748 Florida Entomologist 94(4) December 2011

DISTRIBUTION AND ABUNDANCE OF PHORETIC (ASTIGMATA, ) ON FERRUGINEUS (COLEOPTERA: )

MOHAMMAD ALI AL-DEEB1, SABIR BIN MUZAFFAR2, ABDULLAH MOHAMED ABUAGLA3, AND EYAS MOHAMMAD SHARIF4 1Biology Department, Faculty of Science, United Arab Emirates University, P.O. Box 17551, Al Ain, UAE Phone: 00971-507435734; E-mail: [email protected]

2Biology Department, Faculty of Science, United Arab Emirates University

3Abu Dhabi Food Control Authority, Development Sector, Agriculture Research Stations (Kuwaitat), Protection Laboratory, Al Ain, UAE

4Al Foah Organic Farm, Al Ain, UAE

ABSTRACT

The red palm weevil, Rhynchophorus ferrugineus Olivier, is the most important pest on date palms. Weevils were collected from randomly selected infested date palms in Al Ain, United Arab Emirates (UAE). Mites from three families were recorded. sp. (: ) were the most common phoretic mites. Curculanoetus sp. (Ac- ari: ) were second in abundance. orbicularis (Acari: ) was recorded on one . The abundance of phoretic mites varied among body parts of R. ferrugineus, and the maximum numbers occurred in the subelytral space. The mean in- tensity, mean abundance, and prevalence of Uroobovella and Curculanoetus mites did not differ between male and female weevils. Uroobovella had significantly greater mean inten- sity, abundance and prevalence compared to Curculanoetus. Most Uroobovella and Curcu- lanoetus aggregated under the sublytral space, which presumably offers protection from the hot and dry environment. This study is the first to document the presence of phoretic mites on R. ferrugineus in UAE and will help to direct future research on their interac- tions.

Key Words: Rhynchophorus ferrugineus, Red palm weevil, Uropoda orbicularis, Uroobovella, Curculanoetus, phoresy

RESUMEN

El picudo rojo de la palma, Rhynchophorus ferrugineus Olivier, es el insecto plaga más im- portante de la palmera de dátiles. Picudos fueron colectados de palmas de dátiles infestadas seleccionadas al azar en Al Ain, Emiratos Árabes Unidos (EAU). Ácaros de tres familias fue- ron encontrados. Los ácaros foréticos más comunes fueron Uroobovella sp. (Acari: Urodin- ychidae). Curculanoetus sp. (Acari: Histiostomatidae) fueron segundos en orden de abundancia. Uropoda orbicularis (Acari: Uropodidae) se encontró en solo un picudo. La abundancia de ácaros foréticos en las diferentes partes del cuerpo de R. ferrugineus fue va- riable, los números más altos se encontraron el espacio subelitral. La intensidad promedio, abundancia promedio, y prevalencia de los ácaros Uroobovella y Curculanoetus no fue dife- rente entre picudos macho o hembra. Uroobovella tuvo una mayor intensidad promedio, abundancia y prevalencia que Curculanoetus. La mayoría de Uroobovella y Curculanoetus se agregaron en el espacio subelitrico, el cual presumiblemente ofrece protección de un am- biente caliente y seco. Este es el primer estudio que documenta la presencia de ácaros foré- ticos sobre R. ferrugineus en los EAU y servirá para direccionar futuras investigaciones sobre sus interacciones.

The red palm weevil (Rhynchophorus ferrug- and more recently into Western Europe (Conti et ineus Olivier) is a pest of a broad range of palms al. 2008). Rhynchophorus ferrugineus was first de- (Palmae) in southern Asia (Murphy & Briscoe tected in the United Arab Emirates (UAE) in 1986 1999). In the 1980s, the expanded its range and has since been an important cause of decline and invaded into the Middle East, North Africa in date production (Abraham et al. 1998). The date (Abraham et al. 1998; Murphy & Briscoe 1999), palm (Phoenix dactylifera L.) is the most com-

