Allelochemicals as Determinants of Insect Damage Across the North

Chapter 39

Allelochemicals as Determinants of Insect Damage Across the North American Continent Biotypes and Biogeography J. Mark Scriber , M. T. Stephen Hsia, Pius Sunarjo , and Richard Lindroth 1

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Downloaded by UNIV OF MICHIGAN ANN ARBOR on September 18, 2015 | http://pubs.acs.org Publication Date: January 8, 1987 | doi: 10.1021/bk-1987-0330.ch039

Department of Entomology, University of Wisconsin, Madison, WI 53706

Insects feeding on plants have varying degrees of specificity which are related to the chemistry of the leaves (or other plant part) fed upon and also to the behavioral, physiological, and ecological adaptations of the insect itself. To permit understanding of the ecological significance of allelochemicals in agriculture and forestry, our research efforts must deal with the interactions of insects and their food plants at a l l of these levels of biological organization. As an agricultural example, we describe how a change in foodplant preferences has resulted in an obscure and virtually unknown insect (the hop vine borer, Hydraecia immanis, a Noctuid moth) becoming a major pest of corn in Wisconsin and adjacent states. As an example of tree-feeding insects, we describe our recent research with tiger swallowtail butterflies (Papilionidae). We have directed particular attention upon tulip poplar ( Liriodendron tulipifera) and quaking aspen (Populus tremuloides) because of their dramatically different underlying allelochemical effects on related insect herbivores. We emphasize the ecological implications of the differences in leaf chemistry between these plant species because the temporal, spatial, qualitative, and quantitative aspects of phytochemistry are so poorly documented. Nonetheless we are currently attempting to identify the specific chemical(s) involved and their mode of action against "unadapted" species, subspecies, and geographic populations. Subtle differences in a lielochemically based host preference and/or the ability to survive on various hosts may have very significant implications for the population dynamics and geographical ecology of insects (1-4). Differential adaptations 1

Current address: Department of Entomology, Michigan State University, East Lansing, MI 48824 Current address: Department of Plant Protection, College of Agriculture, Hasanuddin University, Ujung Pandang, Indonesia

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0097-6156/87/0330-0439$06.00/0 © 1987 American Chemical Society

In Allelochemicals: Role in Agriculture and Forestry; Waller, G.; ACS Symposium Series; American Chemical Society: Washington, DC, 1987.


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of phytophagous insect species to the various allelochemicals i n their hosts w i l l generally be accompanied by a number of other behavioral, physiological, morphological, and ecological adaptations. A recent review by Diehl and Bush (4_) proposes the following c l a s s i f i c a t i o n to help standardize terminology regarding the term "biotype"; (1) nongenetic polyphenisms (also called ecomorphs or phenocopies) i n which the same genotype produces various phenotypes i n different environments, (2) polymorphic and/or polygenic variants within populations (due to discontinuous or continuous v a r i a t i o n within a freely breeding population with a genetic b a s i s ) , (3) geographic races, which are geographically isolated biotypes (e.g. semispecies or subspecies), (4) host races as "a population of a species that i s p a r t i a l l y reproductively isolated from other conspecific populations as a d i r e c t consequence of adaptation to a s p e c i f i c host" (whether due to i s o l a t i o n by host preference, host-associated allochronic i s o l a t i o n , or some other form of assortative mating a r i s i n g as a d i r e c t r e s u l t of different host use), and (5) species as "natural populations that are reproductively isolated from one another and that follow d i s t i n c t and independent evolutionary paths" (with s i b l i n g species morphologically so s i m i l a r that recognition requires additional careful studies of biochemical, c y t o l o g i c a l , or behavioral t r a i t s ) . These five categories are not necessarily mutually exclusive, and we do find biotypes at several stages of evolutionary divergence amid various processes of speciation (_5). While allelochemicals are fundamentally important considerations i n the development of host s h i f t s , host races, and speciation, they are only part of the ecological/evolutionary story, and by themselves f a l l far short of explaining insect/plant interactions, even at the chemical l e v e l (6, 7). Variation i n a g r i c u l t u r a l / s i l v i c u l t u r a l systems for herbivory intensity must consider insect genetics as a major future research e f f o r t . Our f i r s t example concerns a new midwestern corn pest, the hop vine borer (HVB), Hydraecia immanis Guenee, and i t s introduced congener the potato stem borer (PSB), U_. micacea Esper. A major s h i f t in host use from hops to corn has occurred suddenly with the HVB, and this has resulted i n s i g n i f i c a n t economic losses for growers. This danger i s complicated by the a r r i v a l i n Wisconsin of the more polyphagous r e l a t i v e (the PSB) and the fact that the expanding geographic d i s t r i b u t i o n s with economic damage to corn for both species has brought them into natural contact. Our second example concerns the North American tree-feeding swallowtail b u t t e r f l i e s of the Papilio genus (Papilionidae: Lepidoptera). In this species complex, we observe reciprocal i n a b i l i t i e s of c e r t a i n taxa to u t i l i z e the favorite foodplant families of other taxa, implying phytochemically based negative genetic correlations (8). Geographic v a r i a t i o n in the a b i l i t i e s of various populations of a given subspecies or species to accept/consume/grow and reproduce on plants of these families i s also s i g n i f i c a n t (2,3). A Recent Example from Midwest Agriculture The hop-vine borer (HVB), Hydraecia immanis Guenee, i s a stemfeeding c a t e r p i l l a r (Lepidoptera: Noctuidae) which has only very recently l>een causing severe l o c a l i z e d damage to corn i n large portions (more than 50 different counties) of Wisconsin, In Allelochemicals: Role in Agriculture and Forestry; Waller, G.; ACS Symposium Series; American Chemical Society: Washington, DC, 1987.


