Introduction

Palms (Arecales: Arecaceae) form a group of highly diverse monocots in tropical and subtropical regions of the world (Tregear et al 2011). Their economic importance in international trade is due to their high ornamental value and potential use in food products (Baker et al 2009). The cultivation of ornamental palms has recently become an important source of income for producers entering the market (Ramírez-Rojas et al 2011), and the pests that threaten palm yield, quality, and marketing must be monitored in order to effectively sustain production (MacLeod & Hussein 2017). Currently, the palm agribusinesses of central Veracruz and other Neotropical regions of Mexico have reported yield losses mainly caused by Rhynchophorus palmarum L. (García-Hernández et al 2003, Osorio-Osorio et al 2003, Sumano et al 2012, Landero-Torres et al 2015a, b).

The South American palm weevil (R. palmarum) has severely impacted the yield of ornamental palm agroecosystems in central Veracruz. Particularly, in the Tuxpango Valley prior to 2009, the palm species Washingtonia robusta Wendl. had the highest consumer demand. However, in this same year, the first cases of R. palmarum infestation in ornamental palms were reported. This pest directly and indirectly damaged palm crops of W. robusta and caused economic losses in the study region of approximately $6000.00 USD/ha. Since 2011, the infestation of palms with R. palmarum larvae in addition to the effects of red ring and bud rot diseases has led to a decreased demand for W. robusta in the national market (Landero-Torres et al 2015a).

In general, the South American palm weevil is a primary pest of palms cultivated for food or for ornamental purposes in the Americas (Esparza-Díaz et al 2013, Mazza et al 2014, Soto-Hernández et al 2016). This insect directly damages palms because females lay their eggs in palm crowns, and the hatched larvae then feed on meristematic tissue, preventing palms from producing new fronds (Plata-Rueda et al 2016). The larval phase of this weevil is the most destructive since larvae can tunnel palm stems and often destroy the growth point or damage the lower stem and rhizomes, eventually causing palm death (Alpizar et al 2002). Rhynchophorus palmarum also causes indirect damage as a vector of the oomycete Phytophthora palmivora Butler (Peronosporales: Pythiaceae), which is the causal agent of bud rot disease (Sarria et al 2008), and of the nematode Bursaphelenchus cocophilus (Cobb) (Tylenchida: Aphelenchoididae), which is the causal agent of the red ring disease (Moya-Murillo et al 2015, Plata-Rueda et al 2016). When a palm is infected by one of these pathogens, the associated disease may then rapidly spread among surrounding palms as a result of the foraging activity of R. palmarum through transmission by feeding (Moya-Murillo et al 2015). For this reason, the population monitoring of this pest in palm crops is a necessary tool for the implementation of any control strategy involving an integrated pest management approach (Moura et al 2006, Carreño-Correa et al 2013).

Among the methods for controlling R. palmarum, the most common one is the removal of diseased palms (inoculum) to reduce breeding sites (Oehlschlager et al 2002, Griffith et al 2005). However, various trap types and food attractants combined with synthetic aggregation pheromone have been widely used in the Americas to capture this weevil (Osorio-Osorio et al 2003, Quintero 2010, Carreño-Correa et al 2013, Moya-Murillo et al 2015, Rodríguez et al 2016). The prior studies differ significantly in trapping methods and suggest that the trapping effectiveness of R. palmarum could vary as a function of the trap–bait attractivity, season, and type of palm (i.e., for food or ornamental purposes).

In Mexico, one of the most common trap–bait combinations is a yellow bucket trap made from expensive materials that requires the use of chemical insecticides formulated with deltamethrin or methomyl and synthetic aggregation pheromone (Osorio-Osorio et al 2003, Sumano et al 2012). However, the insecticides used in these traps often cause the death of some beneficial insects and vertebrates that are also attracted to the utilized food attractants. Environmental contamination with insecticides may also occur during bait renewal when baits contaminated with insecticide are discarded. In addition, rainwater may enter into traps, leach insecticides from baits, and then drain to the soil surface (Sumano et al 2012). For this reason, it is important to provide an affordable, environmentally friendly management option for low-income growers that would significantly reduce insecticide applications.

