Status quo of honeybee (Apis mellifera L.) pests and ...

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Presented at: The 23 International Congress of Entomology, 6 – 12 July 2008, International Convention Centre, Durban/ South Africa.

Status quo of honeybee (Apis mellifera L.) pests and diseases in Sudan MOGBEL A. A. EL-NIWEIRI and ABDALLA A. SATTI Environment and Natural Resources Research Institute, National Centre for Research, Khartoum, Sudan. [email protected] Abstract Introduction: Honeybees are found naturally in Sudan since ancient time and traditional beekeepers are present. Recently, modern beekeeping has been flourished using imported colonies, so the threat of spreading exotic pests and diseases was expected. Since few data is available in this field, it was aimed by this work to recognize important pests, predators, diseases and parasites of honeybees and their incidences in different parts of the country. Methods: Data were collected through intensive surveys and questionnaires covering nine bee areas (States) in Sudan during the period 2003 - 07. Different modern and traditional apiaries and wild colonies were inspected, where the percentages of affected colonies by major pests or diseases were indicated in most areas. Samples taken included 122 local colonies and 350 Carnio-Egyptian colonies plus 30 colonies of Apis florea. Detected insects were mostly identified at the Insect Collection of the Agricultural Research Corporation(ARC), Sudan, whereas vertebrate species identified either at the Wild Life Research Centre, ARC or Sudan Institute for Natural Sciences. Suspected diseases were confirmed through laboratory culturing and biochemical tests followed at the Department of Microbiology, Faculty of Veterinary Sciences-University of Khartoum. Results: Lists of more than 35 pests and predators of honeybees were recorded at variable levels in different areas. They include mainly insect and vertebrate species and few spiders. Among these, twenty species were new records e.g. the hive beetles, bee wolves, squirrel and honey badger. However, many species were found causing serious problems such as Galleria moth (86.3% infested colonies), ants and two predatory birds (Merops spp.). On the other hand, all areas were found free of most bacterial and fungal diseases, except the bacterial brood disease, Serratia marcescens, found in 2.6% of Khartoum colonies. Moreover, the parasitic mite, Varroa jacobsoni, was found firstly infecting 75% of colonies in Khartoum State as new record, thenceforth detected in Sennar and Kordofan States. Conclusions: Various indigenous pests of honeybees were found in Sudan and some exotic pest and disease species were introduced through commercial beekeeping. Introduction According to Crane (1979), honeybees in tropics suffer more injury and mortality from pests attack than from diseases caused by microorganisms. In Sudan, honeybees are found naturally since ancient time, and few numbers of beekeepers are present most of them are traditional beekeepers (El-Sarrag et al., 1988). Therefore, bee colonies are generally found in various types of hives which located at different nesting sites. Wild honeybees (Apis mellifera) establish their nests in holes of trees and fallen logs, holes of white ant mounds, on rocks roofs and other similar places (El-Sarrag, 1977), while domesticated honeybees inhabit mainly traditional hives and very rarely Langstroth hives. There are at least two subspecies of honeybees in Sudan: a yellow banded group Apis mellifera sudanensis nov subsp and mixed group Apis mellifera nubica (Ruttner). The former subspecies is a little honeybee distributed all over the Sudan between latitudes 3N and 16 20’N, while A. mellifera nubica distributed along the international boundaries of Sudan, Ethiopia and Uganda (El Sarrag et al., 1992). The three clusters of the Sudanese bees were classified to three sub-clusters; the smallest bee of Sudan Apis mellifera yemenitica Ruttner, the medium bee Apis mellifera sudanensis Rashad, and the largest bee Apis mellifera bandasii (Mogga, 1988). However, another exotic small honeybee Apis florea was introduced to Sudan in 1985 (Lord and Nagi, 1987; Mogga and Ruttner, 1988). The large areas of natural vegetations plus the diverse crops cultivated in various agricultural schemes, make the environment very conducive for establishing great honeybees industry.

