HERBIVORE-INDUCED RICE GRAIN VOLATILES AFFECT ATTRACTION BEHAVIOR OF HERBIVORE ENEMIES QingFeng Tang, TianSheng Yang and JunQi Jiang

SUMMARY

The responses of female Lariophagus distinguendus (Hy- vae damaged grains. Further experiments revealed the expe- menoptera: ) to volatile signals derived from rienced L. distinguendus females were apparently attracted herbivore-induced rice grain was investigated in the static by the odors released from rice induced by the saliva of the four-chamber olfactometer. Results showed that the L. dis- weevil larvae. Moreover, we compared the responses of fe- tinguendus females, irrespective of experience, were appar- male parasitoids to odors released from rice induced by pro- ently attracted by the odors released from rice grain. The tein substances of regurgitant and non-protein substances. active chemicals in the saliva of the maize weevil, Sitophi- The experiments revealed that volatiles attracting parasitoid lus zeamais, that elicit the production of rice volatiles was L. distinguendus are possibly induced by the some protein investigated. Results showed that artificially damaged grains substances from weevil larvae saliva. The effect of experi- do not emit large amounts of volatiles that attract the ex- ence on the response of the parasitoids to several stimuli perienced parasitoid females emitted by the S. zeamais lar- was discussed.

Introduction researchers to evaluate other option is effective in con- particularly for foliage. It is alternative reduced-risk con- trolling pests of stored well documented that carniv- In many parts of the world trol methods for stored-grain products and has a positive orous often use rice is the major component protection (Tang et al., 2009). impact on the quality of volatile chemical cues that are of the diet. Unfortunately, a To resolve the above prob- stored cereal products. These released from the food plants large proportion of the annu- lems, new environmental chemicals that are beneficial of their victims when search- al yield is lost during stor- friendly methods to control for both the carnivores and ing for prey or hosts. By way age, and these losses have the insect damages have be- the plant have been termed of comparison, little is known been partly attributed to in- come of interest to research- ‘herbivore induced syno- about the release of HIS from sect pests resulting in the ers; biological control of mones’ (HIS). Since the first reproductive tissue such as deterioration of the quality pests using parasitoids or description of this interaction rice grain (Tang et al., 2009). and the quantity of stored predators is an example between plants, herbivores The present paper is devoted rice grains (Machado et al., (Scholler et al., 1997). The and carnivores mediated by to a tritrophic system consist- 2008). To protect grains from use of natural enemies such HIS there have been numer- ing of the rice grains (Oryza. the insect damages, tons of as parasitoids for the control ous studies on this phenome- sativa L.), larvae of the maize insecticides have been ap- of stored-product pests has non. There is evidence to sug- weevil Sitophilus zeamais plied to control the pests, been suggested for many gest that HIS can regulate tr- (Coleoptera: Curculionidae) that which have resulted in envi- years (Hase, 1924; Ryabov, itrophic interactions among are endophytic in rice grains, ronmental damages, pest re- 1926). However, little is plants, insect herbivores, and and the pteromalid wasp surgence, pest resistance to known about tritrophic inter- natural enemies of the herbi- Lariophagus distinguendus insecticides, and lethal ef- actions among rice grain, vores (Steinberg et al., 1993; (: Pteromalidae), fects on non-target organ- insect herbivores, and natural Ockroy et al., 2001; Tinzaara an idiobiont ectoparasitoid of isms. Furthermore, because enemies of the herbivores. et al., 2005; Dalessandro beetle larvae, infesting seeds of cost, these pesticides are The use of specific attrac- et al., 2009; Deshpande and and grains. The maize weevil becoming increasingly inac- tants might represent an op- Kainoh, 2012; Peñaflor and S. zeamais is one of the most cessible to farmers, particu- tion to increase the presence Bento, 2013; Desurmont common and destructive stor- larly in developing countries. of the parasitoid wasp in gra- et al., 2015; Yoneya and Miki, age pests of stored cereal This fact, combined with nary or could be coupled with 2015). To date, HIS have been grains in the world. The adult the consumer’s demand for biocontrol programmes to im- demonstrated mostly in the beetles can attack whole residue-free food, prompted prove biocontrol services. The somatic tissue of plants, grains, and eggs are laid

KEYWORDS: / Grain Volatiles / Lariophagus distinguendus / Multitrophic Interaction / Olfactometer Tests / Sitophilus zeamais / Received: 11/26/2015. Modified: 03/31/2016. Accepted: 04/04/2016.

