“Strange behaviours” of parents at the nest in an avian prey species as a potential source of bias when studying nest predation and signs left by different predators
- Authors: Morozov N.S.1
-
Affiliations:
- Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences
- Issue: Vol 103, No 9 (2024)
- Pages: 53-82
- Section: ARTICLES
- URL: https://rjdentistry.com/0044-5134/article/view/654249
- DOI: https://doi.org/10.31857/S0044513424090061
- EDN: https://elibrary.ru/trmlwa
- ID: 654249
Cite item
Abstract
In most passerines, parent birds clean their nests. Egg shells, fecal sacs, and dead nestlings, as well as foreign objects, for example, leaf and twig debris, as they appear, are usually removed from nests in one or another way. If, for one reason or another (nest predation, inclement weather, starvation etc.), all offspring die, parents abandon the nest with egg or/and nestling remains. Finding one or another nest empty and intact before the earliest possible fledging date, observers who monitor nests usually attribute the failure to predation. Automated cameras placed at 148 Fieldfare (Turdus pilaris) nests in 2016–2020 to study nest predation in Moscow City, Russia documented two cases of sanitation (by females) of entire and almost entire (all but one dead nestling) broods of dead nestlings that had died due to inclement weather. This information is one of the very few, probably the second, and for Eurasian species probably the first published evidence of such a behaviour in passerines. In addition, eight cases of removal by parents of the traces of predation were recorded immediately or soon after (within 0.1– 4.2 hours) complete depredation of nest contents: eating at the nest or the removal by parents of egg shells, remains of egg contents, as well as feathers lost by parents as a result of predator attacks, an active or passive elimination of disturbances in the lining of the nest cup. Complete or partial “concealment of evidence” by parents occurred in about every four depredated nests, including those in which predators did not leave any “evidence”. The removal by parents of all evidence of clutch/brood failure that had happened for any reason, not only due to predation, was recorded in approximately every third nest from which all offspring disappeared without a trace before the earliest possible fledging date. These behaviours of parents could possibly be considered as bringing them to the point of absurdity, “by inertia”, a sequence of stereotypic actions to maintain cleanliness, as well as the lining of the nest. An observation was also made of a female adding fresh lining to the nest cup on top of a dead, ca. 7-day old nestling from the failed previous brood and then laying a replacement clutch. All these cases are interesting not only because they provide new information on parental behaviour in the Fieldfare. These “strange behaviours” are also a potential source of bias when studying nest predation and signs left by different predatory species with traditional methods for monitoring the nests, with neither video monitoring nor automatic photography. Furthermore, it must not be excluded that, under some circumstances, even estimates of the relative frequency of different causes of nest failure can be biased due to these behavioural curiosities. That is why it is important to know how many and how frequently do bird species show similar behaviours.
Full Text

About the authors
N. S. Morozov
Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences
Author for correspondence.
Email: morozovn33@gmail.com
Russian Federation, Moscow, 119071
References
- Бережная Т. В., Голубев А. Д., Паршина Л. Н., 2017. Аномальные гидрометеорологические явления на территории Российской Федерации в мае 2017 г. // Метеорология и гидрология. № 8. С. 131–143.
- Бережная Т. В., Голубев А. Д., Паршина Л. Н., 2020. Аномальные гидрометеорологические явления на территории Российской Федерации в мае 2020 г. // Метеорология и гидрология. № 8. С. 129–137.
- Благосклонов К. Н., 1949. Охрана и привлечение птиц полезных в сельском хозяйстве. М.: Учпедгиз. 224 с.
- Дольник В. Р., 1960. О врожденных компонентах инстинктивной деятельности птиц в гнездовой период // Вестник Ленинградского ун-та. № 21. Серия биологии. Вып. 4. С. 101–112.
- Зеленская Л. А., 2019. Экология урбанизированной популяции тихоокеанской чайки (Larus schistisagus) в сравнении с естественными колониями. 1. Особенности размещения гнезд и продуктивность // Зоологический журнал. Т. 98. № 4. С. 420–436.
- Калякин М. В., Волцит О. В., Гроот Куркамп Х. (ред.-сост.), 2014. Атлас птиц города Москвы. М.: Фитон XXI. 332 с.
