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Ecology of Varroa destructor,the Major Ectoparasiteof the Western Honey Bee,Apis melliferaFrancesco Nazzi1 and Yves Le Conte2,∗

1Dipartimento di Scienze Agrarie e Ambientali, Universita degli Studi di Udine, 33100 Udine,Italy; email: [email protected], UR 406 Abeilles et Environnement, Domaine Saint Paul, Site Agroparc,84914 Avignon Cedex 9, France; email: [email protected]

Annu. Rev. Entomol. 2016. 61:417–32

First published online as a Review in Advance onDecember 14, 2015

The Annual Review of Entomology is online atento.annualreviews.org

This article’s doi:10.1146/annurev-ento-010715-023731

Copyright c© 2016 by Annual Reviews.All rights reserved

∗Corresponding author

Keywords

varroa mite, parasitism, semiochemicals, humidity, kairomones,temperature, pathogens

Abstract

Varroa destructor is the most important ectoparasite of Apis mellifera. Thisreview addresses the interactions between the varroa mite, its environment,and the honey bee host, mediated by an impressive number of cues and sig-nals, including semiochemicals regulating crucial steps of the mite’s life cycle.Although mechanical stimuli, temperature, and humidity play an importantrole, chemical communication is the most important channel. Kairomonesare used at all stages of the mite’s life cycle, and the exploitation of bees’brood pheromones is particularly significant given these compounds func-tion as primer and releaser signals that regulate the social organization ofthe honey bee colony. V. destructor is a major problem for apiculture, andthe search for novel control methods is an essential task for researchers. Adetailed study of the ecological interactions of V. destructor is a prerequisitefor creating strategies to sustainably manage the parasite.

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http://www.annualreviews.org/doi/full/10.1146/annurev-ento-010715-023731


Brood: sum ofimmatures of thehoney bee colony,including eggs, larvae,and pupae

INTRODUCTION

Biological invasions are a common threat for modern agriculture, and apiculture is no exception,having suffered several of these events in its recent history. In fact, beekeeping faced a major crisisin the 1980s due to the invasive species Varroa destructor, and this ectoparasite is surely involvedin the worrying decline experienced by managed bees for the past 10 years (65).

The parasitic mite, initially named Varroa jacobsoni and currently known as V. destructor (3),was first reported outside its natural distribution area, Southeast Asia, in 1949, and thereafter itrapidly spread all over Europe, North America, South America, Africa, and the Asia Pacific region(73, 92). In Asia the varroa mite shifted from its natural host Apis cerana to Apis mellifera duringthe first part of the twentieth century and then spread over the continent, reaching Europe in the1970s (73). It is particularly difficult to precisely estimate the damage to the beekeeping industrycaused by the varroa mite since its arrival in the Western world. However, the fact that varroosisis considered the major zoonosis in the context of honey bee pathology (102, 108) and the factthat apiculture and pollination are estimated to have an economic value worth billions of dollarsworldwide (2, 36) roughly demonstrate the economic impact of varroa mite infestations on honeybee colonies.

V. destructor is an obligatory parasite, spending its entire life in the bee’s nest either on immaturestages or on adult bees (102, 108). The strict synchronization between the mite’s life cycle andthat of its host and its ability to vector and activate pathogenic agents are important features ofthe natural history of this parasite that account for its central role in bee pathology. Since theextraordinary success of V. destructor adaptation to its new host, the study of the ecology of themite and of host-parasite relationships is a subject worthy of attention both for its biologicalsignificance and for its important practical implications.

Some reviews dedicated to V. destructor (102, 108) provide a good description of the complexbiology and impact of the mite, and much research has been conducted on the mechanisms of miteparasitism. In this article we focus on the ecology of the parasite. First, we describe the currentknowledge on the interactions between the mite and its environment, and then we concentrateon the interactions between the mite and the host A. mellifera, as well as other organisms thatare involved (Figure 1). We focus on different stimuli that mediate host-parasite interactions,including host location and choice, mite mimicry, and detection of the mite by the bees.

AUTOECOLOGY OF VARROA DESTRUCTOR

The varroa mite lives at a temperature corresponding to that of the honey bee nest, which isapproximately 34–35◦C. Laboratory bioassays indicated that V. destructor shows a clear preferencefor temperatures of approximately 32◦C ± 2.9◦C (60) and that temperature preferences differ be-tween winter and young summer mites (93). The mite can discriminate differences in temperatureas low as approximately 1◦C (59). V. destructor ostensibly experiences lower temperatures whenit travels on forager bees outside the hive, as demonstrated by the many mites imported intononinfested honey bee colonies by foraging bees returning from robbing infested colonies (42) ordrifting between adjacent colonies (41).

