Nestling Begging Calls Resemble Maternal Vocal Signatures When Mothers Call Slowly to Embryos.

AbstractVocal production learning (the capacity to learn to produce vocalizations) is a multidimensional trait that involves different learning mechanisms during different temporal and socioecological contexts. Key outstanding questions are whether vocal production learning begins during the embryonic stage and whether mothers play an active role in this through pupil-directed vocalization behaviors. We examined variation in vocal copy similarity (an indicator of learning) in eight species from the songbird family Maluridae, using comparative and experimental approaches. We found that (1) incubating females from all species vocalized inside the nest and produced call types including a signature "B element" that was structurally similar to their nestlings' begging call; (2) in a prenatal playback experiment using superb fairy wrens (Malurus cyaneus), embryos showed a stronger heart rate response to playbacks of the B element than to another call element (A); and (3) mothers that produced slower calls had offspring with greater similarity between their begging call and the mother's B element vocalization. We conclude that malurid mothers display behaviors concordant with pupil-directed vocalizations and may actively influence their offspring's early life through sound learning shaped by maternal call tempo.

Temporal and spatial variation in sex-specific abundance of the avian vampire fly (Philornis downsi).

Understanding the range and behaviour of an invasive species is critical to identify key habitat areas to focus control efforts. Patterns of range use in parasites can differ temporally, across life stages and between sexes. The invasive avian vampire fly, Philornis downsi, spends the larval stage of its life within bird nests, feeding on developing nestlings and causing high levels of mortality and deformation. However, little is known of the ecology and behaviour of the non-parasitic adult fly life stage. Here, we document sex-specific temporal and spatial patterns of abundance of adult avian vampire flies during a single Darwin's finch breeding season. We analyse fly trapping data collected across 7 weeks in the highlands (N = 405 flies) and lowlands (N = 12 flies) of Floreana Island (Galápagos). Lowland catches occurred later in the season, which supports the hypothesis that flies may migrate from the food-rich highlands to the food-poor lowlands once host breeding has commenced. Fly abundance was not correlated with host nesting density (oviposition site) but was correlated with distance to the agricultural zone (feeding site). We consistently caught more males closer to the agricultural zone and more females further away from the agricultural zone. These sex differences suggest that males may be defending or lekking at feeding sites in the agricultural zone for mating. This temporal and sex-specific habitat use of the avian vampire fly is relevant for developing targeted control methods and provides insight into the behavioural ecology of this introduced parasite on the Galápagos Archipelago.

Female in-nest attendance predicts the number of ectoparasites in Darwin's finch species.

Selection should act on parental care and favour parental investment decisions that optimize the number of offspring produced. Such predictions have been robustly tested in predation risk contexts, but less is known about alternative functions of parental care under conditions of parasitism. The avian vampire fly (Philornis downsi) is a myasis-causing ectoparasite accidentally introduced to the Galápagos Islands, and one of the major mortality causes in Darwin's finch nests. With an 11-year dataset spanning 21 years, we examine the relationship between parental care behaviours and number of fly larvae and pupae in Darwin's finch nests. We do so across three host species (Camarhynchus parvulus, C. pauper, Geospiza fuliginosa) and one hybrid Camarhynchus group. Nests with longer female brooding duration (minutes per hour spent sitting on hatchlings to provide warmth) had fewer parasites, and this effect depended on male food delivery to chicks. Neither male age nor number of nest provisioning visits were directly associated with number of parasites. While the causal mechanisms remain unknown, we provide the first empirical study showing that female brooding duration is negatively related to the number of ectoparasites in nests. We predict selection for coordinated host male and female behaviour to reduce gaps in nest attendance, especially under conditions of novel and introduced ectoparasites.

Evidence for rapid downward fecundity selection in an ectoparasite (Philornis downsi) with earlier host mortality in Darwin's finches.

