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 KEY WORDS Heteropsylla cubana, Leucaena leucocephala, Psyllaephagus yaseeni, biological control, agroforestry, sampling Leucaena leucocephala (LAM.) de Wit (Leguminosae: Mimosoideae) is a fast-growing tree of Central American origins planted worldwide for tropical reforestation, agroforestry, and silvipastoral uses (Brewbaker 1987). These plantings are attacked extensively by the leucaena psyllid Heteropsylla cubana Crawford. In the early 1980s, this pest began spreading westward from its native Central America and became a pantropical problem within 10 yr. In the Þrst 2 yr of infestation, the psyllid caused hundreds of millions of dollars in damage in the AsiaÐPaciÞc region (Heydon and Affonso 1991), with losses in biomass production reaching 33% (Oka 1989). The economic importance of the tree has spurred considerable research into its agronomics (NAS 1977), host plant resistance to the psyllid (Wheeler and Brewbaker 1990) and biological control of the psyllid (Napompeth 1989). Chemical controls of the psyllid have proven ineffective and costly, except when used to protect nursery stocks of leucaena (NFTA 1987). For ecological and economic reasons, classical biological control has been deemed the most appropriate management strategy to control the psyllid in its new range. The most widely introduced biological control agent is the parasitoid Psyllaephagus yaseeni Noyes (Encyrtidae); however, its efÞcacy has not been well quantiÞed. The coccinellid predator Curinus coeruleus Mulsant has had partial success in Hawaii (Nakahara et al. 1987) and Indonesia (Mangoendihardjo and Wagiman 1989, Wagiman et al. 1989), but has failed to establish in many seasonal-dry areas and is a poor disperser (Funasaki et al. 1989, Oka 1989, Wagiman et al. 1989). The coccinellid Olla v-nigrum (Mulsant) has also been widely introduced but appears ineffective (Chazeau et al. 1992). The parasitoid Tamarixia leucaenae Boucek (Eulophidae) has been introduced recently in Tanzania, but its effectiveness has not been assessed. Despite the economic importance of leucaena, the effectiveness of biological control agents for H. cubanaÑand the fundamental physiological ecology of the tree and its psyllid pestÑremain poorly understood. Several studies have documented the population dynamics of this psyllid and its natural enemies (Braza 1987, Bray and Woodroffe 1988, Villacarlos et al. 1989, Shivamurthy et al. 1991, Doungsa-ard 1992, Room et al. 1993). Some evidence suggests that temperature causes the wide seasonal ßuctuations of H. cubana observed in Thailand and elsewhere (Yasuda and Tsurumachi 1988). The effects of temperature on H. cubana development have been measured in 2 laboratory studies (Yasuda and Tsurumachi 1988, Baker et al. 0046-225X/00/0076Ð0086$02.00/0 q 2000 Entomological Society of America Downloaded from https://academic.oup.com/ee/article/29/1/76/385909 by guest on 17 June 2022 Environ. Entomol. 29(1): 76Ð86 (2000) ABSTRACT The fast-growing Central American tree Leucaena leucocephala (Lam.) de Wit (Leguminosae: 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 .3 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 9.68C, respectively. Psyllid abundance was negatively correlated to temperature. When maximum temperatures exceeded 368C, 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 parasitoid Psyllaephagus yaseeni Noyes (Hymenoptera: Encyrtidae), native coccinellids, and spiders showed little correlation to the psyllid populationÕs intrinsic rate of increase. Percentages of parasitism by P. yaseeni were low (mean 5 1.2Ð1.9%, maximum 5 6.0%) and no evidence of density dependent regulation was found. February 2000 GEIGER AND GUTIERREZ: ECOLOGY OF H. cubana Materials and Methods Statistical Analyses. All statistical analyses were performed using SYSTAT version 5.2 (Wilkinson et al. 1992). Data were tested for linearity, normality, and equal variance in all regression analyses, and outliers were identiÞed by DFFITs scores .1 (Velleman 1988). SE(y) denotes standard error of the estimate (square root of residual mean-square error). Study Sites. All studies were conducted between September 1992 and March 1994 at 2 sites in Chiang Mai Province of northern Thailand (188 409 N, 998 029 E). The valley site is near Mae Jo, elevation 220 m, and the highland site is 20 km away near Mae Sa Mai, elevation 1,000 m. There are 3 seasons in both areas: the warm rainy season (southwest monsoon), the cool dry season, and the hot dry season. The climate at the valley site is seasonal-dry tropics, with 900 Ð1,100 mm of precipitation per year. Climate at the highland (Mae Sa Mai) site is similar but on average is '58C cooler than the valley site, with an additional 200 Ð300 mm of precipitation. Soil at the highland site is reddish-brown, well-drained, inactive lateritic clay, pH 4.2Ð5.1. Soil at the valley site is dark grayish-brown, poorly drained, low humic clay soil, pH 6.2Ð 6.7. Three-month-old L. leucocephala trees (ÔK8Õ) were planted at both sites (284 trees at the valley site, 154 in the highlands) and inoculated with Rhizobium sp. and vesicular-arbuscular mycorrhizal fungus. The strains of microorganisms used are speciÞc to L. leucocephala and facilitate nitrogen Þxation and nutrient uptake, respectively. Trees in Þeld plots were divided into sprayed (label rates of imidachloprid) and unsprayed treatments, with all other conditions held constant. Because many tropical