- Карташев Н. Н., 1949. Птичьи базары Восточного Мурмана // Охрана природы. Сборник 7. М.: Всероссийское общество охраны природы. С. 115–122.
- Кривошеина Н. П., Морозов Н. С., Худяков В. В., 2017. К биологии паразита птиц Neottiophilum praeustum (Meigen 1826) (Diptera, Neottiophilidae) // Зоологический журнал. Т. 96. № 8. С. 937–942.
- Кривошеина Н. П., Морозов Н. С., Худяков В. В., 2018. Двукрылые насекомые (Diptera) в гнездах рябинника (Turdus pilaris) на территории Москвы // Зоологический журнал. Т. 97. № 4. С. 408–421.
- Локощенко М. А., 2018. Снежный покров // Эколого-климатические характеристики атмосферы Москвы в 2017 г. по данным Метеорологической обсерватории МГУ имени М. В. Ломоносова / Ред. М. А. Локощенко. М.: МАКС Пресс. С. 47–59.
- Мальчевский А. С., 1959. Гнездовая жизнь певчих птиц. Размножение и постэмбриональное развитие лесных воробьиных птиц европейской части СССР. Л.: Изд-во Ленинградского ун-та. 281 с.
- Мельников Ю. И., 2012. Адаптация околоводных и водоплавающих птиц к гнездованию в условиях динамичного гидрологического режима: достройка гнезд по мере подъема уровня воды // Бюллетень Московского общества испытателей природы. Отдел биологический. Т. 117. № 2. С. 3–15.
- Морозов Н. С., 2022. Роль хищников в формировании городских популяций птиц. 3. Хищники в российских городах – препятствие для синурбизации видов-жертв? // Зоологический журнал. Т. 101. № 1. С. 37–66.
- Морозов Н. С., Худяков В. В., 2016. Дрозд-рябинник (Turdus pilaris) в Москве в 2015 г.: сроки гнездования и последствия двух аномальных метеорологических явлений // Шиловцева О. А. (ред.). Эколого-климатические характеристики атмосферы в 2015 г. по данным метеорологической обсерватории МГУ. М.: МАКС Пресс. С. 220–268.
- Морозов Н. С., Худяков В. В., Панфилова И. М., 2015. Рябинник (Turdus pilaris) в большом городе: особенности размножения и репродуктивные потери из-за хищников // XIV Международная орнитологическая конференция Северной Евразии (Алматы, 18–24 августа 2015 г.). I. Тезисы. Алматы: Мензбировское орнитологическое общество. С. 342–343.
- Нумеров А. Д., 2003. Межвидовой и внутривидовой гнездовой паразитизм у птиц. Воронеж: ФГУП ИПФ Воронеж. 517 с.
- Паршина Л. Н., 2020. Погода на территории Российской Федерации в мае 2020 г. // Метеорология и гидрология. № 8. С. 123–129.
- Сатина Н. В., 2017. Погода на территории Российской Федерации в мае 2017 г. // Метеорология и гидрология. № 8. С. 126–131.
- Строков В. В., 1968. Выбрасывание птенцов из гнезд взрослыми птицами // Зоологический журнал. Т. 47. № 6. С. 951–952.
- Шутова Е. В., 1997. Влияние паразитирования каллифорид Calliphoridae (Diptera) на выживание птенцов воробьиных птиц // Русский орнитологический журнал. Экспресс-выпуск 22. С. 8–12.
- Ackerman J. T., Eadie J. Mc A., Yarris G. S., Loughman D. L., McLandress M.R., 2003. Cues for investment: nest desertion in response to partial clutch depredation in dabbling ducks // Animal Behaviour. V. 66. № 5. P. 871–883.
- Arcese P., Smith J. N.M., Hatch M. I., 1996. Nest predation by cowbirds and its consequences for passerine demography // Proceedings of the National Academy of Science of the USA. V. 93. № 10. P. 4608–4611.
- Arheimer O., Svensson S., 2008. Breeding performance of the Fieldfare Turdus pilaris in the subalpine birch zone in southern Lapland: a 20 year study // Ornis Svecica. V. 18. № 1. P. 17–44.
