Delayed Plasticity of an Instinct: Recognition and Avoidance of 2 Facing Eyes by the Jewel Fish
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Delayed Plasticity of an Instinct:
Recognition and Avoidance of 2
Facing Eyes by the Jewel Fish
RICHARD G. COSS
Department o f Psychology
University of California
Davis, California
A model depicting 2 horizontally positioned black spots resembling facing eyes, as compared
with models depicting other spot arrangements, elicits intense flight activity in young African jewel
fish (Hemichromis bimuculatus) under 5 months of age and 7-month-old subadults reared apart
from conspecifics with eyeless cave fish (Anoptichthys jorduni). In contrast, subadults permitted to
observe or interact fully with conspecifics during development exhibited attenuated discriminative
flight activity. These findings suggest that visual experience with facing conspecifics, irrespective of
physical contact, modifies the flight-eliciting properties of the innate mechanism subserving
eye-schema recognition, but only during later maturation.
Among vertebrates with well-developed vision, being confronted with 2 facing eyes
is one of the most widespread and ancient signals of impending danger. Presentations
of 2 schematic facing eyes induce prolonged tonic immobility in lizards (Hennig, 1977)
and avoidance in various species of birds (Blest, 1957; Scaife, 1976). Mouse lemurs
look less at a model depicting 2 horizontally placed concentric circles than they do at
other circle arrangements (Coss, 1978a). The fry of certain mouth-brooding cichlids,
such as Tilapia mossambica and Hemihaplochrornis multicolor, appear to differentiate
eyelike schemata early in their development. When presented a model depicting 2
horizontally placed spots, they often swarm or flee depending on the quality of the
model's movement (Goude, Edlund, Engqvist-Edlund, & Andersson, 1972; Peters,
1937).
African jewel fish fry (Hemichromis bimaculatus) exhibit a tendency to flee from
black discoid models soon after the emergence of free-swimming behavior (Baerends &
Baerends-van Roon, 1950; Noble & Curtis, 1939). More important, an approaching
model presenting 2 black spots, schematically arranged as facing eyes, elicits evasive
flight activity in a significantly greater percentage of 13-18 day-old fry than do less
facelike models' presenting other numbers of spots (Coss, 1978b). Discrimination of
2 schematic facing eyes continues throughout development, albeit the flight response
of adults is greatly attenuated as compared with that of juveniles (Coss, 1972).
Moreover, juveniles as they age seem to be less &timidated by the facing eyes of other
fish as represented by increasing intensities of face-to-face fighting (Coss, 1978b).
Reprint requests should be sent to Dr. Richard G . Coss, Department of Psychology, University of
California, Davis, California 95616, U.S.A.
Received for publication 14 April 1977
Revised for publication 23 January 1978
Developmen tul Psychobiology, 1 2(4) :3 35-345 (1 9 79)
0 1 9 7 9 by John Wiley & Sons, Inc. 0012-1630/79/0012-O335$01 .OOJewel fish, like many other cichlids living in shallow water, are subjected to
intense predation throughout their development. As fry, accidental ingestion by
foraging parents takes a toll; more intense predation occurs after leaving the nest,
especially by older juvenile conspecifics. As the fish grow larger, the threat of
predation shifts away from other fish toward reptilian and avian predators better able
to cope with their larger body size (Fryer & Iles, 1972; P. Loiselle, personal
communication).
In light of this intense predation pressure and the early appearance o f discrimina-
tive flight behavior in fry, the epigenesis of the ability to recognize 2 facing eyes
appears to be predetermined (see Sperry, 1971) rather than probabilistic (Gottlieb,
1973; Jacobson, 1974). That is, the underlying neural substrate subserving this
recognition is functionally organized through genetic processes operating irrespective o f
relevant configurational input. This expectation is based on the assumption that natural
selection would favor individuals capable of detecting and interpreting the predaceous
behaviors of other fish prior to experiencing an attack over those possessing perceptual
mechanisms dependent on conditioning as a by-product of unsuccessful predatory
strikes.
