Appl. Entomol. Zool. 42 (4): 669–674 (2007) http://odokon.org/
Laboratory studies on larval feeding habits of Amara macronota (Coleoptera: Carabidae: Zabrini)
Kôji SASAKAWA* Graduate School of Agricultural and Life Sciences, The University of Tokyo; Bunkyo-ku, Tokyo 113–8657, Japan (Received 20 February 2007; Accepted 3 July 2007)
Abstract Many studies have suggested that some carabids (tribes Zabrini and Harpalini; Coleoptera: Carabidae) feed on seeds during their adult stage (i.e., granivore or omnivore with a tendency toward granivory), but relatively few studies have investigated the larval feeding habits of those species. In the present study, larval development on different diets was examined in a Zabrini carabid Amara (Curtonotus) macronota. Six diet types were tested: Solidago altissima seeds, Bidens frondosa seeds, Setaria spp. seeds, mixed seeds, insect larvae (Diptera), and insect larvae mixed seeds. Be- cause of the high mortality during larval overwintering under laboratory-rearing conditions, survival and developmen- tal duration through pre-overwintering stages (1st and 2nd instars) were compared. The insect larvae mixed seeds diet showed high survival (85%), followed by the insect larvae diet (40%). All seed diets showed low survival rates (0–10%). Developmental durations were not significantly different, although some diets could not be compared due to a small sample size. These results suggest that A. macronota larvae are omnivores with a tendency toward carnivory. Larval morphometry, which is useful in determining the instars of field-collected larvae, was used.
Key words: Granivory; ground beetle; omnivory; rearing experiment; seed
granivory is widely recognized in carabid beetle INTRODUCTION tribes Zabrini and Harpalini (Hartke et al., 1998; Although most carabids are carnivores, some Hu° rka, 1998; Hu° rka and Jaroˇsík, 2001, 2003; carabids have been considered granivores because Saska and Jaroˇsík, 2001; Fawki and Toft, 2005; feeding on seeds has been occasionally observed in Saska, 2005). the field (e.g., Habu and Sadanaga, 1961; Trautner In Carabidae, larvae generally show a narrower and Geigenmüller, 1987; Lindroth, 1988; Hu° rka, diet range than adults (Thiele, 1977). Larvae of 1996). Later studies examining the contents of the carnivorous species are always carnivorous, but alimentary canal supported granivory in some adults occasionally eat plants such as vegetables or species (Johnson and Cameron, 1969; Hengeveld, fruit (Brandmayr, 1990); moreover, larvae of those 1980; Ishitani, 1996). Most of these studies were, species can be further divided into several types however, based on the examination of adults; there- (e.g., insectivore, snail eater or earthworm eater), fore, granivory in carabid larvae had not been con- although most adults are generally carnivores firmed until recently. Brandmayr (1990) was the (Trautner and Geigenmüller, 1987; Hu° rka, 1996). first to successfully rear harpaline carabids (genera Larvae of ‘granivorous’ species are carnivorous, Harpalus s. str. and Ophonus) on only seeds. Later, omnivorous or granivorous, but adults are usually based on laboratory-rearing experiments with suffi- omnivores with a tendency toward granivory cient replicates and statistical analyses, Jørgensen (Johnson and Cameron, 1969; Hengeveld, 1980; and Toft (1997a, b) provided additional strong evi- Jørgensen and Toft, 1997a, b; Hu° rka and Jaroˇsík, dence of larval granivory in two carabid species, 2001, 2003; Saska and Jaroˇsík, 2001; Fawki and Amara similata and H. rufipes. Since their study, Toft, 2005; Saska, 2005). This narrower diet range there has been increasing evidence that larval of larvae suggests that the larval feeding habit is
*E-mail: [email protected] DOI: 10.1303/aez.2007.669
