IJABR Vol. 10(1): 37- 51 (2019)

Original article

SURVEY OF THE DISTRIBUTION AND DIVERSITY OF (INSECTA: BLATTARIA) ON THE CAMPUS OF A HIGHER INSTITUTION IN SOUTH-WESTERN NIGERIA Sosan, M.B*., Ajibade, R.O. and Adeleye, A.O. Department of Crop Production and Protection, Obafemi Awolowo University, Ile-Ife, 220005, Nigeria

Submitted: April, 2019; Accepted: May, 2019; Published: June, 2019

ABSTRACT

Cockroaches are pests of medical and public health importance. They play a role in disseminating pathogens, serve as intermediate hosts of parasites, causes allergic effects like asthma and could cause entomophobia. This study was conducted to investigate species composition, relative abundance, and population diversity of cockroaches in Obafemi Awolowo University, (OAU) Ile-Ife, Nigeria. The were trapped between 2015 and 2017 in locations within Obafemi Awolowo University Campus, Ile-Ife, Nigeria. These were identified and biodiversity index was calculated. A total of 867 cockroaches was trapped from various locations during the survey period (2015-2017) and seven species of cockroaches from two families were identified. The Blatellidae family include German , ( germanica L.), brown-banded cockroach (Supella longipalpis F.), and field cockroach (Blattella vaga Hebard) while the Blattidae family include American cockroach (Periplaneta americana L.), oriental cockroach (Blatta orientalis L.), Australian cockroach (Periplaneta australasiae F.), and smokey brown cockroach (Periplaneta fuliginosa Serville). The B. germanica and P. americana accounted for 78% of the total specimens collected. The proportion of other species included B. orientalis (7.2%), S. longipalpis (5.0%), B. vaga (4.0%), P. fuligonosa (3.7%) and P. australasiae (2.1%). The relative abundance of the insects are in the order, B. germanica > P. americana > B. orientalis > S. longipalpis > B. vaga > P. fuliginosa > P. australasiae. The species diversity was low for all sampling years and there existed the dominance of German and American cockroach over other species. This study provided baseline information on the cockroach species present and their prevalence in the University community, thereby giving an insight into the likely incidence of diseases caused by infestation of different cockroach species that could pose health risks to humans. Keywords: cockroach species; relative abundance, diversity, dominance *Corresponding Author: [email protected] INTRODUCTION The American (Periplaneta americana), German (Blattella germanica), oriental (Blatta Cockroaches are insects, which have been in orientalis), smokey brown (Periplaneta existence since ancient times [1]. There are fuliginosa), and brown-banded (Supella about 4,600 valid species of cockroach but longipalpis) cockroaches are the common only 30 species are considered pests [2, 3]. species that inhabit homes [4]. 37

Sosan et al. International Journal of Applied Biological Research 2019 The cockroach dwells in any place where food, the world, there are records of different water and shelter are available and can reside insects’ species available within any both indoors and outdoors while some often geographical region. For instance, the records reside in commercial and large buildings such and biodiversity of cockroaches in other as restaurants, hostels, grocery stores, countries of the world have been bakeries, food processing facilities, hotel documented; In Yasuj City, south-western rooms, nursing home, bathrooms, basements Iran, only five species of cockroaches have and plumbing areas and kitchen [5, 6]. Their been reported [26] and a checklist of 26 biology such as filthy habits, undiscriminating species of cockroaches reported in all part of diet, feeding mechanisms and morphology, the country [27]. In Pakistan, four species make them suitable to at least acquire, were reported [15] while in Malaysia, 10 mechanically transport and spread pathogens species and 6 species respectively were [7]. They contaminate the food by leaving an reported [28, 29]. In Thailand, 12 cockroach oily lipid that has offensive odour or contain species were noted [30] but in Turkey and bacteria that can cause food poisoning [8] Cameroon, only 3 species were identified [31, probably because they frequently feed on 32]. However, there is dearth of information human faeces [9]. on species composition, relative abundance and biodiversity of cockroaches in Nigeria Cockroaches are pests of medical and public most especially in the study area. Therefore, health importance and they play an important the present study was undertaken to role in disseminating bacteria and serve as investigate species composition, relative intermediate hosts for pathogenic helminths, abundance, and population diversity of viruses, protozoa and fungi that affects human cockroaches in OAU, Ile-Ife, Nigeria with a [1, 7, 10, 11, 12, 13] and thus regarded as view to updating the existing information on insects recognized to be mechanical vectors of this insect. disease-causing agents [14]. For instance, the cockroach-borne pathogenic bacteria causes typhoid fever, food poisoning, amoebiasis, MATERIALS AND METHODS shigellosis, dysentery, and urinary infections Study area [15, 16]. In Nigeria, the incidence, species The study was carried out at Obafemi composition and relative abundance of Awolowo University campus, Ile-Ife, Nigeria. parasites and pathogens present in one or two Ile-Ife is an ancient town in southwest Nigeria most common cockroaches and their located on Latitude 7o 31ꞌ 06ꞌꞌN, Longitude 4o potential to cause diseases have been 31ꞌ 22ꞌꞌN and 244 m above sea level. The reported [17, 18, 19]. Studies have reported University is located within the tropical robust association between cockroach climate with rainy season which starts from infestation and development of asthma as April to October and the dry season which relevant allergens have been identified in the runs from November to March. body and secretions from the insect body [20]. Obafemi Awolowo University (OAU) formerly Exposure to cockroach allergens (through University of Ife was established in 1962 and saliva, fecal material, secretions, cast skins, situated on a vast expanse of land and debris, and dead bodies) are connected with comprises of central campus area, the student asthma-related health problems [9, 15, 21, 22, residential areas, the staff quarters, and a 23]. The allergen and potential health hazard Teaching and Research Farm (T&RF). There associated with cockroaches can also cause are nine halls of residence in the University entomophobia [1, 24]. with an estimated population of about 40,000 Most of the species of cockroach are found in students with the rooms originally designed the tropics but only few occur in temperate for between 2 and 4 students but now regions [2, 3]. Nigeria is an afro-tropical officially have between 8 and 10 students per country in which vast majority of insects are room due to large increase in student unknown [25], whereas, in other countries of admission without corresponding increase in