In 2 experiments I examined the influence of experience and maturation on the
reaction to 2 facing eyes by jewel fish. The 1st experiment has 3 parts in which the
same group of juveniles was studied between the ages of 83 and 160 days. In this
experiment I sought to determine the precision of discriminative flight behavior and
concomitant longitudinal changes in flight intensity. In the 2nd experiment I examined
the role of experience in facilitating the recognition of 2 facing eyes. I accomplished
this by comparing 6 groups of subadults reared with differential exposure to
conspecifics. Another objective of the 2nd experiment was to investigate whether flight
attenuation in older jewel fish is the result of some maturational process functioning
independently of experience or whether it was a combination of both processes.
Experiment I-Part 1
Methods
Subjects
Thirty juvenile jewel fish (Hemichromis bimaculatus) were tested at 83-88 days, of
age. Hatched apart from their parents, the fish were reared in a crowded community
aquarium with white substratum and light brown walls, which offered sparse pattern
stimulation beyond that provided by the fish themselves. Timing of the experiment
was set to coincide with the onset of face-to-face fighting in the largest fish so that the
group would have had only a limited amount of experience in agonistic encounters
before being tested.
Stimulus Models
Five models ( 3 2 X 27 mm) shaped roughly like the frontal view of an adult were
developed to present 0-4 (6 mm diameter) black eyelike spots. These spots were
designed to constitute a continuum of numerical and spatial features that wouldRECOGNITION OF 2 FACING EYES 337
provide information on the specificity of response to eyelike patterns. All models were
colored 2 hues of orange-red (ventral portion: Munsell 2.5 YR 6/14; dorsal portion: 10
YR 8/8) to stimulate the reproductive coloration of the adult.
Apparatus and Procedure
A repeated measures design was employed in which individual fish were exposed
successively to each of 5 models presenting 0 to 4 spots. Each model was mounted
perpendicularly to the axis of a slender arm (40 cm length) and advanced manually
toward the subject positioned in a net adjacent to the glass wall of a 19-liter model
presentation aquarium. The model was presented outside the aquarium from a distance
of 30 cm, with a mean approach velocity of 39.6 cm/sec (SO = 2.6), as determined by
video recordings. Presenting the models by hand, in an attempt to simulate a
predaceous attack from an adult conspecific, eliminated problems of motorized systems
that are incapable of targeting the subject appropriately and produce unwanted noise,
overhead shadows, and other extraneous stimuli that might elicit inadvertent flight
behavior (see Dill, 1974a, 1974b; Noble & Curtis, 1939; Rodgers, Melzack, & Segal,
1963; Russell, 1967).
During the experiment, the subject was transferred via a small-volume net (620 ml)
which was locked to the side of the model presentation aquarium containing fresh
water at 27°C. The net opening provided a 12.5 X 9-cm window from which the model
could be viewed as it approached to w i t h 5 mm in front of the glass and stopped,
where it remained for approximately 5 sec. Although the net restricted the distance of
flight from the model, it provided a soft, resilient surface to strike during repeated
escape maneuvers following frequent bouts of turning toward the model. In each
session, the models were presented once in a balanced randomized order with an
interstimulus interval of not less than 1 min. Models were only presented when the
subject was near the glass wall in a facing or parallel orientation.
The diaphanous properties of the net and size of the fish permitted detailed video
recordings of flight activity in plan view using a mirror mounted under the aquarium.
A Sony video camera (AVC 3260) and videocorder (AV 3650) with slow-motion
playback permitted frame-by-frame tracings of flight behavior in 16-msec time incre-
ments, which were transferred to a paper record for caliper measurements.
Results
A 1-factor within-subjects analysis of variance (ANOVA) applied to the data for 2
sec of flight revealed that significantly different flight distances were elicited by the
models (F = 14.75, df= 4/116, p < .0005). Further analysis of flight distance means
with Duncan’s New Multiple Range Test indicated that the model depicting 2
horizontally placed spots elicited significantly greater flight activity < .001) than
@J
any of the other models (Fig. 1A).
