Final Report Summary - LIPAUGUS (Control of reproductive behaviors in an equatorial sub-oscine bird: Implication for biodiversity studies.)
Control of reproductive behaviors in an equatorial sub-oscine bird: Implications for biodiversity studies.
Although birds are the best-studied vertebrate group, most studied species are endemic to the temperate zones, while about half of all bird species life in the tropics. Further, among the tropical species many belong to the so-called sub-oscine passerines, while temperate zones are dominated by their sister-group, the oscine passerines known as the songbirds. The knowledge of the biodiversity of reproduction mechanisms of tropical species including the sub-oscines is essential to understand the generality of behavioral mechanisms derived from temperate zone species and required for conservation efforts.
Thus, the first goal of this project was the study of the reproductive behavior of a tropical bird species, the passerine Lipaugus vociferans (screaming piha), the voice of the Amazon. The species inhabits range over most lowland forest areas of the Amazon basin and lives at the middle and canopy level of rainforests. It is a polygynus and sexually monomorphic species (Ridgely and Tudor, 1994, Snow 2004, Ohlson et al., 2007). Like many Cotingas, the screaming pihas are structured in groups that follow a lek-based mating system, i.e. a communal area, in which an assembly of males perform vocal courtship displays to attract females (Snow, 2004). These birds have a complex group organization in which dominance-subordination relationships are established. In the obstructed environment of the raining forest the acoustic channel is widely used to establish social relationships between members of the group, and reproductive success of this species depends on vocalization-based female mate choice.
To study the lekking-behavior in the forest, we developed an interdisciplinary approach between neurophysiologists (Gahr department of the Max Planck Institute of Ornithology, Seewiesen, Germany), ethologists (Aubin department of Centre National de Recherche, located at University Paris South (XI), France) and field ornithologists (da Silva department at the Federal of Para, Belem, Brazil). The study site was a primary forest fragment at Gunma near Belem. First, we established a new auditory recording system in the forest that allows the localisation and identification of the individual birds based on overlapping triangulation (Huetz and Aubin, 2013). This system is now available for the scientific community to perform biomonitoring in the rainforest or open habitats. This monitoring system allowed to study precisely the timing of the singing interactions between males during the day and during the year, allowed to decipher the coding characteristics of the different acoustic signals exchanged during these interactions, and to check the responses of males and females to these different categories of signals. Interestingly, male pihas that are located in the centre of the lek, produce significantly more completed songs than males located at the periphery of the lek. Since each male is identified by the acoustic feature of his song, the completeness of the song might inform the females about the most dominant males (Sebe et al., in preparation).
Concerning the reproduction, it is generally assumed that changes in testosterone production are involved in changes of reproductive behaviors such as courtship of birds. A prerequisite for this is that the underlying brain structures and muscles are indeed sensitive for these hormones, i.e. express the particular receptor protein such as the testosterone receptor (Gahr, 2007). However, this hormone dependency of courtship behaviors has neither been studied in detail in tropical birds nor in sub-oscines in general.
Vocal lekking behavior of the pihas was monitored year-round, i.e. we obtained for the first time the annual song activity pattern of individual tropical birds throughout the year. The individual song was highly constant year-round, but lekking activity decreased during the rainy season. Testicle size was smallest during the rainy season. Although we could not measure the level of circulating testosterone in the male pihas, the seasonality of the testis suggest that the singing activity is testosterone regulated. To confirm this would require hormone treatment studies, which are very difficult to carry out in tropical birds in their natural habitat due to low capture-recapture success.
On the anatomical level we found that the sound producing muscles (syrinx) of the screaming piha are highly androgen-sensitive. However, so far we could not detect androgen-sensitive vocal control regions. These results suggest that potential seasonality of song patterning would occur on the level of the syrinx.
The sister-group of sub-oscines are the oscines, the songbirds. A hallmark of the songbirds is their ability to learn vocalizations. In difference, sub-oscines are thought to not learn their songs. In fact, evidence for innate song development in sub-oscines comes from only one group, the flycatchers (Kroodsma, 1984), but a more recent study (Kroodsma et al., 2013) provides evidence for song learning in bellbirds that are quite closely related to the screaming piha in the Contingidae clade of sub-oscines. However, although we did not aim studying song development of the piha there is little evidence for song learning in this species. E.g. there was no lek-typical signature of songs of pihas, i.e. songs of individuals in a lek are as different as songs of individuals of different leks.
Next to song pattern per se, the males might learn the timing of the singing in the lek display. However, there is so far no indication that the temporal structure of vocal lekking behavior differs between neighbouring leks or at different location throughout the amazon region. In correlation with this behavioral evidence, we did not find brain regions that appear homologous to the so-called song control regions that are required for the production of learned vocalizations (Lobato et al., in preparation). Thus, neuroendocrine mechanisms of vocal learning of sub-oscines might differ between genus such as the genus Lipaugus and the genus Procinas. This provides a very interesting model to learn about ecological conditions that favor vocal learning.
