Hormone profiles of obligate avian brood parasites during the breeding season

The ultimate explanations for avian brood parasitism have been studied intensively as a model system for coevolution, but little is known about the proximate mechanisms, for example hormonal regulation, underlying brood parasitic behaviour. In this study, we explored seasonal hormone profiles in two brood parasitic Cuculus species breeding in the Republic of Korea. As brood parasites have relatively simple breeding stages without incubation and provisioning, we predicted that during the breeding season individuals would exhibit similar levels of testosterone (T) and stress‐induced corticosterone (CORT), hormones that are known to be closely related to the transition of breeding stages. We also assessed how these hormone profiles were associated with traits such as body size and sex. Overall, male cuckoos showed similarly high T levels throughout the breeding season, as predicted, but individual variation became greater as the season progressed. Individual CORT levels tended to decrease as the season progressed, although the decrease was significant only in Common Cuckoos Cuculus canorus. We also found that male Lesser Cuckoos Cuculus poliocephalus showed a much higher level of T than females, as expected, but this sexual difference was not observed in Common Cuckoos. Our results suggest that the seasonal hormone profiles of avian brood parasites are likely to be similar to typical hormone profiles expected for non‐brood parasites during the breeding season. This may suggest that not only the breeding cycle but also other factors such as social interaction may be affected by hormonal changes. Further studies are needed to fully understand the proximate mechanism of avian brood parasitism.     

Striking difference in response to expanding brood parasites by birds in western and eastern Beringia

Two species of obligate brood‐parasitic Cuculus cuckoos are expanding their ranges in Beringia. Both now breed on the Asian side, close to the Bering Strait, and are found in Alaska during the breeding season. From May to July 2017, we used painted 3D‐printed model eggs of two cuckoo host‐races breeding in northeastern Siberia to test behavioral responses of native songbirds on both sides of the Bering Strait, with particular attention to species that are known cuckoo hosts in their Siberian range. Each host nest was tested after the second egg was laid and, if possible, again 4 days later with a model of a different type. Although our Siberian study site was also outside the known breeding ranges of the cuckoos, we found that Siberian birds had strong anti‐parasite responses, with 14 of 22 models rejected. In contrast, birds in Alaska had virtually no detectable anti‐parasite behaviors, with only one of 96 models rejected; the rejecters were Red‐throated Pipits (Anthus cervinus). Such differences suggest that the cuckoos might successfully parasitize naïve hosts and become established in North America whether or not their historic host species are widely available.     

Predicting the responses of native birds to transoceanic invasions by avian brood parasites

Three species of brood parasites are increasingly being recorded as transoceanic vagrants in the Northern Hemisphere, including two Cuculus cuckoos from Asia to North America and a Molothrus cowbird from North America to Eurasia. Vagrancy patterns suggest that their establishment on new continents is feasible, possibly as a consequence of recent range increases in response to a warming climate. The impacts of invasive brood parasites are predicted to differ between continents because many host species of cowbirds in North America lack egg rejection defenses against native and presumably also against invasive parasites, whereas many hosts of Eurasian cuckoos frequently reject non‐mimetic, and even some mimetic, parasitic eggs from their nests. During the 2014 breeding season, we tested the responses of native egg‐rejecter songbirds to model eggs matching in size and color the eggs of two potentially invasive brood parasites. American Robins (Turdus migratorius) are among the few rejecters of the eggs of Brown‐headed Cowbirds (M. ater), sympatric brood parasites. In our experiments, robins rejected one type of model eggs of a Common Cuckoo (C. canorus) host‐race, but accepted model eggs of a second cuckoo host‐race as well as robin‐mimetic control eggs. Common Redstarts (Phoenicurus phoenicurus), frequent hosts of Common Cuckoos in Eurasia, rejected ～50% of model Brown‐headed Cowbird eggs and accepted most redstart‐mimetic control eggs. Our results suggest that even though some hosts have evolved egg‐rejection defenses against native brood parasites, the invasion of brood parasites into new continents may negatively impact both naïve accepter and coevolved rejecter songbirds in the Northern Hemisphere.     

