Implementing sanitation practices against the hibiscus bud weevil Anthonomus testaceosquamosus (Coleoptera: Curculionidae)

1 Introduction

In the United States, nearly 70 % of the total number (approximately 10 million) of tropical hibiscus plants (Hibiscus rosa-sinensis L.; Malvaceae), hereafter hibiscus, sold in 2019 were produced in Florida (USDA-NASS 2020). As the number one U.S. county for floriculture, greenhouse, and nursery commodities (market value), Miami-Dade contributes significantly to hibiscus production in the state (USDA-NASS 2017). Therefore, when the hibiscus bud weevil, Anthonomus testaceosquamosus Linell (Coleoptera: Curculionidae), originally from northeastern Mexico and southern Texas, was detected on hibiscus in Miami-Dade county in 2017 (Skelly and Osborne 2018), there was legitimate cause for concern. Large hibiscus bud weevil infestations can lead to aesthetically poor hibiscus plants due to the damage resulting from hibiscus bud weevil feeding and oviposition activity (Bográn et al. 2003). Specifically, hibiscus buds drop from plants after hibiscus bud weevil females oviposit inside. Larval and pupal development occurs within these aborted buds, with hibiscus bud weevil adults emerging after approximately 16 days (egg to adult) at 27 °C (Revynthi et al. 2022).

Given that average temperatures exceed 25 °C for half of the year in Miami-Dade county, hibiscus nurseries in south Florida are forced to battle multiple hibiscus bud weevil generations each year (NOAA-NESDIS 2022). The significance of the threat posed by the hibiscus bud weevil to the South Florida hibiscus industry was well understood by the Florida Department of Agriculture and Consumer Services-Division of Plant Industry (FDACS-DPI), and the hibiscus bud weevil was designated as a regulated pest shortly after its discovery in the state (Skelly and Osborne 2018). To prevent the spread of the hibiscus bud weevil and to reduce its population, a compliance agreement was issued by FDACS-DPI to hibiscus growers found with the pest. The compliance agreement allows hibiscus growers to ship their products if they have taken action to guarantee that there is no indication of weevil presence.

Currently, the only management tool recommended by the compliance agreement is contact insecticide application. However, as an overreliance on pesticides can lead to adverse environmental effects and resistance issues, a variety of management solutions are necessary to manage pests sustainably (Barzman et al. 2015). While the development of tactics such as biological control, host plant resistance, and mass trapping can be important tools in integrated pest management (IPM) programs, a considerable amount of research, time, and effort must be invested before these management options are accessible to growers. Management options that do not require specialized knowledge or application technologies may prove useful.

In nursery and greenhouse production systems, sanitation practices (e.g., removal of weeds and plant debris) play a significant role in the maintenance of a clean production environment (Cloyd and Herrick 2021) and in the reduction of pesticide applications and associated costs (Kleczewski and Egel 2011). If not removed, pests developing within discarded or loose plant debris have the potential to reinfest growing plants (Cloyd and Herrick 2021). Hogendorp and Cloyd (2006) demonstrated the importance of removing or otherwise isolating (e.g., stored in containers with tight-sealing lids) greenhouse debris, as thousands of whiteflies, Bemisia spp. (Hemiptera: Aleyrodidae) and hundreds of western flower thrips, Frankliniella occidentalis Pergande (Thysanoptera: Thripidae), were found to emerge from greenhouse-collected plant debris placed in refuse containers over a 6-month period.

Sanitation practices are environmentally friendly, cost-effective, and easy to implement, as these activities can be performed during routine production procedures (Hogendorp and Cloyd 2006). Furthermore, as a key component of a systems-based pest management approach (i.e., a practice that focuses on pest prevention at each operational phase of a nursery system), sanitation practices can mitigate the concerns associated with regulated pests in nursery settings by providing growers with reduced pest movement through the crop cycles, and thereby improving their ability to respond and recover when pests are detected (Cochran et al. 2014).