QingFeng Tang. Ph.D., Anhui TianSheng Yang. B.S., AAU, JunQi Jiang. Ph.D., AAU, Protection, AAU. 130# West Agricultural University (AAU), China. Master Degree Candi- China. Professor, AAU, China. Changjiang Road, Hefei China. Professor, AAU, China. date, AAU, China. Address: Department of En- 230036, P. R. China. e-mail: tomology, School of Plant [email protected]

MAY 2016, VOL. 41 Nº 5 0378-1844/14/07/468-08 $ 3.00/0 319 SUSTANCIAS VOLÁTILES DE GRANOS DE ARROZ INDUCIDAS POR HERVÍBOROS AFECTAN LA ATRACCIÓN DE ENEMIGOS HERBÍVOROS QingFeng Tang, TianSheng Yang y JunQi Jiang RESUMEN

En un olfatómetro de cuatro cámaras se estudiaron las res- por las larvas de S. zeamais de granos dañados. Experimen- puestas de hembras de Lariophagus distinguendus (Hymenop- tos adicionales revelaron que las hembras experimentadas de tera: Pteromalidae) a señales volátiles provenientes de granos L. distinguendus eran aparentemente atraídas por los olores de arroz e inducidas por herbívoros. Los resultados mostraron desprendidos de los granos de arroz e inducidos por la saliva que las hembras de L. distinguendus, independientemente de de las larvas de gorgojos. Adicionalmente se compararon las su experiencia, son atraídas por los olores despedidos por los respuestas de los parasitoides hembra a olores emanados del granos de arroz. Se investigaron las sustancias activas presen- arroz inducidas por proteínas del vómito y por sustancias no tes en la saliva del gorgojo del maíz, Sitophilus zeamais, que proteicas. Los experimentos mostraron que los productos vo- inducen la producción de sustancias volátiles en el arroz. Los látiles que atraen los parasitoides de L. distinguendus son in- resultados mostraron que los granos de arroz artificialmente ducidos probablemente por algunas sustancias proteicas de la dañados no emiten cantidades de sustancias volátiles capa- saliva del gorgojo. Se discute el efecto de la experiencia previa ces de atraer a parasitoides hembras experimentadas emitidas en la respuesta de los parasitoides a diversos estímulos.

SUBSTÂNCIAS VOLÁTEIS DE GRAÕS DE ARROZ INDUZIDAS POR HERVÍBOROS AFETAM A ATRAÇÃO DE INIMIGOS HERBÍVOROS QingFeng Tang, TianSheng Yang e JunQi Jiang RESUMO

Em um olfatômetro de quatro câmaras se estudaram as res- zeamais de grãos danificados. Experimentos adicionais revela- postas de fêmeas de Lariophagus distinguendus (Hymenoptera: ram que as fêmeas experimentadas de L. distinguendus eram Pteromalidae) a sinais voláteis provenientes de grãos de arroz aparentemente atraídas pelos odores desprendidos dos grãos e induzidas por herbívoros. Os resultados mostraram que as de arroz e induzidos pela saliva das larvas de gorgulhos. Adi- fêmeas de L. distinguendus, independentemente de sua experi- cionalmente se compararam as respostas dos parasitoides fê- ência, são atraídas pelos odores desprendidos pelos grãos de meas a odores emanados do arroz induzidas por proteínas do arroz. Investigaram-se as substancias ativas, presentes na sa- vômito e por substancias não proteicas. Os experimentos mos- liva do gorgulho do milho, Sitophilus zeamais, que induzem à traram que os produtos voláteis que atraem os parasitoides produção de substâncias voláteis no arroz. Os resultados mos- de L. distinguendus são induzidos provavelmente por algumas traram que os grãos de arroz artificialmente danificados não substâncias proteicas da saliva do gorgulho. Discute-se o efei- emitem quantidades de substâncias voláteis capazes de atrair to da experiência prévia na resposta dos parasitoides a diver- parasitoides fêmeas experimentadas emitidas pelas larvas de S. sos estímulos.

