Cereal aphid survival under flooding conditions

Zeitschrift für pflanzenkrankhciten und pflanzenschutz Journal of Plam Díseases and Protectíon ~ 98(2), 168--173, 1991, ISSN 0340-8159 -po © Eugen Ulrrter GmbH & Co., Stuttgart

Cereal aphid survival under flooding conditions Überleben yon Getreideblattlausen unter Überflulungsbedingungen

Jaime E. ARAYA Departamento de Sanidad Vegetal, Facultad de Ciencias Agrarias y Forestales, Universidad de Chile, Casilla 1004, Santiago, Chile, and Department of Entomology, Purdue University, West Lafayette, IN 47907, USA A. FERERES Consejo Superior de Investigaciones Científicas. CIB, Madrid 28006, España Received 29 December 1989; accepted 18 April 1990

Summary

Laboratory colonies of Diuraphis noxia, Macrosiphum avenae, Metopolophium dirhodum, and Rhopalosiphum padi on wheat were used in an experimentdesigned to measure survival of cereal aphids under flooding. Groups of 100 wingless aphids of each species were put into 'h 1 glass jars with 10 cm of rested tap water for treatment periods of 30, 60, 90, 120, 150 and 1.80 min flooding, with six replicates per species. After the time treatments, the floating and submerged aphids surviving were counted. The aphids surviving under water were initíally encased into a small and shining air buble covering their bodies. Floating D. noxia survived longer than the other aphid species; second in survival resulted R. padi, followed by M. avenae and M. dirhodum. Overall, the lowest survival under water occurred with M. dírhodum, followed ínitially by M. avenae. The highest survival occurred with R. padi, followed initially by D. noxia, similarly to the survival of floating aphids. The 50 % mortality time for floating and submerged aphids varied from 2.%-7. lO h and 1.75-2.43 h, respectively. The longest 50 % mortality time for floating aphids occurred for R. padi, followed by D. noxia, and M. dirhodum. The least 50 % mortality time of floating aphids occurred with M. avenae. Among submerged aphids, R. padi had the longest 50 % survival, followed by M. avenae, D. noxia, and M. dirhodum. Sorne of the aphids dislodged by rains in the field may survive flooding for relatively long periods of time. Within - field dispersal of cereal aphids capable of vectoring BYDV may be somewhat íncresed by light rainfall. Key words: Cereal aphids; Diuraphis noxia; flooding, Macrosiphum (Sitobion) avenae;

Metopolophium dírhodum; Rhopalosiphum padi; survíval Zusammenfassung

Im Laboratorium angezogene Kolonien von Diuraphis noxia, Macrosiphum avcnae, Metopo­ lophium dirhodum und Rhopalosiphum padi an \Veizen wurden in einer Untersuchung zum Überleben von Getreideblattlausen bei Überflutung verwendet. Gruppen von je 100 flügello­ sen Blattlausen der erwahnten Arten wurden in 6facher Wiederholung in 0,5 1 fassende Glas­ gefaBe, die 10 cm hoch mit Leitungswasser gefül.1t waren, eingebracht und verschieden lange darin belasscn (30, 60, 90, 120, 150 und 180 min.) Nach Ablauf der Behandlungszeit wurden

pflKrankh.

e r,

2/91

Cereal

169

die sc!Jwimmenden und untergetauchten lebenden 13lattBi.use gezahlt. Die unter Wasser über­ lebenden Blattlause waren anfanglich in einer kleinen, glanzenden Luftblase eirigeschlossen, die ihren Korper umhül1te. SchwiOlmende D. noxia überlebten langer als die anderen Blatt­ lausarten; an zweiter Stelle. stand R. padi, gefolgt von M. avenac und M. dirhodum. 1nsgesamt gesehen überlebte M. dirhodum die kürzeste Zeit unter Wasser, zuerst gefolgt von M. avcnac. Am langsten überlebte R. padi, gefolgt von D. noxia, ahnlich wie bei den schwimmenden Blattlausen. Die Zeit für ein 50(Yoiges Absterben schwankte bei schwimmenden und unterge­ tauchten 13lattlausen von 2,96 bis 7,10 h bzw. 1,75 bis 2,43 h. Bei schwimmenden Blattlausen war bei R. padi die Zeitspanne bis ZUIll 50°!.,igen Absterben am langsten, es foJgten D. noxia und M. dirhodum. Die geringste Zeit wurde bei M. avcnac beobachtet. Bei den untergetauch­ ten B1attlausen dauerte es bei R. padi am langsten, bis 50 % der Lause abgestorben waren, dann folgten M. avenac, D. noxia und M. dirhodum. Einige der Blattliuse, die im Freiland durch Regen abgespült werden, k6nnen Überflmungen relativ lange Zeit überleben. Die Aus­ breitung von Getreideblattlausen, die BYDV übertragen k6nnen, kann innerhalb eines Bestan­ des durch leichten Regen zu einem gevú~sen Grad gef¿¡rdert werden. Stichwórter: Getreideblatdiuse; Diuraphis noxia; Überflutung; Macrosiphum (Sitobion) avc­ nae; Metopolophium dirhodum; Rhopalosiphum padi; Überleben

