Bull. ent. Res. 73, 137-151 137 Published 1983
l'TIte assessment of mealybugs (Pseudococcidae) and other Homoptera on mame cocoa trees in Ghana
/ C. A. M. CAMPBELL * Cocoa Research Institute, P.O. Box 8, New Tafo, Ghqna
Abstract The numbers of mealybugs and other Homoptera on 96 coco a trees in Ghana were assessed by examining four branches from each tree. The trees were then felled and examined in detail. Ten species of mealybugs, eight other coccoids, an aphid and a psyIlid were recorded. Ninety-five of the trees were infested with mealybugs, 66, 90 and 69 trees, respectively, with Planococcoides njalensis (Laing), Planococcus citri (Risso) and Phenacoccus htJrgreavesi (Laing). Stictococcus sjostedti CkIl., a species of Gascardia near G. zonata (Newst.) and Mesohomotoma tessmanni (Aulm.) were found on 70, 68 and 48 trees, respectively. The remaining 14 species were found on fewer than 48 trees. All species oíher than Pseudococcus calceolariae (Mask.) and Ferrisia virgata (Ckll.) were most prevalent in the canopy. In the field, mealybug densities recorded on shoots underesti mated true leveIs by an average of 95%. Branches were as effective as whole trees for detecting mealybugs, but less effective for other Homoptera. Branches were suitable sample units for estimating population densities of mealybugs, stictococcids and psyIlids. All species of mealybug other than F. virgata infested vegetative buds. An average of 21'7% of buds on the youngest shoots were infested. Samples of buds can be used for detecting mealybug infestations.
Introduction Mealybugs (Pseudococcidae) of cocoa are important pests in West Africa because most species are vectors of cocoa swollen shoot virus (CSSV). In the Eastern Region of Ghana, cocoa production has been devastated by swollen shoot disease, and elsewhere large sums have also been spent in eradication measures (Legg, 1979). Studies of factors affecting the abundance of mealybugs on mature cocoa have be en hampered by the lack of an efficient technique for estimating population densities. The first of the two main techniques used on mature cocoa involves examining trees after felling (Strickland, 1951.a; Hanna et al., 1952; Cornwell, 1955, 1957; Entwistle, 1959; Bigger, 1981a). The main limitations are that it precIudes re-sampling, sorne trees of interest may not be available for felling, the environment is altered progressively, and felling is costly in time and labour. These drawbacks were avoided by the visual inspection of trees to either eye or hand height (Donald, 1955; SutherIand, 1955; Entwistle, 1958). However, on comparing estimates of mealybug abundance from felling with those from visual inspection, it was found that most of the mealybug population was in the
• Present address: East MaIling Research Station, East Mailing, Maidstone, Kent, UK. 138 C. A. M. CAMPBELL
canopy, and because preferences between the main trunk and canopy varíed among species, sorne species were virtualIy undetected by visual inspection (Donald, 1955). Entwistle (1958) also recognised the inadequacy of counts to hand height. Attempts have been made to improve sampling techniques using simple branch sampling or other procedures (Anon., 1950; CornwelI, 1955), but detailed results were not reported. The primary aim of the present study was to improve techniques for estimating densities of the several species of mealybugs on cocoa. CornwelI (1958) demonstrated dispersal of nymphs of Planococcoides njalensis (Laing) between the interlocking canopies of adjacent trees, which probably explains the local spread of swolIen shoot disease around initial foei of virus infection. Strick land (1951a) recorded almost 90% of P. njalensis in the canopy, and similarly high per centages were found by Donald (1955) and CampbelI (1975). However, Bigger (1972) observed that the proportion in the canopy varied in response to environmental fac torso Over the last 30 years at Tafo, the predominance of P. njalensis over other species of mealybugs has declined (Bigger, 1972, 1981h). The limited data available at the start of this study suggested that most of the other species which are now important are also most numerous in the canopy (Donald, 1955). The abundance of P. nj.alensis and sorne other mealybugs is inter-related with that of stictococeid and coccid scales which are also tended by coccidophilic ants for honeydew (Strickland, 1951h; Bigger, 1981a). From 1973 to 1976 Bigger (unpub lished) recorded the changing abundance of ants and Coccoidea in a plot of 866 trees. He found that as the boundaries of neighbouring territories of dominant ants altered (Leston, 1970), corresponding changes occurred among honeydew-producing Homop tera. Leston (l973) and later Majer (1975) argued that manipulating the ant mosaic to encourage so-caHed beneficial species of ants, notably Oecophylla longinoda (Latreille) and Tetramorium aculeatum (Mayr), neither of which habituaHy tend mealybugs, would result in partial protection from swoHen shoot disease and other maladies. Sampling techniques were needed, therefore, not only for mealybugs, but also for stictococcid and coccid scales and possibly other species of Homoptera of unknown importance in the dynamics of cocoa pests (Entwistle, 1972).
