Variegated Fairy-wren Research Articles

Plural breeding among unrelated females and other insights on complex social structure in the cooperatively breeding Variegated Fairywren

ABSTRACT Cooperatively breeding species vary widely in degree of social complexity, and disentangling relationships among group members can reveal the costs and benefits of cooperation. Here, we describe the social system of the cooperatively breeding Variegated Fairywren (Malurus lamberti) and explore how social complexity and group dynamics may affect cooperation and conflict. We used a combination of field-based population monitoring and detailed social association observations to determine group membership annually across four breeding seasons (2014–2017) and used a ddRAD-seq genotyping method to determine genetic relationships within social groups. Social groups ranged in size from two to eight individuals and nearly half of all social groups had multiple adult individuals of both sexes. Approximately half of all groups exhibited plural breeding, in which multiple females within the same social group nested individually in the same territory. Genetic relationships were diverse among social groups due to high rates of extra-pair paternity and immigration, with most groups containing close relatives and non-relatives of each sex. Notably, although related females were often present within a social group, co-breeding females in the same social group were never closely related to each other. Given the extensive variation in relatedness among group members, cooperation in the Variegated Fairywren is likely maintained by a combination of direct and indirect fitness benefits.

Reproductive promiscuity in the variegated fairy-wren: an alternative reproductive strategy in the absence of helpers?

Cooperative breeding, in which auxiliary group members help rear related, but nondescendent young, is often explained by kin selection. Reproductive monogamy is predicted in cooperatively breeding systems, as monogamy increases intragroup relatedness and maximizes auxiliary inclusive fitness. While monogamy is observed across many systems, including eusocial insects and cooperatively breeding mammals, some cooperatively breeding birds exhibit high rates of extrapair paternity. Here we quantify paternity and examine the role of auxiliaries on extrapair paternity in the highly cooperative variegated fairy-wren, Malurus lamberti, a species with both male and female auxiliaries. Extrapair paternity occurred in 55.4% of nests, and 39.8% of offspring were the result of extrapair matings. The presence of both male and female auxiliaries had a positive relationship with the percentage of within-pair young sired by dominant males, however, the presence of male auxiliaries had a stronger impact than the presence of females. The number of extrapair young sired by dominant males decreased as the number of male auxiliaries increased. The total number of young sired by dominant males, however, was not predicted by group size or relatedness to their social partner, nor did group composition or relatedness to the breeding pair predict the reproductive success of subordinate males. We hypothesize that breeders use alternative reproductive strategies in the presence or absence of auxiliaries. Males and females may seek extrapair reproductive opportunities when no help is available in their group and nest survival is expected to be low. When help is available, breeders may reduce extrapair paternity, either to increase intragroup relatedness or because confidence in nest survival is high. Our data suggest that group composition is important in understanding extrapair paternity rates in cooperatively breeding birds and that variation in extrapair paternity rates may be the result of flexible breeding strategies when auxiliary presence and identity varies.

Double-digest RAD sequencing outperforms microsatellite loci at assigning paternity and estimating relatedness: A proof of concept in a highly promiscuous bird.

Information on genetic relationships among individuals is essential to many studies of the behaviour and ecology of wild organisms. Parentage and relatedness assays based on large numbers of single nucleotide polymorphism (SNP) loci hold substantial advantages over the microsatellite markers traditionally used for these purposes. We present a double-digest restriction site-associated DNA sequencing (ddRAD-seq) analysis pipeline that, as such, simultaneously achieves the SNP discovery and genotyping steps and which is optimized to return a statistically powerful set of SNP markers (typically 150-600 after stringent filtering) from large numbers of individuals (up to 240 per run). We explore the trade-offs inherent in this approach through a set of experiments in a species with a complex social system, the variegated fairy-wren (Malurus lamberti) and further validate it in a phylogenetically broad set of other bird species. Through direct comparisons with a parallel data set from a robust panel of highly variable microsatellite markers, we show that this ddRAD-seq approach results in substantially improved power to discriminate among potential relatives and considerably more precise estimates of relatedness coefficients. The pipeline is designed to be universally applicable to all bird species (and with minor modifications to many other taxa), to be cost- and time-efficient, and to be replicable across independent runs such that genotype data from different study periods can be combined and analysed as field samples are accumulated.

