The olfactory pathway for individual recognition in the American lobster Homarus americanus
Boston University Marine Program, Marine Biological Laboratory, Woods Hole, MA 02543, USA
Author for correspondence (e-mail:
atema{at}bu.edu)
Accepted 19 May 2005
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Summary |
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Key words: lobster, Homarus americanus, Crustacea, aesthetasc, chemoreceptor, pheromone, individual recognition
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Introduction |
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The best understood crustacean model for individual recognition in its
social biological context is H. americanus. In typical first
encounters between size-matched, naïve opponents, lobsters fight and
establish dominance. In subsequent encounters, however, the previous loser
avoids a fight with the previous (known) winner. Yet, this same loser will
fight and can win fights against unknown winners of other fights,
demonstrating that the loser recognizes the individual winner and not
only the dominance status of any winning lobster, as appears to be
the case in some species of crayfish
(Breithaupt and Eger, 2002;
Copp, 1986
;
Gherardi and Daniels, 2003
;
Zulandt Schneider et al.,
2001
). A separation of 12 weeks may be the limit of the
memory of a former opponent; this memory is not affected by multiple social
interactions with other lobsters
(Karavanich and Atema, 1998a
).
Individual recognition allows lobsters to form stable dominance relationships
(Jacobson, 1977
;
Morschauser and Atema, 2003
),
which have consequences for mate selection and reproductive success
(Cowan and Atema, 1990
) and
access to shelter (Atema et al.,
1979
; Atema and Voigt,
1995
), two of the most important aspects of lobster survival.
Lobsters are covered with chemoreceptive setae, many of which are clustered
into at least five different chemoreceptor organs, each specialized for
different functions (Atema and Voigt,
1995; Derby and Atema,
1982
). The thoracic appendages, which include the walking legs and
the maxillipeds, appear in function and neuroanatomy more like vertebrate
taste organs and serve important feeding functions. The cephalic appendages,
including first and second antennae, resemble olfaction organs, as they
monitor the external fluid environment
(Atema, 1977
) and project to
specialized sensory brain areas (Sandeman
et al., 1992
). Physiologically, the cephalic appendages of H.
americanus are both chemoreceptive
(Voigt and Atema, 1992
) and
mechanoreceptive (Miller-Sims and Atema,
2004
). The first antenna, known as the antennule, is composed of a
lateral and a medial flagellum standing on a set of basal segments. The
behavioral functions of the medial flagellum and the second antenna remain
unknown, despite several lesion studies (e.g.
Atema et al., 1999
;
Devine and Atema, 1982
). The
lateral flagellum is considered the organ most specialized for chemosensory
detection and plays a leading role in tracking odor plumes
(Devine and Atema, 1982
) and
individual recognition (Karavanich and
Atema, 1998b
). Lobster memory and individual recognition are
mediated by chemical signals in urine released during a fight
(Karavanich and Atema,
1998b
).
The lateral antennular flagellum uses two separate chemosensory pathways:
aesthetasc and non-aesthetasc. The sensory neuroanatomy of antennular pathways
is best known for spiny lobsters (Schmidt and Ache
1992,
1993
,
1996a
,
b
,
1997
;
Schmidt et al., 1992
). The
aesthetasc sensilla are the most abundant setal type and are located in a
distal tuft. Each of the 50 tuft annuli of the lateral flagellum of a mature
lobster (H. americanus) carries two rows of some 12 aesthetascs, each
containing
300 olfactory receptor neurons
(Atema and Voigt, 1995
;
Oleszko-Szuts and Atema, 1977
)
that project to the glomeruli of the olfactory lobes
(Sandeman et al., 1992
). A
variety of morphologically different non-aesthetasc sensilla
(Oleszko-Szuts and Atema,
1977
; Guenther and Atema,
1998
) contain unimodal and bimodal chemo- and mechanoreceptor
neurons that project to the lateral antennular neuropils, which lack
glomerular organization (Schmidt and Ache,
1992
; Schmidt and Ache,
1997
). The prominent guard hairs are bimodal, containing some 20
receptor neurons (Cate and Derby,
2001
). In H. americanus each of the 50 tuft annuli carry
up to four guard hairs for a total of 4000 receptor neurons, most of which
appear chemoreceptive based on axon diameter (J. Atema, unpublished
observation). Several other setal types are found on this flagellum, but their
function is not known and homology with setae described in spiny lobsters
(Cate and Derby, 2001
) is
still unclear.
