in

Short-term behavioural impact contrasts with long-term fitness consequences of biologging in a long-lived seabird

  • 1.

    Dean, B. et al. Behavioural mapping of a pelagic seabird: combining multiple sensors and a hidden Markov model reveals the distribution of at-sea behaviour. J. R. Soc. 10, 20120570–20120570 (2013).

    Article  Google Scholar 

  • 2.

    Daniel Kissling, W., Pattemore, D. E. & Hagen, M. Challenges and prospects in the telemetry of insects. Biol. Rev. https://doi.org/10.1111/brv.12065 (2014).

    PubMed  Article  Google Scholar 

  • 3.

    Williams, H. J. et al. Optimizing the use of biologgers for movement ecology research. J. Anim. Ecol. https://doi.org/10.1111/1365-2656.13094 (2019).

    PubMed  Article  Google Scholar 

  • 4.

    Bowlin, M. S., Cochran, W. W. & Wikelski, M. C. Biotelemetry of New World thrushes during migration: Physiology, energetics and orientation in the wild. Integr. Comp. Biol. 45, 295–304 (2005).

    PubMed  Article  Google Scholar 

  • 5.

    Shoji, A. et al. Foraging behaviour of sympatric razorbills and puffins. Mar. Ecol. Prog. Ser. 520, 257–267 (2015).

    ADS  Article  Google Scholar 

  • 6.

    Guilford, T. et al. Migration and stopover in a small pelagic seabird, the Manx shearwater Puffinus puffinus: Insights from machine learning. Proc. Biol. Sci. 276, 1215–1223 (2009).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 7.

    Handcock, R. N. et al. Monitoring animal behaviour and environmental interactions using wireless sensor networks, GPS collars and satellite remote sensing. Sensors 9, 3586–3603 (2009).

    PubMed  Article  Google Scholar 

  • 8.

    Padget, O. et al. In situ clock shift reveals that the sun compass contributes to orientation in a pelagic seabird. Curr. Biol. 28, 275-279.e2 (2018).

    CAS  PubMed  Article  Google Scholar 

  • 9.

    Votier, S. C., Bicknell, A., Cox, S. L., Scales, K. L. & Patrick, S. C. A bird’s eye view of discard reforms: Bird-borne cameras reveal seabird/fishery interactions. PLoS ONE 8, e57376 (2013).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 10.

    Barron, D. G., Brawn, J. D. & Weatherhead, P. J. Meta-analysis of transmitter effects on avian behaviour and ecology. Methods Ecol. Evol. 1, 180–187 (2010).

    Article  Google Scholar 

  • 11.

    Bodey, T. W. et al. A phylogenetically controlled meta-analysis of biologging device effects on birds: Deleterious effects and a call for more standardized reporting of study data. Methods Ecol. Evol. 9, 946–955 (2018).

    Article  Google Scholar 

  • 12.

    Aldridge, H. D. J. N. & Brigham, R. M. Load carrying and maneuverability in an insectivorous bat: A test of the 5% ‘rule’ of radio-telemetry. J. Mammal. https://doi.org/10.2307/1381393 (1988).

    Article  Google Scholar 

  • 13.

    Hammerschlag, N., Gallagher, A. J. & Lazarre, D. M. A review of shark satellite tagging studies. J. Exp. Mar. Biol. Ecol. https://doi.org/10.1016/j.jembe.2010.12.012 (2011).

    Article  Google Scholar 

  • 14.

    Irvine, A. B., Wells, R. S. & Scott, M. D. An evaluation of techniques for tagging small odontocete cetaceans. Fish. Bull. (1982).

  • 15.

    van der Hoop, J. M. et al. Bottlenose dolphins modify behavior to reduce metabolic effect of tag attachment. J. Exp. Biol. 217, 4229–4236 (2014).

    PubMed  Article  Google Scholar 

  • 16.

    Putaala, A., Oksa, J., Rintamaki, H. & Hissa, R. Effects of hand-rearing and radiotransmitters on flight of gray partridge. J. Wildl. Manage. https://doi.org/10.2307/3802136 (1997).

    Article  Google Scholar 

  • 17.

    Jepsen, N., Thorstad, E. B., Havn, T. & Lucas, M. C. The use of external electronic tags on fish: An evaluation of tag retention and tagging effects. Anim. Biotelemetry https://doi.org/10.1186/s40317-015-0086-z (2015).

    Article  Google Scholar 

  • 18.