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Actually this situation has already attracted modern beekeeping investments, where thousands of honeybee colonies were imported every year for commercial production during the last two decades. More interest and expansion in this field is progressively increasing, hence the threat of spreading exotic pests and diseases was expected. Moreover, very meagre data is available about pests and diseases of bees in the country (Marshal, 1955; Mohamed, 1988, and El-Sarrag et al., 1993), a subject which emphasized by several scientists (e.g. El-Sarrag, 1977). Accordingly, it was aimed by this research work to recognize the prevailing pests, predators, parasites or diseases of honeybees and to study their distribution and incidences in different bee areas of Sudan. Materials and Methods Surveys, questionnaires and samplings: Surveys of pests and diseases of honeybees were carried out in nine bee areas of Sudan during the period 2003 – 2007. Such areas included Khartoum, Kordofan, Darfur, Blue Nile, Kassala, Gezira, White Nile and River Nile States in addition to southern Sudan. The surveys were supported with questionnaires, where modern and traditional beekeepers and honey hunters were interviewed about pests and diseases and any abnormalities ever been observed on honeybees colonies in their respective areas. The main purposes of the study were to indicate the prevailing species of pests and diseases and their incidences in such different areas. The inspection covered different bee colonies in modern and traditional apiaries and wild colonies of Apis mellifera. Damages induced whether on hives, wax combs, honey or honeybees individuals were reported. Moreover, the hives entrances and foraging honeybees were observed in different locations to check for the presence of bees predators. Samples taken included 122 local colonies representing 17 modern apiaries and 39 wild colonies from different States plus 324 and 26 Carnio-Egyptian colonies from Khartoum Airport and River Nile State, respectively. About 30 colonies of Apis florea from Khartoum and River Nile were also included. Detection of pests and predators: Identification of insect pests and predators were mostly done at the Insect Collection of the Agricultural Research Corporation(ARC), Wad MedaniSudan, whereas vertebrate species were identified either at the Wild Life Research Centre, ARC or Sudan Institute for Natural Science. But, the authors depending on morphological and behavioural characters according to literature (e.g. Williams and Arlott, 1989, and Kingdon, 2001) recognized some well known species. However, counts of damage or infested colonies were done for important pests and the percentages of affected colonies were indicated in most areas. Finally, lists of the detected species were prepared. Detection of diseases and parasites: Symptoms of brood diseases (Foulbrood, Stonebrood, Chalkbrood and Sacbrood) were observed carefully in all areas. Suspected combs were wrapped with papers and transferred to the laboratory for further investigations and biochemical tests according to El-Sanousi et al. (1987), Cowan and Steel (1993) and Shimanuki and Knox (2000). Hence, Foulbrood was checked utilizing the Rop test and microscopic examination. For the presence of Paenibacillus larvae spores, beeswax samples were boiled in water and after removal of cake the water was centrifuged at 5000G for 20 minutes before the sediment being examined under the microscope. Also, steps adopted by the first two authors for isolation, culturing, examination and biochemical tests leading to identification of Serratia marcescens were followed at the Department of Microbiology, Faculty of Veterinary Sciences-University of Khartoum. Moreover, antibiotics sensitivity test was also done for checking this disease using the Plasmatic Lap. Products ltd. Disk (Buxton and Fraser, 1977). Regarding protozoan parasites (e.g. Nosema), clean preparation of mounts from digestive tracts of bees were obtained and examined under the high dry objective of a compound microscope as described by Shimanuki and Knox (2000). A washing technique of adult bees described by the same latter author (2000) was also followed in checking Varroa parasitic mite. In addition, inspection of capped brood cells for any mites presence was achieved using magnifying lens, where the cell walls being illuminated with the aid of small hand torch. The tobacco smoke detection technique was used according to Morse and Hooper (1985) for mites inspection in three imported patches (108 packages)of honeybees. On the other hand, the tracheal mite (Acarapis woodi) inspection was also considered according to Shimanuki and Knox (2000).

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Results Insect pests and predators: Numerous species of insect pests and predators were recorded during this study, causing variable damage to honeybee colonies in different parts of the Sudan. Some species are affecting wax combs, honey and hives, while others are predators on bees, among which are some predatory spiders. A list of more than twenty encountered insect pests and predators (including spiders) is shown in table (1). Table 1.The encountered insect pests and predators (+spiders) of honeybees in Sudan, during the study period 2003-07. Vernacular names

Arabic common name

Order

Species

Location

Bee wolf (Palarus)

Daeb El nahel

Hymenoptera

Palarus latifrons

In most locations

Bee wolf

Daeb El nahel

Hymenoptera

Philanthus triangulum

Kordofan

Hornet#

Daboure El ballah

Hymenoptera

Vespa orientalis

Khartoum and Eastern Sudan

Ants

Namel

Hymenoptera

Three spp.?