38

Sosan et al. International Journal of Applied Biological Research 2019 hostel facilities [33]. This has resulted in an were placed in labelled collection boxes for increased pressure on existing facilities with preservation at the insectarium. increased garbage accumulation which could lead to the spread of cockroaches in the halls Data analysis of residence. Another feature among OAU The data on individuals trapped were students as common in most Nigerian normalized using square root transformation University hostels is the stocking of foodstuffs and subjected to Analysis of Variance by individual students inside their rooms, (ANOVA). The means were separated using especially under their beds and inside the Fisher’s Least Significant Difference (LSD) at wardrobe [33, 34]. These practices among p = 0.05 using the SAS statistical package [37]. others, largely contribute to the proliferation Bar chart was also used to show trend of of cockroaches in the students’ halls of cockroaches’ population encountered during residence. the sampling period.

Sample collection Abundance and biodiversity indices Surveys were carried out in halls of residence Relative abundance (RA) is the population of of the University between 2015 and 2017 as individual species divided by total population part of the student collection for Agricultural of species in percentage. population of individual species Entomology course. For each year, students RA = x 100 were divided into 10 groups to search and total population of species collect cockroaches. The insects were Shannon Diversity Index (H) is an index that collected randomly with the help of sticky is commonly used to characterize species traps and hand catch method using sterile diversity in a community. It accounts for both hand-gloves. The yellow sticky traps were abundance and evenness of the species placed at strategic locations where present. It is the proportion of species i cockroaches were likely to be found, such as relative to the total number of species (pi), under beds, bathrooms, toilets, kitchenettes, and then multiplied by the natural logarithm near rubbish bins, cupboards, in drawers and of this proportion (ln pi). The resulting in the corners of rooms. The collections were product is summed across species, and made for a period of 30 days with the sticky multiplied by -1 [38, 39]. The higher scores traps set up and damaged or spoilt traps show higher diversity. frequently replaced. Traps were examined s from time to time for the collection of trapped H = - ∑i=1 Pi ln Pi cockroaches which were counted and Simpson’s Dominance Index (D) is a measure recorded. Using sterile hand gloves, trapped of diversity which takes into accounts both cockroaches that are whole and alive were the number of species per sample as well as killed in labelled insect jar containing cotton relative abundance of the different species soaked in diluted 10% chloroform and [40] preserved in 70% alcohol. The sticky trapped ∑ 푛(푛−1) 퐷 = 1 − 푖=1 roaches were removed using absolute 푁(푁−1) ethanol. Where: D = Dominance index, ni = number Insect identification of individuals in the ith species, N = total The collected specimens were regularly number of entities in the dataset. examined under the dissecting microscope at RESULTS the Insectarium of the Department of Crop Results revealed that seven cockroaches Production and Protection for identification (Periplaneta americana, Periplaneta up to species level using standard and reliable australasiae, Blattella germanica, Blattella taxonomic keys [3, 35, 36] and compared with orientalis, Blattella vaga, Supella longipalpis, reference specimens maintained in the and P. fuliginosa were trapped from the Department. Some of the identified species various locations within OAU campus 39

