Nest-type associated microclimatic conditions as potential drivers of ectoparasite infestations in African penguin nests.
African penguin
Fleas
Nest characteristics
Soil moisture
Soil temperature
Ticks
Journal
Parasitology research
ISSN: 1432-1955
Titre abrégé: Parasitol Res
Pays: Germany
ID NLM: 8703571
Informations de publication
Date de publication:
Nov 2020
Nov 2020
Historique:
received:
01
06
2020
accepted:
17
09
2020
pubmed:
1
10
2020
medline:
20
11
2020
entrez:
30
9
2020
Statut:
ppublish
Résumé
Nest design and characteristics can influence the microclimatic conditions in the nest. Nest-dwelling ectoparasites are sensitive to temperature and moisture and as such the conditions in the nest can influence parasite infestations. The endangered African penguin (Spheniscus demersus) breeds in different nest types and as yet little is known with regard to the microclimate and parasite infestation within these nests. This study characterized the microclimatic conditions in natural open, natural covered (with vegetation) and artificial nests, and assessed the relationship between nest characteristics (type, age, distance from the coast, orientation and entrance opening) and in-nest ectoparasite infestations and the health of African penguins in Stony Point, South Africa. Penguins (50 adults and 192 chicks) and their nests (n = 308) were sampled in 2016 and 2017. Soil temperature was higher in artificial than in natural nests, and soil and nest material moisture was lower in artificial and natural covered nests than natural open. Ectoparasite infestations were higher under warmer and drier conditions, in artificial nests and nests near the coastline. Penguin (adult and chick) body mass and chick body condition were lower in warmer nests and total plasma protein (in adults and checks) was lower in drier nests. Given the potential adverse effects of ectoparasites on host species, it is recommended that conservation agencies implement a monitoring programme to assess the ectoparasite infestation in artificial nests across multiple colonies. This information will facilitate a more holistic penguin conservation management plan that may prevent further detrimental effects on this endangered penguin species.
Identifiants
pubmed: 32996052
doi: 10.1007/s00436-020-06895-x
pii: 10.1007/s00436-020-06895-x
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
3603-3616Références
Abdallah F, Chaieb M (2012) The influence of trees on nutrients, water, light availability and understorey vegetation in an arid environment. Appl Veg Sci 15:501–512. https://doi.org/10.1111/j.1654-109X.2012.01201.x
doi: 10.1111/j.1654-109X.2012.01201.x
Ancel A, Beaulieu M, Gilbert C (2013) The different breeding strategies of penguins: a review. C R Biol 336:1–12. https://doi.org/10.1016/j.crvi.2013.02.002
doi: 10.1016/j.crvi.2013.02.002
pubmed: 23537764
Angilletta MJ Jr, Sears MW, Pringle RM (2009) Spatial dynamics of nesting behavior: lizards shift microhabitats to construct nests with beneficial thermal properties. Ecology 90:2933–2939. https://doi.org/10.1890/08-2224.1
doi: 10.1890/08-2224.1
pubmed: 19886501
Barnosky AD, Matzke N, Tomiya S, Wogan GO, Swartz B, Quental TB, Marshall C, McGuire JL, Lindsey EL, Maguire KC, Mersey B (2011) Has the Earth’s sixth mass extinction already arrived? Nature 471:51–57. https://doi.org/10.1038/nature09678
