Naked Mole-Rat is Sensitive to Social Hierarchy Encoded in Antiphonal Vocalization

The maintenance of social relationships is critical for group-dwelling species. Social animals often exhibit behaviors such as antiphonal vocalizations that reduce conflict and maintain affiliations. Naked mole-rats ( Heterocephalus glaber ) have a complex hierarchical society comparable to that of bees and ants. They are also known for their extensive vocal repertoire, which may have evolved in the absence of visual cues. The most frequent vocalization used by naked mole-rats is the soft chirp (SC). It has an antiphonal nature and may function in rank identification and in maintaining affiliations. Relative body weight differences, which are directly related to social rank, are positively correlated with SC emission rates. SCs are elicited from either physical touch or the SC of another conspecific, and other cues might contribute to SC utterance. In the current study, we examined whether an SC alone was able to elicit SC responses. Specifically, we presented artificial SC-like sounds and determined whether the response rate was modulated by the acoustic properties of the stimulus. An analysis of response latency revealed that animals responded to the audio stimuli, and a single audio stimulus could elicit responses from two animals. Thus, antiphony in naked mole-rats may occur among three or more animals. We also found that animals were able to discriminate the acoustic properties of the stimulus and responded more frequently to audio stimuli resembling SCs from large animals than to those resembling SCs from small animals. Therefore, naked mole-rats may be able to judge social relationships (dominant or subordinate) based solely on SCs. The constraints of subterranean habitats and increased social complexity may have led to the evolution of this communication system.     

Bilateral lesions of the medial frontal cortex disrupt recognition of social hierarchy during antiphonal communication in naked mole-rats (<Emphasis Type="Italic">Heterocephalus glaber</Emphasis>)

Generation of the motor patterns of emotional sounds in mammals occurs in the periaqueductal gray matter of the midbrain and is not directly controlled by the cortex. The medial frontal cortex indirectly controls vocalizations, based on the recognition of social context. We examined whether the medial frontal cortex was responsible for antiphonal vocalization, or turn-taking, in naked mole-rats. In normal turn-taking, naked mole-rats vocalize more frequently to dominant individuals than to subordinate ones. Bilateral lesions of the medial frontal cortex disrupted differentiation of call rates to the stimulus animals, which had varied social relationships to the subject. However, medial frontal cortex lesions did not affect either the acoustic properties of the vocalizations or the timing of the vocal exchanges. This suggests that the medial frontal cortex may be involved in social cognition or decision making during turn-taking, while other regions of the brain regulate when animals vocalize and the vocalizations themselves.     

The communicative content of the common marmoset phee call during antiphonal calling

Vocalizations are a dominant means of communication for numerous species, including nonhuman primates. These acoustic signals are encoded with a rich array of information available to signal receivers that can be used to guide species‐typical behaviors. In this study, we examined the communicative content of common marmoset phee calls, the species‐typical long distance contact call, during antiphonal calling. This call type has a relatively stereotyped acoustic structure, consisting of a series of long tonal pulses. Analyses revealed that calls could be reliably classified based on the individual identity and social group of the caller. Our analyses did not, however, correctly classify phee calls recorded under different social contexts, although differences were evident along individual acoustic parameters. Further tests of antiphonal calling interactions showed that spontaneously produced phee calls differ from antiphonal phee calls in their peak and end frequency, which may be functionally significant. Overall, this study shows that the marmoset phee call has a rich communicative content encoded in its acoustic structure available to conspecifics during antiphonal calling exchanges. Am. J. Primatol. 72:974–980, 2010. © 2010 Wiley‐Liss, Inc.     

Do age- and sex-related variations reliably reflect body size in non-human primate vocalizations? A review

In vocal communication, the mechanisms of sound production are well understood. The length of the vocal folds determines the minimum fundamental frequency, while the size and the shape of the vocal tract affect its filtering characteristics and hence, the resonant frequencies. Both measures-vocal fold length and vocal tract length-are related to body size and therefore, acoustic features are expected to vary with body size. Because direct measures of body size are difficult to obtain from free-ranging animals, age and sex have often been used as proxies. We surveyed studies which included direct measures of size or weight, and also studies in which only age and/or sex differences were examined. The main purpose was to examine whether age- and sex-related variations in acoustic features meet the predictions generated from our knowledge about sound production. Our survey revealed that compared to smaller animals, larger animals utter longer calls, with a lower fundamental frequency, with smaller formant dispersion, and with the energy concentrated in lower frequencies. Age and sex reliably reflect the influence of body size on acoustic features when gross size differences are examined. However, within age- and sex classes, this relationship may break down. In addition to body size, other factors such as internal state or social context may also influence the structure of vocal signals and highlight the richness of information in calls that is potentially available to listeners.     

