The Pool of Coccinellids (Coleoptera: Coccinellidae) to Control Coccids (Homoptera: Coccoidea) in Portuguese Citrus Groves

Home , Icerya purchasi, Planococcus citri, Scymnini, Scymnus (beetle), Scymnus auritus

Bol. San. Veg. Plagas, 25: 311-320, 1999

The pool of Coccinellids (Coleoptera: Coccinellidae) to control Coccids (Homoptera: Coccoidea) in Portuguese citrus groves

A. MAGRO & J. L. HEMPTINNE

Integrated Pest Management programmes in Portugal pay main attention to coccids. The study of coccinellids for the biological control of those pests was undertaken. This paper aimed firstly to determine which coccidophagous ladybirds are more likely to control coccids by examining Dominance, Constancy and Persistence along the year. A second goal was to shed some light on the feeding regime of several species of the Scymnini tribe. Eight coccidophagous ladybirds have been observed to have a strong presence in Portuguese citrus groves. They correspond to species regularly considered as important for the biological control of coccids in other Mediterranean countries. Five species of the Scymnus genus are also very important in the sampled orchards. Though usually considered as aphidophagous, their abundance is correlated to the appearance of coccinellids which are predators of coccids. A first large scale phenology of the most important ladybird beetles in citrus orchards is provided which can help to schedule chemical interventions.

Key words: Coccinellids, coccids, citrus, biological control, Scymnus spp.

INTRODUCTION fight against the referred phytophagous (HODEK, 1970, COPPEL & MERTINS, 1977, Integrated pest management research pro- IPERTI, 1987, MAJERUS, 1994, DIXON, et al, grammes have been developed in Portuguese 1997). citrus groves since 1990. Main attention is A large scale survey of citrus orchards in paid to Planococcus citri (Risso), Saissetia Portugal revealed the richness of communi- oleae (Olivier), and Lepidosaphes beckii ties of coccidophagous ladybirds (MAGRO, et (Newman) that are considered as key pests in al, submitted). There were also many mem- continental Portugal (CARVALHO et al., in bers of the Scymnini tribe the feeding prefe- press). rences of which are hardly known. Biological control is an important issue in The tendency in biological control is to the above mentioned programmes. The study neglect the vast potential of indigenous pre- of the coccinellids present in citrus groves dators. Frequently they are often regarded as and their contribution for the biological con- inefficient and practitioners tend to adopt trol of coccids was undertaken for these pre- classical biological control and to rely on dators have proved often successful in the well known exotic species that are subse-

