Although can occur yearround, the frequency of flying-fox mating increases significantly during the mating season (V. Jones, 2008, personal communication).  During the mating season, the typical flying-fox social group is a mixed-sex group, called a harem, in which one male protects up to five females and guards his territory on a tree limb within the colony (Welbergen, n.d.).  These territories, which are about 3.3 body lengths along a branch, serve the function of mating territories, as well as a place to rest during the day (Welbergen, 2006).  Males establish their territories through agonistic encounters and maintain them by scent marking the branches, which is performed primarily immediately before emergence from the colony each night. Once these territories are established, however, aggressive encounters diminish and territories are often maintained through vocalizations (Nelson, 1965) and wing-flapping (Banack & Grant, 2002). If a male leaves his harem unattended, extra-pair copulations may occur between the females and another male (Welbergen, n.d.).  For this reason, the primary mating system for flying-foxes is female-defense polygyny.

There is some discrepancy in the literature as to whether female flying-foxes aid in the defense of territories in the summer camp.  Nelson (1965) suggests that the females of a harem will help the harem-holding male in defending the territory from intruders.  Welbergen (n.d.) on the other hand, proposes that they do not.  Territory ownership is one of the factors a female considers in her mate selection and therefore must be established prior to mate choice (Welbergen, n.d.). 

Mate selection for the grey-headed flying fox occurs from December to January.  During this time period individuals of both sexes return to the summer camps.  Sexual contact is initiated by the male who approaches the female.  A female rejects a male through vocalizations and wing flaps or flying away (Nelson, 1965).

As mentioned above, the primary mating system of the flying-fox is female-defense polygyny, however there are also monogamous pairs within the camp.  Polygynous groups are usually located at the center of the camp and monogamous pairs are usually located towards the outskirts.  Welbergen (n.d.) indicates that the prevalence of the various mating systems in flying-fox colonies is dependent on the availability of female mates. Presumably, in an abundance of females, the less dominant males on the outskirts of the camp are able to find a female to mate with.

Copulation between two flying-foxes.