Experiment I-Part 2
Several aspects of the critical stimulus configuration eliciting intense flight activity,
such as the number of spots and their spatial orientation, could conceivably affect338 COSS
I80 - D
-
180-
160 160 - / =-- -=- -0
1
/ \
\
5'0 \
120 e,
-
too - 100
80 -
3'
60 -
60 -
40 -
4 *'
/
0 *' .-.
% 40 -
20 - 20 -
0-
Models
Fig. 1 . The mean swimmmg distance (mm) of jewel fish fleeing from models drpicting various
arrangements of black spots. (A) Two seconds of flight activity for 30 young juveniles 83-88 day,
of age. (B) Two seconds of f i g h t activity for t h e same juveniles at 126-131 days of age. (C) and
(D) One second of flight activity for 6 groups of 10 subadults (196-259 days of age) experiencing
different rearing conditions. The numbers in C and D refer to rearing groups
pattern recognition. Studies of discrimination learning by a wide variety of fish
indicate that the general number of salient features and orientation are importamt
recognition cues (Hager, 1938; Mackintosh & Sutherland, 1963; Schulte, 1957;
Sutherland, 1968).
Method
Subjects and Procedures
Using 3 models depicting 2 spots in the vertical, 50" diagonal, or horizontal planes
and the same experimental procedure, I retested the 30 juveniles at 126-131 days of
age to determine if the discrimination of 2 facing eyes was indeed dependent upon
specific spatial orientation.RECOGNITION OF 2 FACING EYES 339
Results
The horizontal orientation of 2 spots clearly increases the flight distance traveled
for 2 sec of flight activity ( F = 18.48, df= 2/58, p < .0005). Duncan’s New Multiple
Range Test applied to the flight distance means revealed that the model depicting 2
horizontally placed spots elicited significantly more intense flight activity (p < .OOl)
than was elicited by models presenting the other spot orientations (Fig. 1B). Although
these results were not based on a discrimination training procedure, they support the
findings of such training experiments on orientation discrimination using other species
of fish.
Further analysis of the 1st 100 msec of flight revealed that the initial tail-beating
activity was not a discriminative response to the perceptual differences of the models
and, thus, is most reasonably viewed as a startle response to sudden model arrival. As
has been examined in zebra fish (Brachydanio rerio), this apparent startle response to a
rapidly approaching model may be the result of a critical threshold in the rate of
change in the retinal image (Dill, 1973, 1974a, 1974b).
After this initial phase of flight, the fish characteristically paused momentarily,
often turning toward the model, and then resumed rapid tail beating. Slow-motion
video analysis of these pauses revealed that the critical model with 2 horizontally
placed spots evoked a significantly briefer mean pause of 164 msec as compared with
372-381 msec for the other spot orientations ( F = 6.66, df= 2/58, p < .OOS). These
latencies may reflect pattern processing differences elicited by the perceptual aspects of
the models. In support of the supposition that these pauses reflect central decision-
making processes, the briefest pauses were in the range of 100-120 msec, which is
longer than the 70-100 msec visually evoked response latencies recorded from sustained
on, off, and on-off single units in the goldfish optic tectum (see Jacobson & Gaze,
1964; Sutterlin & Prosser, 1970). On the other hand, visually evoked tegmental units
(probably tecto-bulbar fibers leaving the tectum; see Page & Sutterlin, 1970) and
intertectal commissural fibers (Mark & Davidson, 1966) exhibit response latencies
which are closer to the briefest pause latencies evoked by the critical model.
