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23 September 2021 Population Fluctuations of Diaphorina citri and Its Natural Enemies in Response to Various Management Practices in Florida
Binita Shrestha, Xavier Martini, Lukasz L. Stelinski
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Abstract

The Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Liviidae), is a serious threat to citrus production because it transmits the bacterium, Candidatus Liberibacter asiaticus Jagoueix (Hyphomicrobiales: Rhizobiaceae), that causes huanglongbing. Currently, there is no cure for huanglongbing, and vector management is implemented to reduce the spread of pathogen. In Florida, calendar-based insecticide application had been used widely for D. citri management, but the evolution of insecticide resistance in D. citri and associated reductions of natural enemy populations mandate more sustainable approaches. The objective of our study was to compare the effects of organic management versus intermittent use of conventional insecticides on population suppression of D. citri by natural enemies in Florida. We conducted a survey of natural enemies in citrus groves that were managed organically versus intermittently treated with conventional insecticides from Mar to Dec 2019. We also compared mortality of D. citri in those groves by deploying sentinel psyllids on leaf flush with or without exclusion cages. The abundance of natural enemies was recorded by visual observations made on tree branches for 2 min intervals. Finally, we estimated tree flush density and monitored adult D. citri populations. Survival of sentinel D. citri was significantly lower on uncaged flush when natural enemies had access to eggs and nymphs during spring, summer, and fall in organic groves; however, such a difference was not observed between caged and uncaged D. citri in intermittently sprayed groves, particularly during summer and fall. Similarly, organic sites had lower numbers of adult D. citri compared to intermittently sprayed sites throughout most of the sampling period, suggesting that natural enemies contributed to regulation of D. citri populations in organic groves more so than in the intermittently treated conventional groves. The most common natural enemies found were Coccinellidae, Chrysopidae, Formicidae, Eulophidae, Syrphidae, Dolichopodidae, and Arachnida. Among these groups, formicids were most abundant in organic groves, whereas dolichopodids and coccinellids were most abundant in intermittently managed groves. Our results suggest that intermittent spraying for D. citri with conventional insecticides could affect activity of natural enemies even though such practices did not entirely eliminate their populations.

The Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Liviidae), is a major economic pest of citrus worldwide (Tiwari et al. 2011; Martini et al. 2014; Monzo & Stansly 2017) and vector of the pathogen, Candidatus Liberibacter asiaticus Jagoueix (Hyphomicrobiales: Rhizobiaceae) (CLas), that causes huanglongbing. The disease affects all commercial citrus varieties accounting for $1 billion in annual losses in Florida, USA, and thousands of lost jobs (Qureshi et al. 2009; Alvarez et al. 2016; Tomaseto et al. 2019; Li et al. 2020). In the US, huanglongbing has reduced production of processed and fresh citrus by approximately 21 and 72%, respectively, from 2007 to 2008 and from 2017 to 2018 (Dala-Paula et al. 2019).

Huanglongbing initially was discovered in South Florida in Aug 2005, and today over 90% of grove acres and over 80% of trees are infected (Zhang et al. 2014; Alvarez et al. 2016). The vector, D. citri, was identified in Florida in 1998 (Zhang et al. 2014; Alvarez et al. 2016). Recommended management practices for huanglongbing include use of disease free stock, inoculum removal by destruction of infected trees, and suppression of D. citri populations with insecticides (Brlansky et al. 2009; Alvarez et al. 2016; Pelz-Stelinski et al. 2017). To date, there is no cure for the disease. Other tactics, including shoot tip grafting, thermotherapy, and antibiotics, have shown modest feasibility as possible huanglongbing therapies under greenhouse conditions, but have not been effective under field conditions (Zhang et al. 2014).

Given the effectiveness of primary and secondary pathogen spread by D. citri, vector control remains a critical component of disease management. Although various vector control strategies have been explored in citrus groves, including cultural, chemical, and biological control, insecticide use has been the most prevalent method employed by growers given the rapid and visible effects on pest mortality (Qureshi & Stansly 2007; Boina & Bloomquist 2015). Although management practices for D. citri vary among Florida citrus growers (Pelz-Stelinski et al. 2017), use of foliar and systemic insecticides is the most common tactic for reducing D. citri populations (Qureshi & Stansly 2009; Boina & Bloomquist 2015). Until recently, growers following standard commercial management practices have made between 8 and 12 insecticide applications per yr, including neonicotinoids, organophosphates, and pyrethroids (Grafton-Cardwell et al. 2013).

