Behavioral Ecology Vol. 12 No. 3: 367-368
© 2001 International Society for Behavioral Ecology
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Is nonparental egg carrying parental care?
a Department of Biology, University of Oulu, Box 3000, FIN-90 014 Oulu, Finland b Department of Theoretical Ecology, Ecology Building, University of Lund, S-223 62 Lund, Sweden c Departamento de Ecología y Comportamiento Animal, Instituto de Ecología A.C., Apartado Postal 63, Xalapa, Veracruz 91000, Mexico d Department of Zoology, University of Stockholm, S-106 91 Stockholm, Sweden
Address correspondence to A. Kaitala. E-mail: arja.kaitala{at}oulu.fi .
Received 11 February 2000; revised 14 July 2000; accepted 26 July 2000.
Golden egg bug (Phyllomorpha laciniata Vill) females oviposit on
the bodies of conspecifics of both sexes. Studies on the golden egg bug have
opened a new approach to understanding how forces arising from sexual conflict
act in breeding systems (Kaitala,
1998
,
1999;
Kaitala and Miettinen, 1997;
Hardling and Kaitala, in
press), in particular, how females are able to exploit males'
sexual interests by dumping eggs on courting or mating individuals. These
studies also show that social interactions among individuals may be
complicated by sexual conflicts of interest. Many aspects of the peculiar
behavior of the golden egg bug are already known, although much of it is still
unexplained and theoretically poorly understood.
Here we comment on the paper by Reguera and Gomendio
(1999) to clarify what really
makes the golden egg bug so interesting and unique. The golden egg bug is not
unique among insects in the sense that individuals carry eggs (see
Smith, 1997), but rather it is
unique because no simple explanation can be given for egg carrying. We
strongly feel that it is incorrect to assume a priori that the bug's behavior
is parental care, as Reguera and Gomendio
(1999) do, only because eggs
are attached on the backs of conspecifics. Below we expand on this claim and
emphasize the known aspects of the bug's behavior.
Egg dumping or parental care?
In the papers describing the egg-laying behavior of the golden egg bug, two
reasons for the behavior have been suggested: parental care or intraspecific
parasitism. Egg carrying has been suggested to be intraspecific parasitism
because egg carrying is costly and the bugs commonly carry unrelated eggs
(Kaitala, 1996,
1998,
1999;
Kaitala and
Axén, 2000;
Kaitala and Miettinen, 1997;
Kaitala et al., 2000). As the
egg-laying female benefits from the behavior, these studies show that laying
eggs on conspecifics is a maternal strategy for offspring survival, not the
strategy for an egg-carrying bug to enhance survival of the eggs it carries.
All published evidence shows that host "back" selection is made
solely by females. After tens of hours of videotaping we have not found any
indication that males had actively encouraged females to lay eggs on their
backs. Instead, females seem to lay eggs on individuals around them regardless
of sex and mating history (see below). No active female care has been noted
either. The reported evidence that egg carrying is not parental care comes
from three sources.
First, one third of the eggs are carried by females
(Kaitala, 1996;
Kaitala and Miettinen, 1997;
Reguera and Gomendio, 1999).
Due to morphological constraints that prevent ovipositing on themselves,
females do not carry their own eggs. By definition then, egg carrying by
females is not parental care as suggested by Reguera and Gomendio
(1999). Parental care should
reasonably be provided by parents.
Second, nonparent males carry eggs. In laboratory experiments, females did
not select the back by paternity but laid eggs at random on all backs
available (Kaitala, 1998,
1999;
Kaitala and Miettinen, 1997).
Receiving eggs is often unavoidable for bugs. They cannot resist receiving
eggs while mating themselves because nonmating females often dump eggs on
their backs (Kaitala and Miettinen,
1997). Females also commonly dump eggs on courting males
(Kaitala, 1998;
Miettinen and Kaitala,
2000).
It has also been shown that there is often more than a day between mating
and oviposition (Kaitala and Miettinen,
1997). Thus, contrary to other egg-carrying bugs with male
paternal care (see Smith,
1997) eggs are not laid immediately after copulation, which
greatly decreases male paternity certainty. The paternity data on DNA-analysis
indicate that only a very small proportion of eggs are fertilized by the
carrier (Tay MT, Miettinen M, and Kaitala A, unpublished data). The authors
note that "a proportion of eggs they (males) carry are their own
offspring" (Reguera and Gomendio,
1999), but no data are given.
It should be noted that even if males carry some eggs they have fertilized,
it does not mean that egg carrying is maintained or has evolved as a parental
care strategy. A small proportion of eggs carried by males is likely to be
their own even if females lay eggs randomly. In small groups with few mating
partners, a male will mate repeatedly with the same female
(Kaitala and Miettinen, 1997),
and as only a few backs are available for oviposition, females laying eggs at
random naturally lay some eggs on the paternal back.
Third, bugs can actively scrape off eggs from their backs. Egg scraping
depends only on egg load of the individual, not on sex, or on mating history
(Kaitala, 1996,
1999). Egg scraping indicates
that carrying eggs is not a receiver's strategy to enhance egg survival. If
bugs carry only a few eggs, they may be unable to scrape eggs without damaging
themselves. It is also unexplored if (or when) time and energy devoted to
scraping outweigh costs of carrying eggs.
