The coconut rhinoceros beetle (CRB), Oryctes rhinoceros Linnaeus (Coleoptera: Scarabaeidae) is one of the most destructive insect pests of coconut and oil palms (Bedford 2013a). It is native to South and Southeast Asia, where economic losses are estimated to be at around 10% in both India (coconut: ∼ 159.4 million US$) and Indonesia (coconut: ∼ 299.3 million US$), and 25% in Malaysia (oil palm: ∼ 2,853.7 million US$) (Catley 1969, Manjeri et al. 2014, Fauzana et al. 2018, FAOSTAT 2020). The pest was inadvertently introduced into the Pacific in 1909 (Bedford 1980). CRB then spread rapidly throughout Pacific island nations and territories (Fig. 1) and became a major economic threat. In its invaded range, damage from CRB attack can be severe with tree mortality reaching 50–100% (Gressitt 1953, Manjeri et al. 2014). The economic damage from CRB in South Pacific territories in 1968 was estimated to be over one million USD (Catley 1969). Coconut and oil palms are widely cultivated commodities in these areas, with significant contributions toward livelihoods for small holder farmers (Young 1986, Bennett 2020).

The scattered nature of CRB outbreaks and its comparatively low density, in combination with the often-low commercial value of coconuts, have made self-replicating and self-dispersing biological control agents (BCAs) the most feasible option for control of the beetle (Young 1986). Natural enemies of CRB were either introduced from the pest's native range into the invaded range (classical biological control) or the performance of those natural enemies already present in an affected area were improved by augmentation, manipulation, or other means. The first attempts at biological control, with introduction of exotic Metarhizium Sorokin (Hypocreales: Clavicipitaceae) spores, were carried out by Friederichs (1913) and followed intermittently with introductions of BCAs collected from many parts of the world (Surany 1960, Swan 1974, Waterhouse and Norris 1987); mostly organized through the South Pacific Commission (SPC). A major program for control of CRB, with introduction and testing of BCAs, was initiated by United Nations Development Program (UNDP)/SPC in 1965 (Young 1986). The discovery and introduction of a viral pathogen, Oryctes rhinoceros nudivirus Huger (OrNV; formerly Rhabdovirus oryctes and Baculovirus oryctes) not only reduced CRB populations and associated damage effectively but also prevented further spread for more than 30 yr (Huger 2005, Bedford 2014, Marshall et al. 2017).

Fig. 1.

Invasion history and distribution of CRB (Oryctes rhinoceros) in the Pacific. Green indicates the native range whereas invaded range is indicated by orange (redrawn from Catley 1969).

A new wave of CRB invasion into previously CRB free countries and territories was first noted from Guam in 2007, followed by mainland Papua New Guinea (PNG) in 2009, Hawaii in 2013, Solomon Islands in 2015, and New Caledonia in 2019. This has rejuvenated interest in the pest (Mankin and Moore 2010, Ero et al. 2016, Adams 2019, Benedict 2019). The CRB populations in these outbreaks can be distinguished genetically from CRB of the earlier waves of invasion (herein referred to as CRB-S) by a variation in the CO1 gene and were categorized as a new CRB biotype, CRB-G, based on apparent tolerance to commonly used isolates of OrNV (Marshall et al. 2017, Reil et al. 2018). Biotype is used to define a subgroup that is distinct in terms of functional traits such as pathogen resistance or host preference within a wider group of similar genetic composition and morphology (Diehl and Bush 1984). Tolerance of the CRB-G biotype to commonly used isolates of OrNV circulating within the Pacific region is presumed to be one of the phenotypic factors facilitating the rapid expansion and recent invasion wave into the Pacific Island countries and territories (Marshall et al. 2017, Reil et al. 2018).

