Which Species of Coconut Moth Occurs in Brazil: Atheloca subrufella vs. Atheloca bondari (Lepidoptera: Pyralidae)?

The moths, Atheloca subrufella (Hulst 1887) and A. bondari, (Heinrich 1956) are species known for their economic impact on coconut production, which Brazil is the fourth largest global producer. The first record of Atheloca in Brazil was reported by Bondar in 1940, where the author registered it being A. subrufella. The studies performed by C. Heinrich in 1956 related the existence of divergence in specimens of Brazilian Atheloca suggesting the presence of morphological differences between the males of A. bondari and A. subrufella. In this study, Atheloca specimens from the five states of northeastern Brazil were used. Samples from Pernambuco state were sent to taxonomist Dr. V. O. Becker (Uiraçu Institute-BA) for identification. Male individuals from the other states were mounted for photographic documentation, highlighting the characteristics that differentiate the two species. A fragment of the cytochrome c oxidase subunit 1 gene was sequenced and then compared with that of the Atheloca spp. deposited in GenBank. An analysis was conducted to evaluate the genetic distance between A. bondari and A. subrufella. The results indicate greater interspecific (0.030-0.034) than intraspecific (0.000-0.002) genetic variation between the groups, reinforcing the hypothesis of two distinct species. A geographic distribution map and a table with the host plants were constructed based on a literature review. This study concluded that the species occurring in Brazil is A. bondari, as suggested by C. Heinrich. Atheloca bondari and A. subrufella have only been reported in plants of the family Arecaceae, but only the coconut tree (Cocos nucifera L.) is shared by the two species.

Predator performance is impaired by the presence of a second prey species.

The simultaneous infestation of a plant by several species of herbivores may affect the attractiveness of plants to the natural enemies of one of the herbivores. We studied the effect of coconut fruits infested by the pests Aceria guerreronis and Steneotarsonemus concavuscutum, which are generally found together under the coconut perianth. The predatory mite Neoseiulus baraki produced lower numbers of offspring on fruits infested with S. concavuscutum and on fruits infested with both prey than on fruits with A. guerreronis only. The predators were attracted by odours emanating from coconuts with A. guerreronis, but not by odours from coconuts with S. concavuscutum, even when A. guerreronis were present on the same fruit. Fewer N. baraki were recaptured on fruits with both prey or with S. concavuscutum than on fruits with only A. guerreronis. Furthermore, the quality of A. guerreronis from singly and multiply infested coconuts as food for N. baraki did not differ. Concluding, our results suggest that N. baraki does not perform well when S. concavuscutum is present on the coconuts, and the control of A. guerreronis by N. baraki may be negatively affected by the presence of S. concavuscutum.

Evidence of Amblyseius largoensis and Euseius alatus as biological control agent of Aceria guerreronis.

Amblyseius largoensis (Muma) (Acari: Phytoseiidae) and Euseius alatus De Leon (Acari: Phytoseiidae) are predatory mites that are mostly found on leaves and on the exposed fruit surface of coconut plants. Their morphology hampers the access to the microhabitat occupied by Aceria guerreronis Keifer (Acari: Eriophyidae), the most important pest of coconut fruits throughout the world. However, it was suggested that they can prey on A. guerreronis under natural conditions when this pest leaves its refuge to disperse. Since the trophic interactions between A. largoensis or E. alatus and A. guerreronis are unknown, we compare the frequencies of occurrence of A. largoensis and E. alatus under the bracts of coconut fruits and on coconut leaflets. In addition, because phytoseiids feed by liquid ingestion, we used molecular analysis to confirm the potential role of A. largoensis or E. alatus as predators of A. guerreronis and to assess how fast the A. guerreronis DNA fragment is degradated in the A. largoensis digestive tract. Our study demonstrated that E. alatus was only present on coconut leaflets whereas A. largoensis was found mostly on leaflets and, to a much lesser extent, under the bracts of coconuts. Species-specific ITS primers designed for A. guerreronis were shown to have a high degree of specificity for A. guerreronis DNA and did not produce any PCR product from DNA templates of the other insects and mites associated with the coconut agroecosystem. Based on molecular analysis, we confirmed that the predatory mites, A. largoensis and E. alatus, had preyed on the coconut mite in the field. Overall the predatory mites collected in the field exhibited low levels of predation (26.7% of A. largoensis and 8.9% of E. alatus tested positive for A. guerreronis DNA). The fragment of A. guerreronis DNA remained intact for a very short time (no more than 6 h after feeding) in the digestive tract of A. largoensis.

