Chem. Senses 28: 293-300,
2003
© Oxford University Press 2003
Does the Lateral Bundle of the Medial Olfactory Tract Mediate Reproductive Behavior in Male Crucian Carp?
Division of General Physiology, Department of Biology, University of Oslo, Oslo, Norway
Correspondence to be sent to: Kjell B. Døving, Division of General Physiology, Department of Biology, PO Box 1051, University of Oslo, 0316 Oslo, Norway. E-mail: kjelld{at}bio.uio.no
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Abstract |
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The olfactory tract in crucian carp (Carassius carassius) is divided into three distinct bundles: the lateral tract (LOT) and the lateral (lMOT) and medial (mMOT) bundles of the medial tract. The LOT has been shown to mediate information associated with feeding behavior, whereas the mMOT mediates information associated with alarm response. The role of the medial olfactory tract (lMOT and mMOT) in reproductive behavior is still under debate. In the present experiment, male reproductive behavior towards prostaglandin-injected females was investigated before and after cutting off the different olfactory tract bundles, to determine which of the tract bundles is essential for mediating reproductive behavior in male crucian carp. The fish were maintained in physiological saline before and after surgery to preserve the remaining tract bundles. Operations were performed symmetrically on both sides and post-operative inspections revealed the functionality of the intact tracts. Sham-operated males and males with only the lMOT intact showed typical reproductive behavior, with following of the female and inspections of the female anal papilla. However, males in which the lMOT was cut, leaving both the mMOT and the LOT intact, showed reduced reproductive behavior. Our results suggest that the lMOT mediates reproductive behavior in male crucian carp.
Key words: fish, olfaction, smell, nerve transection, spawning, pheromones
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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The fish olfactory system mediates different types of behaviors that are essential for various life processes, such as feeding, alarm reaction and reproduction (Døving, 1986
). In gadids, siluroids and cyprinids, the paired olfactory
tract is clearly divided into three distinct bundles
(Sheldon, 1912). These are
designated as the lateral olfactory tract (LOT), the lateral bundle of the
medial olfactory tract (lMOT) and the medial bundle of the medial olfactory
tract (mMOT). The different tract bundles contain fibers that originate from
different portions of the olfactory bulbs
(Dubois-Dauphin et al.,
1980; Satou et al.,
1983; Satou,
1990). Also, each bundle connects to different brain areas,
although some overlap between bundles seem to exist
(Finger, 1975;
Rooney et al., 1992).
Moreover, the different bundles contain fibers with different
electrophysiological and histological properties
(Døving and Gemne,
1965).
These specific morphological and electrophysiological properties strongly
suggest that the individual bundles also have specific functional properties
and that activity in each individual bundle mediates information about a
specific behavior. Døving and Selset
(Døving and Selset,
1980) first provided evidence that a particular tract bundle
mediates a particular behavioral response. Electrical stimulation of discrete
tract bundles in free-swimming Atlantic cod (Gadus morhua) showed
that the LOT mediates feeding behavior, the lMOT mediates spawning behavior
and the mMOT mediates alarm behavior. Further evidence for a functional
separation of the olfactory tract bundles has been reported in several
behavioral and physiological studies. Goldfish (Carassius auratus)
lost their ability to discriminate between different amino acids after
transection of the LOT (von Rekowski and
Zippel, 1993) and the LOT mediates feeding responses in crucian
carp, Carassius carassius
(Hamdani et al.,
2001). Alarm behavior was absent in crucian carp after transection
of the mMOT (Hamdani et al.,
2000). The MOTs (bundle not specified) are necessary for mediation
of reproductive behavior in male goldfish
(Stacey and Kyle, 1983;
Kyle et al., 1987).
Moreover, known sex pheromones selectively elicited electrical activity in the
MOTs of male goldfish (Sorensen et
al., 1991), whereas goldfish sperm release was induced by
electrical stimulation of the MOTs (Demski
and Dulka, 1984). However, the particular bundle of the MOT
responsible for mediating reproductive behavior has never been differentiated
in an experimental situation involving male and female conspecifics.