The African cichlid fish Astatotilapia burtoni uses acoustic communication for reproduction: sound production, hearing, and behavioral significance

Sexual reproduction in all animals depends on effective communication between signalers and receivers. Many fish species, especially the African cichlids, are well known for their bright coloration and the importance of visual signaling during courtship and mate choice, but little is known about what role acoustic communication plays during mating and how it contributes to sexual selection in this phenotypically diverse group of vertebrates. Here we examined acoustic communication during reproduction in the social cichlid fish, Astatotilapia burtoni. We characterized the sounds and associated behaviors produced by dominant males during courtship, tested for differences in hearing ability associated with female reproductive state and male social status, and then tested the hypothesis that female mate preference is influenced by male sound production. We show that dominant males produce intentional courtship sounds in close proximity to females, and that sounds are spectrally similar to their hearing abilities. Females were 2-5-fold more sensitive to low frequency sounds in the spectral range of male courtship sounds when they were sexually-receptive compared to during the mouthbrooding parental phase. Hearing thresholds were also negatively correlated with circulating sex-steroid levels in females but positively correlated in males, suggesting a potential role for steroids in reproductive-state auditory plasticity. Behavioral experiments showed that receptive females preferred to affiliate with males that were associated with playback of courtship sounds compared to noise controls, indicating that acoustic information is likely important for female mate choice. These data show for the first time in a Tanganyikan cichlid that acoustic communication is important during reproduction as part of a multimodal signaling repertoire, and that perception of auditory information changes depending on the animal's internal physiological state. Our results highlight the importance of examining non-visual sensory modalities as potential substrates for sexual selection contributing to the incredible phenotypic diversity of African cichlid fishes.     

Body size effects on vertical climbing among chimpanzees

I analyzed observations from a yearlong study of the positional behavior of Pan troglodytesat the Mahale Mountains National Park to determine whether there are detectable differences in behavior between large and small individuals. Analysis was complicated by a weak correlation between body size and social rank. To factor out rank effects, I performed two types of analyses, depending on the type of data: (1) multiple regressions or (2) comparisons of similarly ranked animals of different body size. With social rank effects accounted for, larger males fed lower in the canopy, fed on the ground more often, fed preferentially among food tree species with smaller adult heights, and climbed significantly less often than smaller males did. Contrary to expectation, large males utilized smaller weight-bearing structures than small males did. These results suggest that large males minimized climbing versus optimizing support diameters, perhaps because vertical climbing is disproportionally expensive for larger animals. The large body weight of chimpanzees compared with other primates suggests that minimizing altitude changes, and therefore vertical climbing, is an important consideration in budgeting daily energy expenditures.     

Acoustic signals in katydids (Orthoptera,Tettigonidae). Communication 2

Three basic trends in the development of acoustic communication in Tettigonioidea are distinguished. The first one is observed in predatory tettigoniids and conocephalids. It is associated with the improvement of the territorial behavior and results in the appearance of territorial, aggressive and protest sounds (only males stridulate) in the acoustic repertoire. The second trend is caused by the development of defensive mechanisms. It is observed in phytophagous katydids belonging to the family Bradyporidae dwelling in deserts and other exposed habitats. As a rule, their acoustic repertoire includes long-lasting calling songs and disturbance (protest) sounds; rather often, these sounds are produced both by males and females. The unmasking effect of signals is compensated for by specific defense adaptations. The third evolutionary tendency is most completely expressed in phytophagous Phaneropteridae and phytophilous Bradyporidae (Ephippigerinae) as a result of the predator press and the improvement of sexual behavior. It leads to appearance of a “slow” system of communication, when the unmasking effect of songs is minimized by the decrease in the acoustic activity of males. Females produce response signals, while males produce complex calling, courtship, and confirming sounds. The temporal pattern of a signal is one of the most reliable criteria for the discrimination of species and subspecies. It is difficult to use physical parameters of sounds as a criterion for the differentiation of taxa at the superspecies rank, since acoustical signalling is obviously a subject of evolution of the acoustic community rather than of the taxon. Parallelisms and convergences are observed in the evolution of acoustic communication systems, but complex analysis allows revealing the initial type of the acoustic system and defining the reasons for adaptive reorganizations.     