doi: 10.1038/nature09678
pubmed: 21368823
BirdLife International (2018) Spheniscus demersus The IUCN Red List of Threatened Species 2018. https://doi.org/10.2305/IUCN.UK.2018-2.RLTS.T22697810A132604504.en . Accessed 5 July 2019
Bitam I, Dittmar K, Parola P, Whiting MF, Raoult D (2010) Fleas and flea-borne diseases. Int J Infect Dis 14:e667–e676. https://doi.org/10.1016/j.ijid.2009.11.011
doi: 10.1016/j.ijid.2009.11.011
pubmed: 20189862
Bolton M, Medeiros R, Hothersall B, Campos A (2004) The use of artificial breeding chambers as a conservation measure for cavity-nesting procellariiform seabirds: a case study of the Madeiran storm petrel (Oceanodroma castro). Biol Conserv 116:73–80. https://doi.org/10.1016/S0006-3207(03)00178-2
doi: 10.1016/S0006-3207(03)00178-2
Bourgeois K, Dromzée S, Vidal E (2015) Are artificial burrows efficient conservation tools for seabirds? A case study of two sympatric shearwaters on neighbouring islands and guidelines for improvement. Biol Conserv 191:282–290. https://doi.org/10.1016/j.biocon.2015.07.002
doi: 10.1016/j.biocon.2015.07.002
Broughton RK (2020) Current and future impacts of nest predation and nest-site competition by invasive eastern grey squirrels Sciurus carolinensis on European birds. Mamm Rev 50:38–51
doi: 10.1111/mam.12174
Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583. https://doi.org/10.2307/3284227
doi: 10.2307/3284227
pubmed: 9267395
Campbell TW, Ellis CK (2007) Hematology of birds. In: Campbell TW, Ellis CK (eds) Avian and exotic animal hematology and citology. Backwell, Ames, Iowa, pp 3–50
Catry I, Franco AM, Sutherland WJ (2011) Adapting conservation efforts to face climate change: modifying nest-site provisioning for lesser kestrels. Biol Conserv 144:1111–1119. https://doi.org/10.1016/j.biocon.2010.12.030
doi: 10.1016/j.biocon.2010.12.030
Cooper J (1980) Breeding biology of the jackass penguin with special reference to its conservation. Proc IV Pan-Afr Orn Congr 227–231
Crawford RJM, Boonstra HGV, Dyer BM, Upfold L (1995) Recolonization of Robben Island by African penguins, 1983-1992. In: Dann P, Norman I, Reilly P (eds) The penguins: ecology and management. Surrey Beatty & Sons, Chipping Norton, Australia, pp 333–363
Daturi A (1986) A preliminary study of tick populations in jackass penguin nests on Marcus Island, South Africa. Ostrich 57:95–100. https://doi.org/10.1080/00306525.1986.9634131
doi: 10.1080/00306525.1986.9634131
Deeming DC, Mainwaring MC (2015) Functional properties of nests. In: Deeming DC, Reynolds SJ (eds) Nests, eggs, and incubation: new ideas about avian reproduction. Oxford University Press, Oxford, pp 29–49
doi: 10.1093/acprof:oso/9780198718666.003.0004
Diehl PA, Aeschlimann A, Obenchain FD (1982) Tick reproduction: oogenesis and oviposition. In: Obenchain FD, Galun R (eds) Physiology of ticks. Pergamon Press, Exeter, pp 277–350
doi: 10.1016/B978-0-08-024937-7.50014-7
Du Feu C (2005) Nestboxes. Extracts from BTO field guide number 23. British Trust for Ornithology Guide, Norfolk
Duffy DC (1983) The ecology of tick parasitism on densely nesting Peruvian seabirds. Ecology 64:110–119. https://doi.org/10.2307/1937334
doi: 10.2307/1937334
