Abstract
Constant nest attentiveness, which benefits avian embryos, and body maintenance activities (e.g., foraging trips) by incubating parents are mutually exclusive activities. To balance these, parents must schedule the time spent on and off their nests according to a wide range of environmental conditions that change the costs and benefits of breaking or continuing an incubation bout. Here, we used data from 38 camera-monitored nests over two breeding seasons on Robben Island, Southern Africa to examine how African Black Oystercatchers Haematopus moquini, a biparental incubator, varied incubation bout length in relation to environmental variables that would have affected energy/water budgets: tide phase, air temperature, windspeed and time of day (day versus night). We predicted that incubation bout duration would decrease at high temperatures and wind speeds when energetic and water needs increase and increase at high tides when foraging opportunities decrease. Oystercatchers’ overall nest attentiveness was high at 95%. Incubation bout length was longer at high tide and at night than at low tide and during the day. Incubation bout length decreased with increases in temperature but had a non-linear relationship with windspeed that varied by the time of day: it increased sharply with windspeed and plateaued at high windspeed during the day, but largely declined with moderate to high windspeeds at night. These results suggest that oystercatchers’ energetic, thermoregulatory, and hydration needs may have increased with high heat loads during the day but decreased at night and with increased windspeed during the day, and oystercatchers responded by varying incubation bout lengths accordingly. The proximity of their nests to the intertidal zone, which means short travel time and quick access to food, water, and thermoregulatory opportunities, seems to be of vital importance to their capacity to maintain high nest attentiveness and deal with increasing heat loads.
Zusammenfassung
Zeitmanagement bei brütenden Kapausternfischern Haematopus moquini : Einflüsse von Wetter, Gezeiten und Tageszeit
Ständige Nestfürsorge, die den Vogelembryos zugutekommt, und Selbsterhaltungsmaßnahmen (beispielsweise Nahrungssuche) der brütenden Elterntiere sind Aktivitäten, die sich gegenseitig ausschließen. Um diese miteinander vereinbaren zu können, müssen die Eltern die auf dem oder fern vom Nest verbrachte Zeit abhängig von einem breiten Spektrum an Umweltvariablen organisieren, welche Kosten und Nutzen der Entscheidung, eine Brutpause einzulegen oder nicht, verändern. Auf der Grundlage von an 38 kameraüberwachten Nestern über zwei Brutsaisons auf Robben Island (Südafrika) gewonnenen Daten untersuchten wir, wie Kapausternfischer Haematopus moquini, eine Vogelart, bei der beide Elternteile brüten, die Dauer der Brutphasen im Verhältnis zu Umweltvariablen mit Einfluss auf ihren Energie- und Wasseraushalt veränderten: Gezeitenphase, Lufttemperatur, Windgeschwindigkeit und Tageszeit (Tag/Nacht). Wir erwarteten, dass die Länge der Brutabschnitte bei hohen Temperaturen und Windgeschwindigkeiten mit wachsendem Energie- und Wasserbedarf abnähmen; wenn bei Flut die Nahrungssuche schwieriger wird, sollte die Länge der Brutphasen dagegen zunehmen. Insgesamt verbrachten die Austernfischer mit 95% einen Großteil der Zeit auf dem Nest. Die Brutphasen waren bei Flut und des Nachts länger als bei Ebbe und tagsüber. Die Dauer der Brutphasen nahm mit zunehmender Umgebungstemperatur ab, stand jedoch mit der Windgeschwindigkeit in einem nichtlinearen Verhältnis, welches sich mit der Tageszeit änderte: Tagsüber stieg die Dauer mit der Windgeschwindigkeit steil an, um bei hoher Windgeschwindigkeit ein Plateau zu erreichen; nachts dagegen fiel sie bei mittleren bis hohen Windgeschwindigkeiten zumeist ab. Diese Ergebnisse deuten darauf hin, dass der Bedarf der Austernfischer hinsichtlich Energie, Thermoregulation und Wasserzufuhr mit wachsender Wärmebelastung im Tagesverlauf angestiegen, bei Nacht jedoch sowie bei zunehmender Windgeschwindigkeit bei Tag gesunken sein könnte und dass die Austernfischer darauf mit entsprechenden Änderungen in der Brutdauer reagierten. Die räumliche Nähe der Nester zur Gezeitenzone bedeutet kurze Wege sowie schnellen Zugang zu Nahrung, Wasser und thermoregulatorischen Möglichkeiten und scheint von entscheidender Bedeutung für die Fähigkeit der Austernfischer zu starker Nestfürsorge und der Bewältigung zunehmender Wärmebelastung zu sein.
