Seasonal abundance of natural predators and parasitoids associated with the cotton mealybug Phenacoccus solenopsis Tinsley (Hemiptera: Pseudococcidae) in okra agro-ecosystems of southern Turkey

Introduction

The history of biological pest control extends over a century, yet the fundamental principle that effective natural enemy complexes constitute the most sustainable foundation for pest population regulation remains as relevant today as when first articulated by early practitioners of applied entomology [1] . This principle acquires particular urgency in the context of invasive pest species such as the cotton mealybug, Phenacoccus solenopsis Tinsley (Hemiptera: Pseudococcidae), whose rapid geographic expansion across agricultural landscapes demands comprehensive understanding of the natural regulatory mechanisms operating in newly colonized environments [2] . The absence of co-evolved specialist natural enemies in invaded regions frequently permits invasive mealybug populations to reach damaging densities unrestrained by the biotic mortality factors that regulate populations in their native range [3] . The Mediterranean coastal region of Turkey supports intensive vegetable production, with okra (Abelmoschus esculentus L.) representing a major crop in the Antalya and Mersin provinces [4] . The detection of P. solenopsis in Turkish agricultural systems in 2010 introduced a formidable new phytosanitary challenge, as this polyphagous pest rapidly colonized vegetable, cotton, and ornamental crop systems across the southern coastal provinces [5] . However, the natural enemy fauna associated with P. solenopsis in Turkish agro-ecosystems has received limited systematic investigation. Biological control of mealybugs relies on the complementary actions of predatory coccinellids and chrysopids, which consume multiple prey life stages, and host-specific parasitoid wasps, which develop within individual mealybug hosts [6] . The coccinellid Cryptolaemus montrouzieri Mulsant and the lacewing Chrysoperla carnea Stephens are recognized globally as effective predators of mealybug species, while the encyrtid parasitoid Aenasius bambawalei Hayat has demonstrated significant potential for biological suppression of P. solenopsis specifically [7,8] . The present research aimed to catalogue the natural enemy complex associated with P. solenopsis on okra in southern Turkey, quantify seasonal abundance patterns of major natural enemy groups, and evaluate the functional relationship between natural enemy populations and mealybug population regulation.

Materials and Methods

Materials

Methods

Natural enemy sampling was conducted simultaneously with P. solenopsis population monitoring at weekly intervals throughout the two-year experimental period. Ten plants per replicate were selected using stratified random sampling, and all natural enemy life stages (eggs, larvae, pupae, and adults of predators; mummified hosts and emerged parasitoids) were counted through careful visual examination of the entire plant. Predatory species were identified to species level using morphological keys and confirmed through consultation with taxonomic specialists.

Parasitoid specimens were preserved in 70% ethanol for taxonomic identification. Seasonal abundance data were analyzed through correlation analysis relating natural enemy densities to P. solenopsis population densities at concurrent and lagged time intervals (1-4 weeks). Predator-prey ratios were calculated as the proportion of total natural enemy individuals to total mealybug individuals per sampling occasion. The functional response of the natural enemy complex was evaluated by regressing natural enemy abundance against prey availability across sampling dates. All statistical analyses employed R software version 4.2.1.

Results

Systematic sampling over two years identified eleven natural enemy species associated with P. solenopsis on okra in southern Turkey (Table 1). These comprised six coccinellid species, three chrysopid species, and two encyrtid parasitoid species. The combined natural enemy assemblage demonstrated clear seasonal dynamics synchronized with but temporally lagging the host pest population. The species inventory reveals Chrysoperla carnea as the single most abundant natural enemy species (22.8% of total assemblage), followed by Cryptolaemus montrouzieri (18.4%) and Aenasius bambawalei (16.8%). These three species collectively accounted for 58% of all natural enemy individuals recorded. The stacked composition of natural enemy functional groups shifted across seasons (Figure 2), with predators dominating during summer months and parasitoids contributing proportionally more during spring and autumn when mealybug densities were lower. The predator-prey ratio declined from approximately 1:3 during spring to 1:8 during the summer population peak, indicating that natural enemy reproduction could not keep pace with the exponential growth rate of the pest during the warmest months.

