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Has the damson-hop aphid an alate alienicolous morph?
Agriculture, Ecosystems and Environment, 12 (1984/85) 171--180
171
Elsevier Science Publishers B.V., Amsterdam - - P r i n t e d in The Netherlands
HAS THE DAMSON-HOP APHID AN ALATE ALIENICOLOUS MORPH?
C.A.M. CAMPBELL
East Mailing Research Station, Maidstone, Kent ME19 6BJ (Gt. Britain) (Accepted for publication 7 November 1984)
ABSTRACT Campbell, C.A.M., 1985. Has the damson-hop aphid an alate alienicolous morph? Agric. Ecosystems Environ., 12: 171--180. Alate individuals of the damson-hop aphid (Phorodon humuli (Schrank)) from colonies maintained on hops (Humulus lupulus L.) at 20 ± I°C and 16 h/day photoperiod were gynoparae and not alienicolae. A biometric analysis indicated that alatae purported to be alienicolae in a unique description were more probably reproductive primary migrants. No incontrovertible evidence was found for the existence of an alate alienicolous morph of P. humuli. The rarity of the morph (if it exists) ensures that it has no economic importance for hop growers.
INTRODUCTION
Alienicolae of the damson-hop aphid (Phorodon humuli (Schrank)) are monophagous on hops (Humulus lupulus L.). In detailed studies of the aphid's population dynamics on cultivated hop plants, no alate alienicolae were reported from Bulgaria (Tsvetkov, 1962), Germany (Born, 1968; Zohren, 1970), Czechoslovakia (Hrdy et al., 1970), Poland (Micinski and Ruszkiewicz, 1974) or England (Campbell, 1978; Aveling, 1981). Nevertheless, Kolbe (1966) and Hornung (1981) credit that morph with considerable economic importance for hop growers in Germany. Kolbe (1966) concluded that wild hops were a source of alatae for the irregular prolonged invasions of cultivated hops. Prolonged invasions are feared by growers because aphids may then infest the developing cones. Alate alienicolae were not reported from studies of wild hops in Germany (Zohren, 1970), Czechoslovakia (Hrdy et al., 1970) or England (Marsack, 1980), and there are no reports from elsewhere in P. humuli's geographic range. In England, purported sitings of alate alienicolae were restricted to years in which the primary migration from Prunus was prolonged (Massee, 1963). Hornung (1981) suggested that alate alienicolae were produced on hop cultivars that were susceptible to aphid attack ('Northern Brewer' was cited as an example). Hornung argued that the alatae subsequently infested more resistant cultivars, and made control more difficult, Nutritionally, Northern-
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172 Brewer is particularly suitable for apterae of Phorodon humuli (Campbell, 1983), however, no alate alienicolae were found on it during two season's field studies (C.A.M. Campbell, unpublished data, 1984). Hornung referred to observations of Kirschner (1932) and her own laboratory work on the life-cycle of P. humuli (Hornung, 1973a,b), in support of her conclusions. Kirschner (1932) had reported finding alate alienicolae ofP. humuli in only one year. In a unique description of the alienicolous morph, Kirschner made a morphometric comparison of the purported a/ate alienicolae with primary migrants from an undisclosed source. The present paper undertakes a critical examination of the evidence for an alate alienicolous morph of P. humuli. MATERIALS AND METHODS At East Malling, stock cultures of P. humuli maintained at 20 + 1°C and 16 h / d a y photoperiod occasionally produce alatae among hitherto all apterous individuals. In February 1982, female alatae from one such culture were confined singly in clip-cages attached to leaves of either hop or myrobalan (Prunus cerasifera Erh.). The experiment was made in an insectary at 15--20°C and 16 h / d a y photoperiod. Cages were examined daily. Any offspring were removed and reared to determine their morph. When alatae died, they were dissected, and the number of embryos with pigmented eyespots was recorded. Morphological variation in the alate morphs of Phorodon humuli was assessed from samples, each of 20 individuals, collected from six sources in Kent during 1982. Gynoparae were collected from the stock cultures on hops on 2 February and 15 September; males were collected from the same culture on the latter date. Further gynoparae were collected on 13 September from a hop garden at Wye. Two collections were made of primary migrants on the 28 May. One was of unflown pre-reproductive aphids from a damson (Prunus insititia L.) orchard at East Sutton, the other consisted of aphids with u n k n o w n reproductive experience from a hop garden at East Malling. The wingspan, b o d y length, and m a x i m u m width of the abdomen was recorded for each aphid, and a count was made of the hamuli on one wing. Female aphids were dissected, and the numbers of embryos with and w i t h o u t pigmented eyespots were recorded separately. A principal components analysis was used to assess the inter-relationships between variates among the female morphs. RESULTS Alatae from the laboratory cultures settled and reproduced more readily on myrobalan leaves than on those of hops (Table I). After 24 h, 15 alates (75%) had settled on myrobalan, and 6 {30%) on hops (X2 = 8 . 1 2 , P < 0.01). Aphids lived longer on myrobalan, produced a greater proportion of their
173