Sosan et al. International Journal of Applied Biological Research 2019 between year 2015 and 2017. The abundance specimens collected. Other species include B. and distribution of cockroaches based on orientalis (7.2%), S. longipalpis (5.0%), B. years of collection are presented in Table 1. vaga (4.0%), P. fuligonosa (3.7%) and P. The total cockroaches trapped in the year australasiae (2.1%) as the least species 2015, 2016, 2017 were 278, 301, and 288 recorded. The Diversity Index of cockroaches individuals respectively. With regards to total trapped in selected locations decrease with population of cockroach species collected years of collection with the Diversity Index for between 2015 and 2017, B. germanica and P. year 2015, 2016 and 2017 was 1.45, 1.43 and americana had the highest population of 346 1.30 respectively. A similar trend was and 331 individuals respectively while P. observed for the dominance index that australasiae had lowest population of 18 reduced from 0.70 in (2015) to 0.65 in (2017). individuals. For population of individual The P. americana had the highest dominance species of cockroach collected at different index of 0.1581 in year 2016 while B. years, B. germanica increased progressively germanica had highest dominance index of from 106 individuals (2015) to 128 0.1445 in 2015 and 0.1967 in 2017. The P. individuals (2017), S. longipalpis also follows australasiae had the least dominance index of the same trend and increased from 12 (2015) 0.0003, 0.0008 and 0.0001 for year 2015, to 16 (2017). The P. americana, P. australasiae 2016, and 2017 respectively (Table 1). and B. vaga had its peak population in 2016, The analysis of variance (ANOVA) results while the population of B. orientalis declined presented in Table 2 showed that the model throughout the sampling period. explained 80% of variation observed in trapped cockroach species from the In terms of relative abundance, B. germanica university halls of residence and coefficient of and P. americana was most prevalent variation (CV) of 23% which indicates low cockroaches with 39.9% and 38.2% prevalent levels of variations across the sampling rate respectively over the three years' period. locations and periods. These two species made up 78% of the total

40

Sosan et al. International Journal of Applied Biological Research 2019 Table 1: Species composition and relative abundance of cockroaches trapped in Obafemi Awolowo University, Ile-Ife, Nigeria

Species/indices Total Relative Mean Abundance (%) of cockroaches Dominance index (D) population Abundance population (%) /Year 2015 2016 2017 2015 2016 2017 B. germanica 346 39.9 115.3 106 112 128 0.1445 0.1377 0.1967 (38.1) (37.2) (44.4) P. americana 331 38.2 110.3 102 120 109 0.1338 0.1581 0.1424 (36.7) (39.9) (37.8) B. orientalis 62 7.2 20.7 28 (10.1) 19 (6.3) 15 (5.2) 0.0098 0.0038 0.0025

S. longipalpis 43 5.0 14.3 12 (4.3) 15 (5.0) 16 (5.6) 0.0017 0.0023 0.0029

B. vaga 35 4.0 11.7 14 (5.0) 15 (5.0) 06 (2.1) 0.0024 0.0023 0.0004

P. fuliginosa 32 3.7 10.7 11 (4.0) 11 (3.7) 10 (3.5) 0.0014 0.0012 0.0011

P. australasiae 18 2.1 6.0 05 (1.8) 09 (3.0) 04 (1.4) 0.0003 0.0008 0.0001

Total 867 278 301 288 Shannon diversity index 1.45 1.43 1.30 Simpson dominance (1-D) 0.70 0.69 0.65

41

Sosan et al. International Journal of Applied Biological Research 2019 Table 2: Analysis of variance of cockroaches trapped in Obafemi Awolowo University, Ile-Ife, Nigeria Source of Variation Degree of freedom Mean Square F value

Group 9 0.158 0.70 ns

Year (Y) 2 0.097 0.44 ns

Insect Species (S) 6 29.41 130.73**

Error 192 0.225 -

Total 209 -

R2 0.80 (80%)

CV 23.5%

** = significant at p=0.01 ns = not significant.

The species of cockroaches were highly The total population of cockroach species significantly different from one another collected by student groups between 2015 while group and years of collection were and 2017 is shown in Fig 1. In 2015, group not significant at p ≤ 0.05. The mean 10, 7, and 3 trapped a total of 36, 33 and 31 population of cockroaches trapped is cockroaches while group 4 and 6 recorded presented in Table 3. The mean 20 and 21 cockroaches respectively. In population of B. germanica and P. 2016, group 2, 7, 5, and 8 trapped a total of americana were not significantly different 44, 39, 35 and 33 cockroaches respectively but higher than other species of insects while group 1 and 6 had lowest number of detected/trapped (p ≤ 0.05). However, no trapped cockroaches of 20 and 19 significant difference in mean population respectively. In 2017, three groups (4, 1, of S. longipalpis and other species of and 7) trapped highest number of 37, 36 cockroaches with exception of B. orientalis and 32 cockroaches respectively while which recorded higher population than B. group 10, 9, and 8 only trapped 18, 20 and vaga. 21 cockroaches respectively.