Methods Between 1973 and 1977, four trees at each of 24 sites on the Cocoa Research In stitute, Tafo, were investigated. Sites 1-4 were in al-ha plot of Amelonado cocoa planted in 1952 and grown under dense mixed forest-tree shade. The remaining si tes were in a 13-ha 3 x 33 shade-fertilizer experiment planted in 1959 with cocoa of open pollinated Upper-Amazon parentage. At all sites, trees were being destroyed in attempts to control outbreaks of coco a swoIlen shoot virus disease. The four trees at each site were selected at random from both visibly infected and neighbouring trees. Four fan branches from three heights were cut from each tree using a long-handled pruner. One branch (upper) was emergent aboye the main canopy, two branches (middle) were from opposite sides of the tree at canopy level, and one branch (lower) protruded below the main canopy. The branches were about 25 mm in diameter where severed. Sub-samples were cut from each branch. Up to four growth flushes were cut at the morphological discontinuities left by earlier abscissing terminal bud stipules. Each flush was examined separately, but together they formed the shoot's sub-sample. Flush 1, when present consisted of flaccid distal growth; flush 2 was either hardened distal growth, or, if flush 1 was present, the previous growth increment; and flushes 3 and 4 were successive earlier growth increments. The remainder of the branch formed another sub-sample (the framework), which was cut into approximately 150-mm iengths for handling. AH examinations were made in the laboratory using stereo-microscopes. Records were made of the identity, feeding position and numbers HOMOPTERA OF COCOA IN GHANA 139
of all Homoptera. Additional records were made of the numbers of leaves, shoots, vegetative buds and ftower cushions (inc1uding cherelles) examined. Trees visibly infected with cocoa swollen shoot virus were felled below ground level, and contact trees were coppiced at 0'5 m. The girth of all trees at 0'3 m was recorded. Representative specimens of all ants present on the tree were collected for later identi fication. The main branches were then severed from the trunk and separate fractions made of framework and shoots from ftushes 1-4. The fractions were examined in the field using x 10 hand lenses. Records were made of the identity, number and location of all Homoptera, other than aphids and psyllids, which were not counted. Additional records were made of the numbers of shoots examined and the numbers of pods on the trunk and branches. Not more than two trees were examined per day.
Results Environmental conditions at the 24 sites were diverse. The four Amelonado sites were aH similar to weIl-maintained farmers' plantations. Ten of the sites planted with Upper-Amazon hybrids were unshaded, eight and two sites, respectively, were under light and heavy shade of regularly spaced trees (Termina/ia ivorensis). Nine of the 14 ant species or genera listed by Leston (1973) as dominants were represented. O. longi noda was present at 13 sites, Tetramorium aculeatum at 10, Pheidole spp. and Cremato gaster castane,a F. Smith each at nine, C. africana Mayr at four, C. kneri Mayr (representing the C. wellmani ForeI aggregate) and C. stadelmanni Mayr each at two, while Acantholepis capensis Mayr and C. clariventris Mayr were each present at one site. The length of this list indicates that sorne species were at times co-dominant or sub-dominant. C. castanea was found at eight of its sites, and C. kneri at both sites, with O. longinod.a. T. aculeatum and Pheidole spp. were variously found with O. longinoda, C. clariventris and C. africana. Twenty-three trees showed cocoa-swollen shoot virus symptoms. Ants, shade, fertilizers, cocoa variety, season and virus infec tion, all inftuence the abundance of mealybugs and possibly other Homoptera (Strick land, 1951b; CornweH, 1956; Bigger, 1975, 1981a; Campbell, unpublished). In the present study, these factors were not separable because the investigation was dependent upon the sporadic discovery of virus outbreaks. Twenty species of Homoptera were recorded from the 96 trees examined (Table 1). Ninety-five of the 96 trees examined were infested with mealybugs and 73 with sticto coccids. The three most abundant species were from different families: a psyllid, a stictococcid and a mealybug. The most abundant species were not the most widely dispersed, as found by Bigger (1981b). For example, Phenacoccus hargreavesi (Laing) was less than one-twentieth as abundant as Planococcoides njalensis but was present at the same number of sites and on more trees. The most widespread species was Plano coccus citri (Risso), which was present at aH sites and was found on 89 trees. Ten species were found at more than half the sites. Planococcoides njalensis, Planococcus citri, a species of Gascardia near G. zonat.a (Newstead), Stictococcus sjostedti CockereH and Mesohomotoma tessmanni (Aulmann) were usually at high densities and on three or more trees per site, whereas Phenacoccus hargreavesi, Pseudo coccus concavocerarii James, Steatococcus sp., Cribrolecanium andersoni (Newstead) and Aspidiotus elaeidis Marchal were present at lower average densities and on fewer trees per site. Parastictococcus hargreavesi (Vayssiere), P. multispinosus (Newstead) and Tylococcus westwoodi Strickland occurred at high densities but were localised. T. westwoodi was found only on trees with the coccidophilic ant Crematogaster stadel manni. The remaining seven species in Table I were present at low densities but often at several si tes. For example, Pseudococcus longispinus (Targioni-Tozzetti), Maconel /icoccus ugandae (Laing) and Ferrisia virgata (CockereIl) were found at 7, 6 and 5 sites, respectively, but rarely on more than two trees per sire. Surprisingly, Toxoptera aurantii (Boyer de Fonscolombe) was found ::1t only one site ; a possible reason was that immature basal chupons, which are the preferred feeding sites for T. aurantii on mature (6273)-6 140 c. A. M. CAMPBELL