embryo complement, and lived longer after reproduction. Nevertheless, five alatae larviposited on hops. These reproducers were settled on the hop leaves during 17 of the 25 cage examinations (68%), compared with 24 times from 66 cage examinations (36%) for non-reproducers {×: = 7.16, P < 0.01). However, even those aphids that reproduced on hops were settled on leaves less frequently than alates on myrobalan (×2 = 7.39, P < 0.01), which were settled on leaves during 209 of the 238 cage examinations (88%). Although reproducers on hop leaves were settled more often than non-reproducers, the life-span of both groups was similar, and was less than half that of aphids on myrobalan. TABLE I Mean (_+ S.E.) fecundity, unrealised f e c u n d i t y at death, and survival (days) for P. humuli gynoparae on t w o hosts
No. in sample ( f r o m 20) No. o f offspring No, of large e m b r y o s Life span Post-reproductive life
Reproducers
Non-reproducers
Hop
Myrobalan
Hop
Myrobalan
19 6.2 0.6 12,4 8.5
15 0 7.4 -+ 0.4 4.4 -+ 1,2 0
1 0 6 2 0
5 1.8 4.6 5.0 1.0
+- 0.7 + 0.7 + 2.1 -+ 2.5
± 0.4 +- 0.4 t 1.1 _+ 1.3
All offspring on both hosts were oviparae so their parents were gynoparae and not alienicolae. Alate males were also observed in the laboratory cultures, confirming that the sexual phase of the life-cycle was induced. Morphometrics of the alate morphs are given in Table II, which includes comparable data from Kirschner (1932). In the samples from England, primary migrants were the biggest and males the smallest alates. A range of 2--5 hamuli was common to all three morphs, with numbers of hamuli positively associated with body size for each of the morphs. The average wingspan for putative alienicolae recorded by Kirschner (1932) was bigger than that of any of the aphid morphs here, but in other parameters the putative alienicolae resembled primary migrants more than they did gynoparae. By contrast, Kirschner's primary migrants had particularly small wingspans. With the exception of numbers of embryos in primary migrants, differences between the two female morphs were generally greater than those observed between separate samples of the same morph. About 75% fewer embryos were present with pigmented eyespots and two times more younger embryos in primary migrants from hops, as compared to alates from Prunus. Small statistically significant differences in wingspan, body length, body width, and numbers of embryos with pigmented eyespots, were recorded between the samples of gynoparae. Differences of a similar magnitude are common when samples of insects are drawn from restricted sites (Laughlin, 1967).
174 TABLE II Morphometrics of P. humuli alatae (dimensions in mm, n = 20 or unreported 1) Morph
Host
W i n g - Body span length
Body width
No. of hamuli
No. of embryos With eyespots
Without eyespots
2.1 4.6 0.12 0.32
A. Samples from England, 1982 Primary migrant Prunus 6.605 Primary migrant Hop 6.687 Gynopara Hop 5.528 Gynopara Hop 5.460 Gynopara Hop 5.121 Male Hop 4.959
2.042 1.828 1.461 1.670 1.567 1.330
0.922 0.932 0.630 0.697 0.600 0.494
3.7 3.9 3.1 3.0 3.1 3.3
22.5 5.3 4.6 6.6 6.7 0
Standard error of difference
0.115
0.043
0.022
0.2
0.7
B. Samples from Germany, 19251 Primary migrant _4 5.500 Putative alienicola Hop 7.200
2.000 1.704
0.900 0.873
4 53
_4 --'
__4
0; 0.6 __4 __4
1From Kirschner (1932). 2Data not included in the analysis of variance. 3"With few exceptions". 4Not recorded. A p r i n c i p a l c o m p o n e n t s analysis was m a d e on t h e t o t a l v a r i a t i o n a m o n g t h e 80 a p h i d s f r o m f o u r c o l l e c t i o n s ( R o w s 1--4 in T a b l e II). T h e variates w e r e first s t a n d a r d i s e d t o h a v e u n i t variance. All c o e f f i c i e n t s w e r e positive on t h e first c o m p o n e n t (Table I I I ) , indicating t h a t s e p a r a t i o n was m o s t l y o n size. G y n o p a r a e a n d p r i m a r y m i g r a n t s w e r e e q u a l l y r e p r e s e n t e d , a n d so t h e score o f zero was c o n v e n i e n t f o r s e p a r a t i n g t h e c l o u d s o f p o i n t s (Fig. 1). As g y n o p a r a e w e r e m o s t l y smaller t h a n p r i m a r y m i g r a n t s , t h e y h a d negative values o n t h e first axis. N o p r i m a r y m i g r a n t s h a d negative values o n t h e first axis, b u t t h e t h r e e biggest g y n o p a r a e h a d p o s i t i v e values. T r e a t e d as an exercise in allocating individuals to t h e i r c o r r e c t m o r p h , t h e e r r o r was a b o u t 4%. The second component separated primary migrants into two sub-groups c o r r e s p o n d i n g t o w h e t h e r t h e y w e r e c o l l e c t e d f r o m h o p s or d a m s o n . G y n o p a r a e were n o t sub-divided. O n e p r i m a r y m i g r a n t was a l l o c a t e d to t h e w r o n g s u b - g r o u p . T h a t individual h a d t h e highest n u m b e r o f e m b r y o s w i t h pigmented eyespots a m o n g aphids collected f r om hops. Presumably the a p h i d was c o l l e c t e d s o o n a f t e r its m i g r a t o r y flight, a n d b e f o r e it h a d d e p o s i t e d m a n y offspring. An analysis o f p r i n c i p a l c o m p o n e n t s was specifically c h o s e n so t h a t t h e i d e n t i t y o f K i r s c h n e r ' s ( 1 9 3 2 ) p u t a t i v e alienicolae m i g h t be e x p l o r e d .