Dufva R, Allander K (1996) Variable effects of the hen flea Ceratophyllus gallinae on the breeding success of the great tit Parus major in relation to weather conditions. Ibis 138:772–777. https://doi.org/10.1111/j.1474-919X.1996.tb08835.x
doi: 10.1111/j.1474-919X.1996.tb08835.x
Eeva T, Lehikoinen E, Nurmi J (1994) Effects of ectoparasites on breeding success of great tits (Parus major) and pied flycatchers (Ficedula hypoleuca) in an air pollution gradient. Can J Zool 72:624–635. https://doi.org/10.1139/z94-085
doi: 10.1139/z94-085
Espinaze MPA, Hui C, Waller L, Matthee S (2019a) The efficacy of a modified Berlese funnel method for the extraction of ectoparasites and their life stages from the nests of the African penguin Spheniscus demersus. Ostrich 90:271–277. https://doi.org/10.2989/00306525.2019.1616230
doi: 10.2989/00306525.2019.1616230
Espinaze MPA, Hui C, Waller L, Dreyer F, Matthee S (2019b) Parasite diversity associated with African penguins (Spheniscus demersus) and the effect of host and environmental factors. Parasitology 146:791–804. https://doi.org/10.1017/S0031182018002159
doi: 10.1017/S0031182018002159
pubmed: 30724152
Frost PGH, Siegfried WR, Burger AE (1976) Behavioural adaptations of the jackass penguin, Spheniscus demersus to a hot, arid environment. J Zool 179:165–187. https://doi.org/10.1111/j.1469-7998.1976.tb02289.x
doi: 10.1111/j.1469-7998.1976.tb02289.x
Gardner WH (1965) Water content. In: Black CA, Evans DD, Ensminger LE, White JL, Clark FE (eds) Methods of soil analysis. Academic Press, Madison, WI, pp 82–127
George RS (1959) Fleas from nests of the pied flycatcher and other species in the forest of Dean. Bird Study 6:132–136. https://doi.org/10.1080/00063655909475944
doi: 10.1080/00063655909475944
Gray JS, Estrada-Peña A, Vial L (2013) Ecology of nidicolous ticks. In: Sonenshine DE, Roe RM (eds) The biology of ticks, 2nd edn. Oxford University Press, New York, pp 39–60
Hansell M (2000) Bird nests and construction behaviour. Cambridge University Press, Cambridge. https://doi.org/10.1017/CBO9781139106788
doi: 10.1017/CBO9781139106788
Hansell M (2005) Animal architecture. Oxford University Press, Oxford
doi: 10.1093/acprof:oso/9780198507529.001.0001
Hebda G, Wesołowski T (2012) Low flea loads in bird’s nests in tree cavities. Ornis Fenn 89:139–144
Heeb P, Kölliker M, Richner H (2000) Bird–ectoparasite interactions, nest humidity, and ectoparasite community structure. Ecology 81:958–968. https://doi.org/10.1890/0012-9658(2000)081[0958:BEINHA]2.0.CO;2
doi: 10.1890/0012-9658(2000)081[0958:BEINHA]2.0.CO;2
Heenan CB (2013) An overview of the factors influencing the morphology and thermal properties of avian nests. Avian Biol Res 6:104–118. https://doi.org/10.3184/003685013X13614670646299
doi: 10.3184/003685013X13614670646299
Heylen D, Müller W, Vermeulen A, Sprong H, Matthysen E (2015) Virulence of recurrent infestations with Borrelia-infected ticks in a Borrelia-amplifying bird. Sci Rep 5:16150. https://doi.org/10.1038/srep16150
doi: 10.1038/srep16150
pubmed: 26553505
pmcid: 4639849
Huang WS, Pike DA (2011) Climate change impacts on fitness depend on nesting habitat in lizards. Funct Ecol 25:1125–1136. https://doi.org/10.1111/j.1365-2435.2011.01855.x
doi: 10.1111/j.1365-2435.2011.01855.x
