Resistance of prey to predation and strike rate of the predators, Mononchoides longicaudatus and M. fortidens (Nematoda : Diplogasterida)

Anwar L. BILGRAMIand M. Shamim JAIRAJPURI

Section of Nematology, Department of Zoology, Aligarh Muslim University, Aligarh-202002, India.

SUMMARY

Resistance of prey to predation, strike rate of the predators, Mononchoides longiwzudatus and M. fortidens and their ability to wound prey and feed upon them was determined on agar plates. M. longicaudatus and M. fortidens attacked al1 kinds of prey nematodes. The second stage juvenilesof Meloidogyne incognita and tritici and the adultAcrobeloides sp., Cephalobus sp., and Panagrellus redivivus were most susceptible to predation while Hemicriconenzoides mangiferae and indicus were totally resistant. Hirschmanniella o yzae, indicus, mashhoodi, Xiphinema americanunz, Rhabditis sp., Trichodorus sp., and Longidorus sp., were attacked with intermediate frequencies. M. longicaudatus took a minimum of 15-25 min. to finish a juvenileof M. incognita and maximum 80-110 min. for theLongidorus sp., white M. fortidens consistently consumed prey at a faster rate.

RÉSUME

Résistance des proies à la prédation et taux d'attaque des prédateurs Mononchoides longicaudatus et M. fortidens (Nematoda :Diplogasterida)

La résistance des nématodes-proies à la prédation, le taux d'attaque des prédateurs, Mononchoides longicaudatus et M. fortidens, 8' ainsi que leur habiletéà blesser les proies et s'en nourrir ont été déterminés sur plaques de gélose.M. longicaudatus et M. fortidens attaquent tous les types de proies. Les juvéniles de deuxième stade de Meloigyne incognita et d'dnguina tritici et les adultes d'dcrobeloides sp. Cephalobus sp. et Panagrellus redivivus sont les plus exposés à la prédation tandis que Hemicriconenzoides mangiferae et sont totalement résistants. Hirschmanniella oyzae, Helicotylenchus indicus, Tylenchorhynchus mashhoodi, Xiphine'ma anzericanunz, Rhabditis sp., Trichodorus sp. et Longidorus sp. sont attaqués avec des fréquences moyennes. Il faut à M. longicaudatus un minimum de 15 à 25 minutes pour achever un juvénile de M. incognita, et un maximum de 80-110 minutes pour Longidorus sp., tandis que M. fortidens ingère se$ proies plus rapidement.

The predatory nematodes use a varietyof mechanisms The present work describes experiments conducted to to obtainprey. Similarly, prey nematodespossess certain determinethe degree of resistance/susceptibility of qualities such as the thickcuticle, annulations, chemical differentplant-parasitic and free-living nematodes to secretions, etc., which may protect them from predators predation by Mononchoides longicaudatus(Khera, 1965) (Esser, 1963). Esser (1963) provided a listof nematodes Andrassy, 1984 and M. fortidens (Schuurmans Stekho- that he foundto be susceptible or resistant to predation ven, 1951) Taylor & Hechler, 1966. by different mononchsand dorylaims. Grootaert, Jaques and Small (1977) observed prey selection in Butlerius Materials and methods sp., and measuredsusceptibility and resistance to preda- tion of tylenchid, aerolaimid, enoplid and dorylaimid M. fortidens and M. longicaudatus were cultured by nematodes.Small and Grootaert (1983) described the methods of Bilgrami and Jairajpuri (1988). Adult anti-predationadaptations in prey nematodes. Very Acrobeloides sp., Cephalobus sp., Rhabditis sp., Panagrel- recently, Shafqat, Bilgrami and Jairajpuri (1987) obser- lus redivivus, Trichodorus sp., Longidorus sp., Xiphi- vedprey selection in Dorylaimus stagnalis Dujardin, nema americanum, ,Tylenchor- 1845 and suggested that thethick cuticleof Hoplolaimus hynchus mashhoodi, Hoplolaimus indicus, Helicotylen- indicus Sher, 1963 and chemicalsecretions of Helicoty- chus indicus, Hemicriconemoidesmangiferae andthe lenchus indicus Siddiqi, 1963 may represent anti-preda- secondstage juveniles of Meloidogyneincognita and tion devices. were used as prey.

