On Field Populations of European Corn Borers in Nebraska

Effects of the Microsporidium, Nosema pyrausta, on Field Populations of European Corn Borers· in Nebraska2

ROSCOE E. HILL AND WALTER J. GARY Department of Entomology, University of Nebraska, Lincoln 68583 ABSTRACT Environ. Enlomol. 8: 91-95 (1979) The incidence and development of the protozoan parasite, Nosema pyrausta (Paillol), in field populations of the European corn borer, Ostrinia nubilalis (Hbn.), is documented for 2 Nebraska counties over a ]6-yr period. In one county, N. pyrausta reached epizootic proportions twice and in the other the relationship wasm~t]y enzootic. The epizootic development followed periods of increasing host density. Reduced ECB populations and ]arval weights followed epizootic peaks attesting to the debilitating and mortal effects of-No pyrausta on the hosl. Downloaded from https://academic.oup.com/ee/article/8/1/91/2396372 by guest on 01 October 2021 That the biology of the European corn borer (ECB), et al. ]961, Hill et al. ]967, 1973). In the northeastern Ostrillia Ilubilalis (HUbner) is significantly affected by area (Cuming Co.) corn is grown largely under normal the microsporidium Nosema pyrausta (Paillot), has been rainfall, whereas in the central area (Hall Co.) intensive demonstratcd by several researchers. Zimmack and irrigation farming is practiced. ECB populations were Brindley (1957) reported histo]ogical evidence that fe- determined by counting all larvae and pupae from three males infected with N. pyrausta transmit the parasite 4.05x 10-4 ha (111000 acre) plots in each of 24-30 transovarily. Zimmack et al. (1954) also noted that com- cornfields in both counties. The summer (1st generation) pared to uninfected moths, diseased female moths were census was made when the majority of the borers had shorter lived, and laid fewer eggs. Progeny survival was become full grown or were beginning to pupate. The fall lower and growth slower in infected than in uninfected census was conducted at the time of 2nd-generation larvae. Kramer (] 959a) observed that infected female borer maturity. Borer abundance and density were re- moths transmined the microsporidium to no less than corded as no./plant, % plants infested and % plants in- 50% of their offspring. Among the infected larvae ca. fested/field examined. 14% reached adulthood compared to 75% for their dis- Every fall, from ]957-7], borer samples from the 2 ease-free counterparts. Kramer (l959b) also presented counties were sent to the USDA Corn Insects Research evidence showing that the debilitating effects of micros- Laboratory at Ankeny, Iowa where a minimum of 25 poridiosis interact with temperature extremes to cause larvae from each area was examined for the presence of mortality in host populations in the field. His observa- Nosema pyrausta, the level or intensity of infection (no. tions show that seasonal weather extremes interact with spores/larva) and larval weight. The 1972 collections disease causing larval mortality. were processed by the junior author using method of Several entomologists have suggested this protozoan Raun et al. (1960). may be an important natural control agent closely asso- N. pyrausta infections in corn borers from Nebraska ciated with poor survival and resulting borer population were 1st detected during 1959. That year 18.3 and 2.0% fluctuations in the field (Brindley and Dicke ]963, of the larvae were infected in Cuming and Hall Co., Decker 1960, Van Denburgh and Burbutis 1962). Re- respectively. The percent infection generally increased cently. Lewis and Lynch (1976) studying the interaction over the next few years reaching 100% during 1963 in of Nosema infection and resistant com on com borers Cuming Co. and 44% in Hall Co. during 1964 (Table noted in their experimental plantings that N. pyrausta 1). In each county from 1959-1972 there were 2 waves alone substantially reduced ]arval weight and the number of infection as shown in Fig. I. In Cuming Co. the 1st of borers per plant. They concluded if means existed peak (100% infection) in 1963 was followed by 2 yr of whereby N. pyrausta could be introduced into large seg- very high incidence and greatly lowered corn borer pop- ments of a natural ECB population the suppressive effect ulations. This in turn was followed by a year of low of this protozoan could be tremendous. percentage infection and 3 seasons (1967, ]968, and In this paper we present and discuss the incidence and 1969) when zero infection was found in the fall samples development of N. pyrausta as it has occurred in natura] and during which increasingly high fall borer popula- populations of European corn borers in 2 areas of Ne- tions occurred. The rather high abrupt infection of 48% braska over several years. in the peak borer year of 1970 was followed by another 100% infection in 1971 along with a reduced borer pop- Methods and Results ulation. In 1972 both the borer population and infection Beginning in 1955, an intensive census was con- rate decreased sharply. ducted of ECB populations in 2 Nebraska areas (Chiang The development of N. pyrausta in Hall Co. cornfields was less intense than that described for Cuming

