Urban resources limit pair coordination over offspring provisioning

Royle, N. J., Smiseth, P. T. & Kölliker, M. The Evolution of Parental Care (Oxford University Press, Oxford, 2012).

Google Scholar 

Williams, G. C. Natural selection, the costs of reproduction, and a refinement of Lack’s principle. Am. Nat. 100, 687–690 (1966).

Article  Google Scholar 

Trivers, R. L. Sexual Selection and the Descent of Man 136–179 (Aldine Press, Chicago, 1972).

Google Scholar 

Lessells, C. M. The Evolution of Parental Care (Oxford Univeristy Press, Oxford, 2012).

Google Scholar 

Houston, A. I., Székely, T. & McNamara, J. M. Conflict between parents over care. Trends Ecol. Evol. 20, 33–38 (2005).

Article  Google Scholar 

Lessells, C. M. The evolutionary outcome of sexual conflict. Philos. Trans. R. Soc. B Biol. Sci. 361, 301–317 (2006).

CAS  Article  Google Scholar 

Houston, A. I. & Davies, N. B. The evolution of cooperation and life history in the dunnock, Prunella modularis. Behav. Ecol. Ecol. Conseq. Adapt. Behav. 20, 471–487 (1985).

Google Scholar 

McNamara, J. M., Gasson, C. E. & Houston, A. I. Incorporating rules for responding into evolutionary games. Nature 401, 368–371 (1999).

ADS  CAS  PubMed  Google Scholar 

McNamara, J. M., Houston, A. I., Barta, Z. & Osorno, J. L. Should young ever be better off with one parent than with two?. Behav. Ecol. 14, 301–310 (2003).

Article  Google Scholar 

Lessells, C. M. & McNamara, J. M. Sexual conflict over parental investment in repeated bouts: Negotiation reduces overall care. Proc. R. Soc. B Biol. Sci. 279, 1506–1514 (2012).

CAS  Article  Google Scholar 

Johnstone, R. A. & Hinde, C. A. Negotiation over offspring care – how should parents respond to each other’s efforts?. Behav. Ecol. 17, 818–827 (2006).

Article  Google Scholar 

Royle, N. J., Hartley, I. R. & Parker, G. A. Sexual conflict reduces offspring fitness in zebra finches. Nature 416, 733–736 (2002).

ADS  CAS  Article  Google Scholar 

Johnstone, R. A. et al. Reciprocity and conditional cooperation between great tit parents. Behav. Ecol. 25, 216–222 (2014).

Article  Google Scholar 

Savage, J. L., Browning, L. E., Manica, A., Russell, A. F. & Johnstone, R. A. Turn-taking in cooperative offspring care: By-product of individual provisioning behavior or active response rule?. Behav. Ecol. Sociobiol. 71, 162 (2017).

Article  Google Scholar 

Raihani, N. J., Nelson-Flower, M. J., Moyes, K., Browning, L. E. & Ridley, A. R. Synchronous provisioning increases brood survival in cooperatively breeding pied babblers. J. Anim. Ecol. 79, 44–52 (2010).

Article  Google Scholar 

Mariette, M. M. & Griffith, C. S. The adaptive significance of provisioning and foraging coordination between breeding partners. Am. Nat. 185, 270–280 (2015).

Article  Google Scholar 

Bebbington, K. & Hatchwell, B. J. Coordinated parental provisioning is related to feeding rate and reproductive success in a songbird. Behav. Ecol. 27, 652–659 (2016).

Article  Google Scholar 

Leniowski, K. & Węgrzyn, E. Synchronisation of parental behaviours reduces the risk of nest predation in a socially monogamous passerine bird. Sci. Rep. 8, 7385 (2018).

ADS  CAS  Article  Google Scholar 

Shen, S. F., Chen, H. C., Vehrencamp, S. L. & Yuan, H. W. Group provisioning limits sharing conflict among nestlings in joint-nesting Taiwan yuhinas. Biol. Lett. 6, 318–321 (2010).

Article  Google Scholar 

Savage, J. L. & Hinde, C. A. What can we quantify about carer behavior?. Front. Ecol. Evol. https://doi.org/10.3389/fevo.2019.00418 (2019).

