Subsocial Behavior in Dung Beetles (Scarabaeidae)

                                 Abstract

     Subsocial behavior is characterized as the parental care adults provide for their own nymphs or larvae 
after oviposition.  Tallamy (1984) states that  the evolution of parental care represents an extraordinary 
breakthrough in the adaptation of organisms to their environment .  It is an effective way of neutralizing 
conditions harmful to the young (Tallamy 1984).  Tallamy (1984) continues that there is a cost associated 
with parental care.  Parents that commit much time and energy to the care and survival of a few offspring 
forfeit the chance to produce additional offspring during that period.  This loss of fecundity is adaptive 
only if the survival rate of these young is greater than that of young not receiving care.  Wilson (1971) 
proposes that subsocial behavior is a probable evolutionary link between solitary behavior and eusocial 
behavior.

     Halffter and Edmonds (1982) describe the nesting patterns of dung beetles (Scarabaeidae).  The 
majority of dung beetles do not exhibit subsocial (brood care) behavior.  The general nesting pattern is to 
provision the nest with food, generally in the form of dung, lay the eggs and abandon the nest.  Halffter 
and Edmonds (1982) do report that some dung beetles have been found to exhibit the more advanced 
behavior of brood care.  That is, after the female has laid the eggs, she remains in the nest and provides 
maintenance and protection for the brood until they become adults.  Halffter and Edmonds (1982) state this 
advanced behavior is found only in some paracoprid species of  dung beetles that form individual brood 
balls, but not in any of the ball- rolling dung beetles.  Sato and Imamori (1986,1987,1988) describe for 
the first time a ball-rolling species that creates individual brood pears from a single large dung ball and 
stays with the brood until they develop into adults.  In 1989, Edwards and Aschenborn describe a ball-
rolling species that exhibits extreme parental care.  The female lays just a single egg and remains with it the 
during entire development period.  Klemperer (1983 a) describes an endocoprid dung beetle species that 
forms individual brood balls and exhibits brood care.  Thus, researchers are observing there is more 
diversity in the nesting behavior of dung beetles than originally thought.

     In 1996 Halffter et. al. summarize the results of previous researchers, and include current research of 
their own,  indicating that parental care is an extremely effective strategy for improving the survival of the 
offspring.  These studies statistically determine that survival of the offspring is significantly greater with 
parental care than when the mother is excluded from the nest.   Brood care by the female, as described by 
the studies reviewed in this paper,  include (1) coating the surface of the brood ball with soil and 
excrement to prevent the dessication of the brood ball, (2) repairing cracks in the surface of the brood ball, 
and (3) protecting the brood ball from soil fungi, predators and parasites.  Some researchers also describe 
the cooperative behavior of the male in nesting.Subsocial Behavior in Dung Beetles (Scarabaeidae)

     Subsocial behavior is characterized as the parental care adults provide for their own nymphs or larvae.  
Tallamy and Wood (1986) clearly define this as parental behavior after ovipostion that promotes the 
survival, growth and development of offspring.  They do not include preovipositional behaviors such as 
nest contruction, even though this does eventually benefit the offspring.  Subsocial behavior is a probable 
evolutionary link between solitary behavior and eusocial behavior (Wilson, 1971).  It has arisen 
independently in nine insect orders and occurs in at least nine families of beetles (Coleoptera) (Wilson, 
1971).  

     All dung beetles (Scarabaeidae) provision their young with food, generally in the form of dung 
(Halffter and Edmonds, 1982).  In most families of dung beetles the adults abandon the nest as soon as it 
has been completed and the eggs laid.  They do not exhibit brood care.  However, there are some dung 
beetles in which the female remains in the nest to guard and care for the brood.  This paper is a review of 
research studies that have discovered these subsocial (brood care) behaviors in some dung beetles.

     Dung beetles exhibit a variety of   breeding strategies and dung use.  These patterns have been 
summarized by Doube (1990) and Doube, et. al (1988) and are categorized into four groups on the basis 
of their behavior: (1) paracoprids, which construct their nest and bury dung under the dung pad; (2) 
telecoprids, which detach a portion of dung from the dung pad, form it into a ball and roll it away from the 
dung pad and generally bury it; (3) endocoprids, which nest directly in the dung pad; and (4) 
kleptoparasites, which steal dung from other beetles or use dung already buried.
     