Acaricide-impaired functional predation response of the phytoseiid mite Neoseiulus baraki to the coconut mite Aceria guerreronis.

Acaricides may interfere with a myriad of interactions among arthropods, particularly predator-prey interactions. The coconut mite, Aceria guerreronis Keifer (Acari: Eriophyidae), and its phytoseiid predator, Neoseiulus baraki (Athias-Henriot) (Acari: Phytoseiidae), provide an opportunity to explore such interference because the former is a key coconut pest species that requires both predation and acaricide application for its management. The objective of the present study was to assess the effect of the acaricides abamectin, azadirachtin and fenpyroximate on the functional response of N. baraki to A. guerreronis densities. The following prey densities were tested: 5, 10, 20, 40 and 80 preys. The type of functional response and prey handling time (Th) were not altered by the acaricides. However, the attack rate (a') was modified by abamectin and fenpyroximate, and the consumption peak was reduced by abamectin. All of the acaricides allowed for the maintenance of the predator in the field, but exposure to abamectin and fenpyroximate compromised prey consumption.

Host finding behaviour of the coconut mite Aceria guerreronis.

For the coconut mite, Aceria guerreronis Keifer, its host plant, the coconut palm, is not merely a source of food, but more generally a habitat to live in for several generations. For these minute organisms, finding a new plant is difficult and risky, especially because their main mode of dispersal is passive drifting with the wind and because they are highly specialized on their host plant. Consequently, the probability of landing on a suitable host is very low, let alone to land in their specific microhabitat within the host. How coconut mites manage to find their microhabitat within a host plant is still underexplored. We tested the hypothesis that they use volatile chemical information emanating from the plant to find a specific site within their host plants and/or use non-volatile plant chemicals to stay at a profitable site on the plant. This was investigated in a Y-tube olfactometer (i.e. under conditions of a directed wind flow) and on cross-shaped arenas (i.e. under conditions of turbulent air) that either allowed contact with odour sources or not. The mites had to choose between odours from specific parts (leaflet, spikelet or fruit) of a non-infested coconut plant and clean air as the alternative. In the olfactometer experiments, no mites were found to reach the upwind end of the Y-tube: <5 % of the mites were able to pass the bifurcation of the "Y". On the cross-shaped arenas, however, a large number of coconut mites was found only when the arm of the arena contained discs of fruit epidermis and contact with these discs was allowed. The results suggest that coconut mites on palm trees are not attracted to specific sites on the plant by volatile plant chemicals, but that they arrested once they contact the substrate of specific sites. Possibly, they perceive non-volatile chemicals, but these remain to be identified.

Behaviour of coconut mites preceding take-off to passive aerial dispersal.

For more than three decades the coconut mite Aceria guerreronis Keifer is one of the most important pests of coconut palms and has recently spread to many coconut production areas worldwide. Colonization of coconut palms is thought to arise from mites dispersing aerially after take-off from other plants within the same plantation or other plantations. The underlying dispersal behaviour of the mite at take-off, in the airborne state and after landing is largely unknown and this is essential to understand how they spread from tree to tree. In this article we studied whether take-off to aerial dispersal of coconut mites is preceded by characteristic behaviour, whether there is a correlation between the body position preceding aerial dispersal and the direction of the wind, and whether the substrate (outer surface of coconut bracts or epidermis) and the wind speed matter to the decision to take-off. We found that take-off can sometimes be preceded by a raised body stance, but more frequently take-off occurs while the mite is walking or resting on its substrate. Coconut mites that become airborne assumed a body stance that had no relation to the wind direction. Take-off was suppressed on a substrate providing food to coconut mites, but occurred significantly more frequently on the outer surface of coconut bracts than on the surface of the fruit. For both substrates, take-off frequency increased with wind speed. We conclude that coconut mites have at least some degree of control over take-off for aerial dispersal and that there is as yet no reason to infer that a raised body stance is necessary to become airborne.

Limits to ambulatory displacement of coconut mites in absence and presence of food-related cues.

