A preliminary study on the occurrence and significance of phytophagous arthropods and natural enemies on Sapindus saponaria saplings

Sapindus saponaria (Sapindaceae) is widely distributed throughout the Americas^[1], attaining heights of up to eight meters^[2]. In Brazil, it is ubiquitously present across all regions^[3]. Renowned for its ecological significance, this species is extensively employed for the reclamation of degraded ecosystems globally^[4−6]. Additionally, the fruits of S. saponaria find utility in Brazilian folk medicine, primarily for their saponin content, while its seeds and wood are utilized in the creation of jewelry and baskets, respectively^[2,7]. Despite the economic importance of this plant, the knowledge about its associated arthropods remains largely deficient. A recent discovery in China identified a novel species, Leptopulvinaria sapinda (Hemiptera: Coccidae), as an assailant of S. saponaria^[8]. However, comprehensive insights into the arthropod fauna associated with this plant are still lacking. Notably, insects and mites pose potential threats to S. saponaria saplings, and the mitigating influence of spiders on defoliation caused by beetles is recognized. The intricate interactions between the plant and its arthropod inhabitants warrant further investigation to elucidate the ecological dynamics and potential implications for the sustainability of S. saponaria populations.

The aim of this investigation was to assess the population dynamics of phytophagous insects, mites, and natural enemies associated with 48 S. saponaria saplings over a two-year period. The quantification and comparison of these arthropod species were conducted utilizing the Importance Index-Production Unknown (% I.I.-P.U.), a metric derived as a percentage from the Importance Index (I.I.)^[9,10]. This methodology enabled the classification and ranking of the arthropods based on their relative importance to the studied S. saponaria saplings, providing a quantitative basis for evaluating their ecological significance within the examined timeframe.

This research was undertaken at the 'Instituto de Ciências Agrárias da Universidade Federal de Minas Gerais (ICA/UFMG)', Brazil, spanning the period from April 2015 to March 2017. For comprehensive information regarding climate classification, latitude, longitude, altitude, and soil characteristics, please refer to the supplementary details provided in Alvares et al.^[11] & Silva et al.^[12].

Comprehensive information pertaining to seedling production, the substrate employed, field planting procedures, fertilization practices, irrigation protocols, and other relevant details can be found in Silva et al.^[12]. The quantification of defoliation percentage caused by insects, the assignment of damage scores resulting from sap-sucking insects and mites, and the evaluation of arthropod populations are elaborated upon in the study by Demolin-Leite^[10].

Each replication are the total individuals collected on 12 leaves (three heights and four sides of the sapling) for 24 months. The distribution type (aggregated, random, or regular) for the lost source (LS) or solution source (SS) was defined by the Chi-square test using the R-package 'IIProductionUnknown'^[13] (Supplemental Table S1 & S2). The data were subjected to simple regression analysis, and the parameters were all significant (p < 0.05) using the R-package 'IIProductionUnknown'^[13] (Supplemental Table S3). Simple equations were selected by observing the criteria: (1) data distribution in the figures (linear or quadratic response), (2) the parameters used in these regressions were the most significant (p < 0.05), (3) p < 0.05 and F of the Analysis of Variance of these regressions, and iv) the coefficient of determination of these equations (R²). Only L.S. and SS with p < 0.05 were shown in Supplemental Table S1−S3. The data above were used in the Percentage of Importance Index-Production Unknown (% I.I.-P.U.).

Percentage of Importance Index-Production Unknown (% I.I.-P.U.)^[10] is:

% I.I.-P.U. = [(ks₁ × c₁ × ds₁)/Σ(ks₁ × c₁ × ds₁) + (ks₂ × c₂ × ds₂) + (ks_n × c_n × ds_n)] × 100^[9],

where, i) the key source (ks) is: ks = damage (non-percentage) (Da.)/total n of the LS on the samples or ks = reduction of the total n. of LS (RLS)/total n. of the SS on the samples^[10]. Where Da. or RLS = R² × (1 − P), when it is of the first degree, or (R² × (1 − P)) × (β₂/β₁), when it is of the second degree, where R² = determination coefficient and P = significance of ANOVA, β₁ = regression coefficient, and β₂ = regression coefficient (variable²), of the simple regression equation of the loss source (LS) or solution source (SS)^[10].

