Jpn. Jpn. J Environ 寸 Entomo l. Zoo l. 22 (2) : 93 - 98 (2011) 環動昆第22 巻第2号: 93 - 98 (2011) 顕著

Impact of the invasive crayfish Procambarus clarkii on the giant water bug Kirka 幼lia deyrolli () in rice ecosystems

Shin ぅTa Ohba

Center Center for Ecological Research ，Kyoto University ，Otsu 520-2113 ， ]apan

(Received (Received : February 28 ， 2011 ; Accepted : April14 ， 2011)

Abstract

The invasive crayfish species ， Procambarus clarkii (Decapoda: Cambaridae) has had a serious impact on native Odonata species and rare diving beetle species in ]apan. However ，little scienti 五 c attention has been focused on their impact impact on aquatic Hemiptera. The present study examined the impact of the invasive crayfish p. clarkii on the giant water water bug Kirkaldyia (=) deyrolli (Hemiptera: ) in rice ecosystems. The survival rate of K. dのrolli nymphs in rice fields inhabited by the crayfish was clearly lower than that in rice fields where the crayfish was absen t. To examin 巴 the predation of p. clarkii ，two treatments were set up in laboratory conditions: with and without without crayfish. The survival rate of the K. deyrolli nymphs in the with crayfish group was significantly lower than that that in the without crayfish group due to predation. The crayfish have become common pets aquatic for ]apanese people. people. Therefore ，educational programs concerning the impact and removal of invasive crayfish are recommended for for conservation and the restoration of the fauna in such a habitat inhabited by rare aquatic such as K. deyrolli.

Key words : Aquatic insec t， Heteroptera ，Invasive species ，Red swamp crayfish ， Rice field

Introduction Introduction have reported on the serious impact that P. clarkii have had on the native Odonata species (Fukui ， 2010 ; It It is broadly accepted that non-indigenous species Karube ， 2010) and rare diving beetle species often often affect other species ， communities ， and (Nishihara et al. ， 2006 ; Nishihara ，2010). However ，little ecosystems ecosystems and can exacerbate the negative e妊ects of scientific attention has focused on their impact on both both global climatic warming and other anthropogenic aquatic Hemiptera. sources sources of disturbance (Lodge ， 1993 ; Lodge et al. ， Species of the Belostomatidae (Hemiptera) subfamily 2006). 2006). The red swamp crayfish ，Procambarus clarkii Lethocerinae are cosmopolitan and live in freshwater (Girard) (Girard) (Decapoda: Cambaridae) ， is a freshwater habitats such as ponds ，lakes ，and rivers (Perez crayfish crayfish species that is native to the southeastern Goodwyn ， 2006). The giant water bug ， Kirkaldyia United United States ， but it is also found on other continents ， (=Lethocerus) deyrolli (Vuillefroy) ， is distributed where it is often an invasive pes t. In ]apan ， P. clarkia throughout ]apan from central Honshu to the Ryukyu were introduced from North America during the Islands. Rice fields are an important habitat for K. period period from 1920-1930 ，and the species' distribution deyrolli (Mukai et al. ，2005 ; Ohba et al. ，2008) expanded throughout ]apan until 1980 (Ban ，1980 ， 豆owever ，]apanese populations of K. deyrolli have 2002) 2002) . decreased sharply during the last four decades and are Procambarus clarkii are omnivorous and threaten considered to be a threatened-vulnerable species in the aquatic aquatic plants ， ，shellfish ，and aquatic Red Data Book of Japan (J apan Environment Ag 巴ncy ， insects insects by direct and indirect competition (Gutierrez- 2000). Contributing factors ，such as decreasing Yurrita Yurrita et al. ，1998 ; Smart et al. ，2002 ; Gherardi ， numbers of suitable aquatic habitats ， water pollution ， 2006 2006 ; Takeuchi et al. ， 2011). In ]apan ， researchers pesticide application ，and increased street lighting due

Corresponding Corresponding author : [email protected]

-93 一 Shin-ya Shin-ya Ohba

to to urbanization are of great concern (Ono ，1995 ; mm ; third instar ， 22 - 25 mm ; fourth inst 訂， 31 37 mm ; Japan Environmεnt Agency ，2000 ; Hirai & Inatani ， and fifth instar ，45 - 53 mm. After their capture and 2006 ; Y oon et al. ， 2010). Howεver ， there have been no measuremen t， the nymphs were releasεd carefu 日y at studies studies of the impact of invasive crayfish on K. deyrolli. their point of capture.