During the last decade, CRB has spread at a rate of approximately one new island state every 2 yr, threatening food security and livelihoods for millions of small holder farmers in the region (Ero et al. 2016, Marshall et al. 2017, Benedict 2019). In 2014, a live CRB adult was also intercepted in Mexico with a palm furniture shipment from Indonesia, demonstrating that the pest could pose a threat to Central and South America (Jimenéz Quiroz et al. 2017). The new CRB biotype, CRB-G, has already caused catastrophic damage to coconut palms in the invaded areas (Marshall et al. 2017). Two years post-invasion (2015–2017), 70% of the palms in Honiara, Solomon Islands were severely damaged or dead, posing a significant threat to the country's 17 million USD coconut industry (∼12% of GDP) and food security of more than 40,000 rural households (Vaqalo et al. 2017, Tsatsia et al. 2018). In addition to the production and economic losses, the aesthetic value of tourism locations like Guam and Hawaii are lost due to damage to ornamental palms (Smith and Moore 2008).

CRB adult females lay eggs in standing palms, empty fruit bunches or decomposed stumps where the larvae develop (Bedford 1976, 1980). Adults bore holes into palm crowns and damage developing fronds, resulting in truncated or distorted leaves, often displaying a distinctive ‘notched’ appearance (Fig. 2). CRB damage can predispose palms to subsequent attack by different insects (e.g., palm weevils) and diseases (e.g., bud rot, leaf rot). Excessive feeding damage may also eventually result in tree mortality. The preferred hosts of CRB are coconut palms (Cocos nucifera Linnaeus) and oil palms (Elaeis guineensis Jacquin), but they are recorded to attack more than 30 different genera of plants, including sugarcane, pineapple, pandanus, banana, taro, cycads, and agaves (Gressitt 1953, Bedford 1980, Izaitul Aida et al. 2020, Marler et al. 2020). CRB populations in their native range are controlled by various biotic factors including predators, parasitoids and diseases (e.g., viral, fungal), but it becomes a major threat when introduced to new areas due to a lack of natural enemies to limit population growth (Gressitt 1953). The biology and ecology of CRB are covered in detail in several previous reports (Young 1975, Bedford 1980, Pallipparambil 2014).

Fig. 2.

Characteristic damage to coconut palm fronds caused by adult CRB (Oryctes rhinoceros). Inset (lower left) shows the adult.

In this review, we provide a global overview of the status, use and effectiveness of exotic and indigenous natural enemies (predators, parasitoids, and pathogens) against CRB in both native and invaded areas and identify some of the major successes and failures from the past. A critical assessment of the past claims on BCAs against a current view of potential effectiveness and appropriateness is provided. The emerging threat of CRB-G in the Pacific region is also discussed with future potential of BCAs to limit the spread and associated palm damage from this pest. While there are several complementary integrated pest management (IPM) strategies (e.g., sanitation, pheromone trapping, and insecticides) that are effective against CRB, this review is solely focused on biological control. IPM strategies for CRB in coconut and oil palm have been reviewed elsewhere (Bedford 1980, 2014; Manjeri et al. 2014; Pallipparambil 2014).

Natural Enemies of CRB in Its Native Range

The intransigence of the CRB problem in the Pacific islands and the dominance of the biological control paradigm led to numerous searches, collections, and tests for biological control agents for CRB, which are summarized by Gressitt (1953), Surany (1960), Hoyt and Catley (1967), Manjunath et al. 1969, Swan (1974), and Waterhouse and Norris (1987). Eighty species are reported as putative natural enemies of CRB (predators: 48, parasitoids: 12, pathogens: 18, ectoparasites: 2) from various areas within South and Southeast Asia, Africa, Oceania, North and South America and Europe ( Supp Table S1 [online only]). The majority of these natural enemies (≈75%) were reported from the native range of South and Southeast Asia. A brief overview of major natural enemies from the native range is given below.