Al-Deeb et al.: Phoretic mites on Rhynchophorus ferrugineus 749

monly cultivated plant in the Middle East and arcoptes cooremani (Acari: ), for- North Africa, with hundreds of thousands of tons merly regarded as a phoretic species of the beetle of dates being produced annually; amounting to Chilocorus cacti, has been shown to acquire fluids millions of dollars worth of dates (Murphy & from the hemolymph of its beetle host suggesting Briscoe 1999). Consequently, R. ferrugineus repre- a transition between a phoretic and a truly para- sents a major threat to the industry. sitic association (Houck & Cohen 1995). Although The biology of R. ferrugineus has been studied there is a large body of literature on phoretic in great detail in India on several palm species in- mites and their hosts, a consensus on the func- cluding date palms (Murphy & Briscoe 1999). tions and the adaptive significance of phoresy has Generally, R. ferrugineus assemble on damaged not been reached. parts (and sometimes undamaged parts) of date Uropoda orbicularis (Acari: Uropodidae) is a palms. Larvae burrow through the soft tissue of widespread phoretic found in temperate and the crown or the base of petioles forming exten- arid climates associated with a wide range of - sive tunnels. In severely infested trees, these tun- tle species (Bajerlein & Bloszyk 2004). In temper- nels may cause the crown and trunk to weaken ate climates, U. orbicularis are found amongst and eventually break, resulting in death of the forest leaf litter or on soil as adults but in rela- tree. The larva develops in a cocoon and eventu- tively low densities, with about 30% immature in- ally emerges as an adult weevil (Abraham et al. dividuals being present (Bloszyk et al. 2002). 1998; Murphy & Briscoe 1999). However, they preferentially live in unstable hab- A number of species have been recorded as itats such as compost heaps, manure, and nests of natural enemies of R. ferrugineus including vi- , where their populations are dominated ruses, bacteria, fungi, nematodes, and by immature individuals (about 80%). They re- mites (Murphy & Briscoe 1999). However, limited quire phoretic dispersal between these habitats information exists on the extent to which these (Bloszyk et al. 2002). Over 25 species of species affect R. ferrugineus populations. The re- from several different families have been docu- lationship between some of these species and R. mented as host to U. orbiculairs, suggesting that ferrugineus ranges from phoretic to parasitic. this mite is a generalist without a particular pref- Phoresy is a complex symbiotic association that erence for host species (Bajerlein & Bloszyk has evolved in many organisms as a result of spa- 2004). Similarly, different phoretic Uroobovella tial and temporal isolation of their habitats species were reported to be associated with a cen- (O’Connor 1982). It is defined as a form of com- tipede (Bloszyk et al. 2006a) and in bird nests mensalism facilitating the physical transport of (Bloszyk et al. 2006b), demonstrating a range of one organism on the body of another, during acceptable hosts for this genus. which time no feeding or reproduction occurs in The distribution of U. orbicularis on specific re- the phoretic organism (Binns 1982; O’Connor gions of the host’s body shows considerable varia- 1982). Although the term host is generally associ- tion (Bajerlein & Bloszyk 2004). A study by Ata- ated with , we use the term host to de- kan et al. (2009) reported the presence of scribe carriers of phoretics as well as hosts of par- Uroobovella marginata deutonymphs in the sub- asites, following O’Connor (1982), Houck & elytral space on R. ferrugineus in Turkey. Bajer- O’Connor (1991) and Houck & Cohen (1995). In lein and Bloszyk (2004) found that U. orbicularis the Astigmata, only one of the life stages, the mites studied on 25 beetle species in Poland were deutonymph (sometimes termed a hypopus), ex- mostly attached on the elytra, the ventral surface, hibits phoretic behavior. The hypopi have evolved and the third pair of legs, although the numbers morphological adaptations, such as attachment on the first and second pair of legs and on the devices, to aid in phoresy. Phoretic associations pronotum were also significant. are particularly diverse in astigmatid (Acari: The Histiostomatidae family is one of the larg- Astigmata) and mesostigmatid mites (Acari: Me- est families of the with about 500 sostigmata) that have exploited many species in 58 genera (O’Connor 2009). In this fam- and invertebrate hosts for movement between ily dispersal is done through the deutonymphal suitable habitats. Phoresy in the cohort Uropod- instar (Evans 1992). Histiostomatid mites live in ina (Acari: Mesostigmata) also occurs in the wet substrates such as decaying vegetable matter deutonymphs although some species may not de- (rotting grain, plants, and mushrooms) (Hughes velop phoresy in certain habitats (O’Connor 1982; 1976; Fashing et al. 1996). Species of genera Houck & O’Connor 1991). Bonomoia and may be found on de- Although the primary function of phoresy is caying wood. Species in these genera live on the dispersal, phoretic associations may be complex rotting wood itself and not restricted to insect gal- (Binns 1982; O’Connor 1982; Houck & O’Connor leries as some other taxa (O’Connor 1994). 1991). Some apparently phoretic mites, for exam- Deutonymphs of Curculanoetus rhynchophorus ple, may use the association not only for dis- were found phoretic on the African palm weevil persal, but in some examples may even derive nu- Rhynchophorus phoenicis (Coleoptera: Curculion- trition from their host. The hypopi of the Hemis- idae) (Fain 1974).

