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Keeping the clock set under the midnight sun Fig. 2. Prevalence (%) of the Snow Bunting faecalsamples containing Isospora plectrophenaxia oocysts at Fig. 1. Diurnal pattern of Isospora plectrophenaxia oocyst different day times on Svalbard under continuous appearance in faecal samples of free-ranging Snow sunlight in the wild in 2-h intervals (± S.E.M.) (bars), Buntings on Svalbard under continuous sunlight. Bars and solar UV radiation (UV300-700 nm) at the study site represent vectors of positive faecal samples with on a clear day in July (line).
length = number of positive samples within 2-h intervals,and direction = time of the day; the line indicates P = 0·303, n = 250). Therefore, it was possible to test direction of resulting mean vector ± circular standard the time pattern of oocyst output by the Rayleigh test.
To control for the effects of repeated sampling of some individuals, as well as year- and nest-effects, All the samples were collected individually and in the second analysis, a general mixed model was stored in separate vials with a 2·5% aqueous solution performed. In the model, the oocyst output (0 = of potassium dichromate K2Cr2O7 at room tempera- oocysts absent; 1 = oocysts present) was the response ture until processed. Each sample was labelled with variable, time of the day (2-h intervals) was a fixed date, time of the day, and age of the bird. For factor, while host individual, date and nest were nestlings, individual colour ring combinations were random factors.
also noted, to allow individual attribution. In thelaboratory, oocysts were separated from faeces byfl otation in saturated NaCl solution for 5 min at 375 g, and the surface layer was removed using a All oocysts belonged to the species Isospora plectro- 5-mm diameter loop, deposited on a slide, and phenaxia. Oocysts were found in faeces of 13 immediately examined under ×100 magnification to individual birds, in 19 of the 250 examined samples.
determine the presence of the oocysts (for details, Positive oocyst samples (n = 19) peaked at 4 p.m.
see Dolnik, for species determination, ×1000 (about 37% of all positive) with a prevalence of magnification with oil immersion was used.
33% ±10·5% S.E.M. (Resulting vector: direction The Atmospheric Observatory of the AWIPEV μ=17:37, length r=0·46, concentration 1·034, circu- Base in Ny-Ålesund kindly provided data on the lar variance 0·54, circular standard deviation 71·4°, daily pattern of UV radiation on a clear July day at Rayleigh Z = 4·02, P = 0·016) (and our study site, with the permission to use them for Time (2-h interval) was the significant factor in a this publication.
general mixed model to explain the variance in oocyst Data were analysed using PASW statistics 18 and output state (F = 2·516, D.F. = 11, P < 0·005). Host Oriana 2.0 for circular statistics. In the first approach, individual, nest or sampling date were not associated all faecal samples were treated as independent with oocyst output.
samples, because due to the life cycle of single On a clear day, the UV radiation reaches its parasite individuals, there is no reason to expect maximum at noon, which in July on Spitsbergen that variation between host individuals would explain can be up to 20 W/m2 for UV300-700 nm UVR, variation in the parasite prevalence in different faecal differing 5 times from that at midnight ).
samples. Each sample was assigned to the next evenhour of the day. For each even hour (12 per 24 hours), mean prevalence (% of positive faecal samples) wascalculated. Samples attributed to the next even hour The presence of diurnal periodicity and synchronism were homogenously distributed among these 2-h of oocyst output in the Arctic summer is especially intervals during the day (chi2 = 12·848, D.F. = 11, interesting, because neither its mechanisms, nor Olga V. Dolnik, Benjamin J. Metzger and Maarten J. J. E. Loonen adaptive reasons are clear. However, based on ambient temperature (Erikstad, ). Whatever is literature data available until now, some possible playing the role of Zeitgeber for Isospora of Snow explanations can be discussed.
