Haplaxius crudus
(American palm cixiid)

Haplaxius crudus, commonly known as American palm cixiid, is native to the American tropics and subtropics. The species was first described from Jamaica in 1907 and is currently known from northern South America, Central America, certain islands of the Caribbean, and Florida and southern Texas in the USA. The adults of H. crudus feed mainly on palms, particularly coconut palms, while the nymphs feed mainly on grasses. The main economic impact of H. crudus is as a vector of coconut (or palm) lethal yellowing (LY) caused by Candidatus Phytoplasma palmae, a highly destructive disease that affects at least 37 species of palms, including coconut palm (Cocos nucifera) and date palm (Phoenix dactylifera). Control of LY is best achieved by the planting of resistant cultivars integrated with cultural measures such as ground cover management because chemical control of H. crudus is not practical. International trade in palms from LY-infected areas is prohibited because of the threat of the disease and vector spreading not only to coconuts and date palms, but also to palms that are important as ornamental plants or as local sources of food or fibre.

H. crudus is native to the American tropics and subtropics, including Mexico, Florida (USA), Belize (Kramer, 1979), Cayman Islands (Fennah, 1971), Costa Rica (Kramer, 1979), Cuba (Osborn, 1926), Jamaica (Van Duzee, 1907), Panama (Kramer, 1979) and Trinidad and Tobago (Kramer, 1979).

It has spread as an introduced species to Texas (USA) (Carriere, 1982; Meyerdirk and Hart, 1982), Bahamas (Tsai, 2005), Haiti (Tsai 2005) and Puerto Rico (Segarra-Carmona et al., 2013).

H. crudus is a vector of lethal yellowing (LY) disease, howeverthe current geographical distribution of H. crudus seems to be more limited than that of LY; this may be because the insect has not yet been recorded in areas where the disease is present or because another vector exists. Most of the transmission experiments have been conducted in Florida, USA, and no evidence has been found for additional species of insect vectors of LY there or elsewhere. However, as there are more species of auchenorrhynchous insects on palms in tropical America than in Florida, and little is known about the biology of most of these species, it is possible that other vectors of LY may occur (Howard, 2015).

The most likely way H. crudus could be spread is by the international trade of plant material (Smith, 1997).

H. crudus can be found whever there are suitable palms and grasses for the nymphs (S Halbert, Florida Department of Agriculture and Consumer Services, USA, personal communication, 2016). See Hosts/Species Affected.

The adults of H. crudus feed predominantly on the phloem in the foliage of various species of palm trees (Arecaceae). The major host of H. crudus adults is coconut palm (Cocos nucifera). H. crudus is also very common on Sabal palm (Sabal palmetto)which might be the original host (S Halbert, Florida Department of Agriculture and Consumer Service, USA, personal communication, 2016). Minor hosts include Pritchardia spp. including Fiji fan palm (Pritchardia pacifica), Thurston palm (Pritchardia thurstonii), date palm (Phoenix dactylifera), Canary Island date palm (Phoenix canariensis), windmill palm (Trachycarpusfortunei), Manila palm (Veitchia merrillii) and Washingtonia spp. including Mexican fan palm (Washingtonia robusta) (Meyerdirk and Hart, 1982; Howard et al., 1983, 1984b; Howard and Wilson, 2001; Howard, 2015). In southern Florida, USA, where palm trees are grown as ornamental plants, the insect is found on both native and exotic species (Howard and Mead, 1980) although it is rare on some palm species, including Cuban royal palm (Roystonea regia) and yellow-cane palm (Dypsis lutescens) (Howard and Wilson, 2001; Howard, 2015). Adults also feed on grasses, for example St Augustine grass (Stenotaphrum secundatum), bahiagrass (Paspalum notatum) and Bermudagrass (Cynodon dactylon) (Reinert, 1977, 1980; Howard and Wilson, 2001) and weeping lovegrass (Eragrostis curvula) (Wilson and Wheeler, 2010), and have been observed occasionally on sugarcane (Howard and Wilson, 2001). Many continuous generations have been reared in the laboratory on St Augustine grass (Tsai et al., 1976). Adults have been observed to visit other monocotyledonous plants besides palms and grasses, e.g. common screw-pine (Pandanus utilis) (Pandanaceae) and macawflower (Heliconia bihai) (Heliconiaceae) (Howard and Wilson, 2001). Very occasionally adults have been observed on dicotyledonous shrubs but such cases are rare and they may be vagrants from nearby palm trees (Howard, 1999; Howard and Wilson, 2001).