750 Florida Entomologist 94(4) December 2011

Hypoaspis (Acari: ) consists of a Quantification and Statistical Analysis group of predatory mites which are found associ- ated with many beetles, especially those in the One hundred and five adult R. ferrugineus family Scarabaeidae (Costa 1971). Mites in this were collected from infested trees. In- genus have occasionally been observed eating dividual R. ferrugineus were sexed and mites eggs and larvae of scarabaeid beetles. Hypoaspis were counted on each weevil’s head, thorax, legs, sp. and Tetrapolypus rhynchophori (Acari: Pye- subelytral space, and abdomen under a dissecting motidae) have been found in association with R. microscope. The software Quantitative Parasitol- ferrugineus (Peter 1989). Tetrapolypus rhyn- ogy 3.0, specifically developed to account for ag- chophori are reported to be predators of R. ferrug- gregated distributions and to allow distribution- ineus (Lever 1969), but the frequency and extent free statistical tests, was used to compare loads to which these mites affect beetle populations re- (Reiczigel & Rózsa 2005). We quantified mean in- mains unknown (Peter 1989). To date, there are tensity (mean number of mites per weevil), mean no reports of phoretic organisms associated with abundance (mean number of mites per weevil) R. ferrugineus in the UAE. and prevalence (proportion of weevils that hosted To this end, we examined the mites associated mites) following Rózsa et al. (2000). Confidence with R. ferrugineus collected from Al Ain, UAE. intervals (at 95% confidence level) for mean in- The objectives of this study were to i) determine tensities were computed using bootstrap tech- the species composition and on-host distribution niques with 2000 replications (Rózsa et al. 2000). patterns of mites associated with R. ferrugineus; Exact confidence intervals (at 95% confidence ii) examine patterns in the prevalence and abun- level) were calculated for prevalence using the dance of mites on R. ferrugineus; and iii) discuss Clopper-Pearson method. Mean intensities and the nature of the association between the mites abundance of mites on male and female weevils and their weevil hosts. were compared using bootstrap t-tests, and P-val- ues were generated from 2000 replications (Rózsa et al. 2000). Prevalence of mites on males and fe- MATERIALS AND METHODS males was compared using Fisher’s Exact Test, with the exact P-value reported. Differences in Sample Collection and Preparation the mean intensity, mean abundance and preva- lence of different mite species found on R. ferrug- Live adults and pupae (inside cocoons con- ineus were also compared using the same meth- structed from date palm tree fibers) of R. ferrug- ods. The Index of Discrepancy was calculated to ineus were collected from infested date palm determine aggregated distributions of mites on R. plantations at Al-Ain (24° 11’ N, 55° 45’ E), UAE ferrugineus. from Mar to Nov 2008 and 2009. Adults and pu- pae were individually collected by hand from in- RESULTS fested trees and placed in plastic containers for transportation and were stored in a freezer at -20 Deutonymphs of 2 mesostigmatid mite species, °C in the laboratory. Twenty empty cocoons were Uropoda orbicularis Müller (1776) and placed in plastic containers and kept in an incu- Uroobovella sp., were identified. Deutonymphs of bator 25 °C. Drops of distilled water were added U. orbicularis (Fig. 1) were encountered on 1 sin- every 2 days to maintain good moisture condi- gle young adult R. ferrugineus collected from a tions. Containers were observed daily for 1 broken infested date palm trunk. The number of month. Uroobovella sp. deutonymphs (Fig. 2) on individ- For identification, mites were brushed off the ual male and female weevils ranged from 0 to 381 weevils using a camel hair brush and stored in and 0 to 598, respectively. Because the mean in- 70% ethanol until further processing. Mite tensity (Bootstrap t-test, P >> 0.05), mean abun- specimens were cleared in lactophenol solution, dance (Bootstrap t-test, P >> 0.05), and preva- mounted in Hoyer’s medium on microscope lence (Fischer’s Exact test, P >> 0.05) of the mites slides (Krantz 1978; Evans 1992), and exam- on males and females did not differ significantly, ined under a compound microscope. Scanning the data were pooled (Table 1). Another phoretic Electron Microscopy of selected specimens was mite of the genus Curculanoetus (Astigmata: His- done at the Central Laboratory Unit at UAE tiostomatidae) was recorded mostly in the subely- University. Uropoda orbicularis and tral space, but very rarely in other areas (Fig. 4 A, Uroobovella sp. mites were identified by Dur- D, E). mus Ali Bal, Erzincan Education Faculty, Atat- The prevalence of Curculanoetus (17.1) was urk University, Erzincan, Turkey. Curculanoe- significantly lower than that of Uroobovella (63.8) tus sp. mites were identified by Barry M. O’Con- (Fischer’s Exact test, P < 0.001). Similarly, the nor, University of Michigan, USA. Mite samples mean abundance (3.6) and mean intensity (21.2) were placed in the collection of the Biology De- of Curculanoetus was significantly lower than the partment of UAE University. mean abundance (40.2) and mean intensity (62.9) Al-Deeb et al.: Phoretic mites on Rhynchophorus ferrugineus 751