- Arnold T. W., 1992. The adaptive significance of eggshell removal by nesting birds: testing the egg-capping hypothesis // Condor. V. 94. № 2. P. 547–548.
- Berger A. J., 1953. Reaction of female Horned Larks to banded young // Bird Banding. V. 24. № 1. P. 19–20.
- Blair R. H., Tucker B. W., 1941. Nest sanitation // British Birds. V. 34. P. 206–215, 226–235, 250–255.
- Boal C. W., Mannan R. W., 1999. Comparative breeding ecology of Cooper’s Hawks in urban and exurban areas of southeastern Arizona // Journal of Wildlife Management. V. 63. № 1. P. 77–84.
- Boersma P. D., Rebstock G. A., 2014. Climate change increases reproductive failure in Magellanic Penguins // PLoS ONE 9 (1): e85602.
- Bordjan D., Tome D., 2014. Rain may have more influence than temperature on nest abandonment in the Great Tit Parus major // Ardea. V. 102. № 1. P. 79–86.
- Conrey R. Y., Skagen S. K., Yackel Adams A. A., Panjabi A. O., 2016. Extremes of heat, drought and precipitation depress reproductive performance in shortgrass prairie passerines // Ibis. V. 158. № 3. P. 614–629.
- Crick H. Q.P., Baillie S. R., Leech D. I., 2003. The UK Nest Record Scheme: its value for science and conservation // Bird Study. V. 50. № 3. P. 254–270.
- Davidson-Onsgard A., Jones T. M., Savides K., Kaiser S. A., 2024. Description of a Black-throated Blue Warbler (Setophaga caerulescens) incubating an empty nest and review of this breeding anomaly in birds // Wilson Journal of Ornithology. V. 136. № 3. P. 393–404.
- Dinsmore S. J., Dinsmore J. J., 2007. Modeling avian nest survival in program MARK // S. L. Jones, G. R. Geupel (eds). Beyond Mayfield: measurements of nest-survival data / Studies in Avian Biology. № 34. Camarillo, California: Cooper Ornithological Society. P. 73–83.
- Emlen S. T., Wrege P. H., 1991. Breeding biology of White-fronted Bee-eaters at Nakuru: The influence of helpers on breeder fitness // Journal of Animal Ecology. V. 60. № 1. P. 309–326.
- Etterson M. A., Nagy L. R., Robinson T. R., 2007. Partitioning risk among different causes of nest failure // Auk. V. 124. № 2. P. 432–443.
- Fisher R. J., Wellicome T. I., Bayne E. M., Poulin R. G., Todd L. D. et al., 2015. Extreme precipitation reduces reproductive output of an endangered raptor // Journal of Applied Ecology. V. 52. № 6. P. 1500–1508.
- Gimpel M. E., Carr J. M., 2017. First known case of a passerine presumably returning a dead chick to the nest // Maryland Birdlife. V. 66. № 2. P. 29–35.
- Glutz von Blotzheim U. N., 1962. Die Brutvögel der Schweiz. Eine Zussamenfassung unserer heutigen Kenntnisse über Verbreitung, Bestandesdichte, Ernährung und Fortpflanzung der seit 1900 in der Schweiz als Brutvögel nachgewiesenen Arten. Herausgegeben von der Schweizerischen Vogelwarte Sempach. Aarau: Verlag Aargauer Tagblatt. 648 s.
- Götmark F., 1992. The effects of investigator disturbance on nesting birds // D. M. Power (ed.). Current Ornithology. V. 9. New York: Plenum Press. P. 63–104.
- Guigueno M. F., Sealy S. G., 2012. Nest sanitation in passerine birds: implications for egg rejection in hosts of brood parasites // Journal of Ornithology. V. 153. № 1. P. 35–52.
- Guigueno M. F., Sealy S. G., 2017. Implications of nest sanitation in the evolution of egg rejection // M. Soler (ed.). Avian Brood Parasitism: Behaviour, Ecology, Evolution and Coevolution. Cham: Springer. P. 385–399.