The nymphs are subterranean and develop on the roots of certain species of grasses (Poaceae) and a few species of sedges (Cyperaceae) growing in the vicinity of palms. Their hosts include grasses cultivated as turf or forage, particularly St Augustine grass (Stenotaphrum secundatum), but also other species such as West Indian foxtail grass (Andropogon bicornis), broomsedge (Andropogon virginicus), bufflegrass (Cenchrus ciliaris), swollen fingergrass (Chloris barbata), Bermudagrass (Cynodon dactylon), African Bermudagrass (Cynodon nlemfuensis), Cyperus spp. including yellow nutsedge (Cyperus esculentus), digitgrass (Digitaria eriantha), salt grass (Distichlis spicata), centipedegrass (Eremochloa ophiuroides), pinewoods fingergrass (Eustachys petraea), hurricane grass (Fimbristylis cymosa), Guinea grass (Panicum maximum), fall panic grass (Panicum bartowense), bahiagrass (Paspalum notatum), paragrass (Panicum purpurascens), foxtail (Setaria spp.) and Zoisia [Zoysia] sp. (Tsai and Kirsch, 1978; Howard and Wilson, 2001; Molet, 2013). Other grass species are less favourable for development or are non-hosts (Howard, 2015). Nymphs have also been observed feeding on the roots of sandpaper vervain (Verbena scabra) (family Verbenaceae) (Tsai and Kirsch, 1978).

Reproductive Biology

H. crudus is heterovoltine, the number of generations being affected by temperature (Halbert et al., 2014). Reproduction occurs throughout the year (Smith, 1997). Parthenogenic reproduction has not been observed (Tsai and Kirsch, 1978). The female:male ratio has been reported as 1:1 by Tsai and Kirsch (1978) and 1.7:1 by Reinert (1980), although the ratio may be skewed because females tend to live longer than males (Howard, 1987).

Mating occurs on the palms and the females return to grasses to lay eggs. It is not known if mating also occurs on grasses (Howard and Wilson, 2001).

Eggs are laid singly or in rows of up to five eggs on the lower fronds of grasses, near to the root collar (Howard and Wilson, 2001). Eggs are white and a mean of 0.54 mm long and 0.17 mm wide, with the anterior end asymmetrical and pointed and the posterior end rounded (Wilson and Tsai, 1982).

Physiology and Phenology

Two population peaks of H. crudus were observed in southeastern Florida: one in March-May and the other in June-August (Tsai and Kirsch, 1978). In studies using rotary flight traps to sample flying insects around the groves of coconut palms in southern Florida, H. crudus was trapped throughout the year, with peak flight activity in March, May, September and November (Woodiel and Tsai, 1978). Halbert et al. (2014) saw increased activity of H. crudus in the winter in Florida, USA - H. crudus can overwinter consistently as far north as Gainesville.

There are five nymphal instars, with a mean length of 0.64, 1.01, 1.29, 2.20 and 2.68 mm for the 1st to 5th instar, respectively (Wilson and Tsai, 1982).

The nymphs secrete a cottony wax material from abdominal glands, which helps to protect them from moisture, disease and predators. They form the cottony wax material to make a ‘nest’, in which they live, usually in groups of 2-10 individuals (Tsai and Kirsch, 1978). When disturbed, nymphs become active and can jump about 5-10 cm (Howard and Wilson, 2001).