Fig. 1. Uropoda orbicularis deutonymph, (A) SEM dorsal view; (B) SEM ventral view showing anal pedicel; (C) under light microscope (×100); (D) deutonymphs aggregated on R. ferrugineus head and thorax.

of Uroobovella (Bootstrap t-test, P = 0.006 and P DISCUSSION = 0.01, respectively). Index of Discrepancy values for Curculanoetus and Uroobovella were 0.929 Deutonymph stages of 3 mite species (U. orbic- and 0.802, respectively. Mite loads on different re- ularis, Uroobovella sp. and Curculanoetus sp.) gions of the weevil also varied substantially were associated with R. ferrugineus. Uropoda or- (Fig. 3), with the greatest number of mites located bicularis and Uroobovella sp. were attached to in the subelytra in both sexes (Fig. 4 B, C). The their weevil hosts with the aid of anal pedicels, membrane wings also had large numbers of consistent with other studies (Bajerlein & mites, while the remaining regions of the weevil Bloszyk 2004). In contrast, Curculanoetus sp. harbored few mites in both sexes. Curculanoetus uses sucker plates for attachment to the weevil and Uroobovella mites were not recovered from hosts. Not all R. ferrugineus weevils were associ- the heads of weevils. Uroobovella deutonymphs ated with phoretic mites and the Index of Discrep- were not always phoretic on R. ferrugineus adults ancy values for Curculanoetus and Uroobovella (i.e. attached with anal pedicels to the weevil indicated highly aggregated distributions of these body for transportation). They were present in mites on their weevil hosts. Uroobovella very large numbers on some pupae inside the co- deutonymphs were significantly more prevalent coons (500-800/cocoon) and were noticed actively than Curculanoetus. This is likely because of food moving on the pupal exuvia. availability and environment conduciveness. In addition to uropodid mites Collembolla The large numbers of Uroobovella and Curcul- were observed on the fibers of the R. ferrugineus anoetus, especially in the subelytral space, sug- cocoons, which were incubated at 25 °C. The num- gest that this microhabitat offers protection to the bers of these microarthropods increased consider- mites as the R. ferrugineus walk on the rough ably with increasing stages of fiber decay. date palm tree trunk or under the dense fibers be- 752 Florida Entomologist 94(4) December 2011