42

Sosan et al. International Journal of Applied Biological Research 2019

Table 3: Mean population* of cockroaches trapped in Obafemi Awolowo University, Ile-Ife, Nigeria

Species Means

P. americana 10.799a

B. germanica 11.039a

S. longipalpis 1.224bc

P. australasiae 0.493bc

B. vaga 1.028cd

P. fuliginosa 0.946bc

B. orientalis 1.825b

* Mean from Back- transformed (Original Data) Means in same column followed by the same letter(s) are not significantly different at p ≤ 0.05

50

45

40

35

30 2015

25 2016

20 Insect Insect Population 15 2017

10

5

0 1 2 3 4 5 6 7 8 9 10 Student Groups

Fig. 1: Total population of cockroach species trapped by student groups between 2015 and 2017

43

Sosan et al. International Journal of Applied Biological Research 2019

DISCUSSION The observed trend in the study could also Cockroaches are important insect pests be due to the improvement in the due to their ubiquitous habits and environmental sanitation, recent association with humans and are reported reduction of number of students allowed to be serious vectors of pathogens. The in hostel rooms which drastically reduced species of cockroaches encountered in this overcrowding and congestion, and the study belong to two families; Blatellidae new fumigation plan of the University [German cockroach (B. germanica), management might have also contributed brown-banded cockroach (S. longipalpis), to the number of the dominant species and field cockroach (B. vaga)] and which also affected other species Blattidae [American cockroach (P. considerably. americana), oriental cockroach (B. Blattella germanica population increased orientalis), Australian cockroach (P. progressively throughout the sampling australasiae) and smoky brown cockroach (P. fuliginosa)]. The species diversity was period which might be attributed to low for all sampling years and there was conducive environment for its reproduction or its relatively short life dominance of German and American cycle and ability to reproduce rapidly. cockroaches over other species. The German cockroach is capable of population abundance of the insects was in the order, B. germanica > P. americana establishing a sizable population within a short period of time due to its highest > B. orientalis > S. longipalpis > B. vaga > reproductive potential (number of eggs P. fuliginosa > P. australasiae. Three of the laid and short life cycle) of the house- identified cockroaches (P. americana, B. germanica and B. orientalis) were earlier infesting cockroaches and the females reported in Abraka, Delta State, Nigeria carry their egg capsule for as long as one month before hatching [47, 48]. On the [41]. However, the number of species other hand, a fluctuation in the population encountered in this study was found to be more than those reported in earlier of Periplaneta americana could be as a studies in Jos, Nigeria [42] with only two result of food availability and conducive environment for reproduction that species of the cockroaches (P. americana resulted into population rise while the and B. germanica) found in human habitations in the sampled localities [42, drop in population could be due to recent 43]. Only one species of cockroach (P. implementation of general pest control and management programs in the americana) was reported in Cross River, University. Nigeria [44, 45]. In Cameroon, three species of cockroaches (P. americana, B. The American cockroach, Periplaneta germanica, and B. orientalis) were known americana and the German cockroach, to be dominant in human habitations in Blattella germanica are cosmopolitan in the Melong Subdivision of the country distribution and able to reproduce and [32]. This is similar to what was observed survive more easily in tropical climate in the present study in terms of ranking region. They have been reported to be two based on population of trapped insects. of the most common and notorious The decrease in biodiversity and cosmopolitan pest species in Nigeria [49], and other parts of the world [9, 15, 28]. dominance index over the three year The higher relative abundance of B. period could be as a result of environmental effect as abundance and germanica over P. americana recorded in population fluctuations of cockroaches are this study is consistent with other study in Iran [50]. These species of cockroaches linked to various environmental factors have been noted to be the most frequent such as cleanliness and human population density [46]. species in the human dwellings in West Malaysia followed by P. americana [29, 44

