DYNAMICS OF PECAN APfllDS, MONELLlOPSIS PECANIS AND MONELLIA CARYELLA, ON FIELD-ISOLATED SINGLE

LEAVES OF PECAN','

David R. Alverson and William R. English Department of Entomology

Clemson University, Clemson, SC 29634-0365 (Accepted for publication 3 August 1989)

ABSTRACT

Field chambers were developed for studies of aphids exclusive of their prcdutors on single compound leaves of pecall. Populations of two aphid species, Monelliopsis pecQTlis (Bissell) and MOllellia caryella (Fitch), were induced in separate locations to grow from single, isolated third insuns at various periods during the season. Populations failed to achieve long-tenn stability in the enclosed environments and usually declined to zero within several weeks of reaching variable mnximum densities. Seasonal differences in growth rates, population densities, and time supported on leaves were shO\l..n, with autumnal populations having greater stability and slower growth rates than populations induced in the spring or summer.

Key Words: Pecan aphids, yellow pecan aphid, black-margined aphid, MOflelliopsis pecanis, Monellia car)'eJla, population dynamics. Aphididae.

J. Agric. Entomol. 7(1): 29-38 (January 1990)

The impact of foliar-feeding aphids on pecan production is exhibited as intense reduction in fruit quality and yields resulting from reduced photosynthesis in damaged leaf tissues (Tedders and Thompson 1981, Wood et al. 1987, Tedders et al. 1982, Alverson et al. 1983, Wood and Tedders 1985). The loss of pesticide efficacy for aphid control and the heightened awareness of aphid pest status have created a dilemma fol' growers and pecan entomologists (Dutcher and Htay 1985, Beshears 1988). The two species of primary conccm are the yellow pecan aphid, Monelliopsis pecanis (Bissell), and the black-margined aphid, Monellia caryella (Fitch). These aphids also produce copious amounts of honeydew, a medium for the growth of sooty molds which interfere with photosynthesis (Wood and Tedders 1986).

In ..he Southeast, yellow pecan aphids and black-margined aphids may produce up to 30 parthenogenetic generations in as many weeks from May through November (Tedders 1978). Populations usually reach high levels in late spring or early summer and again in fall (Alverson 1981), almost always exhibiting a population crash phenomenon during mid-summer that produces a characteristic bimodal seasonal population 1>I"ofile. M. caryella is morc sensitive to the crash phenomenon than M. pecanis at al1 periods during the growing season (Tedders 1978), but the reasons are not currently understood. Tedders and Gottwald (1985) reported that M. caryella sometimes reject theil' host when aphid numbers are

HOMOlyrERA; Aphididnc. , 1'echnicnl contrihution No. ·1948 of thc South Carolina l~xperimcl1t Station, Clemson University.

29

1

30 J. Agric. Entomol. Vol. 7, No.1 (1990)

large, fly in large numbers above pecan trees and then leave the orchard on wind currents. Anecdotal speculations among pecan entomologists have suggested predator-prey relationships, temperature regimes, and leaf condition as other reasons for the observed seasonal dynamic. The objective of OUI' study was to characterize seasonal population growth patterns when alate aphids are confined to leaves in the absence of natural enemies.

MATERIALS AND METHODS

Small field chambers were constructed of 3-1 plastic soft-drink bottles modified with access panels, ventilation panels and drainage ports covered with Lumite~ saran screen (Fig. 1). These cages were of sufficient size to contain a single compound leaf within a lightweight, wind- and rain-resistent chamber with minimal alteration of environmental conditions. Bottle necks were slit lengthwise to facilitate placement on stems; these slits were taped over with plastic tape. Each chamber was held in place on selected terminals by a collar of rolled foam rubber which also protected the terminal stem from abrasion. Velcro 'M -edged screen covers provided an access opening as well as ventilation. Temperature differences between the interior and exterior of the chambers were checked by hanging pairs of precalibrated thermometers, one within and one outside the bottle, both inside and outside pecan tree canopies in June, 1987. No differences were observed during daylight hours over a 5-d period, and no condensation was ever observed in the bottles. \-Vhen installing the chambers on leaves supporting aphids, leaves were carefully examined for natural enemies, and all but a single third-instal' aphid were removed.

In 1987, preliminary tests were conducted at Lugoff, se, with M. pecanis as the aphid of study. At the beginning of the normal June population peak, four chambers were initiated; aphid numbel's were recorded weekly until no live aphids remained in the chambers. Additional chambers were installed over leaves having the same species in August, four on a 'Stuart' cultivar and foul' on a 'Schley' cultivar. On 17 September, four additional chambers were initiated on trees that had been protected from earlier aphid infestations by treatment with aldicarb (5.6 kg IAIllha) on May 15.

