J -Borne Dis, June 2017, 11(2): 249–259 H Memona et al.: Diversity and …

Original Article Species Diversity and Distributional Pattern of in Lahore, Pakistan

Hafsa Memona, *Farkhanda Manzoor, Saffora Riaz

Department of Zoology, Lahore College for Women University, Lahore, Pakistan

(Received 28 Apr 2015; accepted 14 May 2016)

Abstract Background: Cockroaches are found as the most common urban pests of tropical countries, prompting economic and serious health risk problem for humans by carrying microbes and allergens, acting as vector for various patho- gens of diseases. The present study was conducted from April 2013 to March 2014 in various human dwelling local- ities of urban area of district Lahore, Pakistan. Methods: Cockroaches were collected randomly by hand, food baited and sticky traps throughout the year. Four species of cockroaches ( Americana (P. amercana), germanica (B. germanica), orientalis (B. orientalis), and Blatta lateralis (B. lateralis) were collected and identified from the study site. Results: B. germanica was the most dominant indoor species with highest diversity indices in study areas. Overall species diversity was highest in July–September, 2013 with highest Simpson index of diversity and Shan- non index as well. P. americana was found second broadly distributed in the study area followed by B. orientalis and B. lateralis were intermediately distributed in residential areas and narrowly distributed in hospitals. Residential ar- eas and hospitals were highly infested with B. germanica followed by P. americana. Population index of B. ger- manica for hospitals was double than residential areas. B. lateralis was observed as displacing B. orientalis in out- door habitat through competing with its habitat and food sources. Conclusion: The infestation rate of different species depends on availability of food sources, sanitary conditions and climatic conditions. Cockroach infestation can be controlled with knowledge about their biology and behavior, at- tention to sanitation and effective use of commercial insecticides.

Keywords: Diversity, Cockroach, Pakistan, P. americana, B. germanica.

Introduction

Out of the 4600 species of cockroaches and impoverished living settings are breeding only 50 species have been reported as pests sites for indoor species especially Blattella ger- of human structures and dwellings world- manica (B. germanica) (Bonnefoy e al. 2008). wide. They randomly infringe in human hab- Poor sanitation, disrepair and clutter contrib- itation and never cause threat to indoor struc- ute to increase population of cockroaches in tures (Cochran et al. 1980, Bonnefoy et al. human habitat. Foodstuffs can be contaminat- 2008). Morphologically cockroaches are char- ed with cockroach feces, body parts and path- acterized by their dorsoventrally flattened ogens. Increased population of cockroaches body, head concealed beneath the pronotum, inside the homes will cause asthmatic aller- chewing mouth parts, prominent antennae and gies in peoples which can be life threatening cerci. They are placed recently in their own in some cases (Lamiaa et al. 2007). order of (Triplehorn and Johnson The predominant species of cockroaches 2005). found in various types of human dwellings All types of human habitations including in Bangkok, Thailand, Kuala Lumpur Federal hospitals and houses are significantly infest- Territory, peninsular Malaysia, Singapore, Chi- ed with cockroaches. Highly populated houses na, Indonesia, India and Pakistan are: Family 249 *Corresponding authors Dr Farkhanda Manzoor, http://jad.tums.ac.ir E-mail: [email protected] Published Online: May 27, 2017 J Arthropod-Borne Dis, June 2017, 11(2): 249–259 H Memona et al.: Species Diversity and …