Humphries DA (1968) The host-finding behaviour of the hen flea, Ceratophyllus gallinae (Schrank) (Siphonaptera). Parasitology 58:403–414. https://doi.org/10.1017/S0031182000069432
doi: 10.1017/S0031182000069432
International Standards Organisation (1993) Soil quality–determination of dry matter and water content on a mass basis–gravimetric method. ISO 11465. International Organization for Standardization, Geneva
Iqbal QJ, Humphries DA (1970) Temperature as a critical factor in the mating behavior of the rat flea, Nosopsyllus fasciatus (Bosc.). Parasitology 61:375–380
doi: 10.1017/S0031182000041214
Jackman S (2017) Pscl: classes and methods for R developed in the political science computational laboratory. R package version 1.5.2. United States Studies Centre, University of Sydney, Sydney
Jordan K (1942) On Parapsyllus and some closely related genera of Siphonaptera. Eos 18:7–29
Kelsey EC, Bradley RW, Warzybok P, Jahncke J, Shaffer SA (2016) Environmental temperatures, artificial nests, and incubation of Cassin's auklet. J Wildl Manag 80:292–299. https://doi.org/10.1002/jwmg.1012
doi: 10.1002/jwmg.1012
Kemper J, Underhill LG, Roux JP (2007) Artificial burrows for African penguins on Halifax Island, Namibia: do they improve breeding success? In: Kirkman SP (ed) Final report of the BCLME (Benguela current large marine ecosystem). Project on Top Predators as Biological Indicators of Ecosystem Change in the BCLME. Avian Demography Unit, Cape Town, pp 101–106
Kohls GM, Sonenshine DE, Clifford CM (1965) The systematics of the subfamily Ornithodorinae (Acarina: Argasidae). II identification of the larvae of the Western Hemisphere and descriptions of three new species. Ann Entomol Soc Am 58:331–364. https://doi.org/10.1093/aesa/58.3.331
doi: 10.1093/aesa/58.3.331
pubmed: 5835857
Krasnov BR (2008) Ecology of haematophagy. In: Krasnov BR (ed) Functional and evolutionary ecology of fleas: a model for ecological parasitology. Cambridge University Press, Cambridge, pp 154–181
doi: 10.1017/CBO9780511542688.011
Lambrechts MM, Adriaensen F, Ardia DR, Artemyev AV, Atiénzar F, Bańbura J, Barba E, Bouvier JC, camprodon J, Cooper CB, Dawson RD, Eens M, Eeva T, Faivre B, Garamszegi LZ, Goodenough AE, Gosler AG, Grégoire A, Griffith SC, Gustafsson L, Johnson LS, Kania W, Keišs O, Llambias PE, Mainwaring MC, Mänd R, Massa B, Mazgajski TD, Møller AP, Moreno J, Naef-Daenzer B, Nilsson JÅ, Norte AC, Orell M, Otter KA, Park CR, Perrins CM, Pinowski J, Porkert J, Potti J, Remes V, Richner H, Rytkönen S, Shiao MT, Silverin B, Slagsvold T, Smith HG, Sorace A, Stenning MJ, Stewart I, Thompson CF, Tryjanowski P, Török J, Noordwijk AJ, Winkler DW, Ziane N (2010) The design of artificial nestboxes for the study of secondary hole-nesting birds: a review of methodological inconsistencies and potential biases. Acta Ornithol 45:1–26. https://doi.org/10.3161/000164510X516047
doi: 10.3161/000164510X516047
Lees AD (1947) Transpiration and structure of the epicuticle in ticks. J Exp Biol 23:379–410
pubmed: 20292371
Lehmann T (1993) Ectoparasites: direct impact on host fitness. Parasitol Today 9:8–13. https://doi.org/10.1016/0169-4758(93)90153-7
doi: 10.1016/0169-4758(93)90153-7
pubmed: 15463655
Lei BR, Green JA, Pichegru L (2014) Extreme microclimate conditions in artificial nests for endangered African penguins. Bird Conserv Int 24:201–213. https://doi.org/10.1017/S0959270913000671
