A N N A L E S U N IV E R S IT A T IS T U R K U E N S IS A II 3 3 8 S a lla K . H ä rk ö n e n GUEST ANTS AND ANT GUESTS IN RED WOOD ANT NESTS Salla K. Härkönen Oy, Turku , Finland 2017 ma Painosala ISBN 978-951-29-7041-4 (PRINT) TURUN YLIOPISTON JULKAISUJA – ANNALES UNIVERSITATIS TURKUENSIS ISBN 978-951-29-7042-1 (PDF) Sarja - ser. AII osa - tom. 338 | Biologica - Geographica - Geologica | Turku 2017 ISSN 0082-6979 (PRINT) | ISSN 2343-3183 (ONLINE) GUEST ANTS AND ANT GUESTS IN RED WOOD ANT NESTS Salla K. Härkönen TURUN YLIOPISTON JULKAISUJA – ANNALES UNIVERSITATIS TURKUENSIS Sarja - ser. A II osa - tom. 338 | Biologica - Geographica - Geologica | Turku 2017 University of Turku Faculty of Mathematics and Natural Sciences Department of Biology Section of Ecology Supervised by Associate Professor Jouni Sorvari Docent Ilari E. Sääksjärvi Department of Environmental Biodiversity Unit and Biological Sciences University of Turku University of Eastern Finland Turku, Finland Kuopio, Finland Reviewed by Professor Toomas Tammaru Docent Atte Komonen Department of Zoology Department of Biological Institute of Ecology and Earth Sciences and Environmental Science Tartu, Estonia University of Jyväskylä Jyväskylä, Finland Opponent Doctor Elva Robinson Department of Biology University of York York, UK Cover illustration by Salla K. Härkönen The originality of this thesis has been checked in accordance with the University of Turku quality assurance system using the Turnitin OriginalityCheck service. ISBN 978-951-29-7041-4 (PRINT) ISBN 978-951-29-7042-1 (PDF) ISSN 0082-6979 (PRINT) ISSN 2343-3183 (ONLINE) Painosalama Oy - Turku, Finland 2017 Contents 3 CONTENTS ABSTRACT ............................................................................................................................... 4 TIIVISTELMÄ ........................................................................................................................... 5 LIST OF ORIGINAL PUBLICATIONS ........................................................................................... 6 1 INTRODUCTION .............................................................................................................. 7 1.1 ANTS AND THEIR IMPORTANCE IN NATURE ............................................................................. 7 1.1.1 Red wood ants ........................................................................................................ 7 1.2 MYRMECOPHILES AND OTHER ASSOCIATES OF ANTS ................................................................. 9 1.3 SOCIAL PARASITISM AMONG ANTS ..................................................................................... 11 1.3.1 Formicoxenus nitidulus ......................................................................................... 12 1.4 FACTORS AFFECTING SPECIES RICHNESS AND ABUNDANCE ....................................................... 13 1.5 WOOD ANTS AND FOREST CLEAR FELLING ............................................................................ 13 1.6 AIMS OF THE THESIS ....................................................................................................... 15 2 METHODS ..................................................................................................................... 17 2.1 STUDY SPECIES ............................................................................................................... 17 2.1.1 Formicoxenus nitidulus (III) ................................................................................... 17 2.2 STUDY AREAS................................................................................................................. 18 2.3 SAMPLING AND OBSERVATION .......................................................................................... 19 2.4 SPECIES IDENTIFICATION .................................................................................................. 22 2.5 SPECIES RICHNESS ESTIMATION.......................................................................................... 22 3 RESULTS AND DISCUSSION ........................................................................................... 24 3.1 ASSOCIATES OF ANTS (I, II, III, V) ...................................................................................... 