In In the present study ， our objective was to compare the The Kiritani 悶 Nakasuji-Manly method (Kiritani & survival survival rate of K. deyrolli nymphs between those Nakasuji ， 1967 ; Manly ， 1976) was used to assess the inhabiting inhabiting rice fields that had been invaded by P. frequency of each stage on a series of census clarkii clarkii and those living in non-invaded rice fields in a occasions. Supposing that the ith stage was observed laboratory laboratory experiment in order to evaluate the effects for a time period in which n samples were collected of of P. clarkii on K. deyrolli. with varying time intervals between their collection and that the samples were taken at intervals (hl ， Materials Materials and Methods h2 ・ー)， the area under the frequency trend curve was estimated estimated by the trapezoidal rule : Survival Survival and aquatic predators and prey of K. deyrolli for area Ai :

To investigate the survival of K. deyrolli nymphs ， Ai = 1/2 2: (h L 十 hL+ l) /;L

field field surveys were conducted in water paths where /;L = the number of the It h instar estimated from

connecting rice fields (“ ditches") in northern the samples taken on the Lth occasion ，which was at

Okayama and northwest Hyogo from 1 June to 5 the end of sampling interval h L. There were hL+l August in 2004. P. clarkii had invaded the rice fields in sampling intervals ，and the last interval extended from northern northern Okayama but not those in northwest Hyogo. the last occasion when the stage was present to the Hereafter ， northern Okayama and northwest Hyogo next sampling occasion (when it was found to be are are referred to as the crayfish and no crayfish area ， absent) (Manly ， 1976). respectively. respectively. Three ditches at each study site (no To evaluate the frequencies of tadpoles ， native

crayfish crayfish area : site A : 99.8 x 0.3 m ，B : 62.3 x 0.3 m ， aquatic predators of K. deyrolli nymphs ，and invasive and C : 89.3 x 0.5 m ; crayfish area :D : 35 .4 x 0.3 m ， crayfish ， 1 calculated their relative abundances during E : 37.8 x 0.3 m ，and F : 44 .4 x 0.5 m) were used as the daytime (1 200 - 1700 hours) _A 与mm-mesh D frame census census plots in order to investigate the frequencies of dipnet (28 cm wide) was pulled 20 times for 50 cm K. K. deyrolli and its prey and predators. To measure the along the bottom of the rice field at each site. After number of K. deyrolli present in the ditches ，1 being counted ，all samples were immediately released

conducted conducted censuses along the ridges around the rice back into the ditch. Based on prεVi Olユ s studies (Ohba ， fields fields at intervals of 5 -10 days during the study 2007 ; Ohba and Swar t， 2009) ，Laccotrephes

period. period. They were performed by visual observation of adults and Appasus jα~ponicus adults wer 記 K. K. deyrolli at night using a flashlight (11， 000 lx) from aquatic predators of K. nymphs.

2000 to 0100 hours. Primarily a nocturnal ， K. The survival of K. nymphs and the numb 釘 's deyrolli deyrolli ambush their prey on the water surface after of tadpoles or native aquatic predators were comparεd sunse t. Flashlight illumination does not interfere with using a repeated-measures one-way ANOV A， with

the the foraging behavior of K. deyrolli because they do not locality (cray 五sh or no crayfish area) as the between 問 stop stop fεeding or ambushing their prey ，even in strong subject factor and nymphal stage (first- 師th instar) or

light light (S. Ohba ，unpub l. data). For dirεct observation ， day as the within 引 lbject facto r. Where necessary タ

the the observer maintained a constant distance from the 10g lO transformation or arcsine 司 squ 紅白-root transformation water surface (ca. 0.3 m) and a constant pace (3 m of exact values was performed to standardize variances

min - I walking speed). To maintain sampling and improve normality ，in order to satisfy the assumptions consistency ，sampling was not conducted during of the ANOV A mode l. periods periods of rain. 1 caught K. deyrolli nymphs using a 500 1m mesh dipnet (0 .1 5 m x 0.10 m mouth opening) Predation of K. deyrolli by crayfish and measured their body length with calipers. The To examine the predation of K. deyrolli by P. clarkii ， nymphs were assigned to instars based on data two treatments wεre set up : with and without obtained obtained from rearing experiments (Ohba ， 2008) as crayfish. The experiment was conducted in an follows follows : first instar ， 11 - 12 mm ; second instar ， 15 - 18 aquarium (175 x 300 mm mouth opening ，210 mm height)

