Zealand Robins Research Articles

Improved methods for estimating abundance and related demographic parameters from mark-resight data.

Over the past decade, there has been much methodological development for the estimation of abundance and related demographic parameters using mark‐resight data. Often viewed as a less‐invasive and less‐expensive alternative to conventional mark recapture, mark‐resight methods jointly model marked individual encounters and counts of unmarked individuals, and recent extensions accommodate common challenges associated with imperfect detection. When these challenges include both individual detection heterogeneity and an unknown marked sample size, we demonstrate several deficiencies associated with the most widely used mark‐resight models currently implemented in the popular capture‐recapture freeware Program MARK. We propose a composite likelihood solution based on a zero‐inflated Poisson log‐normal model and find the performance of this new estimator to be superior in terms of bias and confidence interval coverage. Under Pollock's robust design, we also extend the models to accommodate individual‐level random effects across sampling occasions as a potentially more realistic alternative to models that assume independence. As a motivating example, we revisit a previous analysis of mark‐resight data for the New Zealand Robin (Petroica australis) and compare inferences from the proposed estimators. For the all‐too‐common situation where encounter rates are low, individual detection heterogeneity is non‐negligible, and the number of marked individuals is unknown, we recommend practitioners use the zero‐inflated Poisson log‐normal mark‐resight estimator as now implemented in Program MARK.

Memory Performance Influences Male Reproductive Success in a Wild Bird

Despite decades of comparative research, how selection shapes the evolution of cognitive traits remains poorly understood [1-3]. Several lines of evidence suggest that natural selection acts on spatial memory in food-caching species [3-6]. However, a link between reproductive fitness and spatial memory ability has yet to be demonstrated in any caching species [1, 3, 6]. Here, we show that memory performance influences reproductive success differentially for males and females in a caching songbird, the New Zealand robin (Petroica longipes). Males' memory performance in a spatial task during winter influenced their subsequent breeding success; individuals with more accurate performance produced more fledglings and independent offspring per nesting attempt. Males with superior memory performance also provided an increased proportion of large prey items to chicks in the nest and spent less time flying while foraging and provisioning. No such effects were found for females. Previous research reveals that trade-offs may constrain selection and act to maintain variation in cognitive traits [7]. The gender dimorphism in the reproductive benefits of robin memory performance suggests an additional role for divergent selection between the sexes in constraining runaway selection on male memory ability [8], ultimately maintaining variation in this cognitive trait.

Know your enemy? Conservation management causes loss of antipredator behaviour to novel predators in New Zealand robins

While studies of animal behaviour have performed a key role in informing conservation management of threatened species, antipredator behaviours are rarely considered in conservation decision making. This study assessed the impact of the translocation of an endemic New Zealand bird to a predator-free ecosanctuary on its antipredator behaviour. We compared antipredator responses of South Island robins, Petroica australis australis, found inside the ecosanctuary with those of robins inhabiting local predator-dense forests, using taxidermy models of a rat, Rattus norvegicus, and stoat, Mustela erminea. Although mammalian predators are relatively novel in New Zealand, some endemic species such as South Island robins recognize them and show antipredator behaviours. We determined the rate of loss of behaviours after release into the ecosanctuary since founders were translocated from predator-dense environments. Robins inhabiting the ecosanctuary exhibited lower intensities of antipredator behaviour towards the model rat than robins in predator-dense areas within at least 3 years after translocation, a shorter period than previously suggested. A recent stoat incursion in the sanctuary provided the opportunity to discern whether robins regained predator-specific antipredator behaviours or displayed heightened generic vigilance to all novel predators. The more intense antipredator responses recorded towards the model stoat than the model rat within the ecosanctuary indicated that the robins had regained their behaviours towards stoats but had not generalized the predatory features of the stoat to the rat. Our study raises concerns regarding the viability of sanctuary populations as sources for future translocations into areas with predators. We recommend antipredator training to improve species survival.

A Facet Theory Analysis of the Structure of Cognitive Performance in New Zealand Robins (Petroica longipes)

In this report we analyse the cognitive performance of New Zealand Robins (Petroica longipes) using facet theory, smallest space analysis (SSA) and partial order scalogram analysis (POSA). The data set we analyse was originally subjected to principle component analysis in order to develop a test-battery for avian cognitive performance. We extend these analyses by proposing a two facet rather than a single component solution using SSA and we characterize individual birds by their scores on all tasks using POSA. We note problems with the small sample size and call for our exploratory analyses to be replicated using a larger sample of birds and for the development of further test items using the facet theory’s tool the mapping sentence. We suggest that facet theory and the mapping sentences are research approaches suitable for conceiving, designing, analysing and developing theory that may be used within avian cognitive research. We conclude by proposing a mapping sentence for avian cognition, which forms an adaptable template for future avian cognition research.