In most locations

Death’s head (hawk) moth

Farashat El simsim

Lepidoptera

Acherontia atropos

In most locations

Greater wax moth

Dodat El shama

Lepidoptera

Galleria mellonella

In most locations

Small hive beetle

Khanfoos

Coleoptera

Aethina tumida

Darfur, Blue Nile, Kordofan,Khartoum

Isoptera

Hyplostoma fuligineus Various spp.

Darfur and Blue Nile In some locations

Gamol Elnahel

Diptera

Braula sp

Kordofan

Robber fly

Elzubab Elsarig

Diptera

?

Locusts*

El Grad

Orthoptera

Various spp.

Kordofan and Darfur Darfur

Earwigs

Ebret Elagos

Dermaptera

?

Darfur

Silverfish

Elsemak Elfidi

Thysanura

?

Khartoum

Cockroaches

Serasir

Dictioptera

?

Khartoum

Praying mantids

Faras El Naby

Dictioptera

Mantis spp.

In most locations

Dragonflies

Elraashat

Odonata

Various spp.

In most locations

Spiders◙

Ankabout

Araneida

Various spp.(e.g. salticids&thomicids)

In most locations

Large hive beetle

Khanfoos

Coleoptera

Termites

Arda

Bee lice*

(?) = Unidentified species. * = This pest is only documented by questionnaire # = This pest is only documented by literature ◙ = Belong to the class Arachnida (all other species are members of Insecta)

The results of the questionnaire conducted showed that about 64.5%, 95.7%, 22.6%, 7.5%, 59.1%, 8.6% and 2.2% of the respondents mentioned wax moth, ants, wasps, hawk moth, beetles, termites and spiders as pests of honeybees in Sudan, respectively. However, the counts of important insect pests at different States (Table 2) also proved more or less the

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same results as shown by the questionnaire. The mean percentages of infested colonies by greater wax moth, ants (different species), small hive beetle, large hive beetle, and hawk moth were, 86.3 % 77.3 %, 2.4 %, 2.2 % and 0.5 %, respectively. About three unidentified species of ants were considered as serious pests of natural honeybee colonies and apiaries in different parts especially in Darfur area. They include a big black species, locally called ‘El nehsha’, which causes absconding of bee colonies and it was suspected to be a carpenter ant, Componatus sp. The second is small red, probably be a pharaoh ant (Monomorium pharaonsis) while the third is small black ant called ‘El der’. Table 2. Percentage of colonies infested by major insect pests of honeybees in eight different States of Sudan. Infestation percent

Mean percent

States Insects

Khart .

Kord.

Darf.

Blue Nile

Kass.

Gez.

White Nile

River Nile

Greater wax moth 100.0 100.0 24.0 66.6 100.0 100.0 100.0 100.0 86.3 (Galleria sp.) Ants 32.0 36.4 100.0 100.0 50.0 100.0 100.0 100.0 77.3 (various spp.) Small hive beetle 0.0 0.0 8.0 11.1 0.0 0.0 0.0 0.0 2.4 (Aethina tumida) Large hive beetle 0.0 0.0 12.0 5.6 0.0 0.0 0.0 0.0 2.2 (Hyplostoma sp.) Hawk moth 4.3 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.5 (Acherontia sp.) Bee wolf + (Philanthus sp.) Bee wolf + + + + + + (Palarus sp.) (+) Present ; (-) Absent ; Khart. = Khartoum ; Kord. = Kordofan ; Darf. = Darfur ; Kass. = Kassala ; Gez. = Gezira.

Vertebrate pests and predators: The detected vertebrate pests and predators of honeybees are shown in table 3. Besides the tabulated mammalian species, man (honey-hunters), livestock (horses, cattle and camels) and baboons were also regarded as major pests of honeybees in Sudan. Baboons were reported as a pest of honeybee colonies only at the south of Blue Nile State. This area also showed high pressure on wild bees by honey hunters. However, all mammalian species plus one species of lizard (Agamma sp.) in addition to two bird pests (Indicator indicator and Bucorvus abyssinicus) were recorded for the first time as pests of honeybees in Sudan. Although, the former bird species was documented by questionnaires in such regions, it was observed only in Darfur State. Regarding predatory birds, five Merops spp. were dominant in different locations, as shown in table 4. The highest species percent (80%) of the bee-eaters were observed in Khartoum and Gezira States and the lowest (20%) in Kordofan and Kassala States. Merops pusilus was observed in 87% of the surveyed area and later on also found in Northern State, followed by M. orientalis (62%) and M. apiaster (50%). Reptiles, represented by three species of lizards (Mabuya striata, Chalcides ocellatus and Agamma spp.), were found. The latter species were the first record in Darfur area, while the other two were found in all locations but they were only observed under and inside Langstroth hives in Khartoum State. Damage of some mammalian and bird pests, as documented by questionnaires, is shown in table (5). Birds were found to induce more damage than mammalian pests. B. abyssinicus causes the greatest damage (18.3%) and was appeared to be a pest of traditional hives (open & damaged hives) of honeybee colonies especially in Darfur State (Kaboum area) (Pl. 1). According to table (6) about 60.3% of the respondents in questionnaires recorded B.