Although birds are the best-studied vertebrate group, most studied species are endemic to the temperate zones, while about half of all bird species life in the tropics. Further, among the tropical species many belong to the so-called sub-oscine passerines, while temperate zones are dominated by their sister-group, the oscine passerines known as the songbirds. The knowledge of the biodiversity of reproduction mechanisms of tropical species including the sub-oscines is essential to understand the generality of behavioral mechanisms derived from temperate zone species and required for conservation efforts.
Thus, the first goal of this project was the study of the reproductive behavior of a tropical bird species, the passerine Lipaugus vociferans (screaming piha), the voice of the Amazon. The species inhabits range over most lowland forest areas of the Amazon basin and lives at the middle and canopy level of rainforests. It is a polygynus and sexually monomorphic species (Ridgely and Tudor, 1994, Snow 2004, Ohlson et al., 2007). Like many Cotingas, the screaming pihas are structured in groups that follow a lek-based mating system, i.e. a communal area, in which an assembly of males perform vocal courtship displays to attract females (Snow, 2004). These birds have a complex group organization in which dominance-subordination relationships are established. In the obstructed environment of the raining forest the acoustic channel is widely used to establish social relationships between members of the group, and reproductive success of this species depends on vocalization-based female mate choice.
To study the lekking-behavior in the forest, we developed an interdisciplinary approach between neurophysiologists (Gahr department of the Max Planck Institute of Ornithology, Seewiesen, Germany), ethologists (Aubin department of Centre National de Recherche, located at University Paris South (XI), France) and field ornithologists (da Silva department at the Federal of Para, Belem, Brazil). The study site was a primary forest fragment at Gunma near Belem. First, we established a new auditory recording system in the forest that allows the localisation and identification of the individual birds based on overlapping triangulation (Huetz and Aubin, 2013). This system is now available for the scientific community to perform biomonitoring in the rainforest or open habitats. This monitoring system allowed to study precisely the timing of the singing interactions between males during the day and during the year, allowed to decipher the coding characteristics of the different acoustic signals exchanged during these interactions, and to check the responses of males and females to these different categories of signals. Interestingly, male pihas that are located in the centre of the lek, produce significantly more completed songs than males located at the periphery of the lek. Since each male is identified by the acoustic feature of his song, the completeness of the song might inform the females about the most dominant males (Sebe et al., in preparation).
Concerning the reproduction, it is generally assumed that changes in testosterone production are involved in changes of reproductive behaviors such as courtship of birds. A prerequisite for this is that the underlying brain structures and muscles are indeed sensitive for these hormones, i.e. express the particular receptor protein such as the testosterone receptor (Gahr, 2007). However, this hormone dependency of courtship behaviors has neither been studied in detail in tropical birds nor in sub-oscines in general.
Vocal lekking behavior of the pihas was monitored year-round, i.e. we obtained for the first time the annual song activity pattern of individual tropical birds throughout the year. The individual song was highly constant year-round, but lekking activity decreased during the rainy season. Testicle size was smallest during the rainy season. Although we could not measure the level of circulating testosterone in the male pihas, the seasonality of the testis suggest that the singing activity is testosterone regulated. To confirm this would require hormone treatment studies, which are very difficult to carry out in tropical birds in their natural habitat due to low capture-recapture success.
On the anatomical level we found that the sound producing muscles (syrinx) of the screaming piha are highly androgen-sensitive. However, so far we could not detect androgen-sensitive vocal control regions. These results suggest that potential seasonality of song patterning would occur on the level of the syrinx.
The sister-group of sub-oscines are the oscines, the songbirds. A hallmark of the songbirds is their ability to learn vocalizations. In difference, sub-oscines are thought to not learn their songs. In fact, evidence for innate song development in sub-oscines comes from only one group, the flycatchers (Kroodsma, 1984), but a more recent study (Kroodsma et al., 2013) provides evidence for song learning in bellbirds that are quite closely related to the screaming piha in the Contingidae clade of sub-oscines. However, although we did not aim studying song development of the piha there is little evidence for song learning in this species. E.g. there was no lek-typical signature of songs of pihas, i.e. songs of individuals in a lek are as different as songs of individuals of different leks.
Next to song pattern per se, the males might learn the timing of the singing in the lek display. However, there is so far no indication that the temporal structure of vocal lekking behavior differs between neighbouring leks or at different location throughout the amazon region. In correlation with this behavioral evidence, we did not find brain regions that appear homologous to the so-called song control regions that are required for the production of learned vocalizations (Lobato et al., in preparation). Thus, neuroendocrine mechanisms of vocal learning of sub-oscines might differ between genus such as the genus Lipaugus and the genus Procinas. This provides a very interesting model to learn about ecological conditions that favor vocal learning.