Because hibiscus bud weevil development is completed within aborted hibiscus buds on the nursery ground, sanitation (e.g., removal and destruction of fallen hibiscus buds) can disrupt the hibiscus bud weevil life cycle and potentially be an effective management tactic for this pest. Previous recommendations for hibiscus bud weevil management have suggested that sanitation could help reduce hibiscus bud weevil numbers alongside crop rotation and well-timed pesticide applications in nursery settings (Bográn et al. 2003), but the effect of removing aborted buds remains to be tested. Therefore, we initially chose to determine the effect of the hibiscus bud weevil on infested plants by examining the number of fallen buds compared to non-infested plants. We hypothesized that infested plants would have a greater number of aborted flower buds than non-infested plants. Subsequently, we studied the effect of sanitation on plant infestation and productivity as measured by the number of fallen and actively growing buds, respectively. We hypothesized that the removal of infested fallen flower buds from hibiscus plants growing in semi-field conditions would significantly decrease hibiscus bud weevil abundance and significantly increase plant productivity when compared with hibiscus bud weevil-infested plants in which fallen flower buds were not removed.

Hibiscus production in South Florida is extensive, with nurseries maintaining monocultures of hibiscus plants in areas ranging from 2–4 ha. Hence, implementing sanitation practices is not always feasible because it is labor- and time-intensive. Therefore, we also chose to test the time efficiency of three different sanitation methods (manual, vacuum, and blower) for the collection and removal of fallen hibiscus buds from nursery settings. Understanding the magnitude of the effect of sanitation on hibiscus bud weevil population dynamics in hibiscus is important as more management tools are required for the development of a sustainable IPM program for this pest.

2 Materials and methods

3 Results

3.1 Effect of hibiscus bud weevil infestation on dropped and actively growing hibiscus buds in greenhouse settings

The number of actively growing buds per plant was influenced by the interaction between treatment and the week of observation (χ ²  = 8.22; df = 3; P = 0.041) (Figure 1A). A higher number of actively growing buds per plant was observed in the second and third weeks in the control and the second week in the infested plants. However, the number of actively growing buds was not significantly affected by treatment alone (χ ²  = 0.27; df = 1; P = 0.598) but varied with observation time (χ ²  = 12.38; df = 3; P = 0.006). Infested plants exhibited 15 to 17 times more dropped buds per plant than control plants that naturally aborted a few flower buds (χ ²  = 19.49; df = 1; P < 0.001). However, no effects were observed due to the sampling week (χ ²  = 2.96; df = 3; P = 0.396) (Figure 1B).

Figure 1:

Actively growing buds (A) and dropped buds (B) per hibiscus plant (estimated marginal means ± SEM; generalized linear mixed-effects model), across 4 weeks of growth after the infestation of two or zero hibiscus bud weevil adults per plant (infested and control, respectively) in greenhouse trials (n = 3, experiment replicated twice). In the number of actively growing buds, significant differences across treatments and weeks are illustrated with lowercase letters, while lowercase letters separate means among treatments across weeks in the number of dropped buds (Tukey adjustment, α = 0.05).

3.2 Effect of sanitation on hibiscus bud weevil infestation and hibiscus plant productivity

Across weeks, significantly more actively growing buds per plant were observed in the no sanitation treatment in comparison to the sanitation treatment (χ ²  = 20.55; df = 1; P < 0.001). Additionally, more actively growing buds were observed during the first week of sampling than in any other sampling week (χ ²  = 374.78; df = 7; P < 0.001) (Figure 2A). Furthermore, significantly more flowers per plant were observed in the no sanitation treatment in comparison to the sanitation treatment across weeks (χ ²  = 9.10; df = 1; P = 0.002). More open flowers per plant were observed during the first week of sampling than in any other sampling week (χ ²  = 41.98; df = 6; P < 0.001) (Figure 2B). The no sanitation treatment had significantly more dropped buds per plant in comparison to the sanitation treatment across sampling weeks (χ ²  = 11.15; df = 1; P < 0.001); while more dropped buds were observed during the first week of sampling than in any other sampling week (χ ²  = 326.11; df = 7; P < 0.001) (Figure 2C).

