Are fishes good parents?
Stphan G. Reebs
Universit de Moncton, Canada
2007
Parental
care is not the rule in fishes.
Most species are quite content to abandon their offspring to the
vagaries of a world populated by organisms that are fond of eating nutritious
little snacks such as eggs and fry.
These non-parental fishes may show discrimination as to where the eggs
are left (covered by gravel in salmon, in thick mats of weeds for some minnows,
in open water downstream from the reef in some wrasses) but I would classify
this as careful spawning, not parental care.
Though
they may form a minority, parental species are nevertheless very diverse.[1] They belong to many different families,
marine as well as freshwater.
About 80% of these families are represented by species that care only
for eggs. These fishes prepare or
build nests, sometimes nothing more than a cleaned rock, sometimes an
amalgamation of vegetal matter, empty shells, pebbles, sand, or even air
bubbles. At this site the eggs are
vigorously defended against potential predators (some yellow-spotted triggerfish,
Pseudobalistes fuscus, have even sent divers to the hospital with serious
bites to the legs [2] ). Parents also tirelessly fan the eggs –
moving water over the brood with movements of their fins – to provide
them with a good supply of oxygen.
In addition, they clean the eggs by brushing them with their fins. With
their mouth they remove dead or diseased eggs. Some transfer onto their eggs mucus that has anti-microbial
properties.[3]
If the nest is in the intertidal
zone, parents cover the egg batch with algae just before low tide, preventing
desiccation. One species of characin even jumps onto a low-lying leaf above the
water, lays and fertilises eggs that stick to the leaf, and then the male
periodically splashes water from below onto the eggs to keep them moist. The young drop into the water when they
hatch.
Many
species carry eggs with them so that if a big predator makes an entry onto the
scene, the parents can flee and bring the brood with them. The eggs are carried outside or inside
the body. Examples of
outside-carriers include medakas (eggs stuck to the females vent for a few
hours), bagrid and banjo catfishes (eggs embedded on the surface of the belly)
and suckermouth armoured catfishes (eggs attached to the males lower
lip). Inside-carriers include the
numerous species of mouth-brooding cichlids, sea catfishes, lumpfishes,
cardinalfishes, and gouramis (eggs carried inside the mouth, and regularly
churned in there for proper cleaning and oxygenation), many seahorses and
pipefishes (eggs developing inside a special ventral pouch on the male), and
finally, all livebearers as well as many sharks and rays, where young develop
inside the reproductive system of the female, sometimes nourished by special
connections to a placenta-like structure.
It is
estimated that only 20% of parental fishes care not only for their eggs but
also for the fry that hatch out of them.
Fortunately these species include most cichlids, which are well known
because of their popularity in the pet trade business.
Cichlids
that lay eggs on a substrate (as opposed to carrying them in their mouth) are
biparental. Both the male and the
female care for the eggs and young.
Outside of the cichlid family, such gender equality is rarely seen in
parental fishes. In cichlids it is
generally assumed that both parents are needed to defend the mobile fry against
predators. Cichlids breed in areas that are rich in predators, most notably
other cichlids of the same species.
The predation pressure is so high that one guardian alone could not
fully protect the brood.
Miles
Keenleyside demonstrated the necessity for biparental care in cichlids by
forcefully removing one member from a number of parental pairs and then measuring
offspring survival in the presence and absence of potential predators. The parental species he studied was the
rainbow cichlid Herotilapia multispinosa. The predators, introduced soon after
the parents spawned, were either two adult male convict cichlids, two or four
juvenile Managua cichlids, or two juvenile rainbow cichlids. Fry survival was measured as the ratio
of young still present 15 days after spawning relative to the number of eggs
laid – the nest had been raised out of the water and the eggs had been
photographed and later counted on an enlarged print. In the absence of predators (the control treatment), fry
survival was around 50% in parental pairs as well as lone parents (survival was
not 100% because many young commonly die owing to developmental abnormalities
and within-brood competition). In
the presence of predators, fry survival decreased to 30% even when both parents
were present, showing that the chosen predators were not incompetents. The
clincher here is that fry fared even worse when one of the parents was removed:
survival was 15% when only the mother was there, and 10% when only the father
remained. Obviously, biparental
care afforded a much better protection to the young rainbows than the
uniparental alternatives.[4]
Helpers
at the nest
At
least one cichlid species takes the concept of co-operative young-raising to
extremes. In Lamprologus brichardi (=Neolamprologus pulcher), a
substrate-brooder of Lake Tanganyika in Africa, offspring from former broods
stay with their parents and help to raise new broods. On average, 7-8 of these helpers can be found within the
boundaries of the same natal territory, sharing all parental duties, repelling
territory intruders, removing debris, cleaning and fanning the eggs, all for
the benefit of their younger brothers and sisters.[5] As they grow older and bigger, helpers
have the option of moving out to initiate their own breeding venture (often a
dicey proposition because safe spots are limited in their habitat). Some on the other hand prefer to stay a
while longer in the hope of inheriting their parents territory should one of
the parents disappear. Beyond a
certain body size however, helpers are often expelled by the breeding
pair. Helpers try to resist
eviction by adopting submissive postures, but most parents are not easily
dissuaded by such pleas.
Michael
Taborsky, working at the Max-Planck-Institut fr Verhaltensphysiologie in
Germany, conducted a number of interesting experiments with this system, both
in the lab and in the field. In
the lab, he observed that parents who had expelled large helpers welcomed them
back into the fold when potential territory usurpers were introduced into the
tank. This shows that parents
value the defensive contribution of their largest (and most aggressive)
helpers. Taborsky also observed
that natal territories in dense tanks – where competition for space was
intense – held larger helpers, which suggests that parents delayed
eviction of their largest helpers when this suited their needs.[6]
In the
field, Taborsky showed that helpers pay a price for their good deeds: they grow
more slowly than care-free non-helpers.
On the other hand, they enjoy a lower mortality rate thanks to the fact
that they reside inside a territory with good shelter. Taborsky also confirmed that natal
territory inheritance takes place.
In 40% of cases where he experimentally removed one member of a breeding
pair, the replacement was drawn from the pool of on-site helpers. Often the replacement was the helper
most similar in size to the missing parent.[7] Finally, large male helpers sometimes
steal fertilizations from their boss.[8]
Male
versus female care
Not
all cichlids are biparental or co-operative breeders. In most mouthbrooders (those species that carry eggs and fry
within their mouth), only one parent provides care. Only one parent is needed because the brood is mobile. When danger lurks, the parent can flee
and obviously take the brood with him or her. In most mouthbrooding cichlids, it so happens that caregivers
are the mothers (there are very few instances of biparental and male-only
mouthbrooders [9]). This preponderance of female-only care
in mouthbrooders is a mystery.