    Vandenabeele, S. P. et al. Are bio-telemetric devices a drag? Effects of external tags on the diving behaviour of great cormorants. Mar. Ecol. Prog. Ser. 519, 239–249 (2015).

    ADS  Article  Google Scholar 

  • 19.

    Puehringer-Sturmayr, V. et al. Effects of bio-loggers on behaviour and corticosterone metabolites of Northern Bald Ibises (Geronticus eremita) in the field and in captivity. Anim. Biotelemetry https://doi.org/10.1186/s40317-019-0191-5 (2020).

    Article  Google Scholar 

  • 20.

    Booms, T. L., Schempf, P. F. & Fuller, M. R. Preening behavior of adult gyrfalcons tagged with backpack transmitters. J. Raptor Res. https://doi.org/10.3356/jrr-10-115.1 (2011).

    Article  Google Scholar 

  • 21.

    Wilson, R. P. & Wilson, M. T. A peck activity record for birds fitted with devices. J. F. Ornithol. (1989).

  • 22.

    Robert, M., Drolet, B. & Savard, J.-P.L. Effects of backpack radio-transmitters on female Barrow’s goldeneyes. Waterbirds https://doi.org/10.1675/1524-4695(2006)29[115:eobrof]2.0.co;2 (2006).

    Article  Google Scholar 

  • 23.

    Pouliquen, O., Leishman, M. & Redhead, T. D. Effects of radio collars on wild mice, Mus domesticus. Can. J. Zool. https://doi.org/10.1139/z90-239 (1990).

    Article  Google Scholar 

  • 24.

    Wilson, C. D., Arnott, G., Reid, N. & Roberts, D. The pitfall with PIT tags: Marking freshwater bivalves for translocation induces short-term behavioural costs. Anim. Behav. https://doi.org/10.1016/j.anbehav.2010.10.003 (2011).

    Article  Google Scholar 

  • 25.

    Kooyman, G. L. et al. Heart rates and swim speeds of emperor penguins diving under sea ice. J. Exp. Biol. 165, 161–180 (1992).

    CAS  PubMed  Google Scholar 

  • 26.

    Harris, M. P., Bogdanova, M. I., Daunt, F. & Wanless, S. Using GPS technology to assess feeding areas of Atlantic Puffins Fratercula arctica. Ringing Migr. https://doi.org/10.1080/03078698.2012.691247 (2012).

    Article  Google Scholar 

  • 27.

    Wanless, S., Harris, M. P. & Morris, J. A. Behavior of alcids with tail-mounted radio transmitters. Colon. Waterbirds 158–163, https://doi.org/10.2307/1521336 (1989).

  • 28.

    Arlt, D., Low, M. & Pärt, T. Effect of geolocators on migration and subsequent breeding performance of a long-distance passerine migrant. PLoS ONE https://doi.org/10.1371/journal.pone.0082316 (2013).

    PubMed  PubMed Central  Article  Google Scholar 

  • 29.

    Rodríguez, A., Negro, J. J., Fox, J. W. & Afanasyev, V. Effects of geolocator attachments on breeding parameters of Lesser Kestrels. J. F. Ornithol. https://doi.org/10.1111/j.1557-9263.2009.00247.x (2009).

    Article  Google Scholar 

  • 30.

    Scandolara, C. et al. Impact of miniaturized geolocators on barn swallow Hirundo rustica fitness traits. J. Avian Biol. https://doi.org/10.1111/jav.00412 (2014).

    Article  Google Scholar 

  • 31.

    Whidden, S. E., Williams, C. T., Breton, A. R. & Buck, C. L. Effects of transmitters on the reproductive success of Tufted Puffins. J. F. Ornithol. 78, 206–212 (2007).

    Article  Google Scholar 

  • 32.

    Griffioen, M., Iserbyt, A. & Muller, W. Handicapping males does not affect their rate of parental provisioning, but impinges on their partners’ turn taking behavior. Front. Ecol. Evol. 7, 1–7 (2019).

    Article  Google Scholar 

  • 33.

    Ratz, T., Nichol, T. W. & Smiseth, P. T. Parental responses to increasing levels of handicapping in a burying beetle. Behav. Ecol. https://doi.org/10.1093/beheco/arz157 (2019).

    Article  Google Scholar 

  • 34.

    Wiebe, K. L. Negotiation of parental care when the stakes are high: Experimental handicapping of one partner during incubation leads to short-term generosity. J. Anim. Ecol. 79, 63–70 (2010).

    PubMed  Article  Google Scholar 

  • 35.