When it is not possible to separate the Da. between two or more LS, there should be a division of the Da. among the LS as a proportion of their respective 'total n'. Da. = 0 when Da. was non-significant for damage or non-detected by LS in the system^[10]. When an SS operates in more than one LS, that caused damage, its ks are summed. RLS = 0 when Da. by LS or RLS was non-significant for damage by LS or reduced LS by SS in the system^[10].

ii) c (constancy) = Σ of occurrence of L.S. or S.S. on samples, where absence = 0 or presence = 1^[9].

iii) ds (distribution source) = 1 − P of the chi-square test of LS or SS on the samples^[9]. Counts (non-frequency) of L.S. or S.S. are used to perform the chi-square test.

These data, above, are obtained, by R-package 'IIProductionUnknown'^[13].

Percentage of RLS per SS (% RLSSS) = (R.L.S.S.S./total n of the LS – abundance or damage) × 100, where RLSSS = RLS × total n of the SS, with the R.L.S. not being summed in this case^[10]. These data, above, are obtained, by R-package 'IIProductionUnknown'^[13].

The phytophagous arthropods exhibiting the highest % I.I.-P.U. on the leaves of S. saponaria saplings encompassed Liriomyza sp. (mines) (Diptera: Agromyzidae) at 53.49%, Bemisia sp. (Hemiptera: Aleyrodidae) at 13.29% (with a maximum damage score of IV), Phaneropterinae (Orthoptera: Tettigoniidae) at 11.21%, Tetranychus sp. (Acari: Tetranychidae) at 8.95% (with a maximum damage score of III), Tropidacris collaris (Orthoptera: Romaleidae) at 4.61%, and Stereoma anchoralis (Coleoptera: Chrysomelidae) at 1.33% (Table 1).

The natural enemies with the highest % I.I.-P.U. on the leaves of S. saponaria saplings were identified as Cycloneda sanguinea (Coleoptera: Coccinellidae) at 98.94% and Pseudomyrmex termitarius (Hymenoptera: Formicidae) at 1.06%. Notably, the presence of P. termitarius (0.13%) and C. sanguinea (0.02%) led to a reduction in the numbers of Liriomyza sp. mines and Bemisia sp., respectively, on these saplings. Furthermore, the damage inflicted by Bemisia sp. on leaves exhibited a reduction per the number of P. termitarius (2.92%). Conversely, the number of Brachymyrmex sp. (Hymenoptera: Formicidae) resulted in an increase in the number (1.18%) and damage (61.95%) of Bemisia sp. on S. saponaria saplings. The cumulative balances for the reduction in abundance and damage (%) were negative, measuring at −1.03% and −59.03%, respectively, on S. saponaria saplings (Tables 2 & 3).

The phytophagous arthropods, Liriomyza sp., Bemisia sp., Phaneropterinae, Tetranychus sp., T. collaris, and S. anchoralis, demonstrated the highest % I.I.-P.U. on S. saponaria saplings. Liriomyza sp. mines, known to diminish the photosynthetic area in various plants such as Solanum lycopersicon (Solanaceae), Phaseolus vulgaris (Fabaceae), and Terminalia argentea (Combretaceae)^[14−18]. Certain species of Aleyrodidae, exemplified by Bemisia tabaci, are recognized pests inflicting damage on crops including P. vulgaris, Glycine max, Acacia auriculiformis, A. mangium, and Platycyamus regnellii (Fabaceae); Capsicum annuum and S. lycopersicon (Solanaceae); Cucumis melo (Cucurbitaceae); and T. argentea^[10,19−25]. Aleyrodidae, in addition to causing fumagine, are implicated in virus transmission and the introduction of insect toxins^[10,19−25]. Certain species of Tettigoniidae have been documented as causing damage to the fruits of Musa spp. (Musaceae) and the leaves of grasses, A. mangim, A. auriculiformis, and T. argentea^{[10,12,18,26,27]}. Tetranychidae mites, recognized for puncturing the epidermis of leaves, are implicated in G. max, Caryocar brasiliense (Caryocaraceae), S. lycopersicum, and P. vulgaris^[28−33]. T. collaris is known to attack S. saponaria, Casuarina glauca (Casuarinaceae), A. auriculiformis, A. mangium, L. leucocephala, and T. argentea (Combretaceae)^{[12,18,27,34,35]}. Lastly, S. anchoralis has been reported to inflict damage on A. mangium and A. auriculiformis^[10,12,27].