When all bony fishes are considered as a group, female-only care is the
rarest form of parental involvement.
The
most common form is male-only care.
This is not very well exemplified by cichlids. For better examples we must turn to sticklebacks, sunfishes,
blennies, cottids, and pomacentrids, to name only a few. In such species, males aggressively
stake out territories, prepare a spawning site, and court passing females. Females that accept to spawn with a
male do not linger afterwards.
While the males are busy releasing milt over the eggs, the females
promptly take off, leaving the males to keep on defending his territory along
with the eggs he has just fertilized.
The males usually tend to the eggs only, although in a few cases some
attention may be granted to newly-hatched fry for a day or two.
Costs
and benefits of parental care
Be
they male or female, alone or part of a team, most parents seem to incur
tangible costs for their dedication.
Substantial weight loss during the parental phase has been documented
for many species. At least one of these studies even found a correlation between
the size of the brood and the extent of weight loss, large broods being more
detrimental.[10] Weight loss is probably an inescapable
consequence of all the predator-chasing the parents do, as well as a lack of
foraging time (or, in the case of mouthbrooders, a plain and simple inability
to take in food; mouthbrooders cannot eat with their mouth full!) A demanding reproductive cycle may so
deplete energy reserves in parents that they cannot breed again for quite a
while.[11]
Parents
can also be stressed (what a surprise!), and sometimes it doesnt take much.
Take sticklebacks for example, a species where roving gangs of females can
attack the nests of parental males with the intent of eating the eggs inside.
In Gerry FitzGeralds lab, Michelle de Fraipont kept individual male
sticklebacks in aquaria where they could collect the necessary material to
build a nest, and where they had periodical access to gravid females for
spawning. However, the living
space of all of these males was limited to only half of the aquarium. The other half was barred by a
transparent partition pierced with small holes. On the other side of this partition there lived, depending
on the experimental condition, a solitary female, a solitary male, a solitary
female from another stickleback species, or no other fish. De Fraipont observed that only one of
these experimental treatments made any difference for the physical condition of
the parental male. When the male
could see and smell a conspecific female three-spined stickleback on the other
side of the partition, he lost twice as much weight over the study period (80
days), he could not pack in as many reproductive cycles into this period, and
in some cases he did not live as long.
De Fraipont and her co-workers called this the femme fatale effect:
the stress imposed by a known egg predator, a female conspecific in this case,
was said to be detrimental to the males state of health.[12]
So
there are hardships associated with parental care, but parents do get their just
reward. This reward is paid in the only currency recognised by natural
selection: a sizeable number of viable offspring. Parental species often breed
in difficult habitats that impose a need for parental attention if any
reproductive success is to be achieved.
We saw an example above with the necessity for biparental care against
predators in cichlids. Other
factors such as harsh environmental conditions may also render parental
attention mandatory. One lab study
with sticklebacks witnessed the progressive demise of egg clutches following
the removal of their parental caretaker.
Spread of disease, accumulation of debris, and lack of oxygenation were
to blame for the eggs death.[13] Even a mere reduction in fanning
levels, such as when an overabundance of territorial rivals diverts a fathers
attention, can have a measurable negative effect: eggs take longer to hatch,
meaning that they remain vulnerable to predators for a longer period of time.[14]
Some
substrate-brooding New World cichlids from the genus Aequidens lay
their eggs on a submerged loose leaf.
When disturbed, they move the leaf away by grabbing it with their mouth
and swimming backwards with it.
Miles Keenleyside and Cameron Prince conducted some interesting
experiments with Aequidens paraguayensis (=Bujurquina
vittata). They
offered spawning pairs a choice between various artificial leaves made of black
polyethylene. The leaves could be
small or large (19 vs. 79 cm2), and light or heavy (0.9 vs. 8.1 g,
depending on the presence or absence of a piece of lead attached to one
side). Almost all pairs preferred
to spawn on small and light leaves.
With a hydraulic flume, Keenleyside and Cameron proved that such leaves
produce less drag. These results
are consistent with the idea that the parents choose leaves that can be moved
easily.
Next,
Keenleyside and Cameron let a number of A. paraguayensis pairs
spawn on leaves within aquaria with an uneven gravel surface. Some areas within the tank were under
15 cm of water while others were under 30 cm. Some areas offered good cover (many plastic plants) while
other sections were bare. The
researchers measured how often the parents moved the leaf, and where the leaf
ended up lying most of the time, in the presence and absence of a crude
predator model (a minnow-shaped Rapala fishing lure, painted to look like the
predatory two-spot pike cichlid).
When the predator was visible, the parents moved the leaf three times as
much as usual. Most of the time,
the leaf was pulled to a deep area with cover. Keenleyside and Cameron thus supported the notion that
leaf-brooding and leaf-moving are an adaptation to minimise predator attacks on
the eggs.[15]
Egg
care: a broken wing display
As
mentioned above, nest-raiding is an annoying habit of female three-spined
sticklebacks. Shoals of females
roam and sometimes fall upon the nest of a parental male, eating all the eggs
inside and thoroughly devastating it.[16] Males take a dim view of this and they have
worked out a defensive ruse. When
a parental male sees a menacing shoal of hungry-looking females coming his way,
he often swims a short distance 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 this writhing mass of females and
returns to his territory, hoping (consciously or not) that the cloud of
sediments lifted by the feeding frenzy will conceal his own real nest. This striking behaviour is similar to
the broken wing display used by ground-nesting birds to lure predators away
from their nest.[17]
Another
similar behaviour has been reported for the 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.[18]
Cuckoos
that parasitize the parental efforts of other fishes
One
way to guarantee egg care without risking weight loss is simply to let other
fish do the work for you.[19] Sneaky copulations (see page on the sex
lives of fishes) are one way to achieve this. Another way is egg dumping (also called brood
parasitism), a behaviour whereby females deposit eggs inside the nest of other
parents and let them take care of the brood. In fishes, egg dumping usually takes place between
species. For example, many species
of minnows are known to spawn in the nest of various sunfishes. While fussing over his own clutch
– preventing silting over the eggs, fanning, chasing predators –
the parental male sunfish unwittingly provides care to the minnow eggs hidden
within his nest.[20] There are
even some reports of a species of minnow, the golden shiner Notemigonus
crysoleucas, dropping eggs into the nest of two of its predators,
the bowfin and the largemouth bass.
While doing their dirty deed, the minnows wisely stayed near the tail of
the bowfins, avoiding the dangerous mouth area.[21]
This
system superficially resembles the nest parasitism practised by cuckoos,
cowbirds, and other bird species.