24 3.1.1 Associate community in F. polyctena nests (I) ...................................................... 25 3.1.2 Sawtoothed grain beetle (II) ................................................................................. 26 3.2 ISOLATION AND NEST VOLUME IN RELATION TO SPECIES RICHNESS AND ABUNDANCE (I, V) ............ 26 3.3 OCCURRENCE OF FORMICOXENUS NITIDULUS (III) ................................................................. 28 3.4 CLEAR FELLING, NEST MOISTURE CONTENT AND ANT-ASSOCIATED BEETLES (IV & V) .................... 29 4 CONCLUSIONS .............................................................................................................. 32 ACKNOWLEDGEMENTS ......................................................................................................... 34 REFERENCES ......................................................................................................................... 36 ORIGINAL PUBLICATIONS I–V ............................................................................................... 45 4 Abstract ABSTRACT Red wood ants (Formica rufa group) impact forest ecosystems in a multitude of ways and can thus be considered as ecosystem engineers. Although they are highly efficacious predators of many arthropods, their nests host a diverse community of other arthropods. In this thesis, I wanted to highlight the diversity of red wood ant associated guest fauna in order to emphasize the role of red wood ants in the maintenance and conservation of forest biodiversity. I examined the underlying factors shaping the community composition and species richness of associates. Particularly, I studied the factors determining the occurrence of the globally vulnerable shining guest ant (Formicoxenus nitidulus), an obligate social parasite of mound- building wood ants. I also studied the effects of clear felling on ant nest mounds as well as on the ant-associated beetle community. A total of 85 different taxa (mostly beetles), including 26 myrmecophiles (species dependent on ants), were identified in the course of this thesis. One unexpected discovery was the sawtoothed grain beetle (Oryzaephilus surinamensis), which has so far only been recorded as an indoor pest species in Finland. Overall, I found that species richness and occurrence of associates were negatively associated with isolation of the nest mounds. The occurring probability of the guest ant F. nitidulus increased with decreasing isolation and increasing nest mound size. The guest ant was more likely to occur in the nests of the polydomous (multi-nest colonies) Formica polyctena than the monodomous (single nest colonies) Formica rufa. Also, local spreading along the connecting trails between nests in polydomous host colonies seems to be important to F. nitidulus. I found that Formica aquilonia nest mounds in clear fells had significantly lower surface layer moisture content than nests in forests, which reduces the nests’ thermal capacity. Though species richness and community composition of beetles did not greatly differ between clearings and forests, total abundance was lower in clear fell nests. Furthermore, total species richness and abundance as well as myrmecophile abundance decreased with decreasing moisture content. I investigated only the short-term effects of clear felling in active nest mounds. However, nests in clear fells have a high tendency of being abandoned, which will inevitably be detrimental to myrmecophiles. How the associate community develops in the long-term in the nests surviving clear felling needs further study. This thesis reinforces the status of red wood ants as hosts of a highly diverse associate community. This needs to be taken into consideration in the maintenance and conservation of arthropod diversity in temperate and boreal forests. If the whole habitat cannot be protected, forest management practices preserving dense red wood ant populations should be used. Also, colonization chances for the wood ants as well as nest density could be increased by creating small open areas in managed forests, which would also benefit many other forest- dwelling species. Thus, maintaining a varied forest structure could help maintain and even increase the forest biodiversity. Tiivistelmä 5 TIIVISTELMÄ Kekomuurahaisten (Formica rufa ryhmä) vaikutukset metsäekosysteemeihin