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Data and r script are available as supplementary files. Data can also be accessed through University of Cape Town's Zivahub Digital Repository.
References
Adams N, KerleyZ G, Watson J (1999) Disturbance of incubating African Black Oystercatchers: is heating of exposed eggs a problem? Ostrich 70:225–228
Afton AD (1980) Factors affecting incubation rythms of Northern Shovelers. Condor 82:132–137
AlRashidi M (2016) The challenge of coping in an extremely hot environment: a case study of the incubation of Lesser Crested Terns (Thalasseus bengalensis). Waterbirds 39:215–221
AlRashidi M, Kosztolányi A, Küpper C et al (2010) The influence of extreme hot environment on biparental incubation of a ground-nesting shorebird, the Kentish Plover Charadrius alexandrinus. Front Zool 7:1–10
AlRashidi M, Kosztolányi A, Shobrak M et al (2011) Parental cooperation in an extreme hot environment: natural behaviour and experimental evidence. Anim Behav 82:235–243
Amat JA, Masero JA (2004) How Kentish Plovers, Charadrius alexandrinus, cope with heat stress during incubation. Behav Ecol Sociobiol 56:26–33
Amat JA, Masero JA (2007) The functions of belly-soaking in Kentish Plovers Charadrius alexandrinus. Ibis 149:91–97
Amininasab SM, Kingma SA, Birker M et al (2016) The effect of ambient temperature, habitat quality and individual age on incubation behaviour and incubation feeding in a socially monogamous songbird. Behav Ecol Sociobiol 70:1591–1600
Ar A, Rahn H (1980) Water in the avian egg: overall budget of incubation. Am Zool 20:373–384
Azaki BDA (2021) The breeding ecology and behavioural adaptations of African Black Oystercatchers in light of climate change. Ph.D. Thesis University of Cape Town. https://open.uct.ac.za/handle/11427/35657
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48
Battley PF, Rogers DI, Piersma T, Koolhaas A (2003) Behavioural evidence for heat-load problems in Great Knots in tropical Australia fuelling for long-distance flight. Emu 103:97–103
Bourne AR, Ridley AR, Mckechnie AE et al (2021) Dehydration risk is associated with reduced nest attendance and hatching success in a cooperatively breeding bird, the Southern Pied babbler Turdoides bicolor. Conserv Physiol 9:1–16. https://doi.org/10.1093/conphys/coab043
Brambilla M, Scridel D, Sangalli B et al (2019) Ecological factors affecting foraging behaviour during nestling rearing in a high-elevation species, the White-winged Snowfinch (Montifringilla nivalis). Ornis Fenn 96:142–151
Bulla M, Valcu M, Rutten AL, Kempenaers B (2014) Biparental incubation patterns in a high-arctic breeding shorebird: how do pairs divide their duties? Behav Ecol 25:152–164
Bulla M, Stich E, Valcu M, Kempenaers B (2015) Off-nest behaviour in a biparentally incubating shorebird varies with sex, time of day and weather. Ibis 157:575–589
Burger J (2018) Use of intertidal habitat by four species of shorebirds in an experimental array of oyster racks, reefs and controls on Delaware Bay, New Jersey: avoidance of oyster racks. Sci Total Environ 624:1234–1243
Burger J, Niles L, Jeitner C, Gochfeld M (2018) Habitat risk: Use of intertidal flats by foraging Red Knots (Calidris canutus rufa), Ruddy Turnstones, (Arenaria interpres), Semipalmated Sandpipers (Calidris pusilla), and Sanderling (Calidris alba) on Delaware Bay beaches. Environ Res 165:237–246
Buxton EJM (1961) The inland breeding of the oystercatcher in Great Britain, 1958–59. Bird Study 8:198–209
Cantar RV, Montgomerie RD (1985) The influence of weather on incubation scheduling of the White-rumped Sandpiper (Calidris fuscicollis): a uniparental incubator in a cold environment. Behaviour 95:261–289
Cervencl A, Esser W, Maier M et al (2011) Can differences in incubation patterns of common Redshanks Tringa totanus be explained by variations in predation risk? J Ornithol 152:1033–1043. https://doi.org/10.1007/s10336-011-0696-z