soils are nutrient poor and acidic, both research plots were fertilized and lime was added at the highland site to raise the pH by '2 points. (Such soil amendments may not be cost-effective for resource-poor farmers.) The slope of the land was 0 Ð7% at the valley site, and 6 Ð16% at the highland site. The trees were irrigated only during the establishment phase. Soil moisture was plentiful at the valley site because of seepage from nearby irrigation ditches. At the highland site, the moisture-holding capacity of the soil was greater and rainfall generally provided sufÞcient moisture. Bionomics. Temperature Effects on Tree Growth. At each site, new leaßets were labeled weekly on 10 vigorously growing terminal shoots kept free of ßower buds (“terminal shoots” hereafter refers to the apical meristem of a lateral branch, including all new leaves down to and including the 1st fully expanded leaf). Leaf length and internode length and width were recorded weekly for all labeled leaves (n 5 2,045). The growth rate of the leaves in the range of 25Ð50 mm was expressed as percentage increase in leaßet length per day, because this is the leaf size with the least agespeciÞc variance in growth rates. Temperature Effects on Psyllid Growth and Development. Growth and development rates of H. cubana were measured in the Þeld at the valley site using 10 same-age cohorts of '200 psyllid nymphs each. Each cohort was enclosed in a mesh Þeld cage to exclude natural enemies. Body size and instar were recorded from pooled samples of 30 randomly selected individuals taken every 2 d. This study was repeated 9 times throughout the year. Development rates were regressed against ambient mean temperature (corrected for cage effects by adding 18C), and the lower temperature threshold was estimated as the x-intercept. Development rates were computed as the reciprocal of degree-days above 108C elapsing between oviposition and the beginning of the 5th-instar period. Degree-days were calculated using a sine-wave algorithm (Gilbert et al. 1976). Psyllid fecundity was estimated by caging individual, newly emerged, mated female psyllids on leucaena seedlings in the laboratory, and counting the number of eggs laid each day. Two male psyllids were caged with each female to assure mating. Female wing length, body length, and head width were measured at death. Fecundity over a 96-h period was then regressed against female body size variables. Dessicated females were removed from the analysis. Wing length of 30 randomly selected adult females was also measured weekly at both sites, and their fecundity was estimated by dissection. Wing length, egg length, and ovariole number were then regressed on mean temperatures for the 2 previous weeks. Survivorship of the psyllid from egg to 5th instar was estimated using same-aged cohorts in the Þeld (valley site). The cohorts were established at room temperature by isolating mated female psyllids individually on 14-d-old L. leucocephala seedlings for 24 h. The seedlings were fastened to full-grown trees in a partially shaded area at a height of 1.5 m. A petroleum jelly barrier was put around the base of each seedling to exclude natural enemies. Surviving psyllids were counted every 2 d. Observations were also made on seedling and psyllid condition and the occurrence of predation and parasitism. This experiment was repeated 8 times. Downloaded from https://academic.oup.com/ee/article/29/1/76/385909 by guest on 17 June 2022 1993), whereas the effects of temperature on mortality and fecundity are known only for other psyllid species (Hodkinson 1974). Room et al. (1993) concluded that cycles of new leaf growth are partially responsible for H. cubanaÕs seasonal oscillations, as they are for the psyllid Trioza erytreae (Del Guercio) on citrus (Catling 1969). Our objective is to enlarge on previous efforts by measuring a full range of biotic and abiotic factors affecting psyllid populations. For this purpose, a comprehensive data set was collected in north Thailand on soil and weather factors, tree growth and phenology, psyllid populations, and natural enemies. These data were used to examine tree and psyllid physiological ecology, links between tree phenology and psyllid populations, and the impact of natural enemies. Literature reviews of the tree and psyllid, dynamic analyses using simulation models, and further details on methodologies can be found in Geiger (1995). 77 78 ENVIRONMENTAL ENTOMOLOGY Natural Enemy Effects. Predators and mummies of the parasitoid P. yaseeni were counted weekly on 60 shoots per site. The percentages of parasitization were calculated from mummy and 5th-instar counts using the method of Luck et al. (1988): Percentage parasitism 5 ~number of mummies/shoot) (correction factor)(number of 5th instar/shoot) with Correction factor 5 Development time of mummy 9.8 d 5 5 3.8. Development time of 5th instar 2.6 d A 2nd estimate of parasitization was made from monthly dissections of 100 randomly collected 5thinstar nymphs per site. Density dependence of parasitism was examined graphically using scatterplots of parasitization rates versus psyllid 5th-instar density 2Ð 6 wk earlier. This relationship was quantiÞed using PearsonÕs correlation tests. Populations of all natural enemies were compared with psyllid populations and psyllid R0 using scatter plots and simple linear regression/correlation. Results Bionomics. Temperature Effects on Tree Growth. The effects of temperature on tree growth