Cycloneda sanguinea and P. termitarius exhibited the highest % I.I.-P.U., thereby diminishing both the numerical abundance and damage caused by Bemisia sp., as well as the population of Liriomyza sp. on S. saponaria saplings. Cycloneda sanguinea, recognized as a significant predator of sap-sucking insects, has demonstrated efficacy in mitigating pest populations on T. argentea saplings in degraded areas and various crops such as Gossypium hirsutum (Malvaceae), Foeniculum vulgare (Apiaceae), and Abelmoschus esculentus (Malvaceae), both in field conditions and laboratory bioassays^[23,36−38]. Tending ants, exemplified by P. termitarius, have been observed to reduce beetle and caterpillar attacks on leaves and fruits^[39−42]. Additionally, Cephalocoema sp. (Orthoptera: Proscopiidae), along with ants, serves as a bioindicator^[10,43]. The potential influence of these predators, particularly those at the apex of the trophic pyramid such as C. sanguinea, in controlling the abundance of herbivores like Bemisia sp. through top-down effects suggests a mechanism that could contribute to the survival of S. saponaria. However, the nuanced relationships between predators and herbivory in commercial crops of S. saponaria warrant further investigation. Contrary to expectations, a negative effect of P. termitarius on Bemisia sp. damage was observed on S. saponaria saplings, defying the anticipated mutualistic relationship between tending ants and sap-sucking insects (Hemiptera)^[44,45]. While Demolin-Leite^[10] did not identify correlations between this tending ant and Aleyrodidae or Aethalion reticulatum (Hemiptera: Aethalionidae) on A. auriculiformis saplings, an increase in the number (≈ 1%) and leaf damage (≈ 62%) caused by Bemisia sp. was noted in relation to the population of Brachymyrmex sp. on S. saponaria saplings, underscoring the complexity of interactions within this ecological system. Further studies are warranted to elucidate the underlying mechanisms governing these relationships. These outcomes can be attributed to the collaborative interactions between tending ants and sap-sucking insects, leading to an exacerbation of the damage inflicted upon these plants. Analogous findings were observed in the context of A. auriculiformis saplings, where the presence of tending ants, specifically Brachymyrmex sp. (e.g., A. reticulatum), and Cephalotes sp. (e.g., Aleyrodidae), resulted in a substantial increase (≈ 95%) in the populations of A. reticulatum and Aleyrodidae, accompanied by a corresponding rise (≈ 30%) in Aleyrodidae-induced damage to this plant^[10]. The detrimental impact of these interactions was reflected in a negative final balance on A. auriculiformis saplings, with a subsequent rise of approximately 57% in herbivorous insect populations within these saplings^[10], mirroring the observed trends in S. saponaria saplings. Particularly at elevated population densities, sap-sucking insects may establish associations with tending ants^[44,45], wherein these ants collectively and aggressively defend their resources, including phytophagous hemipterans^[44]. The lack of a positive effect of tending ants on the biological control of sap-sucking insects may be attributed to mutualistic relationships with these phytophagous insects^[46,47]. In agricultural systems, this dynamic can potentially exacerbate pest-related challenges^[48]. Although Brachymyrmex sp. initially does not pose a significant issue for S. saponaria saplings, the potential for this tending ant species to proliferate and increase sap-sucking insect populations (e.g., Bemisia sp.) exists, particularly under specific conditions such as monoculture, climate, soil variations, and favorable fertilization. This scenario may pose challenges for S. saponaria saplings, especially in the context of prospective commercial crops with monoculture practices.

Liriomyza sp., Bemisia sp., Phaneropterinae, Tetranychus sp., T. collaris, and S. anchoralis, exhibiting the highest % I.I.-P.U. on S. saponaria, pose a potential threat, indicating their capacity to induce losses in crops of this plant. In contrast, C. sanguinea and P. termitarius, characterized by the most substantial % I.I.-P.U., exhibit potential as agents capable of mitigating herbivorous insects on S. saponaria. Furthermore, an anticipated increase in the abundance of ladybeetles, particularly those with major ecological significance, could be expected in future commercial crops of S. saponaria. It is imperative to accord special attention to the association between Brachymyrmex sp. and Bemisia sp. in prospective S. saponaria commercial crops, as this tending ant species has demonstrated an ability to augment the population of the sap-sucking insect. The % I.I.-P.U. emerges as an effective tool for delineating sources of loss and potential solutions in this plant species within systems characterized by production unknown, such as degraded areas. This innovative index holds promise as a valuable tool in the realm of agricultural technology, particularly for monitoring and managing degraded areas.

The author confirms sole responsibility for the following: study conception and design, data collection, analysis and interpretation of results, and manuscript preparation.

All data generated or analyzed during this study are included in this published article. The data that support the findings of this study are available on request from the corresponding author.