Experiment I-Part 3
As discussed above, 2 schematic facing eyes do not elicit intense flight behavior in
adults. Older juveniles also seem to be less intimidated by facing conspecifics than are
younger juveniles (Coss, 1978b). Therefore I determined whether flight attenuation in
adults would appear in older juveniles that had previously exhibited panic flight to 2 schema-
tic facing eyes. To assess changes in flight intensity, I examined single subjects between the
ages of 137 and 160 days. This series of 12 small experiments had 2 objectives: (1) to deter-
mine the onset of flight attenuation using the same models and procedure adopted in Part 2;
and (2) to induce complete flight habituation to stationary models as a means of measuring
their response-eliciting effectiveness in juveniles at different ages.
Results
Prior to 140 days of age, the model presenting 2 horizontally placed spots elicited
discriminative flight behavior as reported in Part 2. In stationary presentations, this340 COSS
model elicited intermittent flight activity (swimming up and down a small aquarium)
for several hours without apparent habituation. After 140 days of age, however, 1 had
increasing difficulty in eliciting discriminative flight activity. Instead of fleeing from
the approaching models, the juveniles froze or moved only short distances, typicany
performing defensive lateral displays with erected fins (see Baerends & Baerends-van
Roon, 1950).
Experiinent I1
Method
Subjects and Rearing Conditions
As a means of examining the interaction of maturation and experience on
eye-schema recognition and concomitant flight behavior, 6 groups of 10 jewel fish were
reared with different levels of social deprivation and, in 1 group, complete eye schema
deprivation (Table 1).
Group I was derived from a single spawn and transferred individually into tiny (48
ml) light blue aquaria (Munsell 5B 7/4) before their eye buds formed. Alter hatching,
the fry were fed frozen brine shrimp (Artemia nauplii) twice daily, supplemented wich
finely powdered commercial tablets (TetraMin). With water temperature maintained at
27°C +2" and changed daily, the survival of all fish reared in these miniature aquaria
was 74%. Visual stimulation was provided by a moving water siphon and graphics on 2
walls of the aquaria. These walls were covered with thin black lines running parallel in
TABLE 1. Experiment II.
Community
Species Aquaria with
Parent- Total Viewed from Territorial
Group Reared Isolation Compartments Demarcations
I - 1-73 74-214; blind
cave characins
I1 - 1-73 74-228; jewel
fish
111 - 1-73 - 74-259
IV 0-35 - 36-196; jewel
fish
Va 0-35 - - 36-203
VI 0-35 - 36-218
aSubordinate fish constantly chased by members of
Group VI.RECOGNITION OF 2 FACING EYES 341
a meandering curvilinear format designed to counteract problems of short-term
disorientation observed in pattern deprived isolation-reared fish (see Shaw, 1970).
After 73 days of isolation, the young fish were transferred individually into 1 of
12 compartments (23 X 13 X 6 cm) suspended in flat 73-liter aquaria. Each compart-
ment was provided with a 10 X 13-cm window which permitted the isolates a restricted
view of the larger aquarium interior housing 4 eyeless blind cave characins (Anop-
tichthys jordani). This condition was maintained for 140 days prior to discriminative
testing. The selection of blind cave fish as stimulus objects provided a quasinormal
visual setting with fish that superficially resembled the color and morphology of
conspecific adults, yet sustained the specific perceptual deprivation of 2 facing eyes.
Grouped in sets of 3 compartments positioned in 4 rows facing the same direction, the
isolates could see only the cave fish swimming among the rows, occasional movement
of caretakers, and the compartment interiors which depicted black, green, and orange
parallel meandering lines similar to the graphics in the miniature aquaria. All caretakers
wore masks with similar graphics to obliterate their eyes. The compartmentalized
isolates were fed frozen brine shrimp twice daily. The compartments were cleaned
weekly and water changed bimonthly. Filtered and aerated water circulated through
screens placed above the windows and at the compartment bottoms, permitting
dissolved excreta to dissipate.
Group I1 was obtained from the same spawn and reared identically to Group I
with the exception that they were able to observe conspecific adults for 154 days.
These larger fish initially attempted to prey on the young isolates positioned behind
the compartment windows; they also engaged in the usual repertoire of territorial
fighting, pair-bonding, and spawning.