Despite the lack of effective organic measures to manage the huanglongbing pathosystem, some growers have continued to produce certified organic citrus. Others have begun to implement low-input (2–4 annual sprays) of conventional insecticides, because the economic toll of huanglongbing has reduced profit (Hodges & Spreen 2012). Furthermore, consequences have emerged following frequent insecticide applications for D. citri management, including insecticide resistance and elimination of beneficial species (Tiwari et al. 2013; Niu et al. 2014; Boina & Bloomquist 2015; Chen et al. 2017).

Another component of D. citri management includes biological control of psyllid populations by natural enemies such as the introduced parasitoids, Tamarixia radiata (Waterston) (Hymenoptera: Eulophidae) and Diaphorencyrtus aligarhensis (Shafee, Alam & Agarwal) (Hymenoptera: Encyrtidae) (Michaud 2002; Qureshi & Stansly 2009). In Florida, T. radiata and D. aligarhensis were imported in classical biological control programs in 1999 and 2000, respectively, but only T. radiata became widely established (Alvarez et al. 2016). In addition to these parasitic wasps, D. citri also are attacked by several species of predators, including coccinellids, syrphid flies, chrysopids, dolichopodids, formicids, and spiders (Aranae) (Michaud 2004; Qureshi & Stansly 2009; Kistner et al. 2016a). Ants can be predators or are involved in mutualistic relationships with hemipterans such as aphids, scales, or psyllids (Calabuig et al. 2015; Amiri-Jami et al. 2017). Some studies have shown that ant exclusion promotes biological control of D. citri; for instance, ant exclusion increased the parasitism of D. citri by T. radiata because of food-for-protection relationships (Navarrete et al. 2013; Tena et al. 2013; Anastasio et al. 2021). Therefore, it is important to understand the nature of the relationship between certain ant species and D. citri (predator-prey versus mutualism), to design effective management practices in citrus agroecosystems.

In Florida, ladybeetles (Coccinellidae) and T. radiata are key natural enemies of D. citri (Michaud 2004; Qureshi & Stansly 2009). Diaphorina citri also is susceptible to fungal pathogens such as Isaria fumosorosea Wize (Hypocreales: Cordycipitaceae) and Beauveria bassiana (Bals.-Criv.) Vuill. (Hypocreales: Cordycipitaceae) (Avery et al. 2009). The effects of biological control on population suppression of D. citri generally have been assumed to be greater within organic than conventionally managed citrus given that these organisms are susceptible to conventional insecticide sprays targeting psyllids (Tiwari et al. 2011). Therefore, it is important to understand the contribution of biocontrol agents to population suppression of D. citri under various management practices.

The sustainability of citrus production in Florida, where huanglongbing is well established, depends on effective management of D. citri. We hypothesized that the impact of natural enemies on populations of D. citri would be lower in citrus groves managed with intermittent application of conventional insecticides than in organic groves with no insecticide sprays, as suggested by Pelz-Stelinski et al. (2017). The objective of this research was to compare the effects of intermittently applied conventional insecticides versus organic management practices on population suppression of D. citri by natural enemies under high huanglongbing incidence. The study was conducted in Florida citrus groves in 2019 by monitoring survival of sentinel D. citri nymphs using exclusion cages, and comparing psyllid and natural enemy abundance between the 2 management practices.

Materials and Methods

INSECT REARING

A laboratory population of D. citri was reared in a greenhouse at the University of Florida, Citrus Research and Education Center, Lake Alfred, Florida, USA. This strain has been reared since 2000 without exposure to pesticides or subsequent input of field-collected individuals for approximately 330 generations. The culture was maintained on ‘Valencia’ sweet orange (Citrus sinensis (L.) Osbeck (Rutaceae) in a greenhouse at 27 ± 1 °C, with 60 to 65% relative humidity (RH), and a 14:10 h (L:D) photoperiod. The citrus plants were purchased from a local nursery in Dundee, Florida, USA.