Classical Biological Control of CRB: Successes and Failures

Classical biological control is the introduction of co-evolved natural enemies (parasitoids, predators, and pathogens) from the pest's native range to manage invasive pests of exotic origin (Lockwood 1993). Classical biological control has been most successful when the pest and its natural enemy have a close ecological relationship, such that the natural enemy is a specialist on the target pest (Hoddle 2002). There were widespread efforts during the 1950s and 1960s to introduce BCAs from Southeast Asia, Africa, Europe, New Zealand, and the United States of America into the South Pacific Islands against CRB ( Supp Table S1 [online only]). Some of the major introduced biocontrol agents, including predators, parasitoids, and entomopathogens, are described below and the reasons for their success or failure to control CRB are considered.

Augmentative Biological Control For CRB

Augmentative biological control aims to increase populations of existing natural enemies through deliberate releases to successfully manage insect pests (Collier and Van Steenwyk 2004). Augmentative releases of entomopathogens have been tested widely and used to manage CRB in its native range. In Southeast Asia, incorporation of the Metarhizium fungus into breeding sites (e.g., compost heaps) is a popular method (Ramle and Norman 2014, Chandrika et al. 2016, Indriyanti et al. 2017a). The process is relatively cost effective and provides adequate control in some instances. In Malaysia, M. majus conidia produced 37% CRB larval mortality within 3 mo when sporulated maize substrates were applied to breeding sites (Ramle et al. 1999). Conidia suspensions obtained after washing the sporulated substrate were also drenched in oil palm replanting areas; a single application of 5 × 10⁸ conidia/ m² resulted in 51% CRB larval mortality and was found comparatively more effective and economical than broadcasting sporulated substrates (Ramle et al. 1999). Treatment of vermicompost sites in India with M. majus spores produced in coconut water (10⁸ spores/ mL) successfully reduced CRB larval populations by 72% compared to the control (Gopal et al. 2006). In Thailand, treatment of empty oil palm fruit bunches with M. guizhouense resulted in mortality of first-, second-, and third-instar CRB by 93%, 96%, and 76%, respectively after 35 d under field conditions (Pansuwan et al. 2019).

Conidia formulations have been developed and evaluated under laboratory and field conditions against CRB larvae and adults with mortality rates reported between 40 and 100% (Ramle et al. 2006, Ramle et al. 2007, Ramle et al. 2013, Chandrika et al. 2016, Mohd et al. 2016, Indriyanti et al. 2017b). Formulations have been developed as wettable powders (WP), with the most common composition being a mixture of dried conidia and kaolin (20:80) (Hamid et al. 2005, Ramle et al. 2006, Ramle et al. 2007, Indriyanti et al. 2017b). In India, fresh conidial suspensions (TCS) and powder-based formulations (PBF) of M. majus resulted in 85–90% mortality of third-instar CRB larvae within 2 wk (Velavan et al. 2017). Similarly, the treatment of rotting oil palm debris with M. majus based formulations (WP) that were reconstituted in water reduced larval populations by 80% in Malaysia (Ramle et al. 2006).

Direct treatment of breeding sites (decomposing trunks or manure/compost heaps) with the Metarhizium fungus is considered an efficient strategy against CRB in the field (Ramle et al. 2006, Mohan et al. 2010). Notably, the fungal spores in the breeding sites are reported to survive up to 24 mo postapplication under ideal conditions (Latch and Falloon 1976). Artificial breeding sites (ABS: a trough with logs of trunk and decomposing chipped mature palms) treated with Metarhizium are also used to infect and disseminate the fungus and control CRB by attracting the beetles with pheromone traps toward decomposed materials that act as breeding habitat (Ramle et al. 2013). The CRB adults are strong fliers, therefore, the concept is that infected beetles can quickly disperse and distribute conidia to other breeding and feeding sites. In Malaysia, 43% of the CRB populations were infected with the fungus in plots with ABS compared to 32% infection from random field spraying (Ramle et al. 2013). In Thailand, pellet formulations of M. anisopliae Sorokin resulted in 87% CRB larval infection when applied to ABS (Popoonsak et al. 2018).