TABLE l. The numbers 01 Homoptera on 96 cocoa trees, numbers 01 sites (out 01 24) and trees inlested, and percentages 01 units inlested Irom field and laboratory examinations Total NO.of % units insects infested infested* r -"------~ A Lab. Field Sites Trees Lab. Field Pseudococcidae Planococcoides njalensis 2892 4892 23 66 53 38 Planococcus citri 1924 2921 24 89 60 72 Phenacoccus hargreavesi 274 99 23 69 43 29 Phenacoccus sp. O 1 1 1 O 100 Pseudococcus longispinus 15 2 7 10 21 10 Pseudococcus concavocerarii 21 15 15 20 25 SS Pseudococcus ca/ceolariae 2 92 3 3 17 33 Maconellicoccus IIgandae 18 7 6 8 25 38 Ferrisia virgata O 31 S 7 O 100 Tylococcus westwoodi 956 676 2 8 72 63 Combined Pseudococcidae 6102 8736 24 9S 76 79 Margarodidae SteatococclIs sp. 11 103 IS 33 S 82 Coccidae Gascardia sp. nr. G. zonata 559 2400 24 68 17 87 Cribrolecanium andersoni 24 18S 20 42 8 81 S tictococcidae Stictococcus sjostedti 3248 14604 22 70 36 90 Parastictococcus multispinosus 106 1705 2 S SS 80 Parastictococcus hargreavesi O ISI 1 1 O 100 Parastictococcus gowdeyi 2 O 1 1 2S O Combined Stictococcidae 3356 16460 23 73 38 90 Diaspididae Aspidiotus elaeidis 11 472 19 42 100 PsylIidae Mesohomotoma tessmanni 3895 t 16 48 64 t Aphididae Toxoptera aurantii 14 t 2 38 t *Lab. = (No. of infested branches x 100)/4n, where n is the total trees infested from combined lab. and field data. Field = (No. ofinfested trees x loo)/n, where n is as aboye. tNot recorded in the field. cocoa (Entwistle, 1972), were removed during routine maintenance operations. Only two specimens ol Parastictococcus gowdeyi (Newstead) were observed, although high densities were reported on cocoa by Cotterell (1928). The colony was probably newly established. To detect mealybugs, examination of one branch in the laboratory was about as effective as examining the whole tree in the field (Table 1). Seventy-six per cent. of branch sample units from infested trees supported mealybugs, compared with the 79'10 of trees identified as infested from field examination. Similarly, with the exception of F. virg.ata, laboratory examination of one or two branches was as effective for deter rr..ining the presence of any species of mealybug as destructively examining the entire tree. Examination of branches was less effective for detecting coccoids other than mealybugs. On infested trees, stictococcids, the species of Gascardia near G. zonata and A. elaeidis, were generally aggregated on one or two branches. Steatococcus sp. and Cribrolecanium andersoni with densities of only 3-5 insects per infested tree were also present on few branches. Hence, the probabilities of encountering either high density aggregated species or low density dispersed species on a single canopy branch were low. The location of mealybugs within the trees is presented in Table 11 where the per centages are based on field data only to ensure comparability with the results of earlier TABLE 11. The distribution 01 mealybugs within trees Ctotals on 384 branches (laboratory) and 96 trees) Laboratory Field Field data as percentages A A Shootst Branch Shootst Branch Trunk Shoots Branch Trunk framework framework framework Planococcoides njalensis Colonies 379 79 43 210 60 14 67 19 Insects 1234 1658 343 3900 649 7 80 13 Av. col. size 3·3 21·0 8·0 18·6 10·8 Planococcus citri Colonies 690 55 173 124 58 49 35 16 Insects 1433 491 368 1477 1076 13 51 37 :z: Av. col. size 2·1 8·9 2·1 11·9 18·6 O Phenacoccus hargreavesi Colonies 191 17 24 3 1 86 11 4 a:: Insects 254 20 25 73 1 25 74 1 O Av. col size 1 ·3 1·2 1·0 24·3 1·0 ." Pseudococcus longispinus Colonies 12 } 1 O 1 50 O 50 lnsects 14 1 } O 1 50 O 50 Av. col size 1·2 1·0 1·0 1·0 E Pseudococcus concavocerarií Colonies 19 1 13 2 O 87 13 O O lnsects 20 1 13 2 O 87 13 O 'T.I Av. col. size 1·0 1·0 }·O 1·0 (') Pseudococcus calceolariae Colonies 2 O O 1 20 O 5 95 g lnsects 2 O O 1 91 O 1 99 O A v. col. size 1·0 1 ·0 4·6 > Macone/licoccus ugandae Colonies 8 5 2 1 O 67 33 O 2 lnsects 12 6 2 5 O 29 71 O O A v. col. size 1·5 }·2 1 ·0 5·0 Ferrisia virgata Colonies O O 3 4 3 30 40 30 lnsects O O 3 8 20 10 26 65 Av. col. size 1·0 2·0 6·7 ~ Tylococcus westwoodi Colonies 96 3 91 4 O 96 4 O Insects 922 34 660 16 O 98 2 O Av. col. size 9·6 11·3 7·3 4·0 AH species Colonies 1313 161 345 345 136 41 41 17 lnsects 3891 2211 1415 5482 1838 16 63 21 Av. col. size 3·0 13·7 4·1 15·8 12·9 Mean (Iog) 0·200 0·344 0·288 0·444 0·433 col. size J t 19 521 shoots were examined in the laboratory and 104 187 in the field. - Not applicable.