Group 111 was obtained from the same spawn as Groups I and 11, but was released
after 7 3 days of isolation rearing and allowed to develop normally with conspecifics in
(51 X 59 X 24 cm) 73-liter aquaria, provided with distinctively patterned houses to aid
territorial demarcation (see Boer & Heuts, 1973; Figler, Klein, & Peeke, 1976; Heuts &
Boer, 1973).
The remaining 3 groups were derived from a single spawn produced by parents
which were sibs with the parents of the isolates. Parent-reared for 35 days, Group IV
was then placed in compartments surrounded by conspecific adults in conditions
identical to Group II. Groups V and VI were permitted the opportunity to develop
normally in 73-liter community aquaria with patterned houses after being removed
from their parents at 35 days of age. These laboratory aquaria with relatively low
population densities (6 fish/aquarium) did not provide the vaned stimuli experienced
by jewel fish living in natural conditions. Moreover, the aquarium sizes, fixed territorial
markers, and rich diet provided the opportunity for intense territorial fighting, a
phenomenon which is not observed frequently among foraging jewel fish in the wild
(P. Loiselle, personal communication). The high rate of agonistic behavior seen in
aquaria-reared fish, however, provided the opportunity to examine the effect of
noxious stimulation (i.e., mouth biting, tail nipping, chasing, and opercular threat
displays) on discriminative flight behavior. Using territorial sizes and frequency of
winning bouts of face-to-face fighting, as determined by daily time-sampling 30 days
prior to discriminative testing, I separated the normally reared fish into dominant and
subordinate groups. Group V consisted of subordinate fish which had difficulty
maintaining fixed territories and were chased constantly; Group VI consisted of342 COSS
dominant fish approximately equated for territorial sizes and frequencies of winning
bouts of territorial fighting.
Apparatus and Procedure
The groups of subadult fish were tested for discriminative flight behavior at ages
ranging from 196 to 228 days of age, with the exception that the released isolates
(Group 111) were tested at 259 days of age. Delaying the discriminative testing of thlis
latter group provided a time period for the development of territorial behavior roughly
equivalent to that provided the normally reared fish of Group VI. The 5 models
employed in Experiment I were presented using a longer (130 cm) L-shaped model
presentation arm which pivoted through a 90" arc from behind a blind. Thus, the
looming model could be viewed over a greater distance than in the juvenile experi-
ments as it approached at a mean velocity of 136 cm/sec (SO = 9.2). In contrast with
the juvenile experiments, the net was eliminated to provide greater maneuvering space
(40 X 20 X 14 cm) in keeping with the larger size of the subadults. After a 10-mnn
period to allow habituation to the experimental setting, the 1st model was presented
when the subject was in a resting position adjacent to the model presentation wall.
Each model was presented once in a balanced randomized order with an interstimulus
interval of 1 min. Immediately after terminating its response to each model, the
subject was gently coaxed back to its original starting position using a small net.
Results
A mixed (Groups X Models) ANOVA applied to the data from 1 sec of flight
failed to detect significant main effects for rearing conditions or models. However, t'he
simple main effect for models was significant for Group I reared with eyeless cave fish
( F = 3.93, df = 4/21 6, p < .005). Further analysis of the mean flight distance for this
group using Duncan's New Multiple Range Test indicated, as in the juvenile experi-
ments, that the model with 2 horizontally placed spots elicited significantly gieafer
flight (p < .OS) than any of the other models (Fig. 1C-1).
Simple main effects for model treatments were not significant for any rearing
conditions which permitted the subjects to observe the facing eyes of conspecifics. The
differences between groups for the spotless model and models presenting 1 and 2
spots, however, approached significance (p < .lo).
