Mysore J. Agric. Sci., 51(A): 53-58, 2017

Ecological and Foraging Aspects of the Webworm, undalis Fabricius

SIVAPRAGASAM, A. Cabi Southeast Asia Regional Center, Building A19, Mardi, Serdang, Selangor, Malaysia E-mail: [email protected]

ABSTRACT

The paper addresses the influence of temperature, ascertains the weed hosts and elucidates the foraging aspects of the larva of the cabbage webworm (CWW), (Fabr.), a major pest of head or English cabbage (Brassica oleracea var. capitata) grown in the Malaysian lowlands. The optimal temperature for the

development of CWW was 30ºC, whereby the intrinsic rate of increase rm , was the highest. The ubiquitous weed, Cleome rutidosperma (Family: Capparidaceae) was found to be its natural host. The level of infestation of CWW on C. rutidosperma in the field was low, ranging from 0.1 % to 3.45%. Nevertheless, it provided a source population for the monocrop cabbage causing significant damage. The intra and inter plant foraging studies revealed that the CWW larva preferred the cabbage shoot to the leaf and this preference enhances its survival rate in the field.

Keywords: Cabbage webworm, Hellula undalis, temperature, weed host, foraging behavior

INSECT pests and diseases are major biotic factors affecting head or English cabbage production both in the highlands and lowlands of Malaysia (Sivapragasam and Loke 1992). Among the pests which inflict serious damage, particularly in the lowlands, is the cabbage webworm (CWW), Hellula undalis (Fabr.) (: Pyralidae). Although this has also been recorded in the Malaysian highlands (Ooi 1979), it has reached serious pest status only on cabbage grown in the lowlands. Stage specific crop life tables on cabbage (Sivapragasam,

1994) suggested that H. undalis is the most important FIGURE 1. Larva of Hellula undalis pest contributing to about 41 percent of total mortality of the plants during the pre-heading stage.

Although CWW infests other cruciferous plants, such as chinese mustard, Brassica chinensis (L.), chinese , B. oleracea var alboglabra Bailey and , Raphanus sativus (L.), it is more serious on head cabbage because damage by a single larva (Figure 1) boring into the growing shoot of the cabbage plant (Figure 2) before its pre-heading stage could result either in the death of the plant or in producing small-sized multiple cabbage heads which are unmarketable. As such, there is no economic threshold level to initiate insecticide treatments but to FIGURE 2. Hellula damage on head cabbage advocate for preventive applications. 54 SIVAPRAGASAM, A., et al.

