Behavioral Ecology Vol. 12 No. 3: 369-373
© 2001 International Society for Behavioral Ecology
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Egg carrying in the golden egg bug (Phyllomorpha laciniata): parental care, parasitism, or both? Reply to Kaitala et al.
Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales (C.S.I.C.), José Gutiérrez Abascal 2, 28006 Madrid, Spain
Address correspondence to M. Gomendio. E-mail: montseg{at}mncn.csic.es .
Received 15 August 2000; revised 15 September 2000; Female golden egg bugs follow a flexible oviposition strategy because they lay eggs on other conspecifics (male and female) and on the host plant (Paronychia argentea). In natural populations a much higher proportion of males than females carry eggs and, among egg carrying adults, males carry more eggs than do females (see below). Females cannot lay eggs on themselves, so egg carrying females are always carrying other females' eggs. It is less clear whether males carry their own offspring, other males' offspring, or a combination of both. This has generated a controversy about whether egg carrying by males is a form of parental care, a case of intra-specific parasitism, or a combination of both.
Kaitala et al. (2001
, this
issue) criticize our use of term "parental care" in relation to
male egg-carrying in this species in a previous article
(Reguera and Gomendio, 1999).
Their comments raise a general question in relation to the concept of
"parental care," and more specific points that are also worth
addressing.
Parental care has been defined as any form of parental behavior that
appears likely to increase the fitness of the offspring
(Clutton-Brock, 1991).
Phyllomorpha laciniata can be considered as a model organism in which
three types of individuals play different roles in relation to egg carrying:
the laying female, the male who accepts/rejects the eggs, and the female who
accepts/rejects the eggs. Individuals in each of these roles have different
interests and face a different balance of costs and benefits. Thus, it is
worth considering each separately.
The laying female
The main focus of our studies on Phyllomorpha laciniata has been a
natural population in Villaviciosa de Odón
(Madrid) which we have followed for 5 years. In this population, all
individuals are marked and observations are made weekly during the whole
active season (for details see Reguera,
1999). Adults from the previous year become active around March
(depending on weather conditions) and remain active until August, when the
host plant (Paronychia argentea) becomes dry. In addition, we have
carried out a comparative study with another natural population under very
different ecological conditions in Almeria (southern Spain). Finally,
individuals from different populations in the region of Madrid have been used
to carry out experiments both in the field and in the laboratory (facilities
at the Museo Nacional de Ciencias Naturales).
In all the populations that we have studied, females lay eggs both on
plants and on adult bugs. When an egg is laid it is covered by a sticky
substance that glues the egg firmly to any surface on which it is laid,
irrespective of whether it is an adult bug or a plant. This substance dries
quickly after oviposition, so eggs removed from the original surface on which
they were laid no longer have the ability to become attached to a new surface.
While eggs attached to the backs of conspecifics are clearly visible (see
Reguera and Gomendio, 1999),
eggs laid on plants are in most cases placed in the inflorescence where they
are very difficult to detect (Figure
1a,b). This suggests that egg morphology is designed to make it
cryptic on flowers, where survival rates are low
(Reguera and Gomendio, 1999).
Thus, eggs on plants can easily be overlooked, and it is necessary to take the
plants to the lab and carefully search under the dissecting microscope to be
certain that all eggs have been detected. For this reason, we have not been
able to quantify so far the proportion of eggs laid on plants versus adults in
the field. Kaitala et al.
(2001) argue that eggs on host
plants are not common and that "eggs found on host plants are not a
sufficient evidence of female oviposition strategy because eggs on host plant
might be ones that are scraped off by the bugs." This is certainly not
the case in the populations studied by us, since eggs found on plants in the
field are glued to the plant (eggs "scraped off" from the back of
an adult would no longer become glued to the plant), and in the laboratory we
have often observed females laying eggs on plants.
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A more plausible explanation is that the number of eggs that are laid on
plants differ between populations. This hypothesis is supported by the results
of our own experiments which show that around 60% of eggs are laid on plants
when adult density is low (four adults in a 29 x 51 x 32 cm
enclosure), while this proportion decreases to around 20% when adult density
is high (four adults in an 18 x 18 x 10 cm enclosure)
(Reguera, 1999). Thus, a
greater proportion of eggs are laid on plants when bug density is low, due to
the decrease in encounter rates between reproductive females and other adults.