There are, however, important differences. The minnows usually do not depend on the presence of host
nests to breed successfully. They
can spawn on their own if no sunfish nest is available (the minnows just lay
their eggs in weeds and leave them to their fate without any form of care, and
this seems to work well enough).
Moreover, contrary to bird hosts, which have evolved numerous
countertactics to foil parasitic attempts, sunfishes seldom try to stop minnows
from spawning in their nests. In
most cases the sunfish host does not suffer from the presence of minnow eggs
within the nest.[22] Sometimes they may even benefit.
Experiments where different combinations of sunfish, minnows, and/or egg
predators were mixed together and allowed to spawn showed that sunfish egg
survival is better when minnow eggs are also in residence, probably because of
a dilution effect. When predators
succeed in piercing the parents defense, the chances that they will pick up
the parents eggs are reduced because of the simultaneous presence of minnow
eggs.[23]
There
is one fish analogy to the true brood parasitism found in birds. In Lake Tanganyika, the catfish Synodontis multipunctatus
attends the spawning ritual of various mouthbrooding cichlids and lays eggs at
the same time, in the same spot.
The female cichlid, as is her normal habit, picks up all the eggs
present and commences incubating them inside her mouth. Unbeknownst to her, some of those eggs
are catfish. These alien eggs
hatch earlier than cichlid eggs.
While still in the mouth of the female cichlid, the catfish fry finish
absorbing their yolk sac.
Meanwhile the cichlid eggs hatch, but only just in time to be devoured
by the baby catfish! So, all that
the poor female cichlid has to show for her parental effort at the end of her
reproductive cycle is a few fat young that are not even her own species.[24] One can almost picture the female
catfish laughing depravedly on the sidelines.
Above
I wrote that egg-dumping usually takes place between species. There is one
example of egg-dumping within the same species, in the peacock wrasse Symphodus
tinca. Some
large males circumvent the costs of egg care by temporarily usurping the
successful nests of smaller males of the same species, spawning in these nests
with various females for a day or so, and then abandoning the site. The
original owners, whose eggs are still present among those of the usurper, may
not want to let their part of the nest contents be wasted and so they often
come back and resume guarding the nest, protecting the foreign eggs as well as their
own. This tactic on the part of
the big males is called piracy. [25]
Voluntarily
caring for somebody elses eggs, and even stealing eggs!
In some species, females prefer to
spawn in nests that already contain eggs. This preference does not leave males
indifferent. In fathead minnows
for example, big newly reproductive males sometimes evict the owner of an
already established nest rather than occupy a similar but empty site. Such usurpers do not destroy the
previous owners eggs but instead care for them (permanently, not temporarily
like the peacock wrasse above).
Why do these males care for eggs that are not their own? The behavior in fact makes sense when
we learn that female fatheads, like other species, prefer to mate with males
who are already caring for eggs.
This preference may very well have led to the evolution of nest
take-overs and adoption of eggs.[26]
In three-spined sticklebacks, territorial males have
sometimes been observed dashing over to the nest of a neighbour and stealing eggs
from him. They surreptitiously
enter the nest, take a mouthful of eggs, swim back to their domain (often with
the angry parent in pursuit) and deposit the kidnapped eggs into their own
nest.[27] This behavior can only be explained in
the light of females preference for nests that already contain eggs. The thieving males are trying to make
their nest more attractive.[28]
The Magellan plunder fish Harpagifer bispinis is
found in shallow rubble coves along the Antarctic Peninsula. The female
prepares a nest site by cleaning a patch of ground. After her eggs are laid and
fertilized, she remains on the nest, cleaning the eggs and chasing predators
until hatching occurs 4 to 5 months later. This is the longest brooding period
reported for fish (everything takes
longer in cold water!) Interestingly, if the female is experimentally removed,
a second guardian, usually a male, takes her place. If that male is removed, a
third fish, again usually male, moves in and assumes guard responsibilities.
There is as yet no explanation for these altruistic acts of replacement. The
new guardians may be genetically related to the original parent or to the
young, but this is not supported by the fact that captive plunder fish will
often accept to guard broods from other populations experimentally given to
them. It must be said however that the new guardians are less diligent in their
duties than the original parent, and their feeding and growth rates stay on a
par with those of non-guardians, so it seems there is little cost to this type
of substitute care.[29]
As
mentioned above, parental care can sometimes extend beyond the egg stage, into
the fry stage. In addition to cichlids, fry care can be seen in marine
catfishes (family Ariidae), freshwater catfishes (Ictaluridae), in the bowfin
(dont golden shiners know it), and in the damselfish Acanthochromis polyacanthus. Care consists mainly of guarding the
fry against predators but a few peculiarities have also been documented in some
species.
Unlike
birds, fishes generally do not feed their offspring. We can hardly expect them to feed hundreds of fry directly,
nor to be able to collect and carry the microorganisms on which the fry
normally feed. But there are a few
exceptional ways around those problems.
In the
Kampoyo catfish Bagrus meridionalis, which lives in
Lake Malawi, females do not lay a full complement of eggs. Some eggs are unfertilised and held
back within the ovaries. When the
fry are old enough (more than 15 days old), mothers gradually force out these
extra eggs and the young consume them.
Every day, mostly in the morning, a mother hovers 1 m above the bottom
and spreads her fins slightly downwards, at which point her young raise from
the nest, line up at her vent, and grab the small eggs she exudes. Kenneth McKaye has observed this
behaviour and has analysed the stomach content of wild-caught young, showing
that many of them subsisted mostly on these so-called trophic eggs. McKaye and colleagues also reported
that the father, not to be outdone, commonly ploughs into the ground near the
nest to stir up debris on which the young appear to feed. The father can also
scoop up a mouthful of sediments in his mouth, churn it, and release it near
the nest. The young can be seen gathering around the gills of the male as he
opens and closes his opercula. They get small invertebrates that way.[30]
(Trophic
eggs also exist in the cardinalfish Apogon lineatus, but
here their role is to feed the parent male who cares for big egg broods in his
mouth, and who would be sorely tempted to eat the whole brood if he was not
sustained by the trophic eggs [31]
– see filial cannibalism below. The male temporarily spits out his brood
to eat the trophic eggs.)
Several
cichlids from the genus Cichlasoma are known to fin-dig
(like the male catfish above they stir up gravel by vigorously rubbing their
belly and fins against it) and to turn leaves over when they are accompanied by
fry. Several lines of evidence suggest that this is a way for the parent to
turn up food for their young, at least in the case of fin-digging. First, parents fin-dig more than
non-parents. Second, parents with
larger broods fin-dig more. Third,
fin-digging rate increases as the brood gets older and hungrier. And fourth, young gather up near the
fin-digging parent and appear to feed actively on the stirred-up material.