inside kernels in which the volatiles on the taxis behavior relative humidity (r.h.) and a for bioassays larvae feed and develop entire- of L. distinguendus and its photoperiod of L14: D10. To ly and pupate. The oviposition mechanisms. Such research was rear L. distinguendus, 50 newly Parasitoids used in experi- hole is closed with an egg plug of importance to reveal the emerged adult wasps were ments were about 3 days old. (Hill, 1983; Storey, 1987; mechanism of indirect defense placed into Petri dishes (9cm To obtain naive parasitoids for Kouninki et al., 2007). L. dis- of rice grains against larvae of diameter, 1cm high) with ~50g bioassays, freshly emerged male tinguendus has been suggested S. zeamais and, it was also very of rice grains infested by 3rd- and female parasitoids were as a biological control agent important in the understanding 4th instar larvae of S. zeamais collected from the infested against the maize weevil in of the ecological functions of and kept there until their grains within 1h of emergence grain stores. The parasitoid egg herbivore-induced rice grains death. After a developing time and kept in Petri dishes on is laid into the infested grains volatiles. The results would pro- of 19-21 days, parasitoids moistened filter paper in a cli- beside the beetle larva. vide new information to the bi- emerged from the next genera- matic chamber without host Females of L. distinguendus ological control efficiency of tion were collected daily from odors under the same conditions have been reported to locate its parasitic wasp on stored-grain each Petri dish. To rear S. zea- as described above. host by volatiles derived from pests, which represents a tech- mais, 30 adults were allowed To obtain experienced para- infested grain (Steidle and nical support of great demand to oviposit into 300ml of rice sitoid females, recently emerged Scholler, 1997). However, the in green grain storage. grains with about 14% mois- (<24h) wasps were placed into attractiveness mechanisms of ture content in glass jars (8cm Petri dishes containing rice herbivore-induced rice grain Materials and methods diameter, 10cm high). To ob- grains infested by weevil lar- volatiles to parasitoid are still tain unmated males or females vae and imagines of S. zea- unknown. Insect rearing of S. zeamais; adults were sep- mais. Females were allowed to The present study was initiat- arated by dimorphic rostral mate and oviposit for 2 days. ed to elucidate the effects of All insect rearing was car- characteristics within 12h of Subsequently, they were re- herbivore-induced rice grains ried out at 26 ±1ºC, 70 ±5% emergence (Halstead, 1963). moved and kept in Petri dishes