EXPERIMENT STUDY SITES

This study was conducted from Mar through Dec 2019 (spring, summer, and fall seasons) in Florida at 2 geographically separated regions: (1) Lake Wales, Polk County (27.9010°W, 81.5800°N), and (2) Clermont, Lake County (28.5490°W, 81.7700°N). The 2 treatments compared were: (1) organic management with no chemicals applied to control D. citri, and (2) intermittent management where 2 to 4 annual sprays of conventional insecticides (organophosphate, pyrethroid, or neonicotinoid) were applied targeting D. citri. There were 4 pairs of organic and intermittently managed groves (15–20 ha in size) monitored to measure the effect of natural enemies on populations of D. citri. One pair of groves was located in Clermont and the other 3 pairs were in Lake Wales. Pairs of organic and intermittently managed groves in each replicate were separated by less than 100 m and each replicate pair of groves was separated by 30 to 65 km. All 8 sites were comprised of 10 to 12-yr-old sweet orange ‘Valencia’ trees (about 2.5 m3 canopy volume) planted on 2.4 m in-row and 2.4 m between-row spacing. Trees were managed by 3 independent grower operations (2 organic and 1 conventional); therefore, all replicates in the conventional treatment belonged to the same grower and were managed similarly. In order to record temperature and humidity, 1 HOBO (Onset Computer Corporation, Bourne, Massachusetts, USA) was deployed in each site from Mar through Dec. Each HOBO device was placed within trees and replaced monthly to download data across the 8 sites.

EXCLUSION EXPERIMENT

Within each 15 to 20 ha replicate block, a smaller 0.4 ha area consisting of 16 trees was selected at random for deployment of sentinel D. citri. A single newly expanded leaf flush just after budbreak was selected on each of these trees and visibly marked with flagging tape tied to the branch. These marked flushes served as sites where cohorts of D. citri were deployed to act as sentinels for measuring impact of biological control on D. citri mortality. We evaluated the effect of biological control with the exclusion cage method as described by Qureshi and Stansly (2009). Cohorts of D. citri were deployed in the field either without exclusion or by enveloping 2 pairs of male and female D. citri adults on previously marked flush within a 1.5-L mesh bag (sleeve cage). Cages consisted of 20 × 30 cm fine mesh (0.45 mm2) bags that excluded small predators and parasitoids, and were placed over flush containing psyllid eggs or nymphs. Flush with sentinel D. citri and without cages were exposed to natural predation. In total, there were 4 open-air and 4 caged flush containing sentinel D. citri per replicate. Insects were allowed to mate and lay eggs on open-air or bagged flush for 4 d after deployment and then removed. Afterwards, the numbers of eggs per flush were counted using a 10× magnifying hand lens and recorded. The numbers of surviving psyllids were counted weekly for 3 wk after deployment until all psyllids either had died or emerged as adults. This process was repeated 9 times throughout the season and initiated on 5 Mar, 25 Apr, 28 May, 2 Jul, 31 Jul, 28 Aug, 1 Oct, 5 Nov, and 3 Dec.

ARTHROPOD ABUNDANCE

All beneficial arthropods that were known potential natural enemies of D. citri at these locations were monitored, and included Coccinellidae, Syrphidae, Eulophidae, Chrysopidae, Formicidae, Dolichopodidae, and Arachnida. Counts were made by visually inspecting each tree branch containing sentinel psyllids for 2 min per sampling period and counting all arthropods found during that period. Inspections were conducted weekly from Mar to Dec 2019. Arthropods were identified to species level where possible. Ants were collected with pointed round paint brushes and preserved in 70% ethanol. Identifications were made subsequently by Robin J. Stuart.

DIAPHORINA CITRI MONITORING

Twenty trees were selected at random in each plot in both organic and intermittently managed groves. Selected trees were marked with flagging tape. Adult D. citri were monitored on these trees by stem-tap samples, where tree branches were struck vigorously 3 consecutive times with a stick (Qureshi & Stansly 2007). The number of D. citri falling onto a 21.6 × 30 cm white board placed below the branch was counted. Samples were taken every 3 wk from May to Dec 2019.