- Guppy M., Guppy S., Marchant R., Priddel D., Carlile N. et al., 2017. Nest predation of woodland birds in south-east Australia: importance of unexpected predators // Emu. V. 117. № 1. P. 92–96.
- Handbook of the birds of Europe, the Middle East and North Africa. The birds of the Western Palearctic. V. 5. Tyrant Flycatchers to Thrushes, 1988 / S. Cramp (ed.). Oxford: Oxford Univ. press. 1063 p.
- Homann P. H., 1963. Reaction of Wood Warbler to young // Bird Banding. V. 34. № 1. P. 95.
- Hoover J. P., Robinson S. K., 2007. Retaliatory mafia behavior by a parasitic cowbird favors host acceptance of parasitic eggs // Proceedings of the National Academy of Sciences of the USA. V. 104. № 11. P. 4479–4483.
- Ibáñez-Álamo J.D., Sanllorente O., Soler M., 2012. The impact of researcher disturbance on nest predation rates: a meta-analysis // Ibis. V. 154. № 1. P. 5–14.
- Inch T., Nicoll M. A.C., Feare C. J., Horswill C., 2024. Population viability analysis predicts long-term impacts of commercial Sooty Tern egg harvesting to a large breeding colony on a small oceanic island // Ibis. Published Online: 2024-05-08. doi: 10.1111/ibi.13326
- Jacobson M. D., Tsakiris E. T., Long A. M., Jensen W. E., 2011. No evidence for observer effects on Lark Sparrow nest survival // Journal of Field Ornithology. V. 82. № 2. P. 184–192.
- Johnsgard P. A., Kear J., 1968. A review of parental carrying of young by waterfowl // O. S. Pettingill, D. A. Lancaster (eds). The Living Bird: Seventh Annual of the Cornell Laboratory of Ornithology. P. 89–102.
- Kirkpatrick C., Conway C. J., Ali M. H., 2009. Sanitation of entire broods of dead nestlings may bias cause-specific nest failure rates // Ibis. V. 151. № 1. P. 207–211.
- Klett A. T., Shaffer T. L., Johnson D. H., 1988. Duck nest success in the prairie pothole region // Journal of Wildlife Management. V. 52. № 3. P. 431–440.
- Larivière S., 1999. Reasons why predators cannot be inferred from nest remains // Condor. V. 101. № 3. P. 718–721.
- Li Q., Bi J., Wu J., Yang C., 2021. Impact of nest sanitation behavior on hosts’ egg rejection: an empirical study and meta-analyses // Current Zoology. V. 67. № 6. P. 683–690.
- Lobato E., Moreno J., Merino S., Sanz J. J., Arriero E. et al., 2006. Maternal clutch reduction in the Pied Flycatcher Ficedula hypoleuca: an undescribed clutch size adjustment mechanism // Journal of Avian Biology. V. 37. № 6. P. 637–641.
- Luro A. B., Hauber M. E., 2017. A test of the nest sanitation hypothesis for the evolution of foreign egg rejection in an avian brood parasite rejecter host species // The Science of Nature. V. 104. Article number 14. https://doi.org/10.1007/s00114-017-1446-8
- Major R. E., 1990. The effect of human observers on the intensity of nest predation // Ibis. V. 132. № 4. P. 608–612.
- Major R. E., 1991. Identification of nest predators by photography, dummy eggs, and adhesive tape // Auk. V. 108. № 1. P. 190–195.
- Manolis J. C., Andersen D. E., Cuthbert F. J., 2000. Uncertain nest fates in songbird studies and variation in Mayfield estimation // Auk. V. 117. № 3. P. 615–626.
- Marini M. A., Melo C., 1998. Predators of quail eggs and the evidence of the remains: implications for nest predation studies // Condor. V. 100. № 2. P. 395–399.
- Martin T. E., 1992. Breeding productivity considerations: what are the appropriate habitat features for management? // J. M. Hagan III, D. W. Johnston (eds). Ecology and Conservation of Neotropical Migrant Land Birds. Washington, DC: Smithsonian Institution Press. P. 455–473.
- Martin T. E., Geupel G. R., 1993. Nest-monitoring plots: methods for locating nests and monitoring success // Journal of Field Ornithology. V. 64. № 4. P. 507–519.