Fig. 2. Deutonymph of Uroobovella sp. (A) SEM dorsal view; (B) under light microscope (×100). tween frond bases. From our field observations, Curculanoetus deutonymphs were found ag- this habitat was also the preferred daytime loca- gregating in the subelytral space near the base of tion of the weevils. The subelytral space probably the elytron and inside a small groove in that re- also gives the mites protection against desicca- gion. Because they were minuscule compared to tion in the extremely arid and hot desert climate the size of U. orbicularis and Uroobovella they of UAE. It can also provide phoretic mites a form could easily go unnoticed. A clear spatial separa- of protection against predatory mites, since larger tion was noticed between the deutonymphs of predatory mites such as Hypoaspis sp. usually re- Curculanoetus and Uroobovella on the elytron. main on the surface of beetles as they seek prey This could be explained by territoriality or by the (Costa 1971). Given that the subelytral space ap- presence of specific elytral morphological advan- pears to be the best choice for phoretic mites, tages utilized by each mite group. Members of the other areas of the host insect, such as membrane family Histiostomatidae have been reported to be wings are likely secondarily populated as subely- involved in phoretic associations with other in- tral spaces become overcrowded. One additional sects: Histiostoma sp., on palm weevils of the ge- possible explanation of the subelytra preference nus Rhynchophorus (Curculionidae: Coleoptera) is that in Coleoptera the elytra are not used ac- (Houck 1994), H. formosana on three subterra- tively in flight, but the membrane wings vibrate nean termite species (Isoptera: Rhinotermitidae) strongly during flight. Our findings on mite dis- (Wang et al. 2002), Histiostoma sp. on Cambala tributions on R. ferrugineus body regions were reddelli (Cokendolpher & Polyak also consistent with findings of Atakan et al. 1996), and C. rhynchophorus on R. phoenicis (2009) and Bajerlein and Bloszyk (2004). It is (Fain 1974). likely that the low numbers of mites on other A limited number of phoretic uropodid and his- body regions could also be due to overcrowding in tiostomatid mites can reasonably disperse on a R. the preferred subelytral space. ferrugineus host without an obvious impact on the

TABLE 1. COMPARISON OF LOADS OF CURCULANOETUS SP. AND UROOBOVELLA SP. MITES ON RHYNCHOPHORUS FER- RUGINEUS.

D Mean Intensity Mean Abundance Prevalence Range Mean Intensity

0-93 17.1 3.6 21.2 0.929 Curculanoetus (10.5-25.7) (1.7-7.9) (11.3-36.8)

0-598 63.8 40.2 62.9 0.802 Uroobovella (53.8-72.9) (26.5-62.1) (42.9-94.6)

Values in parentheses indicate 95% confidence levels for mean abundance, mean intensity, and prevalence computed using 2000 replications. D = Index of Discrepancy, N = 105 adults of R. ferrugineus. Al-Deeb et al.: Phoretic mites on Rhynchophorus ferrugineus 753