Ambulatory movement of plant-feeding mites sets limits to the distances they can cover to reach a new food source. In absence of food-related cues these limits are determined by survival, walking activity, walking path tortuosity and walking speed, whereas in presence of food the limits are also determined by the ability to orient and direct the path towards the food source location. For eriophyoid mites such limits are even more severe because they are among the smallest mites on earth, because they have only two pairs of legs and because they are very sensitive to desiccation. In this article we test how coconut mites (Aceria guerreronis Keifer) are constrained in their effective displacement by their ability to survive in absence of food (meristematic tissue under the coconut perianth) and by their ability to walk and orient in absence or presence of food-related cues. We found that the mean survival time decreased with increasing temperature and decreasing humidity. Under climatic conditions representative for the Tropics (27 °C and 75 % relative humidity) coconut mites survived on average for 11 h and covered 0.4 m, representing the effective linear displacement away from the origin. Within a period of 5 h, coconut mites collected from old fruits outside the perianth moved further away from the origin than mites collected under the perianth of young fruits. However, in the presence of food-related cues coconut mites traveled over 30 % larger distances than in absence of these cues. These results show that ambulatory movement of eriophyoid mites may well bring them to other coconuts within the same bunch and perhaps also to other bunches on the same coconut palm, but it is unlikely to help them move from palm to palm, given that palms usually do not touch each other.

First report of the red palm mite, Raoiella indica Hirst (Acari: Tenuipalpidae), in Brazil.

The presence of the red palm mite, Raoiella indica Hirst, is reported for the first time in Brazil. This invasive mite was found in July 2009 infesting coconut palms and bananas in urban areas of Boa Vista, State of Roraima, in northern Brazil. Comments on the possible pathways of R. indica into the country, present and potential impact of its introduction and mitigating measures to prevent or to delay the mite spread in Brazil are presented.

[Rearing technique and biological traits of Atheloca subrufella (Hulst) (Lepidoptera: Phycitidae) in coconut fruits]. / Técnica de Criação e Aspectos Biológicos de Atheloca subrufella (Hulst) (Lepidoptera: Phycitidae) em Frutos de Coqueiro.

Rearing Technique and Biological Traits of Atheloca subrufella (Hulst) (Lepidoptera: Phycitidae) in Coconut Fruits. Larvae of the coconut moth Atheloca subrufella (Hulst) develop in flowers and fruits of coconut, Cocos nucifera, causing precocious abscission of these structures and, hence, yield decrease. This work studied a feasible and suitable rearing technique for A. subrufella using fruits of coconut. We first determined the appropriate density of larvae to be reared per coconut fruit (among two, three, four or five larvae) and later tested the suitability of this rearing technique for three successive generations. The storage of egg and pupal stages during 0, 5, 10 and 20 days was also studied at 12ºC. Based on the fertility life table parameters, the best results were achieved by rearing two or three larvae per fruit as they yielded the best net reproductive rate and intrinsic rate of population increase. In addition, eggs and pupae of A. subrufella can be stored at 12ºC up to five days with viability higher than 90%. Adult moths emerged from pupae stored for five days at 12ºC produced an average of 219.4 eggs and lived 18.8 days. Storage periods for eggs and pupae over 10 days significantly reduced egg viability and adult fecundity, respectively. Thus, the technique in here described was shown to be suitable for the continuous rearing of A. subrufella in laboratory conditions.

Compatibility of Neoseiulus paspalivorus and Proctolaelaps bickleyi, candidate biocontrol agents of the coconut mite Aceria guerreronis: spatial niche use and intraguild predation.

The eriophyid mite Aceria guerreronis occurs in most coconut growing regions of the world and causes enormous damage to coconut fruits. The concealed environment of the fruit perianth under which the mite resides renders its control extremely difficult. Recent studies suggest that biological control could mitigate the problems caused by this pest. Neoseiulus paspalivorus and Proctolaelaps bickleyi are two of the most frequently found predatory mites associated with A. guerreronis on coconut fruits. Regarding biological control, the former has an advantage in invading the tight areas under the coconut fruit perianth while the latter is more voracious on the pest mites and has a higher reproductive capacity. Based on the idea of the combined use/release of both predators on coconut fruits, we studied their compatibility in spatial niche use and intraguild predation (IGP). Spatial niche use on coconut fruits was examined on artificial arenas mimicking the area under the coconut fruit perianth and the open fruit surface. Both N. paspalivorus and P. bickleyi preferentially resided and oviposited inside the tight artificial chamber. Oviposition rate of P. bickleyi and residence time of N. paspalivorus inside the chamber were reduced in the presence of a conspecific female. Residence of N. paspalivorus inside the chamber was also influenced by the presence of P. bickleyi. Both N. paspalivorus and P. bickleyi preyed upon each other with relatively moderate IGP rates of adult females on larvae but neither species yielded nutritional benefits from IGP in terms of adult survival and oviposition. We discuss the relevance of our findings for a hypothetic combined use of both predators in biological control of A. guerreronis.

