Register      Login
Wildlife Research Wildlife Research Society
Ecology, management and conservation in natural and modified habitats
RESEARCH ARTICLE (Open Access)

Repeated experimental removals unveil sex and age-specific dispersal strategies in a social passerine bird

Farzaneh Etezadifar A , Jacob A. T. Vickers B , Kristine French B , Paul G. McDonald A , Ahmad Barati A , Rose L. Andrew C and Richard E. Major https://orcid.org/0000-0002-1334-9864 B D *
+ Author Affiliations
- Author Affiliations

A Animal Behaviour and Ecology Laboratory, Zoology, University of New England, Armidale, NSW, Australia.

B School of Earth, Atmospheric and Life Sciences, University of Wollongong, Wollongong, NSW, Australia.

C School of Environmental and Rural Science, University of New England, Armidale, NSW, Australia.

D Australian Museum Research Institute, Australian Museum, Sydney, NSW, Australia.

* Correspondence to: richard.major@austmus.gov.au

Handling Editor: Albrecht Schulte-Hostedde

Wildlife Research 50(2) 141-151 https://doi.org/10.1071/WR21170
Submitted: 25 November 2021  Accepted: 23 July 2022   Published: 26 August 2022

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)

Abstract

Context: Sex and age are frequently proposed as drivers of a number of behavioural and demographic patterns that can have important consequences for population dynamics including access to mates, sexual selection, parental care and lifetime productivity. Sex and age might also be important in shaping the movement patterns and colonisation processes of social species moving into vacant habitat. Such information is critical for the management of strongly interacting species such as the noisy miner (Manorina melanocephala), which structure ecological communities through aggressive exclusion of other taxa from areas that they occupy.

Aims: In Manorina colonies, young females are usually dispersive, while males remain in the natal colony as the philopatric sex. Following removal of individuals from an area, we aimed to determine whether female-biased dispersal, particularly of young females, would result in a more equal sex ratio and a younger age structure in the recolonising population.

Methods: These predictions were tested by anatomically ageing and sexing 1856 noisy miners that had been experimentally culled in two regions of New South Wales, Australia, to reduce the aggressive impact of this species on other native species.

Key results: Prior to removal, noisy miner populations were significantly male-biased in both regions (57% and 60%); however sex ratios after each of two removal episodes no longer differed from parity. Immature birds were a dominant feature (65%) of recolonising populations in both regions, however, the age structure of recolonising populations was different in each region, mostly likely due to the respective timing of culls during the year. Furthermore, the culling response in terms of age-specific sex ratio varied between regions. After the final cull, the sex ratio of mature birds had fallen to parity in one region but had become even more male biased (68%) in the other region. There was no sex-ratio bias among immature birds before or after culling.

Conclusion: These results confirm the expectation that immature birds are more likely to be colonisers, but the expectation of greater female dispersal was equivocal.

Implications: The differences in response between regions may reflect variation in population density, landscape connectivity or seasonality, highlighting challenges when implementing culling programs for conservation management.

Keywords: age structure, dispersal, lethal management, Manorina melanocephala, noisy miner, recolonisation, sex ratio, superabundant species.


References

Alexander, MM (1958). The place of aging in wildlife management. American Scientist 46, 123–137.

Arnold, KE (2000). Group mobbing behaviour and nest defence in a cooperatively breeding Australian bird. Ethology 106, 385–393.

Arnold, KE, Griffith, SC, and Goldizen, AW (2001). Sex-biased hatching sequences in the cooperatively breeding noisy miner. Journal of Avian Biology 32, 219–223.
Sex-biased hatching sequences in the cooperatively breeding noisy miner.Crossref | GoogleScholarGoogle Scholar |

Barati A (2017) Cooperative breeding in the noisy miner (Manorina melanocephala): the role of genetic relatedness, sex, extra-pair paternity and acoustic signals. PhD thesis, University of New England, Armidale NSW.