Figure 2:

Actively growing buds (A), open flowers (B), and dropped buds (C) per hibiscus plant (estimated marginal means ± SEM; generalized linear mixed-effects model), across 8 weeks of growth after the infestation of 20 hibiscus bud weevil adults (ten male, ten female) in tunnel tents containing ten plants. Sanitation tents were subject to weekly sanitation via collecting all fallen buds, while sanitation was not performed in no sanitation tents (n = 4). Within weeks, statistically different treatments are separated with lowercase letters, while statistical differences across weeks are separated with uppercase letters (Tukey adjustment, α = 0.05).

The number of eggs per actively growing bud did not vary significantly either with the treatments (χ ²  = 1.52; df = 1; P = 0.217) or with the sampling weeks (χ ²  = 1.97; df = 3; P = 0.578). However, in each sampling week in which eggs were observed in actively growing buds (sampling weeks 1, 2, 4, and 5), more eggs were observed in replicates with no sanitation than in those in which sanitation procedures were performed (Figure 3A). Although there were no significant differences between sanitation and no sanitation treatments on the number of larvae per actively growing bud (χ ²  = 0.86; df = 1; P = 0.350), in each sampling week in which larvae were observed in actively growing buds (all sampling weeks except sampling week 7), more larvae were observed in replicates with no sanitation than in those in which sanitation procedures were performed. Across treatments, significantly more larvae per actively growing bud were observed during the first week of sampling than in any other sampling week (χ ²  = 80.62; df = 6; P < 0.001) (Figure 3B).

Figure 3:

Number of eggs (A) and larvae (B) per actively growing bud on hibiscus (estimated marginal means ± SEM; generalized linear mixed-effects model), recorded over 8 weeks following the infestation of 20 hibiscus bud weevil adults (ten males, ten females) in tunnel tents containing ten plants. In sanitation tents, weekly sanitation was conducted by collecting all fallen buds, while no sanitation was performed in the no-sanitation tents (n = 4).

Seventy percent of all female (20/29) and 90 % of all male (28/31) weevils emerging from dropped buds collected from sanitation replicates were from the first week of sampling. At least one weevil was collected in each sampling event across all sanitation replicates except for sampling weeks 5 and 8. During the first 4 weeks, a significantly higher proportion of dropped buds was observed in the no sanitation treatment compared to those tents receiving sanitation (χ ²  = 26.39; df = 1; P < 0.001), with an estimated marginal mean 22 % larger (0.41 ± 0.05 SEM dropped buds per plant) than that observed when dropped buds were weekly collected (0.32 ± 0.05 SEM dropped buds per plant). No effects were observed due to sampling week (χ ²  = 3.08; df = 3; P = 0.379), and no interaction effects between treatment and sampling week were detected (χ ²  = 5.65; df = 3; P = 0.129).

3.3 Efficiency of sanitation collection methods

The vacuum collection method was significantly more efficient than either the manual collection method (approximately 20 % more time was required) or blower collection method (approximately 30 % more time was required) at gathering 75 decayed hibiscus buds from the enclosure (χ ²  = 30.19; df = 2; P < 0.001), with no differences between the latter two (Figure 4).

Figure 4:

Time spent (s) to collect a total of 75 hibiscus flower buds using three different collection methods (blower, manual, and vacuum) (estimated marginal means ± SEM; linear mixed-effects model). Experiments were conducted within an approximately 13 m² area containing 50 11.4-L plant pots featuring the plant spacing (0.26 pots per ≈ 1 m²) used in commercial nursery settings. Statistically different treatments are separated with uppercase letters (Tukey adjustment, α = 0.05).