-~ 142 C. A. M. CAMPBELL
workers, and because mealybugs were considerably under-recorded on shoots in the field. For example, in the laboratory, four times as many colonies and three times as many mealybugs as were counted in the field were found on shoots from a sample which constituted about one-fifth of that examined in the field. While the level of under-recording was established for shoots, this was not possible for the framework (unknown proportions of which were examined in the laboratory) or the trunk which was always searched in the field. The significantly larger average size of mealybug colonies recorded in the field (shoots, P < 0'01; framework, P < 0'05) shows that large aggregates were more likely to be detected than small colonies or individuals. Numerous small colonies of Plano coccoides n;,alensis were found in the laboratory, whereas with most other species colony sizes in laboratory and field were similar. Smaller colonies were found on shoots than on the framework (P < 0'001 for both field and laboratory), which did not differ significantly in size from those on the trunk. Donald (1955) also observed that mealybug populations on the trunk were on average larger than in the canopy. The degree of under-recording of the abundance of each species was affected by its con spicuousness, which was influenced not only by aggregate size but by the choice of feeding sites and whether the colony was attended by ants or not. Colonies of th05e species attended by Crematogaster spp. and Pheido/e spp. were usually prominent because they were mostIy protected by tents of carton and $Oil particles, respectively. The distribution data in Table 11 are comparable with other results (Strickland, 1951a; Donald, 1955), except that here the canopy populations were slightly under estimated owing to the loss of the four branches per tree examined in the laboratory. This was equivalent to a loss of 16% of canopy shoots and a smaller proportion of the framework. The relative importance of shoots, framework and trunk depended upon species and on whether colonies or total mealybugs were considered. Tylococcus westwoodi only occurred in the canopy, where it was mostly confined to shoots. In contrast, Pseudococcus ca/ceolariae (Maskell) occurred predominantly on the trunk. Except for Planococcus dtri, over 80% of colonies and of individuals of the six commonest species of mealybugs were found in the canopy. Coccoids other than mealybugs were mainly in the canopy (Table 111). Cribrole canium andersoni, A. elaeidis, Steatococcus sp. and the species of Gascardia near G.
TABLE 111. The distribution 01 coccoids other than mealybugs within 96 trees Laboratoryt Field Field and lab. data combined as percentages .A ,...--"-----., ,...- \ , \ Shoots Branch Shoots Branch Trunk Shoots Branch Trunk framework framework framework Steatococcus sp. ti O 101 2 O 98 2 O Gascardia sp. nr. G. zonata 517 42 2352 48 O 97 3 O Cribro/ecanium andersoni 23 1 185 O O 100 O O Stictococcus sjostedti 2731 517 10449 3997 158 74 25 1 Parastictococcus mu/tispinosus 92 14 1511 149 45 89 9 2 Parastictococcus hargreavesi O O 71 80 O 47 53 O Aspidiotus e/aeidis 11 O 472 O O 100 O O f384 branches were examined in the laboratory. AH else was examined in the field. zonata were almost exclusively on shoots. Stictococcids were mostly on branches and shoots, although Stictococcus sjostedti and Parastictococcus mu/tispinosus also occurred occasionally on pods. The data for P. hargreavesi were from one colony and may be unrepresentative of the species where common. . Strickland (1951b) and CornwelI (1957) found that the frequency of numbers of mealybugs per tree followed a logarithmic series. Cornwell also showed that frequencies HOMOPTERA OF COCOA IN GHANA 143
of other measures of mealybug abundance were adequately described by logarithmic series. Using the frequency c1asses and methods of Comwell and Strickland, the frequency of field counts of mealybugs on the 96 trees followed a logarithmic series (X26 = 9'90, n.s.). Insect counts were, therefore, transformed to log (x + 1) to norma lise the distribution prior to analyses of variance on the seven cornmonest species. Strickland (195Ib), Cornwell (1956) and Bigger (1975) all showed that mealybug num bers were positively correlated with the size of the trees. Consequently, counts of insects from the branches examined in the laboratory were initially analysed using, altematively, numbers (.¡ n) of leaves, shoots and vegetative buds as covariates. None of the covariates significantIy reduced the error variances, although the number of leaves was itself affected by the height of the branch in the crown. Signfficantly more leaves (P < 0'05) were present on upper branches than on lower ones. The results from the analyses of variances using log(x + 1) numbers per branch are summarised in Table IV. Only two species exhibited significant height preferences,