175 TABLE III Coefficients for standardised and original variates of principal components I and II for total variation ofP. hurnuli primary migrants and gynoparae
Wingspan Body length Body width No. of hamuli No. of embryos with pigmented eyespots % of total variance
Standardised
Original
I
II
I
II
0.565 0.437 0.623 0.226
0.338 --0.428 0.114 0.399
1.524 2.551 8.026 0.358
0.911 -2.501 1.465 0:634
0.227 75.31
--0.728 11.42
0.034
--0.109
PC2
+3t A PC1
A
.,~
'~
'~
,
+"T "* * " . - , I
A
A
i-2-• •
'Y'i"iii+ ii+ii+! iiii iii+!i
•
•
• II •:~ iiii!i:iii:~ O
+3
+5
-1
:
o%
0
0
-3 Fig. 1. Projection of the first two principal components of P. humuli alate females (o, primary migrants ex-damson; o, primary migrants ex-hop; a, gynoparae from the field; A, gynoparae reared in the laboratory. From Kirschner (1932), v, primary migrants; m, putative alate alienicolae). The stippled areas indicate 95% confidence regions arising from the feasible numbers of embryos with pigmented eyespots estimated from Fig. 2. K i r s c h n e r did n o t r e p o r t t h e n u m b e r s o f e m b r y o s in t h e a p h i d s he e x a m i n e d . H o w e v e r , in t h e p r e s e n t s t u d y , t h e n u m b e r o f e m b r y o s w i t h p i g m e n t e d e y e s p o t s was v e r y highly c o r r e l a t e d w i t h b o d y length (r = 0.72, P < 0.001). M e a n n u m b e r s o f t h o s e e m b r y o s a n d 95% c o n f i d e n c e limits w e r e e s t i m a t e d f o r each o f K i r s c h n e r ' s g r o u p s o f alatae f r o m Fig. 2. T h e r e l a t i o n s h i p bet w e e n t h e variates was m o r e variable f o r p r i m a r y m i g r a n t s (Fig. 2a), t h a n f o r g y n o p a r a e (Fig. 2b), w h i c h is r e f l e c t e d in t h e w i d t h o f t h e c o n f i d e n c e
176 limits. Nevertheless, the estimated means for the putative alienicolae were similar from both regressions at 7.0 embryos from Fig. 2a, and 6.6 from Fig. 2b. The identity of Kirschner's primary migrants is not suspect, so only an estimate from Fig. 2a was made. (a)
30
(b)
Jooo/ oo oo o.6o
,3
T°
20
E 09
o!/o
'5 E
?,
/ ./..T ~
10
/0 i
-'"" •
zO O i
1.5
°
1.7
I°
•
&
I"
-00 t
1,9
0
t
2.1
t
J
I
2.3
1.1
Body
length
I
I
1.3
I
J
1,5
I
I
1.7
I
A
19
(mm)
Fig. 2. Relationship between the number of embryos with pigmented eyespots and body length for P. hurnuli. (a), primary migrants (o, ex-damson; e, ex-hop); (b), gynoparae (% field collected; A, laboratory reared). Estimated mean numbers and 95% confidence intervals for Kirschner's (1932) (u) primary migrants and (=) putative alate alienicolae. For each of Kirschner's groups of alatae, the differences of each variate from the overall mean values (calculated from Rows 1--4 in Table II), were multiplied by the respective loadings for original variates (Table III), and summed to give the principal c o m p o n e n t score. For example, the score (z) on principal component 1 (PC1) for the primary migrant was obtained from z = 1.524 ( 6 . 0 7 0 - 5.500) + 2.551 ( 1 . 7 5 0 - 2.000) + -." + 0.034 (9.725 16.353) The scores are projected onto the axes in Fig. 1, with stippled shading indicating the feasible 95% confidence regions arising from the estimates of the numbers of embryos with pigmented eyespots. The high positive scores on both axes for putative alienicolae emphasize the close morphological similarity with reproductive primary migrants. By contrast, scores for Kirschner's primary migrants exhibit a close resemblance to pre-reproductive examples of that morph. DISCUSSION Despite the relatively high constant temperature and long photoperiod, alatae produced in the stock cultures were gynoparae and males. The en-
177
vironmental conditions here were similar to the 20--23°C and 16 h/day photoperiod used by Hornung (1973a,b), when she contended that Phorodon humuli had produced alate alienicolae. Hornung observed that alate production was enhanced by lower temperatures and shorter photoperiods, conditions which induce the sexual phase of some other species of aphids (Dixon and Glen, 1971; Searle and Mittler, 1982; Takada, 1982). There seems to be a strong possibility, therefore, that the sexual phase of P. humuli's life-cycle was initiated in Hornung's study, as it was at East Mailing. Kirschner (1932) reported that the putative alienicolae were found on hops suffering from an edaphically induced leaf-roll disorder. Leaf-roll is a common disorder of hops in Poland (Micinski, 1969). However, figures illustrating 4 years' catches from a suction trap at Poznan (Ruszkowska and Zlotkowski, 1977), show two flight periods each year for P. humuli. T w o flight periods also occur in England (Taylor et al., 1979; Thomas et al., 1983), where the leaf-roll disorder is not recorded, and in Hungary (Meszeleny et al., 1981). The periods correspond with seasonal alternations among primary and secondary hosts. In contrast, those heteroecious aphids that habitually produce alate alienicolae typically show three peaks of alate production annually. Kirschner (1932) reported that in his study the hop shoots were covered with muslin to prevent colonisation by primary migrants. However, until quite recently (Campbell, 1977), it was not appreciated that primary migrants of P. humuli mostly land on mature leaves from which they walk up to the shoot apices. Previously, the apical zone was considered as the principal landing site (e.g., Hornung, 1973b, p. 191). Unless aphids were stringently excluded from ascending the stems, contamination by primary migrants presents a possible alternative explanation for Kirschner's alatae. Hille Ris Lambers (1966) observed that alate alienicolae "invariably show a morphology similar to or identical with that of (gynoparae) ...", although the morphological differences between primary migrant and gynopara were also small. Crowding and nutritional deterioration of the host are the most frequently cited stimuli for alate alienicola production among aphids (Hille Ris Lambers, 1966; Dixon, 1977). Consequently, for the few species in which sizes were reported, alienicolae were smaller than primary migrants (Dixon, 1976; Woodford and Lerman, 1977). Therefore, Kirschner's data are unusual in that putative alienicolae resemble primary migrants more than they do gynoparae (Table II). The body lengths for primary migrants (Table II) were within the range (1.66--2.2 mm) found by Kriz (1968) for that morph reared on Prunus in the laboratory. However, the range of abdominal widths recorded by Kriz (1968) (0.6--0.75 mm), was smaller than was found here or by Kirschner (1932). The results of the principal components exercise (Fig. 1), clearly indicate that both groups of alatae examined by Kirschner were primary migrants. The negative score on the second axis for Kirschner's primary migrants, suggest that aphids were collected before the onset of parturition. Their