Temperature can also affect the mite’s physiology. In an experiment carried out under lab-oratory conditions, mites reproduced at 34.5◦C whereas no offspring were observed at 31.5◦C(22); when sections of parasitized brood comb were reared at different temperatures, the highestreproductive rate was obtained between 32.5◦C and 33.4◦C (61).

Hygrometric conditions also play an important role, with optimum humidity for reproductionranging from 55% to 70% and only limited reproduction taking place at higher humidity (22, 56,60). In sum, optimal humidity and temperature values for Varroa reproduction match quite well

418 Nazzi · Le Conte

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Environment(e.g., temperature, humidity)

Influence onphysiology

Hemolymph subtractionBiochemical alterations

GroomingHygienic behaviorImmune reactions

Transmissionfacilitation

Possible effects onmite’s fitness

Other organisms(e.g., DWV)

Figure 1The ectoparasitic mite Varroa destructor causes damage to the honey bee, Apis mellifera, and in turn suffersfrom the host’s reactions. Environmental conditions influence this host-parasite interaction, in which otherorganisms are also involved. Abbreviation: DWV, deformed wing virus.

Anemotaxis:behavioral response ofan organism to an airflow

with those found within the hive, although temperatures in the brood nest can vary from 30.5◦Cto 35.5◦C (8, 103) and humidity is more variable than is usually acknowledged (45).

The response to single clean-air puffs (57) indicates a positive anemotaxis by the mite, whichis also attracted by electric charges that may be involved in attraction to adult bees (23). Theeffect of light and vibration on V. destructor has also been studied (50), although it is not clear howillumination and mechanical stimuli affect either the biology or the behavior of the parasite.

SYNECOLOGY OF VARROA DESTRUCTOR

Interactions of the Mite with the Honey Bee

When describing the relationship between the mite and its host, it is useful to refer to the biologicallife cycle of the parasite (102, 108). The life cycle involves two distinct stages: The phoretic phaseis spent on the adult bee and the reproductive phase is spent inside a bee brood cell (Figure 2).The invasion of the brood cell, which represents the beginning of the reproductive phase, occurssome hours before a cell containing a bee larva is sealed. Within the brood cell, the mite feeds onthe bee’s hemolymph and lays its eggs on the surface of the cell wall. The female mite enteringthe cell normally lays eggs that produce at first one male and then a few females. The offspringmate with each other so that when the newly enclosed adult bee exits the cell, both the invading

www.annualreviews.org • Ecology of the Varroa Mite 419

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Adult choiceHydrocarbonsAlarm pheromone components?

Cell invasionFatty acid estersCarboxylic acidsHydrocarbons

ReproductionTrigger of reproduction: ?Sex pheromones: fatty acid esters Inhibitors: hydrocarbons

Phor

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pha

seRe

prod

ucti

ve p

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AddHyddAlaa

RepTriggSexxInhi

Figure 2The life cycle of Varroa destructor involves phoretic periods on adult bees and reproductive periods in brood cells. Several chemicalsmediate nearly every step of this cycle.

female and the mature fertilized female mite offspring leave the cell. They then transfer onto anadult bee, where they spend the phoretic phase, before entering a brood cell to reproduce again.Male mites cannot survive outside the cell, and die. Female mites can go through two or threecycles over the course of their life span.

The reproductive phase. The reproductive phase includes cell invasion by the mite, feeding onthe honey bee immatures, chemical mimicry to escape recognition by the worker bees, oviposition,and mating. Stimuli that involve mutual interactions between the mite and the honey bee andbetween mites themselves are involved in each of these steps (see the sidebar, The Use of HoneyBee Pheromone by the Varroa Mite).

THE USE OF HONEY BEE PHEROMONE BY THE VARROA MITE

The honey bee uses a variety of pheromonal compounds that function as complex releaser and primer signals, andthe mite uses some of these same compounds to find its target for feeding and reproducing. This highly adaptivestrategy allows the mite to optimize its search, as the honey bee pheromone should not evolve rapidly. The mitealso uses ethyl oleate as a mating signal. The molecule is also produced by bee larvae and adults and has primer andreleaser effects within the colony.


