Rose Thorogood

Cuckoos Combat Socially Transmitted Defenses of Reed Warbler Hosts with a Plumage Polymorphism

Learning to Recognize a Cuckoo Species that are parasitized by cuckoos have evolved several strategies for trying to avoid having their nests hijacked—one of the most obvious being outright attacking, or mobbing, of cuckoos that enter the area. However, cuckoos are not without evolved defenses—most common cuckoo females look remarkably similar to a small hawk, and this mimicry deters mobbing. Thorogood and Davies (p. 578; see the Perspective by Mappes and Lindström) show that social learning in parasitized birds can thwart this protective mimicry. When hosts observe mimics being mobbed, they are more likely to mob them, themselves, later. However, the hosts will only mob the color morph that they observed being mobbed. This specificity may have allowed for the evolution and maintenance of two female morphs within common cuckoos. Parasitic cuckoos sporting new colors flourish after their warbler hosts learn to defend against the mainstream fashion. In predator-prey and host-parasite interactions, an individual’s ability to combat an opponent often improves with experience—for example, by learning to identify enemy signals. Although learning occurs through individual experience, individuals can also assess threats from social information. Such recognition could promote the evolution of polymorphisms if socially transmitted defenses depend on enemy morph frequency. This would allow rare variants to evade detection. Female brood parasitic common cuckoos, Cuculus canorus, are either gray or rufous. The gray morph is a Batesian mimic whose hawk-like appearance deters host attack. Hosts reject this disguise through social learning, increasing their own defenses when they witness neighbors mobbing a cuckoo. Our experiments reveal that social learning is specific to the cuckoo morph that neighbors mob. Therefore, while neighbors alert hosts to local cuckoo activity, frequency-dependent social information selects for a cuckoo plumage polymorphism to thwart host detection. Our results suggest that selection for mimicry and polymorphisms comes not only from personal experience but also from social learning.

Maternally invested carotenoids compensate costly ectoparasitism in the hihi

Dietary ingested carotenoid biomolecules have been linked to both improved health and immunity in nestling birds. Here, we test whether maternally invested egg carotenoids can offset the cost of parasitism in developing nestling hihi (Notiomystis cincta) from the bloodsucking mite (Ornithonyssus bursa). Our results reveal clear negative effects of parasitism on nestlings, and that maternally derived carotenoids compensate this cost, resulting in growth parameters and ultimate mass achieved being similar to nonparasitized young. Our results offer an unique example of a direct positive relationship between enhanced maternal investment of carotenoids and an ability to cope with a specific and costly parasite in young birds. As O. bursa infestations reduce population viability in hihi, our findings also highlight the importance of key nutritional resources for endangered bird populations to better cope with common parasite infestations.

Reed warbler hosts fine-tune their defenses to track three decades of cuckoo decline.

Interactions between avian hosts and brood parasites can provide a model for how animals adapt to a changing world. Reed warbler (Acrocephalus scirpaceus) hosts employ costly defenses to combat parasitism by common cuckoos (Cuculus canorus). During the past three decades cuckoos have declined markedly across England, reducing parasitism at our study site (Wicken Fen) from 24% of reed warbler nests in 1985 to 1% in 2012. Here we show with experiments that host mobbing and egg rejection defenses have tracked this decline in local parasitism risk: the proportion of reed warbler pairs mobbing adult cuckoos (assessed by responses to cuckoo mounts and models) has declined from 90% to 38%, and the proportion rejecting nonmimetic cuckoo eggs (assessed by responses to model eggs) has declined from 61% to 11%. This is despite no change in response to other nest enemies or mimetic model eggs. Individual variation in both defenses is predicted by parasitism risk during the hosts egg‐laying period. Furthermore, the response of our study population to temporal variation in parasitism risk can also explain spatial variation in egg rejection behavior in other populations across Europe. We suggest that spatial and temporal variation in parasitism risk has led to the evolution of plasticity in reed warbler defenses.