In order to avoid further damages to ornamental palm crops that would threaten their quality and marketing as well as the income of producers (MacLeod & Hussein 2017), innovative strategies to monitor or control R. palmarum are necessary. This study explores the cost and efficacy of using expensive and inexpensive trap–bait combinations for capturing this weevil. In particular, the efficacy of 16 trap–bait combinations for capturing R. palmarum in four ornamental palm polycultures during three climatic seasons was compared.

Material and Methods

Study area

This study was performed in Tuxpango Valley, located near the localities of Campo Grande, Campo Chico and Capoluca in Ixtaczoquitlan, Veracruz, Mexico (Table 1). The climate is warm and humid with a mean annual temperature of 20°C and precipitation of 2199 mm. There are three distinct seasons in the area: a dry, warm season (March to June); a wet, warm season (July to October); and a relatively dry, cool season (November to February) (Landero-Torres et al 2014a, b). The landscape is a mosaic of small remnants of semi-evergreen forest, human settlements, ornamental crops, and vegetable crops (Landero-Torres et al 2014a, b).

Table 1 Polyculture characteristics (P1–P4) and species composition of planted ornamental palms where Rhynchophorus palmarum adults were monitored.
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Sampling design

In the study area, four commercial polycultures, each with an extension of 4 ha, were selected. Different ornamental palm species are cultivated on these sites (Table 1). These plots were selected based on the accessibility granted by owners and were located from 1 to 3 km apart, with an elevation varying from 793 to 803 m (Table 1). All palm plants had been established for 2 years.

A balanced sampling design was used, consisting of a total of 16 trap–bait combinations (4 trap × 4 bait types) that were assessed during a 16-week period in each of the three climatic seasons. Each polyculture was divided into four blocks of 1 ha containing 600 to 1600 palms. In each block, four palms were selected for installing a different trap–bait combination. In total, 16 trap–bait combinations per polyculture were installed. To avoid any effect from the spatial distribution of traps and baits, the trap–bait combinations were rotated clockwise on a weekly basis among the blocks of each polyculture.

Assessment of trap types

Four different types of traps were used to capture R. palmarum individuals (Fig 1). The first trap, made from a white bucket, was previously used by Sumano et al (2012) and Landero-Torres et al (2015a) (Fig 1a). The second and third traps were handmade from discarded polyethylene (PET) bottles (plastic soda bottles) (Fig 1b, c). The fourth trap type was a common yellow bucket trap that is currently recommended by the Plant Health Committee of the State of Tabasco (CESVETAB 2016) (Fig 1d).

Fig 1
figure 1

Frontal view of the evaluated trap types for capturing Rhynchophorus palmarum. A White bucket trap. B Colorless PET-bottle trap. C Green PET-bottle trap. D Yellow bucket trap.

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The first trap was constructed from a cylindrical white bucket (19-L capacity) with a base diameter of 30.5 cm and a height of 36 cm (NOVATEC PAGANI® S.A. de C.V, Mexico City, Mexico) (Fig 1a). For adult weevil access, four equidistant holes of 5 cm in diameter were perforated on the sides of the bucket near the top rim in addition to four holes of the same diameter on the lid of the bucket. To drain water in case of rain, five holes of 6 mm in diameter were perforated on the bottom of the bucket. One of these holes was positioned in the center, and the other holes were positioned between the center hole and the bottom rim of the bucket. This trap followed the proposed design of Sumano et al (2012).

The second colorless PET-bottle trap was made from colorless polyethylene bottles (PET) of 3-L capacity (PepsiCo® Inc., New York City, New York) (Fig 1b). For adult weevil access, two square holes of 4 × 4 cm were cut into the sides of the bottle at a height of 20 cm from the base. Only three sides of the square opening were cut, as the upper side of the square was left uncut to avoid entry of excess rainwater. These trap openings simulated a ramp of 45° perpendicular to the axis of the bottle. In addition, five 6-mm-diameter holes were cut around the perimeter of the bottle at a height of 5 cm from the base to prevent potential accumulation of rainwater.