Blattidae include Periplaneta americana (P. of yeast, 150 bacterial species, 45 species of americana) (), P. austral- parasitic worms and 90 species of protozoa asiae (Australian cockroach), Periplaneta to human life either biologically or mechan- brunea (P. brunnea) (Burmeister) (Large ically (Tachbele et al. 2006, Al-Marjani et brown cockroach), Periplaneta fuliginosa (P. al. 2008, Saichua et al. 2008, Al-bayati et al. fuliginosa), Blatta orientalis (B. orientalis) 2011, Akinjogunla et al. 2012, Tilahun et al. (Oriental cokroach), rhombifo- 2012, Goralska and Kurnatowski 2013, Vaziri- lia (N. rhombifolia) (Stool) The Harlequin anzadeh et al. 2014). They get infected with cockroach, Blatta () lateralis (B. pathogenic bacteria causing bubonic plague, lateralis) (Walker) (Turkistan cockroach) and leprosy, dysentery, urinary infections, abscess- Hebardina concinna (H. concinna) (Dehaan) es and pimples etc. bacterial species can stay (Sriwichai et al. 2002, Chompoosri et al. 2004). alive on cockroach body surfaces for many Family Blattelidae include B. germanica days (Vahabi et al. 2007). (), Blattella lituricollis (B. The parasitic organisms identified from lituricollis) (Walker) (Smaller German cock- cockroaches include helminthes and proto- roach), longipalpa (S. longipalpa) zoans. The helminthes include Strongyloides (Fabricius) (Brown banded cockroach), Blat- stercoralis (S. stercoralis), Ascaris lumbri- tella vaga (B. vaga) Hebard (Field cockroach), coides (A. lumbricoides), Trichuris trichura (B. asahinai) Mizukubo (T. trichura), Taenia spp and identified pro- (Asian cockroach), Jacobsonina erebis (J. tozoans are Cyclospora spp, Entamoeba his- erebis), pallens (S. pallens) (Smooth tolytica (E. histolytica), Entamoeba coli (E. cockroach) Symploce sphaerica (S. sphaeri- coli), Balantidium coli (B. coli) and Isospora ca), Symploce miyakoensis (S. miyakoensis), belli (I. belli) (Thyssen et al. 2004, Salehza- Symploce okinerabuensis (S. okinoerabuensis), deh et al. 2007, Nyarango et al. 2008, Chamavit Symploce paramarginata (S. paramargina- et al. 2011, El-Sherbini and El-Sherbini 2011). ta) and Symploce evidens (S. evidens). Fam- Cockroaches are contaminated with medical- ily polyphagiadae include Polyphaga aegyp- ly important fungi including Candida, Asper- tica (P. aegyptica) and Polyphaga saussurei gillus niger (A. niger), Mucor, Rhizopus spp, (P. saussurei). Family include Rhy- Aspergillus fumigans (A. fumigans) and Pen- parobia maderae (R. maderae) (Madeira icillium spp. (Tatfeng et al. 2005, Salehza- cockroach). Family Pycnoscelidae include Pyc- deh et al. 2007). noscelis surinamensis (Linnaeus) (P. surina- Cockroach associated bacteria include mensis) the . Family Oxy- Klebsiella pneumoniae (K. pneumoniae), Sal- haloidae include Nauphoeta cinerea (Olivier) monella spp, Escherichia coli (E. coli), Pseu- (N. cinerea) the lobster cockroach (Cochran domonas aeruginosa (P. aeruginosa), Enter- et al. 1980, Zahedi and Jeffery 1996, Boyer obacter cloacae (E. cloacae), Citrobacter freun- and Rivault 2004, Jeffery et al. 2012, Wang dii (C. freundii), Enterobacter aerogenes (E. and Che 2013). aerogenes) and Proteus mirabilis (P. mirabi- Different studies in Pakistan confirms the lis) which are potential pathogens. There was presence of P. americana, B. orientalis and no significant difference between the overall B. germanica species of cockroaches in Pa- bacteria load on the external surface in cock- kistan (Mlso et al. 2005, Saira 2005, Ahmed roaches found in the food-handling estab- et al. 2010, NIH 2010, Wakil et al. 2012, lishments (60.08%) and households (39.92%) Malik et al. 2013, Syed et al. 2014). (Wannigama et al. 2014). Pseudomonas aeru- Cockroaches are one of the most important ginosa has been demonstrated to multiply in agent which can transmit almost 60 species the gut and excretion of the bacteria contin- 250 http://jad.tums.ac.ir Published Online: May 27, 2017 J Arthropod-Borne Dis, June 2017, 11(2): 249–259 H Memona et al.: Species Diversity and …