Longevity

In laboratory studies the mean life span on St Augustine grass (Stenotaphrum secundatum) at 24°C was 7.3 days for males and 7.8 days for females. The mean generation time was 52.6 days at 30°C and 80.8 days at 24°C. Adult longevity was longer on Veitchia merrillii (maximum of 50 days) than on coconut palm (Cocos nucifera) (maximum of 37 days) (Tsai and Kirsch, 1978).

Activity Patterns

The adults are active during the day and night, although more adults are captured during the day (Howard, 1981).

Feeding Behaviour

Mature adults fly to palm foliage and feed by penetrating the tissue of the frond with their stylet and sucking the phloem (Tsai and Fisher, 1993; Howard and Wilson, 2001). They feed on the undersides of leaves or in partly concealed portions of the plant (Kramer, 1979).

Environmental Requirements

H. crudus is not cold hardy, and nymphs reared at 15°C failed to moult to adults (Tsai and Kirsch, 1978), indicating that its distribution will be limited by low temperatures. Tsai and Kirsch (1978) reported that the insect does not occur north of 30° N latitude, although H. crudus has been recorded overwintering as far north as Gainesville in northern Florida, USA (29.63380° N, 82.37200° W), even in cold winters (Halbert et al., 2014).

After hatching the nymphs move down to the soil surface and develop in the root zone of grasses, often beneath small clumps of leaf litter and other organic matter. Larvae have been reported at soil depths up to 20 cm (Howard and Wilson, 2001). Moist sites and longer grasses are favoured over drier sites and short-cut grasses (Howard, 2015).

Natural Dispersal

Natural dispersal of the insect is by flight between host plants and wind dispersal.

Pathogen Transmission

The main economic impact of H. crudus is as a vector of coconut (or palm) lethal yellowing (LY). LY is caused by the phytoplasma Candidatus Phytoplasma palmae, which is transmitted to palms in a circulative-propagative manner by H. crudus (Harrison and Oropeza, 2008; Harrison and Elliott, 2015). H. crudus is considered to be an inefficient vector of LY but is sufficiently abundant to spread the disease (Purcell, 1985 in Smith, 1997). It was thought that absence of the vector in northern areas of Florida set the northern limit on the occurrence of LY (Smith, 1997), but recent observations by Halbert et al. (2014) indicate that probably it is the lack of cold hardiness of the LY phytoplasmas that set a northern limit for lethal yellowing.

H. crudus may also be a vector of Texas Phoenix palm decline (TPPD) but the vector could be a derbid. TPPD is more cold tolerant and is spreading in Gainesville, Florida, USA (S Halbert, Florida Department of Agriculture and Consumer Services, USA, personal communication, 2016).

Few natural enemies have been recorded for H. crudus. Spiders have been observed preying on adults in the palm canopy in Florida (Tsai and Kirsch, 1978). In field observations in south-eastern Florida 250 individuals of web-building spiders were collected from 40 coconut palms. The most abundant species was Theridion melanostictum (Theridiidae) (84.4%) followed by T. adamsoni (8.4%), both of which are thought to have been introduced only recently into Florida. H. crudus was the most commonly identified arthropod in the web contents of both species (Howard and Edwards, 1984). Ants (Solenopsis invicta), lizards and tree frogs also prey on H. crudus (Howard, 1987).

Unidentified parasitic wasps have been reported attacking H. crudus in Mexico and Central America, and parasitic mites in the genera Leptus and Erythraeus have been observed infrequently in Mexico and Florida. The fungus Hirsutella citriformis has been recorded infecting adults of H. crudus in Florida, and a related or possibly the same species attacks the insect in Trinidad and Mexico (Howard, 1987; Howard and Wilson, 2001).