Subsocial behavior in paracoprids

     The most common paracoprid nesting pattern does not include brood care.  Halffter and Edmonds 
(1982) describe this pattern as follows:  the egg is laid on a brood mass which is a quantity of dung that is 
packed into an underground tunnel.  This mass of dung is not further molded into brood balls.   A 
variation of this pattern exhibited by some paracoprid dung beetles is the formation of brood balls from the 
mass of dung taken underground.  In both of  these patterns the females abandon the nest once eggs are 
laid.  A third nesting pattern described by Halffter and Edmonds (1982) for paracoprid beetles includes the 
formation of brood balls underground plus the addition of brood care, the female stays with the eggs until 
the young have fully developed.

     Klemperer (1983b) observed that the formation of brood balls is essential for the development of 
brooding behavior by the female.  He explains that brood balls permit surveillance of individual members 
of the brood and of their food supply in a way that is not possible in the case of a brood mass.  He further 
states that selective pressures favor the strategy of brood balls.  The brood balls are most likely to be more 
resistant to dessication due to the formation of a hard outer shell on the smooth, compact surface of the 
ball.  This hard shell also makes it more difficult for predators and kleptoparasites to break into.  In 
contrast, the surface of a brood mass surrounded by damp soil remains soft and easily breeched by 
predators and kleptoparasites.  Also, as the surrounding soil dries, the brood mass would dry and possibly 
crack, threatening the viability of the developing larvae.

     Details of brood care by the paracoprid dung beetle, Copris lunaris, are discussed by Klemperer 
(1982).  In caring for her brood, a female will right a brood ball so the egg and porous area are uppermost.  
She also repairs the surface of the brood ball and smoothes out any irregularities.  Klemperer (1982) states 
that chemical stimuli from the egg and larva play an essential part in eliciting the righting and repair 
behavior from the female.  Brood balls without this stimuli, such as those containing dead larvae or 
kleptoparasites are not repaired, but destroyed by the female.  This repair and defense of the nest most 
likely contributes to brood survival.

       Tyndale-Biscoe (1984) studied the brood care behavior of another paracoprid dung beetle, Copris 
diversus.  She reported that in nests without parents, many brood balls were destroyed by larvae of sciarid 
flies, dung-living nematodes and fungal growth.  This did not occur in nests with the female providing 
care.  She also reported that the female beetle would take dung from brood balls containing dead larvae and 
plaster it to the outside of brood balls containing live larvae.  This resulted in larger brood balls which 
contained larger progeny.  Most likely, the interior of the larger brood ball did not become dessicated as 
fast as a smaller ball and thus provided food of the appropriate consistency for the larvae for a longer 
period of time.  In turn, these resulting larger beetles buried more dung than smaller beetles, produced a 
larger number of brood balls and thus more young.  Tyndale-Biscoe (1984) concluded that brood care 
enhanced the survival of progeny, and produced larger and more fecund offspring.

     Klemperer (1986) found that Copris laeviceps, a small paracoprid beetle, has the same nesting and 
parental behavior as larger Copris species, such as Copris lunaris.  They both righted and repaired brood 
balls, repaired and defended the nest chamber, and killed larvae of unrelated species.  This guarding and 
maintenance behavior kept the brood balls and nest intact and repelled predators and kleptoparasites.  
However, unlike Copris lunaris that has an annual life cycle, Copris laeviceps matures rapidly and can 
raise several broods in quick succession.  This species lives in the rainforest, an environment with 
unpredictable periods of favorable conditions and harsh conditions.  During favorable conditions, 
Klemperer (1986) found that the female is ready to oviposition in the second and later nests just one week 
after the previous brood had emerged.  However, with unfavorable conditions such as low dung supplies 
or low temperatures, the female could delay oviposition for at least three months.  The small number of 
beetles that survive an adverse situation could then multiply rapidly when favorable conditions returned.  
Klemperer (1986) states that parental care may be essential for offspring to survive in these risky 
conditions, that their superficial nests are likely to be in great danger from predators, competitors and 
kleptoparasites.  In contrast, Klemperer (1986) notes that in the larger Copris species, with an annual life 
cycle in an environment with predictable seasons, parental care contributes to the  maintainance of a stable 
population size.