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abyssinicus as a pest of honeybee colonies followed by bee-eaters (41.1%) and finally honey guide (5.5%). Considering all pests (Table 7), 82.8% of the respondents mentioned birds as pests of honeybees in Sudan, while 38.7%, 31.2%, 23.7% and 6.5% indicated honey badger, squirrels, lizards and other pests such as man (honey robbers), livestock (camels and cattle) and monkeys, as major pests. On the other hand, Merops apiaster and M. nubicus are dangerous predators in apiary, while the other species of bee eaters (M. albicolus, M. orientalis and M. pusilus) have less importance to beekeepers and they were not seen preying on bees.

Table 3. List of vertebrate pests and predators attacking honeybees in Sudan. Vernacular Arabic common Order Species Location names name Reptiles Zwahif Mabuya striata Lizards Sahali Squamata Khartoum Chalcides ocellatus Khartoum Agamma spp. Darfur Birds Tuor Merops apiaster Bee-eaters War war Coraciiformes Found in half locations M. nubicus Coraciiformes BlueNile,Gezira & WhiteNile M. albicolus Coraciiformes Khartoum M. orientalis Coraciiformes Found in half locations M. pusilus Coraciiformes Found in most locations Indicator indicator Honey Morshed Elasel Darfur and guide* (krima) Blue Nile Bucorvus abyssinicus Kordofan, Darfur Ground Abu ondolok Coraciiformes Hornbill &Blue Nile Mammals Thadiat Mell ivora capensis Honey Therban Carnivora Kordofan, Darfur badger* &Blue Nile Squirrel Sengab Rodentia Darfur * Indicated that this pest is documented by questionnaire

Table 4. Distribution of bee-eater species in 8 different States of Sudan. Bee Khart. Kord. Darfur Blue Kass. Gezira White River eaters Nile Nile Nile Merops +++ +++ +++ + apiaster Merops +++ ++ + nubicus Merops + albicolus Merops ++ ++ ++ ++ + + + pusilus Merops + + + + + orientalis Species 80% 20% 40% 60% 20% 80% 40% 60% percent (+) = less than five birds, (+ +) = more than five, (+ + +) = flock, (-) = absent

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Distribution Percent 50.0% 37.5% 12.5% 87.5% 62.0%

Table 5. The percent damage caused by some vertebrate pests (mammals and birds) to honeybee colonies in traditional hives during 2002-2003 (data obtained by questionnaires). Mammals &Birds Honey badger( Mellivora capensis) Rodent (squirrels) Hornbill (Bucorvus abyssinicus) Mean

No. of traditional hives 3092 3092 3092 3092

(a)

Damaged hives Numbers Percentage 32 1.0 % 231 7.5 % 565 18.3 % 276 8.9 %

(b)

Plate 1. (a) Intact traditional hive of honeybee; (b) Symptoms of damage on a traditional hive caused by ground hornbill bird.

Table 6. Distribution of respondents according to bird pests of honeybee, which found in Sudan. Yes No Total Horn bill Count 44 29 73 Percent 60.3% 39.7% 100.0% Bee eater Count 30 43 73 Percent 41.1% 58.9% 100.0% Honey guide Count 4 69 73 Percent 5.5% 94.5% 100.0%

Table 7. Distribution of respondents according to animal pests of honeybee, which found in Sudan Yes No Total Birds Count 77 16 93 Percent 82.8% 17.2% 100.0% Squirrels Count 29 64 93 Percent 31.2% 68.8% 100.0% Rats Count 93 93 Percent 100.0% 100.0% Honey badger Count 36 57 93 Percent 38.7% 61.3% 100.0% Lizards Count 22 71 93 Percent 23.7% 76.3% 100.0% Other things Count 6 87 93 Percent 6.5% 93.5% 100.0%