In 1988, all chambers were installed and initiated with third-instal' blackmargined pecan aphids on a single untreated 'Stuart' pecan tree located at Ridge Spring, se. New chambers were added at intervals throughout the season and monitored until each confined population crashed. All contained aphids were identified as M. carye/la. The bottles were then removed and the leaves were monitored for natural recolonization. The seasonal density of naturally occurring M. caryella. was recorded on unconfined leaves of the same tree. Voucher specimens of the aphid species have been placed in the Clemson University arthropod collection.

RESULTS AND DISCUSSION

M. pecanis populations which were contained in the field chambers increased rapidly from the single third instal' aphids initiated on 19 June, 1987, to variable maximums and then decreased to zero as shown in Fig. 2. The maximum increase occurred in the second week post-initiation, resulting in an average 7·fold increase

FC-~

IS---;: AP'--~

VC-A.

'----VP

DP--'A Fig. 1. Representation of field chambers for isolating aphids on single leaves; AP = Access panel; DP = Drainage Port (with

screen); Fe = foam collar (3 X 3 X 18 em); IS = installation slit (taped after inserting terminal stem); TS = terminal stem (with leaves Inot shown] attached); VC = Velcro strip (for attaching velcro bordered access panel); VP = vent. panel (with scree~. ~

32 J. Agric. Entomol. Vol. 7, No.1 (1990)

during that period. In contrast, M. pecanis failed to increase following most initiation attempts in field chambers during the month of August. In 22 start attempts, no leaves on either cultivar supported aphids for more than 2 wks. The period of failed starts coincided with the naturally occurring mid·season lull in the seasonal profile for these aphids. However, by 10 September all attempted initiations were successful, producing growth patterns shown in Fig. 3. Two leaves (not shown) died following population increases to 90 and 30 aphids/leaf over periods of 3 and ,I wks, respectively, presumably due to intense colonization by these aphids.

On the foliage previously protected by treatment (on 15 May) with the systemic insecticide, aldicarb, all growth responses were similar (Fig. 4). These populations had not crashed by the time the observations were ceased on 29 October.

500 .,---------------,

...... ro Cl> -l ...... Cfl U

.c Cl. «

400

300

200

100

~

• ._..__._~:s_ ....v.

--

12 19

June

Stuart A Stuart B Schley A Schley B

Fig. 2. MonelUopsis pecmlis population densities on leaves isolated in field chambers, summer, 1987.

The 1988 assessment of black-margined aphid densities showed 8 typical bimodal pattern on unconfined foliage (Fig. 5). Within chambers initialized at various times dudng the season with M. cQ')rella, the black-margined pecan aphids responded in ways similar to patterns observed for M. pecanis in 1987. Contained populations developed rapidly to a variable maximum and declined rapidly to zero, but the dynamic~ of change were less severe in populations confined on lateseason foliage (Fig. 6). The examples presented were selected from chambers installed in early-season (May-June), mid-season (July-August) and late-season (September-November). Because of the variation in total numbers of aphids obtained in each field chamber, all population growth data were transformed to percentages of cumulative total attained (Fig. 7). Although these transformations may not produce growth cUlves equivalent to those which might be derived from life tables, they provide a mechanism for equilibrating growth cUlves for individual

33 ALVERSON l1nd ENGLISH: Pecl1n Aphid Dynl1mics

300,-------------------,

200

100 Stuart....

ltl Q) ...l

,-III " 'l:l 0 600.s::. Q,

oct

400

200 Schley

6 13 1 9 26 3 10 17 24 1 8

August September October Fig. 3. Monelliopsis pecan;",; population densities on leaves isolated in field

chambers, autumn, 1987. Populations in two chambers on each cultivar failed to develop.

leaves, and the characteristics of their slopes, computed through non-linear least squares regression, allow for seasonal comparisons.

The regression model fitted to these curves was the logistic expression, Y = 11/ (1 +eA + 81:)1 + e, where x = weeks and Y = cumulative % of aphids attained. The parameters of the logistic curves provide the basis for comparisons of derived aspects of population growth given in Table 1 (Draper and Smith 1981). These data indicate that the build-up time period (A/B) for aphids in the field chambers was greater in late season, while growth rates (B/4 and B/6) were reduced. The expression, B/6, is analogous to the slope of a general linear model of population growth. The reduction in the steepness of the slopes of these curves in late season

34 J. Agric. Entomol. Vol. 7, No. I (1990)

300.---------------

... IJ:I 1Il ...l .....

