8611, JapaneChateau Marine Survey Co., Ltd., 534-0025, Japan

fKansai International Airport Co., Ltd., 549-8501, Japan

Received 11 November 2004; received in revised form 14 February 2005; accepted 15 February 2005

Abstract

How fish find their original habitat and natal home remains an unsolved riddle of animal behaviour. Despite extensive efforts

to study the homing behaviour of diadromous fish, relatively little attention has been paid to that of non-diadromous marine

fish. Among these, most rockfish of the genus Sebastes exhibit homing ability and/or a strong fidelity to their habitats.

However, how these rockfish detect the homeward direction has not been clarified. The goal of the present research was to

investigate the sensory mechanisms involved in the homing behaviour of the black rockfish Sebastes inermis, using acoustic

telemetry. Vision-blocked or olfactory-ablated rockfish were released in natural waters and their homing behaviours compared

with those of intact or control individuals. Blind rockfish showed homing from both inside and outside their habitat. The time

taken by blind fish to reach their home habitat was not significantly different from that of the control fish. In contrast, most

olfactory-ablated fish did not successfully reach their original habitat. Our results indicate that black rockfish predominantly use

the olfactory sense in their homing behaviour.

D 2005 Elsevier B.V. All rights reserved.

Keywords: Biotelemetry; Black rockfish; Homing; Olfaction; Vision

0022-0981/$ - see front matter D 2005 Elsevier B.V. All rights reserved.

doi:10.1016/j.jembe.2005.02.010

T Corresponding author. Tel: +81 75 753 3137; fax: +81 75 753

3133.

E-mail address: mitamura@bre.soc.i.kyoto-u.ac.jp

(H. Mitamura).

1. Introduction

Some marine fish have homing ability and a strong

fidelity to their habitats and spawning sites. Salmonids

return to their natal rivers to spawn (Hasler and Scholz,

1983; Dittman and Quinn, 1996). The olfactory system

y and Ecology xx (2005) xxx–xxx

JEMBE-47672; No of Pages 12

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H. Mitamura et al. / J. Exp. Mar. Biol. Ecol. xx (2005) xxx–xxx2

of salmon is necessary for home-stream detection, and

salmon are also very sensitive to the odours that

emanate from conspecific fish (Doving and Stabell,

2003). Among demersal fish, the homing of the

Atlantic cod to its spawning grounds is well known

(Green and Wroblewski, 2000; Rawson and Rose,

2000; Robichaud and Rose, 2001). Individual cod

range widely but each year return over some hundreds

of kilometres to their specific spawning grounds. Plaice

also migrate between feeding and spawning grounds,

and selective tidal-stream transport is a key factor in

their migratory mechanism (Metcalfe et al., 1990,

1993; Arnold and Metcalfe, 1996). Attempts to explain

homing orientation have evoked a great variety of

proposals regarding the sensory mechanisms involved.

However, the long-distance migrations of fish make it

difficult to observe homing behaviours in the sea.

It has been recognized since the 1970s that many

rockfish of the genus Sebastes also exhibit homing

ability and a strong fidelity to their habitats if displaced

(Carlson and Haight, 1972; Larson, 1980; Love, 1980;

Matthews, 1990; Pearcy, 1992; Starr et al., 2000, 2002;

Love et al., 2002). For example, the black rockfish

Sebastes inermis exhibits fidelity to its habitat

(Numachi, 1971; Shinomiya and Ezaki, 1991) and

can return to its origin after displacement of 1–4 km for

some days (Mitamura et al., 2002). The genus Sebastes

includes about 100 species (Jordan et al., 1930;

Kendall, 1991; Love et al., 2002), and all of them

may display homing ability and strong fidelity to their

habitats (Matthews, 1990; Love et al., 2002). More-

over, the sensory mechanisms they use in returning to

their habitats seem to be common to rockfish of the

genus Sebastes (Matthews, 1990). However, while

previous research focused on the homing patterns,

activity patterns, and habitat preferences of these fish,

no studies have been undertaken to determine how the

rockfish finds its habitat (Love et al., 2002).