, f

1

1

Introduction

Cereal aphids are major small grain pests both because of their direct damage and their capacity of vectoring barley yellow dwarf virus (BYDV) (VICKERMAN and WRA1TEN 1979; CARTER et aL 1980), a serious (ESAU 1957; BRUEHL 1961; FITZGERALD and STONER 1967; GILL 1980) and widespread virus disease of diverse graminaceous plants (SLYKHUIS 1962, 1967; CoN TI et al. 1987). Fall and spring migrations of cereal aphids result in the colonization of wínter wheat and other smaIl grains and in the spread of BYDV. The size of the populations mi grating in the spring is an important factor of cereal aphid outbreaks, particularly in years with a large spring migration (CARTER et al. 1982). Therefore, environmental effects on aphid survival as influenced are of primary importance for the dynamics of cereal aphids/BYDV in smaJl grains. In general, me studies on mortality factors and survival of aphids report on the effects of low temperature levels (e. g., HARRISON and BARLOW 1972; \VOOD and STARKS 1972; DEAN 1974; HAND 1980; WILLIAMS 1980; WILLIAMS and WRA1TEN 1987). It is widely accepted mat the rain dislodges many aphids, which would then be.drowned under flooding, resulting in a reduced pest population for the crop. However, after feeding guppy f¡sh, PClecilia (Lebistes) retículata Peters, 1859 (Atheriniforrnes: Poeciliidae), with aphids from greenhouse colonies, we observed several specimens of both the English grain aphid, MacTOsiphum (Sito­ bion) avenae (F.), and dle bird cherry-oat aphid, Rhopalosiphum padi (L.), that were unnoticed by the fish, survived for several hours under water, crawling over me pebbles and plants of the aquarium. Sorne of them moved thejr appendages while suspended in the water, and a few continued feeding with their beaks inserted in oat leaf pieces under water. To clarify the widespread opinion that temporary flooding eliminates cereal aphids, an experiment was designed to measure survival of cereal aphids under flooding. The implications of the results on the population dynamics of cereal aphids and the spread of BYDV on field grown cereals are discussed.

2

Materials and methods

Diuraphis noxia Mordvilko), Macrosiphum avcnae, Metopolophium dirhodum (Walker), and Rhopalosiphum padi specimens from separatecolonies started from a single virginiparous

170

2/91

Ta.ble 1. Tab.1.

pflKrankh.

Mean survival (%; n ~ 100) of Diuraphis noxia, Macrosiphum avenae, Metopolophium dirhodum, and Rh~/,alosip~um padi after different flooding time periods' DurchsehnÍttliehe Uberlebensdauer (%; n = 100) van D. noxia, M:avenae, M. dirhodum und R. padi naeh versehieden langen Überflutungszeiten

D. noxia

M.avenae

M. dirhodum

R.padi

Flooding tiI11f;(h)

FI

Sub

Fl

Sub

Fl

Sub

FI

Sub

0.5 1.0 1.5 2.0 2.5 3.0

99.3a 98.Sa 94.1b 9Mb 8S.3e 83.9d

84.6a 70.7b 55.3e 48.ge 45.2d 39.2e

95.6a n.2b 88.0e 71.2d 61.2e 50Af

66.6a 62 Aa 54.5b 50.4be 48Acd 43Ad

91.4a SS.lb 8Ube 76.3c 65.6d 6Ud

58.4a 53.9ab 51.7ab 45.8be 38Ac 14.2d

97.9a 93.gb 87.5e 86.5c 71.0d 64.2d

81.5a 78.7b 69.0b M.le 49.8d 27.6e

. Fb floating; Sub: submcrged. Pcn:entages in the same column foUowed by different leu:ers are signlfic:mt1y different (P ~ O.OS), acc:ording tO DUNCAN (lIJSS) muitiple range tests.