    Cantarero, A., López-Arrabé, J., Palma, A., Redondo, A. J. & Moreno, J. Males respond to female begging signals of need: A handicapping experiment in the pied flycatcher, Ficedula hypoleuca. Anim. Behav. https://doi.org/10.1016/j.anbehav.2014.05.002 (2014).

    Article  Google Scholar 

  • 36.

    Saraux, C. et al. Reliability of flipper-banded penguins as indicators of climate change. Nature 469, 203–208 (2011).

    ADS  CAS  PubMed  Article  Google Scholar 

  • 37.

    Beaulieu, M. et al. Can a handicapped parent rely on its partner? An experimental study within Adélie penguin pairs. Anim. Behav. 78, 313–320 (2009).

    Article  Google Scholar 

  • 38.

    Paredes, R., Jones, I. L. & Boness, D. J. Reduced parental care, compensatory behaviour and reproductive costs of thick-billed murres equipped with data loggers. Anim. Behav. 69, 197–208 (2005).

    Article  Google Scholar 

  • 39.

    Dean, B. et al. Simultaneous multi-colony tracking of a pelagic seabird reveals cross-colony utilization of a shared foraging area. Mar. Ecol. Prog. Ser. 538, 239–248 (2015).

    ADS  CAS  Article  Google Scholar 

  • 40.

    Guilford, T. C. et al. GPS tracking of the foraging movements of Manx Shearwaters Puffinus puffinus breeding on Skomer Island, Wales. Ibis (Lond. 1859). 150, 462–473 (2008).

  • 41.

    Shoji, A. et al. Dual foraging and pair-coordination during chick provisioning by Manx shearwaters: empirical evidence supported by a simple model. J. Exp. Biol. 218, 2116–2123 (2015).

    PubMed  PubMed Central  Article  Google Scholar 

  • 42.

    Adams, J. et al. Effects of geolocation archival tags on reproduction and adult body mass of sooty shearwaters (Puffinus griseus). N. Z. J. Zool. 36, 355–366 (2009).

    Article  Google Scholar 

  • 43.

    Phillips, R. A., Xavier, J. C., Croxall, J. P., Xavier, J. C. & Croxall, J. P. Effects of satellite transmitters on albatrosses and petrels. Auk 120, 1082–1090 (2003).

    Article  Google Scholar 

  • 44.

    Pennycuick, C. J., Fast, P. L. F., Ballerstädt, N. & Rattenborg, N. The effect of an external transmitter on the drag coefficient of a bird’s body, and hence on migration range, and energy reserves after migration. J. Ornithol. 153, 633–644 (2012).

    Article  Google Scholar 

  • 45.

    Hazekamp, A. A. H., Mayer, R. & Osinga, N. Flow simulation along a seal: The impact of an external device. Eur. J. Wildl. Res. 56, 131–140 (2010).

    Article  Google Scholar 

  • 46.

    Wilson, R. P. Antennae on transmitters on penguins: balancing energy budgets on the high wire. J. Exp. Biol. 207, 2649–2662 (2004).

    PubMed  Article  Google Scholar 

  • 47.

    Watson, K. P. & Granger, R. A. Hydrodynamic effect of a satellite transmitter on a juvenile green turtle (Chelonia mydas). J. Exp. Biol. 201, 2497–2505 (1998).

    PubMed  Google Scholar 

  • 48.

    Hull, C. L. The effect of carrying devices on breeding royal penguins. Condor 99, 530–534 (1997).

    Article  Google Scholar 

  • 49.

    Elliott, K. H. et al. Age-related variation in energy expenditure in a long-lived bird within the envelope of an energy ceiling. J. Anim. Ecol. 83, 136–146 (2014).

    PubMed  Article  Google Scholar 

  • 50.

    Kelly, K. G., Diamond, A. W., Holberton, R. L. & Bowser, A. K. Researcher handling of incubating Atlantic puffins Fratercula arctica has no effect on reproductive success. Mar. Ornithol. (2015).

  • 51.

    Müller, M. S., Vyssotski, A. L., Yamamoto, M. & Yoda, K. Individual differences in heart rate reveal a broad range of autonomic phenotypes in a free-living seabird population. J. Exp. Biol. https://doi.org/10.1242/jeb.182758 (2018).

    PubMed  Article  Google Scholar 

  • 52.

    Weimerskirch, H. et al. Heart rate and energy expenditure of incubating wandering albatrosses: Basal levels, natural variation, and the effects of human disturbance. J. Exp. Biol. (2002).

  • 53.

