Michelle L. Tomaszycki

Consistency and change in the behavior of rhesus macaque abusive mothers with successive infants

This study investigated the abusive behavior and parenting styles of 7 rhesus macaque mothers with infants born in 2 consecutive years. All subjects lived in captive social groups and were observed during the first 12 weeks of infant life. With the exception of 1 individual, mothers were generally consistent in the frequency with which they abused their successive infants. Similarities were also found in the temporal course of infant abuse, the use of the most common pattern of abuse, and some measures of parenting style, notably those reflecting maternal protectiveness. The findings of this study are discussed in relation to different hypothesized relationships between infant abuse and parenting style in macaques.

Sexual differentiation of the zebra finch song system: potential roles for sex chromosome genes

BackgroundRecent evidence suggests that some sex differences in brain and behavior might result from direct genetic effects, and not solely the result of the organizational effects of steroid hormones. The present study examined the potential role for sex-biased gene expression during development of sexually dimorphic singing behavior and associated song nuclei in juvenile zebra finches.ResultsA microarray screen revealed more than 2400 putative genes (with a false discovery rate less than 0.05) exhibiting sex differences in the telencephalon of developing zebra finches. Increased expression in males was confirmed in 12 of 20 by qPCR using cDNA from the whole telencephalon; all of these appeared to be located on the Z sex chromosome. Six of the genes also showed increased expression in one or more of the song control nuclei of males at post-hatching day 25. Although the function of half of the genes is presently unknown, we have identified three as: 17-beta-hydroxysteroid dehydrogenase type IV, methylcrotonyl-CoA carboxylase, and sorting nexin 2.ConclusionThe data suggest potential influences of these genes in song learning and/or masculinization of song system morphology, both of which are occurring at this developmental stage.

Sex differences in infant rhesus macaque separation-rejection vocalizations and effects of prenatal androgens

Infant and juvenile rhesus macaques exhibit many sexually dimorphic behaviors, including rough and tumble play, mounting, and time spent with nonmother females. This study investigated sex differences in infant rhesus monkey separation-rejection vocalizations (SRVs), and the effects of altering the prenatal hormone environment on these differences. Pregnant females received exogenous androgen (testosterone enanthate), an androgen antagonist (flutamide), or vehicle injections for 30 or 35 days during the second (early) or third (late) trimester of pregnancy. Control females used a greater percentage of coos and arched screams than did control males. In contrast, males used a greater percentage of geckers and noisy screams than did females. Females also had longer SRV bouts, used more calls, and used more types of vocalizations than did males. Mothers were more likely to respond to the SRVs of male infants than to the SRVs of female infants. Prenatal flutamide treatment early in gestation reduced the likelihood that mothers would respond to their male offspring, but prenatal androgen treatment had no effect on response rates of mothers to female offspring. Early, but not late, androgen treatment produced females who vocalized in a male-typical manner. Similarly, early flutamide treatment produced males who displayed more female-typical SRVs. Late flutamide treatments of females produced as much masculinization of SRVs as did early androgen treatment in females. These results demonstrate sex differences in highly emotional vocalizations in infant rhesus macaques and provide evidence that the timing and form of prenatal hormonal exposure influence such vocalizations.

Experimental alteration of male song quality and output affects female mate choice and pair bond formation in zebra finches

Although bird song is thought to be important in mate attraction, little is known about how females perceive differences in song and which specific elements of song females prefer. Most studies, to date, have examined female choice during preference tests for song stimuli, and most have treated females with oestrogen prior to testing. At present, it is unclear whether song preferences during such tests reflect actual mate preferences. This study tested the hypothesis that experimentally altering male courtship vocalizations (song) would affect female mate choice and the formation of long-term socially monogamous relationships. Male zebra finches, Taeniopygia guttata, were vocally distorted using two minor and reversible techniques. Females in a two-choice paradigm preferred control males over vocally distorted or muted males. In a pair bond formation experiment, all control males had paired 5 days into the study, whereas only one vocally distorted male had paired. By the end of 2 weeks, however, four nerve-transected males and one air-sac-punctured male had paired. These results suggest that females do use song quality as a basis for choosing males. However, other male qualities may eventually override vocal quality as the basis for female choice.

Monogamy on the fast track

Social monogamy has evolved multiple times and is particularly common in birds. It is not well understood why some of these species are continuously and permanently paired while others occasionally ‘divorce’ (switch partners). Although several hypotheses have been considered, experimental tests are uncommon. Estrildid finches are thought to be permanently paired because being short-lived opportunistic breeders, they cannot afford the time to form a new pair relationship. Here it is shown through a controlled experimental manipulation that zebra finches (Taeniopygia guttata) allowed to remain with their partners to breed again are faster to initiate a clutch (by approx. 3 days) than birds separated from their mates that have to re-pair, supporting the hypothesis that continuous pairing speeds up initiation of reproduction, a benefit of long-term monogamy in a small, short-lived, gregarious species.

Oxytocin antagonist treatments alter the formation of pair relationships in zebra finches of both sexes.