Of
course, the possibility exists that fin-digging is not a means to provide food
for the young but rather a way to obtain food for the adult itself (after all,
parents, especially those that have been raising large broods for a long time,
are more likely to be hungry themselves).
However, Brian Wisenden and Tanya Lanfranconi-Izawa, working in the
field in Costa Rica as well as in Miles Keenleysides lab in Ontario, did not find
any correlation between the frequency of fin-digging and the number of feeding
bites taken by parental convict cichlids, suggesting that fin-digging was not
necessarily for the benefit of the parent.[32] On the other hand, Dmitry Zworykin,
from the Russian Academy of Sciences, found that Cichlasoma octofasciatum
parents fin-dug more when they were kept on low-food rations. Reconciling this
result with the notion of fry care, he suggested that parents use their own
level of hunger to estimate the need of their young.[33]
One
final way for parents to feed their young also concerns cichlids. In many cichlids such as discus, Midas
cichlid, angelfish, orange chromide, and others, fry can feed off the skin mucus
produced by their parents. [34] The number of visible mucus-producing
glands in the parents skin increases during the fry stage, and the young nip
at the body surface of both the mother and the father. The fry do more nibbling when they are
deprived of other sources of food, which shows that mucus is indeed a dietary
supplement (in discus, it is in fact more than just a supplement: mucus-feeding
appears to be essential for fry survival, even in the wild).
Fry
care: signalling danger to ones young
In
most parental fishes, fry care includes the signalling of danger to the
young. In Siamese
fighting fish for example, the parental male can communicate danger to his
young through surface waves. In
their first few days of independence from the air-bubble nest, young fighting
fish stay in contact with the surface – like most anabantids, they need
to breathe some air. The parental
male stays nearby and if he senses danger he shakes his pectoral fins close to
the surface. The surface wavelets
thus generated are perceived by the young at a distance of up to 40 cm (about a
foot and a half). The young then
swim in the direction of the source, and this action brings them close to the
male who can then suck them up into his buccal cavity and carry them back to
the nest.
In
cichlids, various visual displays seem to warn young in a similar fashion. A mad dashing-about by parents induces
the young to settle quickly to the bottom and remain still. Brief jerks of the head or twitches of
the whole body induce the fry to swarm near the parent. In mouthbrooding species, an alarmed
mother can pitch slightly head-down and swim slowly backwards, upon which the
fry quickly dash into her open mouth for safety.
Some
cichlids, when alarmed, signal their young by flickering their pelvic fins up
and down. At Illinois State University,
James Cole and Jack Ward used parent models to study this signalling behaviour
in orange chromides. Their models
featured a pelvic fin that could be made to bob up and down by pulling on a
string attached to it. They
offered fry a choice between two models, one that flickered versus one that did
not. By and large, the fry
preferred to gather near the model that flickered. More observations by Cole and Ward, this time on intact
broods with their parents, showed that parents flicker more when a small red
ball is swung near their aquarium, and that fry in response form a more compact
swarm.[35]
In
another study on convict cichlids, Michael Shennan, Joe Waas, and Robert Lavery
demonstrated that parents also flick more when they see other parents flickering. The researchers built balsa wood models
of convict cichlids. They mounted
these models on a cardboard background that concealed the experimenter, whose
role was to manually pivot a fake pelvic fin from behind. They placed models next to the tanks of
parental convict parents and either moved the pelvic fin (one flick/second for
30 seconds) or let the fin hang down.
Parents reacted by themselves flickering at a high rate in the presence
of the moving model; in contrast, while viewing the motionless model they
flickered very little.[36]
Fry
care: retrieving the young
Many
cichlids retrieve their fry when danger lurks. The parents suck 2-3 young at a
time into their mouth and bring them back to the old nesting site or to a safe
place where they spit them out. The fry then dart or sink towards the bottom,
where they stay relatively immobile. My convict cichlids do this regularly at
the end of the day. This ensures that by the time darkness comes, the young are
all gathered in one place over which the parents can stand guard all night
long. Dimming the light at the end of the day promotes the expression of this
behaviour, but mid-day dimming does not. However, complete darkness imposed at
midday does trigger retrieving, the parents somehow being able to find their
young and their way back to the gathering place in the dark – as I could
witness using infrared lighting and infrared goggles.[37]
Here
is an old anecdote reported by Konrad Lorenz, one of the founders of ethology,
in his 1952 book King Solomons Ring.[38]
Late one day, Lorenz came to feed a pair of jewel cichlids he was keeping in
his laboratory. That pair had just
finished retrieving their young for the night. The female was keeping watch over the pit full of fry, while
the male was dashing back and forth, looking for stragglers. Lorenz dropped a piece of earthworm
into the water. The female did not
flinch from her guarding post but the male rushed to the worm, seized it and
started chewing. Then he saw a
stray fry swimming by itself away from the pit. Bent on retrieving it, he took it in his already full
mouth... and then paused. What to
do? To eat or not to eat? To
retrieve or not to retrieve? Part
of the mouth content had to go to the nest, the other to the stomach. After a few moments, the father found a
solution: he spat out both the worm piece and the young. Both sank to the
bottom (as I mentioned earlier, heading down is an innate response of cichlid
fry being retrieved, and as for the meat, well, that was only gravity). Then the father ate the worm, taking
his time and watching the nearby fry.
When he was done, he took the fry in his mouth once again and brought it
back to its waiting mother.
Nearby
students watching the scene spontaneously broke out into applause.
Fry
care: brood mixing
It has
been observed, both in the lab and the field, that cichlid parents sometimes
guard swarms of fry that are made up of several sub-groups of different body
size. It seems that such parents
have accepted within their brood the young from other parents (the terms brood
adoption and brood mixing are sometimes used interchangeably). Indeed, it is relatively easy to
experimentally integrate foreign fry into the broods of cichlids kept in
aquaria. The parents accept these
new fry readily, provided that the newcomers are the same size or only slightly
smaller than their own young.
One of
the most thorough studies of this phenomenon has been carried out by Brian
Wisenden during his graduate studies in Miles Keenleysides lab.[39] Laudably, Wisenden worked on convict
cichlids in the field (very unusual given that convicts are so easy to keep and
breed in the lab). Within
stretches of small streams in Northwestern Costa Rica, Wisenden captured and marked
all parental convict cichlids he could find, and at regular intervals he
measured the size of their broods.
He observed that some broods suddenly increased in numbers while others
nearby suddenly decreased, and that smaller fry seemed to have been
incorporated into the new inflated broods, confirming the existence of
brood-mixing and brood adoption in this population. By hand, Wisenden also transferred some fry from one brood
to another. Nine times he released
fry that were bigger than those from the host parents, and every time the
parents ate up these new fry.