320 MAY 2016, VOL. 41 Nº 5 with moistened filter paper until but to enable observations. Responses of L. distinguendus healthy rice grains. Three dif- they were used in the experi- Behavioral data were visually females to S. zeamais larvae ferent experiments were con- ments on the following day. recorded using a stopwatch. To induced rice grains volatiles ducted using the static avoid biased results due to pos- four-chamber olfactometer to Static four-chamber sible side preferences of the A series of experiments were test the attraction of L. dis- olfactometer parasitoids, the position of the conducted to test the attraction tinguendus females to regurgi- olfactometer was rotated 90º of L. distinguendus females to tant induced rice grains vola- The response of female par- clockwise after every test. herbivore-induced odors emit- tiles: 1) Rice grains (50g) were asitoids to different odor sam- Contamination of the walking ted from rice grains using the infused 2μl of the OR extract ples was examined using a arena with sample odors or by static four-chamber olfactome- vs 50g of grains infused 2μl of static four-chamber olfactome- possible pheromones of the ter descried above. Fifty weevil the BR extract, and two empty ter, as described by Ruther and parasitoids was avoided by larvae infested grains from petri dishes. 2) Grains (50g) Steidle (2000). The olfactome- cleaning the walking arenas which larvae, faeces, and egg infused 2μl of the RP extract ter (Figure 1) was made of and glass plates with ethanol plugs had been removed (in- vs 50g of grains infused 2μl of acrylic and consisted of a cyl- and demineralized water before fested grain only; LIGO) vs 50 RNP extract, and two empty inder (4cm high, 19cm diame- each insect. For all experi- healthy grains, which had been petri dishes. 3) Rice grains ter) divided by vertical plates ments, odor samples were re- artificially damaged (artificial- (50g) infused 2μl of RP ex- into four chambers. On the top newed after five parasitoids ly damaged grain; AG). Two tract vs 50g infused 2μl BP of the cylinder, a walking are- had been tested. empty petri dishes (C) were extract, and two empty petri na (1cm high, 19cm diameter) Fifty parasitoids were tested used as control. dishes. The infused rice was was placed consisting of plastic for each type of sample. Each The infested grain tested placed separately in the Petri gauze (0.5mm mesh) with a individual parasitoid was used by weevil larvae was ob- dishes and kept in humidifiers rim of acrylic (0.9cm high) and only once. At the start of each tained by dissecting grains containing a saturated sodium covered with a glass plate to bioassay, the parasitoids were infested by 3rd-4th instar chloride solution at 65-70% prevent parasitoids from escap- released individually in the weevil larvae. The infested r.h. for seven days before be- ing. No airflow was generated. center of the walking arena grain material was cleaned ing used. An odor sample was placed in and their standing times in the from faeces using a fine a Petri dish (5.5cm diameter) four sectors above the arena brush. Artificially damaged Statistical analysis with brown filter paper (4cm were registered for 600s. The grains were cut with scissors, diameter) in one chamber or time the parasitoids spent knives or needles in order to The Friedman ANOVA was in two opposite chambers. walking in the areas directly better mimic damages caused used to test for differences be- Volatiles were allowed to dif- above the Petri dishes with by the gnawing larvae. tween the four areas. In case fuse through the gauze, result- odor samples was compared to that significant differences were ing in an odor field in the the areas with control Petri Responses of L. distinguendus found, the Wilcoxon-Wilcox- walking arena above. The re- dishes and used to assess the females to S. zeamais larvae test for multiple comparisons maining chambers contained stopping effect of an odor regurgitant induced rice (Sachs, 1992) was used to de- Petri dishes with brown filter sample. Parasitoids that grains volatiles termine which sectors are dif- paper as controls. walked for less than 50% of ferent from each other. the total observation time A series of experiments was General methods for bioassays were not included in the sta- conducted to test the attraction Results tistical analysis. of L. distinguendus females to Evaluations were performed regurgitant-induced odors Responses of female under constant temperature and Collection of weevil emitted from rice grains, us- parasitoids to S. zeamais humidity at 26 ±1ºC and regurgitant ing the original regurgitant induced rice grain volatiles 70±5% r.h., in the darkness (OR) or boiled regurgitant under red light to avoid dis- Instars of the maize weevil, (BR). The original regurgitant Naive and experienced L. traction of parasitoids by light S. zeamais, were obtained from was centrifuged at 1000rpm distinguendus females spent rearing facilities. They were for 10min; the pH of the su- significantly (P<0.05) more placed on rice for 12-16h be- pernatant adjusted with citric time in treatment odor fields fore their regurgitant was col- acid and centrifuged again at compared to control odor lected. The collection proce- 15000pm for 30min. The re- fields, in experiments involving dure was described by Turlings sulting supernatant (protein either rice grains infested by S. et al. (1993). Briefly, well-fed substances; RP) was used for zeamais from which weevil, instars were held with a pair of bioassays, while the resulting faeces, and egg plugs had been lightweight forceps and gently precipitate (non-protein sub- removed or artificially dam- squeezed in the head region stances; RNP) was washed aged rice grains (Figures 2 and with another pair. This caused with 0.05M sodium phosphate 3). Naive L. distinguendus fe- the instars to empty their fore- (pH 8.0) and re-dissolved in males showed no statistically gut content (regurgitant), which the same volume of the origi- significant difference (P>0.05) was collected by drawing it via nal solution (RNP). Finally, in their choice between rice a 100ml capillary tube into a part of the protein-containing grains infested by S. zeamais vial under low vacuum. The supernatant (RP) was boiled and artificially damaged rice Figure 1. Static four-chamber-ol- samples were preserved with in order to denature the pro- grains (Figure 2). However, in factometer used for bioassays. 5ml of 0.05M sodium phos- teins (BP). contrast to inexperienced para- a: glass plate, b: arena, c: cylinder, phate (pH 8.0) and used for A 1mm diameter hole, sitoids, experienced L. dis- d: Petri dish. bioassays within 12h. ~2mm deep, was drilled on tinguendus females were

MAY 2016, VOL. 41 Nº 5 321 Figure 4. Mean walking time (± SD; n=50) of naive females of L. dis- Figure 2. Mean walking time (±SD; n=50) of naive females of tinguendus in a four chamber olfactometer. OR: areas above Petri dishes Lariophagus distinguendus in a four chamber olfactometer. LIGO: areas with grains which had been infused 2μl oforiginal regurgitant, BR: areas above Petri dishes with infested grains by weevil larvae from which above Petri dishes with grains which had been infused 2μl of boiled larvae, feces, and egg plugs had been removed; AG: artificially damaged regurgitant, C: areas above control Petri dishes. Bars with different let- grains; C: areas above control Petri dishes. Bars with different letters are ters are significantly different at P<0.05. significantly different at P<0.05.