Despite its potential, widespread use of Metarhizium fungus against CRB has had some challenges (Surany 1960, Bedford 1980). The fungus requires a specific temperature range of between 28°C and 32°C and humidity above 80% to be effective (Mohan et al. 2010). Spore formulation and mycelial growth of a local Sri Lankan isolate of M. anisopliae was negatively affected at a higher temperature of 32.5°C (Subhathma et al. 2013). In Kerala, India, natural infection rates from the fungus are much higher during the rainy season due to high humidity (Gopal et al. 2002). Therefore, the use of the fungus in countries or seasons with relatively less rainfall and higher temperatures is not optimal (Indriyanti et al. 2017b). It is also important to note that heavy rainfall reduces dissemination of the fungus and consequently lowers CRB mortality rates (Indriyanti et al. 2017b). Due to these factors, Metarhizium fungus requires repeated applications leading to increased costs of labor and materials (Vargo 1995, Gopal et al. 2002). The shelf life of fungus sporulated substrates and fresh conidia suspensions is limited, and requires refrigerated storage, which increases the storage cost (Ramle et al. 2013). However, conidia viability can be extended by using proper formulations (e.g., kaolin-based) under suitable temperatures (Hamid et al. 2005).

Entomopathogenic bacteria, nematodes, and viruses have also been tested for augmentative release against CRB. Two bacterial pathogens, B. thuringiensis Berliner (Bacillales: Bacillaceae) and P. popilliae produced 100% mortality in CRB larvae within 3–4 wk in India (Babu et al. 1971). In Malaysia, bacterial pathogens (B. thuringiensis and P. popilliae) in combination with OrNV and Metarhizium sp. produced 88% mortality of third instar CRB larvae (Kamarudin et al. 2007). Two indigenous strains of nematodes from India, S. carpocapsae and H. indica, significantly increased larval mortality in neonates and third-instar larvae in compost heaps (Patil et al. 2014). Heterorhabditis sp. (commercial pesticide, Coleonema) produced 100% mortality 8 wk postapplication in Indonesia, while it only took 5 wk when the nematodes were used in combination with the fungus, M. anisopliae, suggesting a synergistic interaction between BCAs (Indriyanti et al. 2018). A list of commercially available biopesticides from Asia for CRB management is provided in Table 1. Most of them are based on Metarhizium, while a few have B. bassiana and Heterorhabditis sp. as the active ingredients. Novel isolates should be rigorously tested to ensure efficacy before application in widespread control programs.

Table 1.

Details of commercially available biopesticides for CRB management in Asia

Inundative releases of OrNV were successful in several Southeast Asian countries, resulting in significant reduction of CRB populations. In India, the release of OrNV-infected beetles reduced spear damage in oil palms from 71 to 21% (Dhileepan 1994), and frond damage in coconut palms from 34 to 7% (Babjan et al. 1995). Release of OrNV in the Philippines reduced the CRB population by 10–20% compared to preinoculation levels (Zelazny and Alfiler 1987, Zelazny and Alfiler 1991). Similarly, the proportion of infected beetles increased by 35–90% 3 mo postrelease of OrNV in Malaysia (Ramle et al. 2005).

Managing the New Wave of CRB Invasion Using BCAs: Future Perspectives

In the last decade, the new wave of CRB invasion has emerged as one of the major challenges of palm trees in Pacific island countries and territories (Marshall et al. 2017, Tsatsia et al. 2018). Central to the resurgence is the new biotype, CRB-G, which is tolerant to the OrNV isolates commonly used for biological control. Geographical variations in OrNV virulence and genetic diversity, however, are not new. Infection periods and mortality rates of CRB larvae differed after infection with OrNV isolates from the Philippines and Western Samoa (Zelazny 1977). Similarly, genetic variability of OrNV isolates sampled from different locations within Malaysia and Indonesia are also reported (Ramle et al. 2005, Rahayuwati et al. 2020). Therefore, improved understanding of interactions between CRB and entomopathogens (e.g., OrNV, Metarhizium) in different regions are especially important for development and implementation of targeted region-specific biological control programs.