    Fayet, A. L. et al. Lower foraging efficiency in immatures drives spatial segregation with breeding adults in a long-lived pelagic seabird. Anim. Behav. 110, 79–89 (2015).

    Article  Google Scholar 

  • 54.

    Kosztolányi, A., Cuthill, I. C. & Székely, T. Negotiation between parents over care: Reversible compensation during incubation. Behav. Ecol. 20, 446–452 (2009).

    Article  Google Scholar 

  • 55.

    Suzuki, S. & Nagano, M. To compensate or not? Caring parents respond differentially to mate removal and mate handicapping in the burying beetle, Nicrophorus quadripunctatus. Ethology https://doi.org/10.1111/j.1439-0310.2008.01598.x (2009).

    Article  Google Scholar 

  • 56.

    Wright, J. & Cuthill, I. Biparental care: Short-term manipulation of partner contribution and brood size in the starling, Sturnus vulgaris. Behav. Ecol. 1, 116–124 (1990).

    Article  Google Scholar 

  • 57.

    Bijleveld, A. I. & Mullers, R. H. E. E. Reproductive effort in biparental care: An experimental study in long-lived Cape gannets. Behav. Ecol. 20, 736–744 (2009).

    Article  Google Scholar 

  • 58.

    Dearborn, D. C. Body condition and retaliation in the parental effort decisions of incubating great frigatebirds (Fregata minor). Behav. Ecol. 12, 200–206 (2001).

    Article  Google Scholar 

  • 59.

    Navarro, J. & González-Solís, J. Experimental increase of flying costs in a pelagic seabird: Effects on foraging strategies, nutritional state and chick condition. Oecologia 151, 150–160 (2007).

    ADS  PubMed  Article  Google Scholar 

  • 60.

    Brooke, M. The Manx Shearwater. (A & C Black Publishers Ltd, 1990).

  • 61.

    Heggøy, O., Christensen-Dalsgaard, S., Ranke, P. S., Chastel, O. & Bech, C. GPS-loggers influence behaviour and physiology in the black-legged kittiwake Rissa tridactyla. Mar. Ecol. Prog. Ser. https://doi.org/10.3354/meps11140 (2015).

    Article  Google Scholar 

  • 62.

    Fayet, A. L. et al. Carry-over effects on the annual cycle of a migratory seabird: An experimental study. J. Anim. Ecol. https://doi.org/10.1111/1365-2656.12580 (2016).

    PubMed  PubMed Central  Article  Google Scholar 

  • 63.

    Shoji, A. et al. Breeding phenology and winter activity predict subsequent breeding success in a trans-global migratory seabird. Biol. Lett. 11, 20150671 (2015).

    PubMed  PubMed Central  Article  Google Scholar 

  • 64.

    Boersma, P. & Davies, E. Sexing monomorphic birds by vent measurements. Auk 104, 779–783 (1987).

    Article  Google Scholar 

  • 65.

    Guilford, T. et al. Geolocators reveal migration and pre-breeding behaviour of the critically endangered balearic shearwater Puffinus mauretanicus. PLoS ONE 7, e33753 (2012).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 66.

    Benaglia, T., Chauveau, D., Hunter, D. R. & Young, D. S. Mixtools: An R package for analyzing finite mixture models. J. Stat. Softw. https://doi.org/10.18637/jss.v032.i06 (2009).

    Article  Google Scholar 

  • 67.

    Fayet, A. L. et al. Drivers and fitness consequences of dispersive migration in a pelagic seabird. Behav. Ecol. https://doi.org/10.1093/beheco/arw013 (2016).

    PubMed  PubMed Central  Article  Google Scholar 

  • 68.

    Core Team, R. R: A Language and Environment for Statistical Computing. (R Found. Stat. Comput., Vienna, 2018).

  • 69.

    Bates, D., Mächler, M., Bolker, B. M. & Walker, S. C. Fitting linear mixed-effects models using lme4. J. Stat. Softw. https://doi.org/10.18637/jss.v067.i01 (2015).

    Article  Google Scholar 

  • 70.

    Lenth, R., Singmann, H., Love, J., Buerkner, P. & Herve, M. Package ‘emmeans’. Mran.Microsoft.Com https://doi.org/10.1080/00031305.1980.10483031%3e.License (2018).

    Article  Google Scholar 


  • Source: Ecology - nature.com

    Gene expression during bacterivorous growth of a widespread marine heterotrophic flagellate

    Local management and landscape structure determine the assemblage patterns of spiders in vegetable fields