Body size effects on vertical climbing among chimpanzees

I analyzed observations from a yearlong study of the positional behavior of Pan troglodytesat the Mahale Mountains National Park to determine whether there are detectable differences in behavior between large and small individuals. Analysis was complicated by a weak correlation between body size and social rank. To factor out rank effects, I performed two types of analyses, depending on the type of data: (1) multiple regressions or (2) comparisons of similarly ranked animals of different body size. With social rank effects accounted for, larger males fed lower in the canopy, fed on the ground more often, fed preferentially among food tree species with smaller adult heights, and climbed significantly less often than smaller males did. Contrary to expectation, large males utilized smaller weight-bearing structures than small males did. These results suggest that large males minimized climbing versus optimizing support diameters, perhaps because vertical climbing is disproportionally expensive for larger animals. The large body weight of chimpanzees compared with other primates suggests that minimizing altitude changes, and therefore vertical climbing, is an important consideration in budgeting daily energy expenditures.     

Antiphonal Responses to Loud Contact Calls Produced by Saguinus oedipus

We report the results of an experiment designed to investigate whether captive cotton-top tamarins (Saguinus oedipus) selectively call back to an absent cagemate. We removed 2 individuals living in separate cages (cycling through the colony so that each individual was removed 10 times) from the homeroom and played back calls produced by one of them. The caller's cagemate, residing in the homeroom, was more likely to be the first individual to call back antiphonally than any other individual in the colony was. In support of previous work using both habituation-discrimination and phonotaxic techniques, our results show that cotton-top tamarins can recognize cagemates and possibly individuals by voice alone, and that the antiphonal playback method provides yet another tool for investigating acoustic perception in nonhuman primates.     

Bottlenose dolphins that forage with artisanal fishermen whistle differently

Acoustic communication is a taxonomically widespread phenomenon, crucial for social animals. We evaluate social sounds from bottlenose dolphins (Tursiops truncatus) of Laguna, southern Brazil, whose social structure is organized around a cooperative foraging tactic with artisanal fishermen. This tactic involves stereotyped and coordinated behaviour by dolphins and fishermen and is performed by a subset of the dolphin population, splitting it into two distinct social communities. We compared the acoustic parameters and type of whistles emitted by dolphins of the “non‐cooperative” and “cooperative” communities, both during their interactions with fishermen and in times where dolphins were engaged in other types of foraging. Our findings show how dolphins’ social sounds differ between foraging tactics and social communities. The frequencies of six whistle types (ascending, descending, concave, convex, multiple, flat) were significantly dependent on tactics and communities. Ascending whistles were more common than expected during foraging without fishermen, and among dolphins of the non‐cooperative community. Whistle acoustic parameters (duration, number of inclination changes and inflection points, and initial, final, maximum, minimum frequencies) also varied between social communities. In general, whistles emitted by cooperative dolphins, mainly when not interacting with fishermen, tended to be shorter, had higher frequency and more inflections than those emitted by non‐cooperative dolphins. These results suggest that different whistles may convey specific information among dolphins related to foraging, which we hypothesize promote social cohesion among members of the same social community. These differences in acoustic repertoires add a new dimension of complexity to this unique human–animal interaction.     

Day and night sounds of the Guiana dolphin, <Emphasis Type="Italic">Sotalia guianensis</Emphasis> (Cetacea: Delphinidae) in southeastern Brazil

Many cetaceans are known to be acoustically active at night. However, for most dolphin species, there is little information about their nocturnal acoustic activities. To study the acoustic repertoire of Sotalia guianensis, diurnal and nocturnal sounds (whistles, burst pulses, low-frequency narrowband (LFN) sounds, and clicks) were identified in the Cananéia estuary (25° 01′ S–25° 13′ S/47° 52′ W–48° 06′ W), south of the state of São Paulo, southeastern Brazil, during April, June, and November of 2012. The emission rate of these sounds was compared between daytime and nighttime using the chi-squared statistical test. The mean values of the acoustic parameters of whistles, burst pulses, LFN sounds, and clicks were compared using the t test. Whistles, burst pulses, and LFN sounds were more frequent at night, as these individuals require greater acoustic communication in the absence of light, mainly for social communication. Echolocation emission rates were similar in both day and nighttime. Dolphin sound structure also varied throughout the day, with dolphins emitting lower-frequency sounds at night. Low-frequency sounds, with longer wavelengths, provide many advantages for dolphins active at night because such sounds propagate greater distances. This study demonstrates that the sounds produced by S. guianensis are dependent on the time of day, with social communication sounds being more influenced by the presence of light.     