ovat moninaiset ja niinpä niitä voidaankin pitää ekosysteemi-insinööreinä. Vaikka ne ovat hyvin tehokkaita niveljalkaisten petoja, niiden pesät pitävät sisällään monimuotoisen yhteisön muita niveljalkaisia. Tässä väitöskirjassa halusin korostaa kekomuurahaispesien vieraslajiston monimuotoisuutta painottaakseni kekomuurahaisten roolia metsien monimuotoisuuden ylläpidossa ja suojelussa. Tarkastelin pesävieraslajistoa ja -lajimäärää muokkaavia tekijöitä. Erityisesti tutkin maailmanlaajuisesti vaarantuneen norkomuurahaisen (Formicoxenus nitidulus), kekomuurahaispesissä elävän sosiaalisen loisen, esiintymistä sääteleviä tekijöitä. Tutkin myös metsähakkuiden vaikutuksia kekoihin sekä niissä pesävieraina eläviin kovakuoriaisiin. Kaiken kaikkiaan tämän väitöskirjan aikana määritettiin 85 eri taksonia (enimmäkseen kovakuoriaisia), mukaan lukien 26 myrmekofiiliä eli muurahaisista riippuvaista lajia. Eräs odottamaton löytö oli riisihärö (Oryzaephilus surinamensis), kovakuoriaislaji, joka on tähän mennessä tavattu Suomessa ainoastaan elintarviketuholaisena. Yleisesti ottaen havaitsin, että pesävieraiden lajirunsaudella ja esiintymisellä oli negatiivinen yhteys kekojen eristyneisyyteen. Norkomuurahaisen esiintymistodennäköisyys kasvoi kekojen eristyneisyyden pienentyessä sekä keon koon kasvaessa. Norkomuurahainen esiintyi todennäköisemmin monipesäisiä yhdyskuntia muodostavan kaljukekomuurahaisen (Formica polyctena) kuin yksipesäisiä yhdyskuntia muodostavan punakekomuurahaisen (Formica rufa) pesissä. Paikallinen leviäminen monipesäisten yhdyskuntien pesiä yhdistäviä polkuja pitkin vaikuttaisi olevan tärkeää norkomuurahaiselle. Havaitsin, että tupsukekomuurahaisten (Formica aquilonia) pesissä oli merkittävästi kuivempi pintakerros hakkuualueilla kuin metsissä, mikä heikentää kekojen lämpökapasiteettia. Vaikka pesävieraskovakuoriaisten lajirunsaus tai lajisto ei eronnut merkittävästi hakkuualueiden ja metsien välillä, kokonaisyksilömäärä oli alhaisempi hakkuukeoissa. Lisäksi kokonaislaji- ja yksilömäärä sekä myrmekofiilien yksilömäärä pienenivät kosteuspitoisuuden pienentyessä. Tutkin ainoastaan hakkuiden lyhytaikaisia vaikutuksia aktiivisissa keoissa. Hakkuualueiden keoilla on kuitenkin suuri todennäköisyys tulla hylätyiksi, mikä on väistämättä haitallista myrmekofiileille. Sitä, kuinka pesävierasyhteisö kehittyy pitkällä aikavälillä hakkuista selviytyvissä keoissa, tulee tutkia lisää. Tämä väitöskirja korostaa kekomuurahaisten asemaa erittäin monimuotoisen pesävierasyhteisön isäntinä. Tämä tulee ottaa huomioon niveljalkaisten monimuotoisuuden ylläpidossa ja suojelussa lauhkean ja boreaalisen vyöhykkeen metsissä. Mikäli koko elinympäristöä ei voida suojella, metsätaloudessa tulisi pyrkiä käyttämään menetelmiä, jotka ylläpitävät kekomuurahaisten korkeaa pesätiheyttä. Lisäksi kekomuurahaisten kolonisaatiomahdollisuuksia voitaisiin lisätä luomalla talousmetsiin pieniä aukkoja, mikä hyödyttäisi myös monia muita metsälajeja. Vaihtelevalla metsärakenteella voitaisiin siten auttaa ylläpitämään ja jopa lisäämään metsien monimuotoisuutta. 6 List of Original Publications LIST OF ORIGINAL PUBLICATIONS This thesis consists of the following publications and manuscript, which are referred to in the text by their Roman numerals: I Härkönen, S. K. & Sorvari, J. (2014) Species richness of associates of ants in the nests of red wood ant Formica polyctena (Hymenoptera, Formicidae). Insect Conservation and Diversity 7: 485–495. II Sorvari, J., Härkönen, S.K. & Vesterinen, E.J. (2012) First record of an indoor pest sawtoothed grain beetle Oryzaephilus surinamensis (Coleoptera: Silvanidae) from wild outdoor wood ant nest. Entomologica Fennica 23: 69–71. III Härkönen, S. K. & Sorvari, J. (2017) Effect of host species, host nest density and nest size on the occurrence of the shining guest ant Formicoxenus nitidulus (Hymenoptera: Formicidae) Journal of Insect Conservation 21: 477–485. IV Sorvari, J., Elo, R.A. & Härkönen, S.K. (2016) Forest-built nest mounds of red wood ant Formica aquilonia are no good in clear fells. Applied Soil Ecology 101: 101–106. V Härkönen, S. K. & Sorvari, J. Comparison of ant-associated beetle communities inhabiting mounds of forest-dwelling ants in forests and forest clearings. Manuscript. Articles I - IV are reprinted with the permission of John Wiley & Sons, the Editorial Board of Entomologica Fennica, Springer, and Elsevier respectively. Contributions to the individual publications: I II III IV V Original idea JS JS JS, SKH JS, RAE, SKH JS, SKH Field work SKH SKH SKH JS JS Identification SKH, others SKH, TC - - SKH DNA Barcoding - EJV - - - Statistics SKH, JS - SKH JS SKH Writing SKH, JS JS, SKH, EJV SKH, JS JS, RAE, SKH SKH, JS Commenting IES NW IES DB RAE SKH = Salla K. Härkönen, JS = Jouni Sorvari, EJV = Eero J. Vesterinen, RAE = Riikka A. Elo, IES = Ilari E. Sääksjärvi, TC = Tom Clayhills, NW = Niklas Wahlberg, DB = Daniel Blande, others = Jari Haimi, Veikko Rinne, Seppo Koponen, Kaj Winqvist, Tom Clayhills, Lubomír Masner Introduction 7 1 INTRODUCTION 1.1 Ants and their importance in nature Jones et al. (1994) defines ecosystem engineers as organisms that directly or indirectly modulate the availability of resources to other species, by causing physical state changes in biotic or abiotic materials. Through the modification, maintenance and/or creation of habitats for other organisms they can significantly impact ecosystem dynamics. Social insects, particularly ants, are among the most successful organisms on Earth, and the key to their success lies in their social organisation. Ants, just like all termites, and some bees and wasps, are eusocial, i.e. truly social, insects (Wilson 1971). Their societies are divided into reproductive and worker castes, where overlapping generations of the more or less sterile workers cooperate in taking care of the brood of the reproductive caste. These insect colonies are often referred to as superorganisms, because the functions collectively performed by the individuals in the colony resemble the physiological properties of different organs and tissues (Wheeler 1928; Wilson 1971; Hölldobler & Wilson 1990). Currently, there are around 14 000 known ant species, and more are described all the time (Agosti & Johnson 2017). The diversity of ants is vast especially in the tropics where a single tree may hold dozens of ant species (e.g. Longino et al. 2002). In Finland, around 60 ant species can be found (Finnish Biodiversity Info Facility, FinBIF 2017). Over their more the 100 million years of existence, ants have risen to occupy key roles in many environments and have had a major influence in the shaping of present-day terrestrial ecosystems (Hölldobler & Wilson 1990; Wilson & Hölldobler 2005). Apart from Antarctica and some distant islands, ants can be found nearly everywhere, and in most parts, they are among the main predators of other invertebrates (Wilson 1971; Hölldobler & Wilson 1990). In most terrestrial habitats, they even exceed vertebrates in biomass and energy consumption (Wilson 1971). 1.1.1 Red wood ants Red wood ants of the Formica rufa group are dominant species in the boreal and temperate forests of Eurasia, where they build large perennial mound nests consisting of forest litter, resin and soil particles. The above ground nest mound may reach over 2 metres in height and have a volume of several cubic metres. The six species in the group are genetically closely related and morphologically very similar (Collingwood 8 Introduction 1979; Goropashnaya et al. 2004). Despite their large populations, the effective population sizes (i.e. the number of reproductive individuals) of red wood ants are relatively small and, thus, the conservation needs of the species may be easily underestimated (Sorvari 2016). Red wood ants are globally classed as Near Threatened species according to the World Conservation Union (IUCN 2015), and they are protected by law in many European countries (Sorvari 2016). In Finland, there are five red wood ant species (F. rufa, F. polyctena, F. aquilonia, F. pratensis, and F. lugubris). The number of queens and nests in a colony varies considerably within and between species (Ellis & Robinson 2014). Most Finnish populations of F. rufa, F. lugubris and F. pratensis are monogynous and monodomous, i.e., the colonies have only queen and they are contained within a single independent nest mound. On the other hand, F. polyctena and F. aquilonia are polygynous and polydomous, i.e., there are multiple queens per colony and the colonies may consist of several inter-connected nest mounds (Rosengren & Pamilo 1983). The species differ also in their