Seasonal and diurnal patterns of black-capped chickadee (Poecile atricapillus) vocal production

Changes in vocal behaviour observed in temperate songbirds have been linked to changes in photoperiod. Research has focused on the fluctuation of hormones that lead to photosensitivity, photostimulation and photorefractoriness, as well as the 'dawn chorus' observed in numerous species. However, photoperiod in the natural environment is a complex event that occurs as seasons change. To determine the natural relationships between photoperiod and vocal behaviour we sampled vocal production of black-capped chickadees for three major vocal classes over one year at dawn, meridian and sunset. Fee-bee song production increased twice, once in the winter and once in the spring, and occurred almost exclusively at dawn. Chick-a-dee call production was highest in autumn and winter generally at the meridian. Gargle production did not differ significantly by season; however, the most gargle production occurred during the winter at the meridian.     

Experimental enlargement of nest size does not increase risk of predation or brood parasitism in the Great Reed Warbler Acrocephalus arundinaceus

We assessed whether nest size affects the probability of nest loss using dyads of large and small (large being twice the size of small) inactive Great Reed Warbler Acrocephalus arundinaceus nests placed at similar sites in Great Reed Warbler territories. Large nests were not predated significantly more frequently than small nests. Experimentally enlarged active Great Reed Warbler nests suffered non‐significantly higher predation compared with non‐manipulated control nests. Our experiments did not support the nest‐size hypothesis and suggested that nest size does not appear to be a factor affecting the risk of nest predation in this species. The probability of brood parasitism by the Common Cuckoo Cuculus canorus was also unaffected by experimental nest enlargement, supporting the commonly accepted hypothesis that the Common Cuckoo searches for suitable host nests by host activity during nest building rather than nest size.     

The evolution of host specialisation in avian brood parasites

Traditional ecological theory predicts that specialisation can promote speciation; hence, recently derived species are specialists. However, an alternative view is that new species have broad niches, which become narrower and specialised over time. Here, we test these hypotheses using avian brood parasites and three different measures of host specialisation. Brood parasites provide an ideal system in which to investigate the evolution of specialisation, because some exploit more than 40 host species and others specialise on only one. We find that young brood parasite species are smaller and specialise on a narrower range of host sizes, as expected, if specialisation is linked with the generation of new species. Moreover, we show that highly virulent parasites are more specialised, supporting findings in other host–parasite systems. Finally, we demonstrate that different measures of specialisation can lead to different conclusions, and specialisation indices should be designed taking into account the biology of each system.     

Automated acoustic monitoring of endangered common spadefoot toad populations reveals patterns of vocal activity

1. In the context of global amphibian decline, monitoring and restoration programmes are important. Acoustic monitoring is a possible approach for underwater vocalising species like the rapidly declining European common spadefoot toad (Pelobates fuscus). In this study, our aim was to design a dedicated software detector to be used in combination with programmable audio recorders to process the large amount of data generated by long-term acoustic monitoring and to use it for investigating the seasonal and circadian patterns of P. fuscus vocal activity.
2. The software detector targets advertisement calls of the species. Based on acoustic analysis of that call, we developed a detector that utilises both frequency and time features of the calls. Data collected during three breeding seasons in four known or potential P. fuscus breeding sites of north-eastern France were used to build a ground truth in order to test the performance of the detector. Then, we used the detector for analysing four acoustic monitoring campaigns conducted in two different sites over two breeding seasons to gain insight into the seasonal and circadian patterns of vocal activity of this species.
3. Evaluation of the P. fuscus call detector against a ground truth returned false-positive rates below 1.5% and true-positive rates ranging from 53% to 73%. These figures are compatible with long-term monitoring of the presence of the species. Running the software detector on standard hardware, the computation time for post-processing the 360 hr of a typical 3-month monitoring campaign was less than 1 day.
4. The seasonal pattern of P. fuscus underwater vocal activity is more complex than previously recognised. Over the whole ostensible 3-month breeding season, the actual time window for vocalising and breeding can last from a few days up to several weeks and may be split into clearly distinct episodes. When vocalisations occurred at both night- and daytime, the circadian vocal activity of P. fuscus occasionally proceeded uninterrupted for 24 hr but usually a several hour lull occurred immediately prior to sunset. When vocalisations occurred at both night- and daytime, the vocal activity pattern followed a bimodal distribution with a nocturnal highest peak of activity and a second peak occurring in the morning.
5. Our results demonstrate that it is feasible to monitor presence of P. fuscus in north-eastern France using a dedicated software detector combined with programmable audio recorders. Based on the outcomes of the detector applied to long-term audio data sets, we reveal temporal patterns of the vocal activity of the species and subsequently provide recommendations for attended and unattended acoustic monitoring.