Entomopathogens have proven effective against scarabs in general (Jackson and Klein 2006). Since OrNV and Metarhizium were the most successful BCAs in the past, variants of these entomopathogens are the most likely candidates to manage the new wave of CRB invasion in the Pacific region and beyond. Viewed through a modern lens, OrNV stands out as a suitable agent for classical biological control of CRB. It is comparatively host-specific and has a well-documented impact on the target pest (Huger 2005, Bedford 2013b). Despite tolerance to the standard OrNV biocontrol strains (Marshall et al 2017), some isolates of OrNV from the Philippines (imported through AgResearch, New Zealand) have produced promising results against CRB-G in Solomon Islands (Tsatsia et al. 2018). In Guam, various OrNV isolates (OrNV-X2B from Philippines, OrNV-I from India, OrNV-TAS and -TAP from Samoa, and OrNV-Ma1B from Malaysia) produced CRB adult mortality following hemocoelic injection, but statistically significant mortality was not observed through oral delivery (Marshall et al. 2017).

Most of the many other BCAs (predators, parasitoids, and pathogens) considered previously for classical biological control ( Supp Table S1 [online only]) were imported without consideration of the factors that have become standards of modern biological control: host specificity, climate matching, or significant impact on population suppression of the target pest (Hoddle 2002). Despite this, some did establish successfully ( Supp Table S1 [online only]). For example, predatory beetles, A. speciosus and L. fuscipes, that were imported into Western Samoa from the native CRB range, did establish successfully and preyed on CRB (Catley 1969). Similarly, establishment of P. laevicollis, and P. parvulus was also confirmed but their impacts are not known (Catley 1969, Swan 1974). The parasitic wasp, S. ruficornis, is reported to have established in several Pacific Island countries (Catley 1969, Swan 1974). These BCAs may be potential candidates for conservation or augmentative biological control. There are, however, no published studies since the mid-1970s that report the activity or impact of these agents on CRB and they are not commonly found in field sampling. Thorough assessments of these agents' geographic and habitat range, predation or parasitism rates, and their current contribution to CRB control are needed. Similarly, further investigation is needed to determine whether local predators and parasitoids, that were historically reported as enemies of CRB, are still contributing to population control. Without recent data, it is impossible to determine what impact these introduced agents and local natural enemies, both individually and in combination, now have on CRB populations. The rapid expansion of newly invasive populations in the Pacific does suggest that there is very little natural control. There may be potential to increase the impact of these BCAs through habitat manipulation or deliberate mass rearing and release. Their impacts could enhance the biological control provided by OrNV, or by new classical BCAs that may be introduced against CRB in future.

Failure of the majority of BCAs to either establish or reduce CRB populations does not mean that there are no other potential agents available within the native range of CRB. It is often noted that CRB damage is much worse in the invasive zones than within its native range, indicating suppression of the native populations by biotic factors (Gressitt 1953). The successful agent, OrNV, was isolated from diseased CRB larvae in Malaysia (Huger 2005), which is considered the center of origin for this pest. Scarab BCAs are often highly host specific (Jackson and Klein 2006), so care should be taken to search for new agents in the center of origin, not just of the species as a whole, but also of specific CRB biotypes. Scarabs are frequently resistant to commonly known generalist entomopathogens, but effective BCAs for the Scarabaeidae often show a high level of host specificity. This, coupled with a wide range of microbial agents from different classes for different species, suggests a high level of co-evolution between these pathogens and their scarab hosts (Jackson 1999). With modern developments in genetic screening and identification of potential pathogens, it is possible that new pathogens may be isolated and identified from CRB. Recently, a novel Picorna-like virus (OrPV1) was reported in CRB larvae collected from Taiwan. This novel virus shared some genetic identity with viruses infecting honeybees and Asian lady beetle (Etebari et al. 2020), but pathogenicity toward CRB has yet to be demonstrated for this novel virus. The picorna-like viruses are also reported from Helicoverpa armigera Hübner (HaNv), infecting gut tissues of both adults and larvae (Yang et al. 2019). Sequencing results from Hawaiian CRB specimens identified three contigs displaying similarity matches to genes from other insect associated DNA viruses (classified under the Baculoviridae, Entomopoxvirinae, and Genomoviridae families), which are known to be capable of infecting beetles and other insect species (Mitsuhashi et al. 2014, Adams 2019). Further details are needed to determine the potential suitability of these viruses, or others yet to be discovered, as possible classical BCAs: 1) to test their efficacy against CRB; 2) investigate their climatic range; and 3) to conduct host specificity tests with potential nontarget species. All these steps are best conducted initially in the native range of the potential agent. Only if the agent passes this initial screening, should it be considered for further testing under quarantine conditions in the proposed country or region of introduction. If quarantine facilities are not available in the region of introduction, collaboration with international partners may be needed to complete the risk assessment and provide sufficient information to determine the agent's suitability. Finally, the potential for competition between the new agent and other pre-existing control agents, particularly OrNV and Metarhizium, should be investigated before a new agent is released (Gopal and Gupta 2002, Kamarudin et al. 2007).