unpublished data). Finding a large number of deutonymphs near and on the non-flying stage (pupa) could be explained by shelter- and/or mois- ture-seeking inside the cocoon. This could also be an attempt of deutonymphs to be as near to the newly emerging adult weevil as possible in order to secure an attachment point on its body. In addition to Uoorobovella deutonymphs, col- lembolans were observed on the fibers of some of the cocoons of R. ferrugineus. Numbers of mites and collembolans increased considerably with in- creasing stages of decay at 25 °C in the laboratory. Eventually fibers dried out and resembled saw- dust. Decaying plant matter can provide food di- rectly or indirectly for many invertebrates (Lase- Fig. 3. The distribution of Curculanoetus sp. bikan 1977). In our study, soil is the likely source Uroobovella sp. deutonymphs on different regions of male of microarthropod (mites and collembolans) colo- and female R. ferrugineus. nization of the cocoons. Our laboratory observa- tions suggest that mites and collembolans pro- gressively build up their populations as decompo- sition progresses. Additionally, we observed few weevil’s ability to fly. However, excessively large uropodid adults on and in the dry remains of de- numbers on an individual insect could be a burden caying dead bodies of R. ferrugineus adults. and may limit the insect’s flight performance. It is This study did not investigate what mecha- unknown if phoretic U. orbicularis, Uroobovella, nism attracted the phoretic mites to the R. ferrug- and Curculanoetus could have a detrimental impact ineus weevils. However, it is known that R. fer- to the host, if, by virtue of their presence in ex- rugineus males produce aggregation pheromones tremely large numbers. Such potential negative im- (Oehlschlager et al. 1995) to attract individuals of pacts may include reduction in the efficiency of for- the same species. Uropoda orbicularis, aging activities or of movement, making the weevils Uroobovella, and Curculanoetus mites probably more susceptible to predation. Therefore, behav- use these pheromones to find potential hosts. Nio- ioral experiments need to be performed to illustrate gret et al. (2006) showed that the phoretic mite if high mite loads are detrimental to R. ferrugineus. Macrocheles saceri (Acari: Mesostigmata) used The negative impacts of phoresy could lead to para- semiochemicals of the cuticle as kairomonal sig- sitism and is often regarded as a transition between nals to differentiate and locate Scarabaeus dung phoresy and parasitism (Houck & Cohen 1995). beetle hosts (Coleoptera: Scarabaeidae). Behav- Parasitism generally implies some sort of transfer ioral experiments are warranted to elucidate the of resources and an associated negative effect on re- mite attraction process to R. ferrugineus. productive success of the host. Many mites live on In conclusion, this study documented preferen- hosts without seemingly harming them (Krantz tial distribution of phoretic U. orbicularis and 1978; Houck & O’Connor 1991). However, quantita- Uroobovella sp. on R. ferrugineus weevils in palm tive estimates with regard to this aspect of phoresy trees. It also documented the presence of phoretic are limited. For example, Houck and Cohen (1995) Curculanoetus sp. deutonymphs on this insect documented a transfer of fluid from the hemolymph pest and the presence of collembolans on the co- of the host beetle into the ‘phoretic’ mite, suggesting coon fibers. The interactions between these spe- a first step toward parasitism. It has been demon- cies are not necessarily straightforward and need strated that Rhyzopertha dominica (Coleoptera: further careful studies. Collectively, Curculanoe- Bostrichidae) adult take-off ability was significantly tus and Uroobovella were numerically abundant decreased in the presence of high mite loads (>7 on R. ferrugineus and the effects of this associa- mites per host) of phoretic mites (Rocha et al. 2009). tion may be more detrimental to the host than Elzinga and Broce (1988) mentioned that house suggested by mere phoresy. The possible detri- flies (Diptera: Muscidae) were so burdened with his- mental role of excessive phoretic mites on the tiostomatid hypopi that they were unable to fly or weevils needs further investigation. Large field exhibit normal behavior. surveys on microarthropods in date palm planta- In this study it was noticed that phoresy was tions is warranted as there is the possibility of not a mandatory choice for every Uoorobovella finding local natural enemies, especially on eggs deutonymph. Many of these deutonymphs were or neonates, which could be used in successful bi- observed in large numbers inside and outside co- ological control of R. ferrugineus. To our knowl- coons moving freely on the fibers and on the pupal edge, this study is the first record of U. orbicu- cast skin while adult weevils emerged from these laris, Uroobovella sp., and Curculanoetus sp. cocoons carrying phoretic deutonymphs (Al-Deeb, mites in UAE. 754 Florida Entomologist 94(4) December 2011

Fig. 4. (A) Curculanoetus sp. deutonymphs on subelytron; (B, C) Uroobovella sp. deutonymphs on subelytron un- der dissecting stereoscope; (D) Curculanoetus sp. dorsal view (×400); (E) Curculanoetus sp. ventral view showing sucker plate (×1000) under light microscope.