Corrigendum: Reassessment of a possible case of intraspecific gene flow across Australia’s Great Dividing Range in the variegated fairy wren, Malurus lamberti (Aves: Maluridae), and its systematic consequences

The authors apologise for a typographical error on pages 216-217 in the sub-section 'PLUMAGE' of the 'RESULTS' section of the article. The original published version of the article contained the following incorrect sentence: Supporting Information, Fig. S5 shows that all nuptially plumaged males sampled in the PZI have the M. l. assimilis phenotype of darker blue on the dorsal surface, which does not contrast between the ear coverts and crown as in M. l. lamberti. This sentence has now been corrected to read as follows: Supporting Information, Fig. S5 shows that all nuptially plumaged males sampled in the PZI have the M. l. assimilis phenotype of darker blue on the dorsal surface, which results in contrast between the ear coverts and crown unlike the more concolorous pattern of crown and ear coverts in M. l. lamberti.

Reassessment of a possible case of intraspecific gene flow across Australia’s Great Dividing Range in the variegated fairy wren, Malurus lamberti (Aves: Maluridae), and its systematic consequences

Two subspecies of the variegated fairy wren Malurus lamberti, Malurus lamberti lamberti and Malurus lamberti assimilis, are thought to exemplify a surprisingly rare case of intraspecific gene flow across eastern Australia's Great Dividing Range. We screened 71 individuals within and beyond their putative hybrid zone for diversity in one mitochondrial and two anonymous nuclear loci, four microsatellite markers and diagnostically different plumage traits. Almost all supposed hybrid zone individuals were genotypically and phenotypically M. l. assimilis, but some carried mitochondrial DNA typical of M. l. lamberti. We infer an intermittently 'leaky' genetic boundary between the two taxa. Integrating this study with our earlier work on the M. lamberti group, we argue that speciation, albeit with some gene flow, between M. l. lamberti and all other taxa recently assigned to M. lamberti is essentially complete. A two-species taxonomy whereby one species, M. lamberti Vigors and Horsfield, 1827 (variegated fairy wren), comprises only what is currently called M. l. lamberti, and a second species, Malurus assimilis North, 1901 (purple-backed fairy wren), is for all other populations recently assigned to M. lamberti should be adopted and further tested.

Phylogeography and geno-phenotypic discordance in a widespread Australian bird, the Variegated Fairy-wren, Malurus lamberti (Aves: Maluridae)

The Variegated Fairy-wren Malurus lamberti as currently construed occurs across almost all of mainland Australia. If Pleistocene biogeographical barriers limited gene flow in this species, then geographical restriction of haplotypes should mirror those barriers. We used phylogeographic analyses of one mitochondrial and eight nuclear DNA markers to reconstruct the bird’s history, especially for its arid and tropical populations. Robustly supported phylogeographic structure between M. l. lamberti of central eastern Australia and all other populations suggests vicariance by the Great Dividing Range of eastern Australia; time to their most recent common ancestor origin traces to approximately 148 000 years ago (Kya; 95% highest posterior density interval 62–312). Estimates of divergence time for populations of M. l. assimilis east and west of the central southern Australian Eyrean Barrier converged at 86 Kya (45–133), the youngest estimated divergence being between two tropical taxa (14 Kya, 0–30). Taxonomic implications of our data question the current circumscription of M. lamberti, but support taxonomic recognition of structuring east and west of the Eyrean Barrier within what is currently M. l. assimilis. Genetic diversity in two tropical taxa is incompletely sorted or at early stages of divergence with gene flow.