Buntings, this factor either does not exist in Except in the Polar Regions, daylight is the main experimental House Sparrows under continuous external time cue (i.e. Zeitgeber) for synchronization light, or for some reason does not play the role of of circadian rhythms in living organisms (Kumar trigger for oocyst output from House Sparrows.
et al. In the wild, a 24-h period of light-dark Therefore, further research is needed to reveal which cycle synchronizes the rhythm of melatonin secretion alternative Zeitgeber is used by Isospora parasites in in pineal organ of the bird, which in turn coordinates the Polar Regions.
the circadian rhythm of bird's activity. These cyclic Possible adaptive reasons of afternoon oocyst changes of melatonin concentrations in the host's output also remain unclear. The discrepancy between blood are used by avian Isospora for oocyst output the results of the present study on the parasites of synchronization (Wild, Brandmeier, High Arctic inhabitants in the wild and those of However, the very slight increase of melatonin birds in captivity (Boughton, Wild, ; around midnight, shown for Lapland Longspurs Brandmeier, suggests the adaptive significance at 68th latitude in Alaska indoors (Hau et al. of synchronizing the circadian rhythms in continuous can be expected to be even lower in free-ranging daylight conditions. The absence of a foraging Snow Buntings at the 78th latitude. Indeed, in the activity pattern of Snow Buntings gives the afternoon experiments on Snow Buntings at Spitsbergen, it was appearance of the oocysts no advantages of being shed confirmed that the slight differences of light intensity at the feeding grounds. The most reasonable expla- between ‘day' and ‘night' is not effective as the nation is adaptation of exogenous stages to changes in Zeitgeber for the birds (Krüll et al. Low or UV-radiation. The sun's irradiance, though being more or less constant melatonin leads to a destruction lowest in the Arctic, still varies significantly through- of the bird's own circadian rhythm under exper- out the day, in clear summer days increasing 5 times imental conditions (Gwinner et al. and in the at noon compared to midnight. Humidity as another wild (Cockerm, Reierth et al. and is not abiotic factor which has been suggested as an adaptive enough to synchronize oocyst output rhythms of reason for afternoon oocyst output of Isospora species Isospora (Brandmeier, in temperate zones (Dolnik, ; Martinaud et al.
Therefore, Isospora parasites of birds in the High can hardly be of significant importance for Arctic must be more sensitive to the slight changes in I. plectrophenaxia on Svalbard, because it remains melatonin concentrations than their congeners from over 70% throughout the day there.
temperate zones, if we assume that they still use it as a An alternative explanation can be that the adaptive Zeitgeber under polar day conditions. Otherwise, if reason is linked to endogenous stages of the parasite's host's melatonin is not available as a Zeitgeber for life cycle. First, it can be that the circadian rhythm of Isospora parasites, the oocyst output can be synchro- I. plectrophenaxia evolved on the winter grounds of nized with an alternative Zeitgeber, namely the host's the host in the temperate zone, and continues at the foraging activity (Wild, Brandmeier, host's breeding grounds. However, in this case the However, this alternative Zeitgeber is also not question with the alternative Zeitgeber remains open.
available for I. plectrophenaxia on Svalbard, as Second, it might be that synchronic re-colonization foraging activity of Snow Buntings seems to be of new cells during merogony has advantages in randomly distributed throughout the 24 h, except the fight against the host's immune system. This is for a 2-h break around midnight (Haarhaus, ; indirectly supported by the data of Grulet et al.
Loonen, personal observations). In the absence of (showing that all stages of the Isospora life this alternative Zeitgeber, Isospora of experimental cycle in the House Sparrow are strictly synchronized.
House Sparrows are not able to synchronize their The third possible advantage of synchronic oocyst rhythms any more, and the oocyst output loses its output might be that it is crucial for the parasite to diurnal periodical pattern (Wild, ; Brandmeier, reach a high concentration of oocysts in a droplet ). On the contrary, although also lacking a of faeces, to enable the infection of the next possibility to use the host's melatonin or foraging host. Indeed, the dose-dependent effect of coccidian activity rhythm to synchronize their circadian rhyth- infection is known for both domestic and wild mic, Isospora parasites of Snow Buntings on Svalbard animals (Long, Dolnik, ). If so, for the nevertheless synchronize their life cycle, with a peak parasite, even in the High Arctic, massive synchro- of oocyst output during the afternoon hours. This nized oocyst release, enabling higher oocysts con- might be triggered by (1) endogenous rhythmicity in centration in faecal droplet, might take over the any other physiological parameter of the bird, e.g.