Based on this sensory neuroanatomy it was believed that crustaceans would
need functional aesthetasc sensilla to perform complex chemoreception tasks,
such as discriminating odor mixtures and locating odor sources. Some
behavioral results seemed to support this notion. Removal of one lateral
antennular flagellum prevented H. americanus from making correct
initial directional decisions when tracking food odor; selectively shaving off
the aesthetasc sensilla of one flagellum still had a noticeable, though
lesser, effect (Devine and Atema,
1982). This suggested a major role for aesthetasc sensilla and a
minor role for non-aesthetasc sensilla in odor tracking. However, detailed
studies on spiny lobsters, in which either aesthetasc chemoreceptors or
non-aesthetasc chemoreceptors were ablated, showed that aesthetascs are not
required for seemingly complex olfactory tasks. Without aesthetascs they can
still discriminate between complex food odor mixtures
(Steullet et al., 2002
), and
can locate food odor sources in low flow environments
(Steullet et al., 2001
) and
track odor plumes in a narrow flume
(Horner et al., 2004
). If the
aesthetascs are not essential for food mixture detection and source
localization, what then is unique about this major chemosensory input system
with its large glomerular olfactory lobes?
We focus here on the role of aesthetasc sensilla in individual recognition
in H. americanus. We know that the individual recognition function is
limited to the lateral flagella and cannot be supported by the medial flagella
and antennae (Atema et al.,
1999; Karavanich and Atema,
1998b
). However, as these lesion studies were based on treatment
with distilled water, which eliminates all chemoreceptor function
(Derby and Atema, 1982
), it
remained unknown if the aesthetasc pathway is uniquely involved. Such
knowledge would facilitate identification of pheromone receptors and the
central processing of individual memory.
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Materials and methods |
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Experimental design
The design used to address these questions includes two separate
experimental groups: (1) aesthetasc shaved and (2) guard hair shaved. Each
group contains three sequential treatments: for Group 1 these are (A) first
interaction, normal untreated; (B) second interaction, aesthetasc or guard
hair shaved; (C) third interaction, lateral flagella lesioned using distilled
water. Treatment designations for group 2 will be AA, BB and CC, respectively.
The only difference between the two groups is treatment B (aesthetasc shaved)
vs BB (guard hair shaved). If aesthetasc sensilla are important for
individual recognition, we expected that their shaving would prevent
recognition and result in long and intense second interactions (B) not altered
by subsequent water lesion in third interactions (C). In contrast, guard hair
shaving would not affect recognition, leading to reduced second interactions
(BB) and a return to long and intense interactions after water lesion
(CC).
All 60 lobsters in this study were size matched so that fighting pairs were
within 3 mm CL; this close matching is known to make the fight outcome
unpredictable by size (Scrivener,
1971). These 30 fighting pairs were randomly assigned to either of
the two experimental groups: 15 pairs to be aesthetasc shaved and 15 pairs to
be guard hair shaved. Each pair, regardless of group designation, had to
complete a series of three 20 min interactions in a `boxing tank' on 3
consecutive days. In interaction A, the pair fought to establish dominance.
26 h later either aesthetascs or guard hairs were shaved according to
group designation. One day (24±4 h) after the first interaction, the
pair was brought together again in interaction B. Approximately 22 h after the
conclusion of interaction B, each pair, regardless of group, was given a 10
min distilled water immersion of both lateral flagella exclusively. 2 h later
the pair was reintroduced for a third and final time in interaction C. After
completion of the experiments both lateral flagella were removed from all
animals and preserved in formalin for future inspection of shaving efficiency.