The black rockfish grows relatively slowly, is long-

lived (Harada, 1962; Hatanaka and Iizuka, 1962;

Yokogawa and Iguchi, 1992; Utagawa and Taniuchi,

1999) and is a typical site-specific fish. Generally,

compared with mobile pelagic fish, site-specific fish

are more likely to learn landmarks because they

inhabit areas with distinctive features, such as are

found in rocky habitats (Dodson, 1988; Reese, 1989).

This suggests that the rockfish, including the black

rockfish, may use visual cues such as landmarks or

topographic features when homing (Matthews, 1990;

Mitamura et al., 2002; Love et al., 2002).

Some reports have suggested that the olfactory

sense is also used as a navigational cue in rockfish

homing (Matthews, 1990; Mitamura et al., 2002).

Many rockfish have a relatively small home range

(Love et al., 2002). However, long-distance homing

from as far away as 22.5 km has been reported

(Carlson and Haight, 1972), suggesting that rockfish

home from outside their habitats. In other displace-

ment experiments, rockfish initiated their homing

journey with small random movements around the

release site, and then moved into a fixed direction

towards their home (Matthews, 1990; Mitamura et al.,

2002). This fact also suggests that rockfish can start

the homeward journey from outside their home range

in which familiar visual landmarks would occur.

The objective of this study was to detect the primal

cue for homing in displaced black rockfish. We

focused on visual cues and olfactory cues, and

conducted experiments with both vision-blocked and

olfactory-ablated fish.

2. Methods

2.1. Tagging with coded ultrasonic transmitters

All fish (Table 1) used in the visual-cue and

olfactory-cue experiments were over 150 mm in total

length and were considered to be mature (Mio, 1960;

Yokogawa et al., 1992). We used ultrasonic coded

transmitters (V8SC-6L; Vemco Ltd., Nova Scotia,

Canada) that are 8.5 mm in diameter, 25 mm long, and

weigh 2.2 g in water. The transmitter was implanted

surgically into the peritoneal cavity of the fish in

accordance with the Japan Ethological Society guide-

lines for the experimental use of animals. Surgical

treatments were carried out under anaesthesia induced

with 0.1% 2-phenoxyethanol. The implant operation

took approximately 5 min. The fish was placed

between rubber sponges in a bath of fresh bubbling

seawater throughout the operation. An incision about

10 mm in length was made in the abdomen of the fish

and the transmitter was inserted. The wound was

closed with an operating needle and sutures. The

antibiotics oxytetracycline hydrochloride and poly-

mixin B sulfate were applied. The fish were held in a

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Table 1

Summary of treatment, total length, date monitoring began, date monitoring finished, homing duration, and time of day when homing, type of

homing performance, capture point, release point, and site of final destination of the tagged fish

ID Treatment Total

length

(mm)