I Lepidoptera: Pynlidae. Co. The ]st peak of 44% in 1964 was followed by a 2- , Contribution No. 423. Department of Entomology. University of Nebraska. Published with approval of the Director as Poper No. 5495 in the Journal Series, yr decline in percent infection. Another rise in infection Nebraska Agricultuml Experimenl Station. Lincoln. Contributory to North Central occurred in 1967, 1968, and 1969 reaching 40% the lat- ~f~~nol Projects NC-20. NC-87. and NC-105. Received for publication Feb. 13. ter 2 yr and then dropping through 20 to 0% in 1970 and

Table I.-European corn borer populations, their spatial distribution and trends in Nosema pyrausta infections of corn borer larvae in Cuming and Hall Co., NE.a

% fields infested 61 + % Avg wt all Year & % in summer & % larvae Avg no. larvae corn borer Avg no. plants 100% infected by spores/infected examined generation borers/plant infested in fall N. Pyrausta larvax 1()6 (mg) Cuming Co. 1957 1st 0.23 32.8 12.5 2nd 5.50 97.3 66.7 0.0 1958 1st 0.72+ 66.1+ 62.5+ 2nd 4.74 99.9+ 95.8+ 0.0 1959 1st 0.28 36.9 20.8 2nd 2.25 86.5 25.0 18.3+ 19.2+ 97.7+ 1960 1st 0.80+ 55.2+ 45.8+ 2nd 2.68+ 91.7+ 20.8 28.0+ 4.4 112.5+

1961 1st 0.31 40.4 16.7 Downloaded from https://academic.oup.com/ee/article/8/1/91/2396372 by guest on 01 October 2021 2nd 0.99 86.4 20.8 20.8 8.9+ 86.5- 1962 1st 0.24 27.2 20.8+ 2nd 1.74+ 93.1+ 50.0+ 36.0+ 20.6+ 98.6+ 1963 1st 0.36+ 44.2+ 29.2+ 2nd 2.83+ 99.9+ 95.8+ 100.0+ 48.7+ 116.6+ 1964 1st 0.52+ 47.1+ 33.3+ 2nd 0.96 72.0 16.7 76.0 14.4 101.3- 1965 1st 0.27 30.4 20.8 2nd 0.39 62.3 4.2 88.0+ 10.8 81.9- 1966 1st 0.14 24.4 4.2 2nd 1.38+ 73.7+ 12.5+ 8.0 7.8 85.1+ t967 1st 0.20+ 22.1 3.3 2nd 0.61 52.3 3.3 0.0 0.0 92.9+ 1968 1st 0.Q7 15.9 0.0 2nd 1.83+ 81.6+ 30.0+ 0.0 0.0 102.3+ 1969 1st 0.38+ 47.2+ 23.3+ 2nd 4.66+ 97.7+ 83.3+ 0.0 0.0 105.2+ 1970 1st 0.85+ 77.0+ 2nd 6.00+ 100.0+ 100.0+ 48.0+ 13.2+ 82.6- 1971 1st 0.80 73.5 2nd 2.61 96.8 66.7 100.0+ 23.6+ 73.7- 1972 1st 2nd 0.49 41.6 0.0 10.5 9.2 76.9+ Hall Co. 1957 1st 0.17 30.3 12.5 2nd 3.70 98.0 75.0 0.0 1958 1st 0.41+ 40.2+ 25.0+ 2nd 1.83 100.0+ 100.0+ 0.0 1959 1st 0.13 20.8 4.2 2nd 1.98+ 85.0 20.8 2.0+ 8.4+ 97.4+ 1960 1st 0.36+ 33.9+ 16.7+ 2nd 2.31+ 90.0+ 41.7+ 4.0+ 0.6 109.3+ 1961 1st 0.27 34.7+ 12.5 2nd 1.12 82.7 8.3 11.9+ 0.6 94.5- 19621st 0.44+ 40.0+ 29.2+ 2nd 3.28+ 97.0+ 70.8+ 20.0+ 12.2+ 94.3- 1963 1st 0.10 17.6 0.0 2nd 1.98 97.9+ 54.1 36.0+ 20.4+ 105.7+ 1964 1st 0.18+ 20.5+ 0.0 2nd 2.15+ 99.0+ 83.3+ 44.0+ 8.5 113.7+ 1965 1st 0.15 21.6+ 4.0+ 2nd 1.33 83.3 12.5 30.0 2.2 92.3- 19661st 0.13 16.5 0.0 2nd 2.98+ 96.4+ 62.5+ 8.0 2.6+ 99.4+ 1967 1st 0.26+ 24.7+ 6.7+ 2nd 0.66 61.8 10.0 35.0+ 4.2+ 86.5- 1968 1st 0.01 2.7 0.0 2nd 0.98+ 69.2+ 20.0+ 40.0+ 5.8+ 98.8+ 1969 1st 0.02+ 8.6+ 0.0 2nd 1.12+ 74.4+ 13.3 40.0+ 7.0+ 103.4+ 1970 1st 0.05+ 13.7+ 2nd 1.85+ 94.7+ 23.3+ 20.0 0.6 102.2- 1971 1st 0.67+ 64.8+ 2nd 5.15+ 97.0+ 70.0+ 0.0 0.0 94.4- 1972 1st 2nd 0.78 48.8 0.0 1.7+ 6.4+ 93.5-