669 670 K. SASAKAWA one of the most important life-history traits of checked daily. Hatched larvae were divided into six Carabidae, because selection pressures associated groups which were reared on a different diet type: with food resources (e.g., interspecies competition Solidago altissima L. seed, Bidens frondosa L. for resource utilization, and/or influence of the seed, Setaria spp. seed, mixed seeds, insect larvae habitat environment via food supply) would be (Lucilia spp. (Diptera); cut into pieces), and insect more intense during the larval stage than during the larvae mixed seeds (n 15 or 20, see Fig. 1). All adult stage. Nevertheless, our knowledge of this plant species examined were abundant at the col- trait is as yet insufficient; therefore, it is important lected site. Larvae were reared individually in a to describe the larval feeding habit of each species. plastic cup (3.5 cm diameter, 5.5 cm high) filled to Amara (Curtonotus) macronota (Solsky) is an a depth of 0.5 cm moistened garden soil. Death and East Asian species of the tribe Zabrini (Tanaka, moulting were checked daily and, at the same time, 1985; Hieke, 2003). In Japan, it inhabits lowland food was replaced. In carabids with larval over- grasslands, and is one of the most common species wintering (i.e., autumn breeders), the mortality in arable fields (Habu and Sadanaga, 1965). Earlier rate during overwintering is markedly high under studies have revealed the annual life cycle (Habu laboratory-rearing conditions (e.g., Habu and and Sadanaga, 1965; Ishitani, 1996; Kubota, 1998; Sadanaga, 1965, 1970; Jørgensen and Toft, 1997b; Yamazaki et al., 1999), adult feeding habit (Ishi- Saska, 2005); therefore, most studies have ana- tani, 1996), and larval morphology (Habu and lyzed only pre-overwintering developmental stages Sadanaga, 1965) of this species; however, no stud- (e.g., Jørgensen and Toft, 1997b; Saska, 2005). In ies have examined the larval feeding habit. the present study, data after the 3rd instar were not The main purpose of the present study was to in- used in analyses. vestigate the larval feeding habit of A. macronota All rearings and experiments were conducted in based on laboratory-rearing experiments. Larval an unheated room of a laboratory in the University development on six diet types including all carniv- of Tokyo, Tokyo, Japan (35°43 N, 139°46 E), orous, omnivorous and granivorous was studied. under a natural photoperiod. All data on rearing Larval morphometry, which is useful in determin- larvae are shown in the Appendix. During the ex- ing the instars of field-collected larvae, was also periments (from mid-November 2006 to mid-Janu- used. ary 2007; Appendix), the temperature gradually decreased. The average temperature (°C) in mid- and late November, early, mid-, and late December, MATERIALS AND METHODS and early and mid-January was 13.3, 12.5, 9.4, Insects and rearing adults. Amara (Curtonotus) 10.0, 9.1, 7.4, and 7.1, respectively (data obtained macronota (Coleoptera: Carabidae: Zabrini) is an from website of the Japan Meteorological Agency autumn breeder. Overwintered larvae (3rd instar) (http://www.jma.go.jp/jma/index.html)). pupate, and new adults emerge from May to June. Statistics. Effects of diets on larval development After an inactive period in summer, adults mate were evaluated by survival and developmental du- and reproduce from September to November (Habu ration. Calculations were performed using JMP and Sadanaga, 1965; Ishitani, 1996; Kubota, 1998). version 6.0.0 (SAS Institute, 2005). Adult beetles were caught in Chiba Prefecture, Survival on the different diets was compared Japan (35°41 N, 140°02 E) in early November with the log-rank test (Pyke and Thompson, 1986), 2006, using pitfall traps baited with silkworm pupa followed by pairwise comparisons with signifi- powder. Five pairs of adults were reared in a plastic cance levels adjusted using Bonferroni correction. box (12.0 12.0 8.5 cm) filled to a depth of In survival analyses of moulting invertebrates, ‘age 4.0 cm with moistened garden soil. Beetles were at death’ could be measured in days and/or devel- fed seeds of Bidens frondosa L. and minced beef. opmental stages. Saska and Jaroˇsík (2001) and Every third day, egg laying was checked, and food Saska (2005) suggested that the measurement of was replaced. developmental stages better reflect the suitability Larval development on different diets. Eggs of a diet than days. In this study, to ensure the va- were transferred to a Petri dish (9.0 cm diameter, lidity of results, ‘age at death’ was measured in 2.0 cm high) lined with moistened filter paper, and both days and developmental stages. Larval Feeding Habit of Amara macronota 671