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Olfactometer:experimental devicewith which to studyolfaction-mediatedbehavior

Cuticularhydrocarbon (CH):hydrocarbons secretedon the cuticle of allinsects

Cell invasion. V. destructor enters a brood cell containing a bee larva 15 to 20 h before workerbrood cells are sealed and 40 to 50 h before drone brood cells are sealed (11). The mite does notreach the brood cell on its own but is carried there by a nurse bee, which is abandoned only a shortdistance from the bee larva that will be parasitized (10). Apart from some physical stimuli, such asthe distance from the bee larva and the cell rim (40), several chemicals mediate the attraction ofthe mite toward the brood and the following arrestment. In 1989, Le Conte et al. (63) used a four-armed olfactometer under controlled temperature conditions (34◦C) to show that some fatty acidesters (i.e., methyl palmitate, ethyl palmitate, and methyl linolenate) are involved in the attractionof the mite to bee larvae. Later, the arrestant effect of these compounds was demonstrated using adifferent bioassay (16). The two methyl esters are also components of the bee brood pheromone,inducing nurse bees to cap brood cells (62). Therefore, the mite’s use of these pheromones as akairomonal cue to synchronize cell invasion is an example of chemical espionage, or eavesdropping,and resembles other cases often observed in chemical ecology (110, 118).

Additional compounds produced by larvae have either attractant or arrestant effects on themite. Using a servosphere, Rickli et al. (99) found that palmitic acid has an attractant effect;using a different bioassay, the authors showed also that some cuticular hydrocarbons (CHs) ofintermediate chain length (C21–C29) elicit arrestment behavior in Varroa females (98). Aumeieret al. (6) found that Varroa females are arrested by fifth instar larvae collected from brood cells21 h before cell capping, and related such attraction to the bee’s CHs. However, they foundno differences in fatty acid esters or intermediate chain length hydrocarbons (C21–C29) betweenEuropean and Africanized bees, despite a marked difference in their attractiveness, suggesting thatother chemical cues are involved in cell invasion.

Along this line of reasoning, the marked preference of the mite for nurse bees over brood (54,67) makes it unlikely that a substance from the brood may be the only factor responsible for cellinvasion, which implies that the mite leaves the nurse bee to move onto the larva. Therefore, otherpossible sources of attractive compounds from the cell were tested, leading to the identification ofhoney bee larval food, which is present inside the cell at the time of invasion, as another source ofattraction for the mite (90); later, 2-hydroxyhexanoic acid from larval food was shown to be activeboth in the laboratory and under field conditions, affecting the distribution of the mite amongbrood cells that were treated or not treated with this chemical prior to capping (89).

V. destructor shows a strong preference for drone brood. In A. mellifera carnica colonies, forexample, drone brood is infested approximately eight times more frequently than worker brood(34); this preference could be due to the presence of greater amounts of attractant compoundseither on drone larvae (63, 111) or in the larval food contained in such cells (89), as well as tothe longer duration of the invasion period (11) and differences in the number of visits made byinfested nurse bees to drone brood compared to worker brood. Conversely, queen cells are rarelyinvaded by mites, suggesting that these cells could be repellent to the mite (17). A laboratorystudy, followed by a field validation, showed that octanoic acid, which is abundant in royal jellyand scarce in worker and drone larval food, is repellent to the varroa mite, possibly explaining thereduced infestation of queen cells (83).

In a brood comb, it is common to find larvae infested by two, three, or more mites as wellas many cells that are not infested. This observation illustrates that the distribution of the miteamong brood cells is not random but rather aggregated (31, 33). Aggregation, which has also beenobserved under laboratory conditions (21), could indeed favor exogamy and may have an adaptivevalue for the mite. However, it is not known whether this phenomenon is related to an aggregationpheromone or to the higher attractiveness of certain larvae either to the mite or to the nurse beescarrying the mite to the brood cell. Moreover, other findings, resulting from different statisticalapproaches, are contradictory and do not support the aggregation hypothesis (72, 106).


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Semiochemical:a chemical substanceor a mixture thatcarries a message forintra- or interspecificcommunication

Nestmaterecognition:a process whereby twoencounteringindividuals assesscolony affiliation bymatching theperceived label with abuilt-in template

Altogether these studies collectively demonstrate that the invasion of the brood cell by the miteis a complex mechanism involving several attractive and arrestant compounds coming from boththe bee larva and the brood cell together with repellent chemicals from royal jelly. The identifi-cation of several compounds as well as the demonstration of the activity of some of them undernatural conditions represents a promising step toward novel control methods based on behavioralmanipulation of the parasite. However, to our knowledge few such efforts have been undertaken.The fatty acid esters were tested for mite trapping in the field, but only a small proportion ofthe parasites infesting the colony could be trapped with this method (Y. Le Conte, personal ob-servations); other preliminary field trials with semiochemicals from larval food did not yield verypromising results (F. Nazzi, personal observations). In general, the peculiar characteristics of thebees’ nest (e.g., high temperature, lipophilic composition of combs), as well as the fact that theinvasion process depends partly on the honey bee, make the attempt to disrupt cell invasion usingsemiochemicals a challenging task for researchers.