It has been shown experimentally that egg carrying is costly due to
increased risk of predation by ants
(Kaitala and
Axén, 2000;
Kaitala et al., 2000), by great
tits (Reguera and Gomendio,
1999) and by chickens (Kaitala A, Swartling S and Gamberale G,
unpublished data). The fact that females dump eggs on the back of courting
males (Kaitala, 1998) means
that the conflict of interest between the sexes in this species has unusual
ingredients. Males want to mate, but courting puts them at risk of receiving
costly eggs. Females need an oviposition site (a back) but do not need nor
want to mate as it is costly, for example, because of the risk of receiving
eggs while in copula. This aspect of the interaction is the key to
understanding the behavior, and how it influences the social interactions
among individuals is a very interesting and exciting question.
Why do females carry fewer eggs than males?
Unequal distribution of eggs among the sexes
(Kaitala, 1996;
Kaitala and Miettinen, 1997;
Reguera and Gomendio, 1999)
will occur as an effect of random egg laying if individuals live in small
subpopulations. Because females do not carry their own eggs, for example, in a
group of two males and two females one third of the eggs will be laid on a
female's back as a consequence of random egg laying. This is exactly the
proportion of eggs carried by females in field
(Kaitala, 1996). Reguera and
Gomendio (1999) suggested that
females carry fewer eggs because they minimize the costs of egg carrying.
However, in addition to random egg laying in small populations, males receive
more eggs than females due to their sexual activity (e.g., while courting,
Kaitala, 1998;
Kaitala and Miettinen, 1997;
Miettinen and Kaitala, 2000).
Thus random egg laying and male sexual activity may explain the unequal egg
distribution in nature. It is unlikely to be only due to active avoidance of
eggs.
In addition, the number of eggs in the population studied by Reguera and
Gomendio (1999) was much lower
than what has been previously published for early June
(Kaitala, 1996) and the
proportion of individuals carrying eggs was very low. Natural variation in
number of carried eggs is high because:
- The cumulative number of eggs carried increases during the 1-3 month long
reproductive period.
- Individuals may scrape off eggs and predators may pick off eggs (Kaitala
1996,
1999;
Kaitala et al., 2000).
- In Catalonia, new generation bugs overwinter and do not commonly carry eggs
before breeding next spring (Kaitala A, Katvala M and Miettinen M, unpublished
data).
The new overwintering generation starts emerging in June in Catalonia, and
this is likely to occur earlier in the south. The data by Reguera and Gomendio
(1999) close to Madrid was
gathered by following individuals from March to August. If one would count
also nonreproductive individuals that are going to overwinter as potential egg
carriers (or parents), the low numbers are achieved. Thus one should consider
that nonreproductive bugs are going to carry eggs in the following spring.
Flexible reproductive strategy?
Females were said to follow a flexible strategy in their choice of
oviposition site, which leads to a situation in which some offspring receive
no care "while others are carried"
(Reguera and Gomendio, 1999).
Occasionally, we have noted a few eggs on host plant but to our knowledge this
is common only in exceptional circumstances, as in mountain populations
(Mineo, 1984). We have not
seen any other published evidence that females commonly lay eggs on the host
plant as a part of their reproductive strategy. Therefore the suggestion made
by Reguera and Gomendio (1999)
that females frequently use the host plant as an oviposition substrate is
especially interesting given that other populations in the Iberian Peninsula
do not follow such a strategy (Kaitala,
1996; Kaitala A, Katvala M and Miettinen M, unpublished data). It
should be noted that eggs found on host plants are not sufficient evidence of
female oviposition strategy because eggs on a host plant might be ones that
are scraped off by the bugs (Kaitala,
1996,
1999).
Furthermore, in many habitats of the bugs, arthropod eggs do not survive
(unless carried) because of intense ant predation
(Du Merle et al., 1978;
Kaitala, 1996;
Kaitala et al., 2000). The ant
Pheidole pallidula, a pollinator of the host plant Paronychia
argentea (Espadaler X, personal observation), has been noted to be one of
the main predators of the bug (Kaitala et
al., 2000). These ants are very efficient foragers
(Delalande, 1985;
Retana et al., 1992), and in
similar habitats as those occupied by the golden egg bug, they are able to
detect arthropod corpses in less than 5 min
(Retana et al., 1991). The
ants use both chemical and visual cues while foraging, and it has been shown
that even eggs hidden on the flowers cannot survive
(Kaitala, 1996).
Conclusions and future prospects
At the current state of research, there is no evidence to call egg carrying
parental care. Available data support that the system is driven by the
egg-laying female behaving often like an intraspecific parasite
(Kaitala, 1998,
1999;
Kaitala and Miettinen,
1997).
However, defining behavior solely as intraspecific parasitism is only a
part of the explanation, because some bugs (especially males) do accept
unrelated eggs voluntarily (Kaitala and
Miettinen, 1997; Miettinen and
Kaitala, 2000).
All these results make the golden egg bug a fascinating study object and a challenging task for future work because simple evolutionary explanations for egg-carrying are not supported. We feel that the main problem for future work is to explain how this system has evolved, why individuals accept carrying unrelated eggs, and what role sexual conflict plays on the behavior of the species.
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