1 Ecole Nationale Supérieure Agronomique de Toulouse, Av. de l'Agrobiopole, Auzeville-Tolosane, BP 107-F31326 Castanet - Tolosan Cedex, France. 2 Ecole Nationale de Formation Agronomique, BP 87-F31326 Castanet-Tolosan Cedex, France. quently introduced. Such an approach is cle- MATERIALS AND METHODS arly illustrated in the context of attempts to control aphids. Coccinella septempunctata Samples of adult coccinellids were collec- L. has been purposely released in the USA ted in citrus groves from Algarve, Setúbal against cereal aphids despite the presence of and Santarém, the three main citrus regions diversified guilds of indigenous ladybirds in Portugal (Table 1). (SCHAEFER, et al, 1987). On the contrary, in Ladybirds were collected following the Europe, C septempunctata has a reputation «Beating method», recommended by IOBC of inefficiency (CRAWLEY, 1992) and there is (AMARO & BAGGIOLINI, 1982). 100 branches a move towards releasing Harmonia axyri- uniformly distributed in each orchard were dis Pallas. Similarly, the coccidophagous selected and beaten with a stick. In order to Cryptolaemus montrouzieri Mulsant is now standardise the sampling method, each established all around the world and, in Por- branch was stricken three times. The insects tugal, Nephus reunioni Fiirsch was care- so dislodged fell in a j ar attached at the bot- lessly tested and released in the vicinity of tom of a tray in a form of a funnel. This met- Lisbon. It is now regularly extending its hod mainly yielded adult ladybirds but few range throughout the country (MAGRO, et al., larval instars. Orchards were visited one or submitted). two times a month as indicated in Table 1. The side effects of these introductions that Coccinellids were identified with keys often follow an hit-and-miss (KAREIVA, published by CHAZEAU, et al. (1974), Gou- 1996) approach are now questioned RREAU (1974), RAIMUNDO & ALVES (1986), (HOWARTH, 1991, TOWNSEND, 1991, MILLS, FÜRSCH (1987 a, b) and RAIMUNDO (1992). 1994, CLOUT, 1995, ELLIOTT, et al, 1996, Most identifications were achieved by consi- SIMBERLOFF & STILING, 1996). The best solu- dering external characters but extraction and tion to avoid such possible effects is to use observation of genitals was needed for about the word «efficient» with an extreme pruden- 1100 individuals. ce and to improve the knowledge on indigenous predators. ANALYSIS OF RESULTS This paper prolongs previous works on biological control of citrus coccids (MAGRO, Dominance, Constancy and Persistence 1997, MAGRO, et al, in press). It aims firstly to determine which coccidophagous species The values of Dominance (D) and Cons- are more likely to control coccids by exami- tancy (C) were calculated for the guilds of coc- ning dominance, constancy and persistence cid predators and those with unknown food of species in different communities. A preferences in citrus in each grove and year: second goal is to shed some light on the feeding regime of several species of the Scym- D = xlOO and C = -^-xl00 nini tribe. N

Table 1. - Period, periodicity of sampling, number of sampled groves (NG) and total number of collected samples (CS) per region.

Region NG Period Periodicity CS Algarve 12 Monthly 131 Setúbal 2 Every week till the end of October 1991 168 and every two weeks afterwards Santarém 1 Every week till the end of October 1991 74 and every two weeks afterwards where n. is the number of captured individuals in species /, N is the total number of captured individuals, pi is the number of samples where the species i was present and p the total number of collected samples. Mean and extreme values of those two Covariation between species parameters where calculated for each of the three years of captures in the groves of Setú- Covariation was calculated from the acti- bal and Santarém and for the total of the 12 vity periods (see 2.). Spearman's rank coeffi- groves in Algarve. Species were then classi- cients were used because they best evaluate fied according to the following intervals: similarities between species based on abundance data (LEGENDRE & LEGENDRE, 1984 and LUDWIG & REYNOLDS, 1988). The software «Stecol» (LUDWIG & REYNOLDS, 1988) Dominant was chosen for the analysis. Sub-dominant In order to identify the groups of species Accessory closer in terms of adult population dyna- Vestigial mics in citrus, an hierarchical and agglome- rative clustering based on the results of Spearman's rank coefficient was perfor- med. Distance between objects was compu- Constant ted using Lance and Williams linear combi- Sub-constant natorial equation with parameters corres- Incidental ponding to Ward's method. Clustering was done with the software «Progiciel R. Persistence (P), which measures the num- Analyse multidimensionnelle, analyse spa- ber of years a species is present in the sam- tiale» (LEGENDRE & VAUDOR, 1991). The ples, was calculated for the groves of Setúbal results of the cluster analysis were sumari- and Santarém. sed in a dendrogram. The importance of the presence of different coccinellids in citrus was then compared on the basis of the values of A C and P. Sampling for immature stages of Scymnus spp and Nephus spp. Periods of activity From Spring to Summer 1995 samples of fruits, leaves and young branches of citrus The results of captures from all the groves infested with S. oleae, L. beckii, various and years were considered. For each month mealybugs, A.floccosus and different aphids and species, the mean number of captured were collected. The samples were brought individuals per month was calculated. The back to laboratory and carefully searched for percentage of activity (A) was calculated: eggs and larval stages of Scymnus spp. and Nephus spp.