o Exceptfor 1972data,all infectiondeterminationsweremadeby USDAComInsectsResearchLaboratorypersonnel.The 1972dataweredeterminedby WalterGary usin~e methodof Raunet al (1960). + notesupwardtrendswhere1stand2ndgenerationdatashowedgainsoverthepreceding1stor 2ndgeneratinnsrespectively. - Denoteslowerlarvalweightfromthatof precedingyear. February 1979 HILL AND GARY: Nosema INFECTIONAND ECB POPULATIONS 93

Hln County ------% liolds 100% plontl infest..! in foil % boron inf.",oclwilll H•••••••• 100 , , ,," ., 80 ,' ,, ,~ ~ ' , ,, ,.., ,' , , , , I I , , I I 80 \ I , , '\\ J• I I I '.' , I I I I I I \ I I , I I I I , I I I 40 I I I \ '"#. \ , I , , I I I I , I \ ~, \ ZO I \ \

I Downloaded from https://academic.oup.com/ee/article/8/1/91/2396372 by guest on 01 October 2021 0 51 68 69 50 51 52 53 64 6S 66 61 66 69 10 11 12 Cuming County %liold. 100% pI.nll inf••tocl in loll % bor.n infected with Nos.me 100 ,"\ ,,".,, , \ , 80 I \ f' I \ I I \ I , I .' I I j 80 I I I , I , I .e I I I I J 40 \ I #. I , \ I· I 20 .-- , ,, ," ...... •.....•' 0 51 68 59 50 61 62 53 64 6S 66 61 68 69 10 11 12

FIG. i.-Percent of fall-sampled cornfields with all (100%) plants infested with com borers and % of borers infected with Nosema pyrausla in Cuming and Hall Co., NE, 1957-72.

