Summary
The persistence of the entomopathogenic nematode (EPN), Steinernema carpocapsae, was evaluated following application on date palm (Phoenix dactylifera) trees infested with the red palm weevil (RPW) Rhynchophorus ferrugineus in an arid environment. Live S. carpocapsae were detected in different sections of the tree trunk, including internal parts, in the soil, and from RPW cadavers. EPN third-stage infective juveniles were extracted from the palm stem tissue and soil up to 45 days and 180 days after application, respectively. Results support the high potential of commercial S. carpocapsae application as a useful biological control agent for R. ferrugineus in date palms in arid environments.
The red palm weevil (RPW), Rhynchophorus ferrugineus (Olivier) (Coleoptera: Curculionidae), is among the most severe wood borers of palm trees worldwide. The weevil, which originated in Southeast Asia, is highly invasive. It is known to occur in high densities in all Mediterranean countries as an aggressive pest of palm trees. The outbreak of RPW in countries cultivating date palm (Phoenix dactylifera L.) has put the yield and quality of date production at risk (Kehat, 1999; Saleh & Alheji, 2003; Elkahky & Faleiro, 2020). In the date palm, the injury is inflicted mostly by the larvae feeding on the inner trunk tissue, avoiding exposure on external tissues. Therefore, RPW management usually relies on treatments with synthetic insecticides applied as a spray, or by injection or augmentation (Soroker et al., 2005; Al-Dosary et al., 2016; Elkahky & Faleiro, 2020; Ferry & Gomez, 2020; Kassem et al., 2020).
The RPW larvae can be found in all date palm stem sections. However, the major colonisation sites differ among palm species. In Canary palm (Phoenix canariensis), the RPW establishes itself mostly in the crown where the larvae feed on its soft tissues, killing the main bud and, consequently, the tree. In the date palm, adult weevils strongly prefer the lower part of the stem, where the offshoot joins the trunk, or wounds of detached offshoots, which serve as oviposition spots. The neonate larvae start feeding extensively on the tissues, generating feeding tunnels inside the trunk. Heavy infestation affects stem stability and the palm may collapse, usually before any visible symptoms appear. The biology and concealed feeding behaviour of the RPW make it a most challenging pest to control (Blumberg, 2008). Management of crown infestation by direct application of chemical or biological means to the crown is possible (Dembilio et al., 2010; Jacas et al., 2011). Even though a few known natural enemies have been found associated with RPW (Mazza et al., 2014; Ortega et al., 2017), no parasitoids or predator arthropods have been found that significantly and effectively control them. By contrast, microbial control agents such as bacteria, viruses and entomopathogenic fungal isolates have been found in diverse geographical areas associated with RPW life stages (Yasin et al., 2017; Sutanto et al., 2021). Another group of potential biological control agents consists of entomopathogenic nematodes (EPN) (Dembilio et al., 2010; Nurashikin-Khairuddin et al., 2022).
EPN are well known naturally occurring enemies of insect pests and today they routinely serve as biological control agents in integrated pest management strategies. Steinernema carpocapsae (Steinernematidae) and Heterorhabditis bacteriophora (Heterorhabditidae) are the major EPN applied to control insect pests (Griffin, 2012). The third-stage infective juvenile (IJ) of these EPN actively searches for a suitable host, invades it, and releases species-specific symbiotic bacteria (Xenorhabdus and Photorhabdus for Steinernematidae and Heterorhabditidae, respectively) that infect the host haemocoel. This process leads to the mortality of the invaded insect via bacterial septicemia and/or toxemia (Kaya & Gaugler, 1993).