94 Impact of an invasive crayfish on the giant water bugs

maintained 試呂 water temperature of 25.5-31.0 oC in experiments were completed within a week of capture. July July 2010. Dεchlorinated tap water was addεd to a The K. deyrolli nymph survival rate was calculated depth depth of 100 凹. A stick (1 5 mm diameter ， 150 mm long) by dividing the number of individuals surviving at the

and three Myriophyllum spp 目 water plants were end of the experiment by the initial number of supplied supplied as perches. Five Rana limnocharis tadpoles ，5 individuals. The Mann-Whitney U test was used to first first instar nymphs of K. deyrolli ，and 1 P. clarkii compare the survival rate between the with and (40 .2 6 :t 0.12 mm ，mean shelllength 士 SE ，n = 5) were without crayfish groups. Statistical significance was set introduced introduced into the aquariu m. Half an hour before the at 0.05. beginning beginning of the experimen t. the were added to to the aquarium and allowed to acclimate. The number Results of of surviving K. deyrolli nymphs was counted at 24 hours after the beginning of the experiment. Five Seasonal changes in the frequency of the K. deyrolli replicates replicates were performed. All study animals ， are shown in Fig. 1. First-instar nymphs appeared in excluding excluding the 1st instar K. deyrolli nymphs ，were two areas from June to mid-July. From June to July ， collected collected from rice fields 200 m away from the crayfish second and third-instar nymphs appeared and area area in northern Okayama in July 2010. R. limnocharis developed at two study sites as the season progressed. tadpoles tadpoles at Gosner stage 35 - 40 (Gosner ， 1960) were From late June to Augus t. fourth and fifth-instar used used as the prey. Adult K. deyrolli were collected from nymphs appeared. Newly emerged adults appeared rice rice fields in northwest Hyogo ，and their hatchlings from mid-July to August at sites A D ，E ，and F. No (as (as first instars) were used in the experimen t. All new adults appeared at site B or C. The survival rate animals were returned to the laboratory and of K. deyrolli nymphs in the no crayfish area tended to maintained maintained individually in plastic cups until testing. All be higher than that in the crayfish area (Fig. 2). A

Okayama (crayfish a 開 a) ト1yogo (no c間同sha 階特 ;;叫LLJ~-.-LLL :;ム LLL k_li: ijJ; ムLLLu_J_{~W 1~~LL LL-J-;:' ;;ーLLLLL~' ;;巴 LLL L. LJ

Fig. Fig. 1 Seasonal changes in the frequency of Kirkaldyia deyrolli at six sites within two areas. For K. deyrolli adult ， the OW and NE indicate overwintered adults and the newly emerged adults ，respectively.

-95 一 Shin-ya Shin-ya Ohba

repeated 回 measures one-way ANOV A revealed that in the without crayfish group (Mann-Whitney U-test :

locality locality and nymphal stage were significant factors u= 25 ，P く 0.001 ; Fig 圃 3) .

(locality (locality : Fl ，4 =27.0 ， P=0.006 ， nymphal stage :