Chaurand T, Weimerskirch H (1994) Incubation routine, body mass regulation and egg neglect in the Blue Petrel Halobaena caerulea. Ibis 136:285–290
Cresswell W (1997) Nest predation: the relative effects of nest characteristics, clutch size and parental behaviour. Anim Behav 53:93–103
Cresswell W, Holt S, Reid JM et al (2003) Do energetic demands constrain incubation scheduling in a biparental species? Behav Ecol 14:97–102
Cresswell W, Holt S, Reid JM et al (2004) The energetic costs of egg heating constrain incubation attendance but do not determine daily energy expenditure in the Pectoral Sandpiper. Behav Ecol 15:498–507
Dawson WR (1982) Evaporative losses of water by birds. Comp Biochem Physiol 71A:495–509
De Marchi G, Chiozzi G, Dell’Omo G, Fasola M (2015) Low incubation investment in the burrow-nesting Crab Plover Dromas ardeola permits extended foraging on a tidal food resource. Ibis 157:31–43
Dickinson AM, Goodman AM, Deeming DC (2019) Air movement affects insulatory values of nests constructed by Old World Warblers. J Therm Biol 81:194–200
Ekanayake KB, Weston MA, Nimmo DG et al (2015) The bright incubate at night: sexual dichromatism and adaptive incubation division in an open-nesting shorebird. Proc R Soc B Biol Sci 282:20143026
Gerson AR, McKechnie AE, Smit B et al (2019) The functional significance of facultative hyperthermia varies with body size and phylogeny in birds. Funct Ecol 33:597–607
Grant GS (1982) Avian incubation: egg temperature, nest humidity, and behavioural thermoregulation in a hot environment. Ornithol Monogr 30:1–75
Grémillet D (1997) Catch per unit effort, foraging efficiency, and parental investment in breeding Great Cormorants (Phalacrocorax carbo carbo). ICES J Mar Sci 54:635–644
Hall KRL (1959) Observations on the nest-sites and nesting behaviour of the Black Oystercatcher Haematopus moquini in the Cape Peninsula. Ostrich 30:143–154
Heenan CB, Seymour RS (2012) The effect of wind on the rate of heat loss from avian cup-shaped nests. PLoS One 7:e32252
Hilton GM, Ruxton GD, Reid JM, Monaghan P (2004) Using artificial nests to test importance of nesting material and nest shelter for incubation energetics. Auk 121:777–787
Hockey PAR (1981) Morphometrics and sexing of the African Black Oystercatcher. Ostrich 52:244–247
Hockey PAR (1983) Ecology of the African Black Oystercatcher Haematopus moquini. University of Cape Town, Cape Town
Hoppe IR, Harrison JO, Raynor EJ et al (2019) Temperature, wind, vegetation, and roads influence incubation patterns of Greater Prairie-Chickens (Tympanuchus cupido pinnatus) in the Nebraska Sandhills, USA. Can J Zool 97:91–99. https://doi.org/10.1139/cjz-2018-0130
Klimczuk E, Halupka L, Czyż B et al (2015) Factors driving variation in biparental incubation behaviour in the Reed Warbler Acrocephalus scirpaceus. Ardea 103:51–59
Kohler S, Bonnevie B, Dano S (2009) Can eyeflecks be used to sex African Black Oystercatchers Haematopus moquini in the field? Ostrich 80:109–110
Leseberg A (2001) The foraging ecology, demographics and conservation of African Black Oystercatchers Haematopus moquini in Namibian nursery areas. University of Cape Town, Cape Town
MacDonald EC, Camfield AF, Jankowski JE, Martin K (2013) Extended incubation recesses by alpine-breeding Horned Larks: a strategy for dealing with inclement weather? J F Ornithol 84:58–68
Martin TE, Scott J, Menge C (2000) Nest predation increases with parental activity: separating nest site and parental activity effects. Proc R Soc B Biol Sci 267:2287–2293
Martin TE, Auer SK, Bassar RD et al (2007) Geographic variation in avian incubation periods and parental influences on embryonic temperature. Evolution 61:2558–2569