TABLE IV. Population densities on branches at three heights (mean log(x + 1» and optimum number 01 samples per tree (n) t Branch height Standard errors n of differences Lower Middle UI?per Replication* j k J j-j j-k Planococcoides njalensis Colonies 0·202 0·194 0·205 0·0289 0·0250 0·9 Insects 0·263 0·249 0·295 0·0444 0·0385 0·8 Planococcus citri Colo ni es 0·333 0·303 0·316 0·0329 0·0285 0·7 Insects 0·429 0·379 0·417 0·0508 0·0440 0·8 Phenacoccus hargreavesi Colonies 0·164 0·124 0·097 0·0260 0·0225 0·7 Insects 0·180 0·139 0·119 0·0306 0·0265 0·7 Tylococcus westwoodi Colonies 0·515 0·515 0·195 0·1095 0·0949 0·4 Insects 0·799a }·027 0·344a 0·2397 0·2076 0·4 Stictococcus sjostedti Insects 0·231 0·317 0·296 0·0569 0·0492 0·6 Gascardia sp. nr. G. zonata Insects 0·070 0·102 0·070 0·0281 0·0243 0·8 Mesohomotoma tessmanni Insects 0·325 0·350 0·401 0·0636 0·0551 0·8 t n = fIl where S; and S; are intra-tree variance and inter-tree intra-site variance. respectively. r.jS[ * j = 96 and k = 192 for species other than T. westwoodi, where j = 8 and k = 16. Means underlined or followed by the letter a are not significantly different (P = 0·05). but with neither species was the preference strong. Phenacoccus hargreavesi occurred less frequently on upper (U) branches (P < 0'05) than on middle and lower ones, as did T. westwoodi (Colonies, P < 0'01; Insects, P < 0'05 for middle (M) > U only). In contrast, Mesohomotoma tessmanni showed the opposite trend. with lower abun dance at lower levels, 'a1though the differences were not significant. For all species, counts for sites and trees within sites were more variable than samples within trees, Inter-site differences were highly significant (P < 0'01) for all spedes other than T. westwoodi (only data from two sites were used for that analysis). Similarly, inter-tree: intra-tree variance ratios were also significant (P < 0'05) for an species. As costs were the same for both sampling repeatedly within a tree and moving to another tree at the same site, for any given level of effort, maximum precision of estimates is obtained when the sampling fraction in each stratum is proportional to the square root of the variance in that stratum. The optimum sample was a fraction of between 0'4 and 0'9 branches per tree (Table IV), which in practice mean s one branch per tree. 144 C. A. M. CAMPBELL
Planococooide$ njalensis exhibited a significant inter-action between sites and its abundance at the three branch heights. This species was most abundant on the Amelonado cocoa at sites 1-4. Interactions occurred at sites 1, 2 and 4. The number of insects decreased with height at site 1 (Lower (L)
TABLE V. Number 01 occurrences 01 inlrequently recorded Homoptera
Branch height xl Lower Middle Upper No. examined 96 192 96 Pseudococcus longispinus 5 7 o 4·50 Pseudococcus concavocerarU 6 9 5 0·27 Pseudococcus calceolariae 2 o o 6·00 Maconel/icoccus ugandae 2 4 2 0·00 Steatococcus sp. 2 4 1 0·50 Cribrolecanium andersoni 5 5 3 1·90 Parastictococcus multispinosus 4 7 1 1·17 Aspidiotus elaeidis 1 o o 3·00 Toxoptera aurantU o 3 o 3·00 longispinus was the only species showing any apparent preference, but from two to five further records, none in the upper canopy, would be needed to confirm significant non-preference for upper branches by this species. Most other species were dispersed similarly at the three heights. P. calceolariae was recorded twice in the laboratory. On both occasions, single specimens were found on lower branches, lending sorne sup port to the field data (Table 11) that this species avoids the canopy. With the exception of F. virgara (which was not found on branches examined in the laboratory) all mealybug species infested buds (Table VI). No other feeding posi tion was universally used. Preferences for feeding positions varied, as did the propor Hons using any one. For example, 57% of Planococcoides njalensis colonies were found in buds, but beca use colonies were smaller there than OOi bark, this constituted only 15% of its population on branches. Planococcus citr; and T. westwoodi also had many small colonies in buds and fewer but larger colonies on bark. Leaves and tlower cushions were comparatively unimportant, except perhaps the latter for Maconelli coccus ugandae. Infesta.tions were also affected by tissue age (Table VII). Flaccid' leaves of flush 1 (the youngest growth) and terminal buds supported larger populations than older leaves and axiUary buds (both P < 0'001). Conversely, the bark of older shoots was more heavily infested than that of younger shoots (P < 0'001). Because flowering is sea- HOMOPTERA OF COCOA IN GHANA 145
TABLE VI. Feeding sites 01 mealybugs on 384 branches examined in the laboratory Total numbers on 384 branches A Leaves Buds Bark of Flower Bark shoots cushions Planococcoides njalensis Colonies 4 261 1I4 4 7S Insects 4 446 784 4 16S4 Planococcus citri Colonies 1I SSO 126 10 48 Insects 1I 999 420 10 484 Phenacoccus hargreavesi Colonies 1 163 26 S 13 Insects 1 223 29 S 16 Pseudococcus longispinus Colonies 2 8 2 1 O Insects 2 10 2 1 O Pseudococcus concavocerarii Colonies O 17 2 O 1 Insects O 18 2 O 1 PseudococclIs calceolariae Colonies O 2 O O O Insects O 2 O O O Maconellicoccus ugandae Colonies O 6 O 6 1 Insects O 9 O 7 2 Tylococcus westwoodi Colonies 7 48 41 2 1 Insects 34 120 768 33 1
TABLE VII. Influence 01 tissue age on inlestation by mealybugs (al! species) Flusht Total ,-- A 2 3 4 S+ Leaves No. examined 13S0 3948S 8324 18SS O S1014 No. infested 9 IS O O 24 % infested 0·7 0·1 0·0 0·0 0·1 Expected no. 1 19 4 1 2S '1.2 104·0 O·S 3·1 0·2 107 ·8··· Buds No. examined 40S 8S73 231 64 O 9273 No. infested 88 892 7 1 988 % infested 21·7 10·4 3·0 1·6 10·7 Expected no. 43 913 2S 7 988 X' 4S·7 O·S 1I·9 4·1 62·2··· Bark No. examined 411 99S7 S211 3912 t 19S21 No. infested 4 1I0 lIS 66 29S % infested 1 ·0 1 ·1 2·2 1·7 I·S Expected no. 6 IS1 79 S9 29S '1.2 O·S 10·6 IS·7 0·7 27·S··· Flower No. examined O 173 463 S69 1702 2907 cushions No. infested O 2 4 21 27 % infested 0·0 0·4 0·7 1·2 0·9 Expected no. 2 4 S 16 27 '1.2 0·8 0·8 0·1 1·4 3 ·ln.s. tFlush 1 being the youngest growth and S + the oldest (see text). - = not applicable. ···Significant at P < O·001. tNot quantified. n.s. not significant.
sonal, it was not surprising that the proportion of ftower cushions infested was the same from all ftushes.