The duration of development (days) of 1st, 2nd, and 1st 2nd larval instars was determined based on individuals which completed each developmen- tal stage. Among treatments with sufficient sample size (n 5), developmental time was compared using ANOVA after testing for normality (Shapiro- Wilk test) and variance homogeneity (Bartlett’s test) of data sets; if needed, raw data were trans- formed using the Box-Cox method, and adequacy of transformation was confirmed in the same way. Larval morphometry. Habu and Sadanaga (1965) gave morphometric values of all larval in- stars of A. macronota; however, they were dubious about the determination of larval instars because they could not confirm the moulting of all individ- uals (Habu and Sadanaga, 1961, 1965). In most carabids, morphologies of 2nd and 3rd larval in- stars are qualitatively almost identical (e.g., Habu Fig. 1. Survival of Amara macronota larvae on different and Sadanaga, 1961; Luff, 1993); therefore, mor- diets. Numbers in parentheses indicate the initial sample size. phometric values of larval morphology are indis- Different letters indicate statistically significant differences in pensable to distinguish between 2nd and 3rd larval log-rank test calculated as days and instars (small and large instars, particularly when larvae are collected in letters, respectively). the field (e.g., Miyano and Yamaguchi, 1994). In this study, two morphometric values of 2nd and 3rd and they were again not significantly different from larval instars were measured: head width at the the above three treatments. The insect larvae widest point, and circus length. mixed seeds diet had the highest value, and 85% Specimens (underlined individuals in Appendix) larvae reached the 3rd instar. preserved in 70% ethanol were photographed using The durations of 1st, 2nd, and 1st 2nd larval in- a CCD camera attached to a binocular microscope. stars were 19.28–34.50, 14.50–27.00, 35.53–51.00 Measurements were performed using the software days, respectively (Table 1). In all cases, the dura- package NIH image on a personal computer (near tion was markedly longer on Setaria spp. seeds, al- 0.01 mm). though it could not be statistically compared due to the small sample size. Developmental time was compared among the four diets in the 1st instar (in- RESULTS sect larvae mixed seeds, insect larvae, mixed Larval development on different diets seeds and B. frondosa seeds), and between two Survival was significantly different between diets in 2nd and 1st 2nd instars (insect treatments, and the results calculated in days and larvae mixed seeds, and insect larvae). In all instars were almost identical (Fig. 1; log-rank test, cases, there was no significant difference (ANOVA, p 0.01 in both cases). Survival was lowest on S. p 0.05). altissima seeds, and no larvae reached the 2nd in- star. With B. frondosa seeds, no larvae survived be- Larval morphometry yond the 2nd instar. Of the remaining treatments, Table 2 shows the measurement results. These Setaria spp. seeds had the lowest value, and only figures are almost the same as those of Habu and one larva reached the 3rd instar. These three treat- Sadanaga (1965). In both characteristics, measure- ments were not significantly different in the results ments did not overlap between two instars, indicat- calculated for both days and instars. In the mixed ing that morphometric values of these characteris- seeds and insect larvae diets, 10 and 40% larvae tics are useful in determining field-collected larvae. moulted to the 3rd instar, respectively. These two diets did not show significantly different results, 672 K. SASAKAWA
Table1. Duration of developmental time (mean SD (n) [days])
Developmental stageb Dieta 1st instar 2nd instar 1st 2nd instars
Insect larvae mixed seeds 19.28 4.48 (18) 16.00 3.06 (17) 35.53 5.67 (17) Insect larvae 20.30 4.57 (10) 16.38 3.62 (8) 37.00 7.33 (8) Mixed seeds 21.00 2.45 (7) 14.50 4.95 (2) 38.50 4.95 (2) Setaria spp. 34.50 14.85 (2) 27.00 (1) 51.00 (1) Bidens frondosa 21.80 2.86 (5) — —
a No larvae fed Solidago altissima seeds reached the 2nd instar. b Not significantly different in all cases (ANOVA: p 0.05).