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Detection and incidence of diseases: As shown in table 8, all inspected colonies in all locations were found free from brood diseases except the Serratia marcescens. This brood disease was restricted only to Khartoum location at an incidence of 13.5% (2.6% of the total inspected colonies). On the other hand, a none infective dysentery was the only adult disease found during this survey infecting 18.2% of Kordofan colonies (1.7% of the total inspected colonies). In the course of identification of S. marcescens, isolates of the dead honeybee larvae were grown in pure culture (Pl. 2a) and the spores of the causal organism were depicted (Pl. 2b). Growth on blood agar consisted solely of small white colonies 1-2 mm in diameter, slightly raised with convex surfaces. Most of the affected larvae were in the pre-pupal stage. The cappings of the cells containing dead brood were punctured and sunken in appearance. Only 1-2 combs had dead larvae in every infected colony. Direct smears from dead larvae, when examined microscopically, revealed minute gramnegative rods arranged singly and in groups. No morphological difference was observed between the slide taken from the pure culture and that taken from smears. Pl. (2c) shows the antibiotics sensitivity test by using the plasmatic Lap. Products ltd disk. In the disk assay the bacteria was found to be susceptible to streptomycin, ampicillin, chloramphenicol and tetracycline, but resistant to cloxaillin, penicillin, gentamicin, and erythromycin. The properties of the isolate were presented in table 9. It was gram-negative rod, motile. Produce acid and gas from glucose, utilized sucrose as carbon sources. None of the isolates produced oxidase, or utilized malonate or lactose. None produced H2S, aerobic and facultatively anaerobic, Catalase, citrate, and KCN positive. The organism was thus diagnosed as Serratia marcescens according to El-Sanousi et al. (1987) and Cowan and Steel (1993).

Table 8. Percent of diseased and parasitized honeybee colonies in 8 different States of Sudan (No. of infested colonies/ No. of inspected colonies). Diseases Overall percent States Kh. 0

Kor. 0

Dar. 0

B.N. 0

Kas. 0

Gez. 0

W.N. 0

R.N. 0

0.0%

0

0

0

0

0

0

0

0

0.0%

13.5%

0

0

0

0

0

0

0

2.6%

Chalkbrood

0

0

0

0

0

0

0

0

0.0%

Sackbrood

0

0

0

0

0

0

0

0

0.0%

Stonebrood

0

0

0

0

0

0

0

0

0.0%

Nozema

0

0

0

0

0

0

0

0

0.0%

Dysentery

0

18.2%

0

0

0

0

0

0

1.7%

Varroa jacobsoni Acarapis woodi

75.2%

0

0

0

0

0

0

0

10.3%

0

0

-

0

0

0

0

0

0.0%

Tropilaelas clareae Euvarroa sinhai

0

0

-

0

0

0

0

0

0.0%

0

0

-

0

0

0

0

0

0.0%

American foul brood European foul brood Serratia brood

Kh.= Khartoum; Kor.= Kordofan; Dar.= Darfur; B.N.= Blue Nile; Kas.= Kassala; Gez.= Gezira; W.N.= White Nile; R.N.= River Nile; (-)= Not inspected.

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a) b) c) Plate 2. (a): Pure culture of Serratia bacteria isolated from dead larvae of honeybee; (b): Spores of Serratia marcescens; (c): Anti biotic sensitivity test.

Table 9. The test of Serratia marcescens isolated from dead honeybee larvae. Test Result Test Result Test Gram - tive Indole - tive H2S Motile + tive Urease - tive S.F KCN + tive Sucrose + tive MacConkey growth Simmons’citrate + tive Malonate - tive Oxidase Glucose (gas)

+ tive

MR

- tive

Catalase

Result - tive + tive - tive - tive + tive

Detection and incidence of parasitic microorganisms: No infectious protozoan parasites were detected from the routinely conducted examinations. Hence, it was declared that Nozema parasite is not found in Sudan, although a non infective dysentery was observed as mentioned previously (Table 8). Regarding parasitic mites (Acarina) no infected colonies were detected from the Tobacco Smoke Technique in this study. However, results of Washing Technique revealed the presence of the parasitic mite Varroa jacobsoni. Infestation was firstly found in Khartoum State (75.2% infested colonies; Table 8), then detected on imported colonies in Sennar, Gezira (Um Elgura) and Kordofan States during the last year. This mite was not yet detected in southern Sudan. The inspection of brood cells showed that V. jacobsoni was only found in the brood of infested colonies. Wild colonies showed about 27% level of infestation. However, no mites were found in all samples of A. florea inspected in this study. Moreover, the Tracheal mite (Acarapis woodi) was not found in any inspected location (apiaries or wild colonies) of Sudanese honeybees or the imported Carnio-Egyptian (F1) honeybees. However, the presence or absence of such acarine mite were not ensured in Darfur State. The results of questionnaire concerning the awareness of beekeepers about honeybee diseases and the impact of importation on disease spreading are shown in tables 10 and 11, respectively. 94.6% of the respondents mentioned that there was no diseases of honeybee in Sudan, while 5.4% of the respondents mentioned the opposite. Nevertheless, the response showed significant relation between the importation of honeybee and disease incidence (p< 0.00).