Article  Google Scholar 

Baldan, D., Curk, T., Hinde, C. A. & Lessells, C. M. Alternation of nest visits varies with experimentally manipulated workload in brood-provisioning great tits. Anim. Behav. 156, 139–146. https://doi.org/10.1016/j.anbehav.2019.08.004 (2019).

Article  Google Scholar 

Griffioen, M., Müller, W. & Iserbyt, A. A fixed agreement—consequences of brood size manipulation on alternation in blue tits. PeerJ 7, e6826. https://doi.org/10.7717/peerj.6826 (2019).

Article  PubMed  PubMed Central  Google Scholar 

Iserbyt, A., Fresneau, N., Kortenhoff, T., Eens, M. & Muller, W. Decreasing parental task specialization promotes conditional cooperation. Sci. Rep. 7, 20 (2017).

Article  Google Scholar 

Baldan, D., Hinde, C. A. & Lessells, C. M. Turn-taking between provisioning parents: Partitioning alternation. Front. Ecol. Evol. https://doi.org/10.3389/fevo.2019.00448 (2019).

Article  Google Scholar 

Lejeune, L. et al. Environmental effects on parental care visitation patterns in blue tits Cyanistes caeruleus. Front. Ecol. Evol. https://doi.org/10.3389/fevo.2019.00356 (2019).

Article  Google Scholar 

Longcore, T. & Rich, C. Ecological light pollution. Front. Ecol. Environ. 2, 191–198. https://doi.org/10.1890/1540-9295(2004)002[0191:Elp]2.0.Co;2 (2004).

Article  Google Scholar 

Warren, P. S., Katti, M., Ermann, M. & Brazel, A. Urban bioacoustics: It’s not just noise. Anim. Behav. 71, 491–502. https://doi.org/10.1016/j.anbehav.2005.07.014 (2006).

Article  Google Scholar 

McCarthy, M. P., Best, M. J. & Betts, R. A. Climate change in cities due to global warming and urban effects. Geophys. Res. Lett. https://doi.org/10.1029/2010gl042845 (2010).

Article  Google Scholar 

Chamberlain, D. E. et al. Avian productivity in urban landscapes: A review and meta-analysis. Ibis 151, 1–18. https://doi.org/10.1111/j.1474-919X.2008.00899.x (2009).

Article  Google Scholar 

Pollock, C. J., Capilla-Lasheras, P., McGill, R. A. R., Helm, B. & Dominoni, D. M. Integrated behavioural and stable isotope data reveal altered diet linked to low breeding success in urban-dwelling blue tits (Cyanistes caeruleus). Sci. Rep. 7, 5014. https://doi.org/10.1038/s41598-017-04575-y (2017).

ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

Seress, G. et al. Impact of urbanization on abundance and phenology of caterpillars and consequences for breeding in an insectivorous bird. Ecol. Appl. 28, 1143–1156. https://doi.org/10.1002/eap.1730 (2018).

Article  PubMed  Google Scholar 

Seress, G., Sándor, K., Evans, K. L. & Liker, A. Food availability limits avian reproduction in the city: An experimental study on great tits Parus major. J. Anim. Ecol. 00, 1–11. https://doi.org/10.1111/1365-2656.13211 (2020).

Article  Google Scholar 

Wilkin, T. A., King, L. E. & Sheldon, B. C. Habitat quality, nestling diet, and provisioning behaviour in great tits Parus major. J. Avian Biol. 40, 135–145. https://doi.org/10.1111/j.1600-048X.2009.04362.x (2009).

Article  Google Scholar 

Peach, W. J., Mallord, J. W., Ockendon, N., Orsman, C. J. & Haines, W. G. Depleted suburban house sparrow Passer domesticus population not limited by food availability. Urban Ecosyst. 21, 1053–1065. https://doi.org/10.1007/s11252-018-0784-4 (2018).

Article  Google Scholar 

Schoech, S. J. et al. Food supplementation: A tool to increase reproductive output? A case study in the threatened Florida Scrub-Jay. Biol. Cons. 141, 162–173. https://doi.org/10.1016/j.biocon.2007.09.009 (2008).