Revue Nématol. 12 (1) :45-49 (1989) 45 A. L. Bilgrami di M. S. Jairajpuri

The free-living nematodes were obtained from the tancehsceptibility since it is an importantfactor in cultures maintained in the laboratory. These prey nema- predation (Small & Grootaert, 1983). Esser (1987) also todes were culturedin Petri dishes containing 1 O/O suggested thatresistance of a preyis lost if it is wounded water-agar. 5 mg of infant milk powder (Lactogen8) or is in a weakened condition. A wound may result in was spread over the surface of agar to grow bacteria the loss of hydrostatic pressure of the body affecting which served asfood for the preynematodes. The locomotion and thereby making the prey more vuber- second stagejuveniles of M. incognita and A. tntici were :able to predation. Wounding may also permit invasion obtained from population maintained on tomato and theof pathogenic micro-organisms resulting into the death wheat galls respectively. Otherprey nematodes were of prey. The mere encounters between the predator and isolated fresh from soil for each experiment. 500 g of the prey may not necessarily result into woundingof the soil containing nematodeswas processed by decantation PreY. and Baermann's funnel techniques. The percentage of predators which started feeding The encounters (lip contact of predator with the prey after wounding the prey and the percentage of prey at right angle) between predators and prey were obser- which were left unfinished by the predators were also ved in Petri dishes containing 1 O/o water-agar using a determined. Both species of predators were tested sep- stereoscopic binocular microscope. For each encounter arately. The untransformed results were analysed to a new predator and a prey individual was used (irres- obtain correlation coefficients (" r '7, standard error (SE) pective of whether the predator failed or succeeded in and level of significance (" P '7 with the help of the attacking theprey). A prey nematodewas placed in front following statistical tests : VW of the head of an active predator with the helpof a fine LIIL 1 needle without touching (disturbing) the predator in any Correlation coefficient (" r '?= manner. Only those observations were recorded where {CX'E YL' the predators behavedas normally as could be ensured. 1 - r2 To reduce the effects of satiation and prey habituation, Standard error (SE k ) = - 4-6 day starved adult predators were tested. Fifty en- counters were observed between predator and prey. 0 The strike rate of predator may be defined as the percentage of success with which it attacks prey (attack represents the rapid movement of head and the appli- Where X and Y are the deviations measured from cation of suction created by oesophagous of the pred- their respectivemeans and Nis the numberof replicates. ator) and may reflect its predatory potential. The strike Significance of '' r '' values was obtained directly from rate (SR)of M. longicaudatus and M. fortidens could be the Table for the significance of the Correlation coeffi- determined by the followiing formula : cient. EA SR (96) = - x 100 E Results

Where EA = total number of encounters resulting The results show a high degreeof correlation between into attack; E = total number of encounters made by the two species of predators for encounters resulting into the predator. attack (r= 0.89, SE k 0.05, p < 0.05); attacks resulting The resistance of a prey may be definedas the degree into wounding (r = 0.98, SE _t 0.01, p < 0.05); feeding of their ability to avoid predation (wounding) by physi- after wounding (r = 0.98, SE 5z 0.01, p < 0.05) and cal, chemicalor behavioural means. The percentage number of prey left unfinished (r = 0.83, SE k 0.05, degree of resistance of aprey may be calculated as p < 0.05). follows : RESISTANCEOF PREY TO PREDATION AND STRIKE RATEOF PR (96) = EA - AW x 100 M. LONGICAUDATUS EA M. longicaudatus attacked al1 types of prey nematodes Where PR = prey resistance; AW = total number of with lowest strike rate H. mangîferae (46 90). Encoun- attacks resulting into prey wounding. on ters with P. redivivus, Acrobeloides sp., Cephalobus sp., The susceptibility of a prey may be defined as their and the second stage juveniles of M. incognita and A. degree of succumbing to predation (wounding). The tritici resulted in maximum strike rate (92-96 O/o) and percent susceptibility of prey to predation may thus be prey wounding (95-100"O) by M. longicaudatus (Tab. 1). obtained by the following formula : The success of M. longicazldatus in attacking other prey (PS (%) = 100 - PR (PS = prey susceptibility) species ranged between 68-90 %.This predator did not During the present study the wounding was con- succeed in wounding any individual belongingHoplo- to sidered as the primary factor in measuring prey resis- laimus indicus or H. mangîferae but attacked 74 O/O and

46 Predation by Mononchoides longicaudatus and M. fortidens

Table 1 Resistance of prey to predation and strike rate of Mononchoides longicaudatus