ued up to 114 days. Further studies also re- Sampling and identification of cockroaches vealed that Salmonella typhi (S. typhi), Shi- Cockroaches were observed and collected gella dysenteriae (S. dysenteriae) and toxi- randomly from April 2013 to March 2014 genic strains of E. coli retained in the gut of with the help of sticky traps, food baited pit- cockroaches for up to several days (Fotedar fall traps and manual catching by hand. et al. 1993, Pai et al. 2003). Specimens were collected from 20 different Present study was conducted with the sites including hospitals (Punjab Institute of objective to report species composition, di- Cardiology, Mayo Hospital, Sheikh Zaid Hos- versity, abundance, richness and population pital, Jinnah Hospital and General Hospital) dynamics of cockroaches in urban areas of shopping malls/stores (Swera departmental district Lahore. Lahore features a five season store, Metro cash and carry and Hyperstar), semi-arid climate ie foggy winters (15 Nov– institutes/office (LCWU, Punjab university, 15 Feb) with few western disturbances caus- UVAS, GCU Lahore and PASSCO), houses ing rains, pleasant spring (16 Feb–15 April), (Mughalpura, Model town, Shadman, Shalmar, summer (15 April-June) with dust rain storms Maraghzaar, Johar town and Jallo town). and heatwave periods, rainy monsoon (July– Global Positioning System of study sites are 16 September) and dry but pleasant autumn listed in Table 1. Traps were kept on the floor (16 September–14 November) (Punjab Mete- close to the wall of room, under cupboards, orology Department 2014). Due to the high bed, storage racks, under washbasins and population density in the city, 5000 tons per pantry. Each trap was placed in living room, day of solid waste is produced in Lahore that bedroom, bathroom and kitchen of houses, is collected and disposed in one landfill site different wards, store rooms, kitchen stores, at Mehmood Booti and sewage is drained canteen area of hospitals, in grocery area, food into river Ravi (Lahore Waste Management area of shopping store and in each working Company Report 2014). There are few scat- room of the Institute/office units for three tered researches were conducted about spe- consecutive nights. Nymphs along with adults cies composition and abundance in last years. were heavily trapped in baits and traps. The Economic importance of this domestic pest collected specimens were transported to en- should be recognized. However, they are no- tomology laboratory for identification up to torious as vector of nosocomial infections, species level with the help of published keys contaminating and deteriorating food and (Pratt and Littig 1969, Abul Hab 1980, Ha- consumables, carry allergens of asthma and genbuch et al. 1988, Roth 1995, Choate 2009). resistant to insecticidal sprays. Species abundance and richness was evalu- ated in 4 trimesters comprising whole year from April, 2013 to March, 2014. Materials and Methods Weather Data Collection Experimental site Average monthly temperature and humid- Study site is the urban area of district La- ity data were obtained from the Punjab Me- hore lying between 31°15′-31°45′ N and teorological Department, Lahore and com- 74°01′-74°39′ E, 217m elevated from sea paratively analyzed with population density level with total population of 7,566,000. of cockroaches. Samples were collected from different hos- pitals, shopping malls/stores, institutes and Data analysis residential areas in different seasons around The observations were tabulated and data one year. were statistically analyzed using Microsoft

251 http://jad.tums.ac.ir Published Online: May 27, 2017 J Arthropod-Borne Dis, June 2017, 11(2): 249–259 H Memona et al.: Species Diversity and …

excel. Relative Abundance, species richness cies include B. orientalis (9%) and B. lateralis and evenness of each species of cockroaches (11%) of the total specimen trapped. These was calculated. Diversity of different cock- findings are compatible with the studies of roach species on the Simpson and Shannon Sandhu and Sohi (1981). From all the speci- indices was worked out according to Simpson mens captured during study period 62% (8328) (1949) and Shannon-Weiner function (Odum, specimen were at different nymphal stages, 1975). Species relative abundance was com- 27% (3626) adult male and adult females are pared with average monthly temperature and 11% (1479). The number of females was low- relation between population density and er as compared to males in traps because fe- change in temperature was determined. males are less agile and are often hidden in deep crevices, engaged in reproductive ac- Results tivity. During the first trimester of study (April- Identified species of cockroaches June, 2013) the minimum and maximum av- From different types of human dwelling erage temperature was 23.8 °C and 37.6 °C, localities 4 species of cockroaches belonging respectively and relative humidity was 41% to two families (Blattidea and Blattelidae) were (Table 3). The autumn was turning to end and identified during the entire sampling period. summer was started. This is the most compat- 1. American Cockroach (P. americana) able season of breeding of eggs and nymphs. They found in sewers and basements es- In this trimester, nymph collection was more pecially around pipes and drains. prominent as compared to adult males and 2. (B. orientalis): females. Most dominant species (46.78%) of They found beneath the mulch, leaf litter, all catches was B. germanica, followed by P. stones and debris outdoors, garbage, filthy americana (33.50%) while B. orientalis and materials that is going to decay. B. lateralis are 9.96% and 9.75% respective- 3. German Cockroach (B. germanica): ly (Table 2). Diversity indices were worked They found in kitchens, storage areas es- out for all species found in 20 different sites pecially where food being prepared or stored. revealed Shannons index value of -0.51185 4. (B. lateralis): and Simpson’s index of diversity was 0.6495. Turkestan cockroaches are native to large The dominant species of first trimester was area of the Middle East extending from Lib- B. germanica with a value of 0.218879 (Simp- ya Eastward to Central Asia including Af- son index) and -0.15434 (Shannon index). ghanistan, Pakistan, Uzbekistan and south- During sampling the higher number of males ern Russia (Alesho 1997). They were found in food bait traps and sticky traps was not in compost piles, gardens, potted plants and surprising as the males were active predators homes with clay floors. and roam in search of mates. Females were low in number because they conserve energy Distribution and abundance of cockroach for reproduction and found less active and species common. One of the many reason is may be From this study it was revealed that B. the traps were baited with female sex attract- germanica was the most dominant species ants which results in maximum male captur- belonging to family Blattelidae comprising ing in traps. of 45% of the total catch followed by P. During the second trimester of study (Ju- americana (35%) belonging to family Blat- ly–September, 2013) the minimum and max- tidae. These two species comprises 80% of imum average temperature was 24.8 °C and the total specimens collected. Other two spe- 34.1 °C, respectively and relative humidity 252 http://jad.tums.ac.ir Published Online: May 27, 2017 J Arthropod-Borne Dis, June 2017, 11(2): 249–259 H Memona et al.: Species Diversity and …