We have reviewed all the publications by Kaitala and colleagues to find out
under which conditions were their results obtained in an effort to explain
these striking differences in rather basic patterns of behavior. In most
articles (Kaitala, 1996,
1998,
1999;
Kaitala and Axen, 2000;
Kaitala and Miettinen, 1997)
it is described that large numbers of bugs were collected during a few days on
different years from a number of localities in Spain and France and taken to
the laboratories where experiments were conducted. There is only published
information on two experiments carried out in the field: (1) in Kaitala
(1996) an experiment on egg
survival is described which lasted for 8 days; (2) in the last article
(Kaitala et al., 2000) an
experiment which also lasted for a few days was carried out in enclosures in
the field specifically to look at the effect of ant predation. There is no
indication that systematic observations have been made on natural populations,
and no reference is made to how much effort has been put into looking for eggs
on plants. Until this aspect is clarified the possibility remains that
observations carried out in the laboratory with high densities of individuals
have led to very few eggs being laid on plants. If this is the case, the low
numbers of eggs detected on plants by Kaitala et al. should be interpreted as
the result of the particular circumstances under which the experiments were
carried out in the laboratory and not as a common pattern in natural
populations.
The choice of the best possible oviposition site could be regarded as a
form of parental care (however rudimentary) provided it increases the survival
of offspring. Thus, females should try to lay the eggs where survival of the
offspring is likely to be highest. Our results also differ from those coming
from Kaitala's group in this respect. There are two main causes of egg
mortality: predation (mainly by ants) and a parasitoid wasp (Gryon
bolivary), and both act on eggs laid on plants and on eggs laid on adults
but with different intensities. We have carried out experiments in the field
that show that egg survival is higher when eggs are carried by an adult than
on plants (Reguera, 1999).
This explains why females respond to an increase in bug densities by
increasing the proportion of eggs laid on adults, and suggests that females do
prefer to lay eggs on adults, as long as they can find them and as long as
those adults accept them. Kaitala has argued in several articles that eggs do
not survive on plants in the field due to predation (Kaitala,
1996,
1999;
Kaitala and Axen, 2000; Kaitala
et al., 2000,
2001). This often cited
conclusion derives from an experiment that she describes as follows: "I
removed the eggs from the backs of the bugs, and placed them in the
inflorescence of the host plants (Paronychia sp.), three eggs in each
inflorescence. These branches with inflorescences were placed in the middle of
other plants in their original sites...."
(Kaitala, 1996: 383). The
result was that after 6 days all the eggs had "disappeared" and it
is concluded that the cause was predation. As we have already explained when
eggs are experimentally removed from the backs of adults, they have already
lost their stickiness and no longer become attached to the new surface where
they are placed. We tried to follow the same experimental approach and found
that eggs fell to the ground as soon as the plant experienced any movement, or
were blown away by the wind. Thus, such "disappearances" are just
that, and these data cannot be used to extrapolate to mortality rates of eggs
laid on plants by females.
In any case, it seems clear that survival on plants is lower than on adults, leaving the question open as to why do females lay eggs on plants at all. The answer is likely to be related to a number of factors such as encounter rates with other adults, willingness by other adults to accept the eggs, and differences between populations in predation pressure and parasitoid pressure (which are the main causes of egg mortality). These hypotheses will have to await further data to be tested. However, it is worth emphasizing that females lay one-two eggs every 3-5 days over the whole breeding season (which in our main study population lasts for 6 months), and thus each egg represents a small proportion of a female's lifetime reproductive success. In this context, each decision about where to oviposit a single egg must be balanced against the costs of looking for the optimal site and the consequent decrease in fecundity.
From the point of view of the female who looks for an oviposition site, it is in her interest to try to lay the next egg on the back of an adult, but she would not benefit from discriminating between males and females, or between the father and other (unrelated) males. This is because once the eggs are glued to the back of an adult there is no apparent active care from the carrier, so there seem to be no differences in the quality of care provided by the different potential carriers.