FLUSH DENSITY

Sixteen trees were selected at random in each plot in both organic and intermittently managed groves and marked with flagging tape, as described above, to quantify flushing throughout the season. The presence of newly emerged flush was quantified by placing a PVC cube (15 × 15 × 15 cm) into a randomly selected area of the outer tree canopy and recording the total number of flush present within the frame of the cube. Flush was quantified once per mo from Aug to Dec 2019.

STATISTICAL ANALYSES

The data for exclusion experiments, flush density, and D. citri abundance were analyzed using generalized linear model (GLM) fit with negative binomial distributions. Pairwise comparisons were made with Tukey-estimated marginal means (emmeans) following GLM analyses. The arthropod abundance data were analyzed using non-parametric Mann Whitney U test. All analyses were performed in R software (version 4.0.0) at the α = 0.05 significance level (RStudio 2015).

Results

CLIMATIC DATA

The average temperature and relative humidity of all 8 experimental sites are given in Figure 1. The mean daily temperature averaged 17.6 to 27.4 °C at the 4 organic sites. Temperatures ranged between 18.2 to 27.5 °C at each site managed intermittently with conventional insecticides. Relative humidity was similar at all groves investigated, ranging between 60 to 91%.

EXCLUSION EXPERIMENT

There was a significant interaction effect of management practices and caging (caged or uncaged) on mortality of sentinel D. citri during summer (F = 5.66; df = 1, 572; P = 0.017) and fall (F = 8.414; df = 1, 572; P = 0.004), but not during spring (F = 0.79; df = 1, 572; P = 0.371) (Fig. 2). The mortality of uncaged D. citri was significantly higher than that of caged psyllids in organically managed groves during spring (P < 0.001), summer (P < 0.001), and fall (P = 0.025). However, there was no significant effect of caging on psyllid populations in intermittently managed groves during summer (P = 0.189) and fall (P = 0.309), and an effect of biological control was observed only during spring (P = 0.030) in plots intermittently treated with conventional insecticides (Fig. 2).

ARTHOPOD ABUNDANCE

The abundance of arthropods in groves treated with the 2 management practices are shown in Figure 3. The majority of arthropods belonged to the Coccinellidae, Chrysopidae, Formicidae, Eulophidae, Syrphidae, and Dolichopodidae. Spiders also were observed frequently in both groves. The most abundant arthropods foraging on Valencia trees were ants, averaging (± SE) 7.4 ± 0.68 and 5.36 ± 0.55 individuals per sampling interval in organic and intermittently managed groves, respectively. We found various species of ants including Crematogaster cerasi (Fitch), Pseudomyrmex gracilis (Fabricius), Camponotous floridanus (Buckley), Brachymyrmex obscurior (Forel), Dorymyrmex bureni (Trager), Tetramorium bicarinatum (Nylander), and Monomorium pharaonis (Linnaeus) (all Hymenoptera: Formicidae). There were significantly more ants in organic groves than those managed intermittently with conventional insecticides (P < 0.001). Another commonly encountered group of arthropods was spiders with an average of 3.90 ± 0.28 and 3.51 ± 0.22 individuals counted per sampling interval in organic and intermittently managed groves, respectively. However, there was no significant difference in the abundance of spiders between the 2 management practices (P = 0.820). Similarly, we observed a large number of predatory long-legged flies (Dolicopodidae) which were significantly more abundant in conventional than organic groves (P = 0.002). We recorded 1.90 ± 0.13 predatory flies per sample in intermittently sprayed groves, whereas 1.63 ± 0.15 were observed per sampling date in organic groves. Asian lady beetles, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), were the most common generalist predator found in both intermittently sprayed (0.56 ± 0.08 per sampling date) and organically managed (0.26 ± 0.05 per sampling date) groves. There were significantly more lady beetles in intermittently sprayed than organic groves (P < 0.001). Among the groups found, there were few lacewings, Tamarixia (Hymenoptera: Eulophidae), and syrphid flies observed in both types of groves and there were no significant differences among these groups.

Fig. 1.

Average temperature (°C) and relative humidity (%) recorded during surveys at 4 organic (A) and 4 intermittently sprayed (B) citrus grove sites in Florida from Apr to Dec 2019.