F 4，l 6=43 .4 6，P く 0.001) but the locality ゐy-nymphal stage Discussion

interaction interaction was not significant (F 4，l 6= 1. 34 ，P=0.298). The numbers of tadpoles in the crayfish and no The present study examined the impact of the crayfish crayfish areas were not significantly different. A invasive Procambarus clarkii crayfish on the giant water repeated-measures repeated-measures one-way ANOV A revealed that bug in rice ecosystems. The survival rate of K. deyrolli

day was a significant factor (F 札32=7 .4 4，P く 0.001) but nymphs in the crayfish area was clearly lower than locality locality and the day-by-locality interaction was not that in the no crayfish area (Fig. 1 and 2). Generally ，

significant significant (l ocality: F l， 4=2.54 ，P=0.19 ，day X locality survival rate is decreased by not only bottom 同 up but

interaction interaction : FS ，32= 1. 99 ， P=0.08). The mean number of also top-down effects. In the present study ， the low crayfish crayfish in the crayfish area was > 1 throughout the survival rate in the crayfish area was not caused by study period (min : 1. 0，max : 3.0). Laccotrephes food shortages because there was no difference in food japonensis ， the main predator of K. deyrolli nymphs ， resources between the two areas. Therefore ， top-down were found in the no crayfish area (mean: 1. 03 ，min : effects mediated by predators can be used to explain 0，max : 6.7) but no L. japonensis were found in the the low survival rate of K. deyrolli nymphs in the crayfish crayfish area (no statistical analysis was performed crayfish area. Previous studies showed that the aquatic because because all data were 0 in the crayfish area). With Hemiptera Laccotrephes japonensis and Appasus japonicus regards to the other predators of K. deyrolli ， the are native predators of K. deyrolli in rice fields (Ohba ， number of Appasus j α:ponicus was not significantly 2007; Ohba and Swar t， 2009). As no L. japonensis were di 妊erent between the crayfish and no crayfish areas. A found in the crayfish area and the numbers of A. repeated-measures one-way ANOV A showed that japonicus were similar between the crayfish and no

locality ，day ，and the locality-by-day interaction were crayfish areas ，top 四 down effects due to native aquatic

not not significant (locality: F l， 4=0.029 ，P=0.873 ，day : Fs ， Hemiptera are not considered to have reduced the

32=0.125 ，P=0.125 ，locality 回 by 同 day : Fs ，32=0 .4 52 ，P= survival rate of K. deyrolli in the crayfish area. 0.880) 0.880) . Therefore ，it is suggested that predation on K. deyrolli Predation Predation on the K. deyrolli nymphs by the crayfish by crayfish was the main factor reducing K. deyrolli was confirmed in the laboratory experiment. The numbers in the crayfish area.

mean survival rate of the K. deyrolli nymphs in the To ver ・ify the impact of crayfish on K. deyrolli

with with crayfish group was significantly lower than that nymphs ，a laboratory exp 巴riment was carried out

1.01 口No crayfish area E ・Crayfish area 100 ~.~ 1 ~""9、、 号80 百~ 0.61 ~'，仏》、、 !... 布 60 〉 i04 、、 、、口 540 0.2 (J) 20 0.0 0 1 st 2nd 3rd 4th 5th With crayfish Without crayfish Nymphal stage

Fig. Fig. 2 Comparison of survival rates in the Fig. 3 Comparison of the survival rate of K. deyrolli crayfish crayfish and no crayfish areas. Mean :t SE nymphs in the laboratory experimen t. Columns (n (n = 3). show the median + inter-quartile values. ア< 0.05 ， Mann-Whitney U test

-96 一 Impact of an invasive crayfish on the giant water bugs

Most of K. deyrolli nymphs had been eaten by the angelina in Okeganuma area ， Iwata City ， pp. 135- crayfish crayfish after 24h (Fig. 3). Although this result was 142. ln M. Ishii [ed.] ， Decline of the J apanese produced in a simple laboratory experimen t， the insects and the protection. Hokuryukan ， Tokyo. conditions conditions were set according to observations made in [In J apanese] the the wild ，and so it is suggested that crayfish eat most Gherardi ， F. (2006) Crayfish invading Europe : the K. K. deyrolli in wild conditions. 1n Japan ， researchers case study of Procambarus cl αrkii. Mar. Freshwat. have indicated that invasive crayfish have had a Behav. Physiol. 39 : 175 - 191. serious serious impact on native Odonata species (Karube ， Gosner ， K. (1 960) A simplified table for staging 2010; 2010; Fukui ， 2010) and rare diving beetle species anuran embryos and larvae with notes on (Nishihara (Nishihara et al. ， 2006 ; Nishihara ， 2010). As far as 1 identification. Herpetologica 16 : 183 -190.

