Fortuitous Biological Suppression of the Boll Weevil by the Red Imported

Fortuitous Biological Suppression of the Boll WeeviP by the Red Imported Fire Ant2•3

WINFIELD L. STERLING' Department of Entomology, Texas Agricultural Experiment Station, Texas A&M University, College Station 77843

ABSTRACT Environ. EntomoJ. 7: 564-568 (1978) The efficacy of the red imported fire ant (Solenopsis invicta Buren) as a predator of larval stages of the boll weevil (Anthonomus grandis Boheman) was evaluated in 2 areas of Texas. In the Trinity River area the ants consumed up to 85% of the weevils with a weekly avg of 66%. Ants never consumed more than 37% of the weevils in the Brazos-Navasota River area and averaged 22% in Aug. The fire ant exhibits characteristics that may make it a valuable predator of cotton insect pests. It tends to disperse fairly uniformly across cotton fields at high densities and tends to increase in abundance as the growing season progresses. Downloaded from https://academic.oup.com/ee/article/7/4/564/2366799 by guest on 24 September 2021 Ants have been considered the most important predators Trinity River. An 8.3-ha area of cotton, which had been of the boll weevil, Anthonomus grandis Boheman. (Hinds cleared of timber in 1975 and cropped for the 1st time in 1907. Hunter 1917, Hunter and Hinds 1905, Mally 1902). 1977, served as the experimental plot. No chemical insec- Pierce et aI. (1912) and Hunter and Pierce (1912) listed 16 ticides were applied to the area during 1977. The study cot- species of Texas ants reported as predatory on the boll wee- ton field was located at one end of a 202-ha cotton field and vil. Solenopsis geminata (F.), S. molesta Say. andS. texana was buffered by 77 ha of cotton that were occasionally Emery were among the species cited (Pierce et aI. 1912). treated with chemical insecticides to control boll weevils, with S. geminata having a greater impact on weevil abun- cotton fleahoppers, Pseudatomoscelis seriatus (Reuter), dance during the summer than the combined effect of heat tarnish plant bugs. Lygus lineolaris (Palisot de Beauvois), and parasites (Hinds 1907). Since the early 19OO's, two cotton bollworms, Heliothis zea (Boddie), or tobacco bud- additional species of 50Jenopsis, (5. invicta Buren and S. worms, HeJiothis virescens (F.), by ground application richteri Forel), have accidentally invaded the southern equipment rather than by air in an attempt to prevent insec- U.S.A. (Buren ]972). Their efficacy in suppressing boll ticidal drift into the untreated test plot. The remaining] ]6.7 weevil abundance has been largely unknown. Arant et al. ha were treated by TDC with several insecticides by air as (1958) reported that a laboratory colony of imported fire needed for Heliothis spp. control. The boll weevil was ants (species not cited) killed and consumed 20 adult boll treated with azinphosmethyl at 281 gmlha; the cotton flea- weevils in 2 h. These same ant species devoured boll weevil hopper was treated with dimethoate at 224 gm/ha. larvae and other destructive insects in the field. This early A 2nd field, located at the confluence of the Navasota observational research was not followed by careful field and Brazos rivers south of Navasota, Tex., was also used to evaluation. evaluate fire ant predation. This