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FLUSH DENSITY

There was no significant effect of management practice on flush density per m3 of tree canopy (F = 0.012; df = 1, 310; P = 0.910), but there was a significant effect of sampling date (F = 31.89; df = 4, 310; P < 0.001), and the interaction between management type and sampling date was significant (F = 3.185; df = 4, 310; P = 0.013) (Fig. 4). The number of flush shoots counted per m3 was higher in organic than intermittently sprayed groves during Nov and Dec (Fig. 4).

DIAPHORINA CITRI MONITORING

The interaction between management practice and sampling date significantly affected the number of D. citri counted by tap sampling (F = 9.462; df = 7, 1904; P < 0.001). Significantly more adult D. citri were counted per tree stem tap sample in groves sprayed intermittently with conventional insecticides than in organically managed groves throughout the majority of the sampling period, except in Dec (Fig. 5). Diaphorina citri counts were consistently lower in organically managed than intermittently sprayed plots throughout the season, and lacked the population peaks typically associated with spring citrus flush growth that were observed in the intermittently sprayed groves (Fig. 5).

Discussion

Our field observations in Florida suggest that insecticide input has an indirect impact on population regulation of D. citri via effects on their natural enemies. As we hypothesized, fewer D. citri survived in our exclusion cage experiments when natural enemies had access to flush with eggs and nymphs; this was evident in organic groves during spring, summer, and fall (Fig. 1). Because there were no insecticides applied during the experimental period in the organic groves, we speculate that the greater psyllid mortality observed in uncaged versus caged treatments was due to mortality inflicted by natural enemies. This result also is consistent with previous investigations employing exclusion cages to measure the impact of biological control (Michaud 2004; Qureshi & Stansly 2009). However, psyllid mortality was not different between caged and uncaged sentinel psyllids in intermittently managed groves that received 2 to 4 annual sprays of neurotoxins, particularly during summer and fall. These results implicate the importance of natural enemies as a source of D. citri population regulation in organic groves, more so than under intermittent use of conventional insecticides.

There was less variation in the density of natural enemy populations in groves sprayed intermittently with conventional insecticides than those managed organically. During our visual observations, ants appeared to be the most frequently observed beneficial arthropods followed by spiders, long-legged predatory flies, and lady beetles in both types of groves. Ants can have mutualistic or antagonistic relationships with hemipterans such as aphids, scales, or psyllids (Amiri-Jami et al. 2017). Certain species of ants have a mutualistic relationship with D. citri and provide psyllids protection against natural enemies and in return receive benefit from the carbohydrate-rich honeydew secreted by them (Milosavljević et al. 2017). For example, the Argentine ant, Linepithema humile (Mayr) (Hymenoptera: Formicidae), provides D. citri with significant protection against predation through their mutualistic relationship (Milosavljević et al. 2017). Exclusion of Argentine ants from citrus increases parasitism of D. citri by Tamarixia by 90% compared to areas where ant populations are not manipulated (Milosavljević et al. 2018). Similarly, the presence of ants in aphid colonies reduces predation by syrphid flies (Amiri-Jami et al. 2017) and parasitism by many aphidiine wasps. There are several species of ants that tend and collect honeydew from D. citri nymphs, including Crematogaster ashmeadi Mayr (Hymenoptera: Formicidae), D. bureni, B. obscurior, and C. floridanus (Michaud 2004; Chong et al. 2010; Navarrete et al. 2013). Other species, including D. bureni, C. floridanus, and P. gracilis, have been observed carrying D. citri nymphs in the field (Michaud 2004; Peña et al. 2008; Monzo et al. 2014). The large numbers of ants found in organic groves during our observations may explain in part the observed composition of the natural enemy community; however, further investigations are necessary to understand the contributing role of each ant species in the interaction between psyllids and their natural enemies. The mutualistic relationship between ants and D. citri might affect the success of biological control given that ants can disrupt natural enemy activity directly. Thus, future categorization of ant species occurring in Florida citrus as mutualistic or predatory could benefit the design of management practices accordingly.

Fig. 2.

Mean numbers of surviving sentinel Diaphorina citri on caged and uncaged flush in organic and intermittently sprayed citrus groves in Florida during spring, summer, and fall. Bars indicated by different letters indicate significant differences (P < 0.05) among treatments.

