WFSC 448 – Fish Ecophysiology
Fish behavioral ecology—memory and cognition
(Week 11 – 20 Nov 2015)
Organization and text modified from Stéphan G. Reebs, Social intelligence in fishes (2010)
Learning goal: To spark and feed your sense of wonder about nature
We talked about the ability of fish to perform cognitive transference. In animal
behavior, such abilities are generally the line in the sand regarding cognition. In
mammals a classic experiment in tranferrence is assessed with “the mirror test”: an
object is placed on an animal where they cannot see it and a mirror is placed in the
cage. When the animal sees its image with the object—they often reach to the mirror
to inspect the object. Eventually the animal may reach purposefully to that spot on its
own body, indicating they know the image in the mirror is themselves. Thus, they must
have awareness of their “selfness”. My memory suggests people have tried this with
fish but never have succeeded. (Challenge: How would you design such a study?)
Back to what we DO know about fishes…
Remembering good partners
 Bluegill sunfish can recognize and remember
individuals they worked well with. Wilson gave focal
bluegills good and bad foraging partners and then
measured preference for the partners a month later.
There was strong preference for the good partner.
Remembering who was watching
 Siamese fighting fish, Betta splendens, are aware of who watched their battles.
An experiment10 was performed in which a female observed two males that
interacted until a dominant-subordinate relationship. The males were then given
a standard choice trial for the observer female or a new (naïve) female. Dominant
males courted both females equally, but the subordinate male differentially
courted the new female. It appears that the subordinates knew their investment
in courtship was less valuable when invested in a female that saw him as a loser.
 So are fish not self-aware? Are they not concerned
with what others think of them?
 In different experiments spectator females where
shown to pay more visits to a male they have seen
winning a fight than to the loser. So the loser’s
awareness and shifted courtship allocation indeed
pays dividends.11
 These experiments were repeated many times with other males and females and
the result remained the same.12
Recognition of cooperators and cheaters
 The bluestreak cleaner wrasse Labroides
dimidiatus performs an ectoparasite removal
service for large nonconspecific “client” fishes.
 The wrasse also sometimes add to their caloric intake by nipping bites of the body
mucus off their clients. Clients dislike this and may “jolt” and dart off when
cleaners bite them.
 Clients submit to being cleaned. They invite a bout of cleaning either by adopting a
typical posture or simply by remaining motionless near a cleaning station.
 Field observations13 indicate that clients nearly always solicit a cleaner if they saw
that the cleaner’s last client interaction ended without conflict. Clients solicit less
if they did not see the last interaction. Thus, clients pay attention to the fairness of
their potential cleaners.
 Cleaners seem to know they have a reputation. They refrain from biting a client
when many bystanders are watching. Observer-dependent behavior is called an
“audience effect” in animal behavior.
 The reduced biting when a client cue exists may be an indication of awareness
they have a reputation, thought it calso could just mean the “temptation to cheat”
is less given there is a long line of food cued.15
 Finally, cleaner wrasses sometimes work as male-female teams. When the female
“cheats” and bites a client, the male, who is larger, chases her off—a punishment.
It’s as if the male cares about the reputation of his cleaning station. Lab
experiments (with preferred or less preferred foods which could be withdrawn
when the preferred food was chosen) showed that males punished misbehaving
females (those who chose the preferred food, causing all food to be withdrawn).
Females behaved better thereafter (they now chose the less preferred, but more
permanent, food), and that this better behaviour allowed the male partners to
feed more.16 (shades of 5 wet monkeys—clean clip; also discusses creativity)
Interspecific communication
 Cleaner wrasses often begin cleaning sessions by brusing their pelvic and pectoral
fins against the dorsal fins and back of the client. This seems to be a signal used
predominantly for clients that do not adopt the classic postural cue it is there to
be cleaned, or cease motion. Interestingly, the wrasses are also prone to use the
cue much more for hungry predators than recently fed ones19.
Manipulating and deceiving others
 We already discussed deceptive intraspecific cues in
fathead minnows, Pimephales promelas, in which males retain water to mask loss
of condition during nest defense. This “puffed up” appearance is likely to attract
more females and ward off other males and sneakers.
 Wild goose chases are a great way to distract foes. Killdeer feign a broken wing
and lead nest predators away from their nest. Stickleback appear to do the same.
Males defending a nest full of eggs must be wary of shoals of females that
sometimes attack nests to eat eggs. When a parental male sees a menacing shoal
of hungry looking females coming his way, he often swims away from his nest and
starts poking his snout into the ground. This is the same action a female would
perform while raiding a nest. This display commonly fools the females into
believing that a nest has been discovered. They rush to the site and start digging
there too. Meanwhile, the male leaves the shoal and returns to his territory21.
 A similar behavior occurs in bowfin, Amia
calva. Fry follow their male parent for a
while after they hatch. Apparently, when a
fry predator appears on the scene, the male
sometimes moves away and thrashes about in the water as if injured, thus
drawing the attraction of the predator onto himself and away from the fry.22
 If a male Atlantic molly Poecilia mexicana is given a choice
between two females in an aquarium, it choose to invest
courtship activity in the bigger one. (Why?) But if a second
male is introduced, the first male will move to the less
preferred female. Fish are extremely well known for mate
choice copying. Perhaps the first male is trying to draw the
second male’s attention to the less-preferred female23.
 Sailfin silversides offer another deception. One
species, Telmatherina sarasinorum, is an egg
predator. It often follows courting pairs of the
closely-related species T. antoniae. When those
pairs lay eggs, T. sarasinorum darts in and picks at
the eggs, eating them. On several occasions
researchers observed male T. sarasinorum who
were following a pair of courting T.antoniae to chase off chased off the male T.
antoniae and take his place courting the heterospecific female. When female
released eggs the egg predator ate them24. Remind you of any other cases of
deception in the animal kingdom? Shades of Photinus!
Cooperation in fishes
Beginning with Milinski and championed by Dugatkin is the idea that fishes play tit-fortat in predator inspection. I discussed this in class before, but the idea is fish in a group
will take turns advancing toward a predator to gain information about the predator’s
status, thereby sharing and diluting risk to achieve gain. Hungry and motivated
predators can be told apart from fed predators. The former are dangerous; the latter,
not. So the information is useful because non-dangerous predators allow prey to
resume other life functions such as foraging. The theoretical reason to expect
cooperative predator inspection stems from an iterated version of the prisoner’s
dilemma:
graph the fitness payoffs as we did before…
The best strategy in an isolated encounter is to defect regardless of the other player’s
move. However if iterated, the best solution is “tit-for-tat”. What are the payoffs for
the two strategies:
Defect:
Cooperate:
Recall this scene where Chandler prefers not to stand by Brad Pitt:
https://www.youtube.com/watch?v=-Veizisjwdk (28-40s)
 In other guppy experiments, Dugatkin wondered if male
guppies would recognize and prefer to associate with other
males that seem to be less attractive to females, making themselves “look good”.
His experiments involved one female and three males (male A, male B, and a focal
male). Aquaria with each fish were positioned such that one male was observed
by the focal male to be closer to the female. The close male was expected to be
considered a “lady’s man” and male B as a looser. Preference of the focal male to
be near A or B was measured and indicated that 24 of 30 focal males spent more
time on the side of the loser male.26