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Minnesota, Iowa, and I l l i n o i s (9). As indicated by i t s common name, the hop-vine borer had been found i n close association with hop (Humulus lupulus) plants. Wild hops, found from the east coast of the U.S. to the Rocky Mountains, presumably served as the primary host f o r the insect i n North America (10) for the l a s t 100-150 years or longer. In Wisconsin, hop production during the l a s t century was concentrated i n several southern counties where the f i r s t reports of serious l a r v a l damage (HVB) to corn also originated. Although there has been e s s e n t i a l l y no commercial hop production east of the Rocky Mountains since the 1930's , small patches of wild or escaped hop along roadsides and drainage ditches near heavily damaged cornfields have been located and H. immanis larvae were found feeding on below-ground portions of these plants (9)* Thus i t appears that isolated endemic populations have continued to e x i s t even i n the absence of the hop industry and that the HVB has been able to make the t r a n s i t i o n from i t s grass/hops feeding habit to a grass/corn feeding pattern i n these areas (9,11). Since hop i s a perennial and corn i s an annual, this transition i n l a r v a l feeding has c e r t a i n l y been favored by continuous corn production since the 1940's that has made corn a dependable HVB resource. Reasons for the lack of any outbreaks i n corn prior to 1975 are unknown at this time, but i t i s possible that the general use of chlorinated hydrocarbons (e.g., DDT, Aldrin, and Dieldrin) i n the two decades previous to 1970 maintained a general suppressive e f f e c t upon H. immanis. It i s also possible that small populations have only recently been forced onto corn with the removal of perennial hop plants or other hosts along f i e l d edges as a r e s u l t of changing agronomic practices and/or increased herbicide use such as 2,4-D and 2,4,5-T. In any case, poor weed control, continuous corn culture, n o - t i l l , conservation t i l l a g e , and reduced t i l l a g e favor increasing insect population densities and increase the potential for further spread i n the corn b e l t . In Europe, a congeneric potato stem borer (PSB), H_. micacea Esper, i s a problem i n potatoes, as i t i s also i n corn and many other crops such as sugar beet, rhubarb, onions, tomatoes, strawberries, and raspberries i n Scandanavia, the United Kingdom, Russia, and Canada. The PSB has been well established i n Canada since the turn of the century, reaching New York State by the mid1970 s. The PSB has since appeared f o r the f i r s t time as f a r west as Manitoba (C. E l l i s , pers. comm.) and recently (1982) i n Manitowoc and Kewaunee counties of Wisconsin. In 1984, economically damaging levels of potato stem borers i n corn were detected i n several locations of Calumet County, Wisconsin. Because of their similar l i f e cycles, habits, damage to corn, and apparent resistance to conventional corn rootworm i n s e c t i c i d e s , we could expect both the PSB and HBV to increase their densities and/or range throughout the Midwest much as the PSB has (9,12). These concerns are evident i n the 1985 establishment of a multistate regional research e f f o r t e n t i t l e d "Impact of integrated crop management practices on European corn borer and related stalk boring insects". In summary, undetermined factors have recently led to increased l o c a l densities of hop vine borers, Hydraecia immanis, i n the midwest with intense economic damage on corn. This change i n feeding behavior from grass/hops to grass/corn has mediated an apparent geographic range expansion. A simultaneous but even more rapid range expansion of the introduced polyphagous potato stem 1