     

Acoustic activity across a seabird colony reflects patterns of within-colony flight rather than nest density

Passive acoustic monitoring is increasingly being used as a cost-effective way to study wildlife populations, especially those that are difficult to census using conventional methods. Burrow-nesting seabirds are among the most threatened birds globally, but they are also one of the most challenging taxa to census, making them prime candidates for research into such automated monitoring platforms. Passive acoustic monitoring has the potential to determine presence/absence or quantify burrow-nesting populations, but its effectiveness remains unclear. We compared passive acoustic monitoring, tape-playbacks and GPS tracking data to investigate the ability of passive acoustic monitoring to capture unbiased estimates of within-colony variation in nest density for the Manx Shearwater Puffinus puffinus. Variation in acoustic activity across 12 study plots on an island colony was examined in relation to burrow density and environmental factors across 2 years. As predicted fewer calls were recorded when wind speed was high, and on moon-lit nights, but there was no correlation between acoustic activity and the density of breeding birds within the plots as determined by tape-playback surveys. Instead, acoustic indices correlated positively with spatial variation in the in-colony flight activity of breeding individuals detected by GPS. Although passive acoustic monitoring has enormous potential in avian conservation, our results highlight the importance of understanding behaviour when using passive acoustic monitoring to estimate density and distribution.     

Assessing spatial patterns and density of a dolphin population through signature whistles

Some dolphin species produce signature whistles, which may allow the identification of individual dolphins using passive acoustic monitoring (PAM). Identifying individuals by their sounds may enhance the opportunities for monitoring and addressing biological and ecological questions about these species. Here, we explored the potential of signature whistles to investigate ecological aspects of a resident bottlenose dolphin population. Using a limited data set, with few individuals recognized by signature whistles, combined with spatial capture-recapture (SCR) methods, we investigated how effective such approach is describing spatial use patterns and estimating density for this population. The data were collected using 4–6 stationary bottom-moored recorders. Since only eight signature whistles were identified, our density estimate may represent a subset of the entire population. However, even with only a few signature whistles identified, our results confirmed the center of the core area used by these dolphins as the area with the highest encounter probability. In addition, our results provided evidence that these dolphins have the same spatial use pattern at night as during the day. This study shows that SCR analysis of signature whistle data can improve our ecological knowledge and understanding of dolphin populations.     

Differences in intestinal microbiota between avian brood parasites and their hosts

The intestinal microbiota determines the effectiveness of digestion in vertebrates, and is influenced by the external environment (mainly the diet), gut characteristics, and phylogeny. Avian brood-parasitic nestlings of the sub-family Cuculinae develop in nests of phylogenetically distant passerines and can be fed with the host diet. If the shaping of bacterial communities is dominated by phylogenetic constraints, and therefore the microbiota of parasitic nestlings differs from that of host nestlings, the energy and micronutrients that parasites and hosts obtain from a similar amount of food would be different. In this case, the bacterial communities of parasitic and host nestlings would have important consequences with respect to brood parasite development. By experimentally creating mixed broods of magpies ( Pica pica ) and great spotted cuckoos ( Clamator glandarius ), we investigated their cloacal microbiota using ribosomal intergenic spacer analysis. We found significant differences in bacterial assemblages of the parasitic and host nestlings, although none of the phylotypes were specific in either great spotted cuckoos or magpies. Cuckoos presented more complex communities, which could help the brood parasitic life style and allow the digestion of food provided by different potential hosts. Moreover, the intestinal morphology is different between the two species due to phylogenetic differences in the two taxa, which would influence the dissimilar bacterial assemblages. The detected differences in microbiota of great spotted cuckoo and magpie nestlings, which might occur in other brood parasite–host systems, may imply a lower digestion efficiency in parasites. Thus, the higher level requirements of cuckoo nestlings may be explained, at least in part, by cuckoos having a suboptimal bacterial community for processing the host diet.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 406–414.     