plot is referred to hereafter At least one attempt was made to introduce an ant pre- as the USDA field because it was leased by USDA-ARS dator to the United States for boll weevil suppression. O. F. researchers during 1977. The field had been in grass hay Cook distributed 89 colonies of the kelep ant (Ectatomma production for several years prior to 1977. Previous to our tuberculatum Oliver) in Texas (Hunter and Hinds 1905); evaluations starting on Aug. 4, the field had been treated however, as predicted by Wheeler (1904), none survived. with methyl parathion at 280 gmlha and diflubenzuron at The efficacy of ants in suppressing boll weevil abundance 70 gmlha on June 14 and methyl parathion at 1120 gmlha, is variable. Ants destroyed as many as 84% of the weevils and diflubenzuron at 70 gmlha on July 4. in fallen squares at Overton, Tex. and such mortality aver- The Ellis untreated cotton was grown under dryland con- aged 20% in east, south, central, northeast, and southwest ditions, whereas the USDA field was irrigated once. Soils Texas and western Louisiana (Hinds 1907). Boll weevil on the Ellis farm were black clay, cracking soils while those mortality from ant predation at Rorence, S.C., never ex- in the USDA field were largely the same except for some ceeded 2% during 1925 and 1926 (Fenton and Dunnam sandy portions. 1929). Ant predation was highest in eastern and southern The standard experimental technique used in these exper- Texas and western Louisiana. iments was to stake 100 yellow, flared, weevil-infested squares on the ground in a large X pattern across the cotton Materials and Methods field. Engineering flags on wire posts were thrust through The predatory efficacy of the red imported fire ant was one of the square bracts and pegged to the soil near the base evaluated on the Ellis farm of the Texas Department of Cor- of a cotton plant. The immature weevil in the square was rections (TDC) located north of Huntsville, Tex., on the placed in the shade to eliminate heat and desiccation as important mortality factors. A square was flagged every 4 m I An,honomus gmndis 8cheman (Coleoptera: Curculionidae). 1 SoleIWpsis invicra Buren (Hymenoptera: Formicidae). down the row and over 2 rows to complete each transect of , This research was supported iD part by the NatioDal Science Foundation and the En- vironmental PrOlection Agency. through a grant (NSF G8-34718) 10 the Uniy. of Calif. an X pattern. The same pattern was used in both the Ellis The findings. opinions and recommendations expressed herein arc those of the author and and the USDA fields. This technique minimized any effect not necessarily those of the Uniy. of Calif .• the NSF or the EPA. This work was con- dueled in cooperation with the Agricultural Research Service. USDA, and was p:u1ially of predator clumping. supported by Entomology Cooperatiye Agreement DO. 12-14-100-9752 (33). Ap- proved for publication as TA 14197 by Director. Texas Agricultural Experiment Station. Ragged squares were exposed to field mortality factor Received for publication Apr. 17. 1978 . for 3-7 days before being collected. Each of the squares • Associate Professor, Department of Entomology, Texas A&M Uniyersity. College Station 77843. was carefully examined for evidence of fire ant predation,

