Fungal diversity of Macrotermes-Termitomyces nests in Tsavo, Kenya

Peer reviewe

Diversity and ecology of Termitomyces symbionts in Macrotermes mounds of the Tsavo Ecosystem, Kenya

Fungus-growing termites are ecologically important animals in tropical Africa and Asia. Especially in dry savannas, they contribute to local carbon and mineral recycling and alter soil physical properties, thus facilitating the success of many plant species. This, in turn, has indirect impacts also on animals that may e.g. benefit from improved food supply and quality. The success and ecological significance of fungus-growing termites arise from their exosymbiotic relationship with the fungal genus Termitomyces. Termites cultivate fungal symbionts within specialized compost structures in their underground nests where the mycelium assists in degradation of plant matter collected by the termites, thus providing a constant food supply for the large termite colonies. Symbiotic food processing is especially advanced in the termite genus Macrotermes which construct large above-ground soil structures – termite mounds – to enhance ventilation of the below-ground nests and to provide a favorable microclimate for fungal growth even in arid savanna environments. The aim of this thesis was to study interactions between Macrotermes termites and their Termitomyces symbionts in the semiarid Tsavo Ecosystem in Southern Kenya. We assessed the local diversity of the host insects and their fungal symbionts and produced an up-to-date phylogeny of the fungal symbionts based both on our new results and previously published DNA data. We found that the Macrotermes–Termitomyces diversity in the Tsavo Ecosystem involves two host species and three symbiont species that occur in different combinations, and the frequencies of different associations vary over the landscape. Studies on mound architecture and symbiont diversity revealed correlations between the size and type of above-ground mounds and specific host-symbiont combinations. These were linked to architecturally induced differences in nest temperatures, suggesting that different Termitomyces species may differ in their ranges of tolerable growth temperatures. Stable isotope studies provided important new information on the nutritional role of Termitomyces for Macrotermes colonies. Termitomyces promotes the nutrition of the host insects directly, as highly nitrogenous food for queen and young larvae, and indirectly, by decomposing plant matter that is eaten by workers, soldiers, and developing alates. Thereby, the fungal symbiont does not have a single universal role in the nutrition of a termite colony, but instead, different termite castes depend on the symbiosis in different ways. The isotopic imbalance of nitrogen also implied that, although the nutrition of fungus-growing termites is facilitated by the fungal symbionts, also bacterial nitrogen fixing may provide an essential complementary nitrogen source for termite colonies.Afrikassa ja trooppisessa Aasiassa elävät sienenviljelijätermiitit ovat erityisesti kuivien savannien keskeisimpiä ekosysteemiarkkitehteja. Ne osallistuvat merkittävästi elinympäristöjensä hiilen ja ravinteiden kierrätykseen sekä muokkaavat maaperää, näin mm. parantaen monien kasvi- ja muiden eläinlajien elinmahdollisuuksia. Sienenviljelijätermiittien laaja-alainen menestys perustuu pitkälti niiden symbioottiseen suhteeseen erityisten termiittisienten (suku Termitomyces) kanssa. Termiitit viljelevät sieniään maanalaisissa kammioissa, missä ne hajottavat termiittien maastosta kokoamaa kasvikariketta. Sienikammioiden ilmavissa kompostirakenteissa vaikeasti hyödynnettävät kasvisolukot muuttuvat termiiteille käyttökelpoiseksi ravinnoksi. Macrotermes-suvun termiitit rakentavat pesiensä yhteyteen massiivisia mineraalimaasta koostuvia rakenteita, termiittikekoja. Keot ylläpitävät sieniviljelmille optimaalisia lämpötila- ja kosteusoloja sekä tehostavat pesäkammioiden ilmanvaihtoa. Monimutkaisten kekorakenteiden ansiosta Macrotermes-yhdyskunnat ja niiden viljelemät termiittisienet voivat menestyä jopa kuivimmilla ja karuimmilla savanneilla, joilla monien muiden karikkeenlahottajien on mahdotonta elää. Väitöskirjassani tutkin Macrotermes-suvun termiittien sekä niiden viljelemien termiittisienten välisiä vuorovaikutussuhteita. Työssäni selvitin Tsavon puolikuivalla tasankoalueella Keniassa esiintyvien Macrotermes- ja Termitomyces-lajien geneettistä monimuotoisuutta sekä tuotin ajantasaisen fylogeneettisen puun Macrotermes-keoissa maailmanlaajuisesti esiintyvistä termiittisienilajeista. Osoitin, että kukin tutkimistani 172 termiittiyhdyskunnasta viljelee rakentamassaan keossaan aina yhtä alueella esiintyvästä kolmesta termiittisienilajista. Kolmen termiittisienilajin keskinäiset runsaussuhteet vaihtelivat erilaisten savannihabitaattien välillä, minkä lisäksi kekojen monimuotoinen arkkitehtuuri oli yhteydessä siihen, mitä sienilajia kukin termiittiyhdyskunta viljeli. Termiittikekojen sisäisten energia- ja ravinnevirtausten selvittämiseen tähdänneet isotooppitutkimukset osoittivat puolestaan, että yhdyskuntien eri termiittikastit hyötyvät sienenviljelystä eri tavoin: kuningatar ja toukat hyödyntävät sienirihmastoa runsasproteiinisena ravinnonlähteenä, kun taas yhdyskunnan muut jäsenet saavat energiansa pääosin sienirihmaston pilkkomasta kasvimateriaalista. Tuloksemme viittaavat myös siihen, että ravinnosta saatavan typen ohella termiittiyhdyskunnat pystyvät hyödyntämään kasvuunsa ilmakehän typpeä symbioottisten suolistobakteerien välityksellä