were assessed by regressing proportional leaf growth rates (y) on mean temperature (x). The thermal threshold for L. leucocephala growth, estimated from the x-intercept of equation 1, was determined to be 11.28C. y 5 0.00613x 2 0.0689, r2 5 0.85, P , 0.001, n 5 20, SE~ y! 5 0.0006. [1] The thermal threshold should be estimated with other growth factors held at maximum (nonlimiting) levels, hence only the valley data were used in this analysis. Soil moisture was highly collinear with temperature for the highland site trees, whereas the valley site had a fairly constant source of moisture. Temperature Effects on Psyllid Growth and Development. Development times for all instars are presented in Table 1. Minimum development times from the Þeld data were somewhat longer than laboratory estimates (Baker et al. 1993), and no psyllids matured in 2 replicates when mean temperatures inside the Þeld cages were 29.5 and 29.18C and maximum temperatures over 368C. A regression of development rates on mean temperatures yields a lower temperature threshhold of 9.68C (equation 2). By comparison, laboratory data by Yasuda and Tsurumachi (1988) suggest a threshhold of 8.68C (equation 3). The y-intercepts of the 2 regressions are not signiÞcantly different (t 5 0.612, n 5 6, P . 0.50), allowing the Þeld and laboratory data to be pooled. Before pooling, the laboratory data were standardized using the development rate at 288C as the maximum. A threshhold of 9.88C was estimated from pooled data (Fig. 1; equation 4). Downloaded from https://academic.oup.com/ee/article/29/1/76/385909 by guest on 17 June 2022 Sampling. Monitoring Tree Biomass Growth. Trees were destructively sampled twice during the study (9 June 1993 and 24 February 1994). The trees were cut at ground level and the subunits sorted, counted and dried 48 h at 1088C before weighing. Regressions were performed using total stem diameter (MacDicken et al. 1991), tree height, and a combination of these 2 factors as predictors of total tree and stem biomass. In the nondestructive sampling, the diameter and height of every tree in the study was measured every 2 mo at the valley site and every 3 mo at highland site. Psyllid defoliation was rated each time using a 0 Ð9 scale (e.g., no defoliation to complete defoliation, Glover 1987). Reductions of tree biomass caused by psyllid feeding were assessed by comparing the biomass of sprayed and unsprayed trees using 2-way analysis of variance (ANOVA). Leaf area was measured using video imaging and the area was regressed against leaf dry weight. Psyllid Sampling Studies. Twenty-three terminal shoots were clipped into separate plastic bags. Psyllid nymphs and adults were washed off the terminals in the bags using soapy water, and the liquid was strained through wire screens onto muslin Þlters. Psyllid nymphs and adults were stored on these Þlters in 70% ethanol until they were counted by instar. The accuracy of the washing method was evaluated by regressing these counts against absolute counts that included psyllids remaining on the terminal. In a separate analysis, mean counts from population census data (see below) were regressed against sample variances to estimate degree of clumping and to develop sampling decision rules (Taylor 1961). Psyllid eggs were estimated by counting eggs on 1 leaßet of the oldest unexpanded leaf. This leaf is the most attractive oviposition site (Elder and Mayer 1990, Doungsa-ard 1992). Two-way ANOVA was used to determine the relative importance of leaßet position and egg density for estimating total eggs per leaf. A simple linear regression of leaßet egg count on total eggs per leaf was then conducted. Phenology and Population Dynamics. Tree Growth Phenology. Flower buds, ßowers, developing seeds, and dry seeds were counted on each of 10 marked branches weekly at each site to monitor ßowering phenology. Larger branches had proportionately more reproductive parts, hence the data were standardized by dividing each count by its corresponding branch weight, as estimated from the branch widthweight regression. Psyllid Population Dynamics. Psyllid population densities were estimated from 15 cut terminals per site per week, using the sampling method described above. The Þnite rate of increase R0 (cf., Southwood 1991) was estimated for each sample period by comparing current 5th instar counts to counts 1 generation earlier, using a generation time estimate of 321.3 DD (Baker et al. 1993). For this purpose, 5th-instar populations between sampling dates were estimated by linear interpolation. Thus, calculated, R0 represents a measure of population growth between generations. Vol. 29, no. 1 February 2000 GEIGER AND GUTIERREZ: ECOLOGY OF H. cubana 79 Table 1. Field estimates of cumulative developmental time for H. cubana, valley site, compared with laboratory estimates from the literature Estimated cumulative development time (8C-days . 