Additional analyses of the 1st 100 msec of flight distance for Group I revealed
findings similar to the results obtained from 1 sec of flight activity in that the model
presenting 2 horizontally placed spots was significantly more effective in eliciting flight
(p < .05) than any of the other models. In contrast with the findings of the juvenile
experiments, which did not reveal differential responses during the 1st 100 msec of
flight, the results with subadults indicate that model recognition played a greater role
in activating flight than the provocative aspects of sudden model looming
Discussion
In reviewing the findings of recognition and avoidance of 2 schematic facing eyes
by community-reared juveniles under 5 months of age and 7-month-old subadultsRECOGNITION OF 2 FACING EYES 343
deprived of seeing the facing eyes of other fish, we note that the epigenesis of the
underlying cognitive mechanism is predetermined rather than probabilistic. This
selective avoidance in subadults, particularly in the absence of appropriate experience,
demonstrates the innate ability of this cognitive mechanism to infer the risks associated
with the facing orientation of other fish.
Not only is this mechanism finely tuned by natural selection to respond to only
the appropriate assembly of numerical and spatial features, which constitute the
lineamental Gestalt of 2 facing eyes: its epigenetic development is deeply canalized (see
Waddington, 1957). This premise is based on its early functional appearance in 13-day-old
fry (Coss, 1978b) and its persistence in Group I subadults after prolonged stimulus
deprivation. Further study of 4 Group I females, after a year of isolation, revealed the
presence of specific tectal interneurons with markedly reduced receptive surfaces (Coss
& Globus, 1978, 1979). Despite this atrophy of the neural substrate concomitant
with prolonged sensory restriction, continued ability to recognize 2 facing eyes
indicates the existence of adaptations that act as buffers to prevent functional
disruption of this innate cognitive mechanism. Such deterministic maintenance of
pattern recognition, however, was not entirely unexpected because an urgent anti-
predator mechanism should be able to remain dormant for many months of specific
pattern deprivation and yet maintain its capacity to trigger behavior when the
appropriate stimulus is presented. Failure to react accordingly during the 1st predace-
ous encounter, of course, entails considerable risks (see Owings & Coss, 1977). Less
urgent perceptual-motor mechanisms which mature less rapidly, such as the mecha-
nisms mediating social communication (Gottlieb, 1973), might not be expected to
exhibit this high degree of preparedness (Seligman & Hager, 1972).
In terms of adaptive significance and changes in the risks of predation during
development, note that juveniles over 140 days and Groups 11-VI subadults exposed to
the frontal views of conspecifics, irrespective of physical contact, failed to respond
differentially to the models (see Figs. 1C-2, 3, & ID). With the exception of the
constantly chased subordinate fish in Group V, which tended to flee indiscriminately
from all approaching models (see Fig. 1D-5), the subadults reared with conspecifics
often responded defensively to the models in a manner similar to that reported above
for older juveniles.
Prior to 140 days of age, the flight-eliciting properties of the innate cognitive
mechanism do not appear to be labile to experiential influences with facing
conspecifics as represented by the steep generalization gradients generated by the
model presenting 2 schematic facing eyes (see Figs. 1A & IB). Perhaps this delay
of plasticity is an adaptive strategy coinciding with the small size of the juveniles
younger than 140 days of age and their vulnerability to predation. Among older
jewel fish, the reduced threat of predation by a diminishing number of larger
piscivores seems to have yielded a compromise adaptive strategy with costs and
benefits different from that of younger juveniles. The increased flexibility in flight
decision making which accompanies experience with other facing fish, as compared
with the juvenile strategy of all-out flight, could be costly in terms of the ability
to survive a predaceous attack. On the other hand, the benefits of the improved
ability to estimate the risks associated with facing adversaries would provide ad-
vantages in energy expenditure, particularly in defense of territory and protection
of fry.344 COSS
Notes
This research was supported by faculty research grant D922. The author thanks Misses
Margaret Williams and Mary Woo for their technical assistance, Dr. William Mason for his criticism
of the manuscript, and Dr. Paul Loiselle, Department of Zoology, University of California, Berkeley
for permission t o report several unpublished field observations.
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