The social structure and dominance hierarchy of the Mashona mole-rat, Cryptomys darlingi (Rodentia: Bathyergidae) from Zimbabwe

Cryptomys darlingi is a social subterranean rodent mole which inhabits the mesic regions of south-eastern and central Africa. Mashona mole-rats live in small colonies (5-9 animals) in which reproduction is normally restricted to the largest male and female in the colony. The non-reproductive members in a mature colony cannot be placed into clearly defined work-related groups based on body mass.
The dominance hierarchy of a young colony was found to be linear, with a value of 1.00 calculated from Landau's linearity index, while that of a mature colony of nine mole-rats was almost linear (0.77). Dominance was found to be related to gender in the mature colony, with males more dominant than females, and to age in the young colony. The reproductive mole-rats are the dominant animals within their respective genders. Dominance appears to correlate positively with body mass (rs = 0.77 in the mature colony and rs = 0.93 in the young colony).
Popularity studies show that smaller animals and females tend to be more popular than the larger massed individuals or males. In the mature colony which contained predominantly adult animals, the reproductive pair was among the least popular. While in the young colony, composed predominantly of sub-adult and juvenile animals, the reproductive pair was the most popular.
Social organization within Mashona mole-rat colonies is compared with other southern African Cryptomys species.     

The units of perception in the antiphonal calling behavior of cotton-top tamarins (Saguinus oedipus): playback experiments with long calls

We investigated how the acoustic structure of the cotton-top tamarin monkey's (Saguinus oedipus) combination long call relates to the antiphonal calling behavior of conspecifics. Combination long calls can function as contact calls and are produced by socially isolated individuals. Often conspecifics respond to these calls with their own long calls. Structurally, these calls are always composed of one or more 'chirps' followed by two or more 'whistles'. We compared the antiphonal calling responses to playbacks of complete, naturally produced long calls versus single whistles or single chirps. Subjects responded significantly more to whole calls than to either syllable-type alone. Thus, our data suggest that, in terms of the antiphonal calling behavior of socially isolated conspecifics, the whole long call is the unit of perception.     

Overview on the Diversity of Sounds Produced by Clownfishes (Pomacentridae): Importance of Acoustic Signals in Their Peculiar Way of Life

Background

Clownfishes (Pomacentridae) are brightly colored coral reef fishes well known for their mutualistic symbiosis with tropical sea anemones. These fishes live in social groups in which there is a size-based dominance hierarchy. In this structure where sex is socially controlled, agonistic interactions are numerous and serve to maintain size differences between individuals adjacent in rank. Clownfishes are also prolific callers whose sounds seem to play an important role in the social hierarchy. Here, we aim to review and to synthesize the diversity of sounds produced by clownfishes in order to emphasize the importance of acoustic signals in their way of life.

Methodology/Principal Findings

Recording the different acoustic behaviors indicated that sounds are divided into two main categories: aggressive sounds produced in conjunction with threat postures (charge and chase), and submissive sounds always emitted when fish exhibited head shaking movements (i.e. a submissive posture). Both types of sounds showed size-related intraspecific variation in dominant frequency and pulse duration: smaller individuals produce higher frequency and shorter duration pulses than larger ones, and inversely. Consequently, these sonic features might be useful cues for individual recognition within the group. This observation is of significant importance due to the size-based hierarchy in clownfish group. On the other hand, no acoustic signal was associated with the different reproductive activities.

Conclusions/Significance

Unlike other pomacentrids, sounds are not produced for mate attraction in clownfishes but to reach and to defend the competition for breeding status, which explains why constraints are not important enough for promoting call diversification in this group.     

Merging social hierarchies: Effects on dominance rank in male green swordtail fish (Xiphophorus helleri)

When the same set of individuals are placed in different social contexts, some groups members often experience a change in dominance status. We examined the context-dependence of social status using a group fusion protocol in male green swordtail fish (Xiphophorus helleri). Six individuals were matched for size and separated into two groups of three fish. Each triad established a stable hierarchy after which time the two subgroups were merged into one larger assemblage. The maintenance of within- and between-group rank relationships was examined. Relative rank was preserved within each subgroup across social contexts but we found no evidence that familiarity with dominant animals assists individuals of one subgroup in achieving higher rank (coat-tail effects). Dominant individuals from the pre-fusion groups were significantly likely to obtain high status in the merged group and vice versa for subordinate pre-fusion animals. These results demonstrate that social rank in swordtails is relatively impervious to changes in social context, but we address some deviations from this trend. Small differences in standard length were a significant predictor of the most dominant rank in the post-fusion hierarchy, with the largest animals tending to occupy the alpha position. We discuss our results in terms of the potential factors involved in within- and between-group rank maintenance, including individual recognition, winner and loser effects, or asymmetries in dominance-related characteristics.     