Female splendid and variegated fairy-wrens display different strategies during territory defence

Contrary to the traditional view that territory defence is a male behaviour, there is now evidence that female birds actively engage in territory defence, either alone or with their mate. In males, song sharing between neighbours has been shown to facilitate territory defence, but little is known about the importance of song sharing for such behaviour in females. Here, I examined sex roles and song element sharing in two related species: the splendid fairy-wren, Malurus splendens , and the variegated fairy-wren, Malurus lamberti . I first described song structure and song element sharing between partners and neighbours in both male and female songs. I then simulated conspecific intrusions by broadcasting a female or a male song within a pair's territory. Both splendid and variegated fairy-wren females sang songs as complex as their male counterparts and responded to playback of simulated conspecific intrusions. Song element sharing with neighbours was common in both species, but only splendid fairy-wren females shared more elements with their mate than with other recorded males on average. Females in each species engaged in different strategies when responding to territory intruders: female splendid fairy-wrens competed with female intruders, while variegated fairy-wren females coordinated their defence with their mates and exhibited cooperative defence behaviours toward male intruders. I discuss the ideas that variation in levels of extrapair paternity and/or female competition may drive the evolution of different female strategies when responding to territory intruders.

Winter avifauna of Wanjarri Nature Reserve and Lake Mason Conservation Park of the Eastern Goldfields, Western Australia

Surveys of the avifauna of Wanjarri Nature Reserve and Lake Mason Conservation Park during late July 2015 recorded 100 species, with 68 at Wanjarri and 90 at Lake Mason. The greater number of species at Lake Mason Conservation Park was attributed to the presence of 19 species of waterbirds associated with the lake. Although nearly equal numbers of terrestrial species were found at both reserves, the frequency of occurrence records from Lake Mason showed significantly greater frequencies for several species, probably because of the greater availability of surface water there. The significantly higher frequencies of Horsfield’s Bronze-Cuckoo Chalcites basalis and Pallid Cuckoo Cacomantis pallidus at Wanjarri Nature Reserve may have been related to the many hairy caterpillars available there as a food resource. Detrended Correspondence Analysis showed that the major assemblages of bird species were associated primarily with vegetation type and secondarily with the geographic separation of the two reserves. Species associated with Mulga Acacia aneura woodlands, spinifex Triodia grasslands and saltbush Atriplex habitats on Wanjarri and Lake Mason were similar to those recorded in other arid-zone habitats of Western Australia. Species associated with Mulga woodlands included Crested Pigeon Ocyphaps lophotes, Slaty-backed Acanthiza robustirostris , Chestnut-rumped A uropygialis and Inland Thornbills A. apicalis , Singing Lichenostomus virescens and Spiny-cheeked Honeyeaters Acanthagenys rufogularis , Rufous Whistler Pachycephala rufiventris and Red-capped Robin Petroica goodenovii . Species associated more often with spinifex grasslands and saltbush habitats were White-winged Malurus leucopterus and Variegated Fairy-wrens M. lamberti , Australian Magpie Cracticus tibicen , Brown Songlark Cincloramphus cruralis , and several raptors. Inclusion of these two reserves in the conservation estate of Western Australia is important as they are at the margin of the distribution ranges for several species. Data from our surveys will facilitate future assessment of populations of birds and assist in management decisions regarding future protection of the avifauna in these reserves.

Speciation in chestnut-shouldered fairy-wrens (Malurus spp.) and rapid phenotypic divergence in variegated fairy-wrens (Malurus lamberti): A multilocus approach

The chestnut-shouldered fairy-wrens comprise a subgroup of four species in the genus Malurus (Passeriformes: Maluridae). Collectively, they are widespread across the Australian continent but phenotypic variation is strongly structured geographically in just one species, M. lamberti. Earlier phylogenetic analyses of this group have been limited to one or two individuals for each species and have not represented all currently recognised subspecies of M. lamberti. Historically, the taxonomy and nomenclature of the M. lamberti complex has been debated, in part because of morphological similarities among its subspecies and another member of the group, M. amabilis. We reconstructed the phylogeny of all four species of chestnut-shouldered fairy-wrens including all four subspecies of M. lamberti using a mitochondrial gene (ND2), five anonymous nuclear loci and three nuclear introns. Phylogenetic analysis of the mitochondrial ND2 gene nests M. amabilis within M. lamberti rendering the latter paraphyletic. Individual nuclear gene trees failed to reliably resolve each of the species boundaries or the phylogenetic relationships found in the mtDNA tree. When combined, however, a strongly supported overall topology was resolved supporting the monophyly of M. lamberti and its sister species relationship to M. amabilis. Current subspecific taxonomy of M. lamberti was not concordant with all evolutionary lineages of M. lamberti, nominotypical M. l. lamberti being the only subspecies recovered as a monophyletic group from mtDNA. Some genetic structuring is evident and potential barriers to gene flow are discussed.