Sense and sensitivity: responsiveness to offspring signals varies with the parents' potential to breed again

How sensitive should parents be to the demands of their young? Offspring are under selection to seek more investment than is optimal for parents to supply, which makes parents vulnerable to losing future fitness by responding to manipulative displays. Yet, parents cannot afford to ignore begging and risk allocating resources inefficiently. Here, we show that parents may solve this problem by adjusting their sensitivity to begging behaviour in relation to their own likelihood of breeding again, a factor largely neglected in previous analyses of parent–offspring interactions. In two carotenoid-supplementation experiments on a New Zealand passerine, the hihi Notiomystis cincta, we supplemented adults to enhance their propensity to breed again, and supplemented entire broods to increase their mouth colour, thus enhancing their solicitation display. We found that adults that attempted two breeding attempts a season were largely insensitive to the experimentally carotenoid-rich gapes of their brood, whereas those that bred just once responded by increasing their rate of provisioning at the nest. Our results show that parents can strategically vary their sensitivity to begging in relation to their future reproductive potential. By restricting opportunities for offspring to influence provisioning decisions, parents greatly limit the potential for offspring to win parent–offspring conflict.

Salmonella Typhimurium in Hihi, New Zealand

To the Editor: The recent finding of a previously unrecorded Salmonella strain in an endangered New Zealand passerine (the hihi, Notiomystis cincta; [1]) offers the rare opportunity to observe the initial arrival and pathology of an epizootic and to determine its population-level effect. Over 8 days in February 2006, 6 freshly dead hihi were discovered in a free-living island population. Pathologic findings were similar: birds were in good body condition with substantial subcutaneous fat reserves and no gross lesions in the crop, indicating death from a highly pathogenic disease. Histopathologic examination showed septicemia and inflammatory necrosis of organs, particularly the liver and spleen, typical of salmonellosis in birds (2). Microbiologic examination of liver samples isolated heavy growths of the bacterium Salmonella enterica serotype Typhimurium DT195. During the same period, 3 more dead hihi were found, but they were too decomposed for postmortem examination. Hihi are nectar-feeders that declined to near extinction after European colonization of New Zealand and survived on a single island refuge (Hauturu). Since 1980, 14 attempts have been made to reintroduce the species to 6 other sites, resulting in 3 new populations that persist with management. The S. Typhimurium DT195 outbreak occurred within a reintroduced population on Tiritiri Matangi Island. Management includes providing supplementary food (sugar water) diluted with local rain water; feeders are sterilized before each use. Because disease in hihi is closely monitored, the outbreak indicates that S. Typhimurium DT195 is a novel serotype for this species. During December 2005, fecal screening of 18 broods (37 nestlings) from Tiritiri Matagni Island found no evidence of enteric pathogens; screenings in February and May 2005 (40 adult and juvenile birds) from Tiritiri Matagni Island similarly returned negative results. Screening in all hihi populations during 2004 also found no evidence of Salmonella infection (32 adults and juveniles at Tiritiri Matangi, 29 at Hauturu, and 27 at Kapiti), and a 15-year pathology database from 230 dead hihi collected across these populations and a captive breeding facility lists no salmonellosis cases (J.G. Ewen and M.R. Alley, unpub. data). Documentation of the emergent stages of infectious disease in endangered species is rare (3,4). This bacterium strain is absent from New Zealand’s livestock and wildlife (www.surv.esr.cri.nz/enteric_reference/nonhuman_salmonella.php). Nontyphoid Salmonella spp. are a major health concern worldwide (5), and New Zealand conducts intensive surveillance to maintain food safety. The New Zealand Wildlife Health Centre has not reported S. Typhimurium DT195 despite necropsies of >3,000 wild birds during 1996–2006, which suggests this strain is rare in New Zealand, despite its presence in other countries (6). S. Typhimurium DT195 has been detected in 3 human patients in New Zealand (1 each in 2002, 2003, and 2006). The S. Typhimurium DT195 isolated from hihi in the February 2006 outbreak were indistinguishable from those isolated from the human case-patient in 2006 (Figure, panel A) (2). Tiritiri Matangi is an isolated island nature reserve 3 km off the New Zealand coast, which prevents movement of hihi to other areas. How this strain appeared in a human patient and as an epizootic in an isolated island nature reserve is intriguing. The most recent human case was diagnosed on the North Island of New Zealand, but the person was not living in close proximity to the birds. Tiritiri Matangi receives ≈30,000 human visitors per year, but whether the person with S. Typhimurium DT195 ever visited is not known. An unidentified infection source may be present in New Zealand that periodically spills over into alternate host species. Given their historic isolation, hihi may have low or no exposure to many diseases, which makes negative reactions more likely (7). The transmission of S. Typhimurium DT195 to hihi caused a substantial drop in their population (Figure). The 9 bodies recovered represent a small proportion of the birds that died, given the difficulty of recovering dead birds (8). We used mark–recapture analysis (9) to estimate that adult survival probability was 0.64 (95% confidence interval [CI] 0.53–0.74) from September 2005 through February 2006, compared with an expected survival of 0.87 (95% CI 0.85–0.89), according to data from the previous 10 years (data not shown). The quotient of these 2 probabilities is 0.74 (95% CI 0.60–0.84); hence, we can infer that ≈26% of birds were killed by the epizootic. Figure Survival rates from September–February and February–September among hihi in New Zealand during 1996–2006, estimated by using mark–recapture analysis, show that the transmission of Salmonella Typhimurium DT195 to hihi during ... With such high virulence, fade-out may occur as susceptible individuals are rapidly removed from the population (10). Subsequent monitoring has failed to detect further evidence of S. Typhimurium DT195. This apparent fade-out mirrors classic predictions from epidemiology (10). It is unknown whether the pathogen resides in resistant hihi or whether threats from the unknown source remain. The key issues for endangered species management are identifying the risk of pathogens entering a host population and the probability that this occurrence would result in host extinction (3). The 2006 salmonellosis outbreak in hihi could easily have remained undetected, leaving conservation managers unaware of what caused the population decline. How often this occurs in poorly monitored wildlife is unknown. This study shows the need for increased awareness of these processes when considering biodiversity conservation.