Table2. Morphometric values of 2nd and 3rd instar larvae of the species diversity of the genus, and several (mean SD (min–max) [mm]) similar-sized A. (Amara s. str.) species are known to sympatrically occur in most Holarctic regions Larval Measured parts instar (Tanaka, 1985; Trautner and Geigenmüller, 1987; ° (n) Head width Circus length Lindroth, 1988; Hurka, 1996; Ball and Bousquet, 2001; Hieke, 2003). Considering these facts, it is 2nd (13) 1.48 0.09 (1.33–1.63) 0.78 0.06 (0.70–0.87) possible that niche differentiation concerning larval 3rd (12) 1.94 0.05 (1.83–2.01) 1.03 0.06 (0.96–1.15) food resources facilitates speciation of the genus and species coexistence of related species at a given locality. Future studies on the larval feeding habits of more species and species phylogeny DISCUSSION based on reliable data (e.g., molecular sequence Larval feeding habits of the genus Amara data) could provide insights into this hypothesis. Survival was highest on insect larvae mixed seeds (85%), followed by insect larvae (40%). Feeding ecology of A. macronota larvae Seeds had a low value. Even in mixed seeds, which In rearing A. macronota larvae, some individuals showed the highest survival of the seed diets, the continued to develop during midwinter (January) survival rate was 10%. Moreover, no larvae without showing an inactive phase (Appendix). reached the 3rd instar in the two seed diets. These Previous studies also reported that larvae reached results suggest that A. macronota larvae are omni- the 3rd instar from February to March (Habu and vores with a tendency toward carnivory. Saska Sadanaga, 1965). This suggests that, even during (2005) examined the larval feeding habits of two midwinter, A. macronota larvae sufficiently feed consubgeneric species A. aulica (Panzer) and A. and continue to develop. In Carabidae, larval feed- convexiuscula (Marsham), and concluded that the ing during winter has been already reported, and former and latter are, respectively, granivorous and they could be divided into two types, one repre- omnivorous. Thus, of three A. (Curtonotus) species sented by Harpalus (Plectralidus, Pseudoophonus, examined to date, two show larval omnivory. On etc.) spp., the larvae of which are granivores and the other hand, in the subgenus Amara, most eat seeds stored in their burrow (Kirk, 1972; species show either carnivory (e.g., Hu° rka, 1998; Jørgensen and Toft, 1997b), and another repre- Hu° rka and Jaroˇsík, 2001) or granivory (e.g., sented by various species of Nebria and Carabus, Jørgensen and Toft, 1997a; Saska and Jaroˇsík, the larvae of which are carnivores and forage ac- 2001; Fawki and Toft, 2005; Sasakawa unpublished tively (Nelemans, 1986, 1988; Betz, 1992). Larvae data) with the exception of omnivory in some of A. macronota might be categorized into the lat- species (e.g., Saska and Jaroˇsík, 2001; Hu° rka and ter type, because animal materials (here, insect lar- Jaroˇsík, 2003). According to recent taxonomic vae), which are essential for complete develop- studies, the subgenus Amara is the largest group, ment, are thought to be unsuitable for long-term accounting for 33% (168 of roughly 520 species) storage, even during winter (Jørgensen and Toft, Larval Feeding Habit of Amara macronota 673
1997b). To confirm this, the mark and recapture publics. Kabourek, Zlin. 565 pp. method, which Nelemans (1986, 1988) and Betz Hu° rka, K. (1998) Larval taxonomy, development and diet of (1992) could successfully apply to carabid larvae, Amara (Amara) famelica, A. (A.) littorea and A. (A.) prox- ima (Coleoptera: Carabidae: Amarina). Acta Soc. Zool. would be useful. Bohem. 62: 105–113. Hu° rka, K. and V. Jaroˇsík (2001) Development, breeding type ACKNOWLEDGEMENTS and diet of members of the Amara communis species I thank Dr. V. Jaroˇsík (Charles University, Czech Republic) aggregate (Coleoptera: Carabidae). Acta Soc. Zool. and Mr. S. Niwa (Yokohama National University, Yokohama, Bohem. 65: 17–23. ° Japan) for the literature, Mr. T. Kagaya and Dr. K. Kubota Hurka, K. and V. Jaroˇsík (2003) Larval omnivory in Amara (The University of Tokyo, Tokyo, Japan) for their suggestions aenea (Coleoptera: Carabidae). Eur. J. Entomol. 100: on statistical analyses, and Dr. H. Yamashita (The University 329–335. of Tokyo, Tokyo, Japan) for supplying experimental instru- Ishitani, M. (1996) Ecological studies on ground beetles ments. (Coleoptera: Carabidae, Brachinidae) as environmental indicators. Mis. Rep. Hiwa Mus. Nat. Hist. 34: 1–110 REFERENCES (in Japanese with English summary). Johnson, N. E. and R. S. Cameron (1969) Phytophagous Ball, G. E. and Y. Bousquet (2001) Carabidae Latreille, ground beetles. Ann. Entomol. Soc. Am. 62: 909–914. 