parasitization, weevil mortality due to other factors or adult sion was made to treat most fields with azinphosmethyl at weevil emergence. a rate of 281 gmlha. The untreated field had sufficient num- Fire ants were sampled by taking 30 cm of row sample bers of overwintered weevils to damage 15% of the 1st 1/3 units containing at least one plant per 20-25 paces, while grown squares (flower buds) produced. However, it was walking a large circle through the field. At least 25 of these noticed that essentially no square damage resulted after the samples were taken in each field on each sampling date. FI generation had emerged, indicating a high degree of Ants on the soil were counted on the 20 cm of row extend- mortality in the FI immatures. Therefore, we decided to ing 50 cm on each side of the plants. Upon approaching the assess the reasons for this developmental failure. Initially 30-cm sample unit, the foot was stamped firmly on the soil we examined a number of dried squares with boll weevil ca. 10 cm from the plant stalk before attempting to count egg punctures and with characteristic ant entry holes as re- the ants. This stamping action excited the ants and caused ported by Hinds (1907). To confirm our diagnosis of these them to emerge from their holes and crawl about rapidly on entry holes as being ant caused, we exposed several yellow,

the soil surface where they could be counted. Large plants flared and weevil-infested squares to a laboratory colony of Downloaded from https://academic.oup.com/ee/article/7/4/564/2366799 by guest on 24 September 2021 were spread to allow light penetration and to disturb the soil red imported frre ants and predation was observed. The ants surface which assisted in exciting ants near the plant base rapidly distinguished weevil-infested squares from unin- where they frequently congregate. Using this method, fire fested ones, and within minutes workers chewed holes in ants may be found in cultivated fields where no ant mounds infested squares and removed the immature weevils through are present. As a year or more is required for the fire ant the holes. These fire ant holes can be distinguished from mounds to develop to noticeable size (Green 1962), it is of those made by Heliothis larvae or emerging adult weevils. little value to count only mature mounds in cultivated Heliothis larvae generally make a large excavation in the agroecosystems as an estimate of ant densities. square as they feed on the contents, thus leaving a large Boll weevils were sampled using a biased sample tech- hole and a nearly hollow square. Boll weevil adult exit nique. Our action level was set at finding one adult in the holes are characteristically circular and of sufficient size to field and an avg of 2 adultslStoryR trap on the week during allow adult emergence. Furthermore, when there was doubt which the 1st matchhead squares, i.e., flower buds, were that the emergence hole had been caused by an emerging formed. To find the one adult/field, samples were taken in boll weevil adult, the square was dissected and examined areas of the field nearest weevil overwintering quarters or for the hardened pupal cell, pupal exuvium, and adult fecal in the largest cotton plants. Boll weevils often feed on pre- matter. fruiting cotton at the base of the leaf petioles. This feeding Holes made by the fire ant to remove boll weevil larvae causes the leaf to wilt and is sometimes referred to as a and pupae are often oblong in shape and smaller than those ••flagged leaf. " Thus, in sampling for overwintered adults, produced by the emerging Heliothis or boll weevil adult. we walked slowly through the field looking for flagged Fire ants characteristically gain entry into the square by leaves. When one was found, all plants on the 0.5-m row chewing through the flower petals at the distal end of the on each side of the one with the flagged leaf were searched square rather than through the calyx at its basal end. Where for weevil adults. Using this technique one adult was found an empty larval cell was found under the ant entry hole, we in each field within a period of 30 min. were confident in assessing that the larva had been a victim of fire ant predation. Results During the spring of 1977, adult weevils were found in Ellis Farm Study every field at the Ellis farm, including the untreated one. At the Ellis farm through July and Aug. an avg of 61 % Based on these adult counts taken at 1st matchhead square of the immature boll weevils were consumed by the red (flower bud) stage and on finding at least 2 overwintered imported fire ant (Table 1). Ant predation reached a high of weevils in each Story pheromone trap each week, the deci- 85% on July 21 when total larval mortality from all causes

Table I.-Red imported fire ant predation on boll weevil immature stages at the Ellis Farm of the Texas Department of Corrections.

Date Days % ant" % weevil" Conditions Field started exposure Ants/30 em predation survival during exposureh

Untreated 7-12 3 ca. 2.00 44defg 3a D, F Untreated 7-15 ? ca. 2.00 61 efgh 18 b D, F Treated 7-]6 3 ea. 1.00 21 be 46ed D,G&F Untreated 7-15 3 ca. 2.00 75 gh 21 be D,F Untreuted 7-21 7 ca. 3.58 85h 6a D,G&F Untreated 8-3 7 1.70 33 bcde 67 de 5, G Untreated 8-9 7 ca. 1.70 71 gh 25 be D,G Untreated 8-15 7 3.58 64fgh 23 be D,F Untreated 8-23 7 4.97 82h lOa D, F Untreated 8-30 7 ca. 4.97 67 fgh I7b 5,F Untreated 9-6 7 ca. 4.97 73 gh 27 be 5,F Avg 2.95 61 24