4 Discussion

Previous reports presented anecdotical information on the effects of hibiscus bud weevil infestation on plant productivity (Bográn et al. 2003; Revynthi et al. 2021). Per our observations, after females lay their eggs in the flower buds, they subsequently move to the petiole. There, they pierce the tissue several times, weakening it and potentially making it prone to falling. We propose that this behavior increases female-inclusive fitness via reduced competition, as the induction of bud drop ensures that no other female will lay eggs within the dropped bud. Oviposition exclusion behaviors have previously been reported for the Anthonomus genus, as pepper weevil Anthonomus eugenii Cano (Coleoptera: Curculionidae) females plug oviposition sites using frass in combination with a pheromone to repel additional oviposition from conspecific females (Addesso et al. 2007). In our study, we revealed the effects of hibiscus bud weevil adult infestation on tropical hibiscus flower bud abortion. Notably, plants infested with hibiscus bud weevil exhibited a significant surge in dropped buds, approximately 16 times greater than in the control group, underscoring the need to address this regulated pest. Consequently, it also emphasizes the need for sustained efforts in implementing a comprehensive IPM program to effectively manage the long-term impact of infestations.

Cultural control, defined as the biological or physical alteration of the cultivated field environment during its establishment or growth (Chang et al. 2017), usually presents a cost-effective option that aligns with sustainable alternatives. Such actions potentially serve as a substitute for, or a complement to, chemical insecticides, which are the predominant control method applied in ornamental production. Additionally, these cultural control practices can potentially prevent the development of conditions that reinforce the building of population cycles (All 1999; Norris et al. 2003).

Contrary to our hypothesis, plants in the no sanitation group showed a higher number of actively growing buds and flowers per plant than those in the sanitation treatment in shade house experiments. This phenomenon was similarly observed in the first week of the greenhouse experiment that tested the effects of infestation; however, in the latter scenario, the increase in actively growing buds was not statistically significant. This unexpected increase in plant reproductive organ growth in response to the lack of sanitation, and possibly associated with an increase in pest infestation, may represent the first reported case of overcompensation – a plant’s enhanced growth following damage – in tropical hibiscus. The concept of overcompensation was first identified by Paige and Whitman (1987), and later studies (Paige 2018) have provided further evidence of its adaptive value in plants growing under different environmental stressors. Overcompensation may manifest not just in tissue regeneration, but also in the plant’s production of chemical defenses (van der Meijden et al. 1988; Miles-Mesa et al. 2017). Although our research did not initially aim to investigate this physiological trait in ‘Painted Lady’ tropical hibiscus, our findings suggest that these plants may exhibit a form of host plant tolerance to hibiscus bud weevil infestation. This trait could be advantageous in commercial production settings, as it could constitute a first line of defense (e.g., plant tolerance) in the face of hibiscus bud weevil infestations. However, it is also important to consider that within the range of induced plant defenses, there is also a spectrum of plant manipulation by insects and mites (e.g., gall formation, manipulation of host plant development, and nutritional quality) (Favery et al. 2020). These processes involve the manipulation of plant physiology and development for the benefit of the herbivores. Therefore, at this stage, we cannot rule out the possibility that hibiscus bud weevil females could be inducing higher flower bud production to increase their own fitness. Furthermore, our observations warrant additional research into the specific types of plant responses employed by this hibiscus cultivar in the face of this pest.