Chemical mimicry. The ability of honey bees to recognize their nestmates is a basic feature thatenhances survival (18), allowing them to prevent the robbing of their colony’s provisions by beesfrom other hives. This is especially important during the fall, when there is a shortage of food.Under such conditions, a colony unable to prevent robbing will likely lose its honey storage andwill not survive the winter. Honey bees have evolved an efficient nestmate recognition strategyin which they recognize and learn specific proportions of CHs that chemically signal nestmatesfrom nonnestmates (9, 14, 66). In this variable chemical environment it is vital and particularlyadaptive for the mite to be able to mimic the chemical signature of the host colony so that it avoidsthe recognition and subsequent grooming and destruction by the host. Several studies based onCH profile analysis of the mite have shown that the mite can indeed mimic CHs of bees from itsown honey bee colony (49, 81) and that it can modify its mimicry according to the developmentalstage of the host (70).

Feeding. After entering the cell, the mite crawls between the larva and the cell wall and reachesthe bottom of the cell, where it remains trapped in the larval food (47). Compounds released fromlarval food, particularly 2-hydroxyhexanoic acid, likely play a role in this process (89, 90). Whenlarval food is consumed, the mite begins to feed on the bee larva. The activities carried out by themother mite and her offspring within the cell seem to be rigidly organized with regard to timeand space (28). Some C17–C22 aliphatic alcohols and C19–C22 aldehydes from the cocoon spun bythe bee larva inside the brood cell induce arrestment behavior in V. destructor (29) and may affectthe spatial allocation of the mites in the cell.

During the host’s pupal stage, feeding takes place on a site prepared by the mother mite. Tosuck the hemolymph from the bee, the mother mite pierces a hole through the host’s cuticle (27).The same feeding site is used by the offspring, but there is no information about the cues involvedin this feeding choice. Large colonies of bacteria were found in wounds on worker and dronepupae; some bacteria were Melissococcus pluton but elongate bacteria remained unidentified (48).The feeding activity of the mite has profound implications for the honey bee because of both thedirect damage caused by the parasite consuming the bee’s hemolymph and the indirect effectsrelated to other parasites vectored through feeding.

Several authors have studied the effects of Varroa feeding on the honey bee (102); however, giventhe frequent concurrent presence of viruses with Varroa, such effects could well be related to thecombined action of the parasite and the pathogens than to the mite alone. In fact, honey bees canbe infected by as many as 20 viruses, some of which are associated with V. destructor (20), includingdeformed wing virus (DWV), which is a major cause of widespread colony losses (25). At least inthe case of DWV, the mite acts as a mechanical vector but it also amplifies the virus, which can


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replicate within the parasite (39), although the possible effects of DWV replication on the mite’sfitness have not been investigated in detail. Moreover, V. destructor can trigger viral replication inthe bee and can therefore be considered a facilitator of the viral pathogen. Initially, this ability wasattributed to immunosuppression caused by the mite (115); however, later studies did not confirmthis hypothesis and an alternative hypothesis based on the exploitation of a common immunecurrency was advanced (84, 91). Indeed, repeated feeding through the wound inflicted on the beeat the beginning of the pupal stage (27) activates clotting and melanization, which are under thecontrol of a transcription factor that is also involved in the antiviral response (84). However, otheroptions have been proposed, including the possible interaction between the mite and a viral strainof higher virulence (105). DWV can influence honey bee immunity; this in turn could affect theresponse of the honey bee to mites’ feeding, with important consequences for the trophic activityof the parasite and consequently for its fitness (84).

Several authors (5, 13, 113, 114) have reported reduced weight of newly eclosed adult bees, areduction in protein content in the hemolymph, and a drastic reduction in longevity in infestedbees. Furthermore, various effects of Varroa parasitism on the CHs of adult bees were noted (5,74, 107). Challenging the immune system of bees with lipopolysaccharides or nonliving immunestimulants can change the CH profile of the bees, which can lead to modified and aggressiveconspecific contacts (96, 97). Bees infected with DWV showing altered CH profiles can also beejected from healthy hives (7). In contrast, McDonnell et al. (74) confirmed that the mite canalter the CH profile of the adult bees but did not observe any differential interaction betweeninfested bees and other bees. Both the mechanisms and the factors responsible for this effect needto be clarified within the context of the intricate interactions between virus, mite, and the host’simmune system (84).