Fecundity selection is a critical component of fitness and a major driver of adaptive evolution. Trade-offs between parasite mortality and host resources are likely to impose a selection pressure on parasite fecundity, but this is little studied in natural systems. The 'fecundity advantage hypothesis' predicts female-biased sexual size dimorphism whereby larger females produce more offspring. Parasitic insects are useful for exploring the interplay between host resource availability and parasite fecundity, because female body size is a reliable proxy for fecundity in insects. Here we explore temporal changes in body size in the myiasis-causing parasite Philornis downsi (Diptera: Muscidae) on the Galápagos Islands under conditions of earlier in-nest host mortality. We aim to investigate the effects of decreasing host resources on parasite body size and fecundity. Across a 12-year period, we observed a mean of c. 17% P. downsi mortality in host nests with 55 ± 6.2% host mortality and a trend of c. 66% higher host mortality throughout the study period. Using specimens from 116 Darwin's finch nests (Passeriformes: Thraupidae) and 114 traps, we found that over time, P. downsi pupae mass decreased by c. 32%, and male (c. 6%) and female adult size (c. 11%) decreased. Notably, females had c. 26% smaller abdomens in later years, and female abdomen size was correlated with number of eggs. Our findings imply natural selection for faster P. downsi pupation and consequently smaller body size and lower parasite fecundity in this newly evolving host-parasite system.

Aggressiveness predicts dominance rank in greylag geese: mirror tests and agonistic interactions.

Individual differences in aggressiveness, if consistent across time and contexts, may contribute to the long-term maintenance of social hierarchies in complex animal societies. Although agonistic interactions have previously been used to calculate individuals' positions within a dominance hierarchy, to date the repeatability of agonistic behaviour has not been tested when calculating social rank. Here, we examined the consistency and social relevance of aggressiveness as a personality trait in a free-flying population of greylag geese (Anser anser). For each individual, we quantified (i) aggressiveness using a standardized mirror stimulation test and (ii) dominance ranking based on the number of agonistic interactions won and lost in a feeding context. We found that individual differences in aggressiveness were significantly repeatable and that individuals' aggressiveness predicted their dominance rank position. The flock showed a robust and intermediately steep dominance hierarchy. Social rank was higher in paired birds, males and older birds, and most agonistic interactions occurred between individuals with moderate rank differences. We suggest that selection favours aggressiveness as a personality trait associated with resource acquisition and social rank, whereby a dominance hierarchy may increase the benefits of group living and reduce costs over conflict within dyads.

Age effects in Darwin's finches: older males build more concealed nests in areas with more heterospecific singing neighbors.

Nesting success tends to increase with age in birds, in part because older birds select more concealed nest sites based on experience and/or an assessment of prevailing predation risk. In general, greater plant diversity is associated with more biodiversity and more vegetation cover. Here, we ask if older Darwin's finch males nest in areas with greater vegetation cover and if these nest sites also have greater avian species diversity assessed using song. We compared patterns in Darwin's Small Tree Finch (Camarhynchus parvulus) and Darwin's Small Ground Finch (Geospiza fuliginosa) as males build the nest in both systems. We measured vegetation cover, nesting height, and con- vs. heterospecific songs per minute at 55 nests (22 C. parvulus, 33 G. fuliginosa). As expected, in both species, older males built nests in areas with more vegetation cover and these nests had less predation. A novel finding is that nests of older males also had more heterospecific singing neighbors. Future research could test whether older males outcompete younger males for access to preferred nest sites that are more concealed and sustain a greater local biodiversity. The findings also raise questions about the ontogenetic and fitness consequences of different acoustical experiences for developing nestlings inside the nest. Supplementary Information: The online version contains supplementary material available at 10.1007/s10336-023-02093-5.

Avian vampire fly (Philornis downsi) mortality differs across Darwin's finch host species.

In invasive parasites, generalism is considered advantageous during the initial phase of introduction. Thereafter, fitness costs to parasites, such as host-specific mortality, can drive parasites towards specialism to avoid costly hosts. It is important to determine changes in host specificity of invasive populations to understand host-parasite dynamics and their effects on vulnerable host populations. We examined changes in mortality in the introduced avian vampire fly (Philornis downsi) (Diptera: Muscidae), a generalist myasis-causing ectoparasite, between 2004 and 2020 on Floreana Island (Galápagos). Mortality was measured as the proportion of immature larvae found upon host nest termination. Over the time period, the avian vampire fly was most abundant and had low mortality in nests of the critically endangered medium tree finch (Camarhynchus pauper) and had the highest mortality in nests of hybrid tree finches (Camarhynchus spp.). Low larval mortality was also found in small tree (Camarhynchus parvulus) and small ground finch (Geospiza fuliginosa) nests. Selection could favour avian vampire flies that select medium tree finch nests and/or avoid hybrid nests. Overall, the finding of differences in avian vampire fly survival across host species is parsimonious with the idea that the introduced fly may be evolving towards host specialisation.