RESULTS where Mv.. is the mean value of captures of species / in the monthy and TMvi the sum of 19112 individuals from 38 species were all the monthly mean values for species i captured and seven species were only repre- (along the 12 months of a year). Six classes sented by one individual (Table 2). Table 2 - Total number of species of Coccinellids captured in citrus groves from the regions of Setúbal, Santarém and Algarve, Dominance values (Dv - %) and food preferences (Fp). N = total number of individuals. 1 = Diaspididae, 2 = Coccidae, 3 = Pseudococcidae, 4 = Icerya purchasi, 5 = aphids, 6 = mites, 7 = white flies, 8 = plants, 9 = fungus, 10 = unknown food preferences in citrus orchards.

Chilocorini 1 Noviini Chilocorus bipustulatus L. Rodolia cardinalis (Mulsant) Exochomus nigromaculata (Goeze) Platynaspini E. quadripustulatus L. Platynaspis luteorubra Goeze Coccidulini Scymnini Lindorus lophantae (Blaisdell) Clitosthetus arcuatus (Rossi) Rhizobius chrysomeloides (Herbst) Cryptolaemus montrouzieri Mulsant R. litura Fabricius Nephus bisignatus Boheman Coccinellini Nephus includens (Kirsch) Adalia bipuncatata (L.) Nephus reunioni Fiirsch A. decempunctata (L.) Nephus binotatus Brisout Coccinella septempunctata L. Nephus ulbrichi Fiirsch Oenopia conglobata (L.) Nephus hickei Fiirsch 0. doublieri (Mulsant) Nephus fuerschi Plaza 0. lyncea (Oliv.) Scymnus mediterraneus Khnzorian Propylea quatuordecimpunctata (L.) Scymnus auritus (Thunberg) Psyllobora vigintiduopunctata (L.) Scymnus subvillosus (Goeze) Tytthaspjs sedecimpunctata (L.) Scymnus suturalis Thunberg Epilachnini Scymnus apetzi Mulsant Subcoccinella vigintiquatuorpunctata L. Scymnus interruptus (Goeze) Hippodamiini Scymnus levaillanti Mulsant Hippodamia variegata (Goeze) Scymnus rufipes (Fabricius) Hyperaspini Stethoruspunctillum (Weise) Hyperaspis reppensis Herbst

A few individuals of the species Nephus food preferences in each region. Note that peyerimhoffi Sicard, claimed by Raimundo Dominance values are always calculated (1992) as being present in Portugal, might be against total values that is for all coccinellid among those identified as N. includens which species. Dominance and Constancy are would raise the number of species to 39. We variable for each species either in the same were not able to distinguish these two species year in different groves or in different years due to the unclear descriptions of the genita- in the same grove. However some patterns lia of N. peyerimhoffi provided by Raimundo emerge; the ladybirds can be sorted out in (1992) and Fiirsch (1987b). five groups: The Scymnini tribe is the richer and more dominant one with 18 species corresponding Group I - Dominant and Constant species: to 72% of captured individuals. Table 3 (a and b) shows the results of C. bipustulatus, R. chrysomeloides, N. Dominance, Constancy and Persistence for includens, S. mediterraneus, S. subvillosus, the coccid predators and those with unknown S. interruptus and 5". punctillum. Chilocorus 2-pustulatus Exochomus nigromaculatus E. 4-pustulatus Lindorus lophantae Rhizobius chrysomeloides Adalia 10-punctata Propylea 14-punctata Rodolia cardinalis Clistosthetus arcuatus Cryptolaemus montrouzieri Nephus includens N. reunioni Scymnus apetzi S. interruptus S. levaillanti S. mediterraneus S. subvillosus Stethorus punctillum

Fig. 1, - Periods of activity (monthly) of some species of coccinellids in citrus in Portugal. * absence of data for this month.