Prey nematodes Nunzber NumberNumberStrike ~ ofDegree Feeding Prey Duration of of resistancerate of aBer le$ of encounters encounters of attacks susceptibility wounding unfilzished feeding resulting predator resulting PreY on into in pray single attack wounding attack PreY

(El (EA) SR (96) AW-- PR (96) PS (?6) (%) (96) (mnl

Panagrellus redivivus 50 47 94 46 4 96 100 O 30-35 Acrobeloides96 sp. 48 50 ' 48 O 100 96 O 20-25 Cephalobus sp. 48 50 96 48 O 100 120-25 O0 6 29 36 64 86 16 30-45Rhabditis sp.16 45 86 50 64 3690 29 Anguina tritici juv. 43 5092 46 25-30 10 987 93 Meloidogyneincognita juv. 50 48 96 46 4 96 98 7 15-25 Hirschmanniella o yzae 35 5086 43 19 81 9440-55 30 Tylenchorhynchus mashhoodi 42 21 50 33 84 79 35-5073 25 Helicotylenchus indicus 50 34 2668 25 7458 48 60-70 50 36 72 22Longidorus 72 sp. , 36 50 80-110 50 3956 61 50 34 68 22 35 65 45 50 45 65 35 americanum22Xiphinenza 68 34 50 70-85 Hoplolaimus indicusHoplolaimus 50 37 74 O O O O O O Herrzicriconemoides l lnangiferae 50 23 46 O O O O O O 50 39 78 22 Trichodorus 78 sp. 39 50 44 56 77 47 45-60

Al1 figures are nearest to whole numbers.

46 O/O of the individuals respectively. The second stages RESISTANCE OF PREY TO PREDATION AND STRIKE RATE OF of M. incognita and A. tritici along with the adultAcrobe- M. FORTIDENS loides sp., P. redivivus and Cephalobus sp., were highly susceptible to predation having only 0-6 Yo resistance Though M. fortidens attacked Hoplolaimus indicus against M. longicaudatus (Tab. 1). Other prey nema- and H. mangiferae at success rates of 66 O/O and 56 O/O todes viz., H. oyzae, T. mashhoodi,Helicotylenchus respectively, butnone of them were ever wounded. indicus, X. americanum, Rhabditis sp., Trichodorus sp., Maximum strikerates occurred against P. redivivus, and Longidorus sp., had low tomoderate degree of Acrobeloides sp., Cephalobus sp., and the second stage resistance against predation. The percentage of preda- juveniles of M. incognitaand A. tritici(96-100 "0). These tors which continued feeding on the prey after woun- nematodes were highly susceptiblepredationto ding themwas also highest for the most susceptible prey (PR = 0-2 "0). Consumption of these prey was also high nematodes as mentioned above. The percentage of (96-100 O/o) (Tab. 2). Leastnumber of attacksby predators feeding on Rhabditis sp., was also high (86 "O) M. fortidens resulted into woundingX. americanum and although this species was not wounded as frequently as Longidorus sp., as with M. longicaudatus. Few attacksby themost susceptibleprey species. In contrast,fewer M. fortidens resulted in wounding Rhabditis sp., but M. longicaudatus (27 O/o) continued feeding after woun- wounded were usually consumed. In contrast, ding 74 O/o Helicotylenchus indicus. When feeding occur- only 5 1 O/o of the predators fed on78 O/o of Helicotylenchus red no individual of P. redivivus and Acrobeloides sp., indicus whichwere wounded and 56 O/o of these indi- was left unfinished by M. longicaudatus while 58 O/o of viduals were not completely consumed. No individuals Helicotylenchus indicus, 50 Yo X. americanum and 50 ?'O of P. redivivus and Acrobeloides sp., were left unfinished Longidorus sp., were notcompletely consumed by the predators. M. fortidens required 15-20 min to (p < 0.05). M. longicaudatus took 15-25 min to finish consume a M. incognita juvenile Acrobeloides sp., and a M. incognita juvenile but 80-110 min for Longidorus Cephalobus sp., and 60-80 min to consume Longidorus a sp., (Tab. 2). SP 9 47 A. L. Bilgrami & M. S. Jairajpuri

Table 2 Resistance of prey to predation and strike rateof Mononchoides fortidens Prey nematodes NumberNumberSttike Degree of Feeding Prey Duration of of of rate of of left afterresistance of encounters encounters predator attacks susceptibility woundingunfinished feeding resulting resulting PreY on single into in prey PreY attack wounding