1810. In American Beetles. Vol. 1. Archostemata, Myx- Jørgensen, H. B. and S. Toft (1997a) Role of granivory and ophaga, Adephaga, Polyphaga: Staphyliniformia (R. H. insectivory in the life cycle of the carabid beetle Amara Arnett and M. C. Thomas eds.). CRC Press, New York, similata. Ecol. Entomol. 22: 7–15. pp. 32–132. Jørgensen, H. B. and S. Toft (1997b) Food preference, diet Betz, J. O. 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food requirements in nine species of Amara (Coleoptera: 029/61117(61130)/-/-, 030/61120(61201)/-/-. Carabidae). Plant Protect. Sci. 37: 103–110. Setaria spp. seeds: 031/61125/70109(70121)/-, Tanaka, K. (1985) Carabidae (Pterostichinae, Zabrinae). In 032/61125/61219/70115, 033/61129(61228)/-/-, The Coleoptera of Japan in Color. Vol. II (S. Ueno, Y. Kurosawa and M. Satô eds.). Hoikusha, Osaka, pp. 034/61125(61229)/-/-, 035/61129(61224)/-/-, 105–138 (in Japanese). 036/61117(61212)/-/-, 037/61125(61215)/-/-, Thiele, H. U. (1977) Carabid Beetles in Their Environments. 038/61129(61216)/-/-, 039/61129(61218)/-/-, Springer, Berlin. 369 pp. 040/61129(61213)/-/-, 041/61117(61210)/-/-, Trautner, J. and K. Geigenmüller (1987) Tiger Beetles, 042/61117(61207)/-/-, 043/61125(61206)/-/-, Ground Beetles, Illustrated Key to the Cicindelidae and Carabidae of Europe. Josef Margraf Publisher, Aichtal. 044/61117(61208)/-/-, 045/61117(61201)/-/-. 488 pp. Mixed seeds: 046/61203(70123)/-/-, Yamazaki, K., S. Sugiura and K. Kawamura (1999) Over- 047/061203(70117)/-/-, 048/61128/61222/70109, wintering ground beetle assemblages along the Kizu 049/61127/61218(70108)/-, 050/61128(70101)/-/-, River, Kyoto. Entomol. Sci. 2: 33–40. 051/61120/61214/61225, 052/61127(61225)/-/-, 053/61127(61226)/-/-, 054/61126/61214(61225)/-, 055/61123/61211(70105)/-, 056/61126/61217(61226)/-, APPENDIX 057/61203(61225)/-/-, 058/61123(70107)/-/-, Data on rearing larvae 059/61119(61225)/-/-, 060/61123(61221)/-/-, Data indicate ‘sample number/hatch date/moult 061/61123(1215)/-/-, 062/61119/61210(61215)/-, date to the 2nd instar/moult date to the 3rd instar’. 063/61119(61212)/-/-, 064/61123(61220)/-/-, If larvae died before moulting to the 2nd or 3rd in- 065/61119(61222)/-/-. star, the death date was recorded in parentheses, Insect larvae: 066/61125/61225/70110, and subsequent developmental stages are marked 067/61127/61216/61230, 068/61117/61213/70105, with a hyphen ‘-’. The first three digits of the sam- 069/61116/61201/61220, 070/61125/61213/61226, ple number (i.e., aa0---) and date (i.e., 200-----) 071/61120/61206/61220, 072/61120/61209/61222, were omitted. Underlined specimens were used for 073/61201(70103)/-/-, 074/61201(61231)/-/-, larval morphometry (Table 2). All specimens are 075/61116/61208/61227, 076/61127(61225)/-/-, deposited in the author’s collection. 077/61125/61214(61224)/-, 078/61116/61205(61215)/-, Solidago altissima seeds: 001/61130(70111)/-/-, 079/61125(61217)/-/-, 080/61125(61222)/-/-, 002/61201(70110)/-/-, 003/61201(70101)/-/-, 081/61127(61218)/-/-, 082/61117(61207)/-/-, 004/61201(70105)/-/-, 005/61124(61224)/-/-, 083/61120(61205)/-/-, 084/61120(61203)/-/-, 006/61124(61215)/-/-, 007/61130(61217)/-/-, 085/61120(61205)/-/-. 008/61124(61209)/-/-, 009/61121(61208)/-/-, Insect larvae mixed seeds: 086/61128/61227/70114, 010/61121(61207)/-/-, 011/61119(61206)/-/-, 087/61125/61209/61221, 088/61128/61227/70112, 012/61119(61201)/-/-, 013/61119(61203)/-/-, 089/61126/61211(70112)/-, 090/61128/61222/70110, 014/61119(61205)/-/-, 015/61119(61203)/-/-. 091/61126/61216/70102, 092/61123/61208/61229, Bidens frondosa seeds: 016/61116/61211(61229)/-, 093/61124/61211/61229, 094/61125/61214/61229, 017/61120/61210(70102)/-, 018/61120(61224)/-/-, 095/61126/61214/61228, 096/61128/61218/61231, 019/61117/61211(61218)/-, 020/61120(61217)/-/-, 097/61126/61215/61228, 098/61125/61211/61226, 021/61129(61220)/-/-, 022/61129(61221)/-/-, 099/61128/61215/70107, 100/61126/61210/61225, 023/61129(61213)/-/-, 024/61129(61219)/-/-, 101/61125/61214/61230, 102/61126/61215/61227, 025/61129(61218)/-/-, 026/61120/61208(61220)/-, 103/61127/61220/70104, 104/61127(61226)/-/-, 027/61116(61213)/-/-, 028/61116/61208(61213)/-, 105/61126(61210)/-/-.