Corrigendum to: The abundance and distribution of two species of fairy-wren in suburban and natural habitats

Bird communities in suburban habitats are dominated by generalist species and tend to have fewer specialist species sensitive to disturbance. Superb (Malurus cyaneus) and Variegated (M. lamberti) Fairy-wrens are morphologically and ecologically similar but differ in the degree to which they occupy suburban habitats. The species often occur in sympatry in natural habitats but in suburban habitats Superb Fairy-wrens are much more common than Variegated Fairy-wrens. We compared the characteristics of the habitat of both species in natural and suburban areas to investigate whether habitat requirements differed between the species, and which may explain observed patterns of abundance. Patch-level vegetative and disturbance-related habitat characteristics of territories were compared to those of non-territories in natural and suburban habitats. In natural habitats, Superb Fairy-wrens occupied more disturbed patches than Variegated Fairy-wrens. Vegetated drainages and patches of weedy remnant vegetation were important habitats for suburban Superb Fairy-wrens, which also tolerated the presence of humans whereas Variegated Fairy-wrens were particularly sensitive to human presence. A better understanding of the factors affecting the abundance of the more sensitive native species in suburban areas, such as Variegated Fairy-wrens, may inform conservation actions to enhance suburban biodiversity.

The abundance and distribution of two species of fairy-wren in suburban and natural habitats

Bird communities in suburban habitats are dominated by generalist species and tend to have fewer specialist species sensitive to disturbance. Superb (Malurus cyaneus) and Variegated (M. lamberti) Fairy-wrens are morphologically and ecologically similar but differ in the degree to which they occupy suburban habitats. The species often occur in sympatry in natural habitats but in suburban habitats Superb Fairy-wrens are much more common than Variegated Fairy-wrens. We compared the characteristics of the habitat of both species in natural and suburban areas to investigate whether habitat requirements differed between the species, and which may explain observed patterns of abundance. Patch-level vegetative and disturbance-related habitat characteristics of territories were compared to those of non-territories in natural and suburban habitats. In natural habitats, Superb Fairy-wrens occupied more disturbed patches than Variegated Fairy-wrens. Vegetated drainages and patches of weedy remnant vegetation were important habitats for suburban Superb Fairy-wrens, which also tolerated the presence of humans whereas Variegated Fairy-wrens were particularly sensitive to human presence. A better understanding of the factors affecting the abundance of the more sensitive native species in suburban areas, such as Variegated Fairy-wrens, may inform conservation actions to enhance suburban biodiversity.

A predator-elicited vocalisation in the Variegated Fairy-wren (Malurus lamberti)

We document a previously undescribed vocalisation in the Variegated Fairy-wren (Malurus lamberti), the Type II song, which is given in response to the calls of a specific avian predator. We used playbacks of five species of both predators and non-predators to determine which species most commonly elicit Type II songs. Calls of Grey Butcherbirds (Cracticus torquatus) were the only stimuli to elicit Type II songs. Two other species in the genus Malurus, the Splendid Fairy-wren (M. splendens) and the Superb Fairy-wren (M. cyaneus), are also known to sing Type II songs in response to the calls of specific avian predators. In all these species, Type II songs may function as displays to conspecifics. This study highlights the possibility that predator-elicited display behaviour may be more widespread in the genus Malurus than was previously recognised.