habitat requirements and dispersal abilities. The monogynous and monodomous species prefer forest edges and open forests, whereas the polygynous and polydomous species prefer forest interiors. Monogynous species establish new colonies through temporarily parasitizing the nests of the Formica subgenus Serviformica ants such as Formica fusca. While polygynous species can also use this method, they mainly spread through colony budding, in which a group of workers and queens split from the mother colony to establish a new nest in the neighbourhood. Polygynous species thrive in large continuous forests, while monogynous species are better at dispersing to small and isolated forest patches and are, thus, better adapted to habitat fragmentation (Rosengren et al. 1993; Punttila 1996; Sundström et al. 2005; Mabelis and Korczynska 2016; Sorvari 2017, in press). Wood ants impact their physical surroundings and other organisms in a multitude of ways. Thus, changes in their populations can have wide ranging effects on both local and global ecosystems. Through predation as well as resource and interference competition they affect the species composition of other arthropods (Adlung 1966; Niemelä et al. 1992; Punttila et al. 2004) and also the breeding success of some insectivorous birds (Aho et al. 1999). By their competitive superiority they affect the distribution and abundance of other ant species (Savolainen & Vepsäläinen 1988, 1989; Savolainen et al. 1989). Furthermore, wood ants also have a role as seed dispersers of many plants (Gorb et al. 2000) and may enhance the growth of trees and shrubs by preventing folivory (Mahdi & Whittaker 1993; Atlegrim 2005). On the other hand, as most of their food consists of honeydew they may also hinder the growth of Introduction 9 some trees due to aphid tending (Rosengren & Sundström 1991; Kilpeläinen et al. 2009). The constant input of organic material and prey into their nests strongly impacts the chemical, physical and biological properties of the soil and creates hotspots for mineralization (Lenoir et al. 2001; Frouz & Jílková 2008). They offer also a food source for other animals, such as bears (e.g. Swenson et al. 1999). Finally, their nests are home to a wide variety of other arthropods as well as earthworms (Donisthorpe 1927; Laakso & Setälä 1997, 1998; Parmentier et al. 2014; Robinson et al. 2016). 1.2 Myrmecophiles and other associates of ants Concomitantly with ants, a considerable number of other organisms, comprising of at least 17 orders, over 120 families and hundreds of genera, have evolved to exploit their colonies (Donisthorpe 1927; Kistner 1982; Hölldobler & Wilson 1990; Rettenmeyer et al. 2011; Parmentier et al. 2014; Robinson et al. 2016). The earliest known fossil of a morphologically specialized and apparently obligate associate of ants is around 52 million years old (Parker & Grimaldi 2014). Wood ants have a reputation as aggressive predators that actively defend their nests. Apart from ant- tended aphids, the abundance of different invertebrate groups is generally reduced by the ants (Niemelä et al. 1992; Laakso & Setälä 2000; Punttila et al. 2004). Thus, it may seem surprising that ant nests are filled with a multitude of other organisms, apparently living quite unharmed among the ants. However, once the guest species get past the ants’ defences, ant nests are like fortresses: well protected against most outside threats and filled with stored resources (Hughes et al. 2008). Wood ant nests are also long-lived and fairly stable environments with controlled temperature and humidity conditions (Rosengren et al. 1987; Laakso & Setälä 1998). These characteristics contribute to make them ideal habitats for various invertebrates. Species that are dependent on the ants during at least part of their life cycles are referred to as myrmecophiles (Hölldobler & Wilson 1990). The relations they have with ants are varied, ranging from mutualism to parasitism, and include interactions both within the nests and outside of it. Erich Wasmann (1894) placed myrmecophiles into five categories based on their degree of specialization and integration into the host colony: 1. Persecuted guests (Synechthrans): These are mostly scavengers and predators that are treated with hostility. They survive by their agility and swiftness or by