The lobsters themselves were kept in the laboratory for a few more weeks prior
to release to observe their state of health and possible molting that may have
affected the fight outcome.
Experimental apparatus and procedures
Testing was conducted in a `boxing tank': a 90 cmwidex60 cmx60
cm all-glass aquarium illuminated by two 100 W bulbs suspended 1 m above the
water surface. A water depth of at least 30 cm was maintained during all
fights. Water was drained and replaced after each fight. The lobsters of a
pair were placed in this `boxing tank' on either side of a plastic divider for
510 min prior to the start of the fight in order to acclimate. Then,
the divider was removed and the pair were allowed to interact for at least 20
min. All interactions were recorded with an overhead video camera for later
analysis. Recording ended if the interaction had been a fight with a
definitive winner or if there had been no significant interaction. However, if
the lobsters were still actively engaged in fighting after 20 min, the
recording was continued until a definitive outcome to the interaction was
reached. A definitive outcome was defined as maintenance of a stable dominance
relationship for at least 5 min, as indicated by the loser's continuous
crouched position and avoidance of his opponent.
Shaving of sensilla was accomplished by first restraining the lobsters upside down on a customized barber chair. Lobsters were wrapped with a wet towel and their antennules were constantly wetted to prevent desiccation. Aesthetascs or guard hairs were shaved with a razor blade fragment under a dissection microscope. The procedure took no more than 45 min per lobster. After the shaving procedure, the lobsters were allowed to recuperate in their individual holding tanks. To determine lesion efficiency, the lateral flagella of all animals were removed after the end of experimentation and preserved in formalin. Two independent observers scored the number of intact remaining sensilla on each flagellum. Greatly shortened (<50%) or fallen sensilla were not considered intact (see Discussion).
Applying the distilled water lesion was done by first restraining the lobsters in the same fashion described above. Their lateral flagella exclusively were then briefly rinsed in deionized water and subsequently immersed in a vial of deionized water for 10 min. After this procedure the lobsters were allowed to recuperate for at least 2 h in their individual holding tanks before the beginning of interaction C.
Data analysis
The videotapes were analyzed for fight duration and intensity according to
established procedure (Karavanich and
Atema, 1998a) using slightly modified agonistic levels. As before,
levels 1 and 2 represent avoidance (walking away) and fleeing
(tail flipping, running away), respectively; level 0 means an animal not
facing the other within one body length or no response; level 1 represents
approach behavior and level 2 threat displays (such as meral spread and
antenna and claw pointing) without physical contact. We split the former
`level 3' into a new level 3 consisting of antenna whipping (with contact) and
a new level 4 consisting of claw pushing or boxing. This caused former levels
4 and 5 to become levels 5 (claw lock) and 6 (scissor, rip). We then assigned
a single agonistic score for every 5 s interval of the fight. Since it was
possible for a lobster to be engaged in more than one agonistic level during
one 5 s interval we adopted the following ranking to assign this score.
Agonistic levels 6, 5, 4, 3 and 2 outranked all other levels in decreasing
order (i.e. 6 outranked all other levels, 5 outranked all other levels except
6, etc.); level 1 outranked only level 0; level 2 outranked level
1; both levels 1 and 2 outranked levels 0 and 1. Mean
aggression was then calculated as the sum of all agonistic scores divided by
the number of 5 s time intervals during the fight. Maximum aggression was
calculated as the total number of level-6 scored during the fight. Fight
duration was measured from the start of engagement at aggression level 3 until
the time that aggression dropped below level 3 for 5 min.
Statistics
We measured the duration of each fight and the mean and maximum aggression
of the winner and the loser. The data were not normally distributed.
Therefore, each of these five parameters was evaluated first using a
non-parametric 2 test across groups and treatments (Van der
Waerden test in the program JMP 4.0.0; SAS
Institute Inc., 1995
). Then treatment differences within the two
groups were evaluated with a Friedman ANOVA (Statistica for Windows 5;
Statsoft, Inc., Tulsa, OK, USA). The experimental design allowed us to then
test pairwise for differences between the three sequential treatments
(Wilcoxon signed ranks test; JMP 4.0.0;
SAS Institute Inc., 1995
). We
evaluated the effect of lesion efficiency on fight parameters of winners and
losers by Spearman rank correlation (Statistica; Statsoft Inc. 1995). Mean
values are shown with standard errors
(S.E.M.).