Group II - Sub-dominant and Constant Group V - Vestigial and Incidental species: species: R. litura, H. reppensis, P. luteorubra, N. L. lophantae, R. cardinalis, C. montrou- bisignatus, N. binotatus, N. hiekei, N. fuers- zieri and S. apetzi. chi, S. auritus, S. suturalis and S. rufipes. Group III - Accessory and Constant species: Persistence follows the same decreasing tendency. E. quadripustulatus, N. reunioni and S. levaillanti. The periods of activity of species in groups I to III as well as some well known Group IV - Accessory and Incidental species: and abundantly represented coccinellids N. ulbrichi. from other guilds (A. decempunctata, P. qua- a)

\- A. 10-punctata 6- E. 4-pustulatus \\- R, cardinal is 16-5. mediterraneus 2- C. arcuatus 7- Z,. lophantae 12-R. chrysomeloides 17- 5. punctiilum 3- C. 2-pustulatus 8- JV, inciudens 13-5. apetzi 18- 5. subvillosus 4- C montrouzieri 9- A\ reunioni 14-5. interruptus 5- E. nigromaculatus 10- /*. 14-punctata 15-5. levaillanti

A. 10-punciata C. montrouzieri £ 4-pustulatus S. subvillosus P. 14-punctata R. cardinalis R. chrysomeloides C. 2-pustulatus L. lophantae S. interruptus S. mediterraneus £ nigromaculatus S. apetzi C. arcuatus S. punctiilum N. inciudens N. reunion¡ S. levaillanti