The effects of grazing and fire on vegetation and the vertebrate assemblage in a tropical savanna woodland in north-eastern Australia

We studied the response of vegetation and vertebrate assemblages to fire and grazing, and their interacting effects, in Eucalyptus woodland in north-eastern Australia. In this vegetation type, many pastures remain free of cattle grazing due to the occurrence of a native shrub poisonous to livestock. Vegetation (floristic data and 22 habitat variables) and vertebrate fauna (birds, mammals, reptiles) were sampled in 29 standardized 50 × 50-m quadrats in the 2001 wet season, representing four treatments: sites burnt recently (within 2 y) and grazed by cattle (4–8 ha per livestock unit); sites unburnt (last burnt >2 y ago) and grazed; sites burnt recently and ungrazed; and unburnt and ungrazed sites. Fire and grazing had a significant influence on vegetation: both grazing and fire reduced ground cover (fire in grazed sites 51–23%, fire in ungrazed sites 68–39%) and increased the cover of forbs (8% in burnt and grazed sites, 3% if ungrazed) and tussock grasses (20% in grazed and unburnt sites and 5% when ungrazed). Grazing caused a shift in floristic composition from the perennial hummock grass Trioda pungens to tussock grasses (e.g. Aristida spp., Enneapogon spp.), forbs (e.g. Phyllanthus spp.) and shrubs (e.g. Acacia spp.). Of the vertebrate groups, birds responded more to fire effects (9 species), reptiles to grazing effects (6 species) and mammals to the interaction (2 species). Species reacted to increases in bare ground (e.g. crested pigeon Ocyphaps lophotes, hooded robin Melanodryas cucullatus, Ctenophorus nuchalis) and to the dominant ground cover (e.g. Ctenotus pantherinus) or change in vegetation architecture (e.g. singing honeyeater Lichenostomus virescens, variegated fairy-wren Malurus lamberti). The clearest example of an interacting effect was the cycle of complementary dominance between the rodents Pseudomys delicatulus and P. desertor, the latter's post-fire recovery becoming more muted in sites where cattle grazed (modelled time for population recovery twice as long as in ungrazed sites).

Use of space, foraging behaviour and strategies of survival among three coexisting species of fairy-wrens (Malurus)

Superb, Malurus cyaneus, White-winged, M. leucopterus, and Variegated, M. lamberti, Fairy-wrens coexisting in a semi-arid environment at Booligal, New South Wales, partitioned their use of space. During drought, territories overlapped more than in good years. White-winged Fairy-wrens spent the most time sitting, showed the highest preference for sitting in bushes and allopreened the most. Superb Fairy-wrens foraged the most on the ground, moved up and down to different foraging stations the most rapidly and had the widest variety of foraging stations. White-winged Fairy-wrens foraged mostly on the outer parts of bushes; Variegated Fairy-wrens foraged on the innermost parts of bushes and spent the longest at a foraging station. White-winged Fairy-wrens flew the furthest to a new foraging site. When niche breadths for macrohabitat, foraging heights and foraging stations were represented on orthogonal axes, Variegated Fairy-wrens and White-winged Fairy-wrens are more alike in their use of space than either is to Superb Fairy-wrens and the greatest distance is between Superb and Variegated Fairy-wrens. In terms of survival strategies, Superb Fairy-wrens are ‘opportunists’, White-winged Fairy-wrens are ‘coasters’ and Variegated Fairy-wrens are ‘stayers’.

Habitat and nest-site partitioning in splendid and variegated fairy-wrens (Aves : Maluridae)

Territory size, interspecific interactions, foraging behaviour, habitat use, and nest placement were examined in sympatric populations of splendid (Malurus splendens melanotus) and variegated (M. lamberti assimilis) fairy-wrens. Although these species have similar patterns of life history and biology, they utilise different microhabitats within overlapping territories. Splendid fairy-wrens spent more time on the ground and in open areas, whereas variegated fairy-wrens generally preferred higher and more protected locations. The two species exhibited a similar pattern of separation with respect to foraging behaviour, as splendid fairy- wrens mainly foraged on the ground whereas variegated fairy-wrens preferred bushes. They also partitioned nesting habitat, with splendid fairy-wrens building nests in areas with a greater density of trees than variegated fairy-wrens. Further, splendid fairy-wrens built nests in larger shrubs and farther from the edge of these bushes than variegated fairy-wrens. We suggest that these differences in habitat use decrease interspecific competition between the two species.