     Halffter et. al. (1996) summarize the results of previous researchers indicating that parental care is 
important for offspring survival: in Copris fricator offspring survival in nests receiving care was 96% 
versus 59% when the parents were excluded (Halffter & Mathews 1966); in Copris diversus 76% survival 
with parental care and 32% without (Tyndale-Biscoe 1984); in Cathon cyanellus there was 98% survival 
with parental care versus 68% without (Favila 1992, 1993); and in Kheper nigroaeneus there were no 
survivors without parental care (Edwards 1988b).  In Copris incertus Halffter et. al. (1996) report a 
75.9% survival with parental care and only 22.5% when the parents were excluded.  In this study, 
Halffter et. al. (1996) found that when the female parent was excluded from the nest fungi invaded the 
brood balls and their texture became brittle.  When she was permitted to stay in the nest, there was no 
evidence of fungi and the brood balls maintained their consistency and did not develop cracks.  This study 
also showed that the most vulnerable stage of development was the period from pupae to adult.  Without 
maternal care, mortality was highest during this stage.  This is a time when the offspring are inactive.  
Prior to this, the larvae are active inside the brood ball, coating the interior of the brood ball with their 
excrement.  Halffter also mentions that in the field earth worms destroy most brood balls that are 
abandoned by the mother (Huerta & Halffter, unpublished data).

Subsocial behavior in endocoprids

     Brood care has also been observed in some endocoprid dung beetle species.  Endocoprid species 
typically hollow out a nest chamber on the lower side of the dung pad and construct their brood balls there.  
Klemperer (1983a) describes the details of brood care for a particular endocoprid species, Oniticellus 
cinctus.  They exhibit many behaviors similar to Copris species,  both females repair the nests and brood 
balls and protect them from intruders.  The presence of the brood releases this parental behavior and 
prevents desertion of the nest by the female parent.  However, in O. cinctus, the brood balls themselves 
are built after oviposition, progressively by aggregating small fragments of dung from the floor and side of 
the nest chamber.  Klemperer (1983a) proposes that this technique may have originated from the dung 
gathering behavior used by the beetles to provision their nests.  Klemperer (1983a) also states that 
ovipositioning first, and then enlarging the brood balls allows for the synchronization of brood 
development and permits parental care to take place with a minimal investment of time.  Shortly after the 
new adults emerge, the original female can begin construction of a new nest.  This strategy provides 
increased survival of young due to brood care plus allows broods in quick succession for a rapid 
population increase under favorable conditions.  

     Klemperer (1983a) also noted for O. cinctus that the presence of brood balls inhibited oviposition, even 
if mature follicles were still present in the female and there was an unlimited supply of dung.  Klemperer 
(1983a) states that this strategy is beneficial.  It limits the brood to a number that can be cared for 
effectively as well as limits the metabolic cost of each brood so the female has a increased chance to 
survive to produce future broods.  He further elaborates that control of clutch size may be an important 
aspect in the reproductive strategies of many insects with parental care and in the evolution of certain 
behaviors of eusocial insects.

Subsocial behavior in telecoprids

     The general nesting pattern of telecoprid dung beetles, as described by Halffter and Edmonds (1982), 
involves making a brood ball at the dung pad, rolling it away and burying it.  The brood ball may be made 
by the male beetle alone, or the female may assist.  In most telecoprid species, after the egg is laid on the 
brood ball, the female leaves it to make others, resulting in a high rate of fecundity.  Brood care is absent.   

     Edwards and Aschenborn (1989), however, describe an extreme level of brood care in a telecoprid 
beetle.  This study reveals that for Kheper nigroaeneus the female remains with just a single offspring for 
its entire development period from egg to adult.  Edwards and Aschenborn (1989) contrast this with other 
Kheper species that exhibit brood care but whose nests usually contain 2-3 brood balls.  They also review 
that the nests of brood-caring paracoprid and endocoprid species contain at least 2 brood balls, with some 
species constructing 16 or more.  It is predicted that with low fecundity offspring survival will be 
enhanced and that the adults will be long-lived (Tallamy and Wood, 1986).  Edwards and Aschenborn 
(1989) found that with maternal care, offspring survival was between 58% and 84%.  Care included the 
female coating the brood ball with a mixture of soil and beetle excrement, most likely to inhibit microbial 
growth, reduce dessication and provide protection from predators.  Edwards and Aschenborn (1989) also 
report that the female K. nigroaeneus had the potential to reproduce rapidly again if, during the first third 
of the nesting period, her offspring died.  This was generally the period of greatest mortality, and having 
the ability to renest immediately offsets some of the risk of the extreme parental commitment.  Edwards 
(1988a) observed that some females raise two broods in one year, thus increasing fecundity.  In terms of 
life-span, Edwards (1988a) found that adults can live for two years or more.