know ， the present study is the first study to Gutierrez 悶 Yurrita ，P. ，Sancho ，G. ，Bravo ， M.， Baltanas ， demonstrate the serious impact which invasive A.， and Montes ，C (1998) Diet of the red swamp crayfish crayfish have on aquatic Hemiptera. crayfish Procambarus clarkii in natural ecosystems

Red swamp crayfish P. clarkii are introduced into of the Donana National Park temporary fresh 問

Japan Japan during the period from 1920-1930 as foodstuff for water marsh (Spain). J. Crustacean Biol. 18: 120 目 peoples peoples and prey animals for introduced American 127. bullfrog bullfrog Rana catesbeiana Shaw ，and then are released Hirai ，T. ，and Y. Inatani (2006) Protection of thε as as educational materials uncritically (Ban ，1985 ，2002). endangered giant water bug Lethocerus deyrolli Crayfish Crayfish have also been becoming common aquatic from overcollecting: 1s it effective to replace a pets pets for Japanese people (Ban ， 2002). The impact mercury vapor light with a high-pressure natrium invasive invasive crayfish have on Japanese ecosystems is light? Bul l. Kansai Organization for Nature poorly poorly understood (Ban ，2002). Therefore ，an educational Conservation 28 : 59 - 62. [1n J apanese] program concerning the impact and removal of Japan Environment Agency (2000) Threatened invasive invasive crayfish is recommended to aid conservation Wildlife of Japan. Red Data Book. 2nd ed and the restoration of the fauna in such a habitat Environment Agency of Japan. Tokyo. [I n inhabited inhabited by rare aquatic insects such as K. deyrolli. JapaneseJ Karube ， H. (2010) Decline of the Japanese dragonfly Acknowledgements and the protection ， pp. 53 - 67. ln M. [ed.] 1shii ， Decline Decline of the J apanese and the protection. 1 wish to express my appreciation to Yoshinori 日okuryukan ， Tokyo. [In JapaneseJ Inatani Inatani of Higashi-Matsuyama Nature Club for his Kiritani ，K.， and F. Nakasuji (1967) Estimation of the valuable valuable suggestions. 1 would also like to thank Naoki stage-specific survival rate in the insect Sonoda and Yuri Ohba for their assistance during this with overlapping stages. Res. Popul. Ecol. 9: 143

study. study. This study was supported in part by a Gran 国 in 同 152. Aid for JSPS Fellows (22-4) Lodge ， D. (1993) Biological invasions: lessons for ecology. ecology. TREE 8: 133 - 137. References Lodge ，D. ， S. Williams ， H. Mac1saac ， K. Hayes ， B. Leung ，S. Reichard ， R. Mac k， P. Moyle ，M. Smith ， Ban ， Y. (1980) Crayfish Procambarus clarki - Key of and D. Andow (2006) Biological invasions : invasion invasion success ， pp. 37 43. ln T. Kawai ， H， recommendations for US policy and managemen t. Kawanabe ，and N 悶 izuno [eds.] ，Freshwater Ecol. Appl. 16 : 2035 - 2054. biology biology in Japan -Ecology of 1nvasion and Manly ， B. F. J. (1976) Extensions to Kiritani and disturbance ，Tokai University Press ， Tokyo. [1n Nakasuji' s method for analysing insect stage- JapaneseJ JapaneseJ frequency data. Res. Popul. Ecol. 17 : 191 - 199 Ban ， Y. (2002) Crayfish Procambarus clarki. ， pp. 169. ln Mukai ，Y. ， N. Baba ，and M. Ishii (2005) The water The Ecological Society of Japan [ed.] ，Handbook system of traditional rice paddies as an important of of alien species in Japan ，Chijin Shoin ， Tokyo. [1n habitat of the giant water bug ， Lethocerus deyrollei JapaneseJ JapaneseJ (Heteroptera: Belostomatidae). J. lnsect Conserv. Fukui ，M. (2010) Protection activity of Libellul α 9: 121 129.