108C) n 1st 2nd 3rd 4th 5th Adult 7 5 4 5 5 5 In the laboratory, 258Cb In the Þelda Min. Max Mean SD Mean 53.3 85.0 116.8 150.5 196.3 224.0 87.9 130.6 157.3 185.8 237.7 308.5 70.4 109.8 139.2 171.8 209.2 263.2 11.8 19.8 18.0 14.4 17.4 29.2 52.5 93.7 118.5 139.5 156.0 195.0 Values represent cumulative physiological time from oviposition to the beginning of each instar stage. a Each value summarizes observations from n cohorts, with 30 psyllids sampled per day per cohort. b Calculated from Baker et al. (1993). y 5 20.0555 1 0.00579x, u 5 9.68C, r2 5 0.84, P 5 0.009, n 5 8, SE~ y! 5 0.0012 [2] y 5 20.0405 1 0.00470x, u 5 8.68C, r2 5 0.96, P 5 0.003, n 5 7, SE~ y! 5 0.0054 [3] y 5 20.521 1 0.0534x, u 5 9.88C, r2 5 0.89, P , 0.001, n 5 13, SE~ y! 5 0.0062. [4] Psyllid Mortality. Survivorship curves for the different Þeld cohorts are summarized in Fig. 2. Mortality caused by predation and parasitism was insigniÞcant (,1%), hence these curves primarily reßect mortality caused by intrinsic and abiotic factors. Cohorts reared during hot periods had greater early instar mortality, and this is reßected in the increased concavity of the survivorship curves, whereas those reared during Fig. 1. Lower temperature threshhold (u) for development of H. cubana estimated from Þeld data, compared with threshhold estimated from laboratory data in the literature (Yasuda and Tsurumachi 1988). Fig. 2. Standardized survivorship (Lx) in the Þeld for H. cubana in 5 studies at different temperatures, each with 10 replicates. For clarity, standard error is shown only for 2 studies. Temperatures shown are mean temperatures for the entire study. cooler periods had shallower curves. No nymphs survived past 2nd instar (data not shown) when maximum temperatures were 36.68C or higher. A regression of total survivorship on mean temperature gave a signiÞcant negative correlation, suggesting that mortality increases with temperature in the range 25Ð308C (y 5 852 2 26.2x, r2 5 0.42, P , 0.001, n 5 27, SE[y] 5 5.77). These survivorship data were also Þtted to a parabolic function (Fig. 3) with the x-intercept being the thermal threshold for development (as in Gutierrez 1996). This function implies that there are upper and Fig. 3. Survivorship of H. cubana to 4th instar y plotted against mean temperature x, Þtted to the parabolic function y 5 350Ð2.48(x–19.47)2 (r2 5 0.94). Error bars show standard error of the mean. Downloaded from https://academic.oup.com/ee/article/29/1/76/385909 by guest on 17 June 2022 Instar 80 ENVIRONMENTAL ENTOMOLOGY Vol. 29, no. 1 Fig. 4. H. cubana abundance (A, E), parasitism (B, F) and predator abundance (C, D, G, H) at the valley (AÐD) and highland (EÐH) sites. lower bounds for survivorship (see ShelfordÕs “Law of Tolerance,” Shelford 1931). Relative humidity had no discernable effect on mortality, supporting the laboratory Þndings of Baker et al. (1993). The population census data provide further evidence of temperature-related mortality. Psyllid populations at valley sites fell dramatically at the onset of the hot season, when mortality and dessication of adult psyllids were widespread (Fig. 4A). Leucaena shoot growth was vigorous at that time, hence food was probably not a limiting factor. During this period, dead psyllids were examined for evidence of predation (mandible marks) and fungal hyphae, but ,1 in 20 deaths could be attributed to these causes. Psyllid Fecundity. SigniÞcant positive relationships were found between various measures of body size and the number of eggs laid over a 96-h period, but variance was high in all cases. Average fecundity (eggs per day 6SD) was 51.0 6 18.0 (n 5 14) for nondesiccated females, with a maximum of 154. The regression of 96-h total fecundity y on measures of body size x (body length 3 head width2) for 37 adult H. cubana in laboratory studies was y 5 516.5x 2 150.1, r2 5 0.42, P , 0.001, n 5 37, SE(y) 5 102.9. Temperature Effects on Psyllid Body Size. Psyllid body size was expected to bear an inverse linear relationship to temperature within the range of temperatures encountered in the Þeld (daily means of 13Ð 308C) (Atkinson 1994). To test this hypothesis, an analysis of covariance was performed using wing length as the dependent variable, site as the categorical independent variable, and mean temperature and log psyllid population (time lagged 1 wk into the past) as independent covariates. The effect of population density was found to be site-speciÞc and not signiÞcant in the full model (n 5 34, P 5 0.81). The negative slopes of wing length versus temperature regressions were not signiÞcantly different between sites (P 5 0.10), allowing pooling of data. In the Þnal model, signiÞcant negative relationships were found between wing length and temperature and between egg length and temperature (Fig. 5; equations 5 and 6). Wing length (mm) 5 62.47 2 0.58(Mean temp, 8C) r2 5 0.66, P , 0.001, n 5 23, SE~ y! 5 1.18 [5] Egg length (mm) 5 30.62 2 0.29(Mean temp, 8C) r2 5 0.64, P , 0.001, n 5 16, SE~ y! 5 0.78. [6] The relationships above suggest that high temperatures reduce not only body size (hence fecundity), but also egg size. This Þnding is consistent with our observation that body size declined steeply during the population crash at the onset of hot weather (NBCRC 1996, Napompeth 1989, Villacarlos et al. 1989). Sampling. Monitoring Tree Biomass Growth and Psyllid Damage. Measurement of tree biomass using repeated destructive samples was impractical in our study. Regressions to convert nondestructive size measurements into dry biomass equivalents were obtained from 2 sets of destructive sampling data. Total stem diameter (Dtot) (MacDicken et al. 1991) proved to be the most reliable predictor of total stem biomass Downloaded from https://academic.oup.com/ee/article/29/1/76/385909 by guest on 17 June 2022 Fig. 5. H. cubana wing length and egg length compared with temperature (mean for the previous week) at 2 valley sites. Slopes for the 2 sites were not signiÞcantly different at P 5 0.05 (t-test). February 2000 GEIGER AND GUTIERREZ: ECOLOGY OF H. cubana 81 Table 2. Parameters and statistics for regression equations estimating total H. cubana per shoot (y) from counts made using the water wash sampling method (x) Instar a b r2 n Sb SE(y) 1st 2nd 3rd 4th 5th All nymphs Adults 2.071 2.418 1.711 0.977 0.957 2.237 0.999 0.925 0.879 0.919 1.011 1.024 0.906 1.035 0.875 0.949 0.927 0.937 0.893 0.960 0.988 23 23 23 23 23 23 23 0.076 0.045 0.056 0.057 0.077 0.040 0.025 0.315 0.273 0.425 0.431 0.422 0.230 0.059 Regressions are of the form y 5 a(x 1 1) b . All P values are ,0.001. Sb is the standard error of the slope, b. Stem biomass: Ms 5 0.038Dtot 2.82 r2 5 0.91, P , 0.001, n 5 62, SE~ y! 5 0.114 [7] Total biomass: Mtot 5 0.00378~Dtot 1.738 !