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Table 10. Distribution of respondents according to honeybee diseases, which found in Sudan. Yes No Total Disease

Count Percent

5 5.4%

88 94.6%

93 100.0%

Dead larvae

Count

3

2

5

Percent

60.0%

40.0%

100.0%

Table 11. Relation between importation of honeybees and diseases, according to respondents. Disease Total yes No Introduce of Yes Coun 5 22 27 honeybees % of 5.4% 23.7% 29.0% No Coun 66 66 % of 71.0% 71.0% Total Coun 5 88 93 % of 5.4% 94.6% 100.0% Chi-Square tests Value Df sig Pearsin Chi-Square 12.917 1 0.000

Discussion The already documented species of insect pests and predators of honeybees include the bee wolf (Philanthus sp.), hornet, ants, hawk moth and greater wax moth (Marshal, 1955; Abd alla, 1988; Mohamed, 1988, and El Sarrag et al., 1993). On the other hand, the rests of the list were considered as new records. The wax moth was found as the most dangerous pest of wax combs of Apis mellifera in most areas, but it was not detected in all inspected colonies of A. florea. The importance of this pest in Sudan was also indicated by several scientists (Marshal, 1955; Nagi, 1984, and Abdalla, 1988). The reasons why A. florea colonies were free of infestation could be due to the fact that the wax moth as noctuid insects they preferred dark habitats, but A. florea used to build its nests in open areas which seem to escape infestation in most cases. On the other hand, the detection of hawk moth, Acherontia atropos, in weak colonies or in untightly closed hives in Khartoum State was also supported by the beekeepers in other States. Smith (1960) stated that the hawk moth might be found on unguarded combs in weak colonies, but strong colonies threw them out in small pieces. However, the pest was firstly reported in Southern Sudan (Marshall, 1955), then two species (Acherontia styx and A. Atropos) were detected to be found (Ahmed, 2002). No bee lice was found because no bee queens were inspected during this study. Bee lice and locust were documented only by questionnaire. The small hive beetle was identified according to Lundie (1940) and Delaplane (2000). It was firstly found in Darfur and Blue Nile and now arrived Kordofan, Gezira and Khartoum States through the movements of beekeeping. Moreover, some insects observed robbing honeybees in western Sudan were suspected to be a robber fly. It was found difficult to catch them for proper identification; hence, they may need to be confirmed. Although, the horn wasp, Vespa orientalis, has already been reported in some neighboring countries such as Egypt (Wafa, 1956) and Saudi Arabia (El-ghamdi, 1990), it was neither being observed nor documented by any beekeepers during the present study. In Sudan it was considered both as a pest of honeybees (Abd alla, 1988, and Mohamed, 1988) and as a pollinator of crops (El-Sarrag et al., 1993). Anyhow, the existence of this species was documented according to the Insect Collection, ARC- Wad Medani, but the pest may not yet be considered as a problem for the Sudanese honeybees, at least in the surveyed areas.