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Results |
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In contrast, only 3 of 15 pairs (20%) did not fight after aesthetasc shaving (`B' fight; Table 2a, BC). When we eliminated these three from analysis we did not find significant differences between treatments (Table 2b, BC).
In sum, guard hair removal and leaving aesthetascs intact resulted in the complete absence of BB fights in nine pairs and shorter BB fights in the remaining six pairs. This greatly and significantly reduced fighting suggests normal function of opponent recognition in the second fight was retained in this group. In contrast, aesthetasc removal and leaving guard hairs intact did not lead to significantly shorter B fights in fighting animals, suggesting interference by the treatment with the process of recognizing previous opponents.
Effects of distilled water lesion
Group 1
Fight duration after aesthetasc shaving did not change significantly after
subsequent treatment with distilled water
(Table 2a, BC). Mean C
fight duration was also not significantly different from the original A level
(Table 2a,AC) indicative
of lost recognition capability. Two of the three pairs that did not fight in
the B encounter started fighting again in the C fight, suggesting that they
had now lost the recognition capability they may have had in the B fight.
Group 2
Similarly, six of the nine pairs that did not fight after guard hair
shaving (BB) started fighting again after distilled water lesion (CC),
indicative of now lost opponent recognition. In this guard hair group,
distilled water lesion also caused a significant increase in fight duration
from (Table 2a, BBCC),
but the mean fight duration of CC fights remained less than in the AA fights
(Table 2a, AACC).
In sum, most pairs that did not fight or had short fights after guard hair or aesthetasc removal started fighting again after distilled water treatment had eliminated the chemosensory capabilities of their lateral flagella.
Mean and maximum aggression of winners and losers
For analysis of mean and maximum aggression, all 17 `no fights' were
excluded from calculations to reveal fight intensity in those that did fight.
Overall, across all fighting pairs, regardless of treatment (N=73),
both mean and maximum aggression were significantly greater for winners (W;
Wmean=3.53±0.08; Wmax=4.62±0.76) than for
losers [L; Lmean=3.0±0.11; Lmax=3.29±0.65;
Wilcoxon signed rank, (WL)mean, rank=1057,
P<0.0001; (WL)max, rank=416, P=0.01].
In winners and losers of both groups, a downward trend in aggression measures
appeared over the three treatments, but none of the differences were
statistically significant (Wilcoxon tests as above). In particular, mean
aggression was remarkably stable among all treatments for both winners and
losers. Winner mean aggression in the six treatments varied from a high of
3.72±0.11 in treatments A and B to a low of 3.23±0.27 in CC.
Loser mean aggression varied from 3.37±0.21 in A to 2.67±0.39 in
BB.
Of the four aggression parameters, only `Maximum Aggression of Winners' showed a significant treatment effect, which occurred in Group 1 (aesthetasc shaved), but not in Group 2 (guard hair shaved; Table 1). The difference was due to a large drop from 5.8±1.2 in the A fight to 1.77±0.72 in the C fight. In the same animals, mean aggression remained nearly unchanged (3.72±0.11 in A to 3.51±0.2 in C).
In sum, treatment did not significantly affect fight intensity: if a pair fought, they did so with characteristic intensity in which winners were more aggressive than losers.
Effectiveness of aesthetasc and guard hair shaving
Guard hairs were always completely removed. However, in most cases at least
a few aesthetasc sensilla were still remaining after shaving. The number of
remaining intact aesthetasc sensilla per pair of antennules varied from
020 per winner/loser pair (013 per animal in winners, 011
in losers), representing 00.5% of the 2500 aethetascs per
animal.