The third green PET-bottle trap (PepsiCo® Inc., New York City, New York) had the same features as colorless PET-bottle trap, with one notable modification aside from the difference in color (Fig 1c). The bottom sides of the square openings, rather than the upper side, were left uncut to form ramps.

The fourth yellow bucket-type trap was made from a yellow plastic container with a base diameter of 30 cm, a top diameter of 37 cm, and a length of 29 cm (Cuplasa® Mexico City, Mexico) (Fig 1d). A circular yellow tray with a diameter of 40 cm and a depth of 10 cm (Cuplasa®, Mexico City, Mexico) was inversely fastened at 5 cm from the top rim of the bucket to allow for adult weevil access.

Each trap was set in the field and hung from a palm frond by a rope tied to the handle of the bucket or the neck of the bottle. In each polyculture, 16 traps were set. Four traps of each trap type were assessed: one per selected palm in each block. To ensure that weevils would enter the traps after perching on palm stems, the hanged traps were carefully adjusted to be in direct contact with the stem of the selected palm at a height of 1.5 m above ground level (Chinchilla & Oehlschlager 1992).

Assessment of baits

Three different bait combinations previously used by Landero-Torres et al (2015b) and the bait–lure combination currently recommended by CESVETAB (2016) were compared. The four bait combinations were (1) a 1:1 mixture of banana (Musa paradisiaca L.; Zingiberales: Musaceae) and pineapple (Ananas comosus Merr.; Poales: Bromeliaceae), (2) a 1:1 mixture of sugarcane (Saccharum officinarum L.; Poales: Poaceae) and sugarcane molasses, (3) a 1:1 mixture of bait 1 and bait 2, and (4) a 1:1 combination of the synthetic aggregation pheromone rhynchophorol (RHYNKO-LURE® ASD, Costa Rica) and banana. This latter bait-lure combination also included the commercial insecticide LANNATE®, which has methomyl as the active ingredient (E.I. du Pont de Nemours and Company, Wilmington, DE).

The baits were placed in the traps in similar amounts (200 g) in addition to 200 mL of water. These amounts were adequate for guaranteeing that the bait would ferment and attract weevils for 7 days until its replacement. To disperse the aggregation pheromone, a commercially available polyethylene diffuser was installed in the middle of the trap. This device has a diffusion rate of 1.6 mg/day and a duration of 45 days, so it was replaced every 4 weeks (Moya-Murillo et al 2015).

Cost estimates for each trap–bait combination

The cost-effectiveness (C E) of each of the 16 evaluated trap–bait combinations (4 baits × 4 traps) was evaluated during 1 year of sampling according to the following equation (Caudell et al 2010):

$$ {C}_{\mathrm{E}}=\left[Cm+(Cb)(Rf)+(Cl)(Lf)\right](Ap) $$

where C E represents the annual estimated cost per trap for capturing adult weevils, considering the necessary materials and supplies for manufacturing the traps and the labor required for the preparation, placement, and maintenance of traps. Cm is the monetary cost of the materials required to make the traps by hand according to the suppliers’ price list. Cb is the average market cost of the exact quantity of evaluated bait according to the price per kilogram of product at Wal-Mart Stores, Inc.®. Rf is the replacement frequency of the baits for each trap–bait combination during 1 year of sampling. Cl is the monetary cost of the required labor, including the hiring of laborers to change baits, as per the minimum salary established by the National Commission of Minimum Wages in Mexico (CONASAMI 2016). Lf is the number of times that manpower was required for collecting weevils in each trap–bait combination during 1 year of sampling. Ap is the number of traps set per polyculture. All monetary costs and C E are expressed in US dollars, considering the average exchange rate from January to December 2016.

Sample processing

All captured specimens were sorted and counted. Of the total captured weevils, 1% were dry mounted to create a reference collection. The remaining 99% of specimens were preserved in 70% alcohol. All representative vouchers were deposited in the Entomological Collection of the Instituto de Ecología A.C. in Xalapa, Veracruz, Mexico (IEXA; Reg. SEMARNAT: Ver. IN.048.0198).