Male New Zealand robin (Petroica longipes) song repertoire size does not correlate with cognitive performance in the wild

Songbirds (Oscines) possess specialized brain regions responsible for the learning and production of their elaborate vocalizations. It has previously been suggested that song may provide a useful indicator of individual cognitive ability, due to its underlying neurobiology, individual variability, and links to developmental health. To date the relationship between song repertoire and cognitive performance has been most extensively examined in wild song sparrows (Melospiza melodia). Two initial studies found that song repertoire size was negatively correlated with spatial memory performance, but positively correlated with inhibitory control performance in a detour reaching task. However, a recent attempt to replicate this research found opposing patterns of association between each of these cognitive measures and song repertoire. It has been suggested that we may gain further insight into the relationship between song learning and other cognitive abilities by investigating species with different ecology to song sparrows, namely caching species. Here we re-examine the relationship between song repertoire size, spatial memory and detour reaching performance in a caching songbird, the toutouwai, or North Island robin (Petroica longipes). We tested both male and female toutouwai in a detour reaching task and a spatial memory task, while also recording the individual song repertoire size for 21 of the males tested. All experiments were carried out in the wild on individuals' territories. We found no associations between song repertoire and performance in either cognitive task, or between the two cognitive task performances. Our results provide further evidence that song repertoire is unlikely to be a useful signal of individual spatial memory and inhibitory control ability in songbirds.

Can cormorants count?

Can cormorants count?

The ontogeny of food-caching behaviour in New Zealand robins (Petroica longipes)

Hoarding or caching behaviour is a widely-used paradigm for examining a range of cognitive processes in birds, such as social cognition and spatial memory. However, much is still unknown about how caching develops in young birds, especially in the wild. Studying the ontogeny of caching in the wild will help researchers to identify the mechanisms that shape this advantageous foraging strategy. We examined the ontogeny of food caching behaviour in a wild New Zealand passerine, the North Island robin (Petroica longipes). For 12-weeks following fledging, we observed 34 juveniles to examine the development of caching and cache retrieval. Additionally, we compared the caching behaviour of juveniles at 12 weeks post-fledging to 35 adult robins to determine whether juveniles had developed adult-like caching behaviour by this age. Juveniles began caching mealworms shortly after achieving foraging independency. Multivariate analyses revealed that caching rate increased and handling time decreased with increasing age. Juveniles spontaneously began retrieving caches as soon as they had begun to cache and their retrieval rates then remained constant throughout their ensuing development. Likewise, the number of sites used by juveniles did not change with age. Juvenile sex, caregiver sex and the duration of post-fledging parental care did not influence the development of caching, cache retrieval, the number of cache sites used and the time juveniles spent handling mealworms. At 12 weeks post-fledging, juveniles demonstrated levels of caching, cache retrieval and cache site usage that were comparable to adults. However, juvenile prey handling time was still longer than adults. The spontaneous emergence of cache retrieval and the consistency in the number of cache sites used throughout development suggests that these aspects of caching in North Island robins are likely to be innate, but that age and experience have an important role in the development of adult caching behaviours.

Male New Zealand robins (Petroica longipes) cater to their mate\u2019s desire when sharing food in the wild

In many species that have bi-parental care, food-sharing males provide vital nutritional resources to their mates during reproduction. However, it is currently unknown whether females can signal specific desires to their mates, or if males can cater to female desire in the wild. Here we investigate whether and how wild male North Island robins (Petroica longipes) respond to changes in their mates’ desires and nutritional need when sharing food. We demonstrate that wild female robins’ desire for particular foods changes over short time periods; when given the choice between two types of insect larvae, females prefer the type they have not recently eaten. In our experiments, wild male robins preferentially shared the larvae type that their mate was most likely to desire and also increased the quantity of food shared if she had begun incubating. Males catered to their mates’ desire when female behaviour was the only cue available to guide their choices. This is the first evidence that females may behaviourally communicate their specific food desires to their mates, enabling males to cater to fine-scale changes in their mates’ nutritional requirements in the wild. Such a simple behaviour-reading mechanism has the potential to be widespread among other food-sharing species.

Commentary: Wild psychometrics: Evidence for ‘general’ cognitive performance in wild New Zealand robins, Petroica longipes

A commentary on Wild psychometrics: Evidence for ‘general’ cognitive performance in wild New Zealand robins, Petroica longipes by Shaw, R. C., Boogert, N. J., Clayton, N. S., and Burns, K. C. (2015). Anim. Behav. 109, 101–111. doi: 10.1016/j.anbehav.2015.08.001

Diversity in the Toll-Like Receptor Genes of the African Penguin (Spheniscus demersus).