~H1.126 ! Fig. 6. Sample sizes required for ennumerative sampling at various conÞdence intervals. D is proportion of sample means falling outside conÞdence interval, a/2 5 0.10, calculated as in Wilson and Room (1982). Adults, solid line; nymphs, dashed line. R2 5 0.97, P , 0.001, n 5 61, SE~ y! 5 0.0924 [8] Leaf area: Al 5 0.9528Ml r2 5 0.97, P , 0.001, n 5 32, SE~ y! 5 0.0001. [9] Equations 7 and 8 were used to convert measurements of tree height and total stem diameter from the nondestructive samples into their dry biomass equivalents. Psyllid Sampling Studies. There was no signiÞcant difference in eggs per leaßet between leaßets at different positions on the 1st unfolded leaf, as determined by one-way ANOVA (F 5 0.894; df 5 8, 277; P 5 0.52). Therefore, 1 leaßet from the 1st unfolded leaf was adopted as the sample unit for sampling psyllid egg densities. Regressions of total eggs per leaf y on eggs per leaßet x were highly signiÞcant (equation 10). Adding leaßet length to the regression did not significantly increase the R2. y 5 11.74x1.020 , r2 5 0.85, P , 0.001, n 5 21, SE~ y! 5 0.099. [10] For sampling of nymphs and adults per shoot, densities estimated using the water wash method were compared with absolute counts (Table 2). Regressions were highly signiÞcant for all life stages; but because separating 1st and 2nd instars was time-consuming these stages were pooled in Þeld samples. Population means (x# ) and variances (S2) are known to have the relationship S2 5 ax# b (Taylor 1961) with the parameter b revealing the type of population distribution. If b 5 1 the data are normally distributed, if b . 1 the distribution is clumped and if b , 1 the distribution is more uniform. In this analysis, b 5 1.72 for adults and 1.92 for nymphs, indicating that both stages have clumped distributions. These so-called TaylorÕs coefÞcients (from equations 11 and 12) may be used to develop sampling decision rules to estimate sample precision over different sample sizes and population densities (Karandinos 1976, Wilson and Room 1982). Adults: S2 5 1.90x# 1.72 , r2 5 0.98, P , 0.001, n 5 27, SE~ y! 5 0.049 [11] Nymphs: S2 5 1.08x# 1.92 , r2 5 0.96, P , 0.001, n 5 24, SE~ y! 5 0.089. [12] The decision rules for different levels of accuracy are graphed in Fig. 6. With 15 samples per date, the percentage of sample means falling within the conÞdence interval is 70 Ð75%. Because psyllid populations ßuctuate over 3 orders of magnitude, this level of error was considered acceptable. Phenology and Population Dynamics. Psyllid Damage. On the average, tree growth in the highlands was considerably slower than in the valley. Eighteen months after transplanting, mean total biomass production for uninfested highland trees was 25.8% that of uninfested valley trees. Biomass accumulation in sprayed and unsprayed trees was compared with estimates of the amount of psyllid damage at each site. Psyllid activity reduced total dry biomass by 18.3% in the valley (F 5 6.55; df 5 1, 64; P 5 0.013) and 62.5% in the highlands (F 5 23.8; df 5 1, 45; P , 0.001). Tree Growth Phenology. Leaf growth was signiÞcantly depressed on trees with developing seeds, as Downloaded from https://academic.oup.com/ee/article/29/1/76/385909 by guest on 17 June 2022 (Ms) (equation 7), whereas total stem diameter plus tree height (H) were the best predictors of total biomass (Mtot) (equation 8). The relationships between leaf area (Al) and leaf mass (Ml)were also determined (equation 9) for use in future modeling studies. (In our samples, mass is in grams; diameter in millimeters, area in square millimeters, and height in centimeters.) 82 ENVIRONMENTAL ENTOMOLOGY Vol. 29, no. 1 Fig. 7. Typical ßowering phenology (AÐD) for a single L. leucocephala branch, valley site, 1993Ð1994. shown by regressing a measure of vegetative growth (leaf bud numbers) on green seed pod counts and tree height (centimeters) (equation 13). In this regression, the positive coefÞcient for tree height simply means that larger trees have greater numbers of leaf buds, whereas the negative coefÞcient for seedpods reßects the impact of a competing sink for photosynthate allocation. Leaf Buds 5 22.297 1 0.0727~Height! 