Oxytocin and vasopressin are known to be important in affiliative behaviors. Although these peptides have been shown to be involved in monogamous pairing behavior in a few mammalian species, their role across monogamous species is not well understood. In particular, monogamy is most common in birds, yet the role of mesotocin and vasotocin (avian homologues of oxytocin and vasopressin) in pair relationships has not been established in any avian species. The goal of the present study was to investigate the effects of an oxytocin antagonist on pairing and pairing-related behaviors in the monogamous zebra finch. To accomplish this, we systemically administered one of three doses of an oxytocin antagonist (1 μg, 5 μg, or 10 μg) or a vehicle to adult male and female zebra finches (in separate experiments) with no prior pairing experience. Subjects were observed over three days and allowed to choose mates. We found that oxytocin antagonists increased the latency to pair and decreased pair formation in both sexes. The effects of these treatments on overall pairing behaviors were more pronounced in females than in males, suggesting sexually differentiated effects on motivation to contact conspecifics. Treatments also reduced courtship, as measured by directed singing, in males. These results suggest that nonapeptides play a key role in pair formation in zebra finches of both sexes, similar to findings in other monogamous species.

Cannabinoid inhibition improves memory in food-storing birds, but with a cost

Food–storing birds demonstrate remarkable memory ability in recalling the locations of thousands of hidden food caches. Although this behaviour requires the hippocampus, its synaptic mechanisms are not understood. Here we show the effects of cannabinoid receptor (CB1–R) blockade on spatial memory in food–storing black–capped chickadees (Poecile atricapilla). Intra–hippocampal infusions of the CB1–R antagonist SR141716A enhanced long–term memory for the location of a hidden food reward, measured 72 h after encoding. However, when the reward location changed during the retention interval, birds that had received SR141716A during initial learning showed impairments in recalling the most recent reward location. Thus, blocking CB1–R activity may lead to more robust, long–lasting memories, but these memories may be a source of proactive interference. The relationship between trace strength and interference may be important in understanding neural mechanisms of hippocampal function in general, as well as understanding the enhanced memory of food–storing birds.

Behavioral effects of progesterone on pair bonding and partner preference in the female zebra finch (Taeniopygia guttata)

Progesterone is a sex steroid known to be involved in reproduction, but its role in pair relationships is not well understood. This study explored the effects of exogenous progesterone (P4) on courtship and pairing behaviors in female zebra finches (Taeniopygia guttata) in two separate experiments: the first focused on courtship and initial pair formation and the second examined the effects on pair maintenance. In these experiments, we tested the hypothesis that P4 increases pairing behaviors and consequently influences their partner preference. In Experiment 1, animals engaged in significantly more pairing behaviors when they were treated with P4 than when they received the vehicle. However, this effect was not partner-specific, since the association index (a marker for female partner preference) did not differ between treatment conditions. In Experiment 2, females were given two weeks to form a pair and then injected with P4 or vehicle. Pairs were observed that day and the subsequent day to determine if P4 caused a decrease in mate-directed behavior and an increase in extra pair behavior. P4 did not affect the quality of the pair relationship and did not increase extra pair behavior. These results suggest that P4 influences the overall quantity of initial pairing behaviors and may slightly increase the likelihood of partner preference formation over short time courses. However, P4 does not alter a previously established bond, suggesting there are likely separate mechanisms for initial pairing behaviors and pair maintenance.

Agonistic screams and the classification of dominance relationships: are monkeys fuzzy logicians?

Scream vocalizations of group-living rhesus macaques provoked by higher-ranking aggressors were examined in two contexts: encounters in which the rank difference between opponents was either large or small. Such vocalizations are important in eliciting support from the callers allies in the group (usually matrilineal kin). Five acoustically distinct recruitment screams encode specific information about features of the agonistic context, for example, relative rank of the opponent and the severity of the attack. Against higher-ranking opponents, noisy screams are most likely to be given during encounters that involve contact aggression, and tonal or undulated screams are most likely for non-contact aggression. We predicted that scream bouts directed to small rank difference opponents would be more likely to comprise calls from scream classes other than the expected type, and that scream bouts from large rank difference encounters would be more in accord with the expected class. For large rank difference bouts, on average 74.2% of calls were of the expected class; for small rank difference bouts, a significantly smaller per cent (53.8%) of calls was accurately predicted. In the large rank difference encounters, 65.6% (55/84) of bouts were composed entirely of expected scream types, but only 47.6% (39/82) were uniformly correct for small rank difference encounters. Large rank difference interactions also yielded significantly fewer bouts where none of the screams produced by the victim of attack belonged to the predicted class. We suggest that a multi-valued or fuzzy logic system, that is one with more than two truth values, might be a more realistic way to conceptualize the categorization of certain referents of monkey vocalizat. Copyright 1998 The Association for the Study of Animal Behaviour.

Is male song quality important in maintaining pair bonds

This study investigated a possible mechanism for maintaining long-term pair bonds in a socially monogamous songbird, the zebra finch (Taeniopygia guttata). Only males sing in this species. Song is thought to be important in female choice, and our earlier research showed that distortion of song by tracheosyringeal nerve transection (TS) and temporary muting by puncturing the interclavicular air sac (AS) both had profound effects on females choice of male mates and pair formation. Males continue to sing when paired, though function and importance of this song is not well understood. The current study investigated whether these same vocal manipulations affected the maintenance of pair bonds. A total of 27 males and females formed pairs in aviaries. After 3 weeks of pairing and one week after the start of egg laying, males were experimentally manipulated. Eggs were then removed, so that females were forced to decide whether or not to engage in another breeding attempt with their mate. Novel unpaired males and females were added to the aviaries for potential extra pair copulation partners or new mates and pairs were then observed for four weeks. Only two pairs separated after song-altering surgery (both in the TS group), and one of these TS males quickly paired with another female. Of the pairs that remained together, there were no significant differences in courtship or pairing behaviors compared with control pairs. These results suggest that song quality has surprisingly little effect on female pairing decisions once the pair has formed, and that the song quality mechanisms of pair bond formation are not required in the maintenance of the pair bond.