Goldfish, crucian carp and common carp (Cyprinus carpio) are the
most extensively studied fish species with regard to the role of olfactory
signals in reproduction. When approaching ovulation, female goldfish release a
mixture of steroid-hormone-derived sex pheromones through the urine, eliciting
reproductive behavior in spermiating males
(Stacey and Sorensen, 1986;
Scott and Sorensen, 1994;
Sorensen et al.,
1995,
1996).
17
,20ß-Dihydroxy-4-pregnen-3-one (DHP) is released preovulatory,
while prostaglandin F2
(PGF2) is released after ovulation, both
pheromones exerting primer and releaser effects. The males respond to DHP
through elevated plasma concentrations of luteinizing hormone, leading to
spermiation and increased sperm volume, the primer effect
(Dulka et al., 1987),
but DHP also stimulates male reproductive behavior, the releaser effect
(DeFraipont and Sorensen, 1993;
Poling et al., 2001).
PGF2 stimulates male reproductive behavior,
including active chasing and nudging of the female (Sorensen et al.,
1988,
1996;
Bjerselius and Olsen, 1993;
Stacey et al., 1994),
but also stimulates male release of luteinizing hormone
(Sorensen et al.,
1989), although through different mechanisms than those mediating
the DHP effect (Zheng and Stacey,
1996,
1997). In behavioral studies,
injections in immature females of PGF2 are often
used. This will induce release of sex pheromones and reproductive behavior in
males and females within minutes
(Partridge et al.,
1976; Stacey,
1981).
The aim of the present study was to investigate which of the olfactory
tract bundles is responsible for mediating reproductive behavior in male
crucian carp. This was investigated by observing the behavior of spermiating
males that had undergone different types of olfactory tract transections
towards PGF2-injected females. In view of
previous results (Døving and Selset,
1980; Hamdani et al.,
2000,
2001), we decided to focus our
investigation on the role of lMOT in crucian carp reproductive behavior.
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Materials and methods |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Experimental animals
Crucian carp (both juveniles and sexually maturing individuals) were caught in a small lake outside of Oslo, Norway (60° N), in June 2002. The fish were transported to the Department of Biology and kept in 700 l fiberglass stock tanks without vegetation. The temperature of the running water was constant between 7 and 9°C, while the photoperiod was maintained at 12 h/12 h light/dark. The fish in the stock tanks were fed once a day on Tetrapond® pond sticks (Tetra GmbH, Germany). The fish were sorted on the basis of sex and kept in separate tanks from the time when spermiating males were first observed (no sexual dimorphism was observed). The fish used in experimental trials had the following body measurements: male (spermiating) body wt was 24.6 ± 1.3 g (mean ± SEM; n = 23) and male gonadosomatic index—GSI = [100 x (gonad wt/body wt)]—was 2.8 ± 0.2. The female (vitellogenic, used as spawning partners) body wt was 42.4 ± 2.2 g (n = 16), while the female GSI was 13.8 ± 0.5.
Experimental design
The reproductive behavior trials were conducted in six 40 l aquaria
containing still, aerated physiological saline (in g/l: NaCl, 8.53; KCl, 0.22;
MgSO4·7H2O, 0.25;
CaCl2·6H2O, 0.28) at 21°C. All aquaria
contained artificial gravel and floating `vegetation' made of green yarn
attached with rubber bands to floating corks. This artificial spawning
substrate covered 
30% of the water surface. All behavioral trials
involved the use of one male (with running milt, tested only once) and one
PGF2-injected vitellogenic female. On day 1,
males were acclimatized to the physiological saline by transferring them from
the stock tank to individual experimental aquaria. At the time of transfer,
the water temperature in the experimental aquaria was identical to the stock
tank temperature. The following day (day 2), when the physiological saline had
reached room temperature (21°C), one
PGF2-injected female was introduced to each
individual male and the behavior was observed and video-recorded for 10 min.