Statistical analysis

From the number of weevils recorded weekly, the number of weevils per trap per day (WTD) was determined. To calculate this index, the number of males, females, and total weevils captured weekly per trap was divided by the number of days in the week (7 days) in order to provide a relative estimate of the average size of the adult population in a given space and time (Aparicio-Del Moral et al 2015). In order to detect the possible effects of trap type, bait mixture, sampling season, sex, and polyculture on the number of weevil captures per trap per day, a generalized linear model was used, assuming a Gaussian error distribution and an identity link function. The analysis was based on a balanced repeated measures design with four fixed factors (trap type, bait mixture, sampling season, and sex). The analyses were performed using the function “glmer” of the R package “lme4” (Bates et al 2014). The models were evaluated according to the Akaike’s Information Criterion (AIC) (Akaike 1987), comparing the ΔAIC of the null model with respect to the aforementioned model. Models with ΔAIC ≤2 were considered equivalent. In order to test for differences among the different levels of the fixed factors, a Tukey’s post-hoc test was performed using the “glht” function of the R package “multcomp” (Hothorn et al 2008). All analyses were performed in the statistical software R 3.2.3 (R Development Core Team 2014).

Results

A total of 4712 R. palmarum adults were captured using 16 trap–bait combinations in four ornamental palm polycultures during 1 year of sampling that comprised three climatic seasons (Table 2). Of the captured weevils, 47.3% were female and 52.7% were male. The colorless PET trap and the yellow bucket trap combined with banana + pineapple + sugarcane + sugarcane molasses and with pheromone + banana + insecticide captured the highest number of adult weevils (~10% each). The remaining 12 trap–bait combinations captured less than 7% of total weevils. Most weevils were captured in the wet, warm season (46%), followed by the dry, cool season (28%) and the dry, warm season (26%). All trap–bait combinations captured at least one weevil per trap per week in the wet, warm season. The total number of zero captures was 19, of which 21% occurred in the dry, cool season and the remaining 79% in the dry, warm season (Table 2).

Table 2 Number of Rhynchophorus palmarum adults captured by 16 trap–bait combinations in four polycultures of ornamental palms during three climatic seasons in Veracruz, Mexico.
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The factors of trap type (F = 254.67, df = 3, P = 0.001), bait mixture (F = 128.97, df = 3, P = 0.001), sampling season (F = 366.97 df = 2, P = 0.001), and sex (F = 28.57, df = 1, P = 0.001) significantly affected the number of captured weevils per trap per day (WTD). However, only the interaction among trap type, bait mixture, and sex led to a significant variation (F = 11.91; df = 9; P = 0.001; Fig 2) in the number of captured WTD. Pairwise tests indicated that both the yellow bucket trap and the colorless PET trap captured a significantly higher number of WTD than the white bucket trap (t = 13.39; P = 0.001) and the green PET trap (t = 17.95; P = 0.001). The bait mixtures of pheromone + banana + insecticide and of banana + pineapple + sugarcane + sugarcane molasses captured a significantly higher number of WTD than the bait mixtures of banana + pineapple and sugarcane + sugarcane molasses (F = 86.02; df = 3; P = 0.001) (Fig 2). When WTD was divided by sex, the observed mean number of males (0.46) was significantly higher than that of females (0.41) over the course of 1 year of sampling (F = 28.57; df = 1; P = 0.001) (Fig 2).

Fig 2
figure 2

Variation or interaction in the number of adult weevils captured per trap per day (WTD) ± standard error (SE) among the different traps and baits evaluated for capturing Rhynchophorus palmarum. The dotted sections of each bar indicate female WTD, and the solid sections indicate male WTD. Bars labeled with the same letter are not significantly different (Tukey’s test, P > 0.05). Baits corresponds with (1) a mixture of banana + pineapple, (2) a mixture of sugarcane + sugarcane molasses, (3) a mixture of banana + pineapple + sugarcane + sugarcane molasses, and (4) a combination of rhynchophorol + banana + insecticide. The ingredients of each bait were of equal ratio.