Hybridisation BetweenMalurus lamberti rogersiandMalurus lamberti assimilisin North-western Australia

(1991). Hybridisation Between Malurus lamberti rogersi and Malurus lamberti assimilis in North-western Australia. Emu - Austral Ornithology: Vol. 91, No. 4, pp. 251-254.

Selection of Nest Sites by Three Species of Fairy-wrens (Malurus)

At Booligal, NSW, Superb Fairy-wrens Malurus cyaneus avoided orienting nest entrances towards the west and White-winged M. leucopterus avoided the south and west. Superb Fairy-wrens favoured the northern sector of bushes and White-winged the north-eastern sector to build nests. There was no relationship between nest position and the number of nests that produced fledglings. Superb Fairy-wrens built nests higher in bushes than White-winged and Variegated Fairy-wrens M. larnbeni. Chenopodium spp. bushes were preferred to others. Superb Fairy-wrens built further into a bush than Variegated and White- winged. There was generally no relationship between bush heights, volumes, distance to closest tree, placement of surrounding bushes and siting of nest. There were no interspecific effects on nest placement and successive nests were not affected by positions of earlier nests. White-winged Fairy-wrens placed their nests more centrally in territories than Superb.

Periodicity of Breeding Behaviour of Three Species of Fairy-wrens (Malurus spp.)

Breeding seasons, as determined from nest record cards, for the Superb Malurus cyaneus, Variegated M. lamberti and White-winged M. leucopterus Fairy-wrens were compared within a 30-40°S latitude band and across high to low rainfall zones. All species bred mostly in spring and summer but the Superb Fairy-wrens had the most, and the White-winged Fairy-wrens the least, clearly defined breeding season. Superb Fairy-wrens in high rainfall zones bred in spring and summer but in low rainfall zones their breeding was less seasonal and followed good rains. The Variegated Fairy-wrens bred throughout most of the year in the high rainfall zone although few nests were started in autumn and winter. White-winged Fairy-wrens bred in all months of the year in low rainfall zones but there were few nests in autumn and early winter. With progression towards lower rainfall zones, species may respond opportunistically to good rains falling out of season because rainfall directly affects the amount of available food. White-winged Fairy-wrens may have a lower threshold of response to rainfall than Superb. In addition, breeding stimuli may be hierarchically arranged with increasing photoperiod being most important, followed by rainfall and food.

Breeding in Three Species of Fairy-Wrens (Malurus): Do Helpers Really Help?

About 240 h were spent observing behaviour at the nests of co-existing Superb Malurus cyaneus, Variegated M. lamberti and White-winged M. leucopterus Fairy-wrens. Feeding rates increased as nestling number increased but not proportionately. Variegated Fairy-wrens shared feeding about equally between the sexes but in the other two species the females were the predominant feeders except when nestlings were very young. There was a correlation between feeding rate and age of nestlings. Superb Fairy-wren helpers were young of the year and contributed most when nestlings were older whereas with White-winged helpers (all adult males) the pattern was reversed. Adults and helpers 'complemented' each other so that the total number of feeds per hour to the nestlings was more stable than any one individual's contribution. Helpers did not lead to an increased feeding rate but rather a decrease in the female's feeding rate and load carried.

The Relationships of the Australo-Papuan Fairy-Wrens as Indicated by DNA-DNA Hybridization

The systematic relationships of the genus Malurus were examined by comparing the radioiodine-labelled ('iSI) single copy DNA sequences of the Variegated Fairy-wren Malurus lamberti with the DNAs of thirty-seven other species of oscine birds. Malurus lamberti was found to be most closely related to other species of Malurus, and to Stipiturus, Amytornis, the acanthizine thornbills and scrubwrens, and the honeyeaters, in that order. Malurus is not closely related to the sylviine warblers, the timaliine babblers, or the muscicapine flycatchers.