There is also potential for indirect damage due Evaluating weed as hosts of CWW to soft rot, Erwinia carotovora. In any case, complete To ascertain which of the weeds found in or near control of CWW solely with insecticides is fraught the lowland cabbage ecosystem were serving as hosts with challenges due to the webbing behaviour of the to CWW, common broad-leaf weed species were larva and to some extend resistance development examined in situ and also collected and brought to the (Sivapragasam 1994). Thus, to develop pragmatic laboratory to examine for eggs and other stages of management strategies of CWW, an understanding of CWW. Feeding tests were also done under laboratory its biology and ecology in the Malaysian context is conditions with temperature ranging from 24ºC to pertinent. Sivapragasam (2005) described some 28ºC and R.H. 80±5%. Fresh young leaf samples of aspects of its biology and development. To each weed were offered to five first and third instars complement the current repository of knowledge, in of CWW confined in a Petri dish (10.0 x 2.0 cm) lined this paper some aspects of the ecology and foraging with moistened filter paper. First and third instars fed behavior are reported. The aspects are: (i) Effect of on cabbage leaves served as the ‘control’. Further temperature on the development of CWW; (ii) details of the experimental set-up are described in Evaluating weeds as host of CWW and (iii) Dispersal Sivapragasam (1994).For each weed species, the tests and foraging behaviour of the CWW larva. were repeated 3xand in all a total of 19 weed species belonging to 12 families were used in the tests. MATERIALS AND METHODS Dispersal and foraging behaviour of the CWW Here, general details of the materials and larva methods are described. For specific details, refer to The intra- and inter-plant movement of CWW Sivapragasam (1994). larva on cabbage were studied in a glasshouse Effect of temperature on development usingcaged 1.5 month old cabbage plants with about 10 leaves. Details of the experimental procedures are The CWW used in this study was obtained from given in Sivapragasam (1994). Briefly, for the intra- cultures maintained in the laboratory on cabbage plant movement study, a cohort of eggs in an leaves. All experiments were conducted in controlled aluminium egg card (< 24h old) was clipped to the temperature incubators (RumedR) maintained at 3rd leaf of each cabbage plant (the ‘egg leaf’). Leaf different constant temperatures of 10, 15, 20, 25, 30, number 1 is the first open leaf from the top. The 35 and 40 ºC. Temperatures were maintained within number of larva on each of the ten leaves was ±1ºC and the R.H. between 80±5 percent at each observed daily for 10 days. The experiment was temperature studied. The development and survival replicated 10x and data from all ten replicates (or rates of the immatures at each temperature were plants) were pooled for analysis. determined using a cohort of at least 100 eggs laid The inter-plant movement studies were within 24 h. At each temperature regimen, newly conducted using a larger cage (Sivapragasam, 1994). emerged larvae were isolated individually in Petri The design of the experiment was as follows: In the dishes (9.0 x 1.5cm2) and fed with excised young centre of the cage was a cabbage plant (hereafter cabbage leaves until pupation. The longevity and called the source plant) with a cohort of 10 eggs (< oviposition of the adult that emerged from each 24h old). The ‘source’ plant was surrounded by four temperature regimen was determined using a rearing similar-aged cabbage plants placed equidistant from jar provided with leaves of Brassica juncea as the each other and the ‘source’ plant. However, one leaf oviposition substrate. The number of eggs laid and from the ‘source’ plant and that of each of the the adults surviving were recorded for at least 20 pairs neighbouring plants was stapled together to form a bridge between them. A corrugated cardboard paper throughout their life span. The intrinsic rate of sprayed with sticker was used as a barrier to prevent increase (r ) was computed using tables of age m larval movement between plants except via the specific oviposition (m ) and survival rates (L ) for the x x ‘bridge’. Daily observations were made on the source age interval (x) of one day using the analytical method and neighbouring plants for CWW larva. The described by Birch (1948). experiment was terminated when all the larvae has ECOLOGY AND FORAGING OF THE CABBAGE WEBWORM 55 pupated in the pupal tray filled with vermiculite placed suggested that the temperature most favorable for at the base of each cabbage plant. The experiment CWW appeared to be around 30ºC. At this was repeated 10 x and the data from all the replicates temperature rm was the highest. This finding agreed were pooled for analysis. with that of Awai (1958) who reported that the optimal temperature for CWW development was 31º C. RESULTS AND DISCUSSION Messenger (1976)illustrated that for a given

environmental condition, rm could be used as a Effect of temperature on development measure of favorability and that the higher the value

Table 1 shows the development from egg to adult rm, the more favorable were the environmental emergence (TDP), percent survival (egg to adult conditions within which the population resides. Based emergence), adult longevity for both the female and on this, it can be inferred that the temperature male, oviposition rate per day and intrinsic rate of conditions in the Malaysian lowlands with the mean monthly temperatures of ca 29º C (range: ca 24ºC to increase (rm) of CWW under various temperature regimens. Egg eclosion occurred from 15ºC until 35º 35ºC) is optimal for CWW development. On the other C; none of the eggs hatched at 10ºC and 40ºC. TDP hand, in the cooler highlands(e.g. Cameron Highlands, ranged from 14.64 days at 35º C to about 108.25 days a major cabbage growing area at1,400 – 1,500 meters at 15 ºC and the survival rate from 47percent at 25ºC above sea level with a mean temperature of 18.7ºC to 3 percent at 15ºC. The number of eggs laid (13.4ºC to 24.3ºC) development is impeded. Sachan generally increased with temperature until 30ºC but and Gangawar (1980) reported the concomitant declined at 35ºC. The longevity of the male and decrease in the importance of CWW with increase in female differed significantly between temperatures altitude (with the concomitant decrease in temperature) at which the cabbage is planted. The (Table 1). The rm values increased with temperature to a maximum at 30º C and then decreased. effect of temperature on the distribution of CWW is explicitly shown from its data in temperate countries Temperature affected the survival, development whereby CWW is reported to be major problem only and other life table parameters including number of in summer to late autumn (AVRDC 1978; Shirai and eggs laid and intrinsic rate of increase. This study Kawamoto 1991).