Date

monitoring

began

Date

monitoring

finished

Homing duration

(days) and time of

day when homing

Type of

homing

performance

Captured

point

Release

point

Site of

final

destination

B01 Black 230 05-Apr-01 09-Apr-01 1, Dusk 3a X Y X

B02 Black 230 05-Apr-01 09-Apr-01 1, Dusk 3a X Y X

B03 Black 215 05-Apr-01 09-Apr-01 1, Dusk 3a X Y X

T01 Transparent 220 05-Apr-01 09-Apr-01 1, Dusk 3a X Y X

T02 Transparent 190 05-Apr-01 09-Apr-01 N N X Y Other

T03 Transparent 220 05-Apr-01 09-Apr-01 2, Dawn 3a X Y X

B04 Black 247 14-May-01 22-May-01 1, Daytime 3b X Z X

B05 Black 215 14-May-01 22-May-01 1, Daytime 3b X Z X

B06 Black 202 14-May-01 22-May-01 N N X Z Other

B07 Black 255 14-May-01 22-May-01 1, Daytime 3b X Z X

T04 Transparent 220 14-May-01 22-May-01 1, Daytime 3b X Z X

T05 Transparent 250 14-May-01 22-May-01 1, Midnight 3b X Z X

T06 Transparent 230 14-May-01 22-May-01 1, Midnight 3b X Z X

T07 Transparent 235 14-May-01 22-May-01 1, Dusk 3b X Z X

I01 Intact 240 16-Nov-01 28-Nov-01 1, Midnight 4a B A B

I02 Intact 225 16-Nov-01 28-Nov-01 7, Midnight 4a B A B

I03 Intact 215 16-Nov-01 28-Nov-01 1, Dawn 4a A B A

I04 Intact 240 16-Nov-01 28-Nov-01 3, Midnight 4a A B A

OA01 Olfactory ablation 245 16-Nov-01 28-Nov-01 N 4b B A Other

OA02 Olfactory ablation 180 16-Nov-01 28-Nov-01 5, Midnight 4d A B A

OA03 Olfactory ablation 210 16-Nov-01 28-Nov-01 N 4c A B Oil-tanker berth

OA04 Olfactory ablation 240 16-Nov-01 28-Nov-01 N 4c B A Oil-tanker berth

OA05 Olfactory ablation 215 16-Nov-01 28-Nov-01 5, Midnight 4d A B A

OA06 Olfactory ablation 225 16-Nov-01 28-Nov-01 N 4c B A Oil-tanker berth

The dashed line on the table separates the visual-cue and olfactory-cue experiments. The identity designations B02 and T06, B03 and B05, and

T01 and T04 specify the same fish. N means no homing. bTime of day when homingQ means the time during the day when the fish homed:

daytime, 9:00–17:00; dusk, 17:00–21:00; midnight, 21:00–5:00; dawn, 5:00–9:00. bType of homing performanceQ means the typical homing

path described in Figs. 3 and 4. X, Y, Z, A, B, and oil-tanker berth are the sites shown in Figs. 1 and 2. Other means other sites. bSite of finaldestinationQ means the place the fish was located at the end of the experiment.

H. Mitamura et al. / J. Exp. Mar. Biol. Ecol. xx (2005) xxx–xxx 3

circular plastic experimental tank (1 m3 in volume) for

about two days to allow them to recover from surgery.

Sufficient fresh bubbling seawater was exchanged. No

effects of surgery on the behaviour of the fish were

observed. Preliminary experiments using dummy

transmitters demonstrated that intraperitoneal implan-

tation had no discernible effects on feeding or

swimming behaviour over a period of about a month.

2.2. Tracking and monitoring systems

Three types of systems (five VR1, 10 VR2, and

one VR28 systems [Vemco Ltd.]) were used to track

and monitor tagged fish. The tracking system on the

research vessel (VR28 system) had four hydrophones

that detected fish direction. Signals from the coded

transmitters were received through a four-channel

receiver by the hydrophone system, and the receiver

was connected to a personal computer. The relative

receiving strengths from the four hydrophones were

used to determine the direction of an individual fish.

The ID number of the coded transmitter and the

position of the vessel established from GPS (Garmin

Ltd., Olathe, KS, USA) were recorded. Garmin GPS

receivers are accurate to within 15 m on average. The

position of a fish was recorded when the receivers

detected signals from that fish (when the tagged fish

was within about 20 m of the receivers).

The monitoring system for the fixed receivers

(VR1 and VR2 systems) was 60 mm in diameter and

340 mm long and logged data on the presence of fish

tagged with a coded transmitter. The system had a

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H. Mitamura et al. / J. Exp. Mar. Biol. Ecol. xx (2005) xxx–xxx4

flash memory to record data and was powered by a

lithium battery that lasts for up to 180 days. The

receiver was installed at mid-water depth between the

release point and their original habitat. The ID

number, date, and time were recorded when a tagged

fish passed within 300–500 m of the receiver. We

installed five fixed monitoring receivers in Maizuru

Bay in the visual-blocked experiments, and 10 fixed

monitoring receivers around the Kansai International

Airport (KIX) island in the olfactory-ablation experi-

ment. In both experiments, the areas between the

release points and the capture sites were monitored by

these monitoring systems (Figs. 1 and 2).

Fig. 1. The study site, fish capture and release sites, and receiver locations i

cue experiment 1; (b) study site of visual-cue experiment 2. Dashed circles

transmitters.

2.3. Visual-cue experiments

The experiments on visual cues were conducted at

Maizuru Bay (Fig. 1). It is about 5–20 m deep, and

the coastline is complex and often rocky. Eleven

black rockfish were collected by angling or in fish

traps within a radius of about 10 m of point X (Fig.