The African penguin, Spheniscus demersus, is listed as Endangered by the IUCN Red List of Threatened Species due to the drastic reduction in population numbers over the last 20 years. To date, the only studies on immunogenetic variation in penguins have been conducted on the major histocompatibility complex (MHC) genes. It was shown in humans that up to half of the genetic variability in immune responses to pathogens are located in non-MHC genes. Toll-like receptors (TLRs) are now increasingly being studied in a variety of taxa as a broader approach to determine functional genetic diversity. In this study, we confirm low genetic diversity in the innate immune region of African penguins similar to that observed in New Zealand robin that has undergone several severe population bottlenecks. Single nucleotide polymorphism (SNP) diversity across TLRs varied between ex situ and in situ penguins with the number of non-synonymous alterations in ex situ populations (n = 14) being reduced in comparison to in situ populations (n = 16). Maintaining adaptive diversity is of vital importance in the assurance populations as these animals may potentially be used in the future for re-introductions. Therefore, this study provides essential data on immune gene diversity in penguins and will assist in providing an additional monitoring tool for African penguin in the wild, as well as to monitor diversity in ex situ populations and to ensure that diversity found in the in situ populations are captured in the assurance populations.

Addition and subtraction in wild New Zealand robins

This experiment aimed to investigate proto-arithmetic ability in a wild population of New Zealand robins. We investigated numerical competence from the context of computation: behavioural responses to arithmetic operations over small numbers of prey objects (mealworms). Robins’ behavioural responses (such as search time) to the simple addition and subtraction problems presented in a Violation of Expectancy (VoE) paradigm were measured. Either a congruent (expected) or incongruent (unexpected) quantity of food items were hidden in a trap door out of view of the subject. Within view of the subject, a quantity of items were added into (and in some cases subtracted from) the apparatus which was either the same as that hidden, or different. Robins were then allowed them to find a quantity that either preserved or violated addition and subtraction outcomes. Robins searched around the apparatus longer when presented with an incongruent scenario violating arithmetic rules, demonstrating potential proto-arithmetic awareness of changes in prey quantity.This article is part of a Special Issue entitled: Cognition in the wild.

Variation at innate immunity Toll-like receptor genes in a bottlenecked population of a New Zealand robin.

Toll-like receptors (TLRs) are an ancient family of genes encoding transmembrane proteins that bind pathogen-specific molecules and initiate both innate and adaptive aspects of the immune response. Our goal was to determine whether these genes show sufficient genetic diversity in a bottlenecked population to be a useful addition or alternative to the more commonly employed major histocompatibility complex (MHC) genotyping in a conservation genetics context. We amplified all known avian TLR genes in a severely bottlenecked population of New Zealand's Stewart Island robin (Petroica australis rakiura), for which reduced microsatellite diversity was previously observed. We genotyped 17–24 birds from a reintroduced island population (including the 12 founders) for nine genes, seven of which were polymorphic. We observed a total of 24 single-nucleotide polymorphisms overall, 15 of which were non-synonymous, representing up to five amino-acid variants at a locus. One locus (TLR1LB) showed evidence of past directional selection. Results also confirmed a passerine duplication of TLR7. The levels of TLR diversity that we observe are sufficient to justify their further use in addressing conservation genetic questions, even in bottlenecked populations.

Strategic Regulation of Body Mass and Singing Behavior in New Zealand Robins

AbstractThe ‘small bird in winter’ paradigm states that body mass is a balance between the conflicting demands of carrying enough energy to survive nightly fasts while minimizing the risk of predation associated with carrying additional fat reserves. We conducted a short‐term food‐supplementation experiment during which New Zealand robins (Petroica australis) were provided with food on the second day of a 3‐d trial. This allowed us to test two predictions from models of strategic mass regulation in small birds: (1) individual birds reach the same end‐of‐day mass despite differences in their initial morning mass while, (2) using surplus energy for increased singing. As expected, robins gained mass at a higher rate early in the morning on the fed day than they did on either of the two control days, but there was no significant difference in their evening masses across the 3 d of the experiment despite birds on day 3 starting at higher initial masses than birds on day 1. Robins displayed a significantly higher rate of singing when receiving food supplements on day 2, supporting a link between energetic reserves and behavior. Our results suggest that potentially energetically costly behaviors, such as song production, are sensitive to short‐term changes in energy reserves, and that both state and behavioral predictions can be successfully integrated to provide tests of state‐based models of behavior.