Article  Google Scholar 

Sol, D., Lapiedra, O. & González-Lagos, C. Behavioural adjustments for a life in the city. Anim. Behav. 85, 1101–1112. https://doi.org/10.1016/j.anbehav.2013.01.023 (2013).

Article  Google Scholar 

Isaksson, C. & Andersson, S. Carotenoid diet and nestling provisioning in urban and rural great tits Parus major. J. Avian Biol. 38, 564–572. https://doi.org/10.1111/j.2007.0908-8857.04030.x (2007).

Article  Google Scholar 

New, T. R. Insect Conservation and Urban Environments (Springer, Berlin, 2015).

Google Scholar 

Helden, A., Stamp, G. & Leather, S. Urban biodiversity: Comparison of insect assemblages on native and non-native trees. Urban Ecosyst. 15, 611–624. https://doi.org/10.1007/s11252-012-0231-x (2012).

Article  Google Scholar 

Tallamy, D. W. & Shropshire, K. J. Ranking lepidopteran use of native versus introduced plants. Conserv. Biol. 23, 941–947 (2009).

Article  Google Scholar 

Burghardt, K. T., Tallamy, D. W., Philips, C. & Shropshire, K. J. Non-native plants reduce abundance, richness, and host specialization in lepidopteran communities. Ecosphere 1, art11. https://doi.org/10.1890/es10-00032.1 (2010).

Article  Google Scholar 

Marciniak, B., Nadolski, J., Nowakowska, M., Loga, B. & Bańbura, J. Habitat and annual variation in arthropod abundance affects blue tit Cyanistes caeruleus reproduction. Acta Ornithol. 42, 53–62 (2007).

Article  Google Scholar 

Neil, K. & Wu, J. Effects of urbanization on plant flowering phenology: A review. Urban Ecosyst. 9, 243–257. https://doi.org/10.1007/s11252-006-9354-2 (2006).

Article  Google Scholar 

Lessells, C. M. & Stephens, D. W. Central place foraging: Single-prey loaders again. Anim. Behav. 31, 238–243 (1983).

Article  Google Scholar 

Orians, G. H. & Pearson, N. E. On the Theory of Central Place Foraging. Analysis of Ecological Systems 155–177 (Ohio State University Press, Columbus, 1979).

Google Scholar 

Arnold, K. E., Ramsay, S. L., Henderson, L. & Larcombe, S. D. Seasonal variation in diet quality: Antioxidants, invertebrates and blue tits Cyanistes caeruleus. Biol. J. Lin. Soc. 99, 708–717. https://doi.org/10.1111/j.1095-8312.2010.01377.x (2010).

Article  Google Scholar 

Ouyang, J. Q., Baldan, D., Munguia, C. & Davies, S. Genetic inheritance and environment determine endocrine plasticity to urban living. Proc. R. Soc. B Biol. Sci. 286, 20191215. https://doi.org/10.1098/rspb.2019.1215 (2019).

CAS  Article  Google Scholar 

Newhouse, M. J., Marra, P. P. & Johnson, L. S. Reproductive success of house wrens in suburban and rural landscapes. Wilson J. Ornithol. 120, 99–104 (2008).

Article  Google Scholar 

Potti, J., Dávila, J. A., Tella, J. L., Frías, Ó & Villar, S. Gender and viability selection on morphology in fledgling pied flycatchers. Mol. Ecol. 11, 1317–1326. https://doi.org/10.1046/j.1365-294X.2002.01545.x (2002).

CAS  Article  PubMed  Google Scholar 

Balogh, A. L., Ryder, T. B. & Marra, P. P. Population demography of Gray Catbirds in the suburban matrix: Sources, sinks and domestic cats. J. Ornithol. 152, 717–726. https://doi.org/10.1007/s10336-011-0648-7 (2011).

Article  Google Scholar 

Stillfried, M. et al. Do cities represent sources, sinks or isolated islands for urban wild boar population structure?. J. Appl. Ecol. 54, 272–281. https://doi.org/10.1111/1365-2664.12756 (2017).

Article  Google Scholar 

Holmes, R. T. Foraging patterns of forest birds: Male–female differences. Wilson Bull. 98, 196–213 (1986).