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The bee wolf, Palarus latifrons, was recorded for the first time during this study in Sudan, preying on bees at the front of hives in different States. The predator was so numerous in Kordofan area to the extend that it drastically decreases honey production especially during autumn seasons. Another bee wolf, Philanthus triangulum, was detected only in Kordofan area, preying on foraging bees away from hives. Specimens of both predators were identified at the Insect Collection, ARC, Wad Medani. The high concentration of these insects in Kordofan area could be attributed to the sandy soil of this region, which seems to be preferred by the wasp for nest building. Such finding came in line with Smith (1960) who reported similar problems induced by P. latifrons in central and southern Africa. The predator was also reported as a new fauna in four areas in Saudi Arabia, causing problems for honeybees (El-ghamdi, 1990). According to El-Borollosy et al. (1972) P. triangulum was reported in Egypt, especially in places of sandy soils. However, Philanthus sp. was said to be found in Sudan (Abd alla, 1988, and Mohamed, 1988) and Saudi Arabia (El-ghamdi, 1990). But, since P. triangulum and P. latifrons have more or less similar behaviours, it seems to be difficult for non experts to differentiate between them visually. The unique difference may be that the former species are not found preying on honeybees around hives, as reported for Palarus wasp (Frisch, 1954, and Smith, 1960). Therefore, the Philanthus sp., which was reported by Abd alla (1988) and Mohamed (1988) could probably be a miss-identified Palarus latifrons. However, among predators of honeybees, different species of spiders (Araneida) were observed preying on foraging bees especially when landing on flowers of different crops. Members of the jumping- (Salticidae) and crab- (Thomisidae) spiders were particularly important predators. The troubles created by ants to honeybee colonies were also documented in several tropical countries, like India (Singh, 1962), Uganda (Roberts, 1971) and South Africa (Lindsey and Skinner, 2001). In Sudan Abdalla (1988) listed ants as one of the major pests of honeybee colonies, especially during dry seasons. Similarly, the reported damage of termites agreed with the finding of Singh (1962) who mentioned the importance of white ants (e.g. Termites obesus (Rab.)) as important pests of wooden hives and other apiary appliances in India. However, it was also indicated from observations that the bee wolves were the most dangerous predators of honeybees especially in Kordofan area, but no true counts on their numbers were performed as seemed to be difficult with such flying insects. Locusts were sometimes devastating flowering vegetations causing severe indirect effects on honeybee forage sources, and the insecticides used for locust control is an additional threats to honeybees. On the other hand, other species considered as secondary pests and predators of honeybees included earwigs, silverfish, cockroaches, praying mantids, dragonflies and robber flies. Honey hunters usually destroy great numbers of wild bee nests in search of honey. They were considered as one of the main factors hampering natural increase of honeybees in Sudan. Sanford (1987) and Ntenga and Mugongo (1992) mentioned man as the greatest pest of honeybees. Moreover, Mogga (1996) reported that honey hunters in Sudan apply much fire and smoke to drive out defender bees when the whole colony is destroyed or much of bee population is killed. Honey badger was recorded as a pest of honeybee colonies in Sudan for the first time in this study. This finding supported Ntenga and Mugongo (1992) who listed honey badger as one of several hazards to beekeeping industry in Tanzania. Squirrels, as well as honey badgers, were observed inhabiting wild and traditional hives. According to the majority of traditional beekeepers, squirrels chew the traditional hives, enter inside them and cause absconding of bee colonies. This result came in line with Caron (1978) who stated that squirrels chewed and destroyed combs to obtain honey and pollens for food supply, and bee equipment should be stored in rodent proof areas to avoid destruction by squirrels. Moreover, it is well known that livestock provoke honeybee colonies. Several traditional beekeepers complain from camels, since camels' odour causing absconding of honeybee colonies. Caron (1978) reported that colonies should not be located in proximity to the area where large livestock are present. The bee-eaters, Merops apiaster and M. nubicus were considered as dangerous predators because they attack honeybee colonies in large flocks. M. nubicus harm is less than M. apiaster because it has other alternative hosts i.e., locust. Numbers of this bird were observed congregated around grass fires because they have learned that bees were abundant when honey hunters apply much fire and smoke to avoid bee stings. Other insects were also abundant when farmers burned grasses with fire. Although, M. orientalis and M.