Intermale aggression of subordinate resident long-evans rats

Dominant male rats were separated from their colonies and subordinate residents were tested for aggression after a two week period. Subordinate animals showed significant increases in body weight and aggressive behavior toward intruders. Replacement of the previously dominant male led to rank reversals in three of six colonies. To assess whether two weeks of separation from the dominant male was necessary for subordinate males to exhibit aggression towards conspecifics, another intruder test was given following an additional two weeks of social housing. At the conclusion of this test, the more aggressive resident was removed and a naive intruder was immediately introduced into the colony with the subordinate male resident and again at 1, 5, and 10 day intervals. Aggressive posturing by the subordinate resident increased immediately following the removal of the dominant male, and remained at a high level throughout the subsequent intruder tests. In contrast, biting was initially low but increased steadily throughout the period of separation. These findings demonstrated that social or situational changes within a colony can greatly influence the aggression of subordinate males.     

The distribution of early recombination nodules on zygotene bivalents from plants.

Early recombination nodules (ENs) are protein complexes approximately 100 nm in diameter that are associated with forming synaptonemal complexes (SCs) during leptotene and zygotene of meiosis. Although their functions are not yet clear, ENs may have roles in synapsis and recombination. Here we report on the frequency and distribution of ENs in zygotene SC spreads from six plant species that include one lower vascular plant, two dicots, and three monocots. For each species, the number of ENs per unit length is higher for SC segments than for (asynapsed) axial elements (AEs). In addition, EN number is strongly correlated with SC segment length. There are statistically significant differences in EN frequencies on SCs between species, but these differences are not related to genome size, number of chromosomes, or phylogenetic class. There is no difference in the frequency of ENs per unit length of SC from early to late zygotene. The distribution of distances between adjacent ENs on SC segments is random for all six species, but ENs are found at synaptic forks more often than expected for a random distribution of ENs on SCs. From these observations, we conclude that in plants: (1) some ENs bind to AEs prior to synapsis, (2) most ENs bind to forming SCs at synaptic forks, and (3) ENs do not bind to already formed SCs.     

Dominance and queen succession in captive colonies of the eusocial naked mole-rat,Heterocephalus glaber.

Naked mole-rat colonies exhibit a high reproductive skew, breeding being typically restricted to one female (the ''queen'') and one to three males. Other colony members are reproductively suppressed, although this suppression can be reversed following the removal or death of the queen. We examined dominance and queen succession within captive colonies to investigate the relationship between urinary testosterone and cortisol, dominance rank and reproductive status; and to determine if behavioural and/or physiological parameters can be used as predictors of queen succession. Social structure was characterized by a linear dominance hierarchy before and after queen removal. Prior to queen removal, dominance rank was negatively correlated with body weight and urinary testosterone and cortisol titres in males and females. Queen removal results in social instability and aggression between high ranking individuals. Dominance rank appears to be a good predictor of reproductive status: queens are the highest ranking colony females and are succeeded by the next highest ranking females. The intense dominance-related aggression that accompanies reproductive succession in naked mole-rats provides empirical support for optimal skew theory.     

The colony structure and dominance hierarchy of the Damaraland mole-rat, Cryptomys damarensis (Rodentia: Bathyergidae), from Namibia

Cryptomys damarensis is one of the few subterranean rodents which is social. This species is found in the semi-arid regions of southwestern and central Africa. The Damaraland mole-rat occurs in coloniesof up to 25 individuals, in which reproduction is limited to one or two of the largest males and the largest female in the colony.
The mean colony size is 18 mole-rats ( n =6 colonies). The mean colony biomass is 2.32 kg and the sex ratio is female biased (0.71–0.78). The number of mole-rats in each colony, the mean body mass and the sex ratio are described for six field-captured colonies, three of which were captured in their entirety.
The dominance hierarchy of two colonies of C. damarensis was found to be linear with a value of between 0.94 and 1.00 calculated from Landau's linearity index. Dominance was found to be related to gender, with the males more dominant than females. The reproductive individuals are the dominant animals within each respective gender. The non-reproductive females rank lowest in the hierarchy.