advantage of being equally distributed over time and body temperature (Willmer et al. 2000), or (2) have exogenous reason, e.g. midnight ‘lull' in foraging Whatever the proximate functions and ultimate activity of the host, due to diurnal variation in food reasons are, we suggest that the ability of success- availability, which in its turn can be caused by Keeping the clock set under the midnight sun ineffectiveness of the ‘classical' ones is kept under Dolnik, O. (2002). Some aspects of the biology and host-parasite positive selection pressure in the wild. This, in its interactions of Isospora spp. (Protozoa: Coccidiida) of passerine birds.
Ph.D. thesis, University of Oldenburg, Oldenburg, Germany.
turn, proves that maintaining synchronization of Dolnik, O. V. (2006). The relative stability of chronic Isospora sylvianthina circadian rhythms of individual Isospora parasites (Protozoa: Apicomplexa) infection in blackcaps (Sylvia atricapilla): within their passerine host remains crucial for evaluation of a simplified method of estimating isosporan infection intensityin passerine birds. Parasitology Research 100, 155–160. doi: 10.1007/s00436- the success and survival of these parasites above the Polar Circle. The reasons for the persistence of the Dolnik, O. V., Dolnik, V. R. and Bairlein, F. (2010). The effect of host synchronized temporal pattern in oocyst output foraging ecology on the prevalence and intensity of coccidian infection inwild passerine birds. Ardea 98, 97–103.
under the High Arctic midnight sun, as well as Dolnik, O. V. and Loonen, M. J. J. E. (2007). Isospora plectrophenaxia n. sp the Zeitgeber for its synchronizing, remain to be (Apicomplexa: Eimeriidae), a new coccidian parasite found in Snow investigated in detail.
Bunting (Plectrophenax nivalis) nestlings on Spitsbergen. ParasitologyResearch 101, 1617–1619. doi: 10.1007/s00436-007-0703-8.
Erikstad, K. E. (1989). The diel activity of Carabid Beetles (Coleoptera)North of the Arctic Circle, with particular reference to Patrobus assimilis Chaud. and Notiophilus aquaticus L. Polar Biology 9, 319–323. doi: 10.1007/ We express gratitude to Janwillem Loonen, Oebele Dijk BF00287430.
Grulet, O., Landau, I., Millet, P. and Baccam, D. (1986). Les Isospora and Yvan Satgé for their great assistance and support du moineau II – Etudes sur la biologie. Annales de Parasitologie Humaine et during the field seasons on Svalbard. We are very grateful to Comparée 61, 161–192.
Siegrid Debatin from AWI-Potsdam for weather-station Gwinner, E., Hau, M. and Heigl, S. (1997). Melatonin: generation data, and to Franz Bairlein and Anton Antonov for their and modulation of avian circadian rhythms. Brain Research Bulletin 44, comments on the manuscript. Permission to ring and handle Snow Bunting nestlings was given by the Stavanger Museum, the Governor of Svalbard and the Norwegian vulgaris) und der Schneeammer (Plectrophenax nivalis). Oecologia 1, Animal Research Authority (project number 07/22333).
176–218.
Hau, M., Romero, L. M., Brawn, J. D. and Van't Hof, T. J. (2002). Effectof Polar Day on plasma profiles of melatonin, testosterone, and estradiol inHigh-Arctic Lapland Longspurs. General and Comparative Endocrinology 126, 101–112. doi:10.1006/gcen.2002.7776.
The work was supported by the Netherlands Organisation Krüll, F., Demmelmeyer, H. and Remmert, H. (1985). On the for Scientific Research (NWO) (grant number 851.40.071).
circadian rhythm of animals in high Polar latitudes. Naturwissenschaften72, 197–203.
Kumar, V., Singh, B. P. and Rani, S. (2004). The bird clock: A complex,multi-oscillatory and highly diversified system. Biological Rhythms Research 35, 121–144. doi: 10.1080/09291010412331313287.