The evolution of acceptance and tolerance in hosts of avian brood parasites

Avian brood parasites lay their eggs in the nests of their hosts, which rear the parasite's progeny. The costs of parasitism have selected for the evolution of defence strategies in many host species. Most research has focused on resistance strategies, where hosts minimize the number of successful parasitism events using defences such as mobbing of adult brood parasites or rejection of parasite eggs. However, many hosts do not exhibit resistance. Here we explore why some hosts accept parasite eggs in their nests and how this is related to the virulence of the parasite. We also explore the extent to which acceptance of parasites can be explained by the evolution of tolerance; a strategy in which the host accepts the parasite but adjusts its life history or other traits to minimize the costs of parasitism. We review examples of tolerance in hosts of brood parasites (such as modifications to clutch size and multi‐broodedness), and utilize the literature on host–pathogen interactions and plant herbivory to analyse the prevalence of each type of defence (tolerance or resistance) and their evolution. We conclude that (i) the interactions between brood parasites and their hosts provide a highly tractable system for studying the evolution of tolerance, (ii) studies of host defences against brood parasites should investigate both resistance and tolerance, and (iii) tolerance and resistance can lead to contrasting evolutionary scenarios.     

Community-level patterns of population recruitment in a generalist avian brood parasite, the brown-headed cowbird

The brown-headed cowbird (Molothrus ater) is a generalist brood parasite that typically parasitizes many host species in a single bird community. Population recruitment in a generalist parasite should be diverse with respect to host species; however, host-specific rates of cowbird recruitment have not been reported in any host community, and the determinants of host quality are poorly known. We studied the combined influence of parasitism level, nest abundance, and host quality on community-level patterns of cowbird recruitment in New Mexico, USA. Our objectives were to: (1) evaluate patterns of host use and quality; (2) compare cowbird egg investment and recruitment among host species; (3) identify host species of most importance to cowbird recruitment. Cowbirds parasitized 11 host species, with five “major” hosts experiencing high parasitism levels (≥1 cowbird egg/nest) and six minor hosts experiencing low parasitism levels (<0.3 cowbird eggs/nest). Parasitism level was not correlated with host species abundance, host mass, host nestling period length, or host success at fledging cowbirds. However, tree-nesting hosts were parasitized more than ground-nesters, and foliage-gleaners more than sally-foragers and ground-foragers. Average estimated survival to fledging of cowbird eggs laid in active host nests was 0.19. Cowbird recruitment was diverse with respect to hosts but was less evenly distributed across the host community than was cowbird egg investment because western tanagers (Piranga ludovicianus) fledged cowbirds more successfully than other hosts. This success in western tanagers was due to high cowbird survivorship in tanager nests and may be associated with the larger body size of tanagers relative to other hosts.     

Humpback whale song variations in La Reunion Island from 2016 to 2018 and in Madagascar in 2018

Male Megaptera novaeangliae produce complex and structured songs which are shared at the population level. Song patterns are culturally transmitted and evolve progressively through time, both over the breeding season and among years. The songs also undergo periods of relatively rapid change, termed “revolutions.” Acoustic monitoring was conducted from 2016 to 2018 in Reunion and throughout 2018 in Madagascar to assess spatiotemporal variation in song structures and population connectivity. A total of 46 high-quality song samples were selected, representing 2,760 min of recordings in Reunion. In Madagascar, 12 samples representing 240 min of recordings were analyzed. Analysis of songs revealed 11 phrases and their variants. Low levels of temporal variations were observed over the breeding season. Songs recorded in June were very similar to those recorded in September. Greater variation was observed between years, and some phrases identified in 2018 may have evolved from phrases recorded in 2017. More variants were described for each phrase type in 2018 compared to 2016. All themes recorded in Reunion were shared with Madagascar, suggesting a high degree of population connectivity during the breeding season.     

Modelling the maintenance of egg polymorphism in avian brood parasites and their hosts

In avian brood parasitism, egg phenotype plays a key role for both host and parasite reproduction. Several parrotbill species of the genus Paradoxornis are parasitized by the common cuckoo Cuculus canorus, and clear polymorphism in egg phenotype is observed. In this article, we develop a population genetics model in order to identify the key parameters that control the maintenance of egg polymorphism. The model analyses show that egg polymorphism can be maintained either statically as an equilibrium or dynamically with frequency oscillations depending on the sensitivity of the host against unlike eggs and how the parasite targets host nests with specific egg phenotypes. On the basis of the model, we discuss egg polymorphism observed in parrotbills and other host species parasitized by the cuckoo. We suggest the possibility that frequencies of egg phenotypes oscillate and we appeal for monitoring of cuckoo-host interactions over a large spatiotemporal scale.     

