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Tropical Phenology: Bi-Annual Rhythms and Interannual Variation in an Afrotropical Butterfly Assemblage 1, 2 3 4 ANU VALTONEN, FREERK MOLLEMAN, COLIN A

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Tropical Phenology: Bi-Annual Rhythms and Interannual Variation in an Afrotropical Butterfly Assemblage 1, 2 3 4 ANU VALTONEN, FREERK MOLLEMAN, COLIN A Tropical phenology: bi-annual rhythms and interannual variation in an Afrotropical butterfly assemblage 1, 2 3 4 ANU VALTONEN, FREERK MOLLEMAN, COLIN A. CHAPMAN, JAMES R. CAREY, 5 1 MATTHEW P. AYRES, AND HEIKKI ROININEN 1Department of Biology, University of Eastern Finland, Joensuu FI-80101 Finland 2Institute of Ecology and Earth Sciences, University of Tartu, Tartu EE-51014 Estonia 3Department of Anthropology and McGill School of Environment, McGill University, Montreal, Quebec H3A 2T7 Canada 4Department of Entomology, University of California, Davis, California 95616 USA 5Department of Biological Sciences, Dartmouth College, Hanover, New Hampshire 03755 USA Citation: Valtonen, A., F. Molleman, C. A. Chapman, J. R. Carey, M. P. Ayres, and H. Roininen. 2013. Tropical phenology: bi-annual rhythms and interannual variation in an Afrotropical butterfly assemblage. Ecosphere 4(3):36. http://dx.doi. org/10.1890/ES12-00338.1 Abstract. Temporal variation and phenology of tropical insect communities and the role of environmental factors controlling this variation is poorly understood. A better understanding is needed, for example, to predict the effects of climate change on tropical insect communities and to assess the long- term persistence of tropical communities. We studied seasonal and inter-annual variation in tropical fruit- feeding butterflies by exploiting a unique 137-month abundance time series of .100 species, sampled at 22 locations in the medium altitude montane rain forest of Kibale National Park, western Uganda. Precipitation peaked twice per year, about 20 d after each equinox. Vegetation greenness peaked approximately 33 d later. Species richness and abundance of butterflies peaked about 2 and 3 months, respectively, after the greenness peak. Furthermore, temporal shifts in peaks of butterfly abundances of each 6-month cycle positively correlated with temporal shifts in peaks of vegetation greenness approximately three months before. The butterfly assemblages of ENSO warm phase years differed significantly from assemblages of the other years. To our knowledge this is the first elucidation of bi-annual rhythms in butterfly assemblages. Host plant availability could explain the seasonal cycles in butterfly abundance and species richness, because the 3-month lag observed matches with the egg-to-adult development time in the studied species. Key words: climate change; community; Enhanced Vegetation Index (EVI); greenness; insect; Lepidoptera; precipitation; similarity; tropical rain forest; Uganda. Received 30 October 2012; revised 24 January 2013; accepted 7 February 2013; published 18 March 2013. Corresponding Editor: J. Weltzin. Copyright: Ó 2013 Valtonen et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. http://creativecommons.org/licenses/by/3.0/ E-mail: [email protected] INTRODUCTION (including carbon cycling). In tropical forests, where seasonal changes in temperature are small, Knowledge of phenology and inter-annual seasonality can be much weaker than in high and variation of tropical communities is essential to mid-latitude communities; these forests can be predict and measure effects of climate change, always green and animal populations can repro- impacting e.g., biodiversity, forestry, agriculture, duce continuously. However, the existence of human health and ecosystem level processes seasonal rhythms also in tropical communities, v www.esajournals.org 1 March 2013 v Volume 4(3) v Article 36 VALTONEN ET AL. typically related to the seasonal variation in controlling the phenology of tropical insect precipitation, has been well established for a communities has remained poorly understood long time (Davis 1945, Dobzhansky and Pavan because time series that encompass multiple 1950, Wolda 1980, 1988, 1989). Since then, generations and years along with long-term data phenology, the study of seasonal timing of on environmental variation have been hard to periodic life cycle events (Rathcke and Lacey collect. To our knowledge, only two long-term 1985), has become an important field of study in studies have addressed the influence of precipita- tropical systems, addressing both species level tion on seasonal variation in tropical insect phenomena, e.g., leaf phenology (Reich et al. communities. A 13-year study of Panamanian 2004) or timing of reproduction in insects cicadas showed strong seasonality in their activity, (Frederickson 2006) as well as community level which did not correlate with the inter-annual events, e.g., changes