Asio, S. M., Simonsen, P. E. and Onapa, A. W. (2009). Analysis of the 24-h microfilarial periodicity of Mansonella perstans. Parasitology Research O'Connor, B., Pärn, H. and Foufopoulos, J. (2009). Feather mites and 104, 945–948. doi: 10.1007/s00436-008-1312-x.
internal parasites in small ground finches (Geospiza fuliginosa, Emberizidae) Barré, N. and Troncy, P. M. (1974). Note on a coccidian of some Ploceidae from the Galapagos Islands (Equador). Journal of Parasitology 95, 39–45.
in Chad: Isospora xerophila n. sp. Zeitschrift für Parasitenkunde 44, 139–147.
Belli, S. I., Smith, N. C. and Ferguson, D. J. P. (2006). The coccidian Long, P. L. (1982). The Biology of the Coccidia. University Park Press, oocyst: a tough nut to crack! Trends in Parasitology 22, 416–423. doi: Baltimore, MD, USA.
Martinaud, G., Billaudelle, M. and Moreau, J. (2009). Circadian Boughton, D. C. (1933). Diurnal gametic periodicity in avian Isospora.
variation in shedding of the oocysts of Isospora turdi (Apicomplexa) in American Journal of Hygiene 33, 161–184.
blackbirds (Turdus merula): an adaptative trait against desiccation and ultraviolet radiation. International Journal for Parasitology 39, 735–739. doi: Veränderung des Melatoninspiegels: Experimentelle Untersuchungen am Reierth, E., Van't Hof, T. J. and Stokkan, K. A. (1999). Seasonal and daily Modell eines Wirt-Parasit-Systems. Ph.D. thesis, University of Munich, variations in plasma melatonin in the High Arctic Svalbard ptarmigan (Lagopus mutus hyperboreus). Journal of Biological Rhythms 14, 314–319. doi: Bünning, E. (1973). The Physiological Clock. Springer-Verlag, New York, Schwalbach, G.
Bush, A. O., Fernandez, J. W., Esch, G. W. and Seed, J. R. (2001).
Coccidien der Gattungen Eimeria, Isospora und Caryospora bei Vögeln Perspectives in Parasitology: The Ecology and Diversity of Parasites.
Cambridge University Press, Cambridge, UK.
Protistenkunde 104, 431–491.
Calisi, R. M. and Bentley, G. E. (2009). Lab and field experiments: are Schwalbach, G. (1960). Die Coccidiose der Singvoegel. I. Der they the same animal? Hormones and Behavior 56, 1–10. doi:10.1016/j.
Cockrem, J. F. (1991). Plasma melatonin in the Adelie penguin (Pygoscelis Infektionskrankheiten und Hygiene 178, 263–276.
adeliae) under continuous daylight in Antarctica. Journal of Pineal Research significance of circadian clocks.
10, 2–8. doi: 10.1111/j.1600-079X.1991.tb00002.x.
Chronobiology International 20, 901–919. doi: 10.1081/CBI-120026099.
Combes, C. (2001). Parasitism. The Ecology and Evolution of Intimate Svobodová, M. (1994). Isospora, Caryospora and Eimeria (Apicomplexa: Interactions. University of Chicago Press, Chicago, IL, USA.
Eimeriidae) in passeriform birds from Czech Republic. Acta Protozoologica Cramp, S. and Perrins, C. (eds.) (1994). Handbook of the Birds of Europe, 33, 101–108.
the Middle East and North Africa: The Birds of the Western Palearctic: Wild, C. (2003). Experimentelle Untersuchung zur Chronobiologie einer Buntings and New World Warblers Vol. IX. Oxford University Press, Wirt-Parasit-Beziehung am Beispiel der Coccidiose (Isospora lacazei) des Haussperling (Passer domesticus). Ph.D. thesis, University of Munich, Dolnik, O. V. (1999). Diurnal periodicity in appearance of Isospora Munich, Germany.
(Protozoa: Coccidea) oocysts from some passerine birds. Proceedings of the Willmer, P., Stone, G. and Johnston, I. A. (2005). Environmental Zoological Institute RAS 281, 113–118.
Physiology of Animals. Blackwell Science, Oxford, UK.

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