Fig. 2. - Covariance between coccinellid species in terms of activity periods in citrus, a) Covariation matrix. Upper part presents values of Spearman's rank coefficient and lower part the significatif covariation (* - a=0,05; ** - a=0,01). b) Dendrogam based on the degree of positive covariation between species (Ward's method). A to E - main detected groups. tuordecimpunctata, E. nigromaculatus and diaspidids, A. decempunctata and P. qua- C. arcuatus) are presented in Figure 1. Sum- tuordecimpunctata on aphids and C. arcua- mer time is the period where the activity is tus on white-flies. higher but we can see that the majority of the coccinellids can be present all over the year. The matrix of covariation between the DISCUSSION AND CONCLUSIONS activity periods and the corresponding dendrogram lead to five groups of species (Figu- The tribes Chilocorini and Coccidulini are re 2, a and b). Group A is an assemblage of better represented in the samples from citrus species having their main activity in Spring orchards than the Coccinellini (Table 2). The and group E in Autumn. The three remaning Scymnini tribe is however dominant in terms display intermediate periods of activity. of richness and abundance but the ecology of The analysis of Figures 1 and 2 can give us all these species remain unclear. some cues on Scymnus spp. possible food Dominance and Constancy values (Table 3 preferences: S. interruptus and S. mediterra- a and b) were highly variable. This is not neus belong to group C and were mainly exclusive to coccinellids but is a consequen- caught in Summer. Their activity is highly ce of the interaction between species of any correlated with that of C. bipustulatus, L. community and their relationship with a fluc- lophantae and E. quadripustulatus. It is the- tuating environment (BEGON, et al., 1996). refore suggested that S. interruptus and S. Variability does not hide a pattern as the spe- mediterraneus are probably predators of coc- cies are distributed in five groups in terms of cids and diaspidids. S. apetzi could be inclu- their dominance, constancy and persistence ded in the same group but is neverthless dis- in the communities. That is the dominant tinctive by a long period during which it does species were always the same even if the hie- not turn up, in the samples. S. subvillosus rarchy within the group was variable in time behaves very similarly to E. quadripustula- and space. The same applies to the other cate- tus which can either feed on coccids, diaspi- gories. This situation was also observed for dids or aphids. S. levaillanti comes very late aphidophagous coccinellid guilds in diffe- being more close to the mealybug predators rent habitats (HEMPTINNE, 1989) and for N. reunioni and N. includens, the mite preda- parasitoid guilds (EHLER, 1994, MILLS, tor S. punctillum or the white-flies predator 1994b). There are hypothesis to explain the- C. arcuatus. se changing hierachies but they need to be A. decempuncata and P. quatuordecim- experimentally tested. In a perspective of punctata are two true aphid predators. There biological control, the impact of species ran- is no species that display a clear correlation king on pest populations remains an impor- with their activity (Fig. 1). The two highest tant research topic (Ehler, 1994). values of Spearman's rank coefficient arose Ladybirds in groups I, II and III have the with the two Exochomus that have a wide strongest presence in citrus orchards.They range of prey and feed on aphids. Although represent a potential pool of species for bio- their fecundity is higher when feed on coc- logical control of citrus coccids in Portugal. cids they can lay eggs on an aphid diet (RAD- They are regularly considered in such a way WAN&LÕVEI, 1982). by KEHAT & GREENBERG (1970), LONGO & In the plant material brought to laboratory BENFATTO (1987), CLIMENT (1990a and b) for the control of immature stages of Scym- and MARI, et al. (1991). Scymnus spp. are nus and Nephus species, we were never able sometimes mentioned for citrus orchards in to find eggs or larvae but for S. interruptus other countries but nobody grant them much and S. subvillosus on aphid colonies at spring importance. time. Larvae of L. lophantae and C. bipustu- The species of the genus Scymnus are latus were though present on coccids and usually considered as aphidophagous (e.g. Table 3. - Species of Coccinellids captured in citrus groves from the regions of Setúbal (Vidais and Várzea), Santarém (C. Cadaval) and Algarve (12 groves), a) Distribution in classes of Dominance: V (vestigial) = [0.01%-l%[, Ac (accesory) = [1% -12%[, Sd (sub-dominant) = [12% - 25%[, D (dominant) = [25% -100%). b) Values of Persistence (P) and distribution in clases of Constancy: In (incidental) = [1% - 20%[, Sb (sub-constant) = [20% - 40%[, C (constant) = [40% - 100%]. * species present in only one sample. • = mean value and |—| = variation interval (minimum and maximum values). HODEK, 1973, iPERTi, 1983, CLIMENT, 1990b). PROTA, et al., 1984, LONGO & Russo, 1986). On the contrary, in our samples the presence However, this strategy of control is not sup- of adults is correlated to the appearance of ported by studies on the dynamics or the rela- coccinellids predators of other pests. They are tive efficiency of each species. The present not correlated with the periods of activity of study points out that as expected these two two true aphid predators, A. decempunctata species are syncronized with their host and and P. quatuordecimpunctata. These results therefore opens the question of the existence suggest that several Scymnus increase the of competition between the two predators. pool of coccidophagous species. Experiments Finally, this work provides a first large have to be undertaken to clarify that point. At scale phenology of the most important lady- the moment it is not possible to firmly rule out bird beetles in citrus orchards. It is a valuable aphidophagy among the Scymnini of this data in the context of an integrated pest study. They could be breeding on aphids out- management because pesticides applications side the orchards and move in later in the sea- can be scheduled to minimize harmful effects son in response to large quantity of honeydew on the beneficial fauna. excreted by coccids and white-flies. HAGEN, et al. (1970) and EVANS (1994) have demons- trated the powerful attraction of honeydew for ACKNOWLEDGEMENTS several predators. C. montrouzieri is the most commonly This paper was written while the first aut- used predator in biological control against P. hor was on a postdoctoral fellowship of the citri. In the late 25 years N. reunioni was Fundação para a Ciência e Tecnologia - Por- introduced in several countries and used in tugal - (Programme Praxis XXI). The rese- inondative releases sometimes in conjuntion arch was supported by a PhD grant from the with C. montrouzieri (ALEXANDRAKIS, 1984, same programme.

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