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Tamarixia radiata has been released widely in southern California for biocontrol of Asian citrus psyllid. Survey data reported here suggest that this ACP natural enemy may have established in about 91 of 100 (i.e., 91 percent of study sites) surveyed release and non-release sites in urban areas. (Photo courtesy of Mike Lewis, Center for Invasive Species Research, UCR)
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Tamarixia radiata has been released widely in southern California for biocontrol of Asian citrus psyllid. A major research question that has arisen from the Tamarixia release program is “Where’s Tamarixia?” Because there have been very high levels of investment into foreign exploration, safety testing, mass production and release efforts, determini...
Citations
... The rationale for attempting to establish D. aligarhensis in California was to complement parasitism by Tamarixia radiata (Waterston) (Hymenoptera: Eulophidae) (sourced from Punjab Pakistan and established in California for D. citri biological in 2012; Hoddle et al. 2016), as the two natural enemies successfully coexist in citrus orchards in the native range of D. citri (i.e., Punjab, Pakistan), and both contribute to D. citri control ). It has been speculated that temperature tolerances for D. aligarhensis and T. radiata may be different, and if so, heterogeneous climates across major citrus production areas may favor establishment of D. aligarhensis in parts of southern California that could be unfavorable for T. radiata (or vice versa) (Milosavljević et al. 2017b). ...
... See top of the fitted lines for associated regression equations R 2 estimates. (Hoddle et al. 2016). Previous research on temperature-driven development of D. citri and associated natural enemy species has been conducted under constant temperature regimens only (Chien et al. 1993, Liu and Tsai 2000, Skelley and Hoy 2004, Gómez-Torres et al. 2012, Li et al. 2018). ...
The effects of fluctuating and constant temperatures on the development and longevity of Diaphorencyrtus aligarhensis (Shafee, Alam, and Argarwal) (Hymenoptera: Encyrtidae), a parasitoid sourced from Pakistan and released in California for the classical biological control of Diaphorina citri Kuwayama (Hemiptera: Liviidae), were examined. The influence of six fluctuating temperatures that averaged 15, 20, 25, 30, 32, and 35°C, over 24 h on the development times and longevity of male and female D. aligarhensis were quantified and compared to six constant temperatures set at the same average temperatures. The development rates of immature stages of D. aligarhensis as a function of temperature were modeled using one linear and four nonlinear models. Fluctuating temperatures had significant effects on parasitoid development times and longevity which differed across experimental temperatures. Degree-days required for completion of cumulative development of D. aligarhensis were significantly different being 21% lower under fluctuating temperature regimens when compared with constant temperatures. The lower temperature threshold estimates above which development occurred were estimated to be lower under constant than fluctuating temperatures. The estimated values of upper and optimum temperature limits were similar for individuals reared under constant and fluctuating temperatures. Diaphorencyrtus aligarhensis lived longer at constant intermediate temperatures and for shorter times at constant lower temperature extremes when compared with their fluctuating temperature counterparts. Daily thermal fluctuations significantly influenced life history parameters of D. aligarhensis and should be considered when assessing likelihoods of establishment and impacts of this parasitoid on D. citri across diverse citrus-growing climates.
... Considerable program success has been achieved with T. radiata over the last five years including the mass production and release of approximately six million parasitoids throughout the infested areas of eight counties in southern California (Imperial, San Diego, Orange, Riverside, San Bernardino, Los Angeles, Ventura and Santa Barbara) ( Table 1). Evidence of widespread establishment at more than 90 percent of release sites in southern California, including recoveries in areas distant from release sites indicating extensive natural dispersal (Hoddle et al. 2016), and parasitism by Tamarixia as high as 63 percent have been observed in some areas at certain times of the year (Kistner et al. 2016a). Post-release monitoring in southern California indicates that average year-round parasitism by T. radiata is moderate at about 21 percent, varying greatly across locations ...
The Asian citrus psyllid (ACP) –‘Candidatus Liberibacter asiaticus’ (CLas) complex associated with
huanglongbing (HLB) has become an increasingly prevalent and serious threat to California citrus producers.
ACP-CLas threatens both backyard, and more importantly, commercial citrus groves. Decisive actions
were made in 2011 and 2014 with the release of two Pakistani biocontrol agents, Tamarixia radiata and
Diaphorencyrtus aligarhensis to combat ACP, and by extension, the spread of CLas in southern California. One
priority for California’s citrus industry has been to slow the spread of CLas by establishing these two natural
enemies across infested regions to suppress ACP populations in areas where management with insecticides
is either minimal or not feasible, such as urban environments or organic citrus groves. It is anticipated that
biological control of ACP in California will complement other management efforts targeting ACP-CLas because
lower density ACP populations will reduce the rate of spread of CLas.
... However, a subsequent study in Florida by found parasitism rates by T. radiata reach 20-56%, depending on time of year and location. In southern California, T. radiata sourced from Punjab (Pakistan) has been widely established in backyard citrus Hoddle et al., 2016) and life table analyses indicate that marginal rates of parasitism of D. citri by T. radiata average 21% in fall (November-September) . ...
