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Ecology of Heteropsylla Cubana (Homoptera: Psyllidae): Psyllid Damage, Tree Phenology, Thermal Relations, and Parasitism in the Field

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Ecology of Heteropsylla Cubana (Homoptera: Psyllidae): Psyllid Damage, Tree Phenology, Thermal Relations, and Parasitism in the Field POPULATION ECOLOGY Ecology of Heteropsylla cubana (Homoptera: Psyllidae): Psyllid Damage, Tree Phenology, Thermal Relations, and Parasitism in the Field CHRIS A. GEIGER AND ANDREW P. GUTIERREZ Center for Biological Control, ESPM-Insect Biology, 201 Wellman Hall, University of California, Berkeley, CA 94720 Downloaded from https://academic.oup.com/ee/article/29/1/76/385909 by guest on 29 September 2021 Environ. Entomol. 29(1): 76Ð86 (2000) ABSTRACT The fast-growing Central American tree Leucaena leucocephala (Lam.) de Wit (Le- guminosae: Mimosoidaeae) has been widely planted in the tropics since the 1970s for agro-forestry, reforestation, and fodder. Since the mid-1980s the tree has suffered serious damage throughout its exotic range from the psyllid Heteropsylla cubana Crawford, which is also native to Central America. This article summarizes Þeld studies on the tree and the psyllid conducted at 2 sites in north Thailand: a cool highland and a warm valley site. In the highlands, mean psyllid densities per shoot were slightly higher, defoliation was greater, and dry matter production losses due to the psyllid were Ͼ3 times higher than those at the valley site (62.5 and 18.3% losses, respectively). Using Þeld data, the lower thermal thresholds for tree growth and psyllid development were 11.2 and 9.6ЊC, respectively. Psyllid abundance was negatively correlated to temperature. When maximum temperatures exceeded 36ЊC, psyllid abundance fell dramatically, mortality increased, and body size decreased. These data suggest that the tree and the psyllid are climatically mismatched. H. cubana prefers new shoots, and population cycles were related to tree growth cycles. Finally, populations of the introduced para- sitoid Psyllaephagus yaseeni Noyes (Hymenoptera: Encyrtidae), native coccinellids, and spiders showed little correlation to the psyllid populationÕs intrinsic rate of increase. Percentages of para- sitism by P. yaseeni were low (mean ϭ 1.2Ð1.9%, maximum ϭ 6.0%) and no evidence of density dependent regulation was found. KEY WORDS Heteropsylla cubana, Leucaena leucocephala, Psyllaephagus yaseeni, biological con- trol, agroforestry, sampling Leucaena leucocephala (LAM.) de Wit (Leguminosae: quantiÞed. The coccinellid predator Curinus coeruleus Mimosoideae) is a fast-growing tree of Central Amer- Mulsant has had partial success in Hawaii (Nakahara ican origins planted worldwide for tropical reforesta- et al. 1987) and Indonesia (Mangoendihardjo and tion, agroforestry, and silvipastoral uses (Brewbaker Wagiman 1989, Wagiman et al. 1989), but has failed to 1987). These plantings are attacked extensively by the establish in many seasonal-dry areas and is a poor leucaena psyllid Heteropsylla cubana Crawford. In the disperser (Funasaki et al. 1989, Oka 1989, Wagiman et early 1980s, this pest began spreading westward from al. 1989). The coccinellid Olla v-nigrum (Mulsant) has its native Central America and became a pantropical also been widely introduced but appears ineffective problem within 10 yr. In the Þrst 2 yr of infestation, the (Chazeau et al. 1992). The parasitoid Tamarixia leu- psyllid caused hundreds of millions of dollars in dam- caenae Boucek (Eulophidae) has been introduced re- age in the AsiaÐPaciÞc region (Heydon and Affonso cently in Tanzania, but its effectiveness has not been 1991), with losses in biomass production reaching 33% assessed. Despite the economic importance of leu- (Oka 1989). The economic importance of the tree has caena, the effectiveness of biological control agents spurred considerable research into its agronomics for H. cubanaÑand the fundamental physiological (NAS 1977), host plant resistance to the psyllid ecology of the tree and its psyllid pestÑremain poorly (Wheeler and Brewbaker 1990) and biological control understood. of the psyllid (Napompeth 1989). Chemical controls Several studies have documented the population of the psyllid have proven ineffective and costly, ex- dynamics of this psyllid and its natural enemies (Braza cept when used to protect nursery stocks of leucaena 1987, Bray and Woodroffe 1988, Villacarlos et al. 1989, (NFTA 1987). For ecological and economic reasons, Shivamurthy et al. 1991, Doungsa-ard 1992, Room et al. classical biological control has been deemed the most 1993). Some evidence suggests that temperature appropriate management strategy to control the psyl- causes the wide seasonal ßuctuations of H. cubana lid in its new range. observed in Thailand and elsewhere (Yasuda and Tsu- The most widely introduced biological control rumachi 1988). The effects of temperature on H. cu- agent is the parasitoid Psyllaephagus yaseeni Noyes bana development have been measured in 2 labora- (Encyrtidae); however, its efÞcacy has not been well tory studies (Yasuda and Tsurumachi 1988, Baker et al. 0046-225X/00/0076Ð0086$02.00/0 ᭧ 2000 Entomological Society of America February 2000 