2 II Percentages in columns followed by the same letter are not significantly different at the 0.05 level using a X test of independence. h Abbreviations are as follows: D = weather dry; 5 = showers; F = boll weevil infested squares used were yellow, flared, and contained ca. 3rd-instar larvae; G = boll weevil infested squares were green and contained eggs or 1st-2nd instars. 566 ENVIRONMENTAL ENTOMOLOGY Vol. 7, no. 4 was 94%. During both months an avg of 24% of the larvae Other Factors Affecting Fire Ant Predation in flagged squares survived. Before these surviving larvae From 1971-74, a pest management program was dem- become reproductive adults, they are exposed to additional onstrated on the Ellis farm (Casey et al. 1975, Sterling and mortality agents such as spiders, and other arthropod pre- Haney 1973). The essence of the management system was dators, vertebrate predators, disease, climatic extremes, and to use a diapause control program for the boll weevil so that physical impact. It is doubtful that 24% of these weevils in-season chemical control would be unnecessary. As a re- survived to become reproductive adults, especially since sult, entomophagous arthropods were conserved and appar- both pupae and young adults are exposed to these additional ently maintained He/iothis spp. below economically dam- mortality agents. If observations from the insecticide treated aging levels, so that no insecticide applications were needed. field are excluded from Table 1, the avg predation climbs Except for cotton fleahopper control on young cotton, no to 66% and survival drops to 22%. chemical insecticides were applied to the cotton during its Comparison of the 3-day exposure of weevils in the azin- fruiting phase when boll weevils never cause serious eco- phosmethyl-dimethoate treated field to the untreated field nomic damage to the crop. Adult weevil counts averaged Downloaded from https://academic.oup.com/ee/article/7/4/564/2366799 by guest on 24 September 2021 reveals significant difference in predation: 21% in the azin- 0.027,0.052,0.003, and 0.024/plant for the 1971 through phosmethyl field and 75% in the untreated one. On the Aug. 1974 seasons, respectively. 3 cohort another factor reduced predation to 33%. Rain In retrospect, we now have a clearer understanding of the showers following an extended dry period apparently inter- factors which probably assisted in maintaining boll weevils fered with predatory activity of the ants. Also, green in- at such low numbers. Fire ants were relatively scarce in fested squares picked from the plant were less likely to be 1970, but their numbers increased 360-fold during the next attacked by the ant than yellow infested ones. Thus, the 3 yr. The seasonal averages were 452, 17,136, 57,878, yellow, flared, infested squares picked from the plant were and 162,898/ha for the years 1970,1971,1972, and 1973, used in this experiment wherever possible. respectively (Sterling, unpublished data). Thus, we can as- Of the 100 immature weevils used in each cohort some sume that these ants were providing assistance to our dia- were killed by ants, some survived and the remainder suc- pause control program, especially during 1972 and 1973. cumbed to unknown factors. In the latter cases, small, dried Apparently, fire ants and diapause control are fairly com- and shriveled larvae were found in the larval cells and the patible. mortality was assumed primarily due to heat and desicca- Prior to the start of the management program in 1970, tion. No parasites were observed on the dead larvae dis- chemcial insecticides were used extensively against both sected from the squares, and no attempt was made to iden- bollworm and the boll weevil at the Ellis farm. Thus, the tify boll weevil pathogens. low numbers of fire ants in 1970 may reflect the controlling effect of these chemicals on ant abundance. The yearly in- USDA Field Study crease in ant abundance during the management program Hinds (1907) reported that boll weevils generally do may be of great importance. If broad spectrum chemical greater damage in river bottoms (i.e., crop production soil insecticides are used in this ecosystem on any given year, 3 adjacent to rivers) than in upland fields. He suggested that or 4 yr may be required for ant recovery. this may be due in part to the absence of ants in river bot- Upon analysis of the reasons for the different levels of toms where their abundance could be affected by flooding. fire ant predation between the 2 fields during 1977, several We chose to verify our results from the Ellis farm which factors stand out. Difference in ant abundance can be ruled though on river bottom soil is protected by a levee, with out since near equal numbers were counted in each field. additional studies on the unprotected Brazos-Navasota river The major difference between the 2 fields was the size of flood plan where ant densities (avg 3.9/30 cm) were higher the cotton plants. The USDA field had larger plants, espe- (Table 2) than the 2.95 avg on the Ellis farm (Table I). cially in the sandy area, because of favorable rainfall and a However, the level of predation, averaging only 22%, was single irrigation. Rain showers fell more frequently in the considerably lower. Boll weevil survival was also much USDA field than on the Ellis farm. Also, the USDA field higher on the USDA field. received 2 applications of insecticides and releases of Tri-

Table 2.-Red imported fire ant predation on boll weevil immature stages at a USDA field in the Brazos Valley.