Demographic consequences of adult sex ratio in a reintroduced hihi population.

1. Male-biased adult sex ratios are frequently observed in free-ranging populations and are known to cause changes in mating behaviours including increased male harassment of females, which can cause injury to females and/or alter female behaviour during breeding. 2. Although we can explain why such behaviours may evolve and have studied their impacts on individuals when it does, we know very little about the demographic consequences of harassment caused by changes in adult sex ratio. 3. Using a 12-year longitudinal data set of a free-living and endangered New Zealand passerine, the hihi (Notiomystis cincta), we show that a changing adult sex ratio has little or no effect on adult female survival or the number of fledglings produced per female. This is despite clear evidence of male harassment of breeding females when the sex ratio was male biased (up to three males per female). 4. The length of the study and major fluctuations in sex ratio observed made it possible to obtain narrow confidence or credible intervals for effect sizes, showing that any effect of sex ratio on demographic rates were small. 5. Our results provide rare empirical evidence for the demographic consequences of biased adult sex ratios in the wild and particularly in a conservation context.

Foraging for carotenoids: do colorful male hihi target carotenoid-rich foods in the wild?

Lay Summary Birds that color their feathers with dietary carotenoid pigments are expected to seek out these pigments when they are molting. We show that molting male hihi, who express carotenoid-based plumage, seek out naturally occurring foods that are rich in carotenoid pigments. Female hihi, who do not express carotenoid-based plumage, do not seek out carotenoid-rich foods. This lends strength to the idea that carotenoid-based plumage reveals an individual’s foraging ability.