Figure 5. Mean walking time (±SD; n=50) of experienced females of L. distinguendus in a four chamber olfactometer. OR, BR and C as in Figure 4. Bars with different letters are significantly different at P<0.05. Figure 3. Mean walking time (±SD; n=50) of experienced females of Lariophagus distinguendus in a four chamber olfactometer. LIGO, AG and 9). Naive L. distinguendus grains which had been infused and C as in Figure 2. Bars with different letters are significantly diffe- rent at P<0.05. females showed no statistically 2μl protein substances and significant difference (P>0.05) grains infused 2μl boiled pro- in choice between between rice tein substances (Figure 9). The strongly (P<0.05) attracted to difference (P>0.05) in choice grains which had been infused results strongly suggested that the rice grains infested by between rice grains which had 2μl protein substances and rice the experienced L. distinguen- weevil larvae from which wee- been infused 2μl OR and rice grains which had been infused dus females were attracted by vil, faeces, and egg plugs had grains which had been infused 2μl non-protein substances the grains which had been in- been removed over the artifi- 2μl BR (Figure 4). However, in (Figure 6). However, in con- fused protein substances. cially damaged rice grains contrast to inexperienced para- trast to inexperienced parasit- (Figure 3). The results strongly sitoids, experienced L. dis- oids, experienced L. distingu- Discussion and Conclusion suggested that the experienced tinguendus females were endus females were strongly L. distinguendus females were strongly (P<0.05) attracted to (P<0.05) attracted to rice Many parasitoids are able to attracted by the specific defen- the rice grains which had been grains which had been infused learn to locate their hosts using sive chemicals released from infused 2μl OR over the rice 2μl protein substances over 10 cues associated with the hosts or infested grains. grains which had been infused rice grains which had been host’s environment (Tumlinson 2μl BR (Figure 5). infused 2μl non-protein sub- et al., 1992; Godfray, 1994; Responses of female stances (Figure 7). Canale et al., 2014). They appear parasitoids to original Responses of female Naive L. distinguendus fe- to associate them with the pres- regurgitant induced rice grain parasitoids to protein males showed no statistically ence of a host (associate learn- volatiles substances from regurgitant significant difference (P>0.05) ing) or generally increase their induced rice grain volatiles in choice between grains in- response to stimuli by a cer- Naive and experienced L. fused 2μl protein substances tain experience, as shown for distinguendus females spent Naive and experienced L. and boiled protein substances parasitoids of many families significantly (P<0.05) more distinguendus females spent (Figure 8). However, in con- (Vet and Dicke, 1992). They time in treatment odor fields significantly more (P<0.05) trast to inexperienced parasit- direct host location by using compared to control odor fields time in treatment odor fields oids, experienced L. distingu- innate cues from different, tax- (Figures 4 and 5). Naive L. compared to control fields of endus females showed statisti- onomically non-related hosts distinguendus females showed the olfactometer in all experi- cally significant difference and host plants (seeds). Like no statistically significant ments (Figures 6 and 7 and, 8 (P<0.05) in choice between numerous other insects, L.

322 MAY 2016, VOL. 41 Nº 5 Figure 8. Mean walking time (±SD; n=50) of naive females of L. Figure 6. Mean walking time (±SD; n=50) of naive females of L. dis- distinguendus in a four chamber olfactometer. RP: areas above Petri tinguendus in a four chamber olfactometer. RP: areas above Petri di- dishes with grains which had been infused 2μl of protein substan- shes with grains which had been infused 2μl of protein substances, ces, BP: areas above Petri dishes with grains which had been infu- RNP: areas above Petri dishes with grains which had been infused 2μl sed 2μl of boiled protein substances, C: areas above control Petri of non-protein substances, C: areas above control Petri dishes. Bars dishes. Bars with different letters are significantly different at with different letters are significantly different at P<0.05. P<0.05.