was 74% (Table 3). Summer season was at lected from different sites. Both species rich- peak and cockroaches were mostly found in ness and abundance was significantly lower indoor sheltered areas. This is the most fa- during colder months of study period. vorable season of metamorphosis of nymphs The fourth trimester of study (January- to change into adults. Different species have March, 2014) Shannon index value was - different life spans and time period to turn 0.52419 and Simpsons index of diversity nymphs into adults varies among different was 0.6687. Most dominant species B. ger- species. In this trimester, late nymph collec- manica (40.82%) was followed by P. ameri- tion was comparable to adult males and fe- cana (37.02%) and B. orientalis and B. lat- males. More dominant species (44.36%) of eralis comprise 7.17% and 14.97% respec- all catches B. germanica was followed by P. tively (Table 2). Overall species evenness and americana (35.81%) while, B. orientalis and richness was found higher in second tri- B. lateralis comprised 8.11% and 11.7% re- mester of study (July–September, 2013). spectively (Table 2). Diversity indices for Previous studies described P. americana this trimester were worked out for all species and B. orientalis as outdoor species of cock- of cockroaches collected from different sites. roaches but they can intrude into indoor en- Shannons index value (-0.51389) and Simp- vironment through severage pipes and crev- sons index of diversity was 0.6547 for this ices in harsh seasons. While B. germanica trimester. The dominant species of this period and B. lateralis always found in indoor envi- was B. germanica with a value of 0.196748 ronment (Rust and Reierson 2007, Jeffery et (Simpson index) and -0.1566 (Shannon index). al. 2012). Residential areas and hospitals are During sampling the higher number of nymphs mostly infected with B. germanica. P. amer- of late instar were found. Now they had gone icana approaches to outdoor environment through metamorphosis to change into adults through sewerage pipes and holes. As B. and are ready for reproduction. In most spe- orientalis and B. lateralis are morpholog- cies time for late instar to turn into females ically similar but their colony can be identified is longer than males. by male members. Houses and hospitals are In third trimester of study (October–De- highly infested with P. americana and B. cember, 2013), B. germanica was most dom- germanica as compared to offices, shopping inant species (44.62%) followed by P. amer- mall and institutes, whereas B. orientalis is icana, B. orientalis and B. lateralis respec- commonly found in houses and institutes fol- tively. Table 2 revealed Shannon index value lowed by shopping malls. Distribution of B. (-0.51187) and Simpsons index of diversity lateralis is most common in institutes, hous- (0.6521) for all species of cockroaches col- es and offices with basements and gardens.