- Marzluff J. M., Withey J. C., Whittaker K. A., Oleyar M. D., Unfried T. M. et al., 2007. Consequences of habitat utilization by nest predators and breeding songbirds across multiple scales in an urbanizing landscape // Condor. V. 109. № 3. P. 516–534.
- Mayer-Gross H., Crick H. Q.P., Greenwood J. J.D., 1997. The effect of observers visiting the nests of passerines: an experimental study // Bird Study. V. 44. № 1. P. 53–65.
- Mayfield H., 1961. Nesting success calculated from exposure // Wilson Bulletin. V. 73. № 3. P. 255–261.
- Mayfield H. F., 1975. Suggestions for calculating nest success // Wilson Bulletin. V. 87. № 4. P. 456–466.
- Montevecchi W. A., 1974. Eggshell removal and nest sanitation in Ring Dove // Wilson Bulletin. V. 86. № 2. P. 136–143.
- Montevecchi W. A., 1976. Eggshell removal by Laughing Gulls // Bird-Banding. V. 47. № 2. P. 129–135.
- Montgomerie R. D., Weatherhead P. J., 1988. Risks and rewards of nest defence by parent birds // Quarterly Review of Biology. V. 63. № 2. P. 167–187.
- Moreno J., 2012. Parental infanticide in birds through early eviction from the nest: rare or under-reported? // Journal of Avian Biology. V. 43. № 1. P. 43–49.
- Newton I., 2004. Population limitation in migrants // Ibis. V. 146. № 2. P. 197–226.
- Nice M. M., 1957. Nesting success in altricial birds // Auk. V. 74. № 3. P. 305–321.
- Nichols J. D., Percival H. F., Coon R. A., Conroy M. J., Hensler G. L., Hines J. E., 1984. Observer visitation frequency and success of Mourning Dove nests: a field experiment // Auk. V. 101. № 2. P. 398–402.
- Nilsson S. G., 1984. The evolution of nest-site selection among hole-nesting birds: the importance of nest predation and competition // Ornis Scandinavica. V. 15. № 3. P. 167–175.
- Paclik M., Misik J., Weidinger K., 2009. Nest predation and nest defence in European and North American woodpeckers: a review // Annales Zoologici Fennici. V. 46. № 5. P. 361–379.
- Pavel V., Chutný B., Petrusková T., Petrusek A., 2008. Blow fly Trypocalliphora braueri parasitism on Meadow Pipit and Bluethroat nestlings in Central Europe // Journal of Ornithology. V. 149. P. 193–197.
- Pieron M. R., Rohwer F. C., 2010. Effects of large-scale predator reduction on nest success of upland nesting ducks // Journal of Wildlife Management. V. 74. № 1. P. 124–132.
- Ralph C. J., Geupel G. R., Pyle P., Martin T. E., DeSante D.F., 1993. Handbook of Field Methods for Monitoring Landbirds. USDA Forest Service General Technical Report PSW-GTR-144. 41 p.
- Ricklefs R. E., 1969. An analysis of nesting mortality in birds // Smithsonian Contributions to Zoology. № 9. P. 1–48.
- Robinson G. L., Conway C. J., Kirkpatrick C., LaRocheet D.D., 2010. Response to nestling throat ligatures by three songbirds // Wilson Journal of Ornithology. V. 122. № 4. P. 806–809.
- Rothstein S. I., 1975. An experimental and teleonomic investigation of avian brood parasitism // Condor. V. 77. № 3. P. 250–271.
- Shaffer T. L., 2004. A unified approach to analyzing nest success // Auk. V. 121. № 2. P. 526–540.
- Shitikov D., Samsonov S., Makarova T., 2019. Cold weather events provoke egg ejection behaviour in open-nesting passerines // Ibis. V. 161. № 2. P. 441–446.
- Skutch A. F., 1976. Parent Birds and Their Young. Austin: University of Texas Press. 503 p.
- Sordahl T. A., 1994. Eggshell removal behavior of American Avocets and Black-necked Stilts // Journal of Field Ornithology. V. 65. № 4. P. 461–465.