     In their study, Edwards and Aschenborn (1989) also describe the investment of the male beetle as 
extremely high.  The male is almost entirely responsible for selecting the dung, constructing a brood ball 
large enough to feed both the female and the offspring, rolling the ball with the female clinging to it, 
selecting the nest site and burying the ball (Edwards and Aschenborn, 1988).  The male then leaves the 
nest area.  Edwards and Aschenborn (1989) explain this strategy is beneficial so the male can attract a mate 
and yet still have time to repeat the sequence with other females.  

     Sato and Imamori (1988) also observed brood care in telecoprid (ball-rolling) dung beetles.  Two 
species, Kheper platynotus and K. aegyptiorum, convert a single buried ball into multiple brood pears and 
the female remains in the nest to care for them.  The general nesting behavior for telecoprid beetles is one 
brood ball per nest and no brood care, a strategy considered primitive by Halffter and Edmonds (1982).  
Sato and Imamori (1986a,b) believe that the creation of two brood pears from just one ball and the addition 
of brood care suggests that the nesting behavior of ball-rolling dung beetles might be as diverse as that of 
the paracoprid dung beetles.  Once K. platynotus  and K. aegyptiorum find a dung source, they collect as 
much dung as possible at once, create it into a large ball and roll it away.  In the environment of the dry 
African savannah, where these species are found, the selective pressures that encourage the formation of a 
large ball that is later transformed into two to four brood pears are: the dung source is unpredictable and 
quickly becomes unacceptable due to dessication and decompostion, competition for dung is severe and 
the breeding period is limited to a short rainy season (Sato and Imamori, 1986b).  

     Sato and Imamori (1988) also report that the brood ball may be constructed by the male alone, by the 
female alone, or by a male-female pair.  In K. aegyptiorum the male invests more time and energy in 
obtaining a female by initiating brood ball construction and attracting the female by releasing sex 
phermones during hind-leg bending behavior on the completed ball (Sato and Imamori, 1988; Sato and 
Hiramatsu, 1993).  The male of K. platynotus does not initiate brood ball construction nor demonstrates 
hind-leg bending behavior (Sato and Imamori, 1987).  However, he does participate in rolling and burying 
the ball, thus insuring his chances of paternity (Sato and Hiramatsu 1993).

     Brood care is compared and contrasted between Copris species and Kheper platynotus by Sato and 
Imamori (1987).  Both species bury a dung mass and cover it with soil or excrement.  They then store it 
for several days for fermentation before they convert it into multiple free- standing brood pears.  The 
Copris females lick the surface of the brood pears and sometimes add a coat of soil.  The K. platynotus 
females scrape the surface.  This behavior most likely enhances the gaseous exchange between the larval 
chamber and the outside by thinning the walls, and also it prevents the growth of microorganisms.

     Another ball-rolling scarab, Canthon cyanellus cyanellus, was observed to demonstrate parental care of 
the brood balls (Favila, 1993).  This study found that parental care was a critical factor in offspring 
survival.  Without parental care the brood balls were immediately attacked by fungi and the larvae died.  
Favila (1993) suggests that although food rolling for eating or nesting is an effective way of dealing with 
the intense competition at the food source, it creates new parental demands.  He states that parents that 
avoid competitors by rolling a fresh food ball are forced to invest additional time and energy in protecting 
that food for the larvae from soil fungi.  He also suggests that the presence of the parents protect the brood 
balls from predators.

Summary

     Edwards and Aschenborn (1989) summarize the nesting and subsocial behavior of dung beetles as 
follows:

          Dung is a nutritious but ephemeral food source, so dung beetles secure their supply, minimizing the 
risk of desiccation and competition, by burying it in underground chambers (Halffter and Edmonds, 
1982). Once an insect group has evolved a nesting behavior such as this, it is a small step for it to develop 
post- ovipositional parental care, as in Kheper (telecoprid), Copris (paracoprid) and Oniticellus 
(endocoprid) dung beetles.  However for true social behavior to evolve in dung beetles it would first be 
necessary that nests be reused by a second generation.  This is unlikely to occur in dung beetles for exactly 
the same reason that favored the evolution of their subsociality, namely that dung is a scattered and 
ephemeral food source.  However, subsocial behavior should not be thought of only as evolution that has  
unaccountably stopped  (Wilson, 1971).  Parental care is an extremely effective strategy for improving the 
survival probabilities of offspring.  The polyphyletic occurrence of this life history pattern is evidence 
enough of its remarkable success.

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