Correlations between the number of intact aesthetasc sensilla remaining after shaving either in winner, loser or both and the duration of fights and aggression levels of winners and losers were not significant (Spearman rank correlation). Thus, the presence of a few remaining aesthetasc sensilla did not significantly affect the overall outcome of this study. Although overall not significant statistically we will discuss the possibility that, particularly in losers, a few remaining aesthetascs could have mediated recognition of a familiar opponent.
Effect of temperature on fight duration and aggression
Fight durations were shorter at the lowest (6°C) and highest
(23.5°C) temperatures (quadratic regression, r2=0.06,
t=2.11, P=0.04). A total of six interactions were
conducted at 6°C. Two of these resulted in no fight, one in an aesthetasc
shaved pair (B) and one in a guard hair shaved pair (BB). Both winners and
losers showed greater mean aggression at higher temperatures (linear
regression, winner: r2=0.29, t=5.44,
P<0.0001; loser: r2=0.18, t=3.95,
P=0.0002), but the clear differences in mean aggression between
winners and losers (see above) were not affected by temperature. The maximum
aggression of losers but not winners increased with temperature
(r2=0.05, t=1.99, P=0.05).
We conclude that the effects of temperature on fight parameters did not differentially impact the treatments and thus the outcome of this study.
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Discussion |
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Normally, in a pair of intact lobsters, the duration of their second fight
17 days later is greatly reduced, frequently to zero. Because the loser
of such a pair will not reduce fight duration when faced with an unfamiliar
animal who has won his previous fight against another lobster, this
second-fight reduction or absence has been interpreted to reflect individual
recognition of the former opponent. Recognition of a former opponent is based
on information transmitted by urine pheromones via the lateral
flagella (Karavanich and Atema,
1998b), but it was not known which sensillar type is involved. In
the present study the removal of aesthetasc sensilla abolished the normal
fight reduction, thus showing that aesthetascs are necessary to mediate
individual recognition. Both the positive control of removing all
chemoreception by distilled water lesion and the negative control of no lesion
had been done several times previously under similar conditions (Karavanich
and Atema, 1998a
,
b
;
Atema et al., 1999
).
Our results in H. americanus complement studies on the role of
aesthetasc sensilla in spiny lobsters, Panilurus argus (Steullet et
al, 2000,
2001
), where their role in
social recognition was not investigated. The importance of aesthetascs in
social behavior was also found in blue crabs
(Gleeson, 1982
) where partial
removal of aesthetascs from the lateral flagella of male blue crabs resulted
in reduced courtship responses in males; the response was absent in males with
total aesthetasc tuft ablation.
While this lesion study focused on aesthetasc sensilla vs guard
hairs, there are several other setal types present on the lateral flagellum of
the antennule of H. americanus
(Guenther and Atema, 1998) and
P. argus (Cate and Derby,
2001
). Most common are the serrulate setae, distributed all over
the antennule, but not among the aesthetasc/guard hair tuft. The serrulate
setae were thus not affected by either of the two shaving lesions and cannot
have affected the differential outcome of the present study; their
chemoreceptors cells could, however, have been affected by distilled water
lesion. In the tuft region, closely associated with the guard hairs, are two
relatively rare and very small setal types, feathered and cork-screw shaped
setae of unknown function, the latter morphologically different from but
perhaps homologous to asymmetric sensilla in P. argus
(Cate and Derby, 2001
). These
setae were not specifically considered in this study. Based on their location
and on post-operation inspection of antennules, both types appeared to be
removed during guard hair shaving, while remaining intact after aesthetasc
shaving. Therefore, we interpret `guard hair shaving' results to include
removal of these additional setal types.
This study on the sensory pathway for individual recognition points to the
olfactory lobe with its typical glomeruli as the initial processing center for
learning and memory of odors associated with social partners. The behavioral
context of individual recognition in dominance is relatively well understood
in lobsters; the fact that it also occurs in other crustaceans (for a review,
see Atema and Steinbach, in
press) suggests that it is more common than we believed at first.