178
relatively small wingspans, and apparent lack of variability in numbers of hamuli suggest a restricted origin. Collection direct from the primary host seems most likely. By contrast, the high positive score on the second axis for the putative alienicolae indicates that probably most of their progeny were deposited. Had they been newly matured alienicolae, a pre-reproductive dispersal flight would have been expected, notwithstanding that n o t all alatae make such flights (Shaw, 1973). The present analysis could help identify the morph and previous reproductive activity of individual alate Phorodon humuli intercepted near hop gardens. For example, consider alatae collected in June and August, respectively. An aphid collected in June would be a primary migrant. Following the procedure outlined above, calculation of the second principal c o m p o n e n t score would indicate whether the aphid was intercepted in trivial or migratory flights. An aphid collected in August might be a late primary migrant, a gynopara, or possibly even an alienicola. Gynoparae and alienicolae would be expected to have similar negative scores on the first axis, and primary migrants a positive score. The presence of embryos with a continuous range of developmental ages would serve to separate an alienicola from a gynopara, as the reproductive strategies of the two morphs differ (Dixon, 1976; Searle and Mittler, 1982). The variates used in the present analysis were chosen specifically because most were recorded by Kirschner (1932). It is likely that fewer variates would suffice, and greater sensitivity might be achieved, by using some other variables. For example, sensoriation of the antennae has proved useful for separating the alate morphs of other species of aphids (Hille Ris Lambers, 1966; Woodford and Lerman, 1977; Hardie, 1983). CONCLUSION
The lack of substantiated evidence for the existence of an alate alienicolous morph of P. humuli suggests that its production is at most an aberrant and infrequent event in the normal life-history of the aphid. Clearly, despite some claims to the contrary, the morph has no economic importance for hop growers. ACKNOWLEDGEMENTS
I thank Mr K.J. Martin for statistical guidance and colleagues for criticising previous drafts of the manuscript.
REFERENCES Aveling, C., 1981. The role of Anthocoris species (Hemiptera: Anthocoridae) in the integrated control of the damson-hop aphid (Phorodon hurnuli). Ann. Appl. Biol., 97: 143--153.
179 Born, M., 1968. Beitrage zur Bionomie yon Phorodon humuli (Schrank, 1801). Arch. Pfianzenschutz, 4 : 37--52. Campbell, C.A.M., 1977. Distribution of damson-hop aphid Phorodon humuli migrants on hops in relation to hop variety and wind shelter. Ann. Appl. Biol., 87: 315--325. Campbell, C.A.M., 1978. Regulation of the damson-hop aphid (Phorodon humuli (Schrank)) on hops (Humulus lupulus L.) by predators. J. Hortic. Sci., 53: 235--242. Campbell, C.A.M., 1983. Antibiosis in hop (Humulus lupulus) to the damson-hop aphid, Phorodon humuli. Entomol. Exp. Appl., 33: 57--62. Dixon, A.F.G., 1976. Reproductive strategies of the alate morphs of the bird cherryoat aphid Rhopalosiphum padi L. J. Anita. Ecol., 45: 593-603. Dixon, A.F.G., 1977. Aphid ecology: life cycles, polymorphism, and population regulation. Annu. Rev. Ecol. Syst., 8: 329--353. Dixon, A.F.G. and Glen, DMI., 1971. Morph determination in the bird cherry-oat aphid, Rhopalosiphum padi L. Ann. Appl. Biol., 68: 11--21. Hardie, J., 1983. Reproductive, morphological and behavioural affinities between the alate gynopara and virginopara of the aphid Aphis fabae. Physiol. Entomol., 5: 385-396. Hille Ris Lambers, D., 1966. Polymorphism in Aphididae. Annu. Rev. Entomol., 11: 47--78. Hornung, U., 1973a. M6glichkeiten ff/r ganzj~[hrige Versuche mit Phorodon humuli Schrank (Homoptera, Aphididae) an Hopfen (Humulus lupulus L.). Pfianzenkr. Pfianzenschutz, 80: 711--717. Hornung, U., 1973b. Zur Biologie der Hopfenblattlaus. II. Zum Auftreten yon "Aphisfliegen". Hopfen-Rundschau, 24: 188, 190--192. Hornung, U., 1981. Selektierung resistenter Blattlauspopulationen -- auch ein Folge des Sortenwandels? In: I. Hrdy and H. Hrdlickova (Editors), Integrated pest and disease control in hops. IOBC/WPRS Bulletin IV/3, pp. 55-60. Hrdy, I., Zeleny, J., Hrda, J. and Bouckova-Konickova, J., 1970. Stability of resistance to thiometon, multiple-resistance and population density of the hop aphid, Phorodon humuli (Schrank), during 1967-68 (Homoptera: Aphididae). Acta Entomol. Bohemoslov., 67 : 143--174. Kirschner, R., 1932. Beitr~ge zur Biologie yon Phorodon humuli Schrk. nebst Bemerkungen und Versuchen ~ber das Entstehen yon geflf~gelten Aphiden. Biol. Zentralbl., 52: 103--117. Kolbe, W., 1966. Studies on the control of aphids and spider mites on hops. Pflanzenschutz--Nachr., 19: 189--242. Kriz, J., 1968. A contribution to the knowledge of the morphology of the spring generations of the hop aphid (Phorodon humuli Schrk.) on primary host plants. Rostl. Vyroba, 14:375--380 (in Czech). Laughlin, R., 1967. Treatment of data on the size of individual insects from field samples. Entomol. Exp. Appl., 10: 131--142. Marsack, P., 1980. Aspects of the integrated control of the damson-hop aphid (Phorodon humuli Schrk.). Unpublished M.Sc. Thesis, University of Reading, 113 pp. Massee, A.M., 1963. Observations of the life-cycle and control of the damson-hop aphid (Phorodon humuli Schrank). Association of Growers of the New Varieties of Hops Annual Booklet, 1963, Maidstone, pp. 7--9. Meszleny, A., Szalay-Marzso, L. and Jenser, G., 1981. Observations on aphid flight in Hungarian orchards in 1978--1979. Acta Phytopathol. Acad. Sci. Hung., 16: 433-445. Micinski, B., 1969. Degeneration diseases of hops in Poland and their control. Biul. Inst. Oehr. Rosl., 44:157--169 (in Polish). Micinski, B. and Ruszkiewicz, M., 1974. The biology of hop aphid (Phorodon humuli Schr.). Pr. Nauk. Inst. Ochr. Rosl., 16:79--101 (in Polish).
