Intense Inhabitation and Relaxed Host-Leaf Preference of Aquatic Chironomid Leaf-Miners in Headwater Streams in Asian Lucidophyllous Forests Makoto Kato*

Journal of Natural History, 2015 Vol. 49, Nos. 31–32, 1891–1903, http://dx.doi.org/10.1080/00222933.2015.1006279 Intense inhabitation and relaxed host-leaf preference of aquatic chironomid leaf-miners in headwater streams in Asian lucidophyllous forests Makoto Kato* Graduate School of Human and Environmental Studies, Kyoto University, Kyoto, Japan (Received 17 February 2014; accepted 2 January 2015; first published online 5 March 2015) Submerged leaf litter in headwater streams covered by Asian lucidophyllous (glossy broad-leaved evergreen) forests was found to be frequently processed by leaf-mining larvae of a chironomid, Stenochironomus okialbus. The larva gnaws plant tissue of the mine wall while swimming and undulating its body in the water- filled mine. To detect the level of the inhabitation and host-preference of the aquatic leaf-miner, extensive samplings of mined leaves were made in various headwater streams covered by lucidophyllous forests in the Japanese Island Arc. The chironomid showed significant preference for leaf texture (evergreen to decid- uous leaves) and for specific taxonomic groups of the host plants (Fagaceae and Lauraceae), whereas diverse taxa of leaves were utilised. The relaxed host-leaf preference unique among herbivorous insects is suggested to be caused by the larval water-circulating behaviour in their porous mines and by leaching and microbial decomposition of plants’ secondary metabolites in submerged leaves. Keywords: host-leaf preference; aquatic leaf-miner; lucidophyllous forest; detritus passway; chironomid midge Introduction In forested headwater stream ecosystems, leaf litter of vascular plants is the most important component in the organic matter budgets, and the plant breakdown proceeds in leaching, microbial decomposition and conditioning, and fragmentation by invertebrate shredders (Kaushik and Hynes 1968; Webster and Benfield 1986; Wallace and Webster 1996; Gessner et al. 1999). The relative importance of microbial vs macroinvertebrate processing changes on a latitudinal gradient with macroinverte- Downloaded by [University of Cambridge] at 05:10 08 April 2016 brate shredders more abundant and diverse in temperate than in tropical streams (Boyero et al. 2011, 2012), and among tropical streams macroinvertebrate shredders are more important at high altitudes (Irons et al. 1994; Yule et al. 2009). Between the microbial and the invertebrate processings, however, a unique process – that is, leaf-mining by Stenochironomus larvae (Insecta: Diptera: Chironomidae) – occurs in some restricted ecosystems such as clear lentic or lotic water in the holarctic region (Borkent 1984) and in the Neotropics (Wantzen and Wagner 2006). Although there are several genera of leaf-mining chironomids which live by filter-feeding, Stenochironomus larvae feed on tissue of submerged leaves (Borkent 1984). In terrestrial ecosystems, leaf-mining habits are ubiquitous among diverse phytophagous insect lineages, and host-specific leaf-miners are quite common *Email: [email protected] © 2015 Taylor & Francis 1892 M. Kato on diverse plant species (Hering 1951). In contrast with the great diversity and abundance of these terrestrial leaf-miners, aquatic leaf-miners of submerged leaf litter are generally less common and have attracted little ecological attention. Through my ecological survey of submerged leaf litter in headwater streams in the Japanese Arc, a great abundance of Stenochironomus leaf-mines has been found in lotic water running in lucidophyllous (evergreen broad-leaved) forests, the dominant trees of which have thick, glossy, long-lived leaves with developed cuticle (Ohsawa 2009). The textural and ecological characteristics of the leaves are consid- ered to be adaptations to various environmental and biological stresses such as much rainfall caused by monsoon during the summer season, cool dry weather in winter, soil nutrient deficiency and intense herbivory (Chabot and Hicks 1982; Prentice et al. 1992; Onoda et al. 2011). The leaves fallen into streams are transported by currents and gathered into brinks, pools or interstitials among gravels and boulders. The thick, glossy, long-lived leaves of lucidophyllous trees are more water-persistent than thin, unglossy, deiciduous leaves, whereas both types of leaves are conditioned by aquatic fungi and microorganisms. The conditioned and softened leaves are often mined by the chironomid leaf-miners, before being consumed by shredders such as trichopteran, ephemeropteran and plecopteran insects, shrimps, crabs and tadpoles. Litter fall is provided by diverse tree species in lucidophyllous forests as in tropical forests (Covich 1988). The physical and chemical attributes of leaves vary among