(E) (EA)(E) SR (96) AW-- PR (96) PS (%) (?6) (S6) lmn)

50 49 98 49 Panagrellus 98 redivivus 49 50 99O 100 O 20-25 50 48 96 47 2 98 100 98 2 47 Acrobeloides 96 sp. 48 50 O 15-20 Cephalobus sp. 50 50 100 50 O 1O0 100 4 15-20 48 96 34 29 71 88 13 25-35 13 88 71 50 Rhabditis29 sp. 34 96 48 Anguina tritici96 juv. 48 50 96 4798 2 4 15-25 Meloidogyneincognita juv.50 50 98 1O0 2 49 100 2 15-20 Hirschnaanniella oryzae 50 44 1630-4088 3718 89 84 Tylenchorhynchrcs 39 11 89 77 20 35-40 mashhoodi20 77 5089 44 11 88 39 50 45 90 35 22 78 22 35Helicotylenchus 90 indicus 45 50 50-5551 56 sp. 50Longidoncs sp. 39 78 30 23 77 60-7067 50 Xiphinema americanumXiphinema 61 4082 5018 33 80 45 40-55 Hoplolaimus indicusHoplolaimus 66 33 50 O O O O O O Hemicriconemoides 50 28 56mangiferae 28 50 O O O O O O sp. 50 42 50Trichodoms sp. 84 25 8040 60 40 35-45

Al1 figures are nearest to whole numbers.

Discussion characteristic.Small andGrootaert (1983) attributed active body undulations and vigorous escape response The high degree of correlation'between M. fortidens of Rhabditis oxycerca,Pelodera sp., and Plectus sp., and M. longicaudatus forencounters resulting into as characteristicsproviding resistance against pre- attack, attacksresulting in prey wounding,,feeding after dation.During present study a combination of high wounding and number of prey left unconsumed indi- attack rate against Rhabditis sp., comparatively lower cates that both species of predators are very similar in rate of woundingand higher rate of feedingupon theirbehaviour and requirements and also thatthe woundedindividuals suggests that thisprey nema- predator-prey relationship measured for one species of tode also relies primarily on active body undulations predator strongly supports the observations made with and vigorous escape response movements toresist pre- other predator. dation by M. longicaudatus and M. fortidens. The prey nematodes can resist predation byphysical, The highdegree of susceptibility topredation of chemical and behavioural characteristics (Esser, 1963, Cephalobus sp., Acrobeloides sp., P. redivivus along with 1987;Esser & Sobers,1964) such as thkk cuticles the second stage juveniles of M. incognita and A. tritici (Esser,1963; Small & Grootaert, 1983); annulations may be due to small body size, slow rate of movement (Esser, 1963); speed (Esser, 1963; Bilgrami, Ahmed & and lack of protectivecuticle adaptations (Bilgrami, Jairajpuri, 1983); vigorous escape response (Grooraert, Ahmad & Jairajpuri, 1983). These characteristics maybe Jaques & Small, 1977; Small & Grootaert, 1983); toxic/ commonamong endoparasitic,phytophagous nema- unfavourable chemical secretions (Esser,1963). Lack of todes (Esser, 1963). predation, during the present experiments, on Hoplo- Esser (1963) observedthat the dorylaim predators laimus indicus and H. mangiferae might have resulted rarely attacked or succeeded in devouring Helicotylen- from their thick cuticles and annulations respectively, chus spp., and suggested some sort of chemical resist- that providedresistance to prey from wounding.Mylon- ance in species of this genus.The present study supports chulus dentatus and Dorylaimus stagnalis also failed to these observations since wounded Helicotylenchus indi- kill or injure Hoplolaimus indicus (Jairajpuri & Azmi, cus were incompletely consumed more than any other 1978;Shafqat, Bilgrami & Jairajpuri, 1987). These prey species. Bilgramiand Jairajpuri (1988) also sugges- authors also attributed thickcuticle as an anti-predation ted the possibility of unfavourable secretions inHelicoty-

