The transition from the female-like great calls to male calls during ontogeny in southern yellow-cheeked gibbon males (Nomascus gabriellae)

Abstract

It is well known that gibbons emit a pattern of vocalizations, which is specific for species and sex. A previous study showed, however, that immature southern yellow-cheeked gibbon (Nomascus gabriellae) males produce only female-like great calls from 2.3 to 5.3 years of age in co-singing interactions with their mothers. To date, nothing is known about how the vocal repertoire of a male changes from the female-like call (great call) to the male call (staccato notes and multi-modulation phrase) during vocal ontogeny. The goal of this study was to describe the transition from the female-like great call to the male call and the ontogeny of the male call. We predicted that the transition from the female-like great call to the male-specific call and the development of the male call is a normal part of the aging proces. If this is the case, the following phenomena will occur: (a) female vocalization should no longer be produced with the mature form of the multi-modulation phrase and (b) all stages of the male vocalization should occur gradually as the young male ages. Young males regularly emit both female-like great calls and male-specific calls between the ages of 5.6 to 7.1 years. Once the young males reached 7.1 years of age, they emitted male calls exclusively, and they continued to do so until the end of the observation period (at 8.11 years of age). It was confirmed that the young males emitted only female-like great calls during periods when they produced non-mature forms of a multi-modulation phrase (Fm0,1—none or one frequency modulation in second notes). Furhermore, the decrease in the number of female-like great calls was attributed to the development of the mature form of the multi-modulation phrase (Fm2—two or more frequency modulation in second notes), which developed with age. We also confirmed that the multi-modulation phrase developed gradually, while the development of the staccato notes occurred in leaps. A multi-modulation phrase developed as the initial part of the male-specific call. It was evolved from a simpler to a more complex form as the maximum frequency and age of the young males increased. Staccato notes subsequently developed in certain young males. Possible explanations for such vocal ontogeny in young males are discussed in this work.

Transient co-singing of offspring and mothers in non-duetting Javan gibbons (Hylobates moloch)

“…This behavior has been reported in duetting gibbons such as H. lar and agile gibbons (H. agilis; Koda et al, 2014), and N. gabriellae, northern white-cheeked gibbon (Nomascus leucogenys), and black crested gibbons (Nomascus concolor; Schilling, 1984;Hradec et al, 2016Hradec et al, , 2017Hradec et al, , 2021. With physical and sexual maturation, young males of N. gabriellae transitioned from female-like songs to a mix of both male and female-like song parts, to male 10.3389/fevo.2022.910260 calls only (Hradec et al, 2021). Similar to immature female gibbons, immature males may also co-sing with their mothers to practice vocalizing.…”

“…Then what could be the evolutionary function of co-singing in H. moloch male offspring? Male offspring may co-sing with their mothers to avoid competition with fathers by female-like great calls, and thus by relaying information about their immature status (Hradec et al, 2021). However, this is unlikely because in both N. gabriellae (Hradec et al, 2021) and H. moloch (present study), co-singing episodes between young males and mothers were no longer observed after 8 years of age.…”

“…Remarkably, while they always produced only female-like great calls when they co-sang with their mothers before 7 years of age, young males produced male-like vocalizations of simple "wa" notes by themselves after 8 years of age. Nomascus gabriellae young males also stopped co-singing with their mothers around 7 years old, while gradually switching to adult male songs after producing both female and male type vocalizations between the age of 5-7 years (Hradec et al, 2021). We speculate that these sudden changes in H. moloch young male vocalizations might result from hormones related to age and sex, which also may influence the larynx growth and acoustic structures (Newman et al, 2000;Barelli et al, 2013).…”

“…Whenever there were adult female or male vocal events, we recorded the presence of any offspring co-singing and the Global Positioning System (GPS) coordinates. We defined co-singing as two individuals (mother and her immature offspring in our study) vocalizing simultaneously (Koda et al, 2013;Hradec et al, 2021), while duetting is usually defined as coordinated vocalization between a female and male pair in gibbons (Marshall and Marshall, 1976). When an offspring co-sang with an adult, we also recorded the age of the offspring.…”

Difference in the songs of paired and unpaired southern yellow-cheeked gibbon males (Nomascus gabriellae): social status or age?

“…Some advances have been made in singing primates, notably in Sulawesi tarsiers (genus Tarsius, Clink et al, 2020), indris (Indri indri, Torti et al, 2013), coppery titi monkeys (Plecturocebus cupreus, Lau et al, 2020), and gibbons (Geissmann, 2002). Additional studies have focused on song dynamics (e.g., rhythm, pitch, and degree of overlap) (Gamba et al, 2016), song flexibility (Clarke et al, 2006;Terleph et al, 2018a;Hradec et al, 2021a), song individuality (Sun et al, 2011;Clink et al, 2021), song ontogeny (Hauser, 1989;Pistorio et al, 2006;Hradec et al, 2017Hradec et al, , 2021bDe Gregorio et al, 2021), song recognition (Raemaekers and Raemaekers, 1985;Mitani, 1987;Caselli et al, 2015), song taxonomy, and genetic relatedness (Konrad and Geissmann, 2006;Torti et al, 2017). However, the question of whether songs by singing primates transmit information about pairing status (i.e., paired vs. unpaired individuals) has received surprisingly little attention.…”