1

I

i

q

1·

lIJ

apterae of each species colIected at the "El EncÍn" farm in Alcalá de Henarés, Madrid, Spain, were used for our experimento The colonies were maintained on 'Talento' 'wheat (Triticum aesti'Vum L.) in environmental chambers at 21 ±1"C and a 16:8 (L:D) photoperiod in the Dept. ·of Crop Protection, Instituto Nacional de Investigaciones Agrarias, Madrid, Spain. Groups of 100 wingless aphids of each species were put into Vi I glass jars per treatment periodusing a small hair brush. These jars were added 10 cm of rested tap water, and were'kept for treatment periods of 30, 60, 90, 120, 150 and 180 min flooding, with six replicates per aphid species. A magnetic stirrer at minimum speed was used to avoid the aphids from crawling the glass walIs and escaping from the jars during the treatment periods. The floating aphids surviving mee these periods were counted, and the water was filtered through absorbent paper to record survival of submerged aphids. The data obtained, transformed by arcsin vi mortality tO attain a normal distribution, were analyzed through an ANOVA and the survival means were sepa­ rated with DUNCAN (1955) multiple range tests. Fifty percent mortality times for floating and submerged aphids were calculated from 2nd degree polynomial equations between time of exposure and % of surviving aphids. . 3

R~st"ts

and

discu~sion

Once put into the jars, the majority of the aphids tended to float and cluster. As me time periods increased in duranon, the aphids became suspended in the water and many specimens fell to the bottom of the jars, were they, however, continued moving their appendages and survived for variable periods of time (Table 1). In his section on morphological structures and adaptanons of aphids, HEIE (1987) states that the surface of very small animals must be kept dry, partiy because adherent liquid will weigh down the animal body so it hardly can move (a smaller body has a relatively larger surface area), partly because the stigmal pori must not be clogged, and that aphids are generalIy protected by wax against soaking. In our study, the aphids surviving under water were initially encased into a small and shining air bubble covering their bodies. These bubbles did not last long, however, and the aphids died as shown in Table 1. As HEIE (1987) explains, aphids in wet habitats are often covered with spínules or nodules, as Sipba littoralis (Walker), which lives in leaf sheats of Spartina plants in coastal salt marhes, and is able of surviving submergence of the host. The connection between such cuticular structures and their possible funcnon of keeping a film of aír over the body under water would have been first suggested by STROYAN (1955), in the

n

~ .J '¡

Ilophium :lum und

~

~

> .;

Table 2. Tab.2..

t

171

Cereal

PflKrankh. 2/91

'Krankh.

2nd degree polynomíal equations for the survival of wingless (nymphs-and adults) floating and submerged cereal aphids after increasing flooding periods in-the.lahoratQry,. theirco.efficients ofcorrelation and the time for.50 % mortality:. -. '._ :" . __ Polynom 2ten Grades für das:Überleben:von flügeJlosim (Nymphenufi4.Adulte) schwimtnen­ den und untergetauchten Blatdausen nach verschieden'langen Béhanalungszeiten, ihre Kor­ relationskoeffizienten und die Zeiten für die 50%ige Mortalirat

~b

.Sa

Aphid species

.lb .Ob

a) Floating aphids

.le

.8d .6e ccording lO

) Spain,

Yiticum e Dept. oups of using a !atmem ~cies. A ss waIls 19 after record attain a 'e sepaing and time of

¡le time ::cimens ges and tes that

1weigh surface ~nerally

all and

md the 'e often ¡eats of ¡st. The film of , in the

D. noxia M. avenae M. dirhodum R. padi

2: polynomial equations (y=a+bx+cx") y= y= y= y=

100.59 99.976 %.166 98.948 -

1.3595 x 4.1684 x 7.5999 x 0.56836 x -

y= y= y= y=

102.62 - 39.178 x + 6.1357 x' 73.739 - 14.200 x + 1.4164 x" 51.178 + 14.238 x - 8.5329 x' 78.739 + 8.1216 x - 8.2150 x'

104036 x' 4.2900 x" 1.4786 x' 0.89036 x'

R'

Time for 50 % monality (h)