1). Whereas two fish (ID B01 and T03) were captured

about five months before release, the remaining nine

fish were captured just before their release due to the

difficulty in collecting more than several black

rockfish at one time in this study site. All fish

sampled were kept in tanks before experimental

n the visual-cue experiments in Maizuru Bay. (a) Study site of visual-

represent the expected signal detection ranges of the coded ultrasonic

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Vertical seawall

Gently sloping seawall

Nursery area

Capture and release point

N

1 km

KIX

Tanker berth

1

2

3

4

5

10

6

78

9

B

A

Tidal current direction

Fig. 2. The study site, fish capture and release points, and receiver location of the olfactory-cue experiment in Osaka Bay. Ten automated

receiver systems were set up to cover the entire seawall of Kansai International Airport. Dashed circles represent the expected signal detection

ranges of the coded ultrasonic transmitters.

H. Mitamura et al. / J. Exp. Mar. Biol. Ecol. xx (2005) xxx–xxx 5

release. To eliminate vision, we attached a mask of

black polyvinyl chloride over the eyes using the

method of Lohmann et al. (1995) and Larisa and

Lohmann (2003). This eliminated any impact on the

fish’s breathing. Transparent polyvinyl chloride was

used on the control fish. Preliminary laboratory

experiments indicated that the mask lasted for

approximately one week. Two fish that had been

kept for 5 months were divided among the blind and

the control fish to remove the bias of data from their

long-term captivity.

In the first release experiment, three vision-blocked

fish and three with transparent masks, were released

on 5 April 2001 at point Y, about 1000 m east of the

capture point and in water about 12 m deep (Fig. 1).

Four fish (B02, B03, T01, and T03) were recaptured

within 20 days in fish traps installed at the capture

site. In the second experiment, four vision-blocked

fish and four with transparent masks, including fish

B02, B03, and T01 recaptured in the first experiment

(Table 1), were released on 14 May 2001 at point Z,

about 150 m west of the capture point and in water

about 7 m deep (Fig. 1). Using a research vessel, we

tracked the fish continuously for about 8 h immedi-

ately after release and for about 3 h on the following

day. Tracking was conducted primarily around the

capture and release points. We also monitored tagged

fish using five monitoring receivers over five and nine

days after release around the capture and release

points, respectively.

2.4. Olfactory-cue experiment

In Maizuru Bay, three individual fish were used in

multiple experiments because it was difficult to collect

several fish in a short period. Therefore, we moved the

study site for the subsequent experiment to KIX (Fig.

2). Commercial fishing has been prohibited in the

KIX island area, where black rockfish are sufficiently

abundant for our study. The sea around the KIX island

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H. Mitamura et al. / J. Exp. Mar. Biol. Ecol. xx (2005) xxx–xxx6

is 18 m deep and the sea floor is extremely soft. Most

of the seawall (8.7 km) around the KIX island is in the

form of a gently sloping rubble mound. The mound is

covered by many kinds of seaweed and is used as a

spawning and nursery area for marine animals. Ten

black rockfish were collected within a radius of about

100 m from points A and B near the eastern seawall of

the KIX island (Fig. 2). All fish sampled were kept for

about four or five days in tanks before experimental

release.

To eliminate olfaction, we plugged the olfactory

pits of the rockfish with petroleum jelly, using the

method of Wisby and Hasler (1954), Hasler and

Scholz (1983), and Yano and Nakamura (1992). We

kept 10 black rockfish with petroleum jelly in their

nares in a tank to determine how long the petroleum

jelly remained in place.

All control and olfactory-ablated fish were released

approximately 2 km from the capture point on 16

November 2001. We monitored the tagged fish for 13

days after release using the 10 fixed monitoring

receivers.

2.5. Statistical analysis

The times taken to reach home were compared

between the fish with black masks and those with

transparent masks in the visual-cue experiments using

a t-test after data standardization using square-root

transformation (Zar, 1996). The Mann–Whitney U-

test was used to compare the homing times of intact

and olfactory-ablated fish in the olfactory-cue experi-

ment. In order to compare these homing times, the

reciprocals of the times were used. The Kruskal–

Wallis test was used to compare the total body lengths

and weights of fish between groups at the two capture

points and the oil-tanker berth (Fig. 2).