If the male showed more than four short followings (Fs) or short followings
directed against the female anal papilla (FsG; see below), the male was
considered sexually active and used in the trials. Males that failed the test
were excluded from the experiment. The video-recorded behavior performed by
the males that passed the test was further analyzed and the frequency of
reproduction-related behaviors (see below) was used as a pre-operative index
of reproductive behavior (pre-operation). These sexually active males
thereafter underwent bilateral transection of one or more of the olfactory
tracts according to the procedure given below. Earlier studies have shown that
the LOT mediates feeding responses
(Hamdani et al.,
2001), while the mMOT mediates alarm behavior
(Hamdani et al.,
2000) in crucian carp. In view of this and also other results
(Døving and Selset,
1980), which indicated that reproductive behavior is mediated
through the lMOT, we decided to investigate the reproductive behavior in three
groups of crucian carp: (i) sham-operated males; (ii) males with the LOT and
the mMOT transected, named `lMOT intact'; and (iii) males with the lMOT
transected, but the LOT and the mMOT intact, named `lMOT cut'. The operated
males were returned to their aquaria directly after surgery and allowed to
recover overnight. The following morning, a new
PGF2-injected female was introduced to each male
and the behavior was video-recorded for 10 min and further analyzed. The
frequency of reproduction-related behavior was used as a post-operative index
of reproductive behavior (post-operation).
Females were injected i.m. on both sides of the dorsal muscles 15 min
before the start of the trial with 200 µl PGF2
(0.5 µg PGF2/g body wt;
www.sigmaaldrich.com)
dissolved in 0.9% NaCl. This induces spawning behavior for at least 1 h
post-injection (Stacey, 1981;
Bjerselius and Olsen, 1993).
Following PGF2-injection, each female was used
for three consecutive trials with three different males from different
treatment groups. The order of males was randomized. After the trials, the
males were decapitated for determination of body wt, sex and GSI. Experimental
trials were conducted from the middle of June to early September, between
09.00 and 14.00 h. All experiments were conducted in accordance with the
Norwegian Animal Welfare Act as approved by the Norwegian Animal Research
Authority.
Surgical procedure
After the pre-operation behavior trial, sexually active males were
transferred from the observation aquaria, anesthetized with benzocaine (45
mg/l;
www.sigmaaldrich.com),
placed in a stand with running water with anesthetic through the mouth and
over the gills and operated on under a stereo-microscope. The skin was removed
from a 0.7 cm2 area on the skull just posterior from the eyes and
the underlying dorsal cranium was removed. Cranial fluid was removed using
filter paper, while the mesenchymal tissue in the brain case and the meninges
around the olfactory tracts were removed with fine forceps. The olfactory
tracts were clearly visible as three distinct bundles running from the
olfactory bulb to the brain (Figure
1). The bundles were gently separated with a needle and specific
bilateral bundle transections were made using fine scissors, taking care not
to disrupt the blood vessels running parallel with the tract bundles.
Approximately 2 mm of the transected bundles was removed to prevent
regeneration (von Rekowski and Zippel,
1993; Zippel et al.,
1993). The males were divided into three treatment groups, as
follows.
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- Eight males were sham-operated, i.e. the brain case was opened and the
meninges and mesenchymal tissue were removed to expose the olfactory tracts
(sham).
- In six males, the lMOTs were left intact, while the LOTs and the mMOTs were
transected (lMOT intact).
- In nine males, the LOTs and the mMOTs were left intact, while the lMOTs
were transected (lMOT cut).
After surgery, the cranial cavity was filled with 2% agar dissolved in physiological saline to reduce infection. Thereafter, the males were returned to their observation aquaria. At the end of the experiment, each fish was visually inspected for possible regeneration of the tract bundles and for proper blood flow in the vessels along the tracts.
Behavioral analysis
All behavioral experiments were conducted with one spermiating male and one
PGF2-injected female at a time. The
video-recorded male–female interactions were analyzed blind for the
following behaviors, modified from earlier studies
(Partridge et al.,
1976; Bjerselius et
al., 2001):
- Short following (Fs): the male follows the female with its head in close
vicinity of the tail of the female for a period of <5 s. The frequency of
the behavior was recorded.