TABLE 1 Development from egg deposition to adult emergence (TDP), percent survival, adult longevity oviposition

rate and intrinsic rate of increase (rm) of Helulla undalis under various temperature regimes Temperature ºC Parameters 15 20 25 30 35 TDP (mean ±day)* 108.25±2.10a 49.31±0.52 b 27.08±0.39 c 19.23±0.36 d 14.64±0.18 e Survival (%, egg to 3.00 18.00 47.00 35.00 28.00 adult) Adult Longevity (days)(mean±day) · Female 11.75±1.91 a 8.77±0.76 b 8.00±0.74 b 3.79±0.48 c 3.08±0.78 c · Male 12.25±2.42 a 6.70±1.11 b 6.79±0.55 b 4.28±0.71 b 4.15±0.66 b Oviposition rate (eggs 1.77 3.96 11.12 22.50 9.01 laid per female/day) Intrinsic rate of 0.01 1.02 1.11 1.15 1.08 increase (rm) * Means with the same letter within a row are not significantly different at P< 0.05 using the Duncan’s multiple range test.

Evaluating weeds as hosts of CWW Research and Development Institute (MARDI), Malaysia. However, the level of infestation of CWW Amongst the weeds examined, CWW was found on C. rutidosperma in the field was low, ranging from feeding only on Cleome rutidosperma DC (Family: 0.1 % to 3.45%. Capparidaceae) (synonym: C. ciliata Schum. & Thonn.). Specimens of adults of both sexes emerging C. rutidosperma is a ubiquitous herbaceous weed from C. rutidosperma were confirmed based on found in the waste grounds and cultivated lands of voucher specimens held at Malaysian Agricultural Malaysia (Barnes and Chandapillai 1972). The 56 SIVAPRAGASAM, A., et al. damage by CWW larva on cleome is evident from the the plants having two larvae per shoot on the sixth closely-webbed leaves in the apical region of the day. However, this number decreased to 10 % by the plant. In this study, only one larva of CWW was found eighth day and by the ninth day, all the plants had only per plant. In other studies, CWW was found on other one larva per shoot. species of Cleome, viz., C. viscose (synonym: C. In the inter-plant movement study, larval icosandra) (Sivapragasam 1994).For example, Alam movement from the ‘source’ plant to the neighbouring et al. (1961-62) recorded CWW on C. viscosa in plants was observed in 8 out of the 10 replicates. By Pakistan. In the Nearctic countries, the host plants the ninth day, 45 % of the neighbouring plants were reported for a congeneric species of Hellula, viz., H. found to have CWW larvae. Most of the larvae (84.6 phidilealis, seemed to be largely confined to plants in %) found earlier on the ‘source’ plants, were found the families Cruciferae and Capparidaceae (Alam on the shoot. On the neighbouring plants, 40 % of 1989). The infestation of cabbage and cleome by the larvae were also found on the shoot and the rest CWW is correlated to the fact that both these families on the leaves. Interestingly, the larvae on the share a similar phytochemical constituency neighbouring plants were first seen on the sixth day characterized by the occurrence of isothiocyanates after the eggs were introduced, i.e., about 3 days after (mustard oils) (van Steenis 1972). The occurrence of eclosion. other crucifer ‘specialists’ such as the flea beetles, Phyllotreta spp., the cabbage leaf webworm, Both the intra-plant and inter-plant studies Crocidolomia pavonana, and the diamondback , indicated that CWW larvae moved to the shoot of the Plutella xylsotella, on Cleome (Sivapragasam 1994) plants from their initial location. Talekar et al. (1981) supports this contention. In addition, Cleome and also indicated that the young CWW larvae preferred cabbage also share quite a similar suite of natural to burrow into the shoot rather than the leaves of enemies (e.g., parasitoids) such as Trathala Chinese cabbage, Brassica campestris. The initial flavoorbitalis (Ichneumonidae), Bassus sp. and increase in the number of larvae per shoot and the Chelonus sp. (both Braconidae) on CWW eventual decrease could be due to the limited space (Sivapragasam and Chua 1997).As for the low in the shoot to accommodate more than one CWW infestation level of CWW on Cleomevis a vis cabbage, larva, particularly that of the later stages. from a foraging perspective, this could be attributed Sivapragasam (1994) suggested that the preference of to the ‘plantapparent’ factor (Feeny 1977). By this it CWW larva for the cabbage shoot to the leaves (which means that cleome grows in the field amongst other were found to be nutritionally better) was largely due weeds and thus has low visibility to CWW, compared to seeking a natural refuge and protection against to cabbage which is grown as a monoculture in natural enemies, viz., predators, of the CWW larva relatively larger patches. This can also be explained under field conditions(Sivapragasam and Chua from a food resource perspective when forage 1997).Although CWW does mine (e.g. in the first for food. Root (1973) suggested the term ‘resource instar), web and fold the cabbage leaf in the later stages to protect itself, the cabbage shoot affords a concentration’ for this phenomenon, i.e., low resource better natural concealment for the larva to protect itself concentration in the case of cleome and a high one without much investment of energy for leaf folding for cabbage. or web making. The trade-off for the larva residing Dispersal and foraging behaviour of the CWW in the shoot was the higher survival rate (about 2.7x), larva and the higher intrinsic rate of increase rm (about 1.5 x) than on the leaves (Sivapragasam and Chua The within (or intra) plant distribution revealed 1997).It is not specifically known what attracts the that during the first 2 days after eclosion, the CWW larva to the shoot. William and Daxenbicher (1981) larva remained on the egg leaf (i.e., the third leaf). On reported that younger and faster growing tissues of the third day after eclosion, one of the cabbage plants Chinese cabbage have higher quantities of (out of 10 used in the experiment) had a larva on the glucosinolates than the older ones. It is not known shoot. From the fourth day onwards, most of the whether there are any specific chemical cues attracting leaves had the larvae on them and from the sixth day the larva to the shoot. In corn, the larva of Pyrausta until the ninth, most of the larvae had moved from the nubilalis (Hueb) settles near those parts of the plant leaves to the shoot of the plants with about 43 % of which are rich in sugar content (Beck 1956). ECOLOGY AND FORAGING OF THE CABBAGE WEBWORM 57