- Spear L. B., Anderson D. W., 1989. Nest-site selection by Yellow-footed Gulls // Condor. V. 91. № 1. P. 91–99.
- Stanley T. R., 2004. Estimating stage-specific daily survival probabilities of nests when nest age is unknown // Auk. V. 121. № 1. P. 134–147.
- Stewart R. M., 1972. Nestling mortality in swallows due to inclement weather // California Birds. V. 3. № 3. P. 69–70.
- Székely T., Webb J. N., Houston A. I., McNamara J.M., 1996. An evolutionary approach to offspring desertion in birds // V. Nolan Jr., E. D. Ketterson (eds). Current Ornithology, Volume 13. New York and London: Plenum Press. P. 271–330.
- Šulc M., Hughes A. E., Mari L., Troscianko J., Tomášek O. et al., 2022. Nest sanitation as an effective defence against brood parasitism // Animal Cognition. V. 25. № 4. P. 991–1002.
- Tella J. L., Hiraldo F., Donazar-Sancho J.A., Negro J. J., 1996. Costs and benefits of urban nesting in the Lesser Kestrel // D. M. Bird, D. E. Varland, J. J. Negro (eds). Raptors in Human Landscapes: Adaptions to Built and Cultivated Environments. London: Academic Press. P. 53–60.
- Tiainen J., Väisänen R. A., 1991. Nest record scheme // Monitoring bird populations: a manual of methods applied in Finland. Helsinki: Zoological Museum, Finnish Museum of Natural History, University of Helsinki. P. 75–86.
- Tinbergen N., Broekhuysen G. J., Feekes F., Houghton J. C.W., Kruuk H., Szulc E., 1962. Egg shell removal by the Black-headed Gull, Larus ridibundus L.; a behaviour component of camouflage // Behaviour. V. 19. № 1/2. P. 74–117.
- Thompson F. R. III, 2007. Factors affecting nest predation on forest songbirds in North America // Ibis. V. 149. Suppl. 2. P. 98–109.
- Vuorisalo T., Andersson H., Hugg T., Lahtinen R., Laaksonen H. et al., 2003. Urban development from an avian perspective: causes of hooded crow (Corvus corone cornix) urbanization in two Finnish cities // Landscape and Urban Planning. V. 62. № 2. P. 69–87.
- Weidinger К., 2008. Nest monitoring does not increase nest predation in open-nesting songbirds: inference from continuous nest-survival data // Auk. V. 125. № 4. P. 859–868.
- Wesołowski T., Tomiałojć L., 2005. Nest sites, nest depredation, and productivity of avian broods in a primeval temperate forest: do the generalisations hold? // Journal of Avian Biology. V. 36. № 5. P. 361–367.
- Westmoreland D., Best L. B., 1985. The effect of disturbance on Mourning Dove nesting success // Auk. V. 102. № 4. P. 774–780.
- Whittingham M. J., Bradbury R. B., Wilson J. D., Morris A. J., Perkins A. J. et al., 2001. Chaffinch Fringilla coelebs foraging patterns, nestling survival and territory distribution on lowland farmland // Bird Study. V. 48. № 3. P. 257–270.
- Wiggins D. A., Pärt T., Gustafsson L., 1994. Correlates of clutch desertion by female Collared Flycatchers Ficedula albicollis // Journal of Avian Biology. V. 25. № 2. P. 93–97.
- Wiklund C. G., 1982. Fieldfare (Turdus pilaris) breeding success in relation to colony size, nest position and association with Merlins (Falco columbarius) // Behavioral Ecology and Sociobiology. V. 11. № 3. P. 165–172.
- Wiklund C. G., Andersson M., 1994. Natural selection of colony size in a passerine bird // Journal of Animal Ecology. V. 63. № 4. P. 765–774.
- Yang C., Wang L., Liang W., Møller A. P., 2015. Nest sanitation behavior in hirundines as a pre-adaptation to egg rejection to counter brood parasitism // Animal Cognition. V. 18. № 1. P. 355–360.
- Zając T., 1995. Selection on laying date in the Blue Tit Parus caeruleus and the Great Tit Parus major caused by weather conditions // Acta Ornithologica. V. 30. № 2. P. 145–151.
Supplementary files