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borer, Hydraecia micacea, has occurred westward across Canada and into Wisconsin. It i s unknown whether or not the wider range of acceptable hosts of the PSB has f a c i l i t a t e d the more rapid range expansion than observed for the HVB. These facts i l l u s t r a t e the need f o r understanding the ecological as well as the allelochemical factors involved i n host race or biotype formation i n phytophagous insect species. It i s important to be able to predict these s h i f t s i n host usage or a t least understand what factors w i l l delineate new geographic range l i m i t s . A cursory perusal of Gibbs (13) has shown no known secondary chemicals i n common for Zea mays L. and Humulus lupulus L. although preadaptation to corn might be expected on the basis of the a d u l t oviposition preferences for grasses. This relationship w i l l receive much more attention i n the near future, owing to i t s economic importance. North American D i s t r i b u t i o n of Tree-feeding P a p i l i o Within Section III of the Papilionidae i t i s tempting to assume that evolutionary resource p a r t i t i o n i n g of foodplants v i a s p e c i a l i z a t i o n a t the plant family l e v e l has occurred (8,14). For example, we generally observe P. t r o i l u s L. on spicebush, Lindera benzoin, and palamedes Drury on red bay, Persea borbornia (both i n the Lauraceae); Papilio eurymedon Lucas on Rhamnaceae; JP. mul ticauda tus Kirby on Rutaceae; the Ca l i f ornia J?. rutulus Lucas on Platanaceae; _P. canadensis R & J and Rocky Mountain _P. rutulus on Betulaceae and Salicaceae; and P. a u s t r a l i s Maynard on only sweetbay, Magnolia v i r g i n i a n a , of the Magnoliaceae. Such patterns of feeding s p e c i a l i z a t i o n i n P a p i l i o have been the basis of many discussions regarding the so-called "chemical arms race" and "coevolution" (15). Since these insects do not migrate or move great distances, the geographic d i s t r i b u t i o n s of insect taxa (Figure 1) are of course closely a l l i e d with the current d i s t r i b u t i o n of their host plants. In fact, the primary factor that has enabled J ^ . g_. canadensis to inhabit Canada (Figure 1) may be the a b i l i t y to u t i l i z e foodplants of the Salicaceae (e.g. , Populus tremuloides Michx., _P. balsamifera L., V. grandidentata Michx., and various Salix spp.) and Betulaceae (e.g. , Be tula papyrifera Marsh and Alnus spp.). These are e s s e n t i a l l y the only suitable foodplants for ^P. glaucus available at latitudes north of 50° (16). The southern subspecies _P. glaucus and j?. g. a u s t r a l i s favor the Magnoliaceae and do not survive well on plants of the Salicaceae and Betulaceae (2_). In the l a s t two years we have investigated the phytochemica1 basis of these d i f f e r e n t i a l u t i l i z a t i o n a b i l i t i e s for P a p i l i o larvae on selected plant species of the Salicaceae and Magnoliaceae. Several compounds have been isolated from leaves of both quaking aspen and t u l i p tree that exhibit b i o l o g i c a l a c t i v i t y against larvae of the highly polyphagous southern armyworm, Spodoptera eridania Cram. (Lepidoptera: Noctuidae) (17,18). While s a l i c i n was extracted i n high concentrations from quaking aspen and i s known to have multitrophic l e v e l effects (19), the most active armyworm antifeedant extracted, isolated, and i d e n t i f i e d i n our studies to date was 1,2-benzenediol (pyrocatecho1). Similar feeding preference tests have been conducted with penultimate and f i n a l instars of Papilio g. glaucus and suggest