180 Ruszkowska, M. and Zlotkowski, J., 1977. Studies of populations of aphid species of economic importance by aerial sampling. II. Seasonal dynamics of flying aphids. Pr. Nauk. Inst. Ochr. Rosl., 19:125--144 (in Polish). Searle, J.B. and Mittler, T.E., 1982. Embryogenesis and oogenesis in alate virginoparae, gynoparae, and oviparae of the aphid Myzus persicae, in relation to photoperiod. J. Insect Physiol., 28: 213--220. Shaw, M.J.P., 1973. Effects of population density on alienicolae of Aphis fabae Scop. IV. The expression of migratory urge among alatae in the field. Ann. Appl. Biol., 74: 1--7. Takada, H., 1982. Influence of photoperiod and temperature on the reproduction of sexual morphs in a green and a red form of Myzus persicae (Sulzer) (Homoptera, Aphididae). I. Experiments in the laboratory. Kontyu, 50: 233--245. Taylor, L.R., Woiwod, I.P. and Taylor, R.A.J., 1979. The migratory ambit of the hop aphid and its significance in aphid population dynamics. J. Anita. Ecol., 48: 955-972. Thomas, G.G., Goldwin, G.K. and Tatchell, G.M., 1983. Associations between weather factors and the spring migration of the damson-hop aphid Phorodon humuli. Ann. Appl. Biol., 102: 7--17. Tsvetkov, D., 1962. Investigations of the hop aphid (Phorodon humuli Schrk.) and its control. Rastit. Zasht., 10:51--62 (in Bulgarian). Woodford, J.A.T. and Lerman, P.M., 1977. The effect of genotype, environment, age and morph on morphological variation in alate Myzus persicae (Sulzer) (Hemiptera: Aphididae). Bull. Entomol. Res., 67: 685--693. Zohren, E., 1970. M6glichkeiten einer integrierten Bek~-npfung von Hopfensch~idlingen. Z. Angew. Entomol., 65: 412--419.
171
Elsevier Science Publishers B.V., Amsterdam - - P r i n t e d in The Netherlands
HAS THE DAMSON-HOP APHID AN ALATE ALIENICOLOUS MORPH?
C.A.M. CAMPBELL
East Mailing Research Station, Maidstone, Kent ME19 6BJ (Gt. Britain) (Accepted for publication 7 November 1984)
ABSTRACT Campbell, C.A.M., 1985. Has the damson-hop aphid an alate alienicolous morph? Agric. Ecosystems Environ., 12: 171--180. Alate individuals of the damson-hop aphid (Phorodon humuli (Schrank)) from colonies maintained on hops (Humulus lupulus L.) at 20 ± I°C and 16 h/day photoperiod were gynoparae and not alienicolae. A biometric analysis indicated that alatae purported to be alienicolae in a unique description were more probably reproductive primary migrants. No incontrovertible evidence was found for the existence of an alate alienicolous morph of P. humuli. The rarity of the morph (if it exists) ensures that it has no economic importance for hop growers.