GEIGER AND GUTIERREZ:ECOLOGY OF H. cubana 77 1993), whereas the effects of temperature on mortality phase. Soil moisture was plentiful at the valley site and fecundity are known only for other psyllid species because of seepage from nearby irrigation ditches. At (Hodkinson 1974). Room et al. (1993) concluded that the highland site, the moisture-holding capacity of the cycles of new leaf growth are partially responsible for soil was greater and rainfall generally provided sufÞ- H. cubanaÕs seasonal oscillations, as they are for the cient moisture. psyllid Trioza erytreae (Del Guercio) on citrus Bionomics. Temperature Effects on Tree Growth. At (Catling 1969). each site, new leaßets were labeled weekly on 10 Our objective is to enlarge on previous efforts by vigorously growing terminal shoots kept free of ßower measuring a full range of biotic and abiotic factors buds (“terminal shoots” hereafter refers to the apical affecting psyllid populations. For this purpose, a com- meristem of a lateral branch, including all new leaves prehensive data set was collected in north Thailand on down to and including the 1st fully expanded leaf). soil and weather factors, tree growth and phenology, Leaf length and internode length and width were psyllid populations, and natural enemies. These data recorded weekly for all labeled leaves (n ϭ 2,045). The Downloaded from https://academic.oup.com/ee/article/29/1/76/385909 by guest on 29 September 2021 were used to examine tree and psyllid physiological growth rate of the leaves in the range of 25Ð50 mm was ecology, links between tree phenology and psyllid expressed as percentage increase in leaßet length per populations, and the impact of natural enemies. Lit- day, because this is the leaf size with the least age- erature reviews of the tree and psyllid, dynamic anal- speciÞc variance in growth rates. yses using simulation models, and further details on Temperature Effects on Psyllid Growth and Develop- methodologies can be found in Geiger (1995). ment. Growth and development rates of H. cubana were measured in the Þeld at the valley site using 10 Materials and Methods same-age cohorts of Ϸ200 psyllid nymphs each. Each cohort was enclosed in a mesh Þeld cage to exclude Statistical Analyses. All statistical analyses were per- natural enemies. Body size and instar were recorded formed using SYSTAT version 5.2 (Wilkinson et al. from pooled samples of 30 randomly selected individ- 1992). Data were tested for linearity, normality, and uals taken every 2 d. This study was repeated 9 times equal variance in all regression analyses, and outliers Ͼ throughout the year. Development rates were re- were identiÞed by DFFITs scores 1 (Velleman gressed against ambient mean temperature (corrected 1988). SE(y) denotes standard error of the estimate for cage effects by adding 1ЊC), and the lower tem- (square root of residual mean-square error). perature threshold was estimated as the x-intercept. Study Sites. All studies were conducted between Development rates were computed as the reciprocal September 1992 and March 1994 at 2 sites in Chiang of degree-days above 10ЊC elapsing between oviposi- Mai Province of northern Thailand (18Њ 40Ј N, 99Њ 02Ј tion and the beginning of the 5th-instar period. E). The valley site is near Mae Jo, elevation 220 m, and Degree-days were calculated using a sine-wave algo- the highland site is 20 km away near Mae Sa Mai, elevation 1,000 m. There are 3 seasons in both areas: rithm (Gilbert et al. 1976). the warm rainy season (southwest monsoon), the cool Psyllid fecundity was estimated by caging individ- dry season, and the hot dry season. The climate at the ual, newly emerged, mated female psyllids on leu- valley site is seasonal-dry tropics, with 900Ð1,100 mm caena seedlings in the laboratory, and counting the of precipitation per year. Climate at the highland number of eggs laid each day. Two male psyllids were (Mae Sa Mai) site is similar but on average is Ϸ5ЊC caged with each female to assure mating. Female wing cooler than the valley site, with an additional 200Ð300 length, body length, and head width were measured at mm of precipitation. Soil at the highland site is death. Fecundity over a 96-h period was then re- reddish-brown, well-drained, inactive lateritic clay, gressed against female body size variables. Dessicated pH 4.2Ð5.1. Soil at the valley site is dark grayish-brown, females were removed from the analysis. Wing length poorly drained, low humic clay soil, pH 6.2Ð6.7. of 30 randomly selected adult females was also mea- Three-month-old L. leucocephala trees (ÔK8Õ) were sured weekly at both sites, and their fecundity was planted at both sites (284 trees at the valley site, 154 estimated by dissection. Wing length, egg length, and in the highlands) and inoculated with Rhizobium sp. ovariole number were then regressed on mean tem- and vesicular-arbuscular mycorrhizal fungus. The peratures for the 2 previous weeks. strains of microorganisms used are speciÞc to L. leu- Survivorship of the psyllid from egg to 5th instar was cocephala and facilitate nitrogen Þxation and nutrient estimated using same-aged cohorts in the Þeld (valley uptake, respectively. Trees in Þeld plots were divided site).
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