No pheromones have been discovered for H. crudus (Molet, 2013). The species has been monitored using visual inspections (e.g. Tsai and Kirsch, 1978), use of adhesive (Tanglefoot^®) applied to the surface of the palm foliage (Howard and Hutchinson, 1977), sweep net sampling (Reinert, 1980; Molet, 2013), rotary flight traps (Woodiel and Tsai, 1978; Tsai and Mead, 1982) and sticky traps (Cherry and Howard, 1984).

A rotary flight trap was successful in sampling flying insects associated with coconut palms in southern Florida. The trap consisted of a triangular unit supporting a boom and net assembly, which was powered by an electric motor. Nearly 90% of the total leafhoppers and planthoppers trapped in the nets at each sampling site were H. crudus, and they were trapped all year round (Woodiel and Tsai, 1978).

In field studies in coconut palms in Florida, the effectiveness of coloured sticky traps in capturing H. crudus was evaluated. The traps were plastic discs (15.7 cm in diameter) covered with adhesive (Tree Tanglefoot^®) and hung by wire under fronds on coconut palms. Blue and white sticky traps captured more adults of H. crudus than any other colour of sticky trap tested (yellow, red, orange, green, brown and black). Significantly more adults were captured in blue sticky traps during the day than during the night. The blue traps also caught significantly more males than expected when compared with field populations on adjacent palms. The use of blue traps was more effective for sampling adults of H. crudus than the application of adhesive to palm trees (Cherry and Howard, 1984). It was later discovered that the blue and white paints used on the sticky traps had higher concentrations of titanium dioxide than the other paints tested, making them more reflective of ultraviolet light and thus more attractive to H. crudus (Howard and Wilson, 2001).

H. crudus is one of the few species in the subfamily Fulgoroidea and the only species of the family Cixiidae commonly found on palm foliage in southern Florida and the Caribbean region, aiding its identification in the field. Other fulgoroids include Ormenaria rufifascia and several derbids.

New World species of Haplaxius can be distinguished primarily on the basis of structural modifications of the male genitalia, especially the aedeagus. Keys to males of the genus are provided in Kramer (1979).

H. crudus may be confused in the field with several species of Derbidae: Cedusa spp., Omolicna spp., and Patara albida. In contrast to H. crudus the derbids have a short apical segment on the rostrum (Redford et al., 2010; Molet, 2013). Ormenaria rufifascia is much larger than H. crudus and thus is unlikely to be confused with it. A cixiid species in the Melanoliarus genus has also been reported on palms in Texas (S Halbert, Florida Department of Agriculture and Consumer Services, USA, personal communication, 2016).

Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.

Prevention

Containment/zoning

The most likely way the vector or pathogen could be spread is by the international trade of plant material (Smith, 1997). Because the disease is difficult to diagnose and has a long incubation period, the importation of palms from countries where LY is present is prohibited. Vigilance is essential to prevent the disease from being introduced to tropical and subtropical countries and islands where coconut palm populations could be decimated.

Date palm (Phoenix dactylifera) is the most important economic crop at risk from LY disease in the EPPO region. Although H. crudus is an inefficient vector of LY and is unlikely to survive in southern Europe, it is possible that existing species of Auchenorrhyncha on palms in the EPPO region may become vectors of LY if the disease was accidentally introduced to that region. Moreover, Europe is an important producer of plant material that is exported around the world, increasing the risk of the disease being spread to more susceptible areas (Smith, 1997).

It is also important that ornamental palms are not moved from infested areas because of the risk of spreading the disease not only to coconuts and date palms but also to valuable protected and outside plantings of ornamental palms (Smith, 1997).

Control

Cultural control

Control is best achieved by integrating the planting of resistant species or cultivars of palms with cultural measures such as ground cover management. Coconut cultivars ‘Panama Tall’ and ‘Malayan Dwarf’ selections and their hybrid ‘MayPan’ (‘Malayan Dwarf’ × ‘Panama Tall’) have shown resistance (Howard and Wilson, 2001; Harrison and Elliott, 2008). However, the long-term resistance of these cultivars is now in doubt because of recent reports of heavy losses due to LY in ‘Malayan Dwarf’ and ‘MayPan’ in some areas of south-eastern Florida (Broschat et al., 2002) and Jamaica (Lebrun et al., 2008).