Barati, A, Andrew, RL, Gorrell, JC, Etezadifar, F, and McDonald, PG (2018a). Genetic relatedness and sex predict helper provisioning effort in the cooperatively breeding noisy miner. Behavioral Ecology 29, 1380–1389.
Genetic relatedness and sex predict helper provisioning effort in the cooperatively breeding noisy miner.Crossref | GoogleScholarGoogle Scholar |

Barati, A, Andrew, RL, Gorrell, JC, and McDonald, PG (2018b). Extra-pair paternity is not driven by inbreeding avoidance and does not affect provisioning rates in a cooperatively breeding bird, the noisy miner (Manorina melanocephala). Behavioral Ecology 29, 244–252.
Extra-pair paternity is not driven by inbreeding avoidance and does not affect provisioning rates in a cooperatively breeding bird, the noisy miner (Manorina melanocephala).Crossref | GoogleScholarGoogle Scholar |

Baumgardt, JA, Goldberg, CS, Reese, KP, Connelly, JW, Musil, DD, Garton, EO, and Waits, LP (2013). A method for estimating population sex ratio for sage-grouse using noninvasive genetic samples. Molecular Ecology Resources 13, 393–402.
A method for estimating population sex ratio for sage-grouse using noninvasive genetic samples.Crossref | GoogleScholarGoogle Scholar |

BirdLife International (2018) Manorina melanocephala. The IUCN red list of threatened species 2018: e.T22704433A132071923. Available at https://dx.doi.org/10.2305/IUCN.UK.2018-2.RLTS.T22704433A132071923.en

Bureau of Meteorology (2021) Monthly climate statistics. Available at http://www.bom.gov.au/climate/averages/tables/cw_050037.shtml

Clarke, MF (1988). The reproductive behaviour of the bell miner Manorina melanophrys. Emu - Austral Ornithology 88, 88–100.
The reproductive behaviour of the bell miner Manorina melanophrys.Crossref | GoogleScholarGoogle Scholar |

Clarke, MF, and Heathcote, CF (1990). Dispersal, survivorship and demography in the co-operatively-breeding bell miner Manorina melanophrys. Emu - Austral Ornithology 90, 15–23.
Dispersal, survivorship and demography in the co-operatively-breeding bell miner Manorina melanophrys.Crossref | GoogleScholarGoogle Scholar |

Cockburn, A, Osmond, HL, Mulder, RA, Double, MC, and Green, DJ (2008). Demography of male reproductive queues in cooperatively breeding superb fairy-wrens (Malurus cyaneus). Journal of Animal Ecology 77, 297–304.
Demography of male reproductive queues in cooperatively breeding superb fairy-wrens (Malurus cyaneus).Crossref | GoogleScholarGoogle Scholar |

Dare, AJ, McDonald, PG, and Clarke, MF (2007). The ecological context and consequences of colonisation of a site by bell miners (Manorina melanophrys). Wildlife Research 34, 616–623.
The ecological context and consequences of colonisation of a site by bell miners (Manorina melanophrys).Crossref | GoogleScholarGoogle Scholar |

Dare, AJ, McDonald, PG, and Clarke, MF (2008). The social and behavioural dynamics of colony expansion in the Bell Miner (Manorina melanophrys). Emu - Austral Ornithology 108, 175–180.
The social and behavioural dynamics of colony expansion in the Bell Miner (Manorina melanophrys).Crossref | GoogleScholarGoogle Scholar |

Davitt, G, Maute, K, Major, RE, McDonald, PG, and Maron, M (2018). Short-term response of a declining woodland bird assemblage to the removal of a despotic competitor. Ecology and Evolution 8, 4771–4780.
Short-term response of a declining woodland bird assemblage to the removal of a despotic competitor.Crossref | GoogleScholarGoogle Scholar |

Department of the Environment (2012) Australia – present major vegetation groups – National Vegetation Information System Version 4.1 (Albers 100m analysis product). Bioregional Assessment Source Dataset. Available at https://data.gov.au/data/dataset/57c8ee5c-43e5-4e9c-9e41-fd5012536374

Donovan, TM, Lamberson, RH, Kimber, A, Thompson, FR, and Faaborg, J (1995). Modeling the effects of habitat fragmentation on source and sink demography of neotropical migrant birds. Conservation Biology 9, 1396–1407.
Modeling the effects of habitat fragmentation on source and sink demography of neotropical migrant birds.Crossref | GoogleScholarGoogle Scholar |

Dow, DD (1975). Displays of the honeyeater Manorina melanocephala. Zeitschrift für Tierpsychologie 38, 70–96.
Displays of the honeyeater Manorina melanocephala.Crossref | GoogleScholarGoogle Scholar |