97- Shin.ya Shin.ya Ohba

Nishihara ， S. (2010) Exclusion methods in invasivε Ono ， Y. Influence of high pressure mercury 司 alien alien species in watεrside ， pp. 179 - 200. ln I. vapour lamps on some insects ，with Washitan i， T. Miyashita ，J. Nishihiro and T reference to the oriental giant water bug ， Kadoya [eds .J， Methods in Conservation Ecology. Lethocerus deyrollei ，and hark moths ，Sphingidae ， Tokyo University Press ， Tokyo. [In JapaneseJ Lepidoptera. Artes Li berales 57 : 155 - 166. [In Nishihara ，S. ， H. Karube ，and 1. Washitani (2006) Japanese with English AbstractJ Status and conservation of diving beetles Perez Goodwyn ， P. (2006) Taxonomic revision of the inhabiting inhabiting rice paddies. Jpn よ Conserv. Ecol. 11 : subfamily Lethocerinae Lauck & Menke 143 143 -157. (Heteroptera : Belostomatidae). Stuttgarter Beitr. Ohba ， S. (2007) Notes on predators and their effect Naturk ， 695 (A) : 1 -71 on the survivorship of the endangered giant Smar t， A.， D. Harper ， F. Malaisse ，S. Schmitz ， S. Coley ，

water bug ，Kirkaldyia (=Lethocerus) deyrolli and A. Gouder ・ de Beauregard (2002) Feeding of (Heteroptera ，Belostomatidae) ， in J apanese rice the exotic Louisiana red swamp crayfish ， 五elds. Hydrobiologia 583 : 377 - 38 1. Procambarus clarkii (Crustacea ，Decapoda) ， in an Ohba ，S. (2008) The number of tadpoles consumed by African tropical lake : Lake Naivasha ，Kenya the the nymphs of the giant water bug Kirkaldyia Hydrobiologia 488 : 129 -142. deyrolli deyrolli under laboratory conditions. Limnology 9: Takeuchi ，T. ， J. lnagaki ，and Y. Yokoyama (2011) 71-73. Effect of the exotic crayfish Procambarus clarkii on Ohba ，S. ， H. Miyasaka ，and F. Nakasuji (2008) The larval survival of the salamander Hynobius role role of prey in the diet and growth of tokyoensis. Jpn. J. Environ. Entomol. Zool. 22 : 33 - 37.

giant giant water bug nymphs in J apanese rice fields. Yoon ，T. ， D. Kim ， S. Kim ，S 目 Jo ，and Y. Bae (2010) Popul. Popul. Ecol. 50 :9- 16. Light-attraction flight of the giant water bug ， Ohba ，S. ，and C. C. Swart (2009) Intraguild predation Lethocerus deyrolli (Hemiptera: Belostomatidae) ， of of water scorpion La ccotrephes japonensis (N epidae : an endangered wetland insect in East Asia. Heteroptera) Heteroptera) .Ecol. Res. 24 : 1207 - 12 11. Aquatic lnsects 32 : 195 - 203

水田生態系におけるアメリカザリガニの夕方、メへの影響

大庭伸也

京都大学生態学研究センター 〒520-2113 滋賀県大津市平野2丁目 509-3

アメリカザリガニ Procambarus clarkii (Girard ，1852) は在来のトンボ類や希少ゲンゴロウ類に重大な影響を及ぼすこ とが知られているが，水生カメムシ類への影響に関する定量的な調査はなされていない.本研究では，水田生態系にお

いてアメリカザリガニのタガメ Kir. 如 ldyia (= Lethocerus) 正leyrolli (Vuillefroy ，1864) に対する影響を野外調査と室内実 験にて評価した.アメリカザリガニが侵入した水田地帯ではタガメ幼虫の推定生存率は，侵入していない水田地帯に比 べて有意に低かった.次に，アメリカザリガニによる捕食の有無を調べるため，アメリカザリガニ在ー不在区を室内条件 下で設置し，それぞれにタガメ幼虫を導入してタガメ幼虫の生存率を調べた，その結果，アメリカザリガニ在区では， アメリカザリガニの捕食によりタガメ幼虫の生存率が不在区に比べて(有意に)低かった.アメリカザリガニは現在で は日本人にとって身近な生物とみなされる場合もあるが，タガメの様な局所的に分布する希少水生見虫類への影響を考 躍すると，そのような希少な水生昆虫類が生息する環境ではヲ駆除などの早急な対策を講じる必要がある.

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