Szent István Egyetem Állatorvos-tudományi Doktori Iskola Host-parasite relationship of birds (Aves) and lice (Phthiraptera) – evolution, ecology and faunistics PhD értekezés Vas Zoltán 2013 Témavezető és témabizottsági tagok: Prof. Dr. Reiczigel Jenő Szent István Egyetem, Állatorvos-tudományi Kar, Biomatematikai és Számítástechnikai Tanszék témavezető Dr. Rózsa Lajos MTA-ELTE-MTM Ökológiai Kutatócsoport témavezető Dr. Harnos Andrea Szent István Egyetem, Állatorvos-tudományi Kar, Biomatematikai és Számítástechnikai Tanszék témabizottság tagja Dr. Pap Péter László Babes-Bolyai Tudományegyetem, Biológia és Geológia Kar; Debreceni Egyetem, Viselkedésökológiai Kutatócsoport témabizottság tagja Készült 8 példányban. Ez a n. …. sz. példány. …………………………………. Vas Zoltán 2 “He [Bonpland] wanted to know what statistics about lice were good for. One wanted to know, said Humboldt, because one wanted to know.” Daniel Kehlmann: Measuring the World [Vermessung der Welt, Rowohlt Verlag GmbH, 2005]; English translation by C. B. Janeway, Quercus, 2007 3 Content Abstract................................................................................................................................. 5 Preface .................................................................................................................................. 6 General introduction ............................................................................................................ 7 Chapter 1 – Louse diversity and its macroevolutionary shaping factors ....................... 19 1.1. Introduction to Chapter 1 ............................................................................................... 19 1.2.1. Case study: Clever birds are lousy: Co-variation between avian innovation and the taxonomic richness of their Amblyceran lice ......................................................................... 26 1.2.2. Case study: Avian brood parasitism and ectoparasite richness – scale-dependent diversity interactions in a three-level host-parasite system ................................................... 38 1.2.3. Case study: Evolutionary co-variation of host and parasite diversity – the first test of Eichler’s rule using parasitic lice (Insecta: Phthiraptera) ....................................................... 53 1.3. Conclusions of Chapter 1 .............................................................................................. 68 Chapter 2 – Louse faunistics and conservation biology ................................................. 72 2.1. Introduction to Chapter 2 ............................................................................................... 72 2.2.1. Hungarian louse fauna and the history of its investigation........................................... 73 2.2.2. Case study: A checklist of lice of Hungary (Insecta: Phthiraptera) .............................. 75 2.2.3. Case study: New species and host association records for the Hungarian avian louse fauna (Insecta: Phthiraptera) ................................................................................................ 78 2.3.1. Louse sampling – methods and their limitations.......................................................... 84 2.3.2. Case study: Ringing procedure can reduce the burden of feather lice in Barn Swallows Hirundo rustica ..................................................................................................................... 87 2.4.1. Endangered parasites ................................................................................................. 93 2.4.2. Case study: A list of co-extinct and critically co-endangered species of parasitic lice (Phthiraptera) with remarkable cases of conservation-induced extinction ............................. 94 2.5. Conclusions of Chapter 2 ............................................................................................ 101 Summary ........................................................................................................................... 103 Acknowledgements .......................................................................................................... 105 References ........................................................................................................................ 106 List of publications........................................................................................................... 132 Appendices ....................................................................................................................... 136 Appendix 1: Lists to 2.2.2 (Vas et al 2012b): A checklist of lice (Insecta: Phthiraptera) of Hungary.............................................................................................................................. 136 Appendix 2: Authors’ affiliations and addresses.................................................................. 275 4 Abstract The host-parasite relationship is one of the most complex and intimate associations in nature. In this thesis I present a multidisciplinary approach to investigate the host-parasite relationship of lice (Insecta: Phthiraptera: Amblycera, Ischnocera) and their avian (and sometimes mammalian) hosts (Vertebrata: Aves, Mammalia). I apply both modern statistical methodologies of evolutionary comparative analysis and classical zoological methodologies such as sampling in the field for faunistical purposes. The understanding of the diversity component of host-parasite relationships is a major and yet scarcely discovered field of evolutionary ecology. Here I present a review of the previous literature and three original studies published by myself and my co-authors concerning the factors that shape louse diversity at macroevolutionary level (Chapter 1). I show a positive co-variation found between avian cognitive capabilities and Amblyceran louse richness; a decrease in louse richness due to the brood-parasitic life-style of the hosts; and a positive diversity interaction between Ischnoceran louse richness and foster species richness of brood-parasitic cuckoos. The supposed positive co-variation between host and parasite diversity – an assumption originating from Eichler (1942, the so called Eichler’s rule) – were revisited and tested for the first time with modern methodologies across a wide range of avian and mammalian hosts and their lice, and showed to be the strongest and most general diversity pattern of host-parasite evolution found so far. Chapter 2 incorporates papers related to different aspects of louse faunistics as well as the review of their background. First, I summarize the Hungarian louse fauna based on formerly published records. Second, I report that this checklist was significantly extended by my own recent collections. The third paper is a methodological contribution that points out a formerly overlooked bias in currently widespread sampling projects: the handling of avian host individuals during the bird ringing procedure can reduce the louse burden. Finally, in the last paper I provide global checklist of critically endangered species of parasitic lice. 5 Preface The host-parasite relationship is one of the most complex and intimate associations in nature. Given the astonishing diversity of parasitic animals, as well as that of their hosts, a huge variety of interactions evolved between the two partners. These interactions can be studied from several different point of view, each field contributing to the general understanding of host-parasite relationships. At an ecological level, this relationship is often characterized as an arms race – emphasizing the conflicting adaptations and counter- adaptations of the partners. Nevertheless, often the present partners’ ancestors have already been associated through evolutionary ages, raising the possibility to study how host and parasite lineages have affected each other’s adaptation and diversification. However, none of these studies is able to draw reliable inference without a sound classical zoological background: faunistics, taxonomy, and systematics. In this PhD thesis I present a multiple approach investigating the relationship of parasitic lice and their avian hosts. The two main chapters indicate the two fields I was most concerned in the recent years: the linkage between host and parasite diversity at a macroevolutionary level and louse faunistics. At first sight, these two main topics may seem distinctly related; however, they are rather deeply bounded. Evolutionary ecological studies on diversity interactions depend on the underlying diversity data that have been produced by faunistical studies published through decades or even centuries. The structure of my thesis follows the two topics described above; each main chapter includes several case studies published by me and my co-authors in scientific journals. These are presented here exactly as they appeared in the published papers, except for a few necessary changes in the format and citations to integrate them into this thesis. A few sentences were added to the papers’ text – both in brackets and in italics – where the reviewer of the thesis requested clarification. As a consequence, there are inevitable recurrences among some case studies, mainly in the introduction and methods sections. However, as each study has its unique set of background and methodology they cannot be pooled and overviewed together. The references are pooled together in the ‘References’ chapter to avoid duplications. Acknowledgements of the original papers are also combined