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Another dominant group of natural enemies observed here were spiders. The most common spiders that have been documented to consume D. citri are ghost spiders, jumping spiders, and yellow sac spiders (Michaud 2004; Qureshi & Stansly 2009; Kistner et al. 2016b). We often observed these species in the current investigation. Although we did not observe spiders directly consuming D. citri, some psyllids were found ensnared within their webs. Dolichopodids, also known as predatory long-legged flies, feed on adult D. citri (Chong et al. 2010; Cicero et al. 2017) and were the third most frequently observed arthropods group in our study. More dolichopodids were found in intermittently sprayed than organic groves. Similarly, lady beetles are the important guild of predators that are known to contribute significantly to the mortality of D. citri (Michaud 2004; Pluke et al. 2005; Milosavljević et al. 2018) and we observed more lady beetles in intermittently sprayed than organic groves. Although coccinellid and dolichopodid abundance was higher in intermittently sprayed than organic groves, we did not observe a difference in survival of D. citri between caged and uncaged psyllids in groves treated with conventional insecticides, which suggests an effect of insecticide sprays on natural enemy activity. It is well known that the susceptibility of natural enemies to insecticides varies depending on their mode of exposure, such as through direct contact, uptake from residues on contaminated plant surfaces, and ingestion of prey or floral resources that were in contact with insecticides (El-Wakeil et al. 2013). Although insecticides cause direct mortality of natural enemies, they also have negative indirect effects on feeding and foraging behavior of natural enemies, and thus may have interfered with predation or prey consumption (Cloyd 2012). Such indirect effects could hinder population regulations of herbivores. Both direct and indirect effects of insecticides should be considered when measuring the impact on natural enemy activity, and disentangling these 2 complementary factors requires further investigation.

Fig. 3.

Mean number of arthropods observed per 2-min visual observation on trees in organic and intermittently sprayed citrus groves in Florida (Mar to Dec 2019). Significant differences (*) are defined at P < 0.05 level.

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Fig. 4.

Mean number of flushes sampled per tree in organic and intermittently sprayed citrus groves in Florida recorded over time. Significant differences (*) are defined at P < 0.05 level.

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Fig. 5.

Mean number of adult Diaphorina citri observed per tree in organic and intermittently sprayed citrus groves in Florida (May to Dec 2019). Significant differences (*) are defined at P < 0.05 level.

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Another key natural enemy of D. citri is T. radiata, which was imported into Florida as part of a classical biological control effort. In addition to parasitism by female T. radiata, adult wasps, particularly females, are known to kill a portion of psyllid nymphs by host feeding (Michaud 2004). The difficulties associated with T .radiata establishment in certain target regions in Florida are perhaps related to indirect competition caused by other predators, such as Coccinellidae and Dolichopodidae. For example, Michaud (2004) found that T. radiata suffer mortality (64–95%) due to predation of parasitized nymphs by lady beetles in central Florida. Also, dolichopodids compete for resources with T. radiata and eat them if encountered during normal host searching/feeding behavior (Cicero et al. 2017). In our study, T. radiata rarely were observed in groves under both management regimes. Other predators such as lacewings and syrphid flies also contribute to the mortality of D. citri (Michaud 2004; Qureshi & Stansly 2009) and are known to account for up to 86% mortality of immature D. citri as revealed by field studies conducted in California (Kistner et al. 2016b). Throughout the duration of our investigation, the abundance of lacewings and syrphid flies was not affected by management regime based on our survey data.

Interestingly, despite the lower abundance of natural enemies in organic groves, we found fewer D. citri in these areas compared to those areas managed with intermittent applications of conventional insecticides throughout the yr (Fig. 5). Populations of adult D. citri peaked during May, Jun, and Jul in conventional groves, while similar peaks were not observed in organic counterparts. Another factor explaining higher psyllid populations in intermittently sprayed than organic groves observed here might be that the level of insecticide input used was insufficient to adequately reduce D. citri populations as similarly observed in Pelz-Stelinski et al. (2017), yet sufficient to disrupt normal activity of natural enemies. More D. citri found in intermittently managed conventional groves also could indicate some level of insecticide resistance among populations of D. citri in these groves. Diaphorina citri in Florida exhibit resistance to various insecticides including imidacloprid, chlorpyriphos, thiamethoxam, malathion, and fenpropathrin (Tiwari et al. 2011; Chen & Stelinski 2017; Chen et al. 2018).