Annoscia et al. (5) linked the alteration of the bee’s CHs to increased water transpirationthrough the cuticle, in turn causing the reduction in weight observed by many authors. Possibleeffects on the adult honey bee endocrine system could be likely in view of the hypothesis thatinfested bees transition prematurely to the foraging stage (100), whereas little is known about theproximate causes that alter the behavior of infested bees noted both within the hive (4) and outsidethe nest during foraging (52).

Transcriptomic studies conducted after the sequencing of the honey bee genome revealed acomplex picture involving several effects associated with a number of genes when the bee pupae areparasitized by the mite (82). The results show that mite parasitism induces downregulation of genesrelated to immune system and embryonic development, which could lead to adult deformities andcognitive impairment (82).

Oviposition. Approximately 60 h after the brood cell is sealed, the mite lays the first egg on thecell wall. Then, at 30-h intervals, up to six more eggs are laid (46, 71). However, ovipositiondoes not always occur and the percentage of reproducing mites varies according to the speciesand subspecies of the host and the sex of the larva. In A. cerana, reproduction rarely takesplace on worker brood and seems to be restricted to drone brood (51). By contrast, 80%and 95% of mites can oviposit on A. mellifera worker and drone brood, respectively (102).Indeed, reduced reproduction on worker brood seems to be the most important factor allowingA. cerana to tolerate mite infestation (95). Successful oviposition on worker brood varies alsobetween different subspecies of A. mellifera. For example, on Africanized honey bees from SouthAmerica, less than 50% of female mites lay any eggs (101); few differences between Europeansubspecies have been reported as well, although within subspecies variability can be quite high(68, 102). Nevertheless, it should be noted that reproduction of the mite depends not only onthe percentage of reproducing females but also on the number of offspring that reach maturity


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Kairomone: achemical or a mixtureof substances emittedby an organism thatbenefits an individualof another species

before the emergence of the parasitized bee as well as the mortality of the mite offspring (78, 80);both factors play an important role and should be carefully considered.

Stimuli inducing Varroa reproduction have been extensively studied for their potential prac-tical value. Several hypotheses have been proposed that involve primer effects of bee hormonesand kairomones. Initially, a signal triggering reproduction was proposed to co-occur with a tran-sient increase in the concentration of the bee’s juvenile hormone soon after cell sealing, but thishypothesis was later disregarded after more detailed analyses proved otherwise (104).

Two different kairomones with opposite effects on Varroa oviposition have been postulated toexist. Initial studies showed that factors promoting egg maturation and triggering oviposition arepresent in brood cells containing larvae and are active within 24 h after the cell is sealed (75, 76,78). A study by Frey et al. (32) revealed that the time frame of the stimuli initiating mite oogenesisis within 12 h and 36 h after worker and drone brood cells are capped, respectively. Once this timeperiod has elapsed, another signal begins acting in an opposite way, interrupting mite oogenesis(32). Stimuli inducing oviposition can be extracted from the bee larva (32, 38, 112). Trouiller& Milani (112) stimulated reproduction by the varroa mite within artificial gelatin cells using apentane extract of fifth instar bee larvae and isolated the bioactive compounds in the most polarfraction of the extract. Frey et al. (32) confirmed the activity of a similar extract and suggestedthat fatty acid ethyl and methyl esters identified in the extract could be involved in stimulatingmite oogenesis. Overall, there is clear evidence that the reproduction of the mite is activatedby factors extractable from the bee larvae. Nevertheless, other sources are possibly involved, asMilani & Chiesa (75, 76) provided evidence that larval food collected from brood cells increasesthe oviposition rate of mites kept in treated artificial cells containing a developing bee.

In general, it is now accepted that both the host and the cell environment play an essential rolein regulating oviposition. Studies on the mite’s reproduction inside artificially infested naturalbrood cells recognized the significance of the cell environment (28, 38, 76). Later, comparisons ofreproduction inside artificial rearing cells made of different materials confirmed that, regardless ofthe conditions of the mite and the host, oviposition takes place only if the rearing cells are suitable(86). Using a new bioassay based on the expression of the mite’s vitellogenin gene, Cabrera Cordonet al. (15) confirmed that oogenesis is initiated only in a suitable rearing cell. In any case, the stimulithat trigger oviposition have not been identified, and this remains an important objective for futureresearch in view of the possible practical implications for controlling the mite.