CONCLUSION Annual Meeting of the Caribbean Food Crop Society (mimeo). The study suggested two important factors that ALAM, M. M., HAFIZ, L. A. AND GHANI, M. A., 1961 – 1962. contributed to the distribution and pest status of CWW Annual report of the scheme for the “Survey of in lowland as opposed to those in the parasites of insect pests of cultivated and useful plants highlands. The first was the effect of ambient and survey of insects destroying weeds and other temperature, and the other was the presence of the parasites. The Commonwealth Institute of Biological weed, C. rutidosperma. The optimal temperature for Control (CIBC), Pakistan Station, Rawalpindi. 53 p. the development of CWW was found to be 30ºC (mimeo). which is close to the mean ambient temperature in the AWAI , D., 1958, A study of the identity, larval stagesand lowlands. natural enemies of Hellula undalis (Fabr.) in Hawaii., M. Sc.Thesis., Graduate School of the University of The study on cleome underscores the fact that if Hawaii. a crop (e.g., cabbage) is introduced into an area where AVRDC, 1978, Cabbage webworm. Progress Report of the there is a closely related endemic weed (e.g., Cleome), Asian Vegetable Research and Development Center, one is likely to see a rapid adaptation by CWW to the Shanhua, Taiwan. pp. 34-35. newly introduced host. This is because of the common BARNES, D. E. AND CHANDAPILLAI, M. M., 1972, Common chemical cues (e.g., mustard oils) found in both crops Malaysian weeds and their control. ANCOM, Shah that are conducive for feeding and oviposition. This Alam, Malaysia. was the case with CWW. BECK, S. D., 1956, The European corn borer, Pyrausta Based on the within and between plant dispersal nubilalis (Hubn.) and its principal host plant. 1. studies, CWW prefers the shoot to the leaf. Although Orientation and feeding behavior of the larvae on the this provides greater survival for CWW larvae against corn plant. Ann. Ent. Soc. Am., 49: 522-528. natural enemies, from a management standpoint it is BIRCH, L. C., 1948, The intrinsic rate of natural increase of easier to control on the shoot. Thus, the farmer needs an insect population. J. Ecol., 17: 233-256. to deliver the insecticide as a shoot application to FEENY, P., 1977, Defensive ecology of the Cruciferae. Ann. effectively manage CWW. In field trials, effective Mo. Bot. Gard. 64: 221-234. control of CWW on cabbage was achieved using MESSENGER, P. S., 1976, Experimental approach to insect weekly treatments of Bacillus thuringiensis for a climate relationships. In: Climate and Rice. IRRI, period of five weeks on the shoot and this approach, Los Banos, Philippines. pp: 347-365. besides being cost-effective, reduced the OOI, P. A. C., 1979, An ecological study of the diamondback indiscriminate use of the insecticide (Sivapragasam moth in Cameron Highlands and its possible and Loke 1992). biological control with introduced parasites. M.Sc. Thesis. University of Malaya, Kuala Lumpur, ACKNOWLEDGEMENT Malaysia., pp. 151. The author is grateful for the financial support ROOT, R. B., 1973. Organization of a plant- provided to him by CABI to participate in the VII association in simple and diverse habitats: the fauna of collards (Brassica oleracea). Ecol. Monogr., 43: 95- International Workshop on Management of the 124. Diamondback Moth and Other Crucifer Insect Pests held in Bangalore, India. He also acknowledges the SACHAN, J. N AND GANGAWAR, S. K., 1980, Vertical distribution of important pests of cole crops in organizers of the Workshop viz., the University of Meghalaya as influenced by the environmental factors. Agricultural Sciences, Bangalore in association with Indian J. Ent., 42: 414-421. Cornell University, USA, and AVRDC-The World Vegetable Center, Taiwan for their invitation and kind SHIRAI, Y. AND KAWAMOTO, K., 1991, Laboratory evaluation of the flight ability of female adults of the cabbage hospitality. webworm, Hellula undalis (Lepidoptera: Pyralidae) and reproductive success after flight. Bull. Natl. Res. REFERENCES Inst. Veg. Ornam. Plants and Tea, Japan, Ser. A. 4: 31-40. ALAM, M. M., 1989, Distribution, host plants and natural enemies of cabbage bud worm SIVAPRAGASAM, A., 1994, Biology and population dynamics (Walker) in the Caribbean. Paper presented at the 25th of Hellula undalis (Fabricius) (Lepidoptera: Pyralidae) 58 SIVAPRAGASAM, A., et al.