Infectivity of these EPN against the RPW has been well established (Dembilio et al., 2010; Atakan et al., 2012; Manachini et al., 2013; Santhi et al., 2015). Commercial formulations of these biological agents against the RPW in Canary palms are applied in urban areas of southern Europe and the Canary Islands (Dembilio et al., 2010), where the nematodes are sprayed onto the tree crown. However, their application as biocontrol agents against this RPW in date palm orchards faces two different challenges: i) harsh abiotic constraints for EPN persistence in the dry and hot environment that typifies date palm cultivation in arid and semiarid regions, which are characterised by long and hot summers, no (or at best low) rainfall, and very low relative humidity level during the ripening period (Abdelouahhab & Arias-Jimenez, 1999); and ii) delivering the nematodes into the cryptic niches inhabited by the insect larvae in date palm trees. Previous studies (Atwa & Hegazi, 2014; Rehman & Mamoon-ur-Rashid, 2022) drilled holes in the date palm trunk and injected a nematode suspension into the RPW tunnels inside the trunk. This methodology provides the EPN with a secure environment, but is controversial due to expected physiological damage to the tree, and the highly accurate visual cues needed to locate RPW tunnels. The dispersal and survival of the EPN IJ in palm tree fibres were tested by Santhi et al. (2015, 2016), demonstrating the ability of H. bacteriophora and S. carpocapsae to locate and infect the various developmental stages of RPW under simulated natural conditions in tubes filed with moist coconut pith. These results implied that EPN, and, in particular, S. carpocapsae, can reach and infect both adult and immature stages of RPW in the tree cavity.
Encouraged by those findings, in the present study we evaluated the fate of the EPN under field conditions. The major objective of the study was to determine the spatial and temporal distribution of the nematodes in the date palm tissues and surrounding topsoil, as well as infection of RPW larvae, pupae and adults in the infested trees, following topical EPN application.
Materials and methods
The experiment was conducted in a palm nursery that was heavily infested with RPWs. It consisted of about 1500 trees, 4-6 years old, planted in sandy soil, and was located in the western Negev desert (31°15′15.6″N 34°28′46.3″E). The trees were irrigated weekly (50 mm per week) without fertilisation. Four hundred trees (six adjacent rows, 60-70 trees in a row) were examined for RPW infestation, which was determined by the presence of emergence tunnels, ranging between 1 and 8, on the date palm trunk (Fig. 1A), dead offshoots and leaf gnawing. Among the RPW-infested trees, 72 were randomly chosen for EPN application. Each of the selected trees was measured for the following parameters: height, trunk size, number of offshoots and number of leaves.
A: Phoenix dactylifera infested with red palm weevil. A burrow made by Rhynchophorus ferrugineus larvae before developing into pupae can be seen near the young offshoot in the centre of the picture (arrow); B: Sampling locations: in the date palm’s roots/tree base (a), inside the trunk (b), and in the upper trunk just below the crown (c); and in the soil in the upper boundary of the root zone (s).
Citation: Nematology 2023; 10.1163/15685411-bja10246
A: Phoenix dactylifera infested with red palm weevil. A burrow made by Rhynchophorus ferrugineus larvae before developing into pupae can be seen near the young offshoot in the centre of the picture (arrow); B: Sampling locations: in the date palm’s roots/tree base (a), inside the trunk (b), and in the upper trunk just below the crown (c); and in the soil in the upper boundary of the root zone (s).
Citation: Nematology 2023; 10.1163/15685411-bja10246
A: Phoenix dactylifera infested with red palm weevil. A burrow made by Rhynchophorus ferrugineus larvae before developing into pupae can be seen near the young offshoot in the centre of the picture (arrow); B: Sampling locations: in the date palm’s roots/tree base (a), inside the trunk (b), and in the upper trunk just below the crown (c); and in the soil in the upper boundary of the root zone (s).
Citation: Nematology 2023; 10.1163/15685411-bja10246
Mean captures of red palm weevil (RPW) adults in five traps (represented as mean number of beetles per trap per day) located in the experimental site. Bars = standard error.
Citation: Nematology 2023; 10.1163/15685411-bja10246
Mean captures of red palm weevil (RPW) adults in five traps (represented as mean number of beetles per trap per day) located in the experimental site. Bars = standard error.
Citation: Nematology 2023; 10.1163/15685411-bja10246
Mean captures of red palm weevil (RPW) adults in five traps (represented as mean number of beetles per trap per day) located in the experimental site. Bars = standard error.
Citation: Nematology 2023; 10.1163/15685411-bja10246
Adult RPW flying activity in the area (Fig. 2) was monitored using five traps (Sansan Prodesing) baited with ethyl acetate, molasses and RPW aggregation pheromone (ChemTica Internacional).