Discussion The general objective of the studies for which sampling techniques were required was to consider factors inftuencing the abundance of the mealybug vectors of cocoa swollen shoot virus, and so to identify those which could be manipulated to decrease the spread of the disease. AH species of Homoptera which may be important were found in the canopy (Tables 11 & III), where population densities were assessed from branch samples. Other than for mealybugs, little has been published on the distribu tion of Homoptera within cocoa trees. The present results (Table 11) agree weH with 146 C. A. M. CAMPBELL
those of Donald (1955) (recalculated from the data he presented). He found that the percentage of the total population in the canopy was 97 for Planococcoides n;alensis, 66 for Planococcus citri, 100 for Phenacoccus hargreavesi, 87 for Pseudococcus con cavocerarii and 28 for F. virgata. The equivalent figures from the present study were 87, 66, 99, 100 and 36%, respectively. Strickland (l951a) also found that 87% of individuals of Planococcoides n;alensis were in the canopy, as here, although in his study 76% were on shoots. The average me for colonies of P. n;alensis reported by Strick land (1951b) was eight mealybugs, the same as shoots here. Sample units smaller than a branch were feasible for sorne species, depending on the objectives of the study. For example, with the exception of F. virgata, aH species of mealybugs were found in vegetative buds (Table VI). Combined with visual inspec tion to eye level, examination of buds was later used in a study where the presence or absence of mealybugs was the criterion (CampbeH, unpublished). Nevertheless, for population studies, one of several important criteria is that the proportion af the population in the sample unit should remain constant (Morris, 1955; Southwood, 1978). Campbell (1975) in a contemporary study found that for Planococcoides njalensis, Planococcus citri and Phenacoccus hargreavesi (the only species considered), the pro portions of the populations on shoots, lea ves and bark of the branch framework, fluctuated in response to the leaf-flushing cycle. Vegetative buds were not examined in that study, but infestation of vegetative buds declined from 21'7% on flush 1 to 10'4% on flush 2 (Table VII). Phenacoccus hargreavesi, T. westwoodi and possibly Pseudococcus longispinus and Planococcoides njalensis an Amelonado coco a varied in abundance on branches at the three heights (Tables IV & V), although all four species were relatively abundant on middle branches. The indeterminate growth of fan branches produces the typical dense interlocking canopy between adjacent cocoa trees. Relatively few branches pro trude from the canopy level, hence most samples of branches collected without bias would come from zones equivalent to the middle branches sampled here. The pre ferences of F. virgata and Pseudococcus calceolariae for the trunk, where they may be assessed by visual inspection, may indicate that these species are relatively less important vectors than canopy-inhabiting species. Planococcoides njalensis was the only species for which there was a significant interaction between sites and its abundance on branches at the three heights, but only on Amelonado cocoa. Donald (1957) commented that P. njalensis was commoner at upper levels in the crown, whereas Bigger (1972) observed that its pattern of distribu tion varied in response to environmental conditions, and this view was thus confirmed. At the time Cornwell (1955) abandoned his attempts to improve sampling techniques, P. njalensis was by far the dominant species of mealybug on coco a (Strickland, 1951a) and Amelonado was almost universally grown. In recent years, P. njalensis has become less prevalent, and few new plantings of Amelonado have been made at Tafo since the early 1950s (Annual Reports of the Cocoa Research Institute). Hybrids are also being used to replace farms devastated by coco a swollen shoot virus, although sorne 80-85% of cocoa in Ghana may still be Amelonado (Legg, 1979). The change in predominance of the mealybug fauna at Tafo (Bigger, 1972) and the change in varieties occurred simultaneously. However, these changes appear to have alleviated the sampling prob lems encountered earlier (Anon., 1950; Cornwell, 1955). The objectives of any specific investigation dictate which species must be studied and the appropriate sampling unit. Subsequent studies involve comparative experiments in which single branches per tree are taken and examined. In most instances, the replication required depends upon establishing a difference for the most important of the less numerous species. For example, consider a comparative experiment in which P. n;alensis is as abundant as at site 1 (Le. mean log (x + 1) = 1'247 per branch) under one treatment, and about one-tenth as abundant in another treatment (e.g. at site 19, mean log (x + 1) = 0'258 per branch). With a standard deviation of 0'3078, three HOMOPTERA OF COCOA IN GRANA 147