Approximately 18 and 36 h after worker and drone brood cells are capped, respectively, thebee produces a stop signal (32). This signal has not been identified, but Garrido & Rosenkranz(37) have demonstrated that pupal volatile compounds can inhibit the onset of oviposition bymites and could therefore be involved. Moreover, the number of eggs laid by a fertile femaleduring each reproductive cycle can be variable but tends to be proportionally smaller when moremites enter the same cell to reproduce (35). A laboratory study revealed that such a reductionwas induced by chemical compounds released inside the infested cell (87); later, Nazzi et al. (88)identified the unsaturated hydrocarbon (Z)-8-heptadecene to be at least partly responsible for thiseffect. The biological activity of this compound was also confirmed under natural conditions (77).Interestingly, 100 ng of (Z)-8-heptadecene also reduces the invasion of brood cells (77), suggestingparsimonious use of this semiochemical by the mite.

Mating. Approximately 6 days after oviposition, mite offspring become adults (1, 46, 71). Matingbetween the male, which emerges from the first egg laid, and the females, which emerge subse-quently, takes place within the sealed brood cell, at the fecal accumulation site (where the mitesaggregate in the cell and defecate) (27). Compounds produced by newly emerged females triggermating attempts by the male (116); three fatty acids (i.e., oleic acid, palmitic acid, and stearic acid)


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Primer signal: apheromone that uponperception affectslong-termphysiological and/orendocrine processes inthe recipient

Releaser pheromone:a pheromone thatupon perceptioninduces changes in theprobability ofperforming onebehavior in favor ofanother behavior

Phoresis: attachmentfor the purpose oftransport, usually by aparasite on the host

Sternite: ventral partof a thoracic orabdominal segmentmade of hardenedexoskeleton

and the respective ethyl esters are the main pheromonal components inducing similar mating andcopulation behavior by the male (117). These chemicals are also produced by bee larvae in relevantamounts within the brood cells and function as both primer and releaser signals. Further researchis needed to determine other possible pheromonal components and to assess the ability of the miteto biosynthesize these compounds.

The phoretic phase. Upon emergence of the adult bee from the brood cell, the mother miteand the mature offspring leave the cell with the bee and move onto a nurse bee (59). The timespent on adult bees by the mite is variable and depends on the amount of brood, the strength ofthe colony, and other factors; in experiments conducted in the Netherlands, the time required forhalf of the mites introduced into a colony to invade a cell ranged from 2 to 8 days (12). During thistime, mites are frequently found hiding between the abdominal sternites of the bee in a positionthat is difficult for other bees to reach. How the mite locates this position is unknown, but bothmechanical chemical and thermal cues are probably used. Radioactive tracer studies documentedthat mites can feed on adult bees during this phase, although the relevancy of these meals for bothmite and bee is not clear (24).

During the phoretic phase, mites prefer nurse bees to forager bees; this preference is relatedin part to the chemical signature of the forager bees (26, 55). The unsaturated hydrocarbon(Z)-8-heptadecene, found in higher amounts on the cuticle of pollen foragers, has a repellenteffect on the mite and is involved in host selection (26). Preference for nurse bees to foragerbees seems to be influenced by the infestation level of the colony, with possible consequences forthe horizontal transfer of mites between colonies (19). Mites may exploit the differences in thecuticular composition of the possible hosts for a refined selection that optimizes the search for abrood cell. In fact, by choosing a nurse bee, which can later take it to a brood cell, the parasiteincreases its reproductive success; further, this behavior reduces the risks related to the outsideactivities of forager bees, which are dangerous for the bee and the mite.

By contrast, the transfer of mites from forager bees robbing an infested colony to foragers fromanother colony, contributing to the horizontal transmission of the parasite between colonies, has tobe a common phenomenon in view of the high number of mites imported into noninfested coloniesduring periods of nectar shortage (42). Kraus (53) hypothesized that compounds from the stingapparatus, which contaminate bees stung to death during fights that occur during robbing, areresponsible for this host shift, although the dosages used in those bioassays were rather unrealistic.Future studies are needed to clearly identify the chemicals involved in this process.

Reactions of the Honey Bee to the Parasite

Behavioral defenses against phoretic and reproducing mites have been documented. In particular,workers of the Eastern honey bee, A. cerana, can detach the mite from the body of a nestmate (i.e.,grooming) calling for help by means of a special dance (94, 95). To display this behavior, the beemust first recognize the mite, possibly by mite-derived chemical signals. Martin et al. (69) usedsolid-phase microextraction techniques to study the volatiles emitted by the mite and identified ablend of compounds that induces a specific response from the worker bee antennae, particularlymethyl and ethyl oleate, which are both pheromones of the bees and components of the mite sexpheromone (66, 117).