doi: 10.1017/S0959270913000671
López-Rull I, Macías Garcia C (2015) Control of invertebrate occupants of nests. In: Deeming DC, Reynolds SJ (eds) Nests, eggs, and incubation: new ideas about avian reproduction. Oxford University Press, Oxford, pp 82–96
doi: 10.1093/acprof:oso/9780198718666.003.0008
Loye JE, Carroll SP (1998) Ectoparasite behavior and its effects on avian nest site selection. Amm Entomol Soc Am 91:159–163. https://doi.org/10.1093/aesa/91.2.159
doi: 10.1093/aesa/91.2.159
Lubbe A, Underhill LG, Waller LJ, Veen J (2014) A condition index for African penguin Spheniscus demersus chicks. Afr J Mar Sci 36:143–154. https://doi.org/10.2989/1814232X.2014.915232
doi: 10.2989/1814232X.2014.915232
Mainwaring MC, Hartley IR, Lambrechts MM, Deeming DC (2014) The design and function of birds’ nests. Ecol Evol 4:3909–3928. https://doi.org/10.1002/ece3.1054
doi: 10.1002/ece3.1054
pubmed: 25505520
pmcid: 4242575
Marshall AG (1981) The ecology of ectoparasitic insects. Academic Press, London
Martin TE, Boyce AJ, Fierro-Calderón K, Mitchell AE, Armstad CE, Mouton JC, Bin Soudi EE (2017) Enclosed nests may provide greater thermal than nest predation benefits compared with open nests across latitudes. Funct Ecol 31:1231–1240. https://doi.org/10.1111/1365-2435.12819
doi: 10.1111/1365-2435.12819
Mazgajski TD (2007) Effect of old nest material in nestboxes on ectoparasite abundance and reproductive output in the European Starling Sturnus vulgaris (L.). Pol J Ecol 55:377–385
Maziarz M, Broughton RK, Wesołowski T (2017) Microclimate in tree cavities and nest-boxes: implications for hole-nesting birds. For Ecol Manag 389:306–313. https://doi.org/10.1016/j.foreco.2017.01.001
doi: 10.1016/j.foreco.2017.01.001
Michielsen RJ, Ausems AN, Jakubas D, Pętlicki M, Plenzler J, Shamoun-Baranes J, Wojczulanis-Jakubas K (2019) Nest characteristics determine nest microclimate and affect breeding output in an Antarctic seabird, the Wilson’s storm-petrel. PLoS One 14:e0217708. https://doi.org/10.1371/journal.pone.0217708
doi: 10.1371/journal.pone.0217708
pubmed: 31194763
pmcid: 6564424
Monahan EC (1968) Sea spray as a function of low elevation wind speed. J Geophys Res 73:1127–1137. https://doi.org/10.1029/JB073i004p01127
doi: 10.1029/JB073i004p01127
Moon KL, Dann P, Chown SL, McGaughran A, Fraser CI (2018) Penguin ectoparasite panmixia suggests extensive host movement within a colony. Auk 135:657–668. https://doi.org/10.1642/AUK-17-226.1
doi: 10.1642/AUK-17-226.1
Morbey YE (1996) The abundance and effects of ticks (Ixodes uriae) on nestling Cassin’s auklets (Ptychoramphus aleuticus) at Triangle Island, British Columbia. Can J Zool 74:1585–1589. https://doi.org/10.1139/z96-172
doi: 10.1139/z96-172
Murray MD, Vestjens WJM (1967) Studies on the ectoparasites of seals and penguins. III. The distribution of the tick Ixodes uriae White and the flea Parapsyllus magellanicus heardi de Meillon on Macquarie Island. Aust J Zool 15:715–725. https://doi.org/10.1071/ZO9670715
doi: 10.1071/ZO9670715
Newton I (1994) The role of nest sites in limiting the numbers of hole-nesting birds: a review. Biol Conserv 70:265–276. https://doi.org/10.1016/0006-3207(94)90172-4
doi: 10.1016/0006-3207(94)90172-4