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D

F i g u r e 1. The g e o g r a p h i c d i s t r i b u t i o n and f a v o r i t e foodplant f a m i l i e s o f the t i g e r s w a l l o w t a i l s o f North A m e r i c a .



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that pyrocatechol may represent one of the important compounds involved i n the non-usage of Salicaceae by larvae of this subspecies. For example, several d i f f e r e n t leaf surface concentrations from 24 g/cm^ to 19 6 g/cm^ a l l s i g n i f i c a n t l y reduced preference and feeding rates on painted black cherry leaves (data of J. Hainze and P. Sunarjo i n Scriber; 20). Also, we have recently discovered that even the Salicaceae-adapted individuals of the northern subspecies, P. g. canadensis, are adversely affected by the quaking aspen constituent pyrocatechol, s a l i c i n , and i s o n i a z i d . These compounds s i g n i f i c a n t l y increased metabolic costs and/or suppressed growth rates for penultimate instar larvae of _g. canadensis (21). S i m i l a r l y , sesquiterpene lactones from t u l i p trees have been found to be most l i k e l y responsible for deterrent and toxic effects against even the "adapted" g_. glaucus subspecies (2 2). Presently, phenolics and terpenoids are the only major c l a s s of secondary plant compounds reported to occur i n the Salicaceae (Table I) (aos 36-39). Among the array of potential secondary compounds i n Populus tremuloides that may be involved i n our observed antixenosis/antibiosis to the J?. glaucus and _P. g_. a u s t r a l i s subspecies are those l i s t e d i n Table I. Only recently has isoniazid (a pyridine alkaloid) been isolated from quaking aspen leaves (Sunarjo, 40). By contrast, the composition of secondary compounds i n t u l i p trees (Table II) and other Magnoliaceae i s highly diverse, including sesquiterpene lactones (42, 48, 50, 52, 54), benzylisoquinoline a l k a l o i d s , cyanogenic glycosides, and various essential o i l s (13,55,56). Table I. Secondary Compounds Identified In Leaves and Bark of Quaking Aspen (Populus tremuloides Michx)

Compounds Chrysin _p-Coumaric acid 1-p-Coumaroylglucose Gentisyl alcohol Grandidenta t i n Pinocembrin Populin Pyrocatechol (catechol) Quercetin Qu e rce t i n - 3 -g a lac tos ide Querce tin-3 -glucoside Querce tin-3-ru tinoside Rhamnetin Sa l i e in Salicortin S a l i c y l alcohol Salicyltremuloidin Salireposide Succinic acid Tremulacin Tremuloidin Triploside

Leaves, References 23

Bark, References 24 24 24 13,25,26

13,23 27-29 29,30 23 29 29 29 26,29 13,23-25,31 13,23,31 13,31 13,24,25,29-31 26,29 13,23,25,26,31, 34 13,24,25,28-30 30

27

26 13,23,31-33 13,23,25,26,31 24 26,32,33 13,23,25,26,31 13,31,33,35


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Table II. Secondary Compounds Identified from Parts of Tulip Tree (Liriodendron t u l i p i f e r a L.) Tissue of B i o l o g i c a l Co mpounds Origin activity (-)-N-Acetylanonanine HW (-)-N-Acetylnornuciferine HW (-)-N-Ac e tylasimilobine HW (+)-N-Ace tylnornantenine HW As imilobine HW -Cyclolipiferolide L Cos tunolide RB cytotoxic Dehydroglaucine HW 11,13-De hydro lanuginolide L Dihydrochrysanolide L Epitulipinolide RB cytotoxic E p i t u l i p i n o l i d e diepoxide cytotoxic L Ep i tulipd ienolide RB Glaucine HW H-( 2 -Hy d roxy - 2 -p heny 1 e thy 1 ) benzamide Β Laurenobiolide L Lipiferolide cytotoxic L -Liriodenolide RB - L i riodenolide RB -Liriodenolide L cytotoxic Li rionol Β Liriodendritoi L i riodendronine SW Liriodenine HW


a

Reference(s) 41 41-4 41,43,44 41 43,44 45 46 43,44 45 45 42,47,48 42 42,48 13,43,44 49 45 42,50 45 45 4 2,50 49 13 51 13,43,44, 50