Reproducing female mites can be damaged while reproduction is systematically interruptedwhen nurse bees displaying Varroa-sensitive hygiene behavior empty Varroa-infested brood cells(43, 44). Such behavior, conferring a certain degree of tolerance to bees, involves recognitionof infested cells and is based primarily on olfactory cues emanating from such cells. The semio-chemicals involved in this process have been studied (69), and Nazzi et al. (85) showed that bees


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can use short-chain unsaturated hydrocarbons, including the alkene Z-(6)-pentadecene, for thispurpose. In general, the chemicals triggering hygienic behavior are likely released by the infestedbees rather than by the mite itself, as previous studies have demonstrated a remarkable similaritybetween the CHs of the varroa mite and the honey bee (49, 70), which is expected from a parasiteinfesting a social insect. Such chemical mimicry can be the result of the passive acquisition of thebees’ cuticular lipids during infestation (49).

In any case, the elucidation of the stimuli triggering hygienic behavior is certainly a field of re-search worthy of considerable effort in view of the potential for the selection of bee strains exhibit-ing higher tolerance to the parasite, as this solution may be one of the most sustainable strategiesfor long-term management of the mite. Along this line, gene expression analysis of the antennaeof worker bees selected for Varroa-sensitive hygiene behavior revealed that the molecular mecha-nisms acting at that level play a key role in the expression of this behavior (79). Moreover, a similartranscriptomic approach applied to a comparison of bees from resistant lines (64) showed overex-pression of genes related to olfaction and responsiveness to stimuli (82). These findings demon-strate the importance of chemical communication between bees upon recognition of the mite.

CONCLUSIONS

This review addresses the interactions between the varroa mite, its environment, and the honeybee host. An impressive number of cues involved in this network of relationships are used bythe mite and the bees to achieve optimum fitness. Clearly, the mite uses such cues to adapt itsactivity to the environment and the host and thus must be equipped with different kinds of sensors.Although mechanical stimuli as well as temperature and humidity parameters play an importantrole, chemical communication is by far the most important channel. A plethora of kairomones areused at all stages of the mite’s life cycle, but the exploitation of brood pheromones is particularlysignificant given these compounds function as primer and releaser signals that regulate the socialorganization of the honey bee colony (66) and given the implications for the possible arms racebetween the host and the parasite. The complexity of chemical communication between bees,which includes context dependency, not uniqueness of the response (58, 109), is also fundamentalto the communication between the varroa mite and the honey bee.

Many years after its arrival in the Western world, V. destructor still represents a major problemfor apiculture, and the search for novel alternative control methods is therefore an essential taskfor researchers. In this respect, detailed studies of the ecological interactions of the parasite areurgently needed to unravel essential aspects that are still poorly understood. Such studies may leadto promising strategies to sustainably manage this parasite. Methods to disrupt the mite’s abilityto sense the bee (30) are an example of future research. Whether acaricides used in mite control,as well as viruses found in the honey bee colonies, can interfere with the chemical communicationbetween honey bees and between varroa mites and honey bees is an interesting issue to solve. Manypheromonal and kairomonal compounds are involved in the chemical ecology of the varroa miteand the honey bee, demonstrating that Varroa and its honey bee host are one of the best-knownmodels to date in chemical ecology. In this regard, research should be continued as a case study.

SUMMARY POINTS

1. The varroa mite uses different types of cues, including physical and environmental signalsfrom the colony, to parasitize the honey bee.


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2. Other organisms, including pathogenic viruses, are involved in the relationship betweenthe mite and the honey bee.

3. Many chemical signals are involved in the varroa mite–honey bee relationship.

4. The varroa mite uses pheromonal signals from the honey bee colony to orient its searchfor the host.

5. Varroa mites mimic cuticular hydrocarbons of the host honey bee to avoid recognitionand destruction by the bees. This mimicry is host species dependent.

6. Chemical cues facilitate the recognition of the mite and concomitant responses by theworker bees.

7. Varroa parasitism alters the ability of bees to recognize mites by modulating expressionof genes involved in chemical communication.

FUTURE ISSUES

1. The interaction between Varroa and its honey bee host is one of the best-known modelsto date in chemical ecology, and research should be continued as a case study.

2. Further efforts are needed to identify and characterize the semiochemicals involved inthe interaction between Varroa mites and honey bees.

3. Genomics and proteomics provide powerful tools with which to decipher host-parasiteinteractions at the molecular level.

4. Scientists should take advantage of the numerous findings on chemical communication inVarroa and honey bees, using the different compounds together and testing for additive,synergistic, or antagonistic effects, to work on a more integrated approach.

5. Applied research should focus on using semiochemicals to develop sustainable manage-ment strategies for Varroa.

DISCLOSURE STATEMENT

The authors are not aware of any affiliations, memberships, funding, or financial holdings thatmight be perceived as affecting the objectivity of this review.