.-III 't:l~ 0.

oCt

Schley A

200

100

II

Schley B Stuart A Stuart B

17 24 1 8 15 22 29

September October

Fig. 4. Monelliopsis pecanis population densities on isolated (confined) foliage previously protected from aphid infestations by aldicarb application in the spring, L987.

30,-----------------

... IJ:I 20 1Il ...l ..... III

'-'t:l~ 0.

oCt 10

MllY Jun Jul Aug Sep Oct Noy

Fig. 5. Naturally occurring (unconfined) Monellia caryella population densities on trees used in 1988 seasonal comparisons.

35

200

100

0..... 400

'" ~ .... en

"'C 200

.I::. a.

0

36 J. Agrie. Entomol. Vol. 7, No. I (l990)

Table 1. Seasonal comparison of regression parameters for the logistic expression of Monellia calJ~lla population growth in field chambers (Y=II/(l + e·O\+lh)l + e).*

PARAi'vIETERSt, t, § SEASONAL SEGMENT AlB B/4 B/6 EARLY (1 MAY - 14 JULY) 3.92a 0.358 0.23a i'vUD (15 JULY - 31 AUG) 3.69ab 0.30a 0.20a LATE (I SEPT - 15 NOV) 5.93b 0.21b 0.14b

• This expression is in tenns of cumulatjo.:e percentage of total aphids recorded per week in the time period from chamuer initiation to I>opuilltion crash ..... ithin chambers.

t Parametric derivlltions from Drupcr nlld Smith (1981), :I: f\/B = midpoinL of regression (,:urvcs in .....eeks (one-hnlf the Lime period from initiation to cmsh);

8/4 = muximUlll slope of regression cUI"\·es. the muximulll rate of change in uccumulating total aphids; 8/6 = average slope of regression curves from initiation to crash.

§ Values in any column follo.....ed by the same leller nrc not significantly different. at the 5% level using linear COlltrasts (LSD).

may be attributed to relative increases in time occupied by aphids on leaves, as the rate funct.ion is based on equilibrated percentages in variable time.

A comparison of actual population variables within the field chambers is given in Table 2. The seasonal divisions are similar to those used for making treatment decisions in control of these aphid species, based on physiological susceptibility of pecan trees to aphid damage (Ellis et al. 1984). They correspond to the three divisions relevant to the bimodal seasonal profile of natw'ally occurring populations: early-season peak, mid-season slump, late-season peak. Aphids stayed on leaves about twice as long in late season as in eady season. This is the reason for the more gradual growth rate in the derived curve parameters for that time.

Table 2. Seasonal comparison of mean (± SE) population density statistics for Monellia caryella contained on individual pecan lcaves.*

MAXIMUM DENSITY TIME ON LEAVES CUMULATIVE TOTAL SEASONAL SEG~'!ENT (APHIDS/LEAP) (WEEKS) APHIDS/LEAF

EARLY (I MAY-14 JUL) 184.7 (82.3)a 5.6 (LO)a 3B 1.6 (206.3).b MID (15 JUL-31 AUG) 104.7 (39.5). 5.1 (0.6)a 195.6 ( 92.4)a LATE (I SEP-15 NOV) 237.0 (56.8)a 10.7 (0.6)b 989.1 (287.l)b

• Meum. in fill)' column followed by Sllme letter are not significnntly different at the a'X level as detennined hy lenst significnnl differences (SAS Institute. Cnf)', NC).

The maximum numbers of aphids attained within the chambers reflect the same modality as obselved in natural population densities, i. e., average maxima were lower in mid season. Accumulating the numbers of aphids recorded on individual leaves within each seasonal division also shows significantly greater (P < 0.05) seasonal support of aphid populations on foliage contained in late season.

Subsequent recolonization of foliage by M. caryella during the period coincident with the normal faU peak was observed on six of the 13 leaves on which aphids had been contained in early season and on one of the seven leaves held in chamber during the mid-season. Mean recolonization density (± SE) in October

37 ALVERSON and ENGLJSH: Pecan Aphid Dynamics

reached 12 (± 5) aphidslleaf, and was not correlated with previous chamber densities. They did not differ significantly from the indigenous population.