The male recipient
In order to decide whether egg-carrying by male golden egg bugs is a form
of parental care, the first step would be to find out whether the eggs have
been fathered by the male who carries them. The only direct evidence available
comes from the DNA analyses carried out by Kaitala and Miettinen, which are
mentioned in several articles as providing evidence that "some" of
the eggs carried by males are their own offspring (see
Kaitala and Miettinen, 1997;
Kaitala et al., 2000,
2001). No data whatsoever are
provided, so it is difficult to judge how robust these results are. However,
if we assume that these results are valid, we then have to accept that males
do carry "some" of their offspring. Therefore, the question is not
whether males look after their offspring, but rather what proportion of the
eggs should belong to the male carrier for us to conclude that it is a form of
parental care. This issue raises an interesting debate. In many bird and fish
species multiple mating by females and/or intraspecific parasitism result in
males looking after broods in which only a proportion of the juveniles are the
male's offspring (e.g., Davies et al.,
1992; Forsgren et al.,
1996; see reviews in
Clutton-Brock, 1991). Is it
possible to find a threshold (in terms of proportion of true genetic
offspring) below which males should not be considered to be engaged in
paternal care? Or should we accept that as long as males have chances of
looking after their own offspring the behavior should be termed paternal
care?
Several theoretical models have explored the relationship between
confidence of paternity or parentage and paternal care, and have shown that
variables such as the male's ability to discriminate between its own and
unrelated offspring, mean parentage between different matings, the magnitude
of the costs for males, and the magnitude of the effect on offspring survival,
influence levels of paternal care (e.g.,
Westneat and Sherman, 1993;
Whittingham et al., 1992). The
most important benefit for males would be to increase their offspring survival
and, as we have already seen, males seem to carry some of their own offspring
and eggs carried by adults experience a marked increase in survival rates.
However, males can also benefit in other ways, as in species in which caring
males increase their attractiveness to females (e.g.,
Jamieson and Colgan, 1989;
review in Jennions and Petrie,
1997). So far the evidence is contradictory, since the results of
experiments show that golden egg bug females do not prefer males with eggs
over males without eggs (Kaitala,
1998), but it has also been reported males captured while mating
had more eggs on their backs than single males
(Kaitala, 1996).
The costs of providing such care should also be considered, since
individuals should be less likely to care for offspring who are not their own,
when costs are high. It has already been shown that adults carrying eggs are
more likely to be preyed upon by birds than those who do not
(Reguera and Gomendio, 1999).
In addition, experiments in the laboratory show that Formica rufa
"attacked" bugs carrying eggs more often than adults without eggs,
but it is not possible to separate attacks on adults from attacks on the eggs
carried by them, since only one adult was killed by ants
(Kaitala and Axen, 2000). In an
experiment carried out in the field, individuals placed around the entrance of
ant nests (Pheidole pallidula) were more likely to disappear if they
carried many eggs when released (Kaitala
et al., 2000). However, the authors explain that "the tip of
one flight wing was cut from P. laciniata individuals with no or only
a few eggs" (Kaitala et al.,
2000: 255) an experimental manipulation which is likely to have
eliminated any differences in locomotor performance between egg carrying and
non-egg carrying adults. Apparently, egg carrying also increases the risk of
predation by chicken (cited in Kaitala et
al., 2001) but the evolutionary significance of this result is
unclear. Together all this evidence suggests that egg carrying conveys
important survival costs for adult golden egg bugs, which may be the result of
an increase in visibility of the bug or a decrease in its ability to escape,
or both. Such high costs associated with egg carrying make it unlikely that
males would only carry unrelated eggs.
This would, of course, depend on whether males can prevent females from
laying eggs on their backs, or whether they can get rid of them once the eggs
are laid. Females tend to lay most eggs on the backs of other adults, where
they remain attached to the wings. In order to lay an egg on another
bu
s back, a female must climb on top of the
other adult, position itself, and lay the egg while standing on top of the
other adult. This takes some time (up to several minutes) and, although we
have observed a few cases in which females seemed to be trying to climb on top
of an unwilling individual, in most instances the potential recipients either
just move away from the female who initiates an attempt to climb or they allow
females to lay eggs with no sign of resistance. Thus, individuals seem to be
able to chose whether they accept or reject the egg laying attempts, although
in some instances females seem to try to force unwilling individuals into
accepting their eggs, most often with little success. In several papers by
Kaitala's group it is stated that individuals accept eggs "voluntarily
and involuntarily" suggesting that they also reach the same conclusion.