Sixteen times he released smaller fry, and every time the parents accepted the
newcomers. Wisenden therefore
showed that adoption is not a blind process, that parents have some say in the
matter, showing a tolerance only for smaller refugees.
Why
should parents accept small fry but not big ones? Indeed, why should they accept any fry at all? Maybe under some circumstances they
cannot tell fry apart. And then
again maybe there are specific advantages to adoption. Wisenden picked up an idea that had
been floating around for a long time: the host parents young might benefit
from a dilution effect when the brood is attacked by a predator. If a brood under attack was made up
entirely of a parents own young, then any success by the predator would
guarantee a lower reproductive success for the parent. If on the other hand the brood was
twice as big but only half of it belonged to the parent, then statistically the
chances for the parents young to be selected for attack would only be 50%. Better still, if the foreign young were
smaller and predators had an easier time capturing smaller and less mobile fry,
then the predator could specifically target the foreign young and leave the
host fry alone. Big pay-off for
the foster parents!
To
test this, Wisenden moved to the lab.
He unleashed natural predators (three juvenile convicts or one juvenile Guapote,
Parachromis dovii) onto broods of 20 fry, the body size of which varied
within the same broods. Looking at
the survivors after 15 minutes, Wisenden saw that the smallest fry had indeed
fallen prey to the predators more often than the largest ones.[40]
In
view of this, why would any convict parents wish to farm out their young, to
promote adoption of their young into a neighbouring brood? Wisenden proposed that if one of the
two parents disappeared, the remaining parent might have too much trouble
raising a brood on its own and might prefer to entrust the frys fate to intact
pairs nearby. Sure, the small
young might suffer differential predation in their new foster family, but
better that than sure death because of insufficient protection by a lone
parent. Back in the field,
Wisenden removed male parents from 21 pairs halfway through the fry stage
(males were removed instead of females because male convicts are known to
sometimes prematurely desert their family, especially if single and
ready-to-breed females are abundant in the vicinity). Of the 21 uniparental broods, in 8 cases the mother steered
the fry close to neighbouring groups and the fry were eventually integrated
within these groups. Of the 13 mothers who decided to raise the brood on their
own, only 5 saw their young survive. The other 8 disappeared, presumably at the
hands of predators. [41]
Longer
fry care in the presence of predators
The
duration of parental care at the fry stage is often dictated by the age of the
young, which after a while simply become too mobile for the parent(s) to watch
over. However, in mouthbrooding species, the parents have a more direct say on
when to end their duties. They can simply expel the young from their mouth and
refuse to take them back in. One such species has given evidence that it can
extend the duration of the incubation period if it perceives that risk of
predation on the fry would be high. In a laboratory experiment, females of the
mouthbrooding cichlid Ctenochromis horei kept young in
their mouth about 4 days longer (beyond a normal incubation period of 15-23
days) when they swam in the presence of another predatory cichlid (Lamprologus
callipterus). These species are both found in Lake Tanganyika.
This extra effort took a toll on the females: they could not feed during those
additional 4 days, and it took them longer to breed again, as compared to
females that were not exposed to the predators and that ended incubation
sooner.[42]
Filial
cannibalism
Parents
who face the spectre of weight loss through the reproductive phase can
counteract this effect with a rather uncaring behaviour: filial cannibalism
(eating ones own eggs or fry). Eggs
represent very nutritious little packages for a hungry fish. That is why egg predators are so
common. Of course, parents must
see their own eggs in a different light; for reproduction to make sense, hungry
parents must resist the temptation to eat their own brood. Most of them succeed in doing
this. But in many families
(cyprinodonts, gasterosteids, centrarchids, hexagrammids, cottids, cichlids,
pomacentrids, tripterygiids, blennids, belontiids), parents sometimes eat a
small part of their brood, and we are not talking about diseased eggs
here. Many of the consumed eggs
appear perfectly viable.[43]
To
test the idea that filial cannibalism is an adaptation to counter the
debilitating physical effects of parental care, an experimenter needs only give
supplemental food to hard-working parents. If parents eat their eggs to avoid starvation, then
cannibalism rates should decrease under conditions of plenty. Evidence of this kind has been obtained
in studies on Cortez damselfish (a field study where some parents were fed eggs
from other nests), a common goby (a lab study where the supplemental food was
mussel meat) and the scissortail sergeant (a field study using crabmeat and
eggs from other nests).[44] Annoyingly however, even the best-fed
individuals still ate a few of their own eggs in these studies. Moreover, in two other studies (one on
three-spined sticklebacks fed freeze-dried shrimp and one on fantail darters
fed earthworms) supplemental rations did not affect the probability nor the
extent of cannibalism.[45] Here we could object that the food
supplements may have lacked some essential nutrients that could only be
obtained from eggs. So, overall,
supplemental food experiments leave us with a rather muddy picture about the
adaptiveness of filial cannibalism.
Better
evidence may be gleaned from another direction: several fish observers have
noted a correlation between the physical condition of the parent and its
tendency to cannibalise. In
painted greenlings, river bullheads, bluegill sunfish, and the cardinal fish Apogon doederleini, the
more emaciated a parental male is, the more of the eggs under his care he
consumes.[46] However, this does not explain why even
males who are in very good condition still eat up a few eggs. A word of wisdom on this subject: there
may be an adaptive side to the behaviour of filial cannibalism, as suggested by
some of the results above, but we must also recognise the possibility, the one
that was favoured by earlier fish observers even though it was non-adaptive,
that cannibalising ones own eggs is a pathological breakdown in the normal
egg-eating inhibition shown by good parents. (The current fashion in animal
behaviour research is to favour adaptive explanation of behaviour over
non-adaptive ones, but this does not mean that the latter should be
overlooked.)
In the
late 1980s and early 1990s, the scientific literature saw a burst of
publications on the topic of brood value.
This was the idea that parents should be careful in how they award
parental effort toward their progeny.
In particular, because the business of looking after young is so costly
in terms of energy, there was a risk for a parent to devote too much care to a
current brood at the expense of its potential for future reproduction. If a parent was stuck with a small
brood, it might consider limiting the energy invested into the care of such a
low-yield evolutionary prospect, and instead save itself for better attempts in
the future. All of these ideas
came under the banner of parental investment theory. Many of the published articles
supported the notion that parents could adjust their level of care as a
function of the value of their brood.
We saw
earlier that parents sometimes eat part of their brood as an insurance against
starvation. In some cases however,
it is the whole brood that is devoured.