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The sampling season factor independently affected variation in captured WTD; a significantly higher number of weevils were captured in the wet, warm season than in the dry, cool season and the dry, warm season (F = 244.77; df = 2; P = 0.001) (Fig 3). Additionally, the interaction among the factors of sampling season, trap type, and sex (F = 2.16; df = 6; P = 0.04) significantly affected the number of captured WTD.

Fig 3
figure 3

Variation or interaction in the total number of Rhynchophorus palmarum adults per trap per day (WTD) ± standard error (SE) captured by four different trap types during the three sampling seasons. The dotted sections of each bar indicate female WTD, and the solid sections indicate male WTD. Bars labeled with the same letter are not significantly different (Tukey’s test, P > 0.05).

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The combined cost of each trap and bait type affected the cost-effectiveness of the 16 trap–bait combinations for capturing R. palmarum (Table 3). The banana + pineapple bait combined with the colorless PET or the green PET trap were the combinations with the lowest annual cost per hectare ($804 USD each), followed by the latter bait combined with the white bucket trap ($831 USD) and the yellow bucket trap ($846 USD). Meanwhile, the mixture of pheromone + banana + insecticide bait combined with the white bucket, the colorless PET, or the green PET trap had an annual cost per hectare of $1636 USD, mainly attributable to the high cost of the pheromone and insecticide. The highest annual cost per hectare ($1678 USD) resulted from the combination of this bait mixture with the yellow bucket trap. Among the trap–bait combinations that captured the highest number of adult weevils (~10% each, Table 2), the mixture of banana + pineapple + sugarcane + sugarcane molasses bait combined with colorless PET trap was the cheapest and the mixture of pheromone + banana + insecticide bait combined with yellow bucket trap was the most expensive.

Table 3 Cost estimates of each trap–bait combinations for capturing Rhynchophorus palmarum in ornamental palm polycultures in Veracruz, Mexico.
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Discussion

Based on the results of the weevil sampling in the present study, some effective and affordable trap types that may be used with food attractant and without insecticide are proposed. In comparing the efficacy of the studied traps, the colorless PET and the yellow bucket traps captured a similar number of weevils per trap per day (Fig 2). One of the characteristics that may have contributed to the efficacy of the colorless PET-bottle trap was design of the trap openings (4 cm × 4 cm) (Fig 1). The trap openings may have facilitated volatile emission (e.g., ethyl acetate) from the fermented baits and the entry of weevils into the trap, as demonstrated by Osorio-Osorio et al (2003) and Landero et al (2015b). In fact, the flaps left uncut on the upper side of the square openings at an angle of 45° with respect to the central axis of the trap (Fig 1) might retain weevils in the trap after their capture. Similar results were demonstrated in a previous study carried out in a palm oil plantation in Colombia (Moya-Murillo et al 2015).

The attraction of weevils to the colorless PET-bottle trap baited with a mixture of banana + pineapple + sugar cane + sugarcane molasses was similar to their attraction to the yellow bucket trap baited with pheromone + banana + insecticide that is normally used by producers (Fig 2). The difference between these trap–bait combinations is that the first does not require insecticides to kill weevils in order to prevent their escape from the trap. In fact, during the experimental period, the captured insects were observed to remain alive at the interior of the colorless PET-bottle trap since food was present. Similar results were demonstrated by Osorio-Osorio et al (2003), Sumano et al (2012), and Landero et al (2015b) for distinct trap types. These authors also suggest that the captured males could remain alive inside traps by feeding on the fermenting bait and could emit aggregation pheromone, attracting other R. palmarum weevils to the trap.

The olfaction of weevils plays an important role in their attraction toward baited traps (Saïd et al 2003). The bait mixtures of banana + pineapple + sugar cane + sugarcane molasses and of pheromone + banana + insecticide captured the highest numbers, which were similar to one another, of weevils per trap per day (Fig 2). Previous studies in the study area and in other palm-producing regions indicate that banana, pineapple, and sugarcane produce ethanol, pentane, and ethyl acetate during fermentation (Oehlschlager et al 2002, Plata-Rueda et al 2016). These compounds are crucial for attracting adults of R. palmarum in field conditions and across short distances (Saïd et al 2003, Moya-Murillo et al 2015, Plata-Rueda et al 2016).