Dow, DD (1977). Indiscriminate interspecific aggression leading to almost sole occupancy of space by a single species of bird. Emu - Austral Ornithology 77, 115–121.
Indiscriminate interspecific aggression leading to almost sole occupancy of space by a single species of bird.Crossref | GoogleScholarGoogle Scholar |

Dow, DD (1978). Breeding biology and development of the young of Manorina melanocephala, a communally breeding honeyeater. Emu - Austral Ornithology 78, 207–222.
Breeding biology and development of the young of Manorina melanocephala, a communally breeding honeyeater.Crossref | GoogleScholarGoogle Scholar |

Dow DD, Whitmore MJ (1990) Noisy miners: variations on the theme of communality. In ‘Cooperative breeding in birds’. (Eds PB Stacey, WD Koenig) pp. 559–592. (Cambridge University Press: Cambridge)

Eberhart-Phillips, LJ, Küpper, C, Carmona-Isunza, MC, et al. (2018). Demographic causes of adult sex ratio variation and their consequences for parental cooperation. Nature Communications 9, 1651.
Demographic causes of adult sex ratio variation and their consequences for parental cooperation.Crossref | GoogleScholarGoogle Scholar |

Ellegren, H, and Sheldon, BC (1997). New tools for sex identification and the study of sex allocation in birds. Trends in Ecology & Evolution 12, 255–259.
New tools for sex identification and the study of sex allocation in birds.Crossref | GoogleScholarGoogle Scholar |

Emlen, ST (1982). The evolution of helping. I. An ecological constraints model. The American Naturalist 119, 29–39.
The evolution of helping. I. An ecological constraints model.Crossref | GoogleScholarGoogle Scholar |

Etezadifar F (2021) Re-colonisation dynamics of a highly social and aggressive bird, the noisy miner (Manorina melanocephala): variations in sex ratio, age composition and physiological condition. Ph.D. Thesis, University of New England.

Ewen, JG, Crozier, RH, Cassey, P, Ward-Smith, T, Painter, JN, Robertson, RJ, Jones, DA, and Clarke, MF (2003). Facultative control of offspring sex in the cooperatively breeding bell miner, Manorina melanophrys. Behavioral Ecology 14, 157–164.
Facultative control of offspring sex in the cooperatively breeding bell miner, Manorina melanophrys.Crossref | GoogleScholarGoogle Scholar |

Gaston, AJ (1978). Demography of the jungle babbler, Turdoides striatus. Journal of Animal Ecology 47, 845–870.
Demography of the jungle babbler, Turdoides striatus.Crossref | GoogleScholarGoogle Scholar |

Grayson, KL, Mitchell, NJ, Monks, JM, Keall, SN, Wilson, JN, and Nelson, NJ (2014). Sex ratio bias and extinction risk in an isolated population of Tuatara (Sphenodon punctatus). PLoS ONE 9, e94214.
Sex ratio bias and extinction risk in an isolated population of Tuatara (Sphenodon punctatus).Crossref | GoogleScholarGoogle Scholar |

Greenwood, PJ, and Harvey, PH (1982). The natal and breeding dispersal of birds. Annual Review of Ecology and Systematics 13, 1–21.
The natal and breeding dispersal of birds.Crossref | GoogleScholarGoogle Scholar |

Grey, MJ, Clarke, MF, and Loyn, RH (1997). Initial changes in the avian communities of remnant eucalypt woodlands following a reduction in the abundance of noisy miners, Manorina melanocephala. Wildlife Research 24, 631–648.
Initial changes in the avian communities of remnant eucalypt woodlands following a reduction in the abundance of noisy miners, Manorina melanocephala.Crossref | GoogleScholarGoogle Scholar |

Griffiths, R, Double, MC, Orr, K, and Dawson, RJG (1998). A DNA test to sex most birds. Molecular Ecology 7, 1071–1075.
A DNA test to sex most birds.Crossref | GoogleScholarGoogle Scholar |

Hatchwell, BJ (2009). The evolution of cooperative breeding in birds: kinship, dispersal and life history. Philosophical Transactions of the Royal Society B: Biological Sciences 364, 3217–3227.
The evolution of cooperative breeding in birds: kinship, dispersal and life history.Crossref | GoogleScholarGoogle Scholar |

Higgins PJ, Peter JM, Steele WK (2001) ‘Handbook of Australian, New Zealand and Antarctic birds.’ (Oxford Univ. Press: Melbourne)

