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 appe- arance 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 indige- nous 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 fee- ding 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 indivi- duals 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 abun- dance data (LEGENDRE & LEGENDRE, 1984 and LUDWIG & REYNOLDS, 1988). The soft- ware «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 diffe- rent 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