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pusilus are widely distributed, they are considered harmless to beekeeping industry because they were not observed preying on bees in flocks. Moreover, the latter species has alternative hosts. The honey guide, Indicator indicator, is well known to honey hunters that guide them to bee nests. It was observed only in forests of Darfur State. This supports Friedmann (1955a) who reported that the guiding behaviour is less common in populated areas, where the number of ratels and baboon are reduced, than in less populated areas. Only the adult birds eat the comb for the wax, which they can digest. They also eat adult bees (Friedmann, 1955b). Similarly, the study revealed the ground hornbill Bucorvus abyssinicus as a first record pest of traditional hives of honeybees in Sudan. Its damage to hives entrances was confirmed by the majority of traditional beekeepers in Darfur State. However, it is believed that such high damage can not be done by this bird alone. Other factors may share in this damage such as rains, wind or other animals. Although the American foulbrood (AFB) is present in most neighboring Arab countries like Saudi Arabia, Jordan, Palestine, Libya, Tunis, Algeria, and Morocco, but some others including Sudan (Anon., 1995), Egypt and Yemen are said to be free from this disease. This could be attributed to plant quarantine justifications, which prevent importation of honeybee colonies in honeybee nuclei. However, Paenibacillus larvae spores were not detected because hive products (beeswax) that inspected was imported from Egypt, which is free from AFB as reported by The Arab Organization For Agricultural Development (Anonymous, 1995). But, the absence of the European foulbrood (EFB) bacterial disease could be due to it’s rare occurrence in Africa. Smith (1960) reported that EFB had not been found in the Tropics, but there were occasional outbreaks in Europe and North America. Recently, it is expected to be spreading in Africa as a result of importation of honeybee colonies in nuclei. On the other hand, the absence of Chalkbrood fungal disease in Sudan could be attributed to the fact that the beekeepers do not used to import pollen grains to feed their bees. ElGhamdi (1990) referred the infection by this disease in Saudi Arabia to the importation of large quantities of pollen grains by beekeepers. The described results of biochemical properties and antibiotic sensitivity test of Serratia marcescens were came in consistency with the findings of El-Sanousi et al. (1987). Although Serratia disease was noticeable in Shambat apiary since earlier time, but it was detected this time in hives kept in Khartoum forest. Data obtained proved that the disease was associated with the importation of honeybees. Moreover, it was suggested that the Serratia bacterial disease could be spread among the wax moth (Galleria mellonella) as stated by El-barony and Hejazi (1994). S. marcescens is not a well known pathogen to honeybees, however new record confirmed that. This disease was identified in dead and diseased larvae in Iraq in 2000 (Al-kazzaz and Al-kazzaz, 2002). Viral disease symptoms were not observed during the current research. However, more investigations on viral diseases must be done because infected adult honeybees are not easily detected as it needs sophisticated techniques which often ignored by bee inspectors and beekeepers. The absence of Nosema disease might be attributed to the hot weather in Sudan. Also, there was no dealing of package bees and no bees used for pollination in green houses. Bailey (1963) suggested that development of the Nozema parasite is inhibited during the summer by temperature, later he attributed that to the bees being freely in summer to defecate away from the colony and the chances of bees contacting spores decrease. So infection declines. The disease usually manifests itself in bees that are confined, so the heartiest infections are found in winter bees, package bees and bees from hive used for pollination in green houses (Shimanuki and Knox, 2000). Nevertheless, more investigations must be done because symptoms of the disease are not clear-cut and sometimes, even at high levels of infection, are difficult to detect (Sanford, 1987). However, the dysentery found at Kordofan area was attributed to the fermented honey that consumed by the infected colonies. The term ‘dysentery’, as used by beekeepers, refers not to any infectious disease but to the involuntary discharge of excreta by the adult bees within and near the hive in late winter. Such dysentery, according to Anon. (1969), is caused by the consumption of unsuitable food during the winter acid-inverted sugar for example, or honey which is too watery. Varroa jacobsoni was reported for the first time in this study. It was firstly found in Khartoum State, thenceforth detected in Sennar, Kordofan and Gezira States and expected to be dispersed to other places that imported honeybees. The importation of honeybee colonies was considered to be the main reason of introducing this dangerous mite in Sudan. It was

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observed that this mite preferred drone brood to worker brood and this result agreed with Ritter and Ruttner (1980) who stated that the most severe parasitism occurs on older bee larvae and pupae, with the mite preferring drone brood to worker brood. Male mites weren’t observed during this survey in accordance to Delfinado-Baker (1984), who reported that male mites are rarely encountered. Mite population levels were found to be high during winter months and quite low in summer months. This could be attributed to the high temperature in summer and this result is similar to what has been mentioned by Webster and Callaway (1992) in that mite levels were generally quite low, and difficult to be caught during the mid-summer (June and July) period. The proportion of fallen mites increases during very hot weather (Webster et al., 2000). Regarding the life cycle of Varroa it seems likely that those genetic stocks of bee with shorter worker developmental rates will be less severely affected by Varroa, because few or no mites will mature to the infective stage before the bees can leave their cells as adults (Ramirez and Otis, 1986). As Sudanese honeybees belong to African honeybee races (Ruttner, 1976), the total developmental period from egg oviposition to emergence of the Sudanese honeybee worker was found to be 19.26 days (Gasma,1982). Therefore, the native honeybees might be resistant to the parasitic mite Varroa jacobsoni.

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