in vegetation greenness (Pau variation in timing of rainy seasons (Wolda 1989). et al. 2010), or insect assemblage structure In a 10-year study of Ecuadorian fruit-feeding (Ahrens et al. 2009). butterflies, the species diversity and similarity With short generation times, high abundance, followed the seasonal rhythm of dry and wet and species richness, insect model systems are seasons (Grøtan et al. 2012), but the effect of inter- well suited to address the temporal dynamics annual variation in timing of rainy seasons was and phenology of tropical communities. Tropical not addressed. To our knowledge, none of the insects show remarkable variation in their sea- long-term studies have studied correlations be- sonal patterns (Wolda 1988). While the abun- tween plant phenology and temporal dynamics of dance of many species increases in the rainy tropical insect communities. Among the short- season and decreases in the dry season (Wolda term studies, no correlation was found between 1980, Wolda and Fisk 1981, Novotny and Basset leaf beetle population fluctuations and leaf-flush- 1998), an opposite pattern has been found in ing phenology in Borneo (Kishimoto-Yamada et areas with very mild dry seasons (Janzen 1973, al. 2010), while the abundance of geometroid Hamer et al. 2005). Populations of some other moths in Malaysia correlated positively with species fluctuate aseasonally (Grimbacher and amount of flowering and leaf-flushing in the Stork 2009, Kishimoto-Yamada et al. 2010). previous month (Intachat et al. 2001). Additionally, there are some long-lived tropical In addition to seasonal changes, natural insect species that seem to keep remarkably populations of short lived organisms also expe- stable (adult) population sizes over multiple rience annual fluctuations in their abundance, generations (Owen and Chanter 1972). and therefore, tropical insect communities can be Seasonal weather fluctuations may control expected to change at inter-annual time scales as population fluctuations or phenology of tropical well. Such changes could be caused e.g., by inter- insect populations either directly or via the annual variation in precipitation due to large- amount of available resources or enemies (Azer- scale climate processes such as El Nin˜o Southern efegne et al. 2001). Seasonal variation in abun- Oscillation (ENSO; e.g., Kishimoto-Yamada et al. dances can also rise from phenological 2009). The degree of inter- vs. intra-annual adaptations to seasonal environmental fluctua- variation in tropical insect communities has tions, i.e., species could respond to environmen- rarely been assessed. A short-term study of talcuessuchaschangesinphotoperiod, beetle populations in Borneo found inter-annual temperature, or moisture, which help them to variation to greatly exceed intra-annual variation, time the life-cycle optimally (Tauber et al. 1986, which supported the characterization of this Wolda 1989). Such seasonality may be mediated rainforest as generally aseasonal with a strong by diapause (Tauber et al. 1986, Molleman et al. ENSO effect (Kishimoto-Yamada et al. 2009). 2005a). For certain species, the seasonal variation In addition, there could be long-term direc- in abundance can also be explained by their tional community changes caused by changes in ability to track resources spatially and migrate the environment, e.g., elephant disturbance over long distances, often over several genera- (Bonnington et al. 2007), fires (Cleary and Genner tions (Brower 1996, Larsen 2005). 2006), deforestation and forest fragmentation The role of different environmental factors (Cleary and Genner 2006, Savilaakso et al. v www.esajournals.org 2 March 2013 v Volume 4(3) v Article 36 VALTONEN ET AL. 2009), changes in tree composition due to Kibale National Park (795 km2), Western Uganda. decimation of seed dispersers (Chapman and The park encompasses medium altitude moist Onderdonk 1998), or climate change (Chen et al. evergreen forests as well as swamps, grasslands, 2009). Even in protected tropical forests, much woodland thickets and colonizing shrubs (Struh- uncertainty remains in how the communities will saker 1997, Chapman and Lambert 2000) and is persist in the presence of habitat disruption, surrounded by agricultural land, including tea hunting and forest product exploitation and plantations and small farms. The mean annual environmental changes immediately outside the rainfall is 1696 mm with two distinct rainy reserves (Laurance et al. 2012). seasons (1990–2011; C. A. Chapman, unpublished Our long-term study was designed to elucidate data; Chapman and Lambert 2000, Stampone et assemblage patterns of fruit-feeding butterflies in al. 2011). In this paper, we will use the term ‘‘dry a protected African rain forest. This is a guild of season’’ for months December, January, February, butterflies attracted by rotten fruits
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