This seems a bit extreme just to fend off starvation! Ethologists now consider that total brood
cannibalism is a manifestation of parental investment theory. The parents eliminate a poor brood
(which represents a low return on their parental investment) so as to be able
to start a new and improved breeding attempt as soon as possible. Confirming this view, observations in many
species have revealed that only small broods are the
victim of total cannibalism. Large
(and therefore more valuable) broods are left intact or only partially
cannibalised.[47]
With a
more experimental touch, Robert Lavery removed eggs from the nest of various
pairs of convict cichlids he was keeping in Miles Keenleysides lab. The diminished broods were 33%, 66% or
100% (untouched control) of their former size. More pairs (6-8 out of 10) consumed what was left of their
brood in the 33% and 66% treatment than in the control 100% situation (only 2
pairs out of 10). And those
parents who resigned themselves to the care of reduced broods did so only
half-heartedly: as compared to the controls, they performed fewer parental
acts, and the ovary weight of the females turned out to be higher at the end of
the experiment, indicating that they had been secretly preparing for a future
reproductive attempt rather than taking good care of the current, low-yield
brood.[48]
Lavery
conducted another experiment on convicts.
He halved or doubled some broods by transferring wrigglers or fry from
one brood to another, taking advantage of the fact that parental cichlid
readily accept foreign fry if those fry are of the same size as their own. He measured parental behaviour such as
the percentage of time spent near the brood, the frequency of retrieving young,
and the intensity of attack on a predator model (which was moved in the water
through an attachment to a toy car running on a portable track resting on top
of the aquaria). Lavery observed
that parental behaviours were more pronounced in the brood-augmented condition
than in the brood-reduced one, lending credence to the theory of parental
investment.[49]
Lavery
was at it again a few years later, still with convicts but this time in Patrick
Colgans lab at Queens University in Kingston, Ontario. He measured parental response to a
predator model for various broods of similar size but at different stages of
development: eggs, wrigglers, and fry.
He found that parents gave more and more protection to their brood as
the young grew from egg to wriggler to fry. This showed that parents view
younger broods as less valuable.
The rationale here is that younger broods are less valuable because
there is still time in the reproductive season to initiate a new attempt, and
energy reserves are still high at that time. With older broods, parents may be too weak, and the season
may be too advanced to start anew.
The old brood may therefore represent the only chance the parents will
have, for a while anyway, to propagate their genes in the next generation, and
the value of this old brood is therefore raised.[50]
Here
is another variation to show that parental investment theory is a rich field
for study. We are back with Brian
Wisenden, still with convict cichlids.
In the lab, Wisenden required his convicts to lay eggs in either a
secure spawning cave (an overturned flowerpot with only one small triangular
opening at the rim) or a risky one (an overturned flower pot again, but with
two large openings). The risk
stemmed from an inability to defend both openings simultaneously against egg
predators. Wisenden counted the
number of eggs laid in each type of cave by various females, and he found that
fewer eggs were entrusted to the protection of risky caves. It was as if the females knew that the
nest was less secure, sensed that the eggs ran a higher risk of perishing, and
did not dare invest too many eggs in this risky venture, preferring perhaps to
keep some energy in reserve (eggs can be reabsorbed) for a future attempt in a
hopefully more secure site the next time around.[51]
Ron
Coleman is also a long-time student of parental investment theory in fishes,
having conducted several tests with bluegill sunfish.[52] Switching to convict cichlids, he and
Alison Galvani went back to the idea that smaller broods hold less value in the
eyes of their parents, and asked: well, what kind of parents? Would size of the parents matter? Would a small brood have the same value
for a small parent as it does for a larger one? For a small female that cannot lay more than 200 eggs at the
best of time, a brood reduced to 100 can still have a fair amount of residual
value, as compared to a large female who can lay as many as 500 eggs. Galvani and Coleman uniformly reduced
the egg batches of small and large female convict cichlids down to 100 by
scraping eggs off the flowerpot on which they had been laid. This represented a relatively more
extensive reduction for the larger females. Six days later, at the fry stage, the model of a tiger
tilapia was moved through the tank, and the number of bites directed at it by
the female was recorded. As
compared to their larger counterparts, smaller females were fiercer and bit the
predator model more, even though the predator probably appeared larger to
them. So, brood value is a
relative thing; it is in the eye of the beholder. Female convict cichlids of different sizes do not value the
same brood number equally. For a
small female, investing in a small brood is not such a bad thing after all.[53]
In
species where cuckolder males are present in the population (see page on the sex
lives of fishes), there is a chance that some of the young under a males care might
not be his. In such a case, what may matter most for parental adjustment is not
brood size, but rather effective brood size, that is, the percentage of the
brood made up of the males own progeny. One may therefore predict that males
would give less care to their brood if they can perceive that they have been
cuckolded. Bluegill sunfish can provide a test of this idea. Males of this
species fan and defend their eggs until they hatch (2-3 days) and protect the
fry from predators until they leave the nest (5-7 days). Care is costly: the
parental males do not feed and they lose about 10 % of their body weight.
Unfortunately for them, other small males are cuckolders and steal
fertilizations. Parents can estimate the risk of cuckoldry from simply seeing small
males in the vicinity of their nest on spawning day, and they can also estimate
how much of their brood at the fry stage is made up of illegitimate offspring
from their different smell.[54]
Research by Brian Neff has shown that parents can indeed adjust their level of
care according to their perceived paternity.[55]
Working
in the field, Neff selected the nests of males that were about to spawn, and he
surrounded those nests with 4 bottles that each contained a small male. This
simulated a risk of being cuckolded. Control nests were surrounded by empty
bottles. The bottles were removed at the end of the spawning day, and the next
day the nest owners parental fervour was tested by pushing towards them a
bottle containing an egg and fry predator (a pumpkinseed sunfish). Neff
observed that the males which had been exposed to potential cuckolders directed
fewer displays and delivered fewer bites to the predator as compared to the
controls, in line with what the theory predicted. He repeated the predator
presentation at the fry stage, and now the treatment males defended their brood
just as much as the controls, presumably because the parents could now see
(well, smell) that they had not in fact been cuckolded and that the whole brood
was theirs.
In
another part of the bluegill colonies, Neff swapped eggs (about a third of each
brood) between nests. He predicted that the level of parental care would remain
the same at the egg stage (since bluegill cannot distinguish between own and
foreign eggs) but that the artificially cuckolded males would be less parental
at the fry stage, now that they could recognize the foreign young from their
different odour. This is indeed what he observed, once again based on the
response of males to a predator presentation.