Sosan et al. International Journal of Applied Biological Research 2019

51]. However, in Nigeria, P. americana been reported to be reservoir and (66.51%) was reported as the dominant mechanical transmitters of pathogenic cockroach species in Sokoto followed by B. microorganisms [44], E. coli, Salmonella orientalis (33.49%) [34] while P. shigella, Staphylococcus, Streptococcus americana was the most predominant were detected in P. americana collected cockroach species in Markurdi that from different kitchens in Lahore, Pakistan accounted for 50.6% of total cockroaches [58] while different forms of caught [52]. The species, P. americana gastroenteritis (food poisoning, (81.33%) was also noted as the most dysentery, diarrhoea, etc.) are known to be prevalent cockroach followed by B. the principal diseases transmitted by germanica (11.53%) in Abraka, Delta oriental cockroaches [59]. State, Nigeria [41]. The difference in location and environmental factors could The Brown banded cockroach Supella be likely reason for the variation observed longipalpa (F.) is a small size insects and in the number of species trapped since has ability to evade predation as well as environmental factors is known to ability to adapt to wide habitat increase. influence the rate of reproduction of the The moderate population recorded for this insect. Also, the degrees of sanitation, insect may be due to its small size and cleanliness and pest management are ability to evade predation as well as ability linked to the spatial distribution and to adapt to wide habitat. They are also abundance of cockroaches in residences referred to as tropical cockroach [60] and [53]. are regarded as peri-domestic and obligate domiciliary insect [56], that are generally The German cockroach is known to have found in drier areas of the household, the greatest potential for being persistent apartments, hotels, and hospitals, and troublesome. The insects have also particularly in bedroom, furniture, been implicated in the spread of typhoid television, clothes cabinets, in dining room and dysentery [54]. A total of 12 areas, on ceilings, high on walls, behind Salmonella, two each of Shigella and picture frames, and near motors of Escherichia coli, 17 Staphylococcus aureus refrigerators and other appliances. etc. and 24 Bacillus cereus were isolated from [28, 61, 62]. About 15% of the insects were this particular species in Addis Ababa, trapped in Benue University student Ethiopia [55] and Entamoeba histolytica hostels in Markurdi, Nigeria [34]. that causes amoebiasis was detected in P. americana and B. germanica in Sokoto, Other cockroach species encountered in Nigeria [52]. this survey include the field Cockroach The third in the ranking in terms of (Blattella vaga) population that is similar to German cockroach in mode of abundance is oriental cockroaches Blatella reproduction as it also carries the ootheca orientalis (L.) and have been earlier until nymphs emerge [48, 61] and prefers reported in Nigeria [41, 52]. This species occurs commonly in and around houses outdoor locations but invade indoor areas when it is hot or dry outdoors and can be and around moist, dark sites especially in seen around streetlights and in lighted floor and storm drains, water-meter display windows [61]. They are not boxes, around plumbing fixtures, moist crawl spaces, sewers, damp basements, repelled by light and has ability to fly [63, 64] and usually found in leaf litter and around garbage, sewers, and forage mostly plant debris feeding on decaying on the first floors of building [48, 56, 57]. vegetation. The smoky brown Cockroach The P. americana, B. germanica and B. orientalis were found to be carriers of Periplaneta fuliginosa (Serville), one of the nematodes eggs and protozoan oocysts least abundant species are native to temperate regions of Asia [64] which [32] while American cockroaches have 45

Sosan et al. International Journal of Applied Biological Research 2019 indicates that there is possibility of being recently introduced into Nigeria. 3. Beccaloni, G. W. (2014) The Australian cockroach (P. Cockroach Species File Online. australasiae), the least abundant, are peri Version 5.0/5.0. World Wide Web domestic cockroaches (cockroaches that electronic publication. Available live mostly outdoors, but occasionally at: found indoors) [65] and are most likely http://Cockroach.SpeciesFile.org attracted into residential areas due to . attraction of light at night [28], food [66] and warmth as the species are not cold 4. Koehler, P. G., Patterson, R. S., and tolerant [57]. This species is believed to Brenner, R. J. (1990). have originated from Africa [65]. There is Cockroaches In: Mallis A, ed. likelihood that the insect might have been Handbook of pest control: the introduced into the country but yet to be behavior, life history and control effectively established as introduced of household pests. 7th ed. household insect pest in Nigeria. Cleveland: Franzak and Foster; pp. 101-174. CONCLUSION This study provided information on the 5. Rust, M. K., Reierson, D. A., and cockroach species present and their Hansgen, K. H. (1991). Control of prevalence in a University community. The American cockroaches major roles of the predominant species of (Dictyoptera: Blattidae) in cockroaches recorded in this survey which sewers. Journal of Medical are known to serve as a reservoir and Entomology, 28: 210-213. potential vectors of some food-borne diseases call for a further investigation 6. Health Canada. (2010). into linking infestation of these insects Cockroaches–What are they?, with incidence and spread of specific Health Canada 1–2. Retrieved diseases. Nonetheless, a substantial effort from is necessary to raise peoples’ awareness www.healthcanada.gc.ca/pmra on the need to safeguard themselves and their food sources from contamination by 7. Adenusi, A. A., Akinyemi, M. I., and cockroaches. This will go a long way in Akinsanya, D. (2018). Domiciliary minimizing the incidence and spread of Cockroaches as Carriers of infectious diseases that are linked to these Human Intestinal Parasites in insect pests in our environment. Lagos Metropolis, Southwest Nigeria: Implications for Public REFERENCES Health. Journal of - 1. Cochran, D. G. (1999). Borne Diseases, 12(2): 141–151. Cockroaches: Their Biology, Distribution and Control. WHO/ 8. Brenner, R. J., Koehler, P. G., and CDS/CPC/WHOPES/99.3. World Patterson, R. S. (1987). Health Health Organization, Geneva. implications of cockroach

infestations. Infections in 2. Nuwer, R. (2013). How Many Medicine 4: 349–358. Species of Cockroaches Plague