However, it has been argued by Kaitala's group that females are most likely to
lay eggs on copulating individuals, since they may be unable to avoid egg
laying under these circumstances. Although some cases of egg laying may occur
under such conditions, it seems unlikely as a general explanation since it
fails to explain why a high proportion of males carry eggs, while very few
females do (see below). When a male and a female are engaged in copulation
neither can resist the attempts of an egg laying female, so if this were a
situation commonly used by egg laying females to accomplish egg laying, male
and female bugs should carry eggs at similar rates.
Kaitala (1999) has also
suggested that individuals get rid of the eggs after they are laid on them,
and this has been interpreted as a counterstrategy to parasitism. The first
description of such behavior can be found in Kaitala
(1996) where it is claimed that
"in the laboratory some individuals actively rubbed off eggs from their
backs." In a more recent article by Kaitala
(1999) the description of this
behavior is "egg-carrying individuals actively brush their backs against
the host plant seemingly in an effort to rub off eggs." In these two
articles it is concluded that egg scraping explains egg loss in nature. We
must admit that we have not seen a single instance of this behavior, neither
in our longitudinal study in the field nor in the experiments carried out in
the lab. It seems surprising that "egg-discarding" could become
widespread since eggs become firmly glued to the backs (most of them to the
wings), it is extremely difficult to remove the eggs, and experimental egg
removal often causes irreversible damage to the bug (generally to the wings
which are critical for flying when the bug is attacked). The difficulty in
removing the eggs is also acknowledged in most of Kaitala's articles, so our
populations do not seem to differ in this respect, and thus
"egg-discarding" would be difficult to achieve by "brushing
the backs against the host plant" and would involve high costs in terms
of risk of injury. In the discussion of Kaitala
(1999) reference is made to the
fact that belostomatids only kick off eggs when stressed under laboratory
conditions (Smith, 1976), an
explanation which may also apply in this case. Another possible explanation
may be related to the fact that in the laboratory individuals tend to end up
with a much larger number of eggs than under natural conditions, due to the
limited space available and increased encounter rates. While in our main study
population the average number of eggs carried by males in four, Kaitala
mentions that males used in her experiments may carry up to 28 eggs
(Kaitala and Miettinen, 1997;
Kaitala et al., 2001). Thus,
egg discarding may occur under rather artificial lab conditions, where the
number of eggs carried is far higher than those reached in natural
populations, and where the presence of several layers of eggs implies that
eggs on the top are glued to each other and not to the bug's body; thus it may
be easier to discard them and not incur injury. This interpretation is
supported by the fact that in Kaitala's study 65% of individuals carrying five
or more eggs rubbed off eggs. In any case, the conclusion that in the field
"eggs are more likely to disappear from an individual's back through the
active attempts of individuals to discard them rather than through
predation" (Kaitala,
1996: 387) seems unfounded since egg-discarding has not been
observed in natural populations, and ants are known to take eggs from the
backs of bugs (Kaitala et al.,
2000; Reguera,
1999).
In summary, from the point of view of the male receiver, although it is
difficult and costly for individuals to get rid of eggs once they are glued to
their backs, they are able to prevent eggs from being laid on them. Thus,
given that the costs, in terms of increased predation risks, are high, it is
reasonable to expect that male acceptance of eggs would only spread in a
population if there are chances that at least some of the eggs on their backs
will belong to them. In this scenario, males should try to ensure paternity,
and the long duration of copulations observed in this species (mean = 32 h;
Reguera, 1999) could well be a
strategy to try to ensure fertilization of the next egg and thus to increase
the chances that eggs accepted after long copulations belong to the male. More
data are needed to test these hypotheses.
The female recipient
Female golden egg bugs cannot lay eggs on themselves, so females never carry their own eggs. This raises two questions: (1) if females never carry their own eggs, why should we expect that males do? and (2) what are the benefits for females of carrying other females' eggs?