Figure 7. Mean walking time (±SD; n=50) of experienced females of L. Figure 9. Mean walking time (±SD; n=50) of experienced females of L. distinguendus in a four chamber olfactometer. RP, RNP and C as in distinguendus in a four chamber olfactometer. RP, BP and C as in Figure 6. Bars with different letters are significantly different at P<0.05. Figure 8. Bars with different letters are significantly different at P<0.05. distinguendus has been shown interactions of substances from marginiventris (Cresson) and enemies. When the larval stag- to learn from experience the herbivore with the damaged its host Spodoptera exigua es of insects or other arthro- (Steidle, 2000). The results plant tissue (Steowe et al., (Hfibner) and, by Mattiacci pods are the targets, a foraging obtained are consistent with 1995). However, so far few et al. (1995) for Cotesia glom- strategy is employed. Under previous studies, in which L. experimental evidences have erata (L.) and its host Pieris the condition that some specif- distinguendus showed learning been reported to support this, brassicae (L.), plant volatiles ic chemical cues are used in ability in an olfactometer. It and the release of herbivore- can be induced by the regur- the communication between will be able to locate further induced synomones (HIS) gitate of caterpillars. Thus, it insect pests and their natural hosts more easily by using has almost exclusively been seems likely that parasitoid enemies (Cox, 2004), the strat- these additional stimuli. demonstrated in somatic plant attracting volatiles are also egy of applying semiochemi- Herbivore-induced plant tissues. In 2005, Steidle et al. induced by the saliva of the cals into the biological con- odors have been reported to be concluded that the grains have weevil larvae or females. trols has been considered to used as chemical cues in the the ability to ‘whisper for help’ Although theoretically less attract parasitoids or predators foraging behavior of natural of the parasitoid L. distinguen- likely, some generalist preda- into a crop or increase the enemies. When plants are in- dus. However, it was not tors appear to make some use amount of time they spend in vaded by larvae of insects or demonstrated whether poten- of plant volatiles to locate a field. Therefore, increased other arthropods, they usually tial HIS were actively pro- prey. Yellow jacket wasps in understanding of the chemical- produce and release defensive duced by infested grains or the Vespula vulgaris species ly mediated interactions be- chemicals that can be recog- are a by-product of grain group are attracted to mix- tween hunters and nized by predators and parasit- metabolism. tures of (E)-2-hexenal with their victims will be useful for oids to locate their victims. Experienced L. distinguen- either a-terpineol or linalo- the biological controls of pests These plant chemicals may dus females were strongly ol-all ubiquitous components on a crop. Our ultimate goal also serve as ‘alarm signals’ attracted to the grains to of volatiles from plants under is to be able to develop that are exploited by predators which protein substances attack by herbivores (Steowe an environmentally friendly and parasitoids to locate their from original regurgitant had et al., 1995). method to control the pest re- victims. There is considerable been applied. As demonstrat- Herbivore-induced plant surgence on a crop and reduce evidence that the volatile ed by Turlings et al. (1991) odors play major roles in the the currently heavy depen- ‘alarm signals’ are induced by for the parasitoid Cotesia foraging behavior of natural dence on pesticides.

MAY 2016, VOL. 41 Nº 5 323 ACKNOWLEDGEMENTS Halstead DGH (1963) The separation Ruther J, Steidle JLM (2000) Mites Watson SA, Ramstad PE (Eds.) of Sitophilus oryzae (L.) and S. as matchmakers: semiochemicals Corn Chemistry and Technology. This work was supported by zeamais Motschulsky (Col., from host-associated mites at- American Association of Cereal the Key Program of Natural Curculionidae), with a summary tract both sexes of the parasitoid Chemists, St. Paul, MN, USA. Science Foundation of the of their distribution. Ent. Mon. Lariophagus distinguendus. J. pp. 185-199. Higher Education Institutions, Mag. 99: 72-74. Chem. Ecol. 26: 1205-1217. Tang QF, Wu YJ, Liu BM, Yu ZL Anhui Province, China (Grant Hase A (1924) Zur Kenntnis wirts- Ryabov MA (1926) The possibilities (2009) Olfactory responses of KJ2014A075), the Key Project chaftlich wichtiger Tierformen. of applying the parasitic Lariophagus distinguendus for University Excellent Young I. 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