ACKNOWLEDGMENTS BAJERLEIN, D., AND BLOSZYK, J. 2004. Phoresy of Uropoda orbicularis (Acari: Mesostigmata) by bee- The authors thank the Central Laboratory Unit tles (Coleoptera) associated with cattle dung in Po- (CLU) at UAE University for assistance in scanning land. Eur. J. Entomol. 101: 185-188. electron microscopy; Ibrahim Cakmak from Adnan BINNS, E. S. 1982. Phoresy as migration: some function- Menderes University, Aydin, Turkey for providing the al aspects of phoresy. Biol. Rev. 57: 571-620. address of Durmus Ali Bal. BLOSZYK, J., BAJERLEIN, D., AND, BLASZAK, C. 2002. The use of pedicels of phoretic deutonymph of Uropoda orbicularis (Acari: Uropodidae) connected with co- REFERENCES CITED prophagous beetles (Insecta: Coleoptera) by Macro- cheles female mites (Acari: Macrochelidae) in the ABRAHAM, V. A., AL SHUAIBI, M. A., FALEIRO, J. R., ABU- process of dispersion. Polskie Pismo. Entomol. ZUHAIRAH, R. A., AND VIDYASAGAR, P. S. P. V. 1998. 71:241-246. An integrated management approach for red palm BLOSZYK, J., BAJERLEIN, D., GWIAZDOWICZ, D. J., HAL- weevil, (Rhynchophorus ferrugineus Oliv.), a key LIDAY, R. B., AND DYLEWSKA, M. 2006a. Uropodine pest of date palm in the Middle East. Sultan Qabus mite communities (Acari: Mesostigmata) in birds’ University. J. Sci. Res. Agric. Sci. 3: 77-84. nests in Poland. Belg. J. Zool. 136: 145-153. ATAKAN, E., ÇOBANOGLU, S., YÜKSEL, O., AND BAL, D. A. BLOSZYK, J., KLIMCZAK, J., AND LESNIEWSKA, M. 2006b. 2009. Phoretic uropodid mites (Acarina: Uropo- Phoretic relationships between Uropodina (Acari: didae) on the red palm weevil [Rhynchophorus fer- Mesostigmata) and centipedes (Chilopoda) as an ex- rugineus] (Olivier, 1790) (Coleoptera: Curculion- ample of evolutionary adaptation of mites to tempo- idae)]. Türk. Entomol. Derg. 33: 93-105. rary microhabitats. Eur. J. Entomol. 103: 699-707. Al-Deeb et al.: Phoretic mites on Rhynchophorus ferrugineus 755