JMP (2019) ‘JMP® Version 15.’ (SAS Institute Inc.: Cary, NC)

Koenig, WD (1981). Reproductive success, group size, and the evolution of cooperative breeding in the acorn woodpecker. The American Naturalist 117, 421–443.
Reproductive success, group size, and the evolution of cooperative breeding in the acorn woodpecker.Crossref | GoogleScholarGoogle Scholar |

Kokko, H, Gunnarsson, TG, Morrell, LJ, and Gill, JA (2006). Why do female migratory birds arrive later than males? Journal of Animal Ecology 75, 1293–1303.
Why do female migratory birds arrive later than males?Crossref | GoogleScholarGoogle Scholar |

Komdeur, J (1994). Conserving the seychelles warbler Acrocephalus sechellensis by translocation from Cousin Island to the islands of Aride and Cousine. Biological Conservation 67, 143–152.
Conserving the seychelles warbler Acrocephalus sechellensis by translocation from Cousin Island to the islands of Aride and Cousine.Crossref | GoogleScholarGoogle Scholar |

Kopps, AM, McDonald, P, and Rollins, LA (2013). Isolation and characterisation of polymorphic microsatellite loci for noisy miners Manorina melanocephala, with successful cross-amplification in bell miners M. melanophrys. Conservation Genetics Resources 5, 39–41.
Isolation and characterisation of polymorphic microsatellite loci for noisy miners Manorina melanocephala, with successful cross-amplification in bell miners M. melanophrys.Crossref | GoogleScholarGoogle Scholar |

Lewis, DM (1982). Dispersal in a population of white-browed sparrow weavers. The Condor 84, 306–312.
Dispersal in a population of white-browed sparrow weavers.Crossref | GoogleScholarGoogle Scholar |

Liker, A, Freckleton, RP, and Székely, T (2014). Divorce and infidelity are associated with skewed adult sex ratios in birds. Current Biology 24, 880–884.
Divorce and infidelity are associated with skewed adult sex ratios in birds.Crossref | GoogleScholarGoogle Scholar |

Mac Nally, R, Bowen, M, Howes, A, McAlpine, CA, and Maron, M (2012). Despotic, high-impact species and the subcontinental scale control of avian assemblage structure. Ecology 93, 668–678.
Despotic, high-impact species and the subcontinental scale control of avian assemblage structure.Crossref | GoogleScholarGoogle Scholar |

Maron, M, Grey, MJ, Catterall, CP, Major, RE, Oliver, DL, Clarke, MF, Loyn, RH, Mac Nally, R, Davidson, I, and Thomson, JR (2013). Avifaunal disarray due to a single despotic species. Diversity and Distributions 19, 1468–1479.
Avifaunal disarray due to a single despotic species.Crossref | GoogleScholarGoogle Scholar |

McDonald, PG, Ewen, JG, and Wright, J (2010). Brood sex ratio does not affect helper effort in a cooperative bird, despite extreme sex-biased dispersal. Animal Behaviour 79, 243–250.
Brood sex ratio does not affect helper effort in a cooperative bird, despite extreme sex-biased dispersal.Crossref | GoogleScholarGoogle Scholar |

Melton, CB, Reside, AE, Simmonds, JS, McDonald, PG, Major, RE, Crates, R, Catterall, CP, Clarke, MF, Grey, MJ, Davitt, G, Ingwersen, D, Robinson, D, and Maron, M (2021). Evaluating the evidence of culling a native species for conservation benefits. Conservation Science and Practice 3, e549.
Evaluating the evidence of culling a native species for conservation benefits.Crossref | GoogleScholarGoogle Scholar |

Montague-Drake, RM, Lindenmayer, DB, Cunningham, RB, and Stein, JA (2011). A reverse keystone species affects the landscape distribution of woodland avifauna: a case study using the noisy miner (Manorina melanocephala) and other Australian birds. Landscape Ecology 26, 1383–1394.
A reverse keystone species affects the landscape distribution of woodland avifauna: a case study using the noisy miner (Manorina melanocephala) and other Australian birds.Crossref | GoogleScholarGoogle Scholar |

Nelson-Flower, MJ, Wiley, EM, Flower, TP, and Ridley, AR (2018). Individual dispersal delays in a cooperative breeder: ecological constraints, the benefits of philopatry and the social queue for dominance. Journal of Animal Ecology 87, 1227–1238.
Individual dispersal delays in a cooperative breeder: ecological constraints, the benefits of philopatry and the social queue for dominance.Crossref | GoogleScholarGoogle Scholar |

NSWSC (2013) ‘Final determination to list ‘Aggressive exclusion of birds from woodland and forest habitat by abundant noisy miners Manorina melanocephala (Latham 1802)’ as a key threatening process.’ (New South Wales Scientific Committee: Sydney)

Pyle P, Howell SNG, Yunick RP, DeSante DF (1987) ‘Identification guide to North American Passerines.’ (Slate Creek Press: Bolinas, California). p. 278.