Based on current knowledge, biopesticides containing M. majus are the strongest candidate for augmentative biological control against the emerging CRB threat (Moore 2018). Three weeks postrelease of M. majus (imported from the Philippines), 10–38% of field collected CRB were infected with the fungus in Guam (Moore 2018). The fungus established successfully in the area but did not have sufficient impact to manage the CRB outbreak on its own. The potential effectiveness of M. majus (commercial product: Ory-X imported from Malaysia) against CRB was also reported from Solomon Islands (Fig. 3) (Tsatsia et al. 2018).

Investigation of local entomopathogens is warranted through collection of potentially infected CRB because there may be opportunities to enhance the activity of local species against CRB. In an experiment conducted in a research laboratory in Hawaii, more than 60% CRB mortality was recorded from five Metarhizium isolates collected from O'ahu, Hawaii (KO-001, KO-002, LA-016, LA-025, and LA-026) (Russo 2019). Similarly, a few local Heterorhabditis spp. from O'ahu, Hawaii also caused first-instar larval mortality after 2–7 d of exposure (Manandhar et al. 2020). While B. thuringiensis and P. popilliae have demonstrated some potential to infect CRB (Babu et al. 1971, Kamarudin et al. 2007), there are no suitable products available commercially (Table 1). Therefore, identifying local entomopathogenic species may provide opportunities to develop local industries that produce biopesticides. Several biopesticide products based on entomopathogenic fungi and nematodes are produced commercially in South and Southeast Asian countries (e.g., India, Indonesia, and Thailand) for CRB control (Table 1). It is vital that robust formulations, produced under strict quality control, are used to maintain the activity of the agent for distribution in tropical conditions.

Fig. 3.

Metarhizium majus sporulated CRB (Oryctes rhinoceros) larvae in a fungus propagation chamber in Solomon Islands.

In summary, ongoing research efforts are needed to design an effective biological control program against the emerging threat of newly invading CRB populations, such as CRB-G. A crucial part of this effort is to enhance existing biological control and to identify and evaluate potential new BCAs for CRB. Investigation of the native range of the invasive species, including specific biotypes, is a high priority in the search for candidate entomopathogens, or other natural enemies. The impact of local natural enemies and past biological control introductions also needs re-evaluation to determine what contribution, if any, these make to CRB control. It is important that BCAs are incorporated into IPM programs for CRB that include other complementary strategies that enhance CRB control, such as sanitation. It is preferable if these complementary strategies are feasible and cost-effective for resource-poor smallholder farmers, as well as commercial plantation operations. Collaboration among government, non-governmental organizations, local industries and farmers through awareness campaigns, field sanitation and biosecurity measures will be extremely important to limit further spread by CRB to new regions. Despite the recent expansion of its range in the Pacific, biological control remains central to effective management of CRB.

Supplementary Data

Supplementary data are available at Annals of the Entomological Society of America online.