Something
similar happens in Telmatherina sarasinorum, a small fish
found in Lake Matano in Indonesia. Increased risk of cuckoldry leads to increased
rates of brood cannibalism by the father. It must be said, however, that this
species is not parental. The eggs are eaten soon after mating. [56]
--------------------------------------
[1]
Keenleyside, M.H.A., 1979, Diversity and Adaptation in Fish Behaviour,
Springer-Verlag, Berlin. For some reviews of parental care in fishes, see also:
Blumer, L.S., 1979, Male parental care in the bony fishes, Quarterly Review of
Biology 54, 149-161; Baylis, 1981, The evolution of parental care in fishes,
with reference to Darwins rule of male sexual selection, Environmental Biology
of Fishes 6, 223-251; Perrone, M. Jr., and Zaret, T.M., 1979, Parental care
patterns of fishes, American Naturalist 113, 351-361.
[2]
Fricke, H.W., 1980, Mating systems, maternal and biparental care in triggerfish
(Balistidae), Zeitschrift fr Tierpsychologie 53, 105-122.
[3]
Knouft, J.H., Page, L.M., and Plewa, M.J., 2003, Antimicrobial egg cleaning by
the fringed darter (Perciformes: Percidae: Etheostoma crossopterum):
Implications of a novel component of parental care in fishes, Proceedings of
the Royal Society of London B 270: 2405-2411; Giacomello, E., Marchini, D., and
Rasotto, M.B., 2006, A male sexually dimorphic trait provides antimicrobials to
eggs in blenny fish, Biology Letters 2, 330-333.
[4]
Keenleyside, M.H.A., 1978, Parental care behavior in fishes and birds, Pp. 3-29
In Contrasts in Behavior (Reese, E.S., and Lighter, F.J., eds.), John Wiley
& Sons, New York. For another
example with convict cichlids, see: Keenleyside, M.H.A., Bailey, R.C., and
Young, V.H., 1990, Variation in the mating system and associated parental
behaviour of captive and free-living Cichlasoma nigrofasciatum
(Pisces, Cichlidae), Behaviour 112, 202-221. Biparental care has given rise to
a number of studies about the division of labour between the sexes, and how
flexible gender roles are when it comes to parental care. For a flavour, see:
Mrowka, W., 1982, Effect of removal of mate on parental care behaviour of the
biparental cichlid Aequidens paraguayensis, Animal
Behaviour 30, 295-297; Lavery, R.J., and Reebs, S.G., 1994, Effect of mate
removal on current and subsequent parental care in the convict cichlid (Pisces:
Cichlidae), Ethology 97, 265-277; Itzkowitz, M., Santangelo, N., and Richter,
M., 2001, Parental division of labour and the shift from minimal to maximal
role specializations: an examination using a biparental fish, Animal Behaviour
61, 1237-1245; Itzkowitz, M., Santangelo, N., Cleveland, A., Bockelman, A., and
Richter, M., 2005, Is the selection of sex-typical parental roles based on an
assessment process? A test in the monogamous convict cichlid fish, Animal
Behaviour 69, 95-105.
[5]
Brouwer, L., Heg, D., and Taborsky, M., 2005, Experimental evidence for helper
effects in a cooperatively breeding cichlid, Behavioral Ecology and
Sociobiology 16, 667-673.
[6]
Taborsky, M., 1985, Breeder-helper conflict in a cichlid fish with broodcare
helpers: an experimental analysis, Behaviour 95, 45-75.
[7]
Taborsky, M., 1984, Broodcare helpers in the cichlid fish Lamprologus
brichardi: their costs and benefits, Animal Behaviour 32,
1236-1252; Balshine-Earn, S., Neat, F.C., Reid, Hannah, and Taborsky, M., 1998,
Paying to stay or paying to breed? Field evidence for direct benefits of
helping behavior in a cooperatively breeding fish, Behavioral Ecology 9,
432-438.
[8]
Dierkes, P., Taborsky, M., and Kohler, U., 1999, Reproductive parasitism of
broodcare helpers in a cooperatively breeding fish, Behavioral Ecology 10,
510-515.
[9] For
one such instance, see: Grter, C., and Taborsky, B., 2004, Mouthbrooding and
biparental care: an unexpected combination, but male brood care pays, Animal
Behaviour 68: 1283-1289, and references therein.
[10]
Sabat, A.M., 1994, Costs and benefits of parental effort in a brood-guarding
fish (Ambloplites rupestris, Centrarchidae), Behavioral Ecology 5, 195-201, and
references therein.
[11] For
example: FitzGerald, G.J., Guderley, H., and Picard, P., 1989, Hidden
reproductive costs in the three-spine stickleback (Gasterosteus aculeatus),
Experimental Biology 48, 295-300; Chellappa, S., Huntingford, F.A., Strang,
R.H.C., and Thomson, R.Y., 1989, Annual variation in energy reserves in male
three-spined stickleback, Gasterosteus aculeatus L. (Pisces,
Gasterosteidae), Journal of Fish Biology 35, 275-286; Lindstrm, K., and
Hellstrm, M., 1993, Male size and parental care in the sand goby, Pomatoschistus
minutus, Ethology Ecology & Evolution 5, 97-106; Balshine-Earn,
S., 1995, The costs of parental care in Galilee St Peters fish, Sarotherodon
galileus, Animal Behaviour 50, 1-7; Gillooly, J.F., and
Baylis, J.R., 1999, Reproductive success and the energetic cost of parental
care in male smallmouth bass, Journal of Fish Biology 54, 573-584; Steinhart,
G.B., Sandrene, M.E., Weaver, S., Stein, R.A., and Marschall, E.A., 2005,
Increased parental care cost for nest-guarding fish in a lake with
hyperabundant nest predators, Behavioral Ecology 16, 427-434.
[12] De
Fraipont, M., Fitzgerald, G.J., and Guderley, H., 1992, Femme fatale –
the case of the threespine stickleback, Ethology 91, 147-152.
[13] Van
Iersel, J.J.A., 1953, An analysis of parental behaviour of the male
three-spines stickleback (Gasterosteus aculeatus L.), Behaviour
Supplement 3, 1-159.
[14]
Sargent, R.C., 1985, Territoriality and reproductive tradeoffs in the
threespine stickleback, Gasterosteus aculeatus, Behaviour 93,
217-226.
[15]
Keenleyside, M.H.A., and Prince, C., 1976, Spawning-site selection in relation
to parental care of eggs in Aequidens paraguayensis
(Pisces: Cichlidae), Canadian Journal of Zoology 54, 2135-2139.
[16] Gerry
FitzGerald has proposed three possible explanations for why female sticklebacks
raid nests. They could do so to
(1) force the male to renest so that they could mate with him, (2) decrease the
number of competitors for their own offspring, and (3) obtain essential
nutrients for the manufacture of their own eggs. Some supportive evidence was obtained for all three
hypotheses. FitzGerald, G.J., and
van Havre, N., 1987, The adaptive significance of cannibalism in sticklebacks
(Gasterosteidae: Pisces), Behavioral Ecology and Sociobiology 20, 125-128;
FitzGerald, G.J., 1992, Egg cannibalism by sticklebacks: spite or selfishness?