(+)-3-Me thoxy-Nacetylnornantenine HW 41 O-Methy1-N-norlirinine Β 49 O-Me thylatheroline HW 43,44 Norushinsunine HW 43,44 Pe roxyferolide antifeedant 52 L (+) -Pinoresinol Β 49 13 Saponins L Syringic acid methyl ester Β 49 (+)-Syringaresinol HW 43 Syringaresinol d i - -glucoside Β 53 (+)-Syringaresinol dimethyl HW 43 e ther Syringaldehyde 43 HW (+)-Syringaresinol Β 49 Tulipinolide RB cytotoxic 46-8 Tulirinol L antifeedant 54 (-)-Tuliferoline 41 HW B = Bark; RB = Root bark; HW = Heiirtwood; L = Leaves; SW = Sapwood e

In addition to the unique and quite dramatic differences i n feeding/surviva1 of larvae of the P. glaucus complex and their hybrids (20) (Table III), t u l i p tree and quaking aspen represent phytochemically intriguing foodplants for several other North


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American insects (see 18). For example, both plants are unacceptable/unsuitable as food for two notoriously polyphagous insects, the cecropia silkmoth, Hyalophora cecropia (57), and the southern armyworm, Spodoptera eridania (Cram.) (3).


Table III. Survival of P a p i l i o glaucus Subspecies 1st instar (neonate) on Three Foodplant Species (1978-1985; Madison, WI). (after Scriber; j^,20) Eastern Tiger swallowtail subspecies

Survival percentage of newly hatched c a t e r p i l l a r s on potential foodplants quaking black tulip tree aspen cherry

_P.

canadensis (n)

7% (420)

glaucus (n)

81% (2117)

Α.-

80% (358)

74% (287 2)

7% (209 1)

81% (5514)

Conclusions Ecological interactions with insect herbivores i n agriculture and forestry depend to a s i g n i f i c a n t extent upon the various allelochemicals and nutrients i n the plant tissues. Superimposed upon this dynamic phytochemical foundation (with d a i l y , seasonal, taxonomic, and stress-induced v a r i a t i o n s ) , the behavioral, p h y s i o l o g i c a l , and ecological v a r i a t i o n i n the herbivore populations render an understanding of the s p e c i f i c mechanisms of chemical adaptation and counter-adaptation d i f f i c u l t indeed. Even with a single chemically defined allelochemical, the mode of action i s variable (dose-dependent, and situation-dependent; 3,58) and the insect response i s not e a s i l y categorized as to whether the effect i s primarily behavioral (e.g. deterrence, or suppressant) or physiological (e.g. toxic; 59). Acknowledgmen ts This research was supported i n part by the National Science Foundation (DEB #7921749, BSR #8306060, and BSR #8503464), by USDA grant #85CRCR-1-1598, the Graduate School and the College of Agriculture and Life Sciences (Hatch 5134), and i n part by NC-105 and NC-180 Regional Research. We thank Mark Evans, Bruce Giebink, John Hainze, William Kraemer, Syafrida Manuwoto, and John Wedberg for their assistance i n various aspects of this work.

Literature Cited 1. 2. 3.

Fox, L.R.; Morrow, P.A. Science, 1981, 211, 887. Scriber, J.M. In "Variable Plants and Herbivores in Natural and Managed Systems"; Denno, R.F.; McClure, M.S., Eds.; Academic Press: New York 1983; pp. 373-412. Scriber, J.M. In "Chemical Ecology of Insects"; Bell, W.; Carde, R.T. Eds.; Chapman and Hall: London, 1984; pp. 159202.