2 0.1741~Seedpods! [13] 2 R 5 0.39, P , 0.001, n 5 54, SE~ y! 5 6.452. Cycles of seed production are of interest because tree reproduction reduces the habitat available for psyllid feeding and oviposition. In general, budding, ßowering, and seed maturation are synchronized within each branch (as shown in sample data from 1 branch in Fig. 7), whereas they are less synchronized among branches on the same tree, and still less so among trees. The effects of various environmental conditions (rainfall, soil moisture, humidity, and temperature) on ßower induction were explored using correlational analysis, but no clear relationships were found. Psyllid Population Dynamics. Because H. cubana prefers to feed on fast growing new leaves, the correlations between psyllid growth and new leaf abundance was assessed. A strong cyclical relationship was observed (Fig. 8). Populations sometimes expanded rapidly, causing massive defoliation and a subsequent crash of the psyllid population. This crash was apparently caused by a lack of suitable feeding and oviposition sites. During periods of defoliation, adults would crowd onto the remaining new growth, often covering the green woody stems with their eggs. Although mortality of the eggs was not quantiÞed, very few early instar psyllids appeared to survive under such conditions. Abundant new shoot growth occurred between 2 and 5 wk after each defoliation, with the highest correlation between psyllid damage and regrowth occurring with a 3 wk lag (Pearsons r 5 0.473, Bonferroni P 5 0.009, n 5 43). However, by the time new growth commenced, very few nymphs and adult psyllids remained. These cycles of defoliation and regrowth were stronger and more synchronized at the highland site. Although psyllid populations also exploded at the valley site, the trees were larger and complete defoliation did not occur. The negative effects of high temperature on psyllid numbers were most dramatic at the valley site, where a regression of mean weekly temperature (x, lagged by 1 wk) and total psyllid nymph densities (y, log transformed) was strongly negative (y 5 2.04 Ð 0.068x, r2 5 0.51, P , 0.001, n 5 86, SE[y] 5 0.19). No such relationship was found for the highland site (P 5 0.65). Natural Enemy Effects. The parasitoid P. yaseeni was prevalent only during the cool season at both sites (Fig. 4 B and F). The rate of parasitism of 5th-instar nymphs as measured by dissection averaged 1.9 and 1.2% at the valley and highland sites respectively, with a maximum of 6% observed on one date at the highland site. Parasitism rates estimated using mummy counts averaged 0.23%, with a maximum of 5.3% (n 5 143, SD 5 0.62). Scatterplots of percentage parasitism versus populations of 2nd through 4th instars were examined using different time lags to test for density related parasitism. At the highland site, parasitism rates showed no increase with density when using a 2-wk time lag (i.e., the time to mummy formation, reßecting the parasitoidsÕ functional response), but the relationship was weakly negative using a 6-wk lag (i.e., the generation time 1 2 wk, reßecting the numerical response, r 5 20.39, P 5 0.01, n 5 38). At the valley site, no signiÞcant trends in parasitism were found using the same time delays. Overall, there was no evidence of density dependent regulation of H. cubana numbers by P. yaseeni. Downloaded from https://academic.oup.com/ee/article/29/1/76/385909 by guest on 17 June 2022 Fig. 8. Cycles of psyllid damage and tree regrowth at valley (AÐD) and highland (EÐH) sites, Chiang Mai, plotted against physiological time (8C-days). Dashed arrows are added to clarify connection between psyllid defoliation events and subsequent regrowth. February 2000 GEIGER AND GUTIERREZ: ECOLOGY OF H. cubana R0 5 0.303 2 2,968 (Coccinellids per psyllid nymph) r2 5 0.47, P , 0.001, n 5 36, SE~ y! 5 0.517. [14] Discussion Ecophysiological Constraints. The ecophysiological tolerances (e.g., temperature, humidity, moisture, or nutrient requirements) of a species help determine that speciesÕ geographical range (Shelford 1931) and its Þtness in a particular environment (Gutierrez 1996). Between a plant and an herbivore, some overlap in geographical range is obviously necessary to make trophic relationships possible. However, their ecophysiological tolerances need not be identical. Some aphid species, for example, have temperature requirements that limit serious infestations to cooler seasons, whereas their plant hosts may prosper at much higher temperatures (Gutierrez et al. 1984). Such differences in environmental tolerances between plant and herbivore (or between an herbivore and its predator or parasitoid) may be further enhanced in exotic species, depending on the speciÞc biotypes introduced and their genetic range (van den Bosch et al. 1982). In the case of a classical biological control introduction, a mismatch of introduced biotypes may result in unsatisfactory control of a pest that is well regulated in its native environment (Huffaker and Messenger 1964). In a plant-herbivore system, the result may be the restriction of serious herbivory to certain environments, identiÞable by their climate, soils, or other abiotic factors. The data presented here suggest such a mismatch between the temperature tolerances of the exotic L. leucocephala ÔK8Õ and its herbivore H. cubana. Field studies found that the lower thermal threshold for growth of the tree is 11.38C, which is consistent with thresholds in other fast-growing tropical legumes (Landsberg 1986). Meanwhile, the Þeld estimate of the lower thermal development threshold for H. cubana is 9.68C (equation 13), which is not signiÞcantly different from the laboratory estimate of 8.68C (Yasuda and Tsurumachi 1988). These thresholds must be considered rough estimates, because of the nonlinear nature of development rate-temperature curves. Still, a mismatch in temperature tolerances between L. leucocephala and H. cubana is supported by our other Þndings as well. For example, early-instar mortality increased considerably with increasing temperatures, with