3. Results

3.1. Visual-cue experiments

In both visual-cue experiments, six of the seven

blind fish and six of the seven control fish returned to

the capture site. Among the 12 fish that homed, eight

returned to the capture site under low light conditions

between dusk and dawn (Table 1).

In vision-blocked experiment 1, all blind fish and

two of three control fish returned to the capture site

between dusk and dawn within two days (Table 1).

The time taken for the blind fish to home was not

significantly different from that of the control fish (t-

test: Nblind=3, mean: 0.71 min�1, upper and lower

limit confidence: 0.71 min�1, Ncontrol =3, mean: 0.71

min�1, upper and lower limit confidence: 0.71 min�1,

P N0.05). The homing paths taken by the blind fish

were almost the same as the paths taken by the control

fish (Fig. 3a). Once the tagged fish had returned to

their original site, they were not tracked or monitored

around the release point until the end of the experi-

ment (Fig. 3a). The control fish (T02) that failed to

home moved in a direction away from the capture site,

and could not be tracked or monitored to determine its

ultimate fate. This fish was the smallest in the

experiment. Fish B01 and T03, which had been kept

in a tank for about five months before release,

returned to the capture site.

In vision-blocked experiment 2, three of the four

blind fish and all the control fish returned to the

capture site within one day (Table 1). The time taken

by the blind fish to home was not significantly

different from that taken by the control fish (t-test:

Nblind=4, mean: 0.71 min�1, upper and lower limit

confidence: 0.70 and 0.72 min�1 Ncontrol=4, mean:

0.71 min�1, upper and lower limit confidence: 0.70

and 0.72 min�1, P N0.05). The homing paths taken by

the blind fish were almost the same as the paths taken

by the control fish (Fig. 3b). In contrast to vision-

blocked experiment 1, the tagged fish that homed

were tracked and monitored near the release point

after homing (Fig. 3b). The blind fish (B06) that failed

to home returned to the capture site at dusk and

subsequently moved from the capture site to the point

designated point A in Fig. 1. It did not return to the

capture site. This fish was the smallest fish in the

experiment. Fish B07, which had been kept in a tank

for about five months before release, returned to the

capture site.

3.2. Olfactory-cue experiment

The laboratory experiment showed that the petro-

leum jelly remained in their nares for 5–10 days.

Plugging with petroleum jelly had no significant

effect on feeding or swimming behaviour.

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a) Exp. 1

b) Exp. 2

Control fish

Blind fish

Blind fish

Control fish

7-Apr. 9-Apr.

7-Apr. 9-Apr.

-May 16-May 18-May 20-May 22-May 24-May

-May 16-May 18-May 20-May 22-May 24-May

Rec

eive

r lo

cati

on

Rel

ease

sit

eO

rigi

nal s

iteR

elea

se s

ite

Ori

gina

l site

Rel

ease

sit

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rigi

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iteR

elea

se s

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Ori

gina

l site

5

4

3

2

15-Apr.

5-Apr.

5

4

3

2

1

4

3

2

114

14

4

3

2

1

Rec

eive

r lo

catio

n

Fig. 3. Typical homing paths of tagged black rockfish in the visual-cue experiments. (a) Shows the results of visual-cue experiment 1 and (b)

those of visual-cue experiment 2. The dashed line on the graph separates visual-cue experiments 1 and 2.

H. Mitamura et al. / J. Exp. Mar. Biol. Ecol. xx (2005) xxx–xxx 7

All control fish returned to their capture sites

almost directly under low light conditions between

dusk and midnight within seven days (Table 1, Fig.

4a). Four of the six experimental fish did not return

to the capture site. One of them moved in the

opposite direction to the capture site and could not

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9

8

7

65

2

3

4

1

10

9

8

7

6

5

2

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4

1

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9

8

7

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10

16-Nov. 19-Nov. 22-Nov. 25-Nov. 28-Nov.

16-Nov. 19-Nov. 22-Nov. 25-Nov. 28-Nov.

16-Nov. 19-Nov. 22-Nov. 25-Nov. 28-Nov.