Facial bristle feather histology and morphology in New Zealand birds: Implications for function

Knowledge of structure in biology may help inform hypotheses about function. Little is known about the histological structure or the function of avian facial bristle feathers. Here we provide information on morphology and histology, with inferences for function, of bristles in five predominantly insectivorous birds from New Zealand. We chose species with differing ecologies, including: brown kiwi (Apteryx mantelli), morepork (Ninox novaezealandae), hihi (Notiomystis cincta), New Zealand robin (Petroica australis), and New Zealand fantail (Rhipidura fuliginosa). Average bristle length corrected for body size was similar across species. Bristles occurred in distinct groups on different parts of the head and upper rictal bristles were generally longest. The lower rictal bristles of the fantail were the longest possessed by that species and were long compared to bristles of other species. Kiwi were the only species with forehead bristles, similar in length to the upper rictal bristles of other species, and the lower rictal bristles of fantails. Herbst corpuscles (vibration and pressure sensitive mechanoreceptors) were found in association with bristle follicles in all species. Nocturnal and hole-nesting birds had more heavily encapsulated corpuscles than diurnal open-nesting species. Our results suggest that avian facial bristles generally have a tactile function in both nocturnal and diurnal species, perhaps playing a role in prey handling, gathering information during flight, navigating in nest cavities and on the ground at night and possibly in prey-detection. These differing roles may help explain the observed differences in capsule thickness of the corpuscles.

Is lack of evidence of inbreeding depression in a threatened New Zealand robin indicative of reduced genetic load?

Continuous inbreeding exposes deleterious recessive alleles to selection and can thereby lead to partial purging of the genetic load and reduced inbreeding depression. Purging has been well documented in experimental laboratory populations, but evidence of reduced inbreeding depression due to purging in wild populations is largely lacking. This study examines the inbreeding load associated with juvenile survival at a protected island site of a bottlenecked population of the Stewart Island robin Petroica australis rakiura. Based on a complete pedigree of the island population, we found little evidence that inbreeding coefficients explained any additional variation in juvenile survival, once demographic factors such as the effects of density, timing of fledging and age of mother were taken into account. Lethal equivalents, a standardized measure of the strength of inbreeding depression, were close to zero (B=0.24, 95% CI=−1.92-1.04, n=326) and lower than that documented for an island population of a widespread congener (B=6.71, 95% CI=−0.66-14.08, n=238) and for several other species for which significant inbreeding depression was detected (B=1.30-7.47). There are several reasons as to why studies can fail to detect pedigree-based inbreeding depression in wild populations, but evidence presented here of low lethal equivalents and relatively high survival of both inbred and non-inbred juveniles are consistent with a population that has undergone partial purging of its genetic load during historical population bottlenecks. Although our study does not imply a complete absence of inbreeding depression, it is one of the first studies of a wild population where weak inbreeding depression for juvenile survival appears to be associated with a prolonged bottleneck.

Declines in common, widespread native birds in a mature temperate forest

Common, widespread species are important for ecosystem structure and function. Although such species have declined in some parts of the world, for most ecosystems there is a lack of information about changes in the population status of common species. We studied the abundance of common, widespread forest birds in Nelson Lakes National Park, New Zealand using standardised 5-min bird counts, carried out over a 30-year time span. There was a significant change in the bird community structure during this period. Five native species (bellbird, rifleman, grey warbler, New Zealand tomtit and tui) declined in abundance during the 30 years. All of these declined in abundance at low but not high altitudes, and the decline was substantial for all but New Zealand tomtit and tui. Three other native species increased in abundance (silvereye, yellow-crowned parakeet and New Zealand robin). There was no change in the abundance of introduced blackbirds. We suggest that invasive alien species are the most likely cause of the ongoing declines in common native species. A peak in brushtail possum abundance and the arrival of a new species of Vespula wasp were two large changes in Nelson Lakes forests that occurred during this study. Both are likely to have added to the ongoing impacts of predation by introduced rats and stoats. We suggest that it is necessary to actively manage introduced species in order to maintain populations of widespread, common native bird species in New Zealand.