Commercial packages containing S. carpocapsae IJ were supplied by e-nema (Schwentinental, Germany). Nematodes were applied in the first week of February, when the temperature near the soil surface was 20°C. To ensure EPN vitality, they were applied in the evening, to avoid the intense solar radiation and high temperatures during the daylight hours that are typical of this region. On each tree, we applied 10 × 106 IJ in a volume of ca 10 l tap water with a mechanical sprayer with a large nozzle (0.8 mm diam.), so that the nematode solution would rinse the whole trunk, offshoots and tree crown around the growing point.
To determine nematode survival and distribution, samples were taken 10, 20, 30 and 45 days after application (DAA). At each sampling date, 8-10 trees were cut down. From each tree, ca 200 ml of tissue was taken from the base (Fig. 1Ba), inside the trunk at mid-height (Fig. 1Bb), crown, and offshoots below the growing point (Fig. 1Bc). In addition, at 45 and 180 DAA, soil samples of ca 500 ml were taken 30-50 cm near the tree base (Fig. 1Bs). Each sample was put in a 0.5 l plastic container and kept in a cool box to reduce exposure to high temperatures during transport.
All samples were examined in the laboratory of the Nematology Division at the Agricultural Research Organization (ARO), Volcani Center, Israel. Prior to application of the EPN, we determined the presence of natural EPN populations in the nursery orchard as follows: soil samples (0.5 l) were taken next to the base of five trees and four late-instar larvae of the greater wax moth, Galleria mellonella, were added to each container as a ‘nematode trap’ (Kaya & Stock, 1997). The containers were incubated for 5 days at 25oC, then the number of dead larvae displaying typical symptoms of EPN infection was determined. No EPN infection was recorded.
To determine the presence of EPN in the samples after their application, each sample was separated into two parts. The first one, ca 200 ml, was placed on a sieve with 80 μm mesh in a water-filled Baermann funnel, and the nematode suspension that settled after 24 h was collected and counted as described by Salame et al. (2010) under an SZX10 stereo microscope (Olympus). The number of IJ obtained from each sample was estimated according to a 1-5 index scale: 0 = no IJ; 1 = 1-10 IJ; 2 = 11-20 IJ; 3 = 21-100; 4 = 101-1000 IJ; 5 = over 1000 IJ. The second part of the sample was kept in the plastic container and incubated as described above with G. mellonella as a nematode trap; the number of dead larvae displaying typical symptoms of EPN infection was determined. Three G. mellonella cadavers from each sample were dissected to check further for nematode infection.
During the tree dissection process, dead or live insects were occasionally found. Most of them were identified in the field as RPW and documented (Table 1). Samples were placed in migration plates (Kaya & Stock, 1997) and incubated for 7 days at 25oC before recovery of nematodes was recorded.
Summary of red palm weevil individuals, classified into different life stages (larvae, pupae, adults), found in the process of date palm dissection at different days after application (DAA) of entomopathogenic nematode, Steinernema carpocapsae.
Citation: Nematology 2023; 10.1163/15685411-bja10246
Summary of red palm weevil individuals, classified into different life stages (larvae, pupae, adults), found in the process of date palm dissection at different days after application (DAA) of entomopathogenic nematode, Steinernema carpocapsae.
Citation: Nematology 2023; 10.1163/15685411-bja10246
Summary of red palm weevil individuals, classified into different life stages (larvae, pupae, adults), found in the process of date palm dissection at different days after application (DAA) of entomopathogenic nematode, Steinernema carpocapsae.
Citation: Nematology 2023; 10.1163/15685411-bja10246
Results
Experimental field characterisation
Physical characteristics of the date palm trees and RPW infestation were recorded. The mean height of the sampled trees in the examined plot was 3 ± 0.6 m (n = 72). Mean number of shoots per tree was 9 ± 3 (n = 71). Mean number of date palm leaves was 16 ± 4 (n = 72). Mean number of RPW tunnels found in the date palm tree trunks was 1.93 ± 1.25 (n = 72). No correlation was found between physical measurements of the sampled date palm tree and number of RPW tunnels observed (tree height χ2 = 29.9,
Red palm weevil activity in the experimental site
The weekly adult captures indicated continuous flying activity throughout the experimental period, peaking in the spring (March-April) (Fig. 2). Mean captures varied between 1 and 5 adults trap−1 day−1. Together with the finding of other life stages in the tree or soil, this suggests overlapping generations of the pest population within the experimental site.