Date Days % ant" % weevil" Conditions Field started exposure Ants/30 cm predation survival during exposureb

USDA 3 8-4 7 1.70 15ab 79d S, G USDA 3 8-9 7 ca. 5.53 24bcd 46 de S, G USDA 3 8-15 7 5.53 27 bcde 49 de S, G & F USDA I 8-16 7 3.54 37 cdef 49 de S,F USDA 4 8-17 7 5.60 23 bcd 53d S,F USDA 5 8-17 7 .55 6a 70 de S,F USDA 6 8-20 6 4.83 19b 53d S,F 3.90 22 57

" Percentages in columns followed by the same letter are not significantly different at the 0.05 level using a X2 test of independence. b Abbrevations are as follows: S = showers; F = boll weevil infested squares used were yellow and flared; G = boll weevil infested squares were green and contained eggs or 1st-2nd instar larvae. August 1978 STERLING: BOLL WEEVIL SUPPRESSION BY FIRE ANT 567 10

I- 9 Z c( ~ 8 e__ e 1973 A- 1972 7 a: +--+ 1971 W A- 6 I-'" Z 5 c( w 4

a: Downloaded from https://academic.oup.com/ee/article/7/4/564/2366799 by guest on 24 September 2021 ;&: 3 0 Z 2 C) •• > c( + 1971 0 .. + 20 30 11 21 11 21 31 10 20 30 9 19 JUNE JULY AUG

FIG.1.- Trendsofimported fireantabundanceon theEllisfarmofthe Texas DepartmentofCorrections.

chogramma for Heliothis spp. control were accomplished as the season progresses and provide additive mortality to by mixing the parasites with bran flakes (Jones et al. 1977): the boll weevil. ants may prefer bran to weevils. These are the factors that Also, the dispersion of the fire ant in the cotton field is might have modified the efficacy of the ant as a predator of sufficiently uniform at high densities to provide excellent the boll weevil. In both fields, the ant was observed to be field coverage (Fig. 2). When ant densities reach 9 or 10 essentially ineffective on immature weevil stages in green ants/30 cm of row, none of the sample units were unin- squares and bolls on the plant. However, once abscission of fested. This suggests that, when the ant density reaches 9 or the square occurred or the boll split, predation increased as 10 ants/30 cm of row, any of these sample units selected reported by Hinds (1907). randomly in the field should have near a 100% probability Another factor affecting the predatory efficacy of the fire of having one or more ants, i.e., of being infested. The only ant is shown in Fig. 1. Unlike many other predators, which qualification to this probability is that every 30-cm sample may leave the colton field when they are needed, the worker unit should contain at least one cotton plant. The ant, a fire ant is wingless and apparently does not emigrate read- polyphagous entomophage, is apparently able to utilize sev- ily. Thus, the trend is for fire ants to increase in abundance eral sources of food to achieve this effective spatial distribution. 100 The geographical distribution of the fire ant in the U.S. embraces much of the area currently inhabited by the boll weevil (Fig. 3) Since the ant is currently extending its distribution, it may ultimately provide some degree of boll 75

a 5 10

NO. ANTS PER 30 eM OF ROW iJ/;,FIRE ANT

FIG. 2.-Relationship between ant density and infested 30-em FIG. 3.-Geographical distribution of the boll weevil and the red samples as an index of dispersion. imported fire ant in the U.S. 568 ENVIRONMENTAL ENTOMOLOGY VoI.7,no.4 weevil suppression in many of the cotton-growing areas of Acknowledgment the U. S. where the boll weevil is a problem. I thank Mr. Allen Dean for his technical assistance in Yields these studies and Dr. Akey Hung for ant identifications. At the Ellis farm, 2054 kg of seed cotton were produced! The cooperation of Dr. Roger Ables in allowing ant samples ha in the untreated field compared to only 655 kg in the to be taken from the USDA field is appreciated. We espe- insecticide treated fields. The twice-treated USDA field cially appreciate the assistance of James Anderson, Ronnie yielded ca. 1700 kg of seed cotton/ha. Thus, in these mostly Bush, Buford Smith, and Charles Watley of the Texas De- dry-land cotton production systems, it is possible to produce partment of Corrections and Frank Gilstrap and Robert van ca. 2.47 bales of cotton/ha by utilizing natural mortality den Bosch for their reviews of this paper. agents alone or together with the judiciously applied chemical insecticides. REFERENCES CITED