0.981 0.981 0.986 0.968

5.54 2.96 3.58 7.10

0.991 0.985 0.962 0.989

2.12 1.75 2.43

b) Submerged aphids D. noxia M. avenae M. dirhodum R. padi

1.92

description of Aspidaphium cuspidati Stroyan. This author also reported Rbopalosipbum nym­ pbaeae (L.) as another example. HEIE (1987) hypothesizes mat spedal hairs like mose mush­ room-shaped of Subsaltusaphis spp. may secure a thin film of air in case of submergence. The tuberc!e-Iíke stigmal plates covering the stigmal pori as opercula and also the formation of very dense colonies of Staticobium statias Theobald may also be interpreted as protecting devices against harmful action of flooding water (HU.-LE RIs LAMBERS 1939; MOLLER 1975). However, these adaptations have been conjectured but not proved (HElE 1987). By comparing survival of aphids floating, it appears that D. noxia, with a smaller body size and a noticeable wax shield covering its cuticle, survived longer than me omer aphid species, as a greater proportion of specimens floated on the water for a longer period of time. Second in survival on the surface resulted R. padi, followed by M. avenae and M. dirhodum, the aphid with me largest body size of all species tested. The relative high survival of floating D. noxia under flooding conditions is particularly interesting. One of the reasons given to argue that me Russian wheat aphid will not infest USstates to me east of its actual distribution in 15 western states (KINDLER and SPRINGER 1989) is that this insect Uves in arid and semi-arid regions, and that it is not well adapted to humid environments. This is yet to be proved, particularly as mis aphid can survive winter and summer in many graminaceous species (KINDLER and SPRINGER 1989). Its poor adaption to cok! was also hoped for creating a barrier to this aphid in its northward dispersion from the first detection point in Texas in 1986 (FERERES et al. 1986; ARAYA et al. 1987). So far, D. noxia has spread to Alberta and Saskatchewan in Canada. Overall, the lowest survival under water was obtained with M. dirhodum, followed initially by M. avenae. These twO species have larger bodies that may have been more affected by hydraulic pressure forces than smaller-bodied aphids, which may help explain meir relatively higher mortality both on the surface and under water. The highest survival occurred wim R. padi, and initially with D. noxia, similarly to me survival of floating aphids. The time for reaching 50 % mortality varied from 2.96 to 7.10 h for floating aphids, and from 1.75 to 2.43 h for submerged aphids (rabIe 2). The longest 50 % mortality time for floating aphids occurred for R. padi, foIlowed in decreasing order by D. noxia and M. dirhodum. The least time for 50 % mortality of floating aphids occurred with M. avenae.

172

Among submerged aphids, the longest 50 % survival occurred wirh R. padi, followed· in decreasing arder by M. avena,e; D. noxia, and M; dirhodum. Anholocyclic overwintering popularions of M. avenai/on wheat iñsoumern England are of particular importance as they alIow within-field spread of BYDV from autumn onwards and earl)' population increase on the crop ¡nthe spring (W1LLlAMS and WRATTEN 1987). A study of rhe hiology of R. p,¡di in winter wheat in northwestern Indiana revealed rhat rhe greatest numbers of the bird cherry-oar aphid were found on volunteer wheat planrs before planting wheat in the fall. These volunteer plants provided BYDV-infested alate migrants for the newly planted whe.1t crops. Although the populations of this aphid during the 2 years of the study were small, the aphids helped spread BYDV (ARAYA et al. 1987). Within-field dispersal of cereal aphids capable of vectoring BYDV may be somewhat increased by short rains. A portion of the popularíon of aphids that are dislodged may survive f1ooding, as demonstrated in this study. Further studies are necessary in the field to determine the effect of rain/flooding on cereal aphid survival.

literature ARAYA, J. E., A. FERERES, J. E. FOSTER: Progress report on' the distribution of the Russian wheat aphid, Diuraphis noxia, in the United States. - FAO PI. Prot. BulL 35, 79-82, 1987. ARAYA, J. E., J. E. FOSTER, S. E. CAMBRON: A srudy of the biology of Rhopalosiphum padi (Homoptera: Aphididae) in winter wheat in northwestern Indiana. - The Great Lakes Ent. 20, 47-50, 1987. BRUEHL, G. W.: Barley yellow dwarf, a vims disease of cereals and grasses. - Monograph N° 1, Am. Phytopath. Soc., 52 pp., 1961. CARTER, N., A. F. G. DIXON, R. RASSINGE: Cereal aphid populatíons: biology, simulation and prediction. - Centre for Agricultural Publishing and Documentation, Wageningen, The Netherlands, 91 pp., 1982. CARTER, N., I. F. G. McLEAN, A. D. WATI', A. F. G. DIXON: Cereal aphids: a case study and review. - Appl. Biol. 5, 271-348, 1980. CONTI, M., C. J. D'ARCY, P. A. BURNETI: The yellow "plague" of cereals: Barley yellow dwarf virus. - Proc. CIMMYT Workshop on Barley Yellow Dwarf, Udine, ltaly, July 6, 1987, Il, 99 pp., 1987. DEAN, G. J.: Effects of temperature on the cereal aphids Metopolophium dírhodum (WIk.), Rhopalosiphum padi (L.) and Macrosiphum avenae (F.) (Hem., Aphididae). - Bul!. ent. Res. 63,. 401-409, 1974. DUNCAN, D. B.: Multiple range and multiple F tests. - Biometncs 11, 1-42, 1955.