Red palm weevil activity in the date palm trunks
Tunnels made by RPW larvae were present in all of the trees, and all of the trees had tunnels in the trunk base area (Fig. 1Ba); 78% of the sampled palms also had tunnels in the trunk part (Fig. 1Bb); 62% of the sampled trees had additional tunnels in the trunk, shoot and tree crown (Fig. 1Bc). Larvae, pupae and adult RPW individuals were found inside all cut palm trees, in all sampling events following EPN application. Table 1 summarises the findings for live and dead RPW, which were limited to the whole tree without segmentation. We did not observe any significant change in mortality of RPW larvae or adults from EPN application onward (Table 1), but the death ratio of pupal life stages showed a positive trend, i.e., increased pupal mortality with time.
Average index value (scale: 0 – no infective juveniles (IJ); 1 = 1-10 IJ; 2 = 11-20 IJ; 3 = 21-100; 4 = 101-1000 IJ; 5 = over 1000 IJ) of Steinernema carpocapsae presence in samples (nematode extracts from: A: Soil and wood fibres in tree base; B: Wood fibres in trunk; C: Wood fibres in crown/shoots; soil, soil near trunk) with time from nematode application in the field. Bars = standard error.
Citation: Nematology 2023; 10.1163/15685411-bja10246
Average index value (scale: 0 – no infective juveniles (IJ); 1 = 1-10 IJ; 2 = 11-20 IJ; 3 = 21-100; 4 = 101-1000 IJ; 5 = over 1000 IJ) of Steinernema carpocapsae presence in samples (nematode extracts from: A: Soil and wood fibres in tree base; B: Wood fibres in trunk; C: Wood fibres in crown/shoots; soil, soil near trunk) with time from nematode application in the field. Bars = standard error.
Citation: Nematology 2023; 10.1163/15685411-bja10246
Average index value (scale: 0 – no infective juveniles (IJ); 1 = 1-10 IJ; 2 = 11-20 IJ; 3 = 21-100; 4 = 101-1000 IJ; 5 = over 1000 IJ) of Steinernema carpocapsae presence in samples (nematode extracts from: A: Soil and wood fibres in tree base; B: Wood fibres in trunk; C: Wood fibres in crown/shoots; soil, soil near trunk) with time from nematode application in the field. Bars = standard error.
Citation: Nematology 2023; 10.1163/15685411-bja10246
Steinernema carpocapsae activity and persistence
Activity and persistence of S. carpocapsae were detected throughout the entire trial period and at all sampling locations: trunk base, internal trunk tissues, offshoots and crown tissues (Fig. 3). The presence of IJ (estimated on a 1-5 scale) indicated a mean index value between 0.5 and 2.5 (Fig. 3). The nematode levels found in samples 10 and 30 DAA were higher in the tree base and in the shoots and crown tissue than in the tree trunk. Nematode levels in samples 20 DAA were higher in the shoots and crown. Nematode level in samples 45 DAA was higher in the tree trunk and tree base than in the shoots or crown.
Mean proportion of insect (Galleria mellonella) mortality due to exposure to Steinernema carpocapsae in collected samples (A: Soil and wood fibres in tree base; B: Wood fibres in trunk; C: Wood fibres in crown/shoots; soil, soil near trunk) with time from nematode application in the field. Bars = standard error.
Citation: Nematology 2023; 10.1163/15685411-bja10246
Mean proportion of insect (Galleria mellonella) mortality due to exposure to Steinernema carpocapsae in collected samples (A: Soil and wood fibres in tree base; B: Wood fibres in trunk; C: Wood fibres in crown/shoots; soil, soil near trunk) with time from nematode application in the field. Bars = standard error.
Citation: Nematology 2023; 10.1163/15685411-bja10246
Mean proportion of insect (Galleria mellonella) mortality due to exposure to Steinernema carpocapsae in collected samples (A: Soil and wood fibres in tree base; B: Wood fibres in trunk; C: Wood fibres in crown/shoots; soil, soil near trunk) with time from nematode application in the field. Bars = standard error.
Citation: Nematology 2023; 10.1163/15685411-bja10246
Exposure of G. mellonella larvae to the recovered nematode populations from the different tree parts displayed a similar pattern among sampling locations. Significant mortality of G. mellonella larvae was found, from 40-70% (Fig. 4). However, there were no clear differences between sample sources. Nematode persistence (Fig. 3) and pathogenesis (Fig. 4) were also recorded 45 DAA, and at a lower level 180 DAA, in the soil samples surrounding the tree.