The Effect of Male Incubation Feeding, Food and Temperature on the Incubation Behaviour of New Zealand Robins

AbstractBecause of finite resources, organisms face conflict between their own self‐care and reproduction. This conflict is especially apparent in avian species with female‐only incubation, where females face a trade‐off between time allocated to their own self‐maintenance and the thermal requirements of developing embryos. We recorded incubation behaviour of the New Zealand robin (Petroica longipes), a species with female‐only incubation, male incubation feeding and high nest predation rates. We examined how male incubation feeding, ambient temperature and food availability (invertebrate biomass) affected the different components of females’ incubation behaviour and whether incubation behaviour explained variation in nest survival. Our results suggest that male incubation feeding rates of 2.8 per hour affect the female’s incubation rhythm by reducing both on‐ and off‐bout duration, resulting in no effect on female nest attentiveness, thus no support for the female‐nutritional hypothesis. The incubation behaviours that we measured did not explain nest survival, despite high nest predation rates. Increased ambient temperature caused an increase in off‐bout duration, whereas increased food availability increased on‐bout duration. While males play a vital role in influencing incubation behaviour, female robins attempt to resolve the trade‐off between their own foraging needs and the thermal requirements of their developing embryos via alternating their incubation rhythm in relation to both food and temperature.

From NOREMARK to MARK: software for estimating demographic parameters using mark–resight methodology

Mark–resight methods can be a less expensive and less invasive alternative to traditional mark–recapture for estimating abundance and related demographic parameters. This is because only a single marking event is required, and subsequent sighting data from both marked and unmarked individuals are used for estimation. Mark–resight is therefore particularly appealing when working with limited budgets or sensitive species. These methods have been applied to many taxa, including avians such as Bald Eagles (Haliaeetus leucocephalu), Sage Grouse (Centrocercus urophasianus), and New Zealand Robins (Petroica australis). However, previous model and software development overwhelmingly focused on abundance estimation and did not extend much beyond classic Lincoln–Petersen methods. For this purpose, Program NOREMARK provided a convenient, but limited, means for analysis. To address these limitations, a new suite of likelihood-based mark–resight estimators has been developed and implemented within Program MARK. Unlike the estimators in NOREMARK, these new models provide a theoretical basis for model selection and multimodel inference, the incorporation of spatio-temporal and individual covariate information, full utilization of the robust design (including the estimation of survival and state transition probabilities), and all the other analysis tools that MARK provides. In addition, MARK no longer requires that the exact number of marked individuals available for sighting be known, thereby greatly extending the potential use of mark–resight methodology for population monitoring. Here, we provide a review of mark–resight methodology and present the various mark–resight estimators that are implemented in Program MARK.

Bayesian analysis of abundance for binomial sighting data with unknown number of marked individuals

The mark-resight method for estimating the size of a closed population can in many circumstances be a less expensive and less invasive alternative to traditional mark-recapture. Despite its potential advantages, one major drawback of traditional mark-resight methodology is that the number of marked individuals in the population available for resighting needs to be known exactly. In real field studies, this can be quite difficult to accomplish. Here we develop a Bayesian model for estimating abundance when sighting data are acquired from distinct sampling occasions without replacement, but the exact number of marked individuals is unknown. By first augmenting the data with some fixed number of individuals comprising a marked “super population,” the problem may then be reformulated in terms of estimating the proportion of this marked super population that was actually available for resighting. This then allows the data for the marked population available for resighting to be modeled as random realizations from a binomial logit-normal distribution. We demonstrate the use of our model to estimate the New Zealand robin (Petroica australis) population size in a region of Fiordland National Park, New Zealand. We then evaluate the performance of the proposed model relative to other estimators via a series of simulation experiments. We generally found our model to have advantages over other models when sample sizes are smaller with individually heterogeneous resighting probabilities. Due to limited budgets and the inherent variability between individuals, this is a common occurrence in mark-resight population studies. WinBUGS and R code to carry out these analyses is available from http://www.stat.colostate.edu/~jah/software.

A less field‐intensive robust design for estimating demographic parameters with mark–resight data

The robust design has become popular among animal ecologists as a means for estimating population abundance and related demographic parameters with mark-recapture data. However, two drawbacks of traditional mark-recapture are financial cost and repeated disturbance to animals. Mark-resight methodology may in many circumstances be a less expensive and less invasive alternative to mark-recapture, but the models developed to date for these data have overwhelmingly concentrated only on the estimation of abundance. Here we introduce a mark-resight model analogous to that used in mark-recapture for the simultaneous estimation of abundance, apparent survival, and transition probabilities between observable and unobservable states. The model may be implemented using standard statistical computing software, but it has also been incorporated into the freeware package Program MARK. We illustrate the use of our model with mainland New Zealand Robin (Petroica australis) data collected to ascertain whether this methodology may be a reliable alternative for monitoring endangered populations of a closely related species inhabiting the Chatham Islands. We found this method to be a viable alternative to traditional mark-recapture when cost or disturbance to species is of particular concern in long-term population monitoring programs.