INTRODUCTION
Alienicolae of the damson-hop aphid (Phorodon humuli (Schrank)) are monophagous on hops (Humulus lupulus L.). In detailed studies of the aphid's population dynamics on cultivated hop plants, no alate alienicolae were reported from Bulgaria (Tsvetkov, 1962), Germany (Born, 1968; Zohren, 1970), Czechoslovakia (Hrdy et al., 1970), Poland (Micinski and Ruszkiewicz, 1974) or England (Campbell, 1978; Aveling, 1981). Nevertheless, Kolbe (1966) and Hornung (1981) credit that morph with considerable economic importance for hop growers in Germany. Kolbe (1966) concluded that wild hops were a source of alatae for the irregular prolonged invasions of cultivated hops. Prolonged invasions are feared by growers because aphids may then infest the developing cones. Alate alienicolae were not reported from studies of wild hops in Germany (Zohren, 1970), Czechoslovakia (Hrdy et al., 1970) or England (Marsack, 1980), and there are no reports from elsewhere in P. humuli's geographic range. In England, purported sitings of alate alienicolae were restricted to years in which the primary migration from Prunus was prolonged (Massee, 1963). Hornung (1981) suggested that alate alienicolae were produced on hop cultivars that were susceptible to aphid attack ('Northern Brewer' was cited as an example). Hornung argued that the alatae subsequently infested more resistant cultivars, and made control more difficult, Nutritionally, Northern-
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172 Brewer is particularly suitable for apterae of Phorodon humuli (Campbell, 1983), however, no alate alienicolae were found on it during two season's field studies (C.A.M. Campbell, unpublished data, 1984). Hornung referred to observations of Kirschner (1932) and her own laboratory work on the life-cycle of P. humuli (Hornung, 1973a,b), in support of her conclusions. Kirschner (1932) had reported finding alate alienicolae ofP. humuli in only one year. In a unique description of the alienicolous morph, Kirschner made a morphometric comparison of the purported a/ate alienicolae with primary migrants from an undisclosed source. The present paper undertakes a critical examination of the evidence for an alate alienicolous morph of P. humuli. MATERIALS AND METHODS At East Malling, stock cultures of P. humuli maintained at 20 + 1°C and 16 h / d a y photoperiod occasionally produce alatae among hitherto all apterous individuals. In February 1982, female alatae from one such culture were confined singly in clip-cages attached to leaves of either hop or myrobalan (Prunus cerasifera Erh.). The experiment was made in an insectary at 15--20°C and 16 h / d a y photoperiod. Cages were examined daily. Any offspring were removed and reared to determine their morph. When alatae died, they were dissected, and the number of embryos with pigmented eyespots was recorded. Morphological variation in the alate morphs of Phorodon humuli was assessed from samples, each of 20 individuals, collected from six sources in Kent during 1982. Gynoparae were collected from the stock cultures on hops on 2 February and 15 September; males were collected from the same culture on the latter date. Further gynoparae were collected on 13 September from a hop garden at Wye. Two collections were made of primary migrants on the 28 May. One was of unflown pre-reproductive aphids from a damson (Prunus insititia L.) orchard at East Sutton, the other consisted of aphids with u n k n o w n reproductive experience from a hop garden at East Malling. The wingspan, b o d y length, and m a x i m u m width of the abdomen was recorded for each aphid, and a count was made of the hamuli on one wing. Female aphids were dissected, and the numbers of embryos with and w i t h o u t pigmented eyespots were recorded separately. A principal components analysis was used to assess the inter-relationships between variates among the female morphs. RESULTS Alatae from the laboratory cultures settled and reproduced more readily on myrobalan leaves than on those of hops (Table I). After 24 h, 15 alates (75%) had settled on myrobalan, and 6 {30%) on hops (X2 = 8 . 1 2 , P < 0.01). Aphids lived longer on myrobalan, produced a greater proportion of their
173
embryo complement, and lived longer after reproduction. Nevertheless, five alatae larviposited on hops. These reproducers were settled on the hop leaves during 17 of the 25 cage examinations (68%), compared with 24 times from 66 cage examinations (36%) for non-reproducers {×: = 7.16, P < 0.01). However, even those aphids that reproduced on hops were settled on leaves less frequently than alates on myrobalan (×2 = 7.39, P < 0.01), which were settled on leaves during 209 of the 238 cage examinations (88%). Although reproducers on hop leaves were settled more often than non-reproducers, the life-span of both groups was similar, and was less than half that of aphids on myrobalan. TABLE I Mean (_+ S.E.) fecundity, unrealised f e c u n d i t y at death, and survival (days) for P. humuli gynoparae on t w o hosts
No. in sample ( f r o m 20) No. o f offspring No, of large e m b r y o s Life span Post-reproductive life
Reproducers
Non-reproducers
Hop
Myrobalan
Hop
Myrobalan
19 6.2 0.6 12,4 8.5
15 0 7.4 -+ 0.4 4.4 -+ 1,2 0
1 0 6 2 0
5 1.8 4.6 5.0 1.0
+- 0.7 + 0.7 + 2.1 -+ 2.5
± 0.4 +- 0.4 t 1.1 _+ 1.3
All offspring on both hosts were oviparae so their parents were gynoparae and not alienicolae. Alate males were also observed in the laboratory cultures, confirming that the sexual phase of the life-cycle was induced. Morphometrics of the alate morphs are given in Table II, which includes comparable data from Kirschner (1932). In the samples from England, primary migrants were the biggest and males the smallest alates. A range of 2--5 hamuli was common to all three morphs, with numbers of hamuli positively associated with body size for each of the morphs. The average wingspan for putative alienicolae recorded by Kirschner (1932) was bigger than that of any of the aphid morphs here, but in other parameters the putative alienicolae resembled primary migrants more than they did gynoparae. By contrast, Kirschner's primary migrants had particularly small wingspans. With the exception of numbers of embryos in primary migrants, differences between the two female morphs were generally greater than those observed between separate samples of the same morph. About 75% fewer embryos were present with pigmented eyespots and two times more younger embryos in primary migrants from hops, as compared to alates from Prunus. Small statistically significant differences in wingspan, body length, body width, and numbers of embryos with pigmented eyespots, were recorded between the samples of gynoparae. Differences of a similar magnitude are common when samples of insects are drawn from restricted sites (Laughlin, 1967).