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4. 5. 6. 7.


8. 9. 10. 11. 12. 13. 14. 15. 16. 17. 18. 19. 20. 21. 22. 23. 24. 25. 26. 27. 28. 29. 30. 31. 32. 33. 34.

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Diehl, S.R.; Bush, G.L. Ann. Rev. Entomol 1984, 29, 471. Barton, N.H.; Charlesworth, B. Annu. Rev. Ecol. Sys t. 1984, 15, 133. Scriber, J.M.; Slansky, F., Jr. Ann. Rev. Entomol. 1981, 26, 183. Slansky, F.; Scriber, J.M. In "Comprehensive Insect Physiology, Biochemistry, and Pharmacology"; Kerkut, G.A.; Gilbert, L.I., Eds.; Pergamon Press: Oxford, 1985; Vol. 4, pp. 87-163. Scriber, J.M. In "Chemical Mediation of Coevolution"; K.D. Spencer, Ed.; AIBS Symposium, Gainesville, FL, 1986, in press. Giebink, B.L.; Scriber, J.M.; Wedberg, J.L. Environ. Entomol. 1984, 13, 1216. Forbes, W.T.M. Cornell Univ. Agric. Exp. Sta. Memoir #329, 1954. Scriber, J.M.; Hainze, J.H. In "Insect Outbreaks: Ecological and Evolutionary Processes"; Barbosa, P.; Schultz, J.C., Eds.; Academic Press: New York, 1986, in press. Deedat, Y.D.; Ellis, C.R. J. Econ. Entomol. 1983, 76, 1055. Gibbs, R.D. "Chemοtaxonomy of Flowering Plants"; McGillQueens university Press: Montreal and London, 1974, 4 volumes. Brower, L.P. Leρid. News 1958, 12, 103. Feeny, P.P.; Rosenberry, L.; Carter, M. In "Herbivorous Insects: Host Seeking Behavior and Mechanisms"; Ahmad, S., Ed.; Academic Press: New York, 1983; pp. 27-76. Scriber, J.M. Tokurana (Acta Rhopalocerologica) 1984b, Nos. 6/7, 1. Sunarjo, P. I.; Hsia, M.T.S. In American Chemical Society, National Meeting, 1984, abstract 108. Manuwoto, S.; Scriber, J.M.; Hsia, M.T.; Sunarjo, P. Oecologia 1985; 67, 1. Smiley, J.T.; Horn, J.M.; Rank, N.E. Science 1985, 229, 649. Scriber, J.M. In "Molecular Mechanisms in Insect Plant Interactions"; Brattsten, L.B.; Ahmad, S., Eds.; Plenum Press: New York, 1986, in press. Lindroth, R.L.; Scriber, J.M.; Hsia, M.T.S. (submitted; J . Chem. Ecol.) Lindroth, R.L.; Scriber, J.M.; Hsia, M.T.S. (submitted; Oecologia) Palo, R.T. J . Chem. Ecol., 1984, 10, 499. Pearl, I.Α.; Darling, S.F.; DeHaas, H.; Loving, B.A.; Scott, D.A.; Turley, R.H.; Werth, R.E. Tappi, 1961, 44, 475. Thieme, H.; Benecke, R. Pharmazie, 1970, 25, 780. Thieme, H.; Benecke, R. Pharmazie, 1971, 26, 227. Pearl, I.Α.; Darling, S.F. Tappi 1964, 47, 377. Pearl, I.A. Darling, S.F. Tappi, 1965, 48, 506. Kinsley, H.; Pearl, I.A. Tappi, 1967, 50, 419. Pearl, I.Α.; Darling. S.F. Tappi, 1967, 50, 193. Thieme, H. Planta Med., 1967, 15, 35. Pearl, I.Α.; Darling, S.F. J . Org. Chem., 1959, 24, 1616. Pearl, I.Α.; Darling, S.F. Tappi, 1967, 50, 324. Thieme, H.; Richter, R. Pharmazie, 1966, 21, 251.


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Allelochemicals as Determinants of Insect Damage Across the North

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