... During previous field releases of T. radiata, we observed L. humile capturing foraging parasitoids and returning this prey to nests. Consequently, although L. humile has not impeded the establishment of T. radiata in urban citrus in Southern California Hoddle et al., 2016), the presence of this ant might have retarded rates of establishment and spread. After the 1st year of releases, T. radiata had been recovered in the majority of release sites and it had spread unassisted up to 13 km from the nearest release areas Hoddle et al., 2016). ...
... Consequently, although L. humile has not impeded the establishment of T. radiata in urban citrus in Southern California Hoddle et al., 2016), the presence of this ant might have retarded rates of establishment and spread. After the 1st year of releases, T. radiata had been recovered in the majority of release sites and it had spread unassisted up to 13 km from the nearest release areas Hoddle et al., 2016). These results indicate that T. radiata has been able to find and parasitize D. citri patches, possibly exploiting those that were unattended by L. humile. ...
The Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Liviidae), is a significant citrus pest and the parasitoid Tamarixia radiata (Waterston) (Hymenoptera: Eulophidae) has been released in various citrus-producing areas in classical biological control programs targeting D. citri. We investigated the effect of host deprivation on the foraging behavior and patch utilization by T. radiata. In the laboratory, females deprived of hosts for 3 days tended to leave patches of 12 nymphs without parasitizing hosts during the ca. 30 min they spent in the patch before leaving. Moreover, half of these females failed to host feed, and those that did host feed, on average, needed more than 15 min to complete feeding. Conversely, non-host-deprived females parasitized on average three nymphs before leaving patches without host feeding during the ca. 39 min they spent in the patch. These laboratory observations were compared to mass-reared female T. radiata that were released onto colonies of D. citri nymphs infesting citrus in the field. Release vials were provisioned with honey and these females had no opportunities to host feed over the 1- to 2-day containment period prior to release. When introduced onto D. citri colonies, 68% T. radiata females abandoned D. citri patches prior to probing hosts, in part, because Argentine ants, Linepithema humile (Mayr) (Hymenoptera: Formicidae), tending colonies disturbed searching parasitoids. These results from laboratory and field studies are discussed in the context of classical biological control, with the aim of understanding how to manipulate host availability and ant activity so establishment rates and impact of T. radiata can be improved.
Diaphorencyrtus aligarhensis (Hymenoptera: Encyrtidae) was first released in California for biological control of Diaphorina citri (Hemiptera: Liviidae) in December 2014. The establishment and parasitism rates of D. aligarhensis, along with those of another introduced species, Tamarixia radiata (Hymenoptera: Eulophidae), first released in 2011, were assessed at 15 D. aligarhensis release and 24 no-release control sites over the period 2016–2018. Study sites with citrus trees that were infested with D. citri eggs, nymphs, and adults, were located in residential areas in southern California that spanned three different climatic zones: coastal, intermediate, and desert interior sites. Parasitism rates of D. aligarhensis were low, averaging 0.62% compared to 21.2% for T. radiata which had spread naturally and established widely through the study area approximately one year earlier. Recoveries of D. aligarhensis at release sites were made eight times in 2016 and 2017. Conversely, T. radiata was recovered consistently at 34 of the 39 sites surveyed. Analyses indicated that parasitism of D. citri nymphs by T. radiata exhibited delayed density-dependence with a 12-month lag associated with reductions of D. citri densities by 50%. Irrespective of the climatic zone, the highest frequency of parasitized D. citri nymphs for T. radiata was recorded during peak periods of citrus flush growth from March through June and October through November each year. The findings reported here suggest that it is unlikely D. aligarhensis has established in California and that competition from T. radiata may, in part, have contributed to establishment failure. Consequently, biological control efforts targeting D. citri in California should focus on T. radiata.
The effects of climate, and ants on population regulation of an invasive citrus pest, Diaphorina citri (Hemiptera: Liviidae), by its parasitoid Tamarixia radiata (Hymenoptera: Eulophidae), in southern California were examined over a four-year period. Densities of D. citri eggs, nymphs, and adults, and Argentine ant, Linepithema humile (Hymenoptera: Formicidae), a mutualist which defends psyllid nymphs from natural enemies, citrus flush growth patterns, and parasitism rates of T. radiata, were monitored every four weeks on grapefruit, lemon, lime, orange, and tangerine trees at 28 urban sites across three climate types (coastal, intermediate, and desert). Significant spatial and temporal effects on D. citri abundance and parasitism rates were observed over this four-year period. Highest D. citri densities and parasitism rates were found in the intermediate and coastal regions during peaks of flushing cycles of citrus plants over March-June and September-November each year. Over the course of this study, population densities of D. citri declined by over 75%. Parasitism by T. radiata was identified as a significant mortality factor often exceeding 60% during periods of peak parasitoid activity. Analyses indicated that parasitism resulted in delayed density-dependent mortality and subsequent reductions in D. citri densities lagged by ∼1yr. Trends in D. citri densities and parasitism rates over time were similar on grapefruit, lemons, limes, oranges, and tangerines. Presence of L. humile in citrus resulted in a 3-fold increase in D. citri densities and control of this pest ant is needed to maximize biological control of D. citri.