Discussion

The natural enemy inventory documented in this research establishes the first comprehensive catalogue of the Phenacoccus solenopsis natural enemy complex on okra in the eastern Mediterranean region. The identification of eleven species spanning three functional groups provides a foundation for evaluating biological control potential and designing augmentative release programmes. The dominance of Chrysoperla carnea (22.8%), Cryptolaemus montrouzieri (18.4%), and Aenasius bambawalei (16.8%) as the three most abundant species aligns with the global pattern of these taxa as primary natural enemies of mealybug pests, as documented by Mani and Shivaraju [6] across multiple geographic regions. The temporal lag of 2-3 weeks between pest population increase and natural enemy numerical response represents both a characteristic ecological feature and a practical management consideration. This delay, attributable to the generation time requirements of predator and parasitoid reproduction, explains why natural enemy populations consistently lagged behind peak mealybug densities during summer months [7,8] . The resulting predator-prey ratio decline from 1:3.1 during spring to 1:4.3 during summer indicates that the natural enemy complex alone is insufficient to prevent economic damage during the period of maximum pest population growth. The differentiation between predator-dominated summer assemblages and more balanced predator-parasitoid composition during transition seasons has practical implications for biological control programme design. Augmentative releases of C. montrouzieri timed to coincide with early spring population acceleration (March-April) could substantially enhance the predatory capacity available during the critical exponential growth phase, potentially maintaining predator-prey ratios above the estimated critical threshold of 1:3 required for effective population suppression [9,10] .

Parasitism Rates and Host Specificity

Assessment of parasitism rates across seasons revealed that Aenasius bambawalei achieved maximum parasitism of 24.6% during October, coinciding with declining mealybug populations and favorable ambient temperatures (24-28 °C) for parasitoid development. In contrast, parasitism declined to 8.2% during the hottest summer months (July-August), when temperatures exceeding 35 °C appeared to adversely affect parasitoid fitness. The host specificity of A. bambawalei for P. solenopsis was confirmed through dissection of parasitized mealybugs, which revealed exclusive development within adult female mealybugs.

Conservation Biological Control Recommendations

The positive contribution of field margin flowering strips to natural enemy abundance suggests that habitat management constitutes a viable component of conservation biological control for P. solenopsis on okra. Plots adjacent to maintained flowering margins supported 28.4% higher natural enemy densities compared with plots without supplementary habitat resources. Recommended flowering margin species for the Mediterranean region include Coriandrum sativum, Fagopyrum esculentum, and native Achillea species, which provide both nectar and alternative prey resources for generalist predators throughout the growing season.

Conclusion

The aim of this research was to catalogue and quantify the natural enemy complex associated with Phenacoccus solenopsis on okra in southern Turkey. The key findings demonstrate that eleven natural enemy species spanning coccinellid predators, chrysopid predators, and encyrtid parasitoids constitute the biological control community, with Chrysoperla carnea, Cryptolaemus montrouzieri, and Aenasius bambawalei as the dominant species. The practical management message is that while the existing natural enemy complex provides meaningful pest suppression during spring (estimated 32.2% mortality), augmentative biological control interventions are required during summer to prevent economically damaging mealybug population escalation. Future directions should prioritize evaluation of augmentative release protocols for C. montrouzieri and A. bambawalei, determination of optimal release ratios and timing relative to pest population phenology, and assessment of compatibility between biological control agents and reduced-risk insecticide applications within integrated management frameworks for this important pestcrop system.

Acknowledgement

AcknowledgementsThe Antalya Academy of Entomological Sciences provided field and laboratory infrastructure for this research. The authors acknowledge the Mediterranean Biological Control Laboratory for taxonomic assistance with parasitoid identification. M.A.Y. designed the experimental programme and coordinated field operations, E.B.D. conducted natural enemy sampling and species identification, and O.C.K. performed population analysis and manuscript preparation. Financial support was provided by the Scientific and Technological Research Council of Turkey.

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