Simple techniques for sexing nestling hihi (Notiomystis cincta) in the field

Abstract Whilst the sexes of adult hihi (Notiomystis cincta) are easily distinguished by their dim orphic plumage, male and female nestling and juvenile hihi appear very similar. Hihi is a threatened bird species, and knowledge of the sex of young is important for conservation management and research. Although molecular sexing techniques exist, an immediate and cheap method for identifying sexes of young birds in the field would be advantageous. In this study, we tested the reliability of morphometric measurements and emerging plumage colour to sex nestlings when they are close to fledging. We conducted a discriminant function analysis on tarsus length, body mass, and head‐bill length measurements of 313 individual nestlings of known sex produced on Tiritiri Matangi Island over the six breeding seasons 1998/99 to 2003/04. Typically, the accuracy of discriminant functions for classification is assessed by reappli‐cation to the original sample. Here we first tested the accuracy of the function (included tarsus length and body mass) using a jack‐knife reclassification procedure. Second, we applied the function to 85 individuals of the 2004/05 cohort, with similar success (jack‐knife reclassification of the six cohorts of 1998/99 to 2003/04, 76.4%; 2004/05 cohort, 69.4%). Use of emerging plumage colour on the 2004/05 cohort was similarly effective (72.9% accuracy), but more so when limited to well‐feathered nestlings. Depending upon the probability of error acceptable to a researcher, these methods may prove useful, but do not replace the more accurate methods for sexing nestling hihi by molecular sexing or observations of surviving recruits.

Copy parents or follow friends? Juvenile foraging behaviour changes with social environment

The first few months of juvenile independence is a critical period for survival as young must learn new behaviours to forage efficiently. Social learning by observing parents (vertical transmission) or others (horizontal/oblique transmission) may be important to overcome naivety, but these tutors are likely to differ in their reliability due to variation in their own experience. How young animals use different social information sources, however, has received little attention. Here we tested if wild juvenile hihi (Notiomystis cincta, a New Zealand passerine) retained foraging behaviours learned from parents, or if behaviour changed after independence in response to peers. We first trained parents with feeders during chick rearing: one-third could access food from any direction, one-third could access food from one side only, and the remaining third had no feeder. During post-fledge parental care, juveniles chose the same side as their parents. Once independent, juveniles formed mixed-treatment groups naturally so we then presented feeders with two equally profitable sides. Juveniles with natal feeder experience were quicker to use these feeders initially, but side choice was now random. Over time, however, juveniles converged on using one side of the feeder (which differed between groups). This apparent conformity was because juvenile hihi paid attention to the behaviour of their group and were more likely to choose the locally-favoured side as the number of visits to that side increased. They did not copy the choice of specific individuals, even when they were more social or more familiar with the preceding bird. Our study shows that early social experiences with parents affect foraging decisions, but later social environments lead juveniles to modify their behaviour.

One of the gang: social group dynamics in a juvenile passerine bird

Living in groups comes with many potential benefits, especially for juveniles. Naïve individuals may learn how to forage, or avoid predators through group vigilance. Understanding these benefits, however, requires an appreciation of the opportunities juveniles have to associate with (and learn from) others. Here we describe social groups in terms of residency, movement, relatedness, and social associations from the perspective of juvenile hihi, a threatened New Zealand passerine bird. Over three years, we identified individuals in groups, their relatedness, and behavioural interactions. Using multistate analysis, we compared movement and residency of adults and juveniles and found that groups were composed predominately of juveniles which remained at group sites for longer than more transient adults. Movement of juveniles between groups did occur but was generally low. There was no evidence that siblings and parents were likely to be seen in groups together. With an initial understanding of group structure, we next asked what characteristics predicted assortment in social network associations. By identifying groups of co-occurring juveniles from time-stamped observations of individual hihi and building a social network, we found that juveniles were most likely to associate with other juveniles. Associations were also predominantly based on locations where hihi spent the most time, reflecting limited movement among separate groups. We suggest groups are best described as “gangs” where young hihi have little interaction with adults. These spatially-separated groups of juveniles may have consequences for social information use during the first few months of independence in young birds.