174 TABLE II Morphometrics of P. humuli alatae (dimensions in mm, n = 20 or unreported 1) Morph
Host
W i n g - Body span length
Body width
No. of hamuli
No. of embryos With eyespots
Without eyespots
2.1 4.6 0.12 0.32
A. Samples from England, 1982 Primary migrant Prunus 6.605 Primary migrant Hop 6.687 Gynopara Hop 5.528 Gynopara Hop 5.460 Gynopara Hop 5.121 Male Hop 4.959
2.042 1.828 1.461 1.670 1.567 1.330
0.922 0.932 0.630 0.697 0.600 0.494
3.7 3.9 3.1 3.0 3.1 3.3
22.5 5.3 4.6 6.6 6.7 0
Standard error of difference
0.115
0.043
0.022
0.2
0.7
B. Samples from Germany, 19251 Primary migrant _4 5.500 Putative alienicola Hop 7.200
2.000 1.704
0.900 0.873
4 53
_4 --'
__4
0; 0.6 __4 __4
1From Kirschner (1932). 2Data not included in the analysis of variance. 3"With few exceptions". 4Not recorded. A p r i n c i p a l c o m p o n e n t s analysis was m a d e on t h e t o t a l v a r i a t i o n a m o n g t h e 80 a p h i d s f r o m f o u r c o l l e c t i o n s ( R o w s 1--4 in T a b l e II). T h e variates w e r e first s t a n d a r d i s e d t o h a v e u n i t variance. All c o e f f i c i e n t s w e r e positive on t h e first c o m p o n e n t (Table I I I ) , indicating t h a t s e p a r a t i o n was m o s t l y o n size. G y n o p a r a e a n d p r i m a r y m i g r a n t s w e r e e q u a l l y r e p r e s e n t e d , a n d so t h e score o f zero was c o n v e n i e n t f o r s e p a r a t i n g t h e c l o u d s o f p o i n t s (Fig. 1). As g y n o p a r a e w e r e m o s t l y smaller t h a n p r i m a r y m i g r a n t s , t h e y h a d negative values o n t h e first axis. N o p r i m a r y m i g r a n t s h a d negative values o n t h e first axis, b u t t h e t h r e e biggest g y n o p a r a e h a d p o s i t i v e values. T r e a t e d as an exercise in allocating individuals to t h e i r c o r r e c t m o r p h , t h e e r r o r was a b o u t 4%. The second component separated primary migrants into two sub-groups c o r r e s p o n d i n g t o w h e t h e r t h e y w e r e c o l l e c t e d f r o m h o p s or d a m s o n . G y n o p a r a e were n o t sub-divided. O n e p r i m a r y m i g r a n t was a l l o c a t e d to t h e w r o n g s u b - g r o u p . T h a t individual h a d t h e highest n u m b e r o f e m b r y o s w i t h pigmented eyespots a m o n g aphids collected f r om hops. Presumably the a p h i d was c o l l e c t e d s o o n a f t e r its m i g r a t o r y flight, a n d b e f o r e it h a d d e p o s i t e d m a n y offspring. An analysis o f p r i n c i p a l c o m p o n e n t s was specifically c h o s e n so t h a t t h e i d e n t i t y o f K i r s c h n e r ' s ( 1 9 3 2 ) p u t a t i v e alienicolae m i g h t be e x p l o r e d .
175 TABLE III Coefficients for standardised and original variates of principal components I and II for total variation ofP. hurnuli primary migrants and gynoparae
Wingspan Body length Body width No. of hamuli No. of embryos with pigmented eyespots % of total variance
Standardised
Original
I
II
I
II
0.565 0.437 0.623 0.226
0.338 --0.428 0.114 0.399
1.524 2.551 8.026 0.358
0.911 -2.501 1.465 0:634
0.227 75.31
--0.728 11.42
0.034
--0.109
PC2
+3t A PC1
A
.,~
'~
'~
,
+"T "* * " . - , I
A
A
i-2-• •
'Y'i"iii+ ii+ii+! iiii iii+!i
•
•
• II •:~ iiii!i:iii:~ O
+3
+5
-1
:
o%
0
0
-3 Fig. 1. Projection of the first two principal components of P. humuli alate females (o, primary migrants ex-damson; o, primary migrants ex-hop; a, gynoparae from the field; A, gynoparae reared in the laboratory. From Kirschner (1932), v, primary migrants; m, putative alate alienicolae). The stippled areas indicate 95% confidence regions arising from the feasible numbers of embryos with pigmented eyespots estimated from Fig. 2. K i r s c h n e r did n o t r e p o r t t h e n u m b e r s o f e m b r y o s in t h e a p h i d s he e x a m i n e d . H o w e v e r , in t h e p r e s e n t s t u d y , t h e n u m b e r o f e m b r y o s w i t h p i g m e n t e d e y e s p o t s was v e r y highly c o r r e l a t e d w i t h b o d y length (r = 0.72, P < 0.001). M e a n n u m b e r s o f t h o s e e m b r y o s a n d 95% c o n f i d e n c e limits w e r e e s t i m a t e d f o r each o f K i r s c h n e r ' s g r o u p s o f alatae f r o m Fig. 2. T h e r e l a t i o n s h i p bet w e e n t h e variates was m o r e variable f o r p r i m a r y m i g r a n t s (Fig. 2a), t h a n f o r g y n o p a r a e (Fig. 2b), w h i c h is r e f l e c t e d in t h e w i d t h o f t h e c o n f i d e n c e
176 limits. Nevertheless, the estimated means for the putative alienicolae were similar from both regressions at 7.0 embryos from Fig. 2a, and 6.6 from Fig. 2b. The identity of Kirschner's primary migrants is not suspect, so only an estimate from Fig. 2a was made. (a)
30
(b)
Jooo/ oo oo o.6o
,3
T°
20
E 09
o!/o
'5 E
?,
/ ./..T ~
10
/0 i
-'"" •
zO O i
1.5
°
1.7
I°
•
&
I"
-00 t
1,9
0
t
2.1
t
J
I
2.3
1.1
Body
length
I
I
1.3
I
J
1,5
I
I
1.7
I
A
19
(mm)
Fig. 2. Relationship between the number of embryos with pigmented eyespots and body length for P. hurnuli. (a), primary migrants (o, ex-damson; e, ex-hop); (b), gynoparae (% field collected; A, laboratory reared). Estimated mean numbers and 95% confidence intervals for Kirschner's (1932) (u) primary migrants and (=) putative alate alienicolae. For each of Kirschner's groups of alatae, the differences of each variate from the overall mean values (calculated from Rows 1--4 in Table II), were multiplied by the respective loadings for original variates (Table III), and summed to give the principal c o m p o n e n t score. For example, the score (z) on principal component 1 (PC1) for the primary migrant was obtained from z = 1.524 ( 6 . 0 7 0 - 5.500) + 2.551 ( 1 . 7 5 0 - 2.000) + -." + 0.034 (9.725 16.353) The scores are projected onto the axes in Fig. 1, with stippled shading indicating the feasible 95% confidence regions arising from the estimates of the numbers of embryos with pigmented eyespots. The high positive scores on both axes for putative alienicolae emphasize the close morphological similarity with reproductive primary migrants. By contrast, scores for Kirschner's primary migrants exhibit a close resemblance to pre-reproductive examples of that morph. DISCUSSION Despite the relatively high constant temperature and long photoperiod, alatae produced in the stock cultures were gynoparae and males. The en-