You eat what you find - Local patterns in vegetation structure control diets of African fungus-growing termites

Fungus-growing termites and their symbiotic Termitomyces fungi are critically important carbon and nutrient recyclers in arid and semiarid environments of sub-Saharan Africa. A major proportion of plant litter produced in these ecosystems is decomposed within nest chambers of termite mounds, where temperature and humidity are kept optimal for the fungal symbionts. While fungus-growing termites are generally believed to exploit a wide range of different plant substrates, the actual diets of most species remain elusive. We studied dietary niches of two Macrotermes species across the semiarid savanna landscape in the Tsavo Ecosystem, southern Kenya, based on carbon (C) and nitrogen (N) stable isotopes in Termitomyces fungus combs. We applied Bayesian mixing models to determine the proportion of grass and woody plant matter in the combs, these being the two major food sources available for Macrotermes species in the region. Our results showed that both termite species, and colonies cultivating different Termitomyces fungi, occupied broad and largely overlapping isotopic niches, indicating no dietary specialization. Including laser scanning derived vegetation cover estimates to the dietary mixing model revealed that the proportion of woody plant matter in fungus combs increased with increasing woody plant cover in the nest surroundings. Nitrogen content of fungus combs was positively correlated with woody plant cover around the mounds and negatively correlated with the proportion of grass matter in the comb. Considering the high N demand of large Macrotermes colonies, woody plant matter seems to thus represent a more profitable food source than grass. As grass is also utilized by grazing mammals, and the availability of grass matter typically fluctuates over the year, mixed woodland-grasslands and bushlands seem to represent more favorable habitats for large Macrotermes colonies than open grasslands.Peer reviewe

Caste-specific nutritional differences define carbon and nitrogen fluxes within symbiotic food webs in African termite mounds

Fungus-growing termites of the genus Macrotermes cultivate symbiotic fungi (Termitomyces) in their underground nest chambers to degrade plant matter collected from the environment. Although the general mechanism of food processing is relatively well-known, it has remained unclear whether the termites get their nutrition primarily from the fungal mycelium or from plant tissues partly decomposed by the fungus. To elucidate the flows of carbon and nitrogen in the complicated food-chains within the nests of fungus-growing termites, we determined the stable isotope signatures of different materials sampled from four Macrotermes colonies in southern Kenya. Stable isotopes of carbon revealed that the termite queen and the young larvae are largely sustained by the fungal mycelium. Conversely, all adult workers and soldiers seem to feed predominantly on plant and/or fungus comb material, demonstrating that the fungal symbiont plays a different nutritional role for different termite castes. Nitrogen stable isotopes indicated additional differences between castes and revealed intriguing patterns in colony nitrogen cycling. Nitrogen is effectively recycled within the colonies, but also a presently unspecified nitrogen source, most likely symbiotic nitrogen-fixing bacteria, seems to contribute to nitrogen supply. Our results indicate that the gut microbiota of the termite queen might be largely responsible for the proposed nitrogen fixation.Peer reviewe

Termite mound architecture regulates nest temperature and correlates with species identities of symbiotic fungi.