Both males and females learn about each other's individual odor in a dominance
context (Atema et al., 1999
),
but this information may be used in more than dominance relationships; for
example, individual recognition in courtship has not been studied in lobsters
but is known in other decapod crustaceans
(Atema and Steinbach, in
press
). Therefore, this study brings us one step closer to
elucidating the physiological mechanisms and evolution of chemical recognition
of individuals in invertebrates in general.
We consider the possibility that even a few aesthetasc sensilla may suffice
to process individual recognition. The contribution of only a dozen sensilla
was suggested in two of the three B pairs that did not fight after incomplete
aesthetasc removal: subsequent deionized water lesion caused fight resumption
in their C encounter, characteristic of now abolished recognition. There was
also a weak negative correlation between the number of remaining intact
aesthetascs in losers and the mean and maximum aggression levels of winners
and losers in B fights (N=15, R=0.37,
r2=0.14, P=0.17). This is interesting since it is
the loser's recognition of the opponent that determines first his aggression
level and then, indirectly, the responding aggression level of the winner and
thus the duration of the fight (Steinbach
and Atema, 2004). If individual recognition might be possible
using only a few aesthetasc sensilla, and if each aesthetasc can be considered
a `replicate unit' (Steullet et al.,
2000
; Spencer,
1986
) of receptor expression across its
300 cells, then about
10 replications of 300 receptor cells might extract sufficient information
from the urine signal to identify the learned odor of a former opponent. A
separate study will be necessary to determine the minimum number needed for
recognition of familiar opponents.
Aesthetasc shaving and distilled water lesion treatments affected primarily
the decision to fight, and only to a smaller degree the intensity of the
fight. This result seemed at first surprising, since we had shown earlier
(Karavanich and Atema 1998a,
b
) that not only fight
duration but also fight intensity decreased in subsequent fights. However, in
the previous work we had included `no-fight' interactions as expressions of
mean fight intensity (expressed as `agonistic value'), so that there too the
reported decrease in mean fight intensity may have been caused primarily by
the effect of no-fights, i.e. zero intensity. We point out that the fights of
the six pairs that still fought after guard hair shaving were significantly
shorter, thus still showing recognition. We interpret this continued fighting
to mean that these six pairs had not completely resolved their dominance
relationship in the first interaction and required some continued fighting.
Such effects have been seen commonly in groups of lobsters freely establishing
dominance relationships in naturalistic tanks
(Morschauser and Atema,
2003
).
Interactions were conducted successfully over a wide range of temperatures
(623.5°C), with the great majority in the range of
1223°C. Most of the six interactions conducted at 6°C showed
shorter than average fight durations, including two resulting in no-fight, one
each in the aesthetasc shaved and the guard hair shaved groups. In general,
below 5°C lobster behavior begins to slow down, as observed in the
laboratory and in the field (Karnofsky et
al., 1989) until movement virtually stops at 2°C (J.A.,
personal observation), leading to hibernation. We conclude that, apparently,
individual recognition occurs over a wide range of temperatures.
One additional point warrants discussion. The analysis of aggression
demonstrates intrinsic winnerloser effects. Excluding `no-fight'
interactions and comparing the remaining interactions revealed that there was
no difference in fight intensity resulting from treatment or group and that
the winner, in all treatments across both groups, always had a higher mean and
maximum aggression score. This winner effect cannot be due to differences in
sex (all males), size (pairs were within 3 mm CL), or molt state (all were
hard-shelled and none molted in the weeks following the fights). Apparently,
eventual winners consistently fight more aggressively than eventual losers.
This intrinsic dominance difference may reflect `confidence' resulting from
genetic differences and from agonistic experience. It can form the basis for
dominance hierarchies without individual recognition in other species (see
discussion in Gherardi and Atema,
2005). It was also noticed earlier in H. americanus
(Breithaupt and Atema, 2000
)
and indicates that both confidence and individual recognition play a role in
the social organization of this species.
These results of this study provide important information and considerations for studies of the identification of individual recognition pheromones and dominance pheromones where it is useful to know not only the behavioral context of signal production but also the receptor pathways involved.
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Acknowledgments |
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Footnotes |
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References |
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