Google Scholar 

Chaves, F. G., Vecchi, M. B. & Alves, M. A. S. Intersexual differences in the foraging behavior of Formicivora littoralis (Thamnophilidae), an endangered Neotropical bird. Stud. Neotrop. Fauna Environ. 52, 179–186. https://doi.org/10.1080/01650521.2017.1335275 (2017).

Article  Google Scholar 

Mänd, R., Rasmann, E. & Mägi, M. When a male changes his ways: Sex differences in feeding behavior in the pied flycatcher. Behav. Ecol. 24, 853–858. https://doi.org/10.1093/beheco/art025 (2013).

Article  Google Scholar 

Kölliker, M., Brinkhof, M. W. G., Heeb, P., Fitze, P. S. & Richner, H. The quantitative genetic basis of offspring solicitation and parental response in a passerine bird with biparental care. Proc. R. Soc. Lond. Ser. B Biol. Sci. 267, 2127–2132 (2000).

Article  Google Scholar 

Naef-Daenzer, B. Patch time allocation and patch sampling by foraging great and blue tits. Anim. Behav. 59, 989–999 (2000).

CAS  Article  Google Scholar 

Jarrett, C., Powell, L. L., McDevitt, H., Helm, B. & Welch, A. J. Bitter fruits of hard labour: Diet metabarcoding and telemetry reveal that urban songbirds travel further for lower-quality food. Oecologia 193, 377–388. https://doi.org/10.1007/s00442-020-04678-w (2020).

ADS  Article  PubMed  PubMed Central  Google Scholar 

Gering, J. C. & Blair, R. B. Predation on artificial bird nests along an urban gradient: Predatory risk or relaxation in urban environments?. Ecography 22, 532–541. https://doi.org/10.1111/j.1600-0587.1999.tb01283.x (1999).

Article  Google Scholar 

Fischer, J. D., Cleeton, S. H., Lyons, T. P. & Miller, J. R. Urbanization and the predation paradox: The role of trophic dynamics in structuring vertebrate communities. Bioscience 62, 809–818. https://doi.org/10.1525/bio.2012.62.9.6 (2012).

Article  Google Scholar 

Vincze, E. et al. Does urbanization affect predation of bird nests? A meta-analysis. Front. Ecol. Evol. https://doi.org/10.3389/fevo.2017.00029 (2017).

Article  Google Scholar 

Griggio, M. & Hoi, H. An experiment on the function of the long-term pair bond period in the socially monogamous bearded reedling. Anim. Behav. 82, 1329–1335. https://doi.org/10.1016/j.anbehav.2011.09.016 (2011).

Article  Google Scholar 

Griffith, S. C. Cooperation and coordination in socially monogamous birds: Moving away from a focus on sexual conflict. Front. Ecol. Evol. https://doi.org/10.3389/fevo.2019.00455 (2019).

Article  Google Scholar 

Alberti, M. Eco-evolutionary dynamics in an urbanizing planet. Trends Ecol. Evol. 30, 114–126. https://doi.org/10.1016/j.tree.2014.11.007 (2015).

Article  PubMed  Google Scholar 

Liebl, A. L. & Martin, L. B. Exploratory behaviour and stressor hyper-responsiveness facilitate range expansion of an introduced songbird. Proc. Biol. Sci. 279, 4375–4381. https://doi.org/10.1098/rspb.2012.1606 (2012).

Article  PubMed  PubMed Central  Google Scholar 

Sepp, T., McGraw, K. J., Kaasik, A. & Giraudeau, M. A review of urban impacts on avian life-history evolution: Does city living lead to slower pace of life?. Glob. Change Biol. 24, 1452–1469. https://doi.org/10.1111/gcb.13969 (2018).

ADS  Article  Google Scholar 

Patricelli, G. L. & Blickley, J. L. Avian communication in urban noise: Causes and consequences of vocal adjustment. Auk 123, 639–649. https://doi.org/10.1093/auk/123.3.639 (2006).

Article  Google Scholar 

Grabarczyk, E. E. & Gill, S. A. Anthropogenic noise affects male house wren response to but not detection of territorial intruders. PLoS One 14, e0220576. https://doi.org/10.1371/journal.pone.0220576 (2019).