Behavioral Ecology and Sociobiology 30, 201-206; Belles-Isles, J.-C., and
FitzGerald, G.J., 1993, A fitness advantage of cannibalism in female
sticklebacks (Gasterosteus aculeatus L.), Ethology
Ecology & Evolution 5, 187-191.
[17]
Whoriskey, F.G., 1991, Stickleback distraction displays: sexual or foraging
deception against egg cannibalism? Animal Behaviour 41, 989-995; Foster, S.A., 1988,
Diversionary displays of paternal stickleback: Defenses against cannibalistic
groups, Behavioral Ecology and Sociobiology 22, 335-340; Ridgway, M.S., and
McPhail, J.D., 1988, Raiding shoal size and a distraction display in male
sticklebacks, Canadian Journal of Zoology 66, 201-205.
[18] Page
89 in: Morris, D., 1990, Animal watching: a field guide to animal behaviour,
Jonathan Cape, London.
[19] For a
review, see: Wisenden, B.D., 1999, Alloparental care in fishes, Reviews in Fish
Biology and Fisheries 9, 45-70.
[20] For a
review, see: Taborsky, M., 1994, Sneakers, satellites, and helpers: parasitic
and cooperative behavior in fish reproduction, Pp. 1-100 In Advances in the
Study of Behavior, Vol. 23 (Slater, P.J.B., Rosenblatt, J.S., Snowdon, C.T.,
and Milinski, M., eds.), Academic Press, San Diego. For more recent papers, see: Shao, B., 1997, Nest
association of pumpkinseed, Lepomis gibbosus, and golden
shiner, Notemigonus crysoleucas, Environmental Biology of Fishes
50, 41-48; Ochi, H., Onchi, T., and Yanagisawa, Y., 2001, Alloparental care
between catfishes in Lake Tanganyika, Journal of Fish Biology 59, 1279-1286.
[21]
Katula, R.S., and Page, L.M., 1998, Nest association between a large predator,
the bowfin (Amia calva), and its prey, the golden shiner (Notemigonus
crysoleucas), Copeia 1998, 220-221; Kramer, R.H., and Smith, L.L.
Jr., 1960, Utilization of nests of largemouth bass, Micropterus salmoides, by
golden shiners, Notemigonus crysoleucas, Copeia 1960, 73-74.
[22] Here
is an exception: In Japan, the minnow Pungtungia herzi tries
to spawn in the nest of the freshwater perch Siniperca kawamebari. The
latter tries to prevent this, but sometimes it just gets swamped by too many
minnows. Within the mass of minnows lurks an intruder, the chub Zacco
temmincki. This fish eats some of the eggs within the nest, and
consequently the perchs nests that are parasitized often end up with a lower
reproductive success. See: Baba, R., Nagata, Y., and Yamagishi, S., 1990, Brood
parasitism and egg robbing among three freshwater fish, Animal Behaviour 40,
776-778. For more on this system: Baba, 1994, Timing of spawning and host-nest
choice for brood parasitism by the Japanese minnow, Pungtungia herzi, on
the Japanese Aucha perch, Siniperca kawamebari, Ethology 98,
50-59.
[23]
Johnston, C.E., 1994, Nest association in fishes: evidence for mutualism,
Behavioral Ecology and Sociobiology 35, 379-383; Shao, B., 1997, Effects of
golden shiner (Notemigonus crysoleucas) nest
association on host pumpkinseeds (Lepomis gibbosus):
evidence for a non-parasitic relationship, Behavioral Ecology and Sociobiology
41, 399-406. For experimental
evidence that the minnows also benefit (from protection given by the host
parent), see: Johnston, C.E., 1994, The benefit to some minnows of spawning in
the nests of other species, Environmental Biology of Fishes 40, 213-218.
[24] Sato,
T., 1986, A brood parasitic catfish of mouthbrooding cichlid fishes in Lake
Tanganyika, Nature 323, 58-59.
[25] Van
der Berghe, E.P., 1988, Piracy as an alternative reproductive tactic for males,
Nature 334, 697-698.
[26]
Unger, L.M., and Sargent, R.C., 1988, Allopaternal care in the fathead minnow, Pimephales promelas:
females prefer males with eggs, Behavioral Ecology and Sociobiology 23, 27-32; Sargent,
R.C., 1989, Allopaternal care in the fathead minnow, Pimephales promelas:
stepfathers discriminate against their adopted eggs, Behavioral Ecology and
Sociobiology 25, 379-385. For a
list of similar examples in many other fish families, see: Taborsky, M., 1994,
Sneakers, satellites, and helpers: parasitic and cooperative behavior in fish
reproduction, pp. 1-100 In Advances in the Study of Behavior,
Vol. 23 (Slater, P.J.B., Rosenblatt, J.S., Snowdon, C.T., and Milinski, M.,
eds.), Academic Press, San Diego; as well as: Bandoli, J.H., 2002, Brood
defense and filial cannibalism in the spottail darter (Etheostoma squamiceps): the
effects of parental status and prior experience, Behavioral Ecology and
Sociobiology 51, 222-226.
[27] Li,
S.K., and Owings, D.H., 1978, Sexual selection in the three-spined stickleback.
II. Nest raiding during the courtship phase, Behaviour 64, 298-304. Largiadr, C.R., Fries, V., and Bakker,
T.C.M., 2001, Genetic analysis of sneaking and egg-thievery in a natural
population of the three-spined stickleback (Gasterosteus aculeatus L.),
Heredity 86, 459-468. Egg stealing
has also been observed in a mouthbrooding cichlid and is harder to interpret:
Mrowka, W., 1987, Egg stealing in a mouthbrooding cichlid fish, Animal
Behaviour 35, 923-925.
[28]
However, in fifteen-spined sticklebacks, egg-stealing exists but females do not
seem to prefer males with more eggs in their nest: stlund-Nilsson, S., 2002,
Does paternity or paternal investment determine the level of paternal care and
does female choice explain egg stealing in the fifteen-spined stickleback?
Behavioral Ecology 13, 188-192.
[29]
Daniels, R.A., 1979, Nest guard replacement in the Antarctic fish Harpager
bispinis: possible altruistic behavior, Science 205, 831-833.
[30]
McKaye, K.R., 1986, Trophic eggs and parental foraging for young by the catfish
Bagrus meridionalis of Lake Malawi, Africa, Oecologia 69, 367-369; LoVullo,
T.J., and Stauffer, J.R. Jr., 1992, Diet and growth of a brood of Bagrus
meridionalis Gnther (Siluriformes: Bagridae) in Lake Malawi,
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