Exploration of the acarine fauna on coconut palm in Brazil with emphasis on Aceria guerreronis (Acari: Eriophyidae) and its natural enemies.

Coconut is an important crop in tropical and subtropical regions. Among the mites that infest coconut palms, Aceria guerreronis Keifer is economically the most important. We conducted surveys throughout the coconut growing areas of Brazil. Samples were taken from attached coconuts, leaflets, fallen coconuts and inflorescences of coconut palms in 112 localities aiming to determine the occurrence and the distribution of phytophagous mites, particularly A. guerreronis, and associated natural enemies. Aceria guerreronis was the most abundant phytophagous mite followed by Steneotarsonemus concavuscutum Lofego & Gondim Jr. and Steneotarsonemus furcatus De Leon (Tarsonemidae). Infestation by A. guerreronis was recorded in 87% of the visited localities. About 81% of all predatory mites belonged to the family Phytoseiidae, mainly represented by Neoseiulus paspalivorus De Leon, Neoseiulus baraki Athias-Henriot and Amblyseius largoensis Muma; 12% were Ascidae, mainly Proctolaelaps bickleyi Bram, Proctolaelaps sp nov and Lasioseius subterraneus Chant. Neoseiulus paspalivorus and N. baraki were the most abundant predators on attached coconuts. Ascidae were predominant on fallen coconuts, while A. largoensis was predominant on leaflets; no mites were found on branches of inflorescences. Leaflets harboured higher mite diversity than the attached coconuts. Mite diversity was the highest in the state Pará and on palms surrounded by seasonal forests and Amazonian rain-forests. Neoseiulus paspalivorus, N. baraki and P. bickleyi were identified as the most promising predators of A. guerreronis. Analyses of the influence of climatic factors revealed that dry ambient conditions favour the establishment of A. guerreronis. Neoseiulus paspalivorus and N. baraki have differing climatic requirements; the former being more abundant in warm and dry areas, the latter prevailing in moderately tempered and humid areas. We discuss the significance of our findings for natural and biological control of A. guerreronis.

Life history of the predatory mites Neoseiulus paspalivorus and Proctolaelaps bickleyi, candidates for biological control of Aceria guerreronis.

The eriophyoid mite Aceria guerreronis Keifer (Eriophyidae), commonly called the coconut mite, is a key pest of coconut fruits. Surveys conducted on coconut palms in Brazil revealed the predatory mites Neoseiulus paspalivorus DeLeon (Phytoseiidae) and Proctolaelaps bickleyi Bram (Ascidae) as the most commonly associated natural enemies of A. guerreronis on coconut fruits. However, virtually nothing is known about the life history of these two predators. We conducted laboratory experiments at 25 +/- 0.1 degrees C, 70-90% RH and 12:12 h L:D photoperiod to determine the life history characteristics of the two predatory mites when feeding on A. guerreronis and other potential food sources present on coconut fruits such as Steneotarsonemus furcatus DeLeon (Tarsonemidae), coconut pollen and the fungus Rhizopus cf. stolonifer Lind (Mucoraceae). In addition, the two-spotted spider mite Tetranychus urticae Koch (Tetranychidae) was tested for its suitability as prey. Both predators, N. paspalivorus and P. bickleyi, thrived on A. guerreronis as primary food source resulting in shorter developmental time (5.6 and 4.4 days, respectively), higher oviposition rate (1.7 and 7.0 eggs/female/day, respectively) and higher intrinsic rate of increase (0.232 and 0.489 per female/day, respectively) than on any other diet but were unable to develop or lay eggs when fed T. urticae. Coconut pollen and S. furcatus were adequate alternative food sources for N. paspalivorus and Rhizopus for P. bickleyi. We discuss the relevance of our findings for natural and biological control of the coconut mite A. guerreronis.