The abundance of R. palmarum significantly increased in the wet, warm season and decreased during the driest season of the year (Fig 3). Similar results have been found in other studies in which higher levels of rainfall and humidity were associated with greater numbers of captured weevils (Ferreira et al 2003, Correia et al 2015, Pinho et al 2016). During the rainy season, the plant fibers used by larvae to pupate are soft and easily opened by insects upon their emergence. However, in the dry season, plant structures are more rigid; insects may have more difficulty emerging or may become trapped and die (Correia et al 2015). This factor should be considered when planning campaigns to monitor this pest. For instance, the number of traps could be increased during the wet, warm season when weevil abundance is higher and could be decreased during drier seasons when weevil abundance is lower.

With regards to the annual cost estimates for each trap–bait combination, the cost of the yellow bucket trap baited with pheromone + banana + insecticide was the highest due to the prices of the LANNATE® insecticide and the rhynchophorol aggregation pheromone (Table 3). The annual investment in materials and maintenance of colorless PET-bottle traps with the bait mixture of banana + pineapple + sugar cane + sugarcane molasses was lower in comparison to of the annual cost of yellow bucket traps baited with the mixture of pheromone + banana + insecticide (a saving of $528 USD). Otherwise, both bait–trap combinations did not significantly differ in terms of weevil attraction or capture. Therefore, the cheaper trap–bait combination may replace the traditional yellow bucket trap that has been widely used by palm producers in Mexico for capturing R. palmarum (CESVETAB 2016).

The use of PET bottles for capturing R. palmarum could have significant advantages for growers. Palm growers with limited economic resources can easily use and construct this highly efficient, cheap, and simple trap, as colorless PET bottles (Figs 1 and 2) are available worldwide. In addition, these traps can last several years (Lasa et al 2014). Thus, the use of these traps could represent significant savings for growers using traps as strategy for capturing R. palmarum. Although the durability of these PET traps was not evaluated, these traps were re-used during the entire experimental period and remained in good enough condition to use for a second year. In contrast, the yellow and the white bucket traps were discarded after the experimental period because the plastic structure of the buckets, lids, and trays had begun to break from use and exposure to climatic conditions (rain and sun). Thus, the overall advantage of using PET traps is that they reduce trap costs without significantly influencing trapping efficacy (Table 3). However, additional tests should be conducted to evaluate the durability of these traps as well as the stability and sensitivity of the utilized baits, whose modification could potentially further improve costs.

From our cost estimate results, additional trap–bait combinations that are cheaper but less attractive can be highlighted for capturing R. palmarum in ornamental palm polycultures (Tables 2 and 3). Palm producers of the studied region often capture adult weevils by hand, collecting them during their times of greatest activity and also killing them by hand, which represents a common cultural control practice (Landero-Torres et al 2015a, b). In other areas of the country, palm producers commonly use the expensive trap made from the yellow bucket and baited with banana + synthetic aggregation pheromone + insecticide for capturing palm weevils (Osorio-Osorio et al 2003, Sumano et al 2012). However, in other municipalities of the state of Veracruz such as Villa Unión, Cuatlapan, Zapoapan, and Zapoapita insecticides are systematically applied to planted palms to protect them from this pest (Landero-Torres et al 2015a). This is considered an ineffective practice since R. palmarum adults do not remain for long periods of time on healthy palm fronds. Adult weevils are only attracted to wounded or diseased palms where they stop and reproduce (Osorio-Osorio et al 2003, Plata-Rueda et al 2016).

In conclusion, the implementation of affordable traps and baits for capturing R. palmarum represents an effective tool for monitoring weevil populations. In particular, the colorless PET-bottle trap baited with a mixture of banana + pineapple + sugar cane + sugarcane molasses may be useful for palm producers. Due to the recent economic importance of ornamental crops in the studied region (Murguía-González et al 2007, Ramírez-Rojas et al 2011, SIAP 2016), the use of a novel and cheap trap–bait combination may provide great benefits to producers in the integrated management of R. palmarum.