COKENDOLPHER, J. C., AND POLYAK, V. J. 1996. Biology LEVER, R. J. A. W. 1969. Pests of the Palm. Unit- of the caves at Sinkhole Flat, Eddy County, New ed Nations Food and Agriculture Organization, Mexico. J. Cave Karst Stud. 58:181-192. Rome. CONTI, F., SESTO, F., RACITI, E., AND TAMBURINO, V. MURPHY, S. T., AND BRISCOE, B. R. 1999. The red palm 2008. Ecological factors affecting the spread of Rhyn- weevil as an alien invasive: biology and the pros- chophorus ferrugineus (red palm weevil). Palms 52: pects for biological control as a component of IPM. 127-132. Biocontrol News and Information 20: 35-46. COSTA, M. 1971. Mites of the genus Hypoaspis Canestri- NIOGRET, J., LUMARET, J. P., AND BERTRAND, M. 2006. ni 1884 s. str. and related forms (Acari: Mesostigma- Semiochemicals mediating host-finding behaviour ta) associated with beetles. Bull. Nat. Hist. Mus. in the phoretic association between Macrocheles Zool. 21: 67-98. saceri (Acari: Mesostigmata) and Scarabaeus spe- ELZINGA, R. J., AND BROCE, A. B. 1988. Hypopi (Acari: cies (Coleoptera: Scarabaeidae). Chemoecology 16: Histiostomatidae) on house flies (Diptera: Mus- 129-134. cidae): a case of detrimental phoresy. J. Kans. Ento- O’CONNOR, B. M. 1982. Evolutionary ecology of Astig- mol. Soc. 61: 208-213. matid mites. Annu. Rev. Entomol. 27:385-409. EVANS, G. O. 1992: Principles of Acarology. Wallingford, O’CONNOR, B. M. 1994. Life-History Modifications in CAB International. Astigmatid Mites, pp. 136-160 In M. A. Houck, [ed.], FAIN, A. 1974: Notes sur quelques hypopes d’Anoetidae Mites: Ecological and Evolutionary Analysis of Life (Acarina: ). Bull. Ann. Soc. R. Belge. History Patterns. Springer. Ent. 110: 58-68. O’CONNOR, B. M. 2009. Cohort Astigmatina, pp. 565-657 FASHING, N. J., O’CONNOR, B. M., AND KITCHING, R. L. In G. W. Krantz and D. E. Walter, [eds.], A Manual of 1996. Adaptations for swimming in the genus Acarology, 3rd edition, Texas Technical University. Creutzeria (Astigmata: Histiostomatidae), pp. 385- OEHLSCHLAGER, A. C., PRIOR, R. N. B., PEREZ, A. L., 388 In R. Mitchell, D. J. Horn, G. R Needham, and W. GRIES, R., GRIES, G., PIERCE, H. D., JR., AND LAUP, S. C. Welbourn, [eds.], Proc. Acarology IX, vol. 1. The 1995. Structure, chirality, and field testing of a Ohio Biological Survey, Columbus, Ohio. male-produced aggregation pheromone of Asian HOUCK, M. A., AND COHEN, A. C. 1995. The potential palm weevil Rhynchophorus bilineatus (Montr.) role of phoresy in the evolution of parasitism: radio- (Coleoptera: Curculionidae). J. Chem. Ecol. labeing (tritium) evidence from an astigmatid mite. 21:1619-1629. Exp. Appl. Acarol. 19: 677-694. PETER, C. 1989. A note on the mites associated with the HOUCK, M. 1994. Mites ecologically and evolutionary red palm weevil, Rhynchophorus ferrugineus Oliv. in analysis of life-history patterns. Springer. 357 pp. Tamil Nadu. J. Insect Sci. 2: 160-161. HOUCK, M. A., AND O’CONNOR, B. M. 1991. Ecological REICZIGEL, J., AND RÓZSA L. 2005. Quantitative Parasi- and evolutionary significance of phoresy in the tology 3.0. Budapest, Hungary. Astigmata (Acari). Annu. Rev. Entomol. 36: 611-636. ROCHA, S. L., POZO-VELÁZQUEZ, E., FARONI, L. R. D’A., HUGHES, A. M. 1976. The mites of stored food and hous- AND GUEDES, R. N. C. 2009. Phoretic load of the par- es. Tech. Bull. Minist. Agric. London. No. 9. asitic mite Acarophenax lacunatus (Cross & Krantz) KHANJANI, M., AND UECHERMANN, E. A. 2005. Hypoas- (: Acarophenacidae) affecting mobility pis (Hypoaspis) polyphyllae n. sp. Mesostigmata: and flight take-off of Rhyzopertha dominica (F.) (Co- Laelapidae) parasite on larvae of Polyphylla olivieri leoptera: Bostrichidae). J. Stored Prod. Res. 45: 267- Castelnau (Coleoptera: Scarabaeidae) in Iran. Int. J. 271. Acarol. 31: 119-122. RÓZSA, L., REICZIGEL, J., AND MAJOROS, G. 2000. Quan- KRANTZ, G. W. 1978. A Manual of Acarology. 2nd Edi- tifying parasites in samples of hosts. J. Parasitol. 86: tion. Oregon State University Bookstore, Corvallis, 228-232. Oregon. 509 pp. WANG, C., POWELL, J., AND O’CONNOR, B. M. 2002. LASEBIKAN, B. A. 1977. The fauna of a decay- Mites and nematodes associated with three subter- ing log of an oil palm tree (Elaeis guineesis Jacq) in ranean termite species (Isoptera: Rhinotermitidae). Nigeria. Ecol. Bull. Stockholm. 25: 530-533. Florida Entomol. 85: 499-506.