Norte AC, Lobato DNC, Braga EM, Antonini Y, Lacorte G, Gonçalves M, de Carvalho IL, Gern L, Núncio MS, Ramos JA (2013) Do ticks and Borrelia burgdorferi sl constitute a burden to birds? Parasitol Res 112:1903–1912. https://doi.org/10.1007/s00436-013-3343-1
doi: 10.1007/s00436-013-3343-1
pubmed: 23430359
Ots I, Murumägi A, Horak P (1998) Haematological health state indices of reproducing great tits: methodology and sources of natural variation. Funct Ecol 12:700–707. https://doi.org/10.1046/j.1365-2435.1998.00219.x
doi: 10.1046/j.1365-2435.1998.00219.x
Paleczny M, Hammill E, Karpouzi V, Pauly D (2015) Population trend of the world’s monitored seabirds, 1950-2010. PLoS One 10:e0129342. https://doi.org/10.1371/journal.pone.0129342
doi: 10.1371/journal.pone.0129342
pubmed: 26058068
pmcid: 4461279
Palinauskas V, Valkiūnas G, Bolshakov CV, Bensch S (2008) Plasmodium relictum (lineage P-SGS1): effects on experimentally infected passerine birds. Exp Parasitol 120:372–380. https://doi.org/10.1016/j.exppara.2008.09.001
doi: 10.1016/j.exppara.2008.09.001
pubmed: 18809402
Perriman L, Steen H (2000) Blue penguin (Eudyptula minor) nest distribution and breeding success on Otago Peninsula, 1992 to 1998. N Z J Zool 27:269–275. https://doi.org/10.1080/03014223.2000.9518235
doi: 10.1080/03014223.2000.9518235
Pinkowski BC (1977) Blowfly parasitism of eastern bluebirds in natural and artificial nest sites. J Wildl Manag 41:272–276. https://doi.org/10.2307/3800604
doi: 10.2307/3800604
Podofillini S, Cecere JG, Griggio M, Curcio A, De Capua EL, Fulco E, Pirrello S, Saino N, Serra L, Visceglia M, Rubolini D (2018) Home, dirty home: effect of old nest material on nest-site selection and breeding performance in a cavity-nesting raptor. Curr Zool 64:693–702. https://doi.org/10.1093/cz/zoy012
doi: 10.1093/cz/zoy012
pubmed: 30538728
pmcid: 6280097
R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Rahn H, Krog J, Mehlum F (1983) Microclimate of the nest and egg water loss of the Eider Somateria mollissima and other waterfowl in Spitsbergen. Polar Res 1:171–184. https://doi.org/10.3402/polar.v1i2.6982
doi: 10.3402/polar.v1i2.6982
Randall RM, Randall BM, Cooper J, La Cock GD, Ross GJB (1987) Jackass penguin Spheniscus demersus movements, inter-island visits, and settlement. J Fld Orn 58:445–455
Ropert-Coudert Y, Cannell B, Kato A (2004) Temperature inside nest boxes of little penguins. Wildl Soc Bull 32:177–182. https://doi.org/10.2193/0091-7648(2004)32[177:TINBOL]2.0.CO;2
doi: 10.2193/0091-7648(2004)32[177:TINBOL]2.0.CO;2
Rothschild M, Clay T (1952) Fleas, flukes and cuckoos, 3rd edn. Macmillan, New York
Schoech SJ, Mumme RL, Wingfield JC (1997) Corticosterone, reproductive status, and body mass in a cooperative breeder, the Florida scrub-jay (Aphelocoma coerulescens). Physiol Zool 70:68–73. https://doi.org/10.1086/639545
doi: 10.1086/639545
pubmed: 9231378
Seddon PJ, Van Heezik Y (1991) Effects of hatching order, sibling asymmetries, and nest site on survival analysis of jackass penguin chicks. Auk 108:548–555. https://doi.org/10.2307/4088094
doi: 10.2307/4088094
Sherley RB, Barham BJ, Barham PJ, Leshoro TM, Underhill LG (2012) Artificial nests enhance the breeding productivity of African penguins (Spheniscus demersus) on Robben Island, South Africa. Emu 112:97–106. https://doi.org/10.1071/MU11055