1971, respectively. In 1972 there was a very slight in- Such a disease may fluctuate between enzootic and epi- fection increase. The percentage of larvae infected over zootic phases depending on the relationship status the years averaged higher in Cuming (38.1) than in Hall among host population, pathogen population, and envi- Co. (20.9) and the avg number of spores per infected ronment (Tanada 1964). larva (the intensity of infection) was over 2 times greater In Cuming Co. there were 2 epizootic waves of N. in Cuming (12.9 X l(6) than in Hall Co. (5.7x l(6). pyrausta infection which peaked following an upward trend of at least 3 successive ECB generations, i.e. Discussion where the 1st and 2nd generations showed gains over the Insect pathogens generally are factors which host spe- preceding 1st or 2nd generation, respectively. Thus, be- cies more often encounter as their populations increase. ginning with the fall population of 1962 which was However, N. pyrausta has not previously been shown to greater than that for 1961, there were successive in- operate as a density-dependent factor with ECB popula- creases in abundance and density over 4 generations: tions (Chiang and Hodson 1972). 2nd 1962, 1st 1963, 2nd 1963, and 1st 1964. In the fall The data in the present paper are presented as evi- of 1963 N. pyrausta spores were found in 100% of the dence that as ECB increased in abundance and density, borers examined. A high incidence of infection persisted expressed in number of borers per stalk, percent of stalks in the fall populations through 1964 (76%) and 1965 infested or in the percentage of heavily infested corn- (88%) during a period of decreasing ECB populations fields, the incidence of N. pyrausta infection also tended and a 30% reduction in larval weight. The intensity of to increase. infection (no. spores/infected larva) also peaked in the The progress of an infectious disease in a population fall of 1963 (48.7x 1(0) after which the rate declined of insects is expressed in the form of an epizootic wave over the next 3 yr (Table 1). A 2nd ECB increasing pop- (Tanada 1964). Among the factors which determine the ulation sequence began in Cuming Co. with the fall gen- shape of these waves are the virulence of the pathogen eration of 1968 and continued for 4 additional genera- and the resistance, density and spatial distribution of the tions or through the fall of 1970 when 48% of the larvae host insect. A disease continually present in a population were infected with N. pyrausta. The 2nd generation of but at a low incidence is termed an enzootic disease. the following year, although less than in 1970, was rel- 94 ENVIRONMENTALENTOMOLOGY Vol. 8, no. I atively large with the infection reaching 100%. In 1972, N. pyrausta probably should be considered as having the ECB population was greatly reduced and only 10.5% been enzootic in Hall Co. and that it actually never did of the larvae were recorded infected. reach epizootic proportions. The incidence never ex- In Hall Co. the initial N. pyrausta buildup began in ceeded 44% and the intensity of infection only once fall 1959 and there was a continual 6-yr steady increase went as high as 20.4x 1()6 spores per infected larva. In in percent infection. However, the ECB generation trends fact, only in 2 yr (1~·J2 and 1963) were more than were up and down alternating by years. Following the lOx 1()6spores recorded per infected larvae. This rate of fall ECB population of 1959, both summer and fall ECB infection was exceeded in 7 yr for larvae in Cuming Co. populations were up in 1960, down in 1961, up in 1962, down in 1963, and up in 1964, when 44% of the larvae Conclusions were infected. Both the percent of plants infested and Both ECB populations and the incidence of Nosema percent of fields 100% infested peaked with the 2nd gen- pyrausta infections varied widely over the years of this eration of 1964. It is questionable that this should be study. There were 2 apparent epizootic waves of N 0- considered an epizootic wave. Rather it resembled an sema infections in Cuming Co. which were associated Downloaded from https://academic.oup.com/ee/article/8/1/91/2396372 by guest on 01 October 2021 enzootic situation. However, the 1964 fall ECB popu- with upward trends in ECB populations extending from lation was followed by 3 declining generations before 3-5 successive borer generations. Peak infections were recovering in the fall of 1966. A 2nd weak surge of N. followed by reduced ECB populations and reduced lar- pyrausta began with the fall population of 1967, and val weights. beginning in the fall 1968 a series of 7 generations of In Hall Co. a weak epizootic wave peaked in the 2nd increasing summer and fall ECB populations occurred. ECB generation in 1964 but from 1965 through 1972 the However, the percentage of infection failed to increase disease appeared to be entirely enzootic and for sug- and dropped from the fall of 1969 (40%) through 1970 gested presumable reasons failed to develop in the in- (20%) to 1971 (0%) although ECB populations rose dur- creased ECB population of 1970 and 1971. ing this period. This was contrary to what had occurred N. pyrausta increased significantly only when the host twice in Cuming Co. and once, although rather weakly, population was increasing and was widespread at a high earlier in Hall Co. when increasing and widespread ECB numerical level. Thus a density relationship is indicated populations were followed by increased N. pyrausta in- and we conclude that a high host density and a wide- fections. A possible explanation for this apparent dis- spread spatial distribution are requisites for the epizootic crepancy may be revealed from a further comparison of development ofN. pyrausta in field populations ofECB. the ECB populations in Hall and Cuming Co. Although there was an upward trend in ECB popula- Acknowledgment tions in Hall Co. the 1st generation was extremely low Except for the 1972 samples, com borer larvae were in each of 3 yr from 1968-1970 averaging only 0.03 processed at the USDA Com Insects Research Labora- larvae/plant and the 2nd generations were relatively light tory at Ankeny, Iowa and especial acknowledgments are averaging 1.31 larvae/plant. Whereas, during the same due K.D. Arbuthnot, George T. York, Earle S. Raun period the upward ECB trend in Cuming Co. was at a and Leslie C. Lewis. The authors further extend to Les- significantly higher density with per plant averages of lie C. Lewis their sincere appreciation for his helpful 0.43 for the I st generation and 4.16 recorded for the 2nd advice during the preparation of the manuscript. generation. These differences in ECB populations may illustrate the importance of host density as expressed by Steinhaus (1949). REFERENCES CITED According to Steinhaus the density of a host popula- Brindley, T. A., and F. F. Dicke. 1963. Significant develop- tion is important during the preepizootic phase of an ep- ments in European com borer research. Annu. Rev. En- izootic wave for where only a few host insects are pres- tomol. 8: 155-76. ent the infection is likely to die out before it has a chance Chiang, H. C., and A. C. Hodson. 1972. Population fluctua- to enter the epizootic phase. However, if a large popu- tions of the European com borer, OSlrinia nllbilalis, at lation exists, the preepizootic phase may be shortened Waseca, Minnesota, 1948-70. Environ. Entomol. I: 7- 16. with a sudden rise in mortality introducing the epizootic Chiang, H. C., J. L. Jarvis, C. C. Burkhardt, M. L. Fair· phase. child, G. T. Weekman, and C. A. Triplehorn. 1961. Thus in Hall Co. the infection died out, but under the Populatiqns of European com borer, Ostrinia nubilalis more favorable host-density situation in Cuming Co. N. (Rbn.) in field com, Zea mays (L.) Mo. Agric. Exp. Stn. pyrausta increased rapidly to a high incidence with, at Bull. 776. 95 pp. least, circumstantial morbidity and mortality effects ev- Decker, G. 1960. Microbial insecticides-and their future. ident in the ECB populations from 1970-1971 (Fig. I Agric. Chemicals 15: 30. and Table I). Not only did the Cuming Co. population Hill, R. E., A. N. Sparks, C. C. Burkhardt, H. C. Chiang, fall in 1971 but the larval weights were reduced 30% M. L. Fairchild, and W. D. Guthrie. 1967. European com borer Ostrinia nllbilalis (Rbn.) populations in field below the preceding peak weight, as was also the case com, Zea mays (L.) in the North Central United States. following the 1963 infection. The great reduction in Nebr. Agric. Exp. Stn. Res. Bull. 225. 100 pp. ECB populations in both Hall and Cuming Co. in 1972 Hill, R. E., H. C. Chiang, A. J. Keaster, W. B. Showers, probably was due primarily to weather conditions, al- and G. L. Reed. 1973. Seasonal abundance of the Euro- though the presence or effects of N. pyrausta in Cuming pean com borer OSlrinianubila/is (Rbn.) within the North Co. could have been a contributing factor. Central United States. Ibid. 255. 82 pp. Febr ary 1979 HiLL AND GARY: Nosema INFECTION AND ECB POPULATIONS 95