- Short following gut (FsG): the male follows the female with its head in
close vicinity of the female anal papilla for a period of <5 s. The
frequency of the behavior was recorded.
- Pushing (Pu): the male pushes the female with the side of his head. A
pushing male makes a horizontal movement with its head so that the operculum
hits the side or the head of the female. The frequency of the behavior was
recorded.
- Biting/nipping (BN): the male bites or nips the female. The frequency of
the behavior was recorded.
- Spawning: the male and the female swim together towards the vegetation.
They turn to the side and swim in parallel while they release gametes. We did
not observe behaviors in the present experiments that could be related to
spawning.
- Picking (Pi): the number of bites directed toward the gravel substrate.
This behavior was included because it has been used to describe reduced
spontaneous feeding activity in sexually aroused males.
To verify that the observed behavior variants were male–female specific, we also observed male–male behavior in the observation aquarium (n = 5). The male–male trials were conducted as for the male–female trials, with one male being acclimated in its aquarium for 24 h and the second male added on day 2.
Data analysis
Data were analyzed using Statistica version 5.1 (Statsoft Inc., Tulsa, OK) and presented as mean values ± SEM. Possible effects of olfactory tract bundle transections on male reproductive behavior were tested using a repeated-measurement analysis of variance (ANOVA), followed by the Tukey HSD post hoc test for unequal sample sizes (Spjotvoll and Stoline test).
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Results |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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The reproductive behavior of spermiating male crucian carp towards PGF2
-injected females was observed before and
after bilateral transection of the different olfactory tract bundles
(Table 1). The following
behavior patterns were observed: Fs, the male made repeated short followings
after the female; FsG, the male made repeated short followings directed
towards the female anal papilla; Pu, the male pushed the female with its head;
and BN, the male bit or nipped on the female body. Occasional picking at the
gravel or at the floating vegetation was also observed. There was no
significant difference between the treatment groups (sham; lMOT intact; lMOT
cut) in the observed behaviors before surgery
(Table 1). However, bilateral
transection of the lMOT significantly affected FsG [F(2,20) = 21;
P = 0.000011] and resulted in a significant decrease in FsG in
post-operated compared to pre-operated males (P = 0.00016;
Figure 2). Furthermore, the
fish with transected lMOT had significantly lower scores of FsG compared to
the other treatment groups: sham pre-operation (P = 0.0053), sham
post-operation (P = 0.00020); lMOT intact pre-operation (P =
0.0029), lMOT intact post-operation (P = 0.00035). We did not observe
significant pre- or post-operative effects between the treatment groups in the
other observed behavior types (Table
1).
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In the male–male behavior trials, two different scenarios were evident. Either the two males remained largely inactive throughout the 10 min observation period, or they displayed aggressive behavior. Two different types of aggressive behavior were evident in the male–male situation: high-speed chasing around the aquarium and also one male blocking the swimming path of the other. None of the male–female-typical behavior patterns were observed between two males.
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Discussion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Extensive experimental evidence indicates that ovulated females in most species of fish, including the crucian carp (Bjerselius and Olsén, 1993
), release pheromone(s) that stimulates reproductive behavior
in male conspecifics. As these pheromones fail to elicit a full response in
males in which olfactory function has been impaired, reproductive behavior
most likely is mediated by the olfactory system
(Liley, 1982). In the present
work, we observed significant differences in reproductive behavior between
males with the lMOT intact and those with the lMOT cut. Although previous
studies have concluded that reproductive behavior is mediated by the MOT
(Stacey and Kyle, 1983), the
present work gives the first direct evidence that only the lateral bundle of
the MOT is necessary for full reproductive behavior in male crucian carp.
Whether this feature is valid for all teleosts remains an open question.