different tree species, and are known to influence leaf litter utilisation by shredders (Anderson and Sedell 1979; Webster and Benfield 1986; Bastian et al. 2007). Aquatic leaf-miners might be more directly influenced by the chemical defence substances than shredders, because they are living in leaf tissue. However, almost no analyses on leaf utilisation pattern of these aquatic leaf-miners have been conducted. In order to clarify the abundance, biology and ecological role of the Stenochironomus species in Asian lucidophyllous forests, I conducted extensive sampling of submerged leaf litter in various streams in the Japanese Arc, and examined density and host-plant utilisation patterns of the chironomid larvae. In this paper, I report the natural history, distribution pattern and relaxed host-leaf preference of the aquatic leaf-miner, which contrasts with the high host-plant specificity of terrestrial leaf-miners. In compiling these data, I discuss an ecological role of the Stenochironomus species in the decomposition chain in streams in lucidophyllous forests. Downloaded by [University of Cambridge] at 05:10 08 April 2016 Materials and methods After a preliminary search for aquatic leaf-miners, extensive samplings of submerged leaf litter in streams were made throughout the Japanese island arc from 1999 to 2010. A scoop of submerged leaves was collected from bathing brinks or pools in streams with a shafted hand net (diameter = 40 cm). Among 48 sampling sites (Figure 1), mined leaves were found at 11 sites (S1–S11) at altitudes from 5 to 250 m and latitudes from 24 to 38°N (Table 1). S1–S7 are located in the Japanese Archipelago, and S8–S11 in the Ryukyu Archipelago. Samples which were collected more than one time at the same site were merged. No specific permissions were required for these locations/activities, and the field studies did not involve endangered Journal of Natural History 1893 Figure 1. A map showing sampling sites in the Japanese Island Arc. Triangles, sites where leaf- mines were not found; circles, sites where leaf-mines were found (S1–S11). Northern limit of Downloaded by [University of Cambridge] at 05:10 08 April 2016 lucidophyllous forests is also shown. or protected species. Although periodic samplings were not made at each site, the sampling dates collectively totally cover all seasons. For the samples at S1–S11, all leaves were identified and examined for presence/ absence of leaf-mines. The common plant species, for which more than nine leaves were collected, are listed in Table 2. For three samples at S8–S10 (S8, 27 August 2006; S9, 30 April 2006; S10, 9 May 2002), frequency distribution of leaf-mines per leaf was investigated. Mining larvae were reared in aquaria whose water was changed every day, and their behaviour and morphology were observed under a microscope. 1894 Table 1. A list of 11 sites (S1–S11) where submerged leaves were mined by Stenochironomus okialbus, with their localities, latitudes, longitudes, altitudes, sampling dates, dominant tree species of each riverside forest and total number of sampled leaves. M. Kato Site Locality Latitude, Altitude Sampling date Dominant tree species of the surrounding No. longitude (m) forest sampled leaves S1 Tsuzura-buchi, Shirahama, 33°38ʹ45ʹʹN, 30 3 Aug., 2 October 2004 Quercus glauca, Castanopsis sieboldii, 189 Wakayama Pref. 135°25ʹ26ʹʹE Myrica rubra S2 Kotonotaki, Susami, 33°33ʹ37ʹʹN, 140 2 September 2002, 2 August Castanopsis sieboldii, Quercus glauca, 203 Wakayama Pref. 135°32ʹ29ʹʹE 2004 Quercus phillyraeoides S3 Takase, Koza-gawa, 33°32ʹ20ʹʹN, 5 11 November 2005, 5 May Castanopsis sieboldii, Machilus japonica, 333 Wakayama Pref. 135°46ʹ53ʹʹE 2008 Alnus serrulatoides S4 Takinohai, Kozagawa, 33°36ʹ22ʹʹN, 70 19 November 2005 Quercus glauca, Zelkova serrata, Quercus 343 Wakayama Pref. 135°45ʹ54ʹʹE phillyraeoides S5 Nachi, Nachi-Katsuura, 33°40ʹ38ʹʹN, 180 28 Auf. 2003 Quercus glauca, Castanopsis sieboldii, 936 Wakayama Pref. 135°53ʹ57ʹʹE Quercus salicina S6 Nakatani, Sakamoto, 32°26ʹ47ʹʹN, 30 11 December 2005 Quercus glauca, Celtis sinensis, Wisteria 635 Kumamoto Pref. 130°39ʹ47ʹʹE floribunda Downloaded by [University of Cambridge] at 05:10 08 April 2016 S7 Tashiro, Kinkou, 31°9ʹ38ʹʹN, 250 11 December 2005 Castanopsis sieboldii, Distylium racemosum, 203 Kagoshima Pref. 130°52ʹ31ʹʹE Ligustrum japonicum S8 Akina, Amami Is., 28°25ʹ6ʹʹN, 60 4 July 1999, 8 June 2002, 19 Castanopsis sieboldii, Quercus glauca, 1764 Kagoshima Pref. 129°33ʹ26ʹʹE December 2005, 27 April Machilus japonica 2006, 5 December 2009 S9 Yakukachi, Amami Is., 28°13ʹ34ʹʹN, 25 18 December 2005, 30 April Castanopsis sieboldii, Styrax japonica, 1928 Kagoshima Pref. 129°21ʹ20ʹʹE 2006, 27 April 2007 Machilus japonica S10 Yona, Okinawa Is., 26°45ʹ13ʹʹN, 80 2 May 2002 Castanopsis sieboldii, Alnus formosana, 735 Okinawa

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