Moreno J (1989) Strategies of mass change in breeding birds. Biol J Linn Soc 37:297–310
Ntiamoa-Baidu Y, Piersma T, Wiersma P et al (1998) Water depth selection, daily feeding routines and diets of waterbirds in coastal lagoons in Ghana. Ibis 140:89–103
Oswald SA, Bearhop S, Furness RW et al (2008) Heat stress in a high-latitude seabird: effects of temperature and food supply on bathing and nest attendance of Great Skuas Catharacta skua. J Avian Biol 39:163–169
R Core Team (2019) R: a language and environment for statistical computing
Ramli R, Norazlimi NA (2016) Effects of tidal states and time of day on the abundance and behavior of shorebirds utilizing tropical intertidal environment. J Anim Plant Sci 26:1164–1171
Sharpe L, Cale B, Gardner JL (2019) Weighing the cost: the impact of serial heatwaves on body mass in a small Australian passerine. J Avian Biol 50:1–9
Sládeček M, Vozabulová E, Šálek ME, Bulla M (2019) Diversity of incubation rhythms in a facultatively uniparental shorebird—the Northern Lapwing. Sci Rep 9:1–11
Spiegel CS, Haig SM, Goldstein MI, Huso M (2012) Factors affecting incubation patterns and sex roles of Black Oystercatchers in Alaska. Condor 114:123–134
Thierry A-M, Massemin S, Handrich Y, Raclot T (2013) Elevated corticosterone levels and severe weather conditions decrease parental investment of incubating Adélie Penguins. Horm Behav 63:475–483
Tulp I, Schekkerman H (2006) Time allocation between feeding and incubation in uniparental arctic-breeding shorebirds: energy reserves provide leeway in a tight schedule. J Avian Biol 37:207–218. https://doi.org/10.1111/j.2006.0908-8857.03519.x
Vafidis JO, Facey RJ, Leech D, Thomas RJ (2018) Supplemental food alters nest defence and incubation behaviour of an open-nesting wetland songbird. J Avian Biol 49:e01672
Weathers WW (1981) Physiological thermoregulation in heat-stressed birds: consequences of body size. Physiol Zool 54:345–361
Wilson AM, Vickery JA, Brown A et al (2005) Changes in the numbers of breeding waders on lowland wet grasslands in England and Wales between 1982 and 2002. Bird Study 52:55–69
Yorio P, Boersma PDEE (1994) Causes of nest desertion during incubation in the Magellanic Penguin (Spheniscus magellanicus). Condor 96:1076–1083
Zhang L, Shu M, An B et al (2017) Biparental incubation pattern of the Black-necked Crane on an alpine plateau. J Ornithol 158:697–705. https://doi.org/10.1007/s10336-017-1439-6
Acknowledgements
This work was supported by the Leventis Foundation through the A. P. Leventis Ornithological Research Institute, Jos, Nigeria. Mr Sabelo Madlala and his team from the Environmental Unit of Robben Island Museum facilitated access to Robben Island. Air temperature data were provided by the South African Weather Services through Elsa DeJager, Lucky Dlamini, and Musa Mkhwanazi. Tide height data for the Cape Town harbour area were supplied by the Hydrographer, South African Navy, Ruth Farre. Professor LG Underhill, Ms Sue Kuyper and all the field assistants who supported fieldwork during this research are acknowledged.
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BDAB: conceptualization, data curation, funding acquisition, methodology design, resources, investigation, formal analysis, visualization, writing—original draft, writing—review and editing; SJC: validation, supervision, writing—review and editing; WC: methodology design, resources, validation, writing—review and editing.
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Braimoh-Azaki, B.D.A., Cunningham, S.J. & Cresswell, W. Incubation scheduling by African Black Oystercatchers: effects of weather, tide phase, and time of day. J Ornithol 164, 139–149 (2023). https://doi.org/10.1007/s10336-022-02023-x
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DOI: https://doi.org/10.1007/s10336-022-02023-x