replicates would be sufficient to confirm the difference with a probability of 0'05 in 80% of cases (see Snedecor & Cochran, 1976, p. 111 for the method). However, in the same experiment, the density of S. sjostedti could also be important. The mean log (x + 1) insects per branch was 0'296 at site 1 and 0'105 at site 19 (the standard devia tion was 0'3939). To confirm this level of difference as significant, 68 replicates would be required. Again, depending on the objectives, economies may be possible for ant attended species. The organised ant actiV'ity associated with attendance of ccecoids high in the canopy is often apparent from the ground. Non-random samples of nearby twigs can confirm the presence or absence of specific insects. Other low density species create special analytical problems because of the high frequency of zero counts (South wood, 1978). Infrequency of occurrence of non-vector species probably indicates that they are unimportant in the epidemiology of cocoa swollen shoot virus. The disparities between field and laboratory estimates of mealybug densities raise doubts about the accuracy of previous absolute population estimates for mealybugs on cceoa. The field procedures were similar to those of previous studies (Strickland, 1951a; Hanna et a!., 1952; Donald, 1955; Cornwell, 1955, 1957; Entwistle, 1959; Bigger. 1972, 1981a), which usually showed means of 6-180 mealybugs/tree, although Comwell (1955) and Hanna et al. (1952) recorded means of 413 and 697-1350 mealy bugs/tree, respectively. Field resultSi from the present study indicate a mean popula tion of 102 mealybugs/tree (Table 11 corrected for the loss of 4 branches), which is consistent with most previous work. The mean may have been slightly reduced, as almost a quarter of the trees showed symptoms of swollen shoot disease. Cornwell (1956) found fewer mealybugs on trees recently infected with cocoa swollen shoot virus than on healthy ones, and numbers declined further as disease symptoms progressed. Nevertheless, he also commented that the pattern of mealybug distribution was the same on healthy and recen ti y infected trees. The present results can also be used to estimate absolute populations (Table VIII), omitting species with estimated populations of less than one insect per tree. Populations on the branch framework and trunks were ca1culated using values for the percentage detected on shoots in the field. For example, 1234 examples of P. njalensis were found on 19521 shoots examined in the laboratory and 343 were detected on 104 187 shoots examined in the field (Table 11). These data give a percentage detected value for P. njalensis of 5'2% in the field and an average population on shoots (1289 shoots per tree) of 81·5 insects. On the frame work, 3900 examples of P. njalensis were counted in the field. This was assumed to represent 5'2;;0 of the actual population. Hence, from Table 11, the total population on the framework was estimated as 74856 plus the 1658 counted in the laboratory, or 797 insects/tree. On the trunk, the numbers detected were assumed to represent 5'2% of the total population actually present. Similar procedures were used for other species. The estimates for T. westwoodi and Phenacoccus hargreavesi (both of which exhibited height preferences (Table IV» were adjusted for a branch frequency of 1: 18: 1 in lower. middle and upper categories, respectively. Because F. virgata and Pseudococcus calceolariae were not found on shoots in the laboratory and field. respectively, an arbitrary 10% detection value was assumed. Sorne uncommon or highly aggregated coccoids were recorded at lower densities on branches examined in the laboratory (Table 1), and for these species all of the population was assumed to have been detected. These assumptions were more likely to underestimate rather than over-estimate abun dances. For example, shoots generally lack the deeply fissured bark, wounds and the profusion of epiphytes and related plants which make the detection of mealybugs especially difficult on older wood, particularIy first instars (about 0'2 mm long (Bigger, 198tb», which constitute over 90% of the mobile population (Cornwell, 1956) and which probably establish most new colonies. The larger average colony size recorded on the framework and trunk compared with shoots (Table II & Donald (1955», may simply reflect the greater ease with which small colonies were detected on shoots rather than behavioural differences. 148 c. A. M. CAMPBELL
TABLE VIII. Estimated arithmetic mean numbers 01 insects per tree % Shoots Branch Trunk Total detected* framework Pscudococcidac Planococcoides njalensis 5·2 82 797 130 1009 Planococcus dtri 4·8 96 325 238 659 PIlenacoccus hargreavesi 1·8 17 42 1 60 PseudOcoccuslongúpinus 1·3 1 O 1 2 PseudOcoccus concavocerarU 12·2 1 O O 1 PseudOcoccus calceolarlae 10 O O 10 10 Maconellicoccus ugandae 3 ·1 1 2 O 3 Ferrúla vlrgata 10 O 1 2 3 -Pc;lococcus westwoodit 13·4 985 19 O 1004 otal Pscudococcidac: 198 1167 382 1747 Margarodidae Steatococcus sp. 100 O O Coccidac Gascardia sp. nr. G. zonata 85 34 1 O 35 Cribrolecanium andersoni 100 2 O O 2 Stictococcidae Stictococcus sjostedti 70 180 65 2 247 Parastictococcus multúpinosus 100 17 2 1 20 Parastictococcus hargreavesi 100 1 1 O 2 Diaspididae Aspidiotus elaeidis 100 5 O O 5 Psyllidae Mesohomotoma tessmanni ? 257 ? ? 257+ *No. of insects per shoot from examination in the field x 100 No. of insects per shoot from examination in the laboratory tOnly on trces with Crematogaster stadelmanni. tT. westwoodi not included. ?Not recorded in the field.