Background Large and complex mounds built by termites of the genus Macrotermes characterize many dry African landscapes, including the savannas, bushlands, and dry forests of the Tsavo Ecosystem in southern Kenya. The termites live in obligate symbiosis with filamentous fungi of the genus Termitomyces. The insects collect dead plant material from their environment and deposit it into their nests where indigestible cell wall compounds are effectively decomposed by the fungus. Above-ground mounds are built to enhance nest ventilation and to maintain nest interior microclimates favorable for fungal growth. Objectives In Tsavo Ecosystem two Macrotermes species associate with three different Termitomyces symbionts, always with a monoculture of one fungal species within each termite nest. As mound architecture differs considerably both between and within termite species we explored potential relationships between nest thermoregulatory strategies and species identity of fungal symbionts. Methods External dimensions were measured from 164 Macrotermes mounds and the cultivated Termitomyces species were identified by sequencing internal transcribed spacer (ITS) region of ribosomal DNA. We also recorded the annual temperature regimes of several termite mounds to determine relations between mound architecture and nest temperatures during different seasons. Results Mound architecture had a major effect on nest temperatures. Relatively cool temperatures were always recorded from large mounds with open ventilation systems, while the internal temperatures of mounds with closed ventilation systems and small mounds with open ventilation systems were consistently higher. The distribution of the three fungal symbionts in different mounds was not random, with one fungal species confined to “hot nests.” Conclusions Our results indicate that different Termitomyces species have different temperature requirements, and that one of the cultivated species is relatively intolerant of low temperatures. The dominant Macrotermes species in our study area can clearly modify its mound architecture to meet the thermal requirements of several different symbionts. However, a treacherous balance seems to exist between symbiont identity and mound architecture, as the maintenance of the thermophilic fungal species obviously requires reduced mound architecture that, in turn, leads to inadequate gas exchange. Hence, our study concludes that while the limited ventilation capacity of small mounds sets strict limits to insect colony growth, in this case, improving nest ventilation would invariable lead to excessively low nest temperatures, with negative consequences to the symbiotic fungus.Peer reviewe

CarbonSink+: Accounting for multiple climate feedbacks from forests

Forests cool the climate system by acting as a sink for carbon dioxide (CO2) and by enhancing the atmospheric aerosol load. whereas the simultaneous decrease of the surface albedo tends to have a warming effect. Here, we present the concept of CarbonSink+. which considers these combined effects. Using the boreal forest environment as an illustrative example, we estimated that accounting for the CarbonSink+ enhances the forest CO2 uptake by 10-50% due to the combined effects of CO2 fertilization and aerosol-induced diffuse radiation enhancement on photosynthesis. We further estimated that with afforestation or reforestation, i.e., replacing grasslands with forests in a boreal environment, the radiative cooling due to forest aerosols cancels most of the radiative warming due to decreased surface albedos. These two forcing components have. however, relatively large uncertainty ranges. resulting in large uncertainties in the overall effect of CarbonSink+. We discuss shortly the potential future changes in the strength of CarbonSink+ in the boreal region, resulting from changes in atmospheric composition and climate.Peer reviewe

The Center of Excellence in Atmospheric Science (2002–2019) — from molecular and biological processes to the global climate

The study of atmospheric processes related to climate requires a multidisciplinary approach, encompassing physics, chemistry, meteorology, forest science, and environmental science. The Academy of Finland Centre of Excellence in atmospheric sciences (CoE ATM) responded to that need for 18 years and produced extensive research and eloquent results, which are summarized in this review. The work in the CoE ATM enhanced our understanding in biogeochemical cycles, ecosystem processes, dynamics of aerosols, ions and neutral clusters in the lower atmosphere, and cloud formation and their interactions and feedbacks. The CoE ATM combined continuous and comprehensive long-term in-situ observations in various environments, ecosystems and platforms, ground- and satellitebased remote sensing, targeted laboratory and field experiments, and advanced multi-scale modeling. This has enabled improved conceptual understanding and quantifications across relevant spatial and temporal scales. Overall, the CoE ATM served as a platform for the multidisciplinary research community to explore the interactions between the biosphere and atmosphere under a common and adaptive framework