Seasonal occurrence of southeast Pacific blue whale songs in southern Chile and the eastern tropical Pacific

Passive acoustic data were collected January 2012 to April 2013 at four sites in the Chiloense Ecoregion (CER) in southern Chile (≈43°S–44°S, 71°W–73°W) and 1996–2002 from one site in the eastern tropical Pacific (ETP) (8°S, 95°W). Automatic detectors were used to detect the two songs (SEP1 and SEP2) described for southeast Pacific (SEP) blue whales. There was a strong seasonal pattern of occurrence of SEP songs in the CER from December to August, peaking March to May. In the ETP, the occurrence of songs was an order of magnitude lower but songs were present year‐round, with a peak around June. These findings support austral summer/autumn seasonal residency in the CER and a seasonal movement of blue whales towards the ETP during June/July, returning in December. Interannual differences in the ETP were possibly linked to the 1997–1998 El Niño event. At both study sites, SEP2 was significantly more common than SEP1; both songs largely followed the same temporal trends. These findings contribute to our understanding of the seasonal movements of endangered SEP blue whales and can inform conservation strategies, particularly in the CER coastal feeding ground. We recommend future year‐round passive acoustic studies in the CER and the ETP (e.g., near the Galapagos Islands), ideally coupled with oceanographic data.     

Seasonal and diurnal variation in vocal behaviour of the South Island robin

Abstract

The proportion of time spent by South Island robins (Petroica australis australis) of different sex, age, and status giving full song, subsong, and downscales, on a monthly and diurnal basis, is described. Females never gave full song. Males did so throughout the year, but least while moulting. Since bachelors sang significantly more than paired males, song probably functioned largely to attract females. Breeding males sang most during the pre-laying stage. From January to April adult males sang significantly more than immature males, but from May to July the reverse was true. Robins sang mainly in the early morning. Robins generally spent less than 0.5% of time during any stage of the breeding cycle giving sub-song. Outside the breeding season, males spent significantly more time giving sub-song than females, and adult males sang more than immature males. Robins in all categories gave more sub-song during the moult than afterwards. The diurnal pattern of sub-song production was bimodal. About half the downscales were followed by no obvious action from the caller or response from other robins, nor were the calls preceded by an obvious event. About 25% of the downscales were associated with interactions between members of a pair; the remainder were associated with territorial defence. Downscales probably served to maintain contact between members of a pair and to advertise possession of territory. These calls were heard rarely in the breeding season, and most frequently in April. Males gave downscales more than females, but use of downscales by both sexes was evenly distributed through the day.     

Song sharing and diversity in the Bering‐Chukchi‐Beaufort population of bowhead whales (Balaena mysticetus), spring 2011

Bowhead whales (Balaena mysticetus) of the Bering‐Chukchi‐Beaufort population migrate in nearshore leads through the Chukchi Sea each spring to summering grounds in the Beaufort Sea. As part of a population abundance study, hydrophones were deployed in the Chukchi Sea off Point Barrow, (12 April to 27 May 2011) and in the Beaufort Sea (12 April to 30 June 2011). Data from these sites were analyzed for the presence of bowhead whale song. We identified 12 unique song types sung by at least 32 individuals during ~95 h of recordings off Point Barrow. Six of these songs were detected at the Beaufort MARU site as well as six additional song types that were not analyzed. These results suggest a shared song repertoire among some individuals. This report represents the greatest number of songs to date during the spring migration for this population. We attribute this greater variety to population growth over the 30 yr since acoustic monitoring began in the early 1980s. Singing during early to mid‐spring is consistent with the hypothesis that song is a reproductive display, but further research is necessary to understand the exact function of this complex vocal behavior.     

Ecophysiology of egg rejection in hosts of avian brood parasites: new insights and perspectives

Egg rejection is the most effective and widespread defense used by host species to counteract the extreme fitness costs frequently imposed by obligate avian brood parasites. Yet, the proximate mechanisms underlying between- and within-individual variation in host responses remain poorly explored. Emerging evidence suggests that egg rejection is dependent on individual physiological states, and draws attention to the role of hormones as mediators of flexible antiparasitic responses. In this perspective article, I outline recent advances in our understanding of the proximate factors that mediate egg rejection. I also point out some areas where knowledge remains still lacking, especially those related to the development and maintenance of effective cognitive functions, the potential role of oxidative stress, immunological state, and developmental stressors. I propose new hypotheses that stimulate future research on behavioral host responses toward brood parasitism.