An additional factor that could have affected the D. citri population is the availability of flush. Feather flush is the only site where D. citri oviposit and nymphs develop (Pluke et al. 2008). Monthly inspections of flush density revealed that flush was available to D. citri at similar times and levels in both the organic and intermittently managed blocks. Therefore, we believe adult psyllids had roughly equivalent resources for egg laying and development in both types of groves investigated here. Although the amount of flush available to D. citri was higher in organic than conventional blocks during Nov and Dec, the opposite trend in D. citri population density was observed during this period. Similarly, studies have shown that abiotic environmental factors, such as temperature and humidity, can affect the flight activity and distribution of D. citri populations (Martini & Stelinski 2017; Martini et al. 2018; Wang et al. 2019). In the current investigation, we did not find significant differences in microclimate variables between organic and intermittently sprayed sites, thus we assume that weather conditions did not influence psyllid populations here.

Diaphorina citri nymphs are suitable prey for a wide range of generalist predators. Although our arthropod survey did not reveal a clear difference in abundance of key natural enemy groups between the 2 management practices, our exclusion cage experiments indicated an overall greater effect of natural enemies on mortality of D. citri in organic than intermittently managed groves. It is possible that cryptic or nocturnal predators could have contributed to the difference in predation observed between treatments as measured by the exclusion cage experiments. For example, adult lacewings are nocturnal, and larvae of lacewings and syrphid flies are cryptic as well as active mostly during dusk and dawn (Hagen et al. 1999; Canard et al. 2001; Keulder & Van den Berg 2013), which may have been overlooked during our visual observations. In future studies, the sampling of natural enemies could be improved by use of additional methods such as sticky traps or vacuums, in addition to visual observations in order to better estimate natural enemy diversity and abundance (Martini et al. 2015). Also, more detailed investigations elucidating the impact of ants and their interaction with generalist predators on biological control of D. citri could further improve management practices for this insect vector (Milosavljević et al. 2018).

The current study suggests that intermittent applications of insecticide sprays for management of D. citri could sufficiently disrupt activity of natural enemy populations to reduce their impact on population regulation of D. citri, even if populations of natural enemies are not eliminated entirely. In contrast, undisturbed populations of natural enemies in organically managed groves in Florida appeared to maintain populations of D. citri at levels lower than observed in nearby conventional groves treated with only 2 to 4 annual sprays. While our work confirms earlier findings from Pelz-Stelinski et al. (2017) regarding the risk of D. citri spread in citrus grove receiving intermittent insecticide sprays, further confirmation of our results among a greater sample size of organic groves in other regions is warranted. Reduction of D. citri populations can improve yield under conditions of near 100% huanglongbing infection, and a threshold has been established beyond which overspraying for D. citri reduces profit (Monzo & Stansly 2017). Recently, a physiological mechanism in citrus has been proposed that may explain why management of D. citri improves yield, even in areas where all trees express huanglongbing. Although inoculation frequency is not related to pathogen load in the phloem, prolonged feeding by D. citri stunts plant growth and decreases salicylic acid-dependent immune response in citrus (Ibanez et al. 2019). Thus, tree defenses against the CLas causal pathogen of huanglongbing appear compromised when populations of D. citri are not adequately managed. Although biological control is unlikely to impact D. citri populations sufficiently to curtail pathogen transmission, it could impact yield indirectly by contributing to population suppression of D. citri below a measurable action threshold when most or all trees are already infected as occurs in Florida.

Acknowledgments

We thank Kayla Kempton for assistance in the field and gratefully acknowledge Wendy Meyer, Angel Hoyte, Kara Clark, and Hunter Gos-sett for technical assistance. We thank Robin J. Stuart for identifying ants to species level.

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Binita Shrestha, Xavier Martini, and Lukasz L. Stelinski "Population Fluctuations of Diaphorina citri and Its Natural Enemies in Response to Various Management Practices in Florida," Florida Entomologist 104(3), 178-185, (23 September 2021). https://doi.org/10.1653/024.104.0306
Published: 23 September 2021
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