Humanity? Available online at 9. Hamu, H., Debalke, S., Zemene, E., https://www.smithsonianmag.co Birlie, B., Mekonnen, Z., and m/smart-news/how-many- Yewhalaw, D. (2014). Isolation of species-of-cockroaches-plague- intestinal parasites of public humanity-180948133/ health importance from 46

Sosan et al. International Journal of Applied Biological Research 2019

cockroaches (Blattella 15. Memona, H., Manzoor, F., and germanica) in Jimma Town, Riaz, S. (2017). Species Diversity Southwestern Ethiopia. Journal of and Distributional Pattern of Parasitology Research: 1- 5. Cockroaches in Lahore, Pakistan. Journal of Arthropod Borne 10. Rivault, C., Cloarec, A., and Disease, 11(2): 249–259. Gruyader, A. (1993). Bacterial load of cockroaches in relation to 16. Naher, A., Afroz, S., and Hamid, S. urban environment. (2018). Cockroach Associated Epidemiology & Infection, 110: Foodborne Pathogens: 317–325. Distribution and Antibiogram Cockroach Associated 11. Okafor-Elenwo, E. J., and Elenwo, Foodborne. Bangladesh Medical A. C. (2014). Human Infecting Research Council Bulletin, 44: 30- Parasitic Worms, In Cockroaches 38. from Odau in the Niger Delta Region of Nigeria, International 17. Adeleke, M. A., Akatah, H. A., Journal of Natural Sciences Hassan, A. O., Sam-Wobo, S. O., Research, 2 (10): 176-184. Famodimu, T. M., Olatunde, G. O., and Mafiana, C. F. (2012). 12. Oyeyemi, O. T., Agbaje, M. O., and Implication of cockroaches as Okelue, U. B. (2016). Food-borne vectors of gastrointestinal human parasitic pathogens parasites in parts of Osogbo, associated with household Southwestern Nigeria. Munis cockroaches and houseflies in Entomology & Zoology, 7 (2): Nigeria. Parasite Epidemiology 1106-1110. and Control, 1(1):10-13. 18. Akinjogunla, O. J., Odeyemi, A. T., 13. Alaku, I. A., Galadima, A. A., and and Udoinyang, E. P. (2012). Mundi, D. A. (2018). Assessment Cockroaches (Periplaneta of the Role of Cockroaches americana and Blattella (Periplaneta americana) as germanica): reservoirs of multi Carriers of Medically Important drug resistant (MDR) bacteria in Parasites and Microorganisms in Uyo, Akwa Ibom State. Scientific College of Agriculture, Lafia, Journal of Biological Sciences, Students Hostels, Nasarawa State, 1(2): 19-30. Nigeria. Annual Research & Review in Biology, 27(1):1-7. 19. Morenikeji, O. A., Adebiyi, A., and Oluwayiose, O. A. (2016). 14. Sia Su, G. L., Carillo, N., Pera, D., Parasites in Cockroaches Sison, S., Tanalgo, B., Sia Su, L. M., Recovered from Residential and Mistika, M. (2016). Parasitic Houses around Awotan Dumpsite infestation in Cockroaches in Ido Local Government Area of (Periplaneta americana) Oyo State, Nigeria. Annual obtained in selected areas of Research & Review in Biology, Metro Manila, International 9(3): 1-10. Journal of Tropical disease & Health, 13(4): 1–4. 20. Sarinho, E., Schor, D., Veloso, M. https://doi.org/10.9734/IJTDH/ A., and Rizzo, J. A. (2004). There 2016/23820. are more asthmatics in homes with high cockroach infestation. 47

Sosan et al. International Journal of Applied Biological Research 2019

Brazilian Journal of Medical and Polyphaga sp. as a new species in Biological Research, 37(4):503- Iran. Journal of Arthropod Borne 510. Diseases. 9: 161–175.

21. Eggleston, P. A., Arruda, L. K., and 28. Lee, C. Y., and Lee, L. C. (2000). Paulo, S. (2001). Ecology and Diversity of cockroach species elimination of cockroaches and and effect of sanitation on level of allergens in the home. Journal of cockroach infestation in Allergy and Clinical Immunology, residential premises. Tropical 10(3): 422–429. Biomedicine, 43: 39–43.

