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Parasites and Population Change of Rock Ptarmigan in Iceland

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Parasites and Population Change of Rock Ptarmigan in Iceland Parasites and population change of rock ptarmigan in Iceland Ute Stenkewitz Faculty of Life and Environmental Sciences University of Iceland 2017 Parasites and population change of rock ptarmigan in Iceland Ute Stenkewitz Dissertation submitted in partial fulfillment of a Philosophiae Doctor degree in Biology Advisor Ólafur Karl Nielsen PhD Committee Karl Skírnisson Gunnar Stefánsson Departmental Coordinator Páll Hersteinsson† Snæbjörn Pálsson Opponents Steve Albon José Alves Faculty of Life and Environmental Sciences University of Iceland Reykjavik, May 2017 Title: Parasites and population change of rock ptarmigan in Iceland Short title: Parasites and population change of ptarmigan Dissertation submitted in partial fulfillment of a Philosophiae Doctor degree in Biology Citation: Ute Stenkewitz. 2017. Parasites and population change of rock ptarmigan in Iceland. PhD dissertation. Faculty of Life and Environmental Sciences, University of Iceland. 172 pp. Copyright © 2017 Ute Stenkewitz All rights reserved Faculty of Life and Environmental Sciences University of Iceland 101 Reykjavik Iceland Telephone: +354 525 4000 ISBN 978-9935-9344-3-7 Printed by: Háskólaprent ehf. Reykjavik, Iceland, May 2017 ABstract The parasite fauna of the Icelandic rock ptarmigan Lagopus muta had just been described when engaging in this project in 2010. The purpose was to study the influence that parasites exhibit on ptarmigan population change over a period of 7 years (2006–2012). The cycles that the Icelandic ptarmigan population has recently been undergoing peak every 5–6 years. Host-parasite interactions are known as one possible regulator of cycling host populations. Measures of the parasite community and pathogenic parasites were analysed. Ptarmigan population density was particularly associated with the prevalence of a coccidian parasite named Eimeria muta. Annual aggregation levels of this eimerid fluctuated inversely with its prevalence, with lows at prevalence peak and vice versa. Both prevalence and aggregation of E. muta tracked ptarmigan population density with a 1.5 year time lag. The time lag could be explained by the host specificity of this eimerid, host density dependent shedding of oocysts, and their persistence in the environment from one year to the next. E. muta prevalence was also negatively associated with ptarmigan body condition, marginally negatively with fecundity, and positively with mortality, indicating their pathogenicity. Further, there were significant associations between fecundity and the chewing louse Amyrsidea lagopi prevalence (negative), excess juvenile mortality and the nematode Capillaria caudinflata prevalence (positive), and adult mortality and the skin mite Metamicrolichus islandicus prevalence (negative). Though this study is correlational, it provides strong evidence that the microparasite E. muta has the potential to destabilize rock ptarmigan population dynamics in Iceland. Útdráttur Sníkjudýrafánu íslensku rjúpunnar Lagopus muta hafði nýlega verið lýst þegar rannsóknir mínar hófust árið 2010. Markmið mitt var að rannsaka hvaða áhrif sníkjudýr hafa á stofnbreytingar rjúpunnar og rannsóknatíminn var 7 ár (2006-2012). Stofnsveifla rjúpunnar hefur breyst á síðustu árum og nú líða um 5-6 ár á milli hámarka. Einn af þeim þáttum sem vitað er að hafa áhrif á stofnsveiflur eru tengsl hýsils og sníkjudýrs. Við greininguna voru skoðuð lýsigildi fyrir sníkjudýrasamfélagið í heild sinni og einstakar meinvirkar sníkjudýrategundir. Þéttleiki rjúpna sýndi sterkt samband við smittíðni hnísilsins Eimeria muta. Dreifing þessarar hníslategundar innan rjúpnastofnsins breyttist í tengslum við breytingar á smittíðni, hnappdreifing þeirra var mest þegar smittíðnin var lægst og svo öfugt. Ferlarnir sem lýsa breytingum á bæði smittíðni og dreifingu E. muta fylgdu ferlinum sem lýsti stofnbreytingum rjúpunnar en með eins og hálfs árs töf. Töfin endurspeglar hýsilsérhæfingu þessa sníkjudýrs, þéttleikháðum útskilnaði þolhjúpa hnísilsins, og langtíma virkni þolhjúpanna, en þeir geta lifað á milli ára í umhverfinu. Meinvirkni E. muta lýsti sér m.a. í neikvæðu sambandi við holdafar fuglanna, og nær marktæku neikvæðu sambandi við frjósemi þeirra annars vegar og jákvæðu sambandi við afföll þeirra hins vegar. Enn fremur voru marktæk neikvæð tengsl á milli frjósemi og smittíðni naglúsarinnar Amyrsidea lagopi, jákvæð tengsl á milli umframaffalla ungfugla og smittíðni þráðormsins Capillaria caudinflata, og neikvæð tengsl á milli smittíðni húðmítilsins Metamicrolichus islandicus og affalla fullorðinna fugla. Þó svo að þessi rannsókn byggi á fylgni þá bendir hún sterklega til þess að sníkjudýrið E. muta hafi alla burði til að skapa óstöðugleika í stofnstærðarstjórnun rjúpunnar á Íslandi. hoc opus, hic labor Virgil Acknowledgements In the first place I would like to express my deep gratitude to Ólafur K. Nielsen from my PhD committee for his support of my PhD study, for his immense knowledge and wisdom, and for letting me see my edges. His guidance and giving me space