CAS  Article  PubMed  PubMed Central  Google Scholar 

Schroeder, J., Nakagawa, S., Cleasby, I. R. & Burke, T. Passerine birds breeding under chronic noise experience reduced fitness. PLoS One 7, e39200. https://doi.org/10.1371/journal.pone.0039200 (2012).

ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

Halfwerk, W. et al. Low-frequency songs lose their potency in noisy urban conditions. Proc. Natl. Acad. Sci. 108, 14549–14554. https://doi.org/10.1073/pnas.1109091108 (2011).

ADS  Article  PubMed  Google Scholar 

Mariette, M. M. Acoustic cooperation: Acoustic communication regulates conflict and cooperation within the family. Front. Ecol. Evol. https://doi.org/10.3389/fevo.2019.00445 (2019).

Article  Google Scholar 

Johnstone, R. A. & Savage, J. L. Conditional cooperation and turn-taking in parental care. Front. Ecol. Evol. https://doi.org/10.3389/fevo.2019.00335 (2019).

Article  Google Scholar 

Ihle, M., Pick, J. L., Winney, I. S., Nakagawa, S. & Burke, T. Measuring up to reality: Null models and analysis simulations to study parental coordination over provisioning offspring. Front. Ecol. Evol. https://doi.org/10.3389/fevo.2019.00142 (2019).

Article  Google Scholar 

Ihle, M. et al. Rearing success does not improve with apparent pair coordination in offspring provisioning. Front. Ecol. Evol. https://doi.org/10.3389/fevo.2019.00405 (2019).

Article  Google Scholar 

Seress, G., Lipovits, A., Bokony, V. & Czuni, L. Quantifying the urban gradient: A practical method for broad measurements. Landsc. Urban Plan. 131, 42–50. https://doi.org/10.1016/j.landurbplan.2014.07.010 (2014).

Article  Google Scholar 

75Johnson, L. S. in The Birds of North America (ed Editor A. F. Poole) (2014).

Pearse, A. T., Cavitt, J. F. & Cully, J. F. effects of food supplementation on female nest attentiveness and incubation mate feeding in two sympatric wren species. Wilson Bull. 116, 23–30 (2004).

Article  Google Scholar 

Greenewalt, C. H. & Jones, F. M. Photographic studies of the feeding of nestling house wrens. Proc. Am. Philos. Soc. 99, 200–204 (1955).

Google Scholar 

Welbers, A. A. M. H. et al. Artificial light at night reduces daily energy expenditure in breeding great tits (Parus major). Front. Ecol. Evol. https://doi.org/10.3389/fevo.2017.00055 (2017).

Article  Google Scholar 

Baldan, D. & Griggio, M. Pair coordination is related to later brood desertion in a provisioning songbird. Anim. Behav. 156, 147–152. https://doi.org/10.1016/j.anbehav.2019.08.002 (2019).

Article  Google Scholar 

Pinheiro J, Bates D, DebRoy S, Sarkar D & Team, R. C. nlme: Linear and nonlinear mixed effects models. (2019).

Rolinski, S., Horn, H., Petzoldt, T. & Paul, L. Identifying cardinal dates in phytoplankton time series to enable the analysis of long-term trends. Oecologia 153, 997–1008 (2007).

ADS  Article  Google Scholar 

Douma, J. C. & Weedon, J. T. Analysing continuous proportions in ecology and evolution: A practical introduction to beta and Dirichlet regression. Methods Ecol. Evol. 10, 1412–1430. https://doi.org/10.1111/2041-210x.13234 (2019).

Article  Google Scholar 

Martin, E. mclogit: Multinomial logit models, with or without random effects or overdispersion (2020).

Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 48 (2015).

Article  Google Scholar 

Cohen, J. Statistical Power Analysis for the Behavioral Sciences (Lawrence Erlbaum Associates, Hillsdale, 1988).

Google Scholar 

Lakens, D. Calculating and reporting effect sizes to facilitate cumulative science: A practical primer for t-tests and ANOVAs. Front. Psychol. https://doi.org/10.3389/fpsyg.2013.00863 (2013).

Article  PubMed  PubMed Central  Google Scholar 

Lenth, R. emmeans: Estimated marginal means, aka least-squares means. (2020).