22. Page, K. (2012). Role of cockroach 29. Jeffery, J., Sulaiman, S., Oothuman, proteases in allergic disease. P., Vellayan, S., Zainol-Ariffin, P., Current Allergy and Asthma Paramaswaran, S., Razak, A., Reports, 12: 448-455. Muslimin, M., Kamil-Ali, O. B., Rohela, M., and Abdul-Aziz, N. M. 23. Rabito, F. A., Carlson, J. C., Hua, He, (2012). Domiciliary cockroaches Werthmann, D., and Schal, C. found in restaurants in five zones (2017). A single intervention for of Kuala Lumpur Federal cockroach control reduces Territory, peninsular Malaysia. cockroach exposure and asthma Tropical Biomedicine, 29(1): morbidity in children. 180–186. Environmental and occupational disease. The Journal of allergy 30. Tawatsin, A., Thavara, U., and and clinical immunology, 140 (2): Chompoosri, J. (2001). Cockroach 565–570. Surveys in 14 Provinces of Thailand. Journal of Vector 24. Lee, C.Y. (1997). Medical Ecology, 26(2): 232–238. importance of domiciliary cockroaches. Singapore 31. Kutrup, B. (2003). Cockroach Microbiologist, 11: 14 -17. Infestation in Some Hospitals in Trabzon, Turkey. Turkey Journal 25. Kehinde, T. Amusan, B. Ayansola, of Zoology, 27: 73–77. A., Oyelade, S., and Adu, W. (2014). Status of Insect Diversity 32. Atiokeng-Tatang, R. J., Tsila, H. G., Conservation in Nigeria: A and Wabo Poné, J. (2017). Review. Ife Journal of Science, 16 Medically Important Parasites (2): 319-329. Carried by Cockroaches in Melong Subdivision, Littoral, 26. Shahraki, G. H., Parhizkar, S., and Cameroon. Journal of Nejad, A. R. S. (2013). Cockroach Parasitology Research, 2017: 1- 8. infestation and factors affecting the estimation of cockroach 33. Bamigboye, A. P. (2006). Rat population in urban infestation in a typical Nigerian communities. International University Halls of residence: Journal of Zoology, 2013:1-6. Implications for hygiene and sanitation. Research Journal of 27. Hashemi-Aghdam, S, S., and Agriculture and Biological Oshaghi, M. A. (2015). A checklist Sciences, 2(6): 328-331. of Iranian cockroaches () with description of 48

Sosan et al. International Journal of Applied Biological Research 2019

34. Omudu, E. A., and Akosu, G. 42. Ejimadu, L. C. Goselle, O. N., (2013). Cockroach and rodent’s Ahmadu, Y. M., and James-Rugu, infestation in Benue State N. N. (2015). Specialization of University students’ hostel in Periplaneta americana Makurdi and their (American cockroach) and epidemiological implications. Blattella germanica (German Journal of Parasitology and cockroach) towards intestinal Vector Biology, 5(5): 60-65. parasites: a public health concern, Journal of Pharmacy and 35. Choate, P. M. (2009). A Biological Sciences, 6: 23–32. Dichotomous Key for the Identification of the Cockroach 43. Ajero, C. M. U., Ukaga, C. N., and Fauna (Insecta: Blattaria) of Ebirim, C. (2011). The role of Florida. Department of cockroaches (Blatta orientalis Entomology and Nematology. and Periplaneta americana) in mechanical transmission of 36. Department of Entomology, parasites in households in IOWA State University, Bugguide; Owerri, South East Nigeria. (2015). Available at Nigerian Journal of Parasitology, https://bugguide.net/node/view 32(2): 153–156. /342386 44. Iboh, C. I., Etim, L. B., Abraham, J. 37. SAS (2003). SAS/STAT Users T., and Ajang, R. O. (2014). Guide. Release V9.2. Cary, NC: SAS Bacteria and parasites infestation Institute. of cockroaches in a developing community, South Eastern, 38. Shannon, C. E., and Weaver, W. Nigeria. International Journal of (1949). The mathematical theory Bacteriology Research, 2(5): 45– of communication. Science, 185: 48. 27-39. 45. Iboh, C. I., Ajang, R. O., Etta, H. E., 39. Beals, M., Gross, L., and Harrell, S. and Abraham, J. T. (2015). Public (2000). Diversity Indices: health implications of Shannon's H and E. available at cockroaches within households http://www.tiem.utk.edu/~gros in Calabar Municipality, Cross s/bioed/bealsmodules/shannon River State, Nigeria. Global DI.html. Journal of Public Health and Epidemiology, 2(2): 114–119. 40. Simpson, E. H. (1949). Measurement of diversity. 46. Rivault, C., and Cloarec, A. (1996). Nature, 163: 688. Cockroach insecticide treatments and human lifestyles in Council 41. Ojianwuna, C. C. (2014). flats in France. In. Proc. The Potentials of cockroach vectors in Second International Conference transmitting parasites of medical on Insect Pests in the Urban importance in Abraka, Delta State Environment. Ed. Wildey, K.B. Nigeria. International Journal of Edinburgh 7-10 July. Applied Biological Research, 6(2): 9–20. 47. Lee, C. Y., Yap, H. H., and Chong, N. L. (1996). Comparison of selected biological parameters of 49