Reichard, M, Polačik, M, Blažek, R, and Vrtílek, M (2014). Female bias in the adult sex ratio of African annual fishes: interspecific differences, seasonal trends and environmental predictors. Evolutionary Ecology 28, 1105–1120.
Female bias in the adult sex ratio of African annual fishes: interspecific differences, seasonal trends and environmental predictors.Crossref | GoogleScholarGoogle Scholar |

Remeš, V, Freckleton, RP, Tökölyi, J, Liker, A, and Székely, T (2015). The evolution of parental cooperation in birds. Proceedings of the National Academy of Sciences 112, 13603–13608.

Ridley, AR, and Huyvaert, KP (2007). Sex-biased preferential care in the cooperatively breeding Arabian babbler. Journal of Evolutionary Biology 20, 1271–1276.
Sex-biased preferential care in the cooperatively breeding Arabian babbler.Crossref | GoogleScholarGoogle Scholar |

Serventy, DL, Nicholls, CA, and Farner, DS (1967). Pneumatization of the cranium of the zebra finch Taeniopygia castanotis. Ibis 109, 570–578.
Pneumatization of the cranium of the zebra finch Taeniopygia castanotis.Crossref | GoogleScholarGoogle Scholar |

Smith, SM (1978). The “underworld” in a territorial sparrow: adaptive strategy for floaters. The American Naturalist 112, 571–582.
The “underworld” in a territorial sparrow: adaptive strategy for floaters.Crossref | GoogleScholarGoogle Scholar |

Stacey, PB, and Ligon, JD (1987). Territory quality and dispersal options in the acorn woodpecker, and a challenge to the habitat-saturation model of cooperative breeding. The American Naturalist 130, 654–676.
Territory quality and dispersal options in the acorn woodpecker, and a challenge to the habitat-saturation model of cooperative breeding.Crossref | GoogleScholarGoogle Scholar |

Székely, T, Liker, A, Freckleton, RP, Fichtel, C, and Kappeler, PM (2014). Sex-biased survival predicts adult sex ratio variation in wild birds. Proceedings of the Royal Society B: Biological Sciences 281, 20140342.
Sex-biased survival predicts adult sex ratio variation in wild birds.Crossref | GoogleScholarGoogle Scholar |

Thackway R, Cresswell ID (1995) ‘An interim biogeographic regionalisation for Australia: a framework for establishing the national system of reserves, Version 4.0.’ (Australian Nature Conservation Agency: Canberra)

Thomson, JR, Maron, M, Grey, MJ, Catterall, CP, Major, RE, Oliver, DL, Clarke, MF, Loyn, RH, Davidson, I, Ingwersen, D, Robinson, D, Kutt, A, MacDonald, MA, and Mac Nally, R (2015). Avifaunal disarray: quantifying models of the occurrence and ecological effects of a despotic bird species. Diversity and Distributions 21, 451–464.
Avifaunal disarray: quantifying models of the occurrence and ecological effects of a despotic bird species.Crossref | GoogleScholarGoogle Scholar |

TSSC (2013) ‘Aggressive exclusion of birds from potential woodland and forest habitat by over-abundant noisy miners (Manorina melanocephala).’ (Threatened Species Scientific Committee, Department of the Environment: Canberra)

Wiley, RH, and Rabenold, RN (1984). The evolution of cooperative breeding by delayed reciprocity and queuing for favorable social positions. Evolution 38, 609–621.
The evolution of cooperative breeding by delayed reciprocity and queuing for favorable social positions.Crossref | GoogleScholarGoogle Scholar |

Woolfenden, GE (1989). Population ecology of the cooperatively breeding acorn woodpecker. Evolution 43, 1129–1130.
Population ecology of the cooperatively breeding acorn woodpecker.Crossref | GoogleScholarGoogle Scholar |