16-Nov. 19-Nov. 22-Nov. 25-Nov. 28-Nov.

a) Intact fishDirectly homing.

b) Olfactory Ablation fish.No homing.

c) Olfactory ablation fish.Staying at another site.

d) Olfactory ablation fishStraying and then homing after loss of ablation jelly.

Rel

ease

sit

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Rec

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Fig. 4. (a) Shows the typical homing path of an intact fish in the olfactory-ablation experiment. (b–d) Show the typical movements of three

experimental fish with olfactory ablation.

H. Mitamura et al. / J. Exp. Mar. Biol. Ecol. xx (2005) xxx–xxx8

be tracked or monitored (Fig. 4b). The other three

moved back and forth along the seawall and

ultimately stayed in the area of stations 5 and 6

(Fig. 4c). Stations 5 and 6 were located around an

oil-tanker berth built on many piles. The piles

provide numerous species with a feeding ground

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H. Mitamura et al. / J. Exp. Mar. Biol. Ecol. xx (2005) xxx–xxx 9

and living space. The black rockfish around the oil-

tanker berth (Mitamura et al., 2002) were signifi-

cantly larger in body size and weight than those

found around points A and B (Kruskal–Wallis test:

H =7.050, df =2, P b0.05) (Fig. 2). These three

experimental fish remained in this high-quality

habitat. The other two experimental fish homed.

They stayed mainly around the oil-tanker berth after

release (Fig. 4d). They then moved back and forth

between the capture and release points along the

seawall and finally homed at midnight five days

after release (Fig. 4d). Because the petroleum jelly

would have remained in their nares for 5–10 days,

they appeared to home after the time at which the

petroleum jelly would be lost from their nares.

Therefore, the time taken by the experimental fish

to home was significantly longer than that taken by

the intact fish (Mann–Whitney U-test: Nintact =4,

Nolfactory ablation=6, P b0.05).

4. Discussion

4.1. Homing mechanism

Our results indicate that the black rockfish

primarily uses olfaction to return to its home habitat,

and does not appear to use visual cues for homing.

In both vision-blocked experiments, the homing

durations of the control fish were slightly longer

than those of the blind fish although there was

statistically no difference between them (Table 1).

This reinforces the results that the rockfish does not

appear to use visual cue for homing although the low

sample size might mask the effect of vision-blocked

treatment. Researchers have thought that rockfish,

including the black rockfish, use visual cues for

homing because displaced rockfish were found on or

near reefs and rocky areas on their return routes

(Matthews, 1990; Love et al., 2002; Mitamura et al.,

2002). The use of landmarks for homing requires a

familiar landmark around the release site, one which

the animals have previously used to move to their

destination (Fred, 1998). In vision-blocked experi-

ment 2, the tagged fish were tracked and monitored

after they returned to their original site around the

release point until the end of the experiment (Fig.

3b). These results imply that the release points in

this experiment were inside the home range of these

fish. However, our results show that the time taken

and the homing paths did not differ between the

blind fish and control fish. This suggests that the

black rockfish might not use vision for homing

inside its home range.

Homing from outside the familiar site was also

examined. In both the olfactory-ablation experiment

and vision-blocked experiment 1, the release point

was outside the home range because the tagged fish

that homed were not tracked and monitored near the

release point after homing (Figs. 3a and 4a). Although

black rockfish can home using landmarks from

outside the home range if they use the area map

developed while searching for a suitable habitat when

young (Matthews, 1990), our experimental results

show that black rockfish use not vision, but olfactory

cues for homing from outside the home range. There

would be little advantage for black rockfish in

memorizing the geographical features outside the

home range that they learned when young because

there would be little likelihood in daily life of being

displaced outside the home range by strong currents

or tides. Furthermore, in this study, 14 of the 18

homing rockfish returned to their habitats between

dusk and dawn. Clearly, vision is used less under low

light conditions than during the day, which implies a

limitation in the use of vision for homing in black

rockfish. However, the fish displaced to an unfamiliar

area could determine their positions relative to the

home site. This fact suggests that the rockfish in the

unfamiliar area could exploit a stimulus from the

familiar area. Therefore, the black rockfish must use

olfaction as its main navigational cue.