In relation to the first question, data from our main study population show
that soon after individuals become active in early spring the proportion of
males carrying eggs increases steadily, until all males in the population
carry eggs after about 2 months (Figure
2). After this peak, the proportion of adult males carrying eggs
decreases down to about 60% of males, because males born on that year become
adults but do not accept eggs until after their first winter
(Reguera, 1999). The
proportion of females carrying eggs remains much lower during the whole season
and never reaches values over 20% of the female population. In addition, when
we consider only adults who carry eggs, males carry more eggs (N =
171, mean = 4.32), than females (N = 103, mean = 2.20). We would like
to emphasize that sex ratio in this natural population was 50:50 during the
whole season, suggesting that differences in the availability of both sexes
cannot explain these trends. The suggestion by Kaitala et al.
(2001) that differences in the
proportion of males and females that carry eggs in natural populations may be
due to the fact that such populations are divided into small sub-units, and
the model of two males and two females used to explain why females may end up
with one-third of the eggs, is once again not applicable to natural
populations, which consist of hundreds of individuals which move along large
ranges.
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Thus, egg carrying by females is minimal compared to egg carrying by males, and this suggests that the balance of benefits and costs for each sex is totally different. The benefits for females are clearly very low, since the eggs they carry are never their offspring. On the other hand, egg carrying seems to be mainly restricted to large females who tend to carry only one or two eggs. There are two possible explanations, either females only accept eggs when the costs are negligible (a few eggs on large females may not increase predation risk significantly), or it reflects the levels of parasitism which individuals cannot avoid (e.g., eggs laid while the females are copulating). If the latter explanation is correct, then the proportion of eggs carried by males which may be attributable to parasitism is very low, and other hypotheses are needed to explain why all reproductive males in the population carry eggs.
The second question derives from the alternative hypothesis that egg carrying by females is the result of a favorable balance of costs and benefits. In this case, reciprocal altruism and kin selection could explain the patterns observed, but these issues are far beyond the scope of this article.
Conclusion
Phyllomorpha laciniata shows a unique flexibility in its
oviposition behavior, which makes it a fascinating model to study the
consequences of the different strategies and their evolutionary implications.
Females lay eggs continuously during the breeding season, placing some on
plants, and some on conspecifics. While eggs on plants have low survival
prospects, on the whole females may benefit from not delaying every egg until
a willing adult is encountered. During the active season, the proportion of
males carrying eggs increases rapidly until it reaches 100% of the population.
On the contrary, a small proportion of females carry eggs and, when they do,
they carry fewer eggs than males. Females never carry their own offspring and
therefore egg carrying by females is either the consequence of parasitism by
other females, or it may reflect a small degree of acceptance below the levels
at which carrying eggs exerts a cost. The fact that all reproductive males in
natural populations carry eggs, and that it has important survival costs,
require other hypotheses to explain this pattern. Preliminary molecular
analyses suggest that a proportion of the eggs that a male carries are his
offspring (Kaitala and Miettinen,
1997; Kaitala et al.,
2000,2001).
This situation is likely to be the outcome of conflicts of interest between
females, who will benefit from laying eggs on any adult, and males, for whom
it may only pay to accept eggs if they increase the survival chances of some
of their offspring. Thus, to argue that egg carrying by male golden egg bugs
is not a form of paternal care because "females did not select the back
by paternity" (Kaitala et al.,
2001) is to miss the point.
As we have shown in this reply the discrepancies between the results from Kaitala's group and ours seem to arise mainly from the different approaches used by the two groups. We would like to emphasize the importance of carrying out systematic observations in the field when evolutionary hypotheses are tested on a poorly known species. Knowledge of the basic biology, reproductive cycle, and variability in individual strategies are essential to understand which selective forces are at work in current populations. Only once this background information is obtained can meaningful experiments be designed to be carried out both in the field and in the laboratory.
ACKNOWLEDGEMENTS
We would like to thank Francisco García González and Eduardo Roldán for their constructive comments, and the photography laboratory at the Museo Nacional de Ciencias Naturales for their good work. We are also grateful to all the people who have helped collecting data in the field. This work was funded by the Ministerio de Eduación y Cultura, grants PB93-0186 and PB96-0880.
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