Kramer, J. P. 19590. Some relationships between Perezia Tanada, Y. 1964. Epizootiology of insect diseases. P. 548- r-yrwistae Paillot (Sporozoa, Nosematidae) and Pyrausta 78. III P. DeBach, ed. Biological Control of Insect Pests lIuhilalis (Hubner) (Lepidoptera, Pyralidae). J. Insect Pa- and Weeds. Reinhold Pub. Corp. New York. thol. I: 25-33. Van Denburgh, R. S., and P. P. Burbutis. 1962. The host- Kramer, J, P. 1959b. Observations on the seasonal incide.nce parasite relationship of the European corn borer, Ostrillia of microsporidiosis in European com borer populations in lIuhilalis, and the protozoan Perezia pyraustae in Dela- Illinois. Entomolphaga 4: 37-42. ware. J. Econ. Entomol. 55: 65-7. Lewis, L. C., and R. E. Lynch. 1976. Influence on the Eu- Zimmack, H. L., and T. A. Brindley. 1957. The effect of the ropean com borer of Nosema pyrausta and resistance in protozoan parasite Perezia pyraustae Paillot on the Euro- maize to leaf feeding. Environ. Entomol. 5: 139-42. pean corn borer. Ibid. 50: Raun, E. S., G. T. York, and D. L. Brooks. 1960. Deter- 637-40. mination of Perezia pyraustae infection rates in larvae of Zimmack, H. L., K. D. Arbuthnot, and T. A. Brindley. the European com borer. J. Insect Pathol. 2: 254-8. 1954. Distribution of the European com borer parasite Steinhaus, E. A. 1949. Principles of Insect Pathology. Mc- Perezia pyraustae, and its effect on the host. Ibid. 47: Graw-Hill Book Co., Inc .• New York. 757 pp. 641-5. Downloaded from https://academic.oup.com/ee/article/8/1/91/2396372 by guest on 01 October 2021

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