on lowland cabbages. Ph. D. Thesis. University of 1992, Universiti Pertanian Malaysia, Serdang, Malaya, Kuala Lumpur, Malaysia., Pp. 224. Selangor. pp. 33-37.

SIVAPRAGASAM, A., 2005, Development of cabbage TALEKAR, N. S., SHIAO, W. F. AND LIN, Y. H., 1981, Insect webworm, Hellula undalis (Fabr.) on head cabbage, pest control of summer Chinese cabbage in Taiwan. Brassica oleracea var. capitata. J. Trop. Agric. Food In: proceedings of the first International Symposium Sci., 33(2): 321-331. 1981, TALEKAR, N. S. AND GRIGGS, T. D. (Eds.): Chinese cabbage:, AVRDC Shanhua, Tainan, Taiwan, SIVAPRAGASAM, A. AND CHUA, T. H., 1997, Natural enemies Republic of China. pp: 163-172.

for the cabbage webworm, Hellula undalis (Fab.) VA N STEENIS C.G.G.J., 1972, Flora Malesiana. Series 1: (Lepidoptera: Pyralidae) in Malaysia. Res. Population Spermatophyta Vol.6. Wolters-Noordhoff Publishing, Ecol., 39: 3-10. Groningen, The Netherlands. WILLIAM, P. H. AND DAXENBICHLER, M. E., 1981, SIVAPRAGASAM, A. AND LOKE, W. H., 1992, Integration of pest Glucosinolates in chinese cabbage. In: Chinese control practices to reduce use in cabbages. In: cabbage: proceedings of the First International Proceedings of Applied Biology in Enhancement Symposium 1981, TALEKAR, N. S. AND GRIGGS, T. D. Quality of Life and Environment. Second Symposium (Eds.), AVRDC, Shanhua, Tainan, Taiwan, Republic of Malaysian Society of Applied Biology, Feb. 25-26, of China. pp: 261-270.