Sosan et al. International Journal of Applied Biological Research 2019

laboratory susceptible and field 52. Bala, A. Y., and Sule, H. (2012). collected strains of the German Vectoral Potential of Cockroaches cockroach, Blattella germanica in Transmitting Parasites of (L.) (Dictyoptera: Blattellidae). Medical Importance in Arkilla, Malaysian Journal of Science, Sokoto, Nigeria. Nigerian Journal 17(A): 37 - 48. of Basic and Applied Science, 20(2): 111-115. 48. Nevada State Department of Agriculture (NDA) (2014). 53. Lee, D., Lee, W., and Sim, J. (2003). Industrial & institutional control Population densities of of insects & vertebrates, Volume cockroaches from human III, Nevada State Department of dwellings in urban areas in the Agriculture. Republic of Korea. Journal of http://agri.nv.gov/uploadedFiles Vector Ecology, 28(1): 90–96. /agrinvgov/Content/Plant/PEST /Study_Manuals/C2%20MANUA 54. Vector Management Program L%202014%20full%203- (2007). Department of Public 2014a.pdf. Health, County of Los Angeles.

49. Anikwe, J. C., Adetoro, F. A., 55. Tachebe, J., Erku, W., Gerbe- Anogwih, J. A., Makanjuola, W. A., Michae, L.T., and Ashenafi, M. Kemabonta, K. A., and (2006). Cockroach associated Akinwande, K. L. (2014). food-borne bacteria from Laboratory and field evaluation hospital and restaurant in Addis of an Indoxacarb Gel bait against Ababa, Ethiopia: distribution and two cockroach species antibiograms. Journal of Rural (Dictyoptera: Blattellidae, and Tropical Public Health, 5:34– Blattidae) in Lagos, Nigeria. 41. Journal of Economic Entomology, 107 (4): 1639–1642. 56. Atkinson, T. H., Koehler, P. G., and Patterson, R. S. (1990). Annotated 50. Fakoorziba, M. R., Eghbal, F., Checklist of the Cockroaches of Hassanzadeh, J., and Florida (Dictyoptera: Blattaria: Moemenbellah- Fard, M. D. Blattidae. Florida Entomological (2010). Cockroaches Society, 73(2): 303–327. (Periplaneta americana and Blattella germanica) as potential 57. Nasirian, H. (2016). New aspects vectors of the pathogenic bacteria about Supella longipalpa found in nosocomial infections. (Blattaria: Blattellidae). Asian Annals of Tropical Medicine and Pacific Journal of Tropical Parasitology, 104: 521-528. Biomedicine, 6(12): 1064-1074.

51. Vahabi, A., Shemshad, K., 58. Malik, K., Jamil, A., and Arshad, A. Mohammadi, P., Sayyadi, M., (2013). Study of Pathogenic Shemshad, M., and Rafinejad, J. Microorganisms in the External (2011). Microbiological study of Body Parts of American domestic cockroaches in human Cockroach (Periplaneta dwelling localities. African americana) Collected from Journal of Microbiology Research, different Kitchens. Journal of 5: 5790-5792. Pharmacy and Biological Sciences, 7(6): 45–48. 50

Sosan et al. International Journal of Applied Biological Research 2019

of Arthropod-Borne Disease, 8 59. Jacobs, S. B. (2013). (3): 53–59. Entomological Notes: Oriental cockroaches. The Pennsylvania 63. Bennett, G. W., Owens, J. M., and State University, HP13: 1–17. Corrigan, R. M. (1997). Truman's Scientific Guide to Pest Control 60. Tsai, T. J., and Chi, H. (2007). Operations. Fifth Edition. Temperature-dependent Advanstar Communication, demography of Supella Cleveland, Ohio. 520 pp longipalpa (Blattodea: Blattellidae). Journal of Medical 64. Gold, R. E., Engler, K., Brown, W., Entomology, 44(5): 772-778. and Merchant, M. (2005). Recognition and Control 61. Rust, M. K., and Reierson, D. A. Cockroaches: Texas Cooperative (2007). Cockroaches. Integrated Extension, 05: 1–5. Pest Management for Home Gardeners and Landscape 65. Jiang, S., and Kaufman, P. E. Professionals. Pest Notes, (2015). Australian cockroach Publication 7467, University of Periplaneta australasiae California Agriculture and Fabricius (Insecta: Blattodea: Natural Resources, California, Blattidae). EENY623 UF/IFAS USA. 7467: 1–7. Extension, 1–4. 66. Lee, C. Y., Chong, N. L., and Yap, H. 62. Vazirianzadeh, B., Dehghani, R., H. (1993). A study on domiciliary Mehdinejad, M., and Sharififard, cockroach infestation household M. (2014). The First Report of in Penang, Malaysia. Journal of Drug Resistant Bacteria Isolated Science, 4(I): 95–98. from the Brown-Banded. Journal

51