ESAU, K.: Phloem degeneration in gramineae affected by the barley-yellow dwarf virus. - Am.

J. Bot. 44, 245-251, 1957. FERERES, A., J. E. ARAYA, J. E. FOSTER: The Russian wheat aphid, a new pest on cereal crops in the United Sutes, and a potential threat to soft red winter wheats. - Purdue Univ. Agríe. Exp. Stn. Bul!. N° 510, 27 pp., 1986. F1TZGERALD, P. J., W. N. STONER: Barley yellow dwarf studies in wheat (Tríticum aestivum L.). I. Yield and quality of hard red winter wheat infected with barley yellow dwarf vims.­ Crop Sci. 7, 337-341, 1967. GILL, C. Assessment of losses on spring wheat naruraUy infected with barley yellow dwarf virus. - PI. Dis. 64, 197-203, 1980. HAND, S. Overwinteringof cereal aphids. - Bul!. SROP 3, 59-61, 1980. HARRISON, J. R., C. A. BARLOW: Population-growth of the pea aphid, Acyrthosiphon pisum (Homoptera: Aphididae) after exposure to extreme temperatures. - Ann. ent. Soco Am. 65, 1011-1015, 1972. HE1E, O. E.: Morphological structures and adaptions. - In: MINKS, A. K., P. HARREWIJN

c.: c.:

PfIKrankh.

2/91

Cereal

conditions

173

(eds.): Aphids, their biology, natural enemics and control, pp. 393-400. Vol. 2 A World crop pests, Elsevier ArflSterda!1l, 1987. HILLE RlS LAMBER~'cD.: CótÍtr'ibution; to a monogr.aph of the Aphididae of EuroRe. n.TIte genera Dactynotus Rafinesque, 1918; Staticobium.oMordwilkó,1914; Macrosipbum Passe­ rini, 1860; Masonapbis nov." gen.; Pbaralis Leach,-1826. -Temminckia 4, 1-134, 1939. KINllLER, S. D., T. L. SPRINGER: Alternate hosts óf" Russian wheat aphid (Homoptera: Aphididae). - J. econ. Ent. 82, 1358-1362, 1989. MÜLl.ER, F. P.: Verbreitung und Biologie der submersen Blattlaus Aspidaphium cuspidati Stroyan, 1955, und anderer Wasserpflanzen-Aphiden. - In: Verhandl. 6. Imerqat. Symp. Entomofaunistik, pp. 47-53, Junk, The Hague, 1975. SLYKI-IUIS, J. T.: An international survey for virus diseases of grasses. - FAO PI. Prot. BullIO, 1962. SLYKHUlS, J. T.: Virus diseases of cereals. Rev. appl. Myco\. 46,401-429, 1967. STROYAN, H. L. G.: Recent additions to the British aphid fauna. Pan 11. - Trans. R. ent. Soco Lond. 106, 283-340, 1955. VICKERMI\N, G. P., S. D. WRATIEN: The biology and pest status of cereal aphids (Hemiptera: Aphididae) in Europe: a review. - Bull. em. Res. 69, 1-32, 1979. WILLlAt.IS, C. T.: Low temperature mortality of cereal aphids. Bul!. SROP 3, 63-{'6, 1980. WILUAMS, C. T., S. D. WRATIEN: The winter development, reproduction and lifespan of viviparae of Sitobion avenae (E) (Hemiptera: Aphididae) on wheat in England. - Bul\. enl. Res. 77, 19-34~ 1987. WOOD, E. A., JR., K. J. STARKS: Effect of temperature and host plant imeraction on the biology of three biotypes of the greenbug. - Envir. Ent. 1,230-234, 1972.