177
vironmental conditions here were similar to the 20--23°C and 16 h/day photoperiod used by Hornung (1973a,b), when she contended that Phorodon humuli had produced alate alienicolae. Hornung observed that alate production was enhanced by lower temperatures and shorter photoperiods, conditions which induce the sexual phase of some other species of aphids (Dixon and Glen, 1971; Searle and Mittler, 1982; Takada, 1982). There seems to be a strong possibility, therefore, that the sexual phase of P. humuli's life-cycle was initiated in Hornung's study, as it was at East Mailing. Kirschner (1932) reported that the putative alienicolae were found on hops suffering from an edaphically induced leaf-roll disorder. Leaf-roll is a common disorder of hops in Poland (Micinski, 1969). However, figures illustrating 4 years' catches from a suction trap at Poznan (Ruszkowska and Zlotkowski, 1977), show two flight periods each year for P. humuli. T w o flight periods also occur in England (Taylor et al., 1979; Thomas et al., 1983), where the leaf-roll disorder is not recorded, and in Hungary (Meszeleny et al., 1981). The periods correspond with seasonal alternations among primary and secondary hosts. In contrast, those heteroecious aphids that habitually produce alate alienicolae typically show three peaks of alate production annually. Kirschner (1932) reported that in his study the hop shoots were covered with muslin to prevent colonisation by primary migrants. However, until quite recently (Campbell, 1977), it was not appreciated that primary migrants of P. humuli mostly land on mature leaves from which they walk up to the shoot apices. Previously, the apical zone was considered as the principal landing site (e.g., Hornung, 1973b, p. 191). Unless aphids were stringently excluded from ascending the stems, contamination by primary migrants presents a possible alternative explanation for Kirschner's alatae. Hille Ris Lambers (1966) observed that alate alienicolae "invariably show a morphology similar to or identical with that of (gynoparae) ...", although the morphological differences between primary migrant and gynopara were also small. Crowding and nutritional deterioration of the host are the most frequently cited stimuli for alate alienicola production among aphids (Hille Ris Lambers, 1966; Dixon, 1977). Consequently, for the few species in which sizes were reported, alienicolae were smaller than primary migrants (Dixon, 1976; Woodford and Lerman, 1977). Therefore, Kirschner's data are unusual in that putative alienicolae resemble primary migrants more than they do gynoparae (Table II). The body lengths for primary migrants (Table II) were within the range (1.66--2.2 mm) found by Kriz (1968) for that morph reared on Prunus in the laboratory. However, the range of abdominal widths recorded by Kriz (1968) (0.6--0.75 mm), was smaller than was found here or by Kirschner (1932). The results of the principal components exercise (Fig. 1), clearly indicate that both groups of alatae examined by Kirschner were primary migrants. The negative score on the second axis for Kirschner's primary migrants, suggest that aphids were collected before the onset of parturition. Their
178
relatively small wingspans, and apparent lack of variability in numbers of hamuli suggest a restricted origin. Collection direct from the primary host seems most likely. By contrast, the high positive score on the second axis for the putative alienicolae indicates that probably most of their progeny were deposited. Had they been newly matured alienicolae, a pre-reproductive dispersal flight would have been expected, notwithstanding that n o t all alatae make such flights (Shaw, 1973). The present analysis could help identify the morph and previous reproductive activity of individual alate Phorodon humuli intercepted near hop gardens. For example, consider alatae collected in June and August, respectively. An aphid collected in June would be a primary migrant. Following the procedure outlined above, calculation of the second principal c o m p o n e n t score would indicate whether the aphid was intercepted in trivial or migratory flights. An aphid collected in August might be a late primary migrant, a gynopara, or possibly even an alienicola. Gynoparae and alienicolae would be expected to have similar negative scores on the first axis, and primary migrants a positive score. The presence of embryos with a continuous range of developmental ages would serve to separate an alienicola from a gynopara, as the reproductive strategies of the two morphs differ (Dixon, 1976; Searle and Mittler, 1982). The variates used in the present analysis were chosen specifically because most were recorded by Kirschner (1932). It is likely that fewer variates would suffice, and greater sensitivity might be achieved, by using some other variables. For example, sensoriation of the antennae has proved useful for separating the alate morphs of other species of aphids (Hille Ris Lambers, 1966; Woodford and Lerman, 1977; Hardie, 1983). CONCLUSION
The lack of substantiated evidence for the existence of an alate alienicolous morph of P. humuli suggests that its production is at most an aberrant and infrequent event in the normal life-history of the aphid. Clearly, despite some claims to the contrary, the morph has no economic importance for hop growers. ACKNOWLEDGEMENTS
I thank Mr K.J. Martin for statistical guidance and colleagues for criticising previous drafts of the manuscript.
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