Discussion
The cultivation environment of P. dactylifera date palms is characterised by extreme high temperature, low humidity and high solar radiation, which are considered unfavourable for EPN persistence (Glazer, 2001; Ramakrishnan et al., 2022). Nevertheless, natural populations of EPN have been isolated from arid and semiarid zones (Glazer et al., 1993; Glazer, 2001). In agroecosystems, these biological control agents are mainly applied against the developmental stages of insects that inhabit the soil or plant-growing substrates. However, in the case of some foliage pests that are highly susceptible to EPN infection, such as the codling moth (Cydia pomonella) and the European corn borer (Ostrina nubilalis), the nematodes are applied directly on the plant surface. Their persistence and efficacy have been attributed to survival in cryptic habitats on the plant (Glazer, 1992). As for the RPW, application of EPN on Canary palm crown reduced the damage caused by this pest and protected the infected trees (Saleh & Alheji, 2003; Dembilio et al., 2010; Atakan et al., 2012; Manachini et al., 2013). Other studies (Atwa & Hegazi, 2014; Rehman & Mamoon-ur-Rashid, 2022), using holes drilled in the date palm trunk to inject nematode suspension into the RPW tunnels inside the trunk, showed sufficient control of the pest. In the present study, we found EPN persistence following spray application in all date palm sampling sites: trunk base, internal trunk tissues, offshoots and crown tissues. As in the case of the aforementioned borer pests, the present findings can also be attributed to the protective characteristic of the tree crown as well as other parts of the tree, such as the dense fibres covering the date palm trunk and the RPW tunnels within it. These findings agree with previous studies by Santhi et al. (2015, 2016) who demonstrated active attraction of EPN to RPW larvae and adults in an artificial trunk-mimicking substrate. Furthermore, Santhi et al. (2020) followed the response of S. carpocapsae IJ to RPW larvae and found that the EPN’s seeking behaviour is affected by cues produced by the host R. ferrugineus, supporting the idea of active searching in the fibre-covered trunk as a method for EPN IJ penetration. Our results suggest that nematodes survive in the cryptic and moist niches in the different tree sections. Differences in nematode presence in tissue samples were not supported by the observed characteristics of the individual palms or environmental factors. It is possible that our sampling did not sufficiently represent nematode distribution within the studied trees. In addition, this observation may be the result of biological processes such as the RPW-EPN dynamics in the tree environment, which we cannot elaborate upon in this study.
In the course of the experiment and the tree dissections, dead RPW larvae and pupae were occasionally found. In most cases, IJ emerged from the cadavers after incubation for 7 days. Although the present study was not aimed at determining efficacy, these findings confirm the ability of S. carpocapsae IJ to follow RPW signals, penetrate the trunk and infect their host. Furthermore, we detected S. carpocapsae nematode activity in soil samples near treated trees 180 DAA, showing promising tolerance to this environment. This is probably because the soil environment is kept moist by weekly irrigation of the trees.
The present study demonstrates, for the first time, the location and persistence of applied EPN in different parts of the date palm tree over extended periods. The internal structure of the date palm trunk and crown may have provided a protective environment for the S. carpocapsae IJ. The sandy soil at the trial site, with its continuous moisture, also provided suitable conditions for nematode persistence. This can be advantageous when RPW adults use the trunk base surrounding environment to estivate.
These convincing outcomes encourage the potential use of EPN (e.g., S. carpocapsae) as biocontrol agents for R. ferrugineus in P. dactylifera date palm plantations. A simple spray application was sufficient for the EPN to follow their host into the cryptic parts of the date palm. Further study needs to be undertaken to develop commercial practice and management based on pest activity and the required density of the EPN agent.
Acknowledgements
We would like to express our gratitude to Zvi Mendel for providing significant feedback on the initial version of the manuscript. We also thank Dana Ment for contributing graphics and providing editorial support. Additionally, we would like to acknowledge the journal editor and anonymous reviewers for taking the time and effort to review the manuscript. We appreciate all the insightful comments and suggestions that helped enhance the quality of the manuscript.
Corresponding author, e-mail: yaacobig@gmail.com
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