Several earlier investigations have indicated a role for the MOT in teleost
reproductive events. For example, only axons in the MOT project to the
ventromedial telencephalon and the preoptic area in goldfish
(Oka et al., 1982;
von Bartheld et al.,
1984) and Atlantic cod (Rooney
et al., 1992). Electrical stimulation in these brain
areas elicits sperm release in anesthetically immobilized goldfish
(Demski and Hornby, 1982).
Lesions in the same areas impair courtship behavior in male goldfish
(Kyle and Peter, 1982;
Koyama et al., 1984)
(Table 2). Also, electrical
stimulation of the olfactory tracts after transection of one or more of the
tract bundles revealed that the MOT induces sperm release in goldfish
(Demski and Dulka, 1984). Known
sex pheromones specifically elicited electrical activity in the MOT of male
goldfish (Sorensen et al.,
1991). A further specification of the roles of the lateral and
medial bundles of the MOT in reproduction-related activity was impossible or
not attempted in the studies noted above.
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To our knowledge, only Døving and Selset
(Døving and Selset,
1980) have successfully differentiated between the different
bundles of the MOT, as they induced different types of stereotypic behavior in
individual free-swimming Atlantic cod by electrical stimulation of single
tract bundles. Electrical stimulation of the lMOT induced spawning-like
behavior, although the responses to conspecifics were not tested in these
fish.
Stacey and Kyle (Stacey and Kyle,
1983) investigated the effect of olfactory tract transection on
male goldfish reproductive behavior. Although they investigated single tract
bundles, they concluded that transection of the entire MOT reduced
reproductive behavior in male goldfish
(Stacey and Kyle, 1983;
Kyle et al., 1987).
However, a closer look at their results reveals some interesting points:
transection of the lMOT reduced the duration of spawning behavior. However,
the same effect was observed after transection of the mMOT. Moreover,
transection of the mMOT and the LOT reduced the duration of spawning behavior,
an effect not observed when the lMOT and the LOT were transected. These
results led the authors (Stacey and Kyle,
1983) to suggest that both the lMOT and the mMOT were involved in
mediation of spawning behavior, hence their general conclusion that the entire
MOT is necessary for full reproductive activity. The present study
demonstrates that bilateral transection of the male lMOT decreases the
frequency of short following directed to the female anal papillae (FsG) in
crucian carp. Moreover, transection of the mMOT and LOT did not affect any of
the observed reproductive behavior patterns, thus contrasting the earlier
results (Stacey and Kyle,
1983). However, Stacey and Kyle
(Stacey and Kyle, 1983)
measured the total duration (and not the frequency) of spawning behavior and
they did not differentiate between Fs and FsG as in the present study. Such
distinction in analysis might explain the differences in the results between
the studies. In studies on anosmic goldfish
(Partridge et al.,
1976), the authors did not differentiate between Fs and FsG. They
(Partridge et al.,
1976) showed that the anosmic goldfish decreased the time spent
following an ovulating female, but increased the frequency of the same
behavior, as compared to control fish. Other sexual behaviors observed in that
study, including Pu and spawning behavior, showed the opposite relation
between frequency and time spent, further indicating that following the female
is not solely a sexual behavior induced by pheromones.
We did not observe actual spawning behavior in the present study, although
this is frequently seen when experiments on goldfish are made under similar
conditions (Bjerselius et al.,
2001). Also, the frequency of Pu was relatively low (0.6/10 min)
in the present study compared to experiments on goldfish: 5–10/10 min
(Partridge et al.,
1976; Bjerselius et
al., 2001). We can think of two possible explanations. First,
the wild-captured crucian carp do not seem to acclimatize as well to
laboratory conditions (they seem to have a higher activation level, i.e. they
get easily scared) compared to the highly domesticated goldfish, even after
several months in captivity. This may influence their reproductive
expenditure, leading to reduced sexual performance. Secondly, it is possible
that our experimental set-up did not allow the males to perform their whole
repertoire of sexual behavior. However, because we essentially copied the
set-up from earlier work (Bjerselius et
al., 2001), we find this explanation rather unlikely. None
the less, the present study showed that spermiating males with the lMOT cut
had a clear decrease in FsG compared to individuals with the LOT and the mMOT
cut. In both Atlantic cod (Døving
and Selset, 1980) and crucian carp
(Hamdani et al.,
2000), the mMOT mediates alarm reaction. Spawning-like behavior
was induced by electrical stimulation of the lMOT in cod
(Døving and Selset,
1980) and our results are in accordance with that finding. Thus,
the findings presented here and in previous studies suggest that only the
lMOT—and not the entire MOT—is necessary for mediating full
reproductive behavior in crucian carp.