LY has not been reported on most palm species that are native to Florida (USA) and the Caribbean Basin, including Paurotis (or Everglades) palm (Acoelorrhaphe wrightii), royal palm (Roystonea regia), cabbage palm (Sabal palmetto) and species of thatch palms (Thrinax spp.), and these may provide alternatives to susceptible species in ornamental plantings (Harrison and Elliott, 2008). However, there is uncertainty surrounding LY resistance of native species in these areas now that TPPD is present: Sabal palmetto is highly susceptible; Roystonea is susceptible to a D strain phytoplasma in Puerto Rico; Washingtonia also might get TPPD (S Halbert, Florida Department of Agriculture and Consumer Services, USA, personal communication, 2016).

In addition, some exotic species used as ornamental trees in Florida, for example Archontophoenix alexandrae, Carpentaria acuminata, Dypsis lutescens, Ptychosperma elegans, Ptychosperma macarthurii, Washingtoniarobusta and Wodyetia bifurcate, are not susceptible to LY and are suitable for use in landscaping in areas where the disease is a threat (Howard and Wilson, 2001).

Research in cultural control measures against H. crudus aims to identify grass or dicotyledonous ground covers in coconut plantations that inhibit the development of the immature stages of the insect or that are non-hosts (Howard, 1999). In laboratory and field studies in Florida, the grasses Brachiaria brizantha, B. dictyoneura, B. humidicola, Chloris gayana, Hemarthria altissima, Hyparrhenia rufa, Pennisetum purpureum and a variety of sugarcane were found to be poor hosts and may have potential as ground cover in coconut plantations to reduce the spread of LY (Howard et al., 1990a,b; Howard and Wilson, 2001). Dicotyledonous plants, such as the legumes Arachis pintoi and Pueraria phaseoloides, which are non-hosts of larvae of H. crudus, may also be used as ground cover in coconut plantations to reduce the population of H. crudus (Howard, 1999; Howard and Wilson, 2001). Research in Jamaica, however, has shown the presence of the lethal yellowing group (16SrIV) of phytoplasmas in some species of dictotyledonous weeds, suggesting that weed control in and around coconuts may assist in the management of LY (Brown et al., 2008a,b; Brown and McLaughlin, 2011).

Certain types of organic mulches have been shown to enhance nymphal development of H. crudus, possibly by providing shelter. Field studies in Florida showed that more adults emerged from coconut plots with St Augustine grass as ground cover when mulched with coconut frond mulch or with eucalyptus or pine bark mulch than from control plots with no mulches. Fewer adults emerged from plots mulched with coarse materials such as pine bark nuggets (Howard and Oropeza, 1998).

Chemical control

Insecticide treatments of palms and grasses have been used as quarantine treatments in an attempt to prevent H. crudus from being transported to new localities (Howard, 2015).

Although chemical control of the vector H. crudus has been shown to be effective and is likely to limit the spread of LY, it is not a practical means of managing the insect because repeated applications of insecticides would be required, which would be costly and environmental damaging (Reinert, 1977; Ennis, 1982; Howard, 1987, 2015). Treatment of LY-infected plants by injection into the trunk of the antibiotic oxytetracycline hydrochloride (OTC) every 4 months has been shown to suppress the symptoms of the disease (McCoy, 1975, 1982; Harrison and Elliott, 2015).

Biological control

The prospects for controlling LY via biological control of the vector are not promising. Although several natural enemies have been identified, they do not appear to reduce the populations of this insect sufficiently where they occur naturally to reduce the spread of LY (Howard, 2015).

03/02/2016 Original text by:

Angela Whittaker, Consultant, UK