In the shade house experiment, a higher number of dropped buds per plant were found in the no sanitation treatment (Figure 2C). This phenomenon is evidently linked to feeding and oviposition activity. Additionally, it was associated with a greater number of actively growing buds observed in the same treatment. Therefore, estimating the proportion of dropped buds provides a way to account for this linkage and helps in contrasting the level of damage between treatments. A higher proportion of dropped buds in the no sanitation treatment aligns with the tendency of higher reproductive activity of the hibiscus bud weevil adults on the plants. This tendency is reflected in a higher number of eggs and larvae per actively growing bud, although this trend was not statistically significant (Figure 3). It is worth noting that during the initial two weeks of the shade house experiment, an infestation of the two-spotted spider mite, Tetranychus urticae Koch (Acari: Tetranychidae) was detected across treatment replicates. Even though this infestation was promptly controlled after releases of the natural enemies Proprioseiopsis ovatus (Garman) and Neoseiolus longispinosus Evans (Acari: Phytoseiidae), it could have resulted in the sudden reduction in plant productivity (i.e., flower buds and flowers) after the first week.

We also demonstrated that the vacuum was the most efficient of all tested collection methods in terms of the time spent on the operation. Additionally, it is important to note that using this system offers additional benefits. Specifically, the vacuum used in these trials shreds the buds it collects, which facilitates the disposal of these final crop residues as surviving larvae and pupae are eliminated in the process. The latter provides a more cost-effective scenario in virtue of the increasing costs of labor in the industry. The identification of a fast and efficient sanitation tool will make the implementation of sanitation easier and more acceptable to the ornamental industry.

In general, sanitation is well accepted in ornamental production and considered a cornerstone strategy for IPM for significant fungal diseases. Removing potential inoculum through sanitation is a key element in limiting the spread of these problems (Benson 2007; Bika et al. 2021). The accumulation of crop residues in the field also creates favorable conditions for insect pests. The benefits of sanitation have been extensively discussed not only in greenhouse environments (Cloyd and Herrick 2022), but also in pest management in open field scenarios. For instance, the larvae of the false wireworms Pterohelaeus spp. (Coleoptera: Tenebrionidae) that feed on plant residues can also target seedlings of various crop plants such as maize, barley, sunflower, soybean, and tomato. Therefore, proper management of crop residues will decrease the chance of infestation on germinating seedlings (Wilson-Rummenie and Radford 2007). In orchards, the management of fallen nuts plays an important role in controlling the navel orangeworm Amyelois transitella (Walker) (Lepidoptera: Pyralidae). Removing the overwintering larvae has proven effective in reducing infestations in the subsequent season (Wilson et al. 2020).

In southern Florida, hibiscus bud weevil populations are usually low between August and January, coinciding with a low availability of hibiscus plants in the nurseries (Revynthi et al. 2021). Pest populations start growing from February until July, with a population peak between March and June during the shipment period. If preventive measures such as sanitation are exercised beginning in February targeting initial pest population growth, other pest management alternatives (e.g., chemical, biocontrol, repellents) may be more efficient at sustaining low pest population numbers during spring. Considering the hibiscus bud weevil life cycle, which at 27 °C can be completed within 16 days (Revynthi et al. 2022), sanitation can be an IPM strategy that reduces hibiscus bud weevil populations in a nursery if implemented twice a month.

While sanitation is an environmentally friendly and effective method, it should not be expected to regulate hibiscus bud weevil on its own. This is because some dropped buds might be unreachable by collection methods, including manual collection. Therefore, complementary alternatives ought to be considered. The application of entomopathogenic nematodes like Steinernema carpocapsae Weiser (Rhabditida: Steinernematidae), which can target fallen buds hidden under the substrate, or those missed at ground level, would be advantageous (Vargas et al. 2024). Currently, additional options for managing hibiscus bud weevil have been proposed, including the use of systemic and contact insecticides (Vargas et al. 2023; Greene et al. 2023). Moreover, the potential application of entomopathogenic fungi and bacteria warrants further study. To effectively integrate a broader range of options into a hibiscus bud weevil IPM program, additional research is needed to enhance monitoring techniques and test the effectiveness of traps baited with lures (Ataide et al. 2024). To foster the implementation of preventive practices that ideally focus on sustainable methods, targeting the initial signs of pest colonization in early spring is vital if crop losses are to be prevented during the shipping season in early summer.