Discussion Downloaded from https://academic.oup.com/ee/article/7/4/564/2366799 by guest on 24 September 2021 Arant, F. S., K. L. Hays, and D. W. Speake. 1958. Facts about The accidental introduction of the red imported fire ant the imported fue ant. Ala. Agric. Exp. Stn. Highlights of into the southern U.S. is an example of what Coppel and Agric. Res. 5: 2 pp. Mertins (1977) calI fortuitous biological insect pest Buren, W. F. 1972. Revisionary studies on the taxonomy of the suppression. Based on the efficacy data we have presented, imported fue ants. J. Ga. Entomol. Soc. 7: 1-27. it is not inconceivable that were the ant not already here, Casey, J. E., R. D. Lacewell, and W. Sterling. 1975. An example of economically feasible opportunities for reducing pes- serious consideration would be given to its importation into ticide use in commercial agriculture. J. Environ. Qual. 4: the U.S. for the biological control of the boll weevil. Iron- 60-4. ically, because its predatory habits were poorly understood Coppel, H. C., and J. W. Mertins. 1977. Biological Insect Pest the fire ant has been widely condemned as a pest species. Suppression. Springer-Verlag, New York. 314 pp. On a personal basis, coexistence with this insect has not Fenton, F. A., and E. W. Dunnam. 1929. Biology of the COllon proven difficult. I was stung occasionally by the ant when boll weevil at Florence, S. C. USDA Tech. Bull. 112. 76 pp. sampling but generally found it to be a minor annoyance. I Green, H. B. 1962. On the biology of the imported fire ant. J. quickly learned not to stand on its mounds or other areas Econ. Entomol. 55: 1003-4. where it congregates. In the 8 yr I have been working in Grossman, E. F. 1929. Control of the cotton boll weevil by insect close proximity to ants, my research group has experienced enemies. Science. 69: 361-2. Hinds, W. E. 1907. An ant enemy of the cotton boll weevil. only a couple incidents of multiple stings and these were on USDA Bur. Entomol. Bull. 63: 43-8. inexperienced scouts. Stinging of field laborers appears to Hunter, W. D. 1917. The boll weevil problem with special refer- be a relatively minor problem, since most laborers ride on ence to means of reducing damage. Farmer's Bull. 848: field equipment where they are removed from the ants. 4-40. Smith (1936) may be correct in claiming that even though Hunter, W. D., and W. E. Hinds. 1905. The Mexican cotton boll fire ants destroy serious insect pests, these beneficial habits weevil. USDA Bur. Entomol. Bull. 51: 181 pp. will hardly offset their many and serious economic injuries. Hunter, W. D., and W. D. Pierce. 1912. The Mexican cotton- However, since the current probability of fire ant eradica- boll weevil. USDA Bur. Entomol. Bull. 114. 188 pp. Jones, S. L., R. K. Morrison, J. R. Ables, and D. L. Bull. tion seems forlorn, we should carefully weigh its attributes 1977. A new and improved technique for the field release of against its shortcomings. A cost-benefit analysis would en- Trichogramma pretiosum. Southwest Entomol. 2: 210-5. able us to make reliable decisions concerning the value of Mally, F. W. 1902. The boll weevil. Report to the President of conserving the ant where it provides substantial benefit. We Texas A&M College. 70 pp. can, on the one hand, control fire ants in populated areas Pierce, W. D., R. A. Cushman, C. E. Hood and W. D. Hunter. and hay fields, where they are not wanted, and on the other, 1912. The insect enemies of the cotton boll weevil. USDA consider means of conserving them in areas such as cotton Bur. Entomol. Bull. 100: 68-73. fields where they have a tremendous potential benefit. Smith, M. R. 1936. Considerations of the fire ant Solenopsis xy- Of the 55 insect enemies of the boll weevil in the U. S., loni as an important southern pest. J. Econ. Entomol. 29: 120-22. all were native species, which were present before the boll Sterling, W. L., and R. L. Haney. 1973. Cotton yields climb, weevil arrived (Grossman 1929). The red imported fire ant, costs drop through pest management systems. Tex. Agric. a newcomer to the natural enemy complex of the boIl wee- Prog. 19: 4-7. vil, has provided substance to Grossman's contention (1929) Wheeler, W. M. 1904. On the pupation of ants and the feasibility that the natural enemies have continued to become more of establishing the Guatemalan kelep or cotton-weevil ant in important as a limiting factor to boll weevil abundance. the United States. Science. 20: 437-40.