motivated and helped me most through this endeavor. I often feel deeply happy and joyful for having made this choice as mentor. My sincere thanks go to Karl Skírnisson from my PhD committee for sharing his specialist knowledge in parasitology, as well as insightful comments, support, and stimulating discussions in the course of my PhD study. His support was crucial to conduct this research. I thank Gunnar Stefánsson from my PhD committee, for sharing his expertise in statistics, for his insightful comments and support very necessary at certain stages of my PhD study. I am very grateful for having been provided with data in excess to the duration of my PhD study which allowed me to study the different phases of a full ptarmigan population cycle. I am sincerely grateful for the office space, use of facilities, and supply with beverages provided at the Icelandic Institute of Natural History and the Institute for Experimental Pathology (Keldur). Especially Natural History Institute has been my main place to conduct research and write. It has been very important to me in providing order, structure, and a place to belong to. The environment of the Natural History Institute can be very inspiring; facilities are newly founded and there is much space to conduct research in the diverse field of natural sciences. I thank the financial supporters of my PhD without who this study would not have taken place: Icelandic Research Fund (Grant Number 090207021; 2010–2012), Icelandic Hunting Card Fund (2012, 2013, 2015), Landsvirkjun Energy Research Fund (2013, 2015), University of Iceland Research Fund (2014), Icelandic Institute of Natural History (2010– 2016), and Erwin B. Stenkewitz (2015–2016). Sincere thanks to all the people (30+), and my colleagues and friends who have assisted in the field and laboratory in sampling and examining rock ptarmigan, in data analyses, and to all reviewers for their valuable comments on manuscripts of this study. I am grateful for the logistical support provided by the Mývatn Research Station in northeast Iceland, in particular Árni Einarsson for letting me use facilities at Skútusstaðir at varying stages of my PhD. I have been feeling a strong urge to return to Mývatn and the northeast again and again. I thank my new friends we met along this path and got to share some time together; how very precious. Most if not all of you went back to settle in home country or are yet travelling in other places, especially: Sonja & family, Chrissi & Olli, Joca, Chloé, Andreas & Zach, Kera, Silke. I thank my good old friends who kept on sharing also this path with me, for staying in touch, for your sincere interest in staying updated, for your support, your visits, for each shared memory: Katja & Mila, Beate & family, Fanny, Sina, Inga Dagmar, Anja & Chris. I thank in particular Jan Kamler for his encouragement to start these studies and support especially in the beginning of this endeavour, and for our shared memories; thank you deeply. What made me come back to this place was Iceland’s natural beauty and wilderness and the fact that Óli and Þór provided me with an unforgettable experience during my first internship in 2005. Upon my return in 2010 some thing happened and this, only this made me endure these studies. I feel deeply grateful for my family, my parents and brother, for their continuous support throughout and sharing the varying stages of my life, for always being there; immeasurable. These studies allowed me to intensely focus on one subject without much distraction; this space has been provided unceasingly by Ólafur K. Nielsen. But it also means to be able to vouch for self. Throughout all that has been happening, this in itself has made me gain freedom often without the feeling of missing out. I dearly wish to hold this space while engaging in new more shared activities and build upon this strong fundament to add more puzzle pieces and solve new mysteries J Contents Abstract l Útdráttur Acknowledgements Tables xiii Figures xv Synopsis 1 The Scene 3 2 Rock Ptarmigan 5 3 Population cycles and host-parasite interactions 9 3.1 Theory 9 3.2 The Icelandic system 11 4 Parasites of rock ptarmigan 13 5 Methods 19 5.1 Study area 19 5.2 Parasite collection and quantification 21 5.3 Body measures 25 5.4 Demographic parameters 27 5.5 Ptarmigan spring densities 29 6 Host-parasite interactions and population change of ptarmigan 31 7 Conclusions & Outlook 37 Publications Clarification of contribution 41 I The relationship between parasites and spleen and bursa mass in rock ptarmigan Lagopus muta 43 II Feather holes of rock ptarmigan are associated with amblyceran chewing lice 61 III Host-parasite interactions and population dynamics of rock ptarmigan 75 IV The parasite fauna of rock ptarmigan in Iceland: Community structure and co-occurrence within the host population 97 References 131 Appendix A 147 Appendix B 157 Appendix C 165 Appendix D 169 Tables Synopsis Table 4.1 Habitat, size, and life cycles of the ectoparasites of Icelandic rock ptarmigan. 15 Table 4.2 Habitat, size, and life cycles of the endoparasites of Icelandic rock ptarmigan. 15 Table 5.1 Plots where rock ptarmigan were censused in spring in northeast Iceland.
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