ACKNOWLEDGMENTS

We are grateful to Fanny Mondet for her kind review and to two anonymous reviewers for theirwork improving the manuscript.

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EN61-FrontMatter ARI 13 February 2016 8:33

Annual Review ofEntomology

Volume 61, 2016Contents

Structure and Evolution of Insect Sperm: New Interpretations in the Ageof PhylogenomicsRomano Dallai, Marco Gottardo, and Rolf Georg Beutel � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 1

Neurobiology of Monarch Butterfly MigrationSteven M. Reppert, Patrick A. Guerra, and Christine Merlin � � � � � � � � � � � � � � � � � � � � � � � � � � � � �25

Pesticide-Induced Stress in Arthropod Pests for Optimized IntegratedPest Management ProgramsR.N.C. Guedes, G. Smagghe, J.D. Stark, and N. Desneux � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �43

The Sensory Ecology of Ant Navigation: From Natural Environments toNeural MechanismsMarkus Knaden and Paul Graham � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �63

Invasion and Management of Agricultural Alien Insects in ChinaFang-Hao Wan and Nian-Wan Yang � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �77

The Genetic Basis of Pheromone Evolution in MothsAstrid T. Groot, Teun Dekker, and David G. Heckel � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �99

Antarctic EntomologySteven L. Chown and Peter Convey � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 119

Remote Sensing and Reflectance Profiling in EntomologyChristian Nansen and Norman Elliott � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 139

Traumatic Myiasis: A Neglected Disease in a Changing WorldMartin J.R. Hall, Richard L. Wall, and Jamie R. Stevens � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 159

Biosynthesis, Turnover, and Functions of Chitin in InsectsKun Yan Zhu, Hans Merzendorfer, Wenqing Zhang, Jianzhen Zhang,

and Subbaratnam Muthukrishnan � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 177

Chemical Ecology of NeuropteraJeffrey R. Aldrich and Qing-He Zhang � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 197

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EN61-FrontMatter ARI 13 February 2016 8:33

Taxonomy, Ecology, and Management of Native and Exotic Fruit FlySpecies in AfricaSunday Ekesi, Marc De Meyer, Samira A. Mohamed, Massimiliano Virgilio,

and Christian Borgemeister � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 219

Reproduction–Immunity Trade-Offs in InsectsRobin A. Schwenke, Brian P. Lazzaro, and Mariana F. Wolfner � � � � � � � � � � � � � � � � � � � � � � � 239

Hearing in InsectsMartin C. Gopfert and R. Matthias Hennig � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 257

Biology, Ecology, and Management of the Diamondback Moth in ChinaZhenyu Li, Xia Feng, Shu-Sheng Liu, Minsheng You, and Michael J. Furlong � � � � � � � � 277

Major Hurdles for the Evolution of SocialityJudith Korb and Jurgen Heinze � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 297

Plasticity in Insect Olfaction: To Smell or Not to Smell?Christophe Gadenne, Romina B. Barrozo, and Sylvia Anton � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 317

Eradication of Invading Insect Populations: From Concepts toApplicationsAndrew M. Liebhold, Ludek Berec, Eckehard G. Brockerhoff,

Rebecca S. Epanchin-Niell, Alan Hastings, Daniel A. Herms,John M. Kean, Deborah G. McCullough, David M. Suckling,Patrick C. Tobin, and Takehiko Yamanaka � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 335

Studying the Complex Communities of Ants and Their Symbionts UsingEcological Network AnalysisAniek B.F. Ivens, Christoph von Beeren, Nico Bluthgen, and Daniel J.C. Kronauer � � � 353

The Layers of Plant Responses to Insect HerbivoresMeredith C. Schuman and Ian T. Baldwin � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 373

Rift Valley Fever: An Emerging Mosquito-Borne DiseaseKenneth J. Linthicum, Seth C. Britch, and Assaf Anyamba � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 395

Ecology of Varroa destructor, the Major Ectoparasite of the WesternHoney Bee, Apis melliferaFrancesco Nazzi and Yves Le Conte � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 417

What Can Plasticity Contribute to Insect Responses to Climate Change?Carla M. Sgro, John S. Terblanche, and Ary A. Hoffmann � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 433

Biology, Ecology, and Management of an Invasive Stink Bug, Bagradahilaris, in North AmericaJohn C. Palumbo, Thomas M. Perring, Jocelyn G. Millar, and Darcy A. Reed � � � � � � � � � 453

The Molecular Evolution of Xenobiotic Metabolism and Resistance inChelicerate MitesThomas Van Leeuwen and Wannes Dermauw � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 475

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