These studies indicate that M. pecanis and M. caryellll can be induced to relatively high population densities by confinement to leaves in the absence of natural enemies at any time in the growing season. Om observations (D. R. A., unpublished data) indicate that the seasonal dynamics of natural enemies, though important in pest regulation, would be insufficient in itself to account for the bimodal aphid pattern. The hot temperatures that often accompany population peaks in June and September would seem to discount temperature as the determinant factor also. Therefore, a host-involved mechanism of regulation is suggested. Confined populations of both species grow rapidly to non-maintainable levels and cl'ash without recovery, and the intensity of growth is greater in late season. Although simultaneous studies were not possible, M. caryella appeared easier to colonize on leaf isolates in mid-season than M. pecanis. Growth of the confined population of A1. pecanis was relatively unhindered on foliage that had been protected from previous aphid infestation. LargeI' cumulative M. cwyella populations were obtained by conlinement on late-season foliage.

ACKNOWLEDGMENT

We gratefully acknowledge the management of Friend's ~eck Farms. Lugoff, SC, and J. C. Watson, Ridge S!lring. 8C, for the use of their orchards and facilities; the Coca-Cola Bottling Company, Anderson, SC, for the donation of plastic bottles; L. W. Grimes for statistical analyses; lind D. W. Parler for his assistance in chamber construction.

REFERENCES CITED

Alverson, D. R. 1981. Yellow pecan aphids in Soulh CiII'Olina ol'ch/ll'ds: leanet infestation indices of population density. ,I. Ga. Enlomo!' Soc. 17: 229·236.

Alverson, D. R., C. S. Gorsuch. and J. B. Aitken. 1983. Foliar pests of pecan: effect on nut. quality and yield. Proc. S. E. Pecan Growers Assoc. 75: 67-72.

Beshears, F. 1988. Report of the Federat.ed Pecan Growers of the United States. Proc. S. K Pecan Growers Assoc. 81: 21.

Draper, N. R., and H. Smith. 1981. Applied regression analysis. 2nd Ed., John Wiley & Sons. K.Y. 709 pp.

Dut.cher. J. D. and T. Htay. ]985. Resurgence and insecticide resislllnce problems in pecan aphid management. In Vol. W. Ncel. W. L. Tedders, and J. D. DULcher. leds.1. Aphids and phylloxeras of pecnn. Ga. Agric. Exp. 8ta. Spec. Publ. 38: 17·29.

Ellis, H. C. P. F. Bertrand, and T. F. Crocker. 19811. Pecan pest management in the Southeast. Coop. Ext. 8er. Univ. of Ga. MP 176, 62 pp.

Tedders, "V. L. 1978. Important biological and morphological chumc.:l:cristics of lhe foliUJ" feeding aphids of pecan. USDA Technical Bulletin 1579. 29 pp.

Tedders. W. L., and T. R. Gottwflld. 1985. Flight. behavior of Mor/Cllia caryclla, Monelliopsis pecanis, and Melallocallis caryae{oliae (Hollloptera: Aphididae) during M. caf)'ClIa population crash. In W. W. Ncel, W. L. Tedders. and .1. D. DUlcher, leds.l, AI>hids and phylloxeras of pecan. Ga. Agric. Exp. 8ta. Spec. Pub!. 38: 51-57.

Tedders, W. L., and ,I. M. Thompson. 1981. Histological investigation of stylet. penetration and feeding damage to pecan foliage by three aphids. Misc. Pub!. Entomol. Soc. ArneI'. 12: 69-83.

Tedders, W. L., B. W. Wood, and J. W. Sno\\'. 1982. gffects of fceding by Monel/iopsis nigropunctata. Monel/in caT}cl/a. and Melanocallis COT}'llc{oliae on growth of pecan seedlings in the greenhouse. J. Econ. Entomol. 75: 287-291.

38 J. Agric. Entoma!. Vol. 7, No. 1 (1990)

Wood, B. W., and W. L. Tedders. 1985. Estimates of cncfI,'}' drain by three pecan aphid species and their influence on leaf net photosynthesis. Itl W. W. Ncel, W. L. Tedders, and J. D. Dutcher, Icds.l. Aphids find Phylloxcras of Pecan Univ. Ga. Spec. Publ. 38: 3142.

Wood, B. W., and W. L. Tedders. 1986. Reduced net photosynthesis of leaves from mature pecan tfees by three species of pecan aphids. J. Eotomol. Sci. 21: 355-360.

Wood, B. W., W. L. Tedders. and J. D. Dutcher. 1987. Energy drain by three pecan aphid species (Homoptera: Aphididae) and their influence on in-shell pecan production. Environ. EntomoJ. 16: 1045-1056.