The average population so estimated was 1747 mealybugs/tree, with an additional 1004 examples of T. westwoodi on trees where C. stadelmanni was the dominant ant. These numbers exceed any previous estimates but resemble those of Cornwell (1955) and Hanna et al. (1952). Cornwell felled and searched 90 trees that were smaller (mean girth 15'5 cm) than those studied here (mean girth 59'4 cm) or by Strickland (I951b) (mean girth 35'5 cm). They were also densely planted (equivalent to 6050/ha; normal planting density is about 1500 trees/ha), which suggests that they were immature. Comwell (1956) later related mealybug numbers (y) on the same 90 trees directly to girths (in inches) using the regression log (y + 1) = (2,606 X log girth) - 0'049. Substituting girths from both Strickland's (l951b) study and the present study (re-caIculated in inches as geometric means) into this equation gives expected geometric means of 725 and 3027 mealybugs/tree, respectively. These estimates must be regarded cautiously, however, as they involve extrapolation beyond the range of Cornwell's data. Nevertheless, for data with a logarithmic distribution, geometric means are always less than the corresponding arithmetic means. For example, Corn welI's 413 mealybugs/tree was equivalent to a geometric mean of about 100 (Corn\\\ell, 1955). Fitting a logarithmic series to a population of 96 trees with an arithmetic mean of 1747 insects gave a corresponding geometric mean of 83 mealybugs/tree, weIl within the expected population caIculated from the girth data using Cornwell's equa tion, and also below the geometric mean found by Cornwell from his much smaller trees. ClearIy, the estimated populations of mealybugs in Table VIII were not high for large trees "thoroughly searched for mealybugs" (CornweIl, 1955). Homoptera other than mealybugs have been less thoroughly investigated on cocoa in West Africa (Entwistle, 1972). Relatively high populations were observed for both HOMOPTERA OF COCOA IN GHANA 149
S. sjostedti and the species of Gascardia near G. ,onata (Table VIII) and other less abundant spedes were also widespread (Table 1). Bigger (1981a) and Strickland (1951a) found tltat S. sjostedti was the most abundant species on cocoa with average popula tions of 69 and 241 insects/tree, respectively. S. sjostedti was also the most abundant species recorded in the field in the present study (Table 1), but it was fourth in corrected results (Table VIII) with about the same average abundance as found by Bigger. Similarly, Steatococcus sp. was found at one/tree in the present study and by Bigger. In contrast, both Bigger and Strickland recorded the species of Gascardia near G. ,onata at 1 per tree compared with the present average of 35/ tree. Bigger (1981 b) discussed the likelihood of bias in the apparent composition of the mealybug fauna caused by the greater ease with which colonies that were large and/or attended by ants (usually Planococcoides njalensis) were detected compared with less aggregated species not attended by ants. Strickland (1951b) found that P. njalensis outnumbered all other spedes combined by almost 100: 1 and 89% were attended by ants. For shoot populations, the percentage detected values indicate the potential for misinterpreting the composition of the mealybug fauna. For both P. njalensis and Planococcus citd, the degree of under-recording was similar, whereas Phenacoccus hargreavesi was the most seriously underestimated of the commoner species. The dark red body of T. westwoodi renders it less conspicuous than species covered in white wax. Nevertheless, because of the activity of its attendant ant, a higher percentage of the population of this species was detected than of any other mealybug, which sup ports Bigger's hypothesis. However, as Planococcoides njalensis and Planococcus citri together considerably outnumber all other species, the poorer detection of the latter group would have little effect on the apparent faunal composition. From 1973 to 1976 at Tafo, the present study was concurrent with that of Bigger (1981b) on smaller trees, albeit using different field procedures. Nevertheless, the results for relative abundance of the commOD'er mealybug species were remarkably similar (Table IX). They confirm a clear change in the composition of the mealybug
TABLE IX. The percentages 01 the diDerent species 01 mealybugs on cocoa lound by diDerent authors Nigeria Tafo, Ghana ,. A . Reference Sutherland Donald Strickland Bigger Present study (1955) (1955) (1951a) (1981b) Field Lab. Years of survey 1951-52 1954-55 1947-49 1973-76 1973-77 Planococco~des njalensis 48·9 26·5 98·9 58·7 56·0 47·4 Planococcus dtri 42·7t 26·5 1·0 28·2 33·4 31·5 Phenacoccus hargreavesi 2·4 1 ·6 >0·1 8·4 1 ·1 4·5 Pseudococcus concavocecarii 1·6 1·7 >0·1 1·6 0·2 0·3 Ferrisia virgata 4·0 8·6 >0·1 3·0 0·4 O Other spp. or unidentified 0·4 35·0 >0·1 0·1 8·9 16·2 tInc\udes Planococcus kenyae (Le Pelley). complex in recent years and a close resemblance to Nigeria's cocoa studied during the early 1950s. Bigger (l981b) emphasised the importance of this change for the epidemio logy of swollen shoot disease, because the species which replaced Planococcoides njalensis are much more mobile. Inaccuracies caused by under-recording have greatest implications for the apparent proportion of trees more or less continuously infested with mealybugs. Strickland (1951a) commented .. It is probably safe to say that approximately half of the trees ... are infested ... with oqe or other of the Pseudococcid species known or suspected as vectors of CSSv." Itf-íhe present study, the field records indicated that for example 25 of 96 trees were infested with P. njalensis, 64 with Planococcus citri, 20 with ISO C. A. M. CAMPBELL
PheTUlCOCCUS hargreavesi and 11 with Pseudococcus concavocerarii (Table 1). The laboratory results showed that a further 41, 25, 49 and 9 trees were infested with each of the aboye species, respectively. The number of trees infested with any species of mealybug increased from 75 to 95. Together with Bigger's (1981b) conclusions on the mobility of the several species of mealybugs found on cocoa, these data suggest that virtually all mature cocoa trees in the Eastern Region of Ghana should be regarded as supporting populations of potential vectors of cocoa swollen shoot virus.
Acknowledgements 1 am grateful to K. J. Martin for statistical advice and many staff at Tafo for technical assistance. This paper is published with the permission of the Director of the Cocoa Research Institute of Ghana. The work was sponsored by the British Overseas Development Administration.
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(Received 23 June 1982)
© Commonwealth Agricultural Bureaux, 1983