48 Revue Nématol. 12 (1) :45-49 (1989) Predation by Mononchoides longicaudatus and M. fortidens

lenchus ' indicus whichelicited meager responses of REFERENCES M. fortidens and M. longicaudatus besides X. america- num and Longidorus sp. The numberof Helicotylenchus BILGRAMI,A. L., AHMAD, 1. & JAIRAJPURI,M. S. (1983). Some indicus, X. americanum and Longidorus sp., left uncon- factorsinfluencing predation by Mononchusaquaticus. sumed by the predators also suggests the presence of Revue Nématol., 6 : 325-326. unfavourable/repellent substance(s) in the bodyof these BILGRAMI,A. L., AHMAD, 1. & JAIRAJPURI,M. S. (-1984). species of prey. The texture of the cuticle of the dory- Observationson the predatorybehaviour of Mononchus laims, X. americanum,Longidorus sp., mayconform aquaticus. Nematol. medit., 12 : 41-45. resistance to wounding. However, the strike rate against this group was alsogenerally lower suggestingother BILGRAMI,A. L., AHMAD, 1. & JAIRAJPURI,M. S. (1986). A . defensive mechanisms may operate. It may be inferred study of the intestinal contents of some mononchs. Revue from the present observations thatHoplolaimus indicus, Nématol., 9 : 191-194. Trichodorus sp., and H. mangiferae acquire physical BILGRAMI,A. L. & JAIRAJPURI,M. S. (1988). Attraction of resistance in the form of thick cuticle and annulations Mononchoides longicaudatusand M. fortidens (Nematoda : respectively; Rhabditis sp. behavioural resistance in the Diplogasterida)towards prey and factors influencing form of active body movements and vigorous escape attraction. Revue Nématol., 11 : 195-202. response; Helicotylenchus indicus chemical resistance in ESSER,R. P. (1963). interactions in plates of the formof toxic/unfavourable secretions; andX. ameri- non-sterile water agar. Proc. Soil Crop Sci. Soc. Ra., 23 : canum and Longidorus sp., resisting predation partly by 121-138. physical and chemical means. ESSER,R. P. (1987).Biological control of nematodes by Ectoparasitic nematodes livingin close proximities to nematodes. 1. Dorylaims(Nematoda : Dorylaimina). Ra predaciousnematodes may have developed more Dept. Agric. di Consumer Sem, Ne?natol. Cire., No. 144 :4 p. anti-predation devices. These mechanismsas mentioned above maybe more effective againstdorylaim, nygolaim ESSER,R. P. & SOBERS,E. K. (1964). Naturalenemies of actinolaimand diplogasterid predators since most of nematodes. Proc. Soil Crop Sci. Soc. Ra, 24 : 326-353. these predators possess piercing type of feeding appar- GROOTAERT,P., JAQUES,A. & SMALL, R.W. (1977).Prey atus and feed by puncturing the cuticle of prey. How- selectionin Butlerius sp.(Rhabditida : ). ever, mononchs overcome the resistanceof prey of dif- Med. Fac. Landbouww. Rijksuniv. Gent., 4212 : 1559-1563. ferent kinds to a larger extent as these do not punc- ture thecuticle of prey but engulf them whole. The ecto- JAIRAJPURI, M. S. & AZMI, M.1. (1978). Some studies on the predatorybehaviour of Mylonchulus dentatus. Nematol. parasiticnematodes are therefore more vulnerable to medit., 6 : 205-212. predation by mononchs.This isevident as many species of mononchs have been found containingspecies MOHANDAS,c. & PRABHOO,N. R. (1980). The feeding Se- of Hoplolaimus, Helicotylenchus, Xiphinema, Henzicrico- haviourand food preference of predatory nematqdes nemoides, Rhabditis sp.,etc., besidesother tylenchs, (Mononchida) from the soil of Kerala (India). Revue Ecol. dorylaims, rhabditis and mononchs entire in their in- Biol. Sol, 17 : 53-60. testine (Bilgrami, Ahmad & Jairajpuri, 1986). SHAFQAT,S., BILGRAMI,A. L. & JAIRAJPURI,M. S. (1987). Mohandasand Prabhoo (1980) also foundintact Évaluation of the predatory behaviourof Do ylaimus stagna- and Xiphinema elongatunz in lis Dujardin, 1845 (Nematoda: Dorylaimida). Revue Néma- the intestine of Iotonchus kherai and I. monohystera. tol., 10 : 455-461. SMALL,R. W. & GROOTAERT,P. (1983). Observations on the ACUNOWLEDGEMENTS predation abilities of some soil dwelling predatory nema- The authors are thankful to the Chairman, Department of todes. Nematologica, 29 : 109-118. Zoology, Aligarh Muslim University, Aligarh for providing neccessary laboratory facilities. Accepté pour publicationle 22 janvier 1988.

Revue Nématol. 12 (1) :45-49 (1989) 49