Table 1. Global Positioning System location of study sites in urban areas of Lahore, Pakistan

Serial. Number Study site Latitude Longitude 1 Punjab Institute of Cardiology 31°32'18.48"N =31.5384667 74°20'9.28"E =74.3359111 2 Mayo Hospital 31°34'18.06"N =31.5716833 74°18'57.04"E =74.3158444 3 Shaikh Zayed Hospital 31°30'29.82"N =31.5082833 74°18'30.17"E =74.3083806 4 Jinnah Hospital 31°29'3.93"N =31.484425 74°17'48.40"E =74.2967778 5 General Hospital 31°27'17.46"N =31.45485 74°21'0.94"E =74.3502611 6 Swera departmental store 31°25'54.81"=31.4318917 74°17'11.38"=74.2864944 7 Metro cash & carry 31°29'34.65"N =31.4929583 74°25'1.57"E =74.4171028 8 Hyperstar 31°32'5.69"N =31.5349139 74°21'47.79"E =74.363275 9 LCWU, Lahore 31°32'41.85"N =31.5449583 74°19'37.97"E =74.3272028 253 http://jad.tums.ac.ir Published Online: May 27, 2017 J Arthropod-Borne Dis, June 2017, 11(2): 249–259 H Memona et al.: Species Diversity and …

Table 1. Continued…

10 Punjab University, Lahore 31°29'44.24"N =31.4956222 74°17'39.17"E =74.2942139 11 UVAS, Lahore 31°34'29.03"N =31.5747306 74°17'57.48"E =74.2993 12 GCU, Lahore 31°34'22.14"N =31.5728167 74°18'29.22"E =74.3081167 13 Passco office 31°33'36.68"N =31.5601889 74°19'56.62"E =74.3323944 14 Mughalpura 31°33'46.53"N =31.562925 74°22'49.35"E =74.380375 15 Model town 31°28'37.18"N =31.4769944 74°19'44.66"E =74.3290722 16 Shadman 31°32'14.97"N = 31.5374917 74°19'50.76"E = 74.3307667 17 Shalamar town 31°35'12.47"N = 31.5867972 74°22'55.29"E = 74.382025 18 Maraghzaar colony 31°29'44.24"N =31.553326 74°17'39.17"E =74.305122 19 Johar town 31°27'43.38"N = 31.46205 74°17'38.90"E = 74.2941389 20 Jallo town 31°35'47.57"N = 31.5965472 74°29'57.97"E = 74.4994361

Table 2. Diversity indices of different cockroach species collected from April 2013– March 2014

Trimester Species No. of Percentage Relative Shannon Simpson Species Cockroaches % abundance index Pi index Pi2XS Evenness (S) Pi (lnPi) H/logS P. americana 1573 33.50 0.3349 -0.15911 0.112202 -0.51185/0.60206 = -0.85016 B. germanica 2197 46.78 0.4678 -0.15434 0.218879 B. orientalis 468 9.96 0.0996 -0.09981 0.009932 1st B. lateralis 458 9.75 0.0975 -0.09859 0.009512 Total 4696 H= - D= 0.3505, 0.51185 1-D= 0.6495

P. americana 2123 35.81 0.358191 -0.15971 0.128301 -0.51389/0.60206 = -0.85355 B. germanica 2629 44.36 0.443563 -0.1566 0.196748 B. orientalis 481 8.11 0.081154 -0.08851 0.006586 2nd B. lateralis 694 11.7 0.117091 -0.10907 0.01371 Total 5927 H= - D= 0.3453, 0.51389 1-D= 0.6547 P. americana 671 36.03 0.360365 -0.15973 0.129863 -0.51187/0.60206 = -0.85019 B. germanica 831 44.62 0.446294 -0.15637 0.199179 B. orientalis 162 8.70 0.087003 -0.09226 0.00757 3rd B. lateralis 198 10.63 0.106337 -0.1035 0.011308 Total 1862 H= - D= 0.3479, 0.51187 1-D= 0.6521 P. americana 351 37.02 0.370253 -0.15976 0.137087 -0.50419/0.60206 = -0.84066 B. germanica 387 40.82 0.408228 -0.15884 0.16665

4th B. orientalis 68 7.17 0.07173 -0.08208 0.005145 B. lateralis 142 14.97 0.149789 -0.1235 0.022437 Total 948 H= - D= 0.4313, 0.50419 1-D= 0.5687

254 http://jad.tums.ac.ir Published Online: May 27, 2017 J Arthropod-Borne Dis, June 2017, 11(2): 249–259 H Memona et al.: Species Diversity and …

Table 3. Trimester average temperature (minimum and maximum and relative percentage of humidity recorded from April 2013 to March 2014

Trimester Average Temperature Average relative No. of cockroaches Percentage °C humidity % trapped % Minimum Maximum 1st (April-June) 23.8 37.6 41 4696 35 2nd (July–Sep) 24.8 34.1 74 5927 44 