an upper temperature threshold of '32Ð338C (Fig. 3). At moderately high temperatures, H. cubana size and fecundity decreased, and cohorts caged in the Þeld failed to survive when maximum temperatures exceeded 36.68C. Field populations declined precipitously at the beginning of the hot season each year, similar to previous observations in Thailand (NBCRC 1996), Vietnam (Napompeth 1989), Australia (Room et al. 1993), and the Philippines (Villacarlos et al. 1989). Tree growth during these hot periods, however, remained vigorous and healthy, so it is unlikely that food quality or quantity is responsible for the psyllid decline. The pronounced negative effects of temperature on H. cubana body size (hence fecundity) and egg size (hence viability) also contribute to its poor performance during the hot season. In other species, body size correlates with nutritional status, fecundity, and intrinsic mortality rates (Murdie 1969, Gutierrez et al. 1984, Denno et al. 1986, Leather 1994). The relationship to fecundity is conÞrmed for H. cubana by this study. Average fecundities here are somewhat lower than those reported in the literature (Maneeratana 1989, Winotai 1989, Baker et al. 1993), possibly because of inadequate humidity controls in the laboratory experiments. Finally, the clear difference in psyllid population dynamics and damage between highland and lowland sites also points toward mismatched temperature tolerances. Freed from extremes of high temperatures, psyllid populations do not fall dramatically each year in the highlands. No strong negative correlation was found between temperature and population as observed in the valley. Thus, the combination of higher psyllid populations and slower tree growth are major factors limiting L. leucocephala production in the highlands, reducing biomass there by 62.5%, or .3 times the damage measured in the valley. It is possible that the H. cubana biotype introduced to Southeast Asia evolved in cooler climes, resulting in Downloaded from https://academic.oup.com/ee/article/29/1/76/385909 by guest on 17 June 2022 Entomopathogenic fungi were only observed during one 2-wk period at the height of the rainy season (12Ð29 September 1993), but were a major source of mortality. Dying adults and nymphs turned pinkish and adhered to leaves, later becoming a mass of greyish-white hyphae. The pathogens involved were identiÞed as Entomophthora sp. and Entomophaga sp., with Fusarium sp. (a weak pathogen-saprophage) also present. During this period, 59% of sampled psyllids had visible hyphae and 32% were dessicated for a total of 91% mortality (n 5 400). Populations of coccinellid predators reached higher levels in the valley than in the highland site, but their presence was more consistent in the highlands (Fig. 4 C and G). Coccinellid populations tracked psyllid populations only in the valley, but they were rarely high enough at either site to have plausible impact. The highest observed coccinellids:psyllids ratio was 1:71, with a median of 1:6,250. The predominant coccinellid predators at all sites were Menochilus sexmaculatus (F.), followed by Oenopia sauzeti Mulsant and O. kirbyi Mulsant (highland site only), and Micraspis discolor (F.) (valley site only). Coccinella transversalis F. and Micraspis lineata (Thunberg) were occasionally observed at the valley site. Numerous spider and dragonßy species, 4 species of ants, vespid wasps, syrphids, reduviids, mirids, 1 Geocoris species, and lacewings were also observed preying on H. cubana, but they were not abundant. A signiÞcant negative correlation of psyllid R0 on natural enemy numbers per psyllid would suggest a possible role in regulating psyllid numbers. However, only coccinellids (all species lumped together) showed a signiÞcant negative correlation with R0, and only at the highland site (equation 14). 83 84 ENVIRONMENTAL ENTOMOLOGY 1982), whereas in the valley psyllid populations have a broad, annual cycle (Fig. 4A). Parasitoids considered desirable as biological control agents are generally thought to operate in a density dependent manner (Huffaker and Messenger 1964, Murdoch et al. 1985), but no evidence of density dependence was found for P. yaseeni. This Þnding could indicate that P. yaseeni is an inefÞcient searcher, does not aggregate to higher psyllid densities, aggregates at a different spatial scale than the one sampled (Morrison and Strong 1980), cannot reproduce quickly enough to keep pace with psyllid populations, or some combination of the above. At least the 1st possibility is unlikely, because we found P. yaseeni during periods when the psyllid was extremely scarce. Whatever the mechanism, low parasitism rates (1.2Ð 1.9%) of the H. cubana population in this study are similar to those observed in Hawaii (Uchida et al. 1992), and appear insufÞcient to suppress psyllid populations. The effectiveness of the other widely released biological control agent, the coccinellid C. coeruleus, was not be assessed in our studies because it had not yet established in north Thailand. In our data, native coccinellid and spider populations increased with H. cubana populations, but their densities were never realistically high enough to control H. cubana. Epizootics of entomopathogenic fungi may cause signiÞcant reductions in H. cubana populations (91% mortality in our measurements), but in our 2-yr study only 1 epizootic was observed. The effects of certain fungal species such as Entomopthora spp. are not easily detected (Villacarlos and Wilding 1994), and their importance may therefore be underestimated. Although individually none of the above agents appears capable of regulating H. cubana populations, it is quite possible that their total effect may delay the onset of outbreaks and reduce their magnitude. Such a scenario would help explain NapompethÕs (1989) observations that since the arrival of H. cubana in Thailand in 1986, the duration and severity of infestations have decreased steadily. Management Implications. There is little doubt that L. leucocephala ÔK8Õ is poorly suited for planting in seasonally dry, tropical highland environments similar to our test site. This conclusion is nothing new (NFTA 1985), but has heretofore been attributed to leucaenaÕs poor tolerance of acid soils (Brewbaker 1987). We propose that increased psyllid herbivory contributes signiÞcantly to the treeÕs poor performance at higher elevations. Proposals to breed acid soil-tolerant leucaena varieties (Blamey and Hutton 1994) should therefore be carefully weighed, especially considering the availability of other species better adapted to highland environments (e.g., Calliandra spp.; see Palmer et al. 1994). For lowland environments with maximum temperatures above 368C for extended periods, the prospects for L. leucocephala remain promising despite losses to the psyllid. Downloaded from https://academic.oup.com/ee/article/29/1/76/385909 by guest on 17 June 2022 an ecophysiological mismatch between L. leucocephala and H. cubana. H. cubana attacks several other species of Leucaena, some of which have more northerly distributions than L. leucocephala. Recent studies of chloroplast DNA in the genus Leucaena suggest that L. leucocephala itself is probably not a distinct species, but instead an amphidiploid that arose under human cultivation, with L. pulverulenta (Schlect.) Bentham as maternal parent (Harris et al. 1994). Thus, it is unlikely that H. cubana evolved on L. leucocephala. L. pulverulenta has a more northerly range, and Þeld trials have shown that it is highly susceptible to H. cubana attack (Sorensson 1989). Hence it is possible that H. cubana evolved on a cool temperature Leucaena species, which could cause a predilection for cooler environments in modern biotypes of H. cubana. Molecular studies comparing H. cubana from different habitats in Central America might shed some light on its evolutionary origins. More importantly, detailed studies on the relative physiological ecology of L. leucocephala and H. cubana could identify environments of high potential for psyllid damage, where planting the tree would be ill advised. Applying these climatic criteria to the psyllidÕs native range might also narrow the search for effective natural enemies. Tree Dynamics. Our Þndings support previous observations that L. leucocephala performs poorly at high altitudes (deÞned by NFTA [1985] as areas above 500 m at latitudes .108, and above 1,000 m at latitudes ,108). The most likely explanations are temperature (discussed above) and soil. Other studies have shown that acid soils severely limit root growth in leucaena (Blamey and Hutton 1994), which in turn limits nutrient uptake and biomass production. Although every effort was made to correct soil deÞciencies at both sites, the highland soils (red inactive tropical clays) retained a lower cation exchange capacity and lower pH than the lowland humic clay soils (especially in deeper soil layers). Soil factors probably contributed to lowering the mean biomass production of highland trees by 25.8%. Flowering in L. leucocephala had a weak seasonal component, with some synchrony within branches, and it is reasonable to consider seed production as either continuous or weakly bimodal (Bhaskar and Rao 1985). The reduction of vegetative growth during periods of high seed production adversely affected psyllid populations as shown by our correlative studies. The dynamic effects of tree reproductive cycles on psyllid populations are better explored using physiologically based models (e.g., Gutierrez et al. 1984). Psyllid Dynamics and Biological Control. Psyllid populations in the highlands exhibited boom-and-bust cycles that constitute a negative feedback loop (Fig. 8). Psyllid populations boomed in the presence of young leucaena leaves, then crashed as they outpaced vegetative growth, causing massive defoliation and exhausting oviposition sites. At the valley site, tree growth was more vigorous, and psyllid populations were limited most severely by high temperatures. As a result, highland populations ßuctuate widely, with a higher characteristic frequency (sensu Allen and Starr Vol. 29, no. 1 February 2000 GEIGER AND GUTIERREZ: ECOLOGY OF H. cubana Acknowledgments Special thanks are due to Banpot Napompeth and Channarong Doungsa-ard at the National Biological Control Research Center in Thailand, the Soil Fertility and Conservation Project at Mae Jo University, and Lina Villacarlos. This project was supported with funding by the Fulbright Foundation, the National Science Foundation, the ARCS Foundation, and the Robert Usinger Memorial Fund. References Cited lems and Management, Bogor, Indonesia. Winrock International, Bangkok, Thailand. Geiger, C. A. 1995. An ecological analysis of the leucaena psyllid, Heteropsylla cubana Crawford (Homoptera: Psyllidae), the major pest of Leucaena leucocephala (Lam.) de Wit (Leguminosae: Mimosoideae) in north Thailand. 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