The black rockfish moved at random along

currents just after displacement (Mitamura et al.,

2002). During this period the fish might search for a

similar stimulus to detect the home ward detection,

although the handling and tagging trauma might

prevent the fish from carrying the random move-

ments. Further studies of homing migration, includ-

ing the monitoring of water currents, are needed to

clarify how black rockfish find the right direction

from the olfactory cues. Subsequently, the fish

started to home after recognizing a previously

experienced stimulus. However, it is unclear what

olfactory cues the black rockfish uses for homing.

We can hypothesize three kinds of olfactory cues

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H. Mitamura et al. / J. Exp. Mar. Biol. Ecol. xx (2005) xxx–xxx10

that could be used in homing because black rockfish

do not move over extensive areas of habitat but form

schools at one location (Harada, 1962). The first

possibility is an olfactory-cue characteristic of the

habitat. The black rockfish might home using a

characteristic habitat olfaction similar to that of the

salmonids (Doving et al., 1985; Kitahashi et al.,

2000; Tanaka et al., 2000). The second possibility is

an olfactory cue from substances, for example urine,

used as individual markers. The third possibility is

an olfactory cue provided by conspecifics inhabiting

the same home range (Sweatman, 1988; Polking-

horne et al., 2001).

It is evident that black rockfish in rocky areas

primarily use olfaction to home, as do salmon in open

waters, although other site-specific fish often use

vision to orient themselves (Doving and Stabell, 2003;

Dodson, 1988; Reese, 1989). The black rockfish is

nocturnal and does not live in very clear waters.

Therefore, it may have developed olfactory cues

rather than visual cues for orientation because it is

easier to use olfaction than vision during the night

time. However, the question bWhat is the olfactory

cue for home?Q remains to be answered. Some recent

reports showed that the nose of another homing fish,

the rainbow trout Oncorhynchus mykiss, may also

detect the Earth’s magnetic field (Walker et al., 1997;

Diebel et al., 2000). The possibility that the black

rockfish uses magnetic fields as well as olfaction in

their homing mechanism might not be discounted.

4.2. Advantages of homing and habitat fidelity

The black rockfish congregates at specific places

and territories, especially males during the repro-

ductive season (Harada, 1962; Shinomiya and

Ezaki, 1991). Moreover, the rockfish copulates in

its habitat (Shinomiya and Ezaki, 1991). These facts

suggest that homing ability and habitat fidelity may

optimize their chances of acquiring future breeding

partners and facilitates higher reproductive success

than could be achieved by drifting among likely

habitats. In our olfactory-cue experiment, mature

black rockfish without ablation returned home

through the habitat of the tanker berth, which is

potentially a better habitat than their original

habitat. These results indicate that once black

rockfish have succeeded in reproducing in a habitat,

they may prefer the known environmental condi-

tions to those that are unknown. In contrast, half the

mature olfaction-ablated rockfish did not find the

homeward direction and stayed at the potentially

better habitat rather than their original home. This

indicates that they selected the new area where a

higher reproductive success could be achieved than

other areas.

In each visual-block experiment, the smallest fish

did not return home. Immature rockfish do not seem

to have homing ability (Carlson and Haight, 1972).

During the reproductive season, small male black

rockfish establish smaller and more peripheral

territories than those of larger males and have

minimal opportunities for courtship because they

are occasionally chased and butted by larger terri-

torial males (Shinomiya and Ezaki, 1991). These

facts indicate that the advantages of homing and

location fidelity may be greater for experienced

mature adults than for immature fish that are unlikely

to achieve reproductive success in their existing

habitats. There may be a reproductive advantage in

young rockfish not returning home but colonizing

new habitat where they have a better chance of

growing to maturity.

Acknowledgements

This study required the help of many people. We

thank M. Ueno and R. Masuda, of the Graduate

School of Agriculture, Kyoto University, for their

kind advice and support of the experiment. We thank

T. Maruo, of Fisheries and Environmental Ocean-

ography, Graduate School of Agriculture, Kyoto

University, for his help to fish Mebaru and for his

daily encouragement. We thank Captain K. Sato, who

operated the research vessel. We also thank H. Ueda

of the Field Science Center for the Northern Bio-

sphere, Hokkaido University, for kind comments

about the methods used in this study.[RH]

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