doi: 10.1071/MU11055
Sonenshine DE (1993) Biology of ticks. Oxford University Press, New York
Sumasgutner P, Jenkins A, Amar A, Altwegg R (2020) Nest boxes buffer the effects of climate on breeding performance in an African urban raptor. PLoS One 15:e0234503. https://doi.org/10.1371/journal.pone.0234503
doi: 10.1371/journal.pone.0234503
pubmed: 32579609
pmcid: 7313736
Sutherland DR, Dann P, Jessop RE (2014) Evaluation of artificial nest sites for long-term conservation of a burrow-nesting seabird. J Wildl Manag 78:1415–1424. https://doi.org/10.1002/jwmg.783
doi: 10.1002/jwmg.783
Tomás G, Merino S, Moreno J, Morales J (2007) Consequences of nest reuse for parasite burden and female health and condition in blue tits, Cyanistes caeruleus. Anim Behav 73:805–814. https://doi.org/10.1016/j.anbehav.2006.06.016
doi: 10.1016/j.anbehav.2006.06.016
Travis EK, Vargas FH, Merkel J, Gottdenker N, Miller RE, Parker PG (2006) Hematology, serum chemistry, and serology of Galapagos penguins (Spheniscus mendiculus) in the Galapagos Islands, Ecuador. J Wildl Dis 42:625–632. https://doi.org/10.7589/0090-3558-42.3.625
doi: 10.7589/0090-3558-42.3.625
pubmed: 17092893
Tripet F, Richner H (1999) Dynamics of hen flea Ceratophyllus gallinae subpopulations in blue tit nests. J Insect Behav 12:159–174. https://doi.org/10.1023/A:1020958615191
doi: 10.1023/A:1020958615191
Venables WN, Ripley BD (2002) Modern applied statistics with S, 4th edn. Springer, New York
doi: 10.1007/978-0-387-21706-2
Vial L (2009) Biological and ecological characteristics of soft ticks (Ixodida: Argasidae) and their impact for predicting tick and associated disease distribution. Parasite 16:191–202. https://doi.org/10.1051/parasite/2009163191
doi: 10.1051/parasite/2009163191
pubmed: 19839264
Vleck CM, Vleck D, Rahn H, Paganelli CV (1983) Nest microclimate, water-vapor conductance, and water loss in heron and tern eggs. Auk 100:76–83. https://doi.org/10.1093/auk/100.1.76
doi: 10.1093/auk/100.1.76
Wesołowski T, Stańska M (2001) High ectoparasite loads in hole-nesting birds–a nestbox bias? J Avian Biol 32:281–285. https://doi.org/10.1111/j.0908-8857.2001.320313.x
doi: 10.1111/j.0908-8857.2001.320313.x
Whittington PA, Hofmeyr JH, Cooper J (1996) Establishment, growth and conservation of a mainland colony of jackass penguins Spheniscus demersus at Stony Point, Betty’s bay, South Africa. Ostrich 67:144–150. https://doi.org/10.1080/00306525.1996.9639700
doi: 10.1080/00306525.1996.9639700
Whittington PA, Randall RM, Crawford RJM, Wolfaardt AC, Klages NTW, Randall BM, Bartlett PA, Chesselet YJ, Jones R (2005) Patterns of immigration to and emigration from breeding colonies by African penguins. Afr J Mar Sci 27:205–213. https://doi.org/10.2989/18142320509504079
doi: 10.2989/18142320509504079
Williams DR, Pople RG, Showler DA, Dicks LV, Child MF, Zu Ermgassen EK, Sutherland WJ (2013) Bird conservation: global evidence for the effects of interventions. Pelagic Publishing, Exeter
Yoder JA, Dutton AM (1998) Water requirements of relapsing fever tick larvae, Ornithodoros turicata (Acari: Argasidae), and the relative humidity of hatching eggs. Int J Acarol 24:87–91. https://doi.org/10.1080/01647959808684132
doi: 10.1080/01647959808684132