This study examined the effects of seven constant and fluctuating temperature profiles with corresponding averages of 12 to 38°C on the life history of the Punjab, Pakistan-sourced Tamarixia radiata (Waterston) released in California for biological control of Diaphorina citri Kuwayama. One linear and seven nonlinear regression functions were fit to egg-to-adult development rate data to characterize thermal performance curves. Temperature fluctuations significantly affected both development and longevity of T. radiata. Estimates of degree-days predicted by the linear model were 30% higher for the fluctuating regime than the constant regime. Nonlinear model estimations of theoretical minimum and maximum developmental thresholds were lower for the fluctuating regime when compared to the constant regime. These predictions align with experimental observations. Parasitoids reared under fluctuating profiles at low average temperatures developed faster (15°C) and survived longer (15-20°C) when compared to those reared under constant regimes with corresponding means. In contrast, high average fluctuating temperatures produced parasitoids with an extended developmental period (35°C) and reduced longevity (30-35°C). A meta-analysis of published T. radiata development datasets, together with the results of this study, indicated convergence in degree-days and theoretical minimum developmental thresholds among geographically distinct parasitoid populations. These findings demonstrate the significant effects of temperature on T. radiata life history and have important implications for optimization of mass-rearing and release efforts, improvement of predictions from climate modeling, and comparison of T. radiata population performance across climatic gradients and geographic regions.
Assessing the oviposition preference and offspring performance of 2 parasitoid species being used to establish classical biological control of Diaphorina citri Kuwayama (Hemiptera: Liviidae) infesting citrus may provide important insight into their potential coexistence in California, USA. Tamarixia radiata (Waterston) (Hymenoptera: Eulophidae), an ectoparasitoid, preferred fourth and fifth instar D. citri nymphs for oviposition in both choice and no-choice experiments. Larval development and adult longevity of T. radiata offspring were positively correlated to female oviposition preference. Oviposition preferences of T. radiata were unaffected by conspecific and heterospecific competitors. Diaphorencyrtus aligarhensis (Shafee, Alam & Agarwal) (Hymenoptera: Encyrtidae), an endoparasitoid, preferred third and fourth instar hosts in choice experiments and fourth instar hosts in nochoice experiments. Parasitoid larvae that developed in these instars performed better than larvae that developed in second and fifth instars. The oviposition preferences of D. aligarhensis were unaffected by competitors in choice arenas, but were affected in no-choice experiments. Populations of T. radiata and D. aligarhensis from Pakistan, where they exist in sympatry and used in the experiments reported here, demonstrated a shared preference for fourth instar D. citri nymphs, which has not been documented previously for populations of D. aligarhensis from other geographic regions. This shared preference did not affect D. citri mortality rates, but it may affect the ability of D. aligarhensis to establish in areas of California where T. radiata is currently present.
In California, Asian citrus psyllid vectors the bacterium Candidatus Liberibacter asiaticus, which causes the lethal citrus disease huanglongbing. The top priority for California's citrus industry has been to diminish the rate of bacterium spread by reducing Asian citrus psyllid populations in urban areas, where this pest primarily resides. Attempts at eradicating and containing the psyllid with insecticides were unsuccessful. An alternative approach has been a classical biological control program using two parasitoids from Pakistan, Tamarixia radiata and Diaphorencyrtus aligarhensis, which attack the psyllid nymphs. T. radiata has established widely and, in combination with generalist predators, natural enemies are providing substantial control of psyllids in urban areas.
Two parasitoids attacking nymphs of Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Liviidae), Tamarixia radiata (Waterston) (Hymenoptera: Eulophidae) and Diaphorencyrtus aligarhensis (Shafee, Alam & Agarwal) (Hymenoptera: Encyrtidae) are being released in California, USA in a classical biological control program. To evaluate the effect of multiple parasitoid species on D. citri mortality, we conducted mesocosm experiments under controlled conditions using a complete block design with six treatments (D. citri nymphs exposed to: no parasitoids; D. aligarhensis or T. radiata alone; D. aligarhensis or T. radiata released first [by 48 h]; and both species released simultaneously). Parasitism of D. citri nymphs by T. radiata exceeded 60% and was unchanged when D. aligarhensis were present. Parasitism by D. aligarhensis was greatest when T. radiata was absent (∼28%) and was reduced in all treatments with T. radiata present (< 3%). D. citri mortality and parasitoid-related mortality of D. citri was consistent across parasitoid treatments. Laboratory results suggest that competition between D. aligarhensis and T. radiata is asymmetric and favors T. radiata. It may be difficult for D. aligarhensis to contribute significantly to D. citri biological control where T. radiata is present. However, results reported here suggest that competition between T. radiata and D. aligarhensis is not likely to reduce parasitism by T. radiata or reduce parasitoid-induced mortality of D. citri. This article is protected by copyright. All rights reserved.