In the present study, not all behavior patterns that are assumed to be
reproduction-related showed reduced frequency in males with the lMOT cut. They
all responded to the female with Fs, Pu, and BN and with frequencies not
significantly different between treatment groups or between pre- and
post-operation trials. Although the olfactory system is required to mediate
full reproductive response, these behavior patterns (Fs, Pu and BN) may also
be mediated by other sensory systems (e.g. the visual and/or tactile), as they
were present with similar frequencies even in males in which the entire
olfactory tract system had been cut (n = 2; data not shown). This is
consistent with earlier results (Partridge
et al., 1976), who found that male goldfish that had been
made anosmic by occlusion of the nares still followed ovulated females about
three times as much as they followed non-ovulated females. Also, while the
female blue gourami (Trichogaster trichopterus) evidently uses the
olfactory system to locate the source of male sex pheromone
(Lee and Ingersoll, 1979),
anosmia has little effect on the spawning success of females that are already
in visual contact with the males (Pollack
et al., 1978). However, our results are in contrast to
those of Bjerselius et al.
(Bjerselius et al.,
2001), who based their analyses of reproductive behavior in male
goldfish on a sexual behavior index that was the sum of the number of Fs, Pu
and spawning attempts within a set time period. Even after adjusting for the
number of spawning attempts observed by Bjerselius et al.
(Bjerselius et al.,
2001), we found no significant differences between treatment
groups or between pre- and post-operated crucian carp males using this index.
The behavior trials described in Bjerselius et al.
(Bjerselius et al.,
2001) were similar to those described in the present study and
included one male and one PGF2-injected female.
It is thus possible that the behavioral patterns on which their index is based
are not mediated solely through the olfactory system, but also through the
visual and/or the tactile systems. Alternatively, although the general
repertoire of behavioral patterns is similar in goldfish and crucian carp,
differences could exist between the species concerning the expression of the
different reproductive behavior patterns.
In conclusion, this study demonstrates that the lMOT mediates odor-induced
reproductive behavior in male crucian carp. Previous studies on crucian carp
have shown that the mMOT mediates alarm reaction
(Hamdani et al.,
2000) and the LOT mediates feeding behavior
(Hamdani et al.,
2001). These ablation experiments indicate that each of the
distinct olfactory tract bundles transmits a unique message to the brain. In
Atlantic cod, electrical stimulation of the olfactory tract bundles induces
different behavior patterns associated with feeding (LOT), reproduction (lMOT)
and alarm (mMOT) (Døving and Selset,
1980). Thus, in two species of teleosts from two different
families, there is accordance between the morphological entities and the
behavioral messages that the olfactory tract bundles mediate. This agreement
between morphology and function supports the idea of `labeled lines' discussed
by Erickson (Erickson, 1963)
and also poses the question of the universality of these findings. Future
studies of `labeled lines' will be aided greatly by new techniques that allow
tracing of the connections that specific sensory neurons make in the brain
(Zou et al., 2001).
One might ask if the association between the morphological entities and the
behavioral messages that the olfactory tract bundles mediate is a general
phenomenon, valid for all teleosts, or if it is a coincidence for these two
species only. Furthermore, there are other behavioral patterns associated with
the olfactory system that have not been associated with a particular bundle of
the olfactory tract, for example homing ability
(Døving and Stabell,
2003). The question of which bundle of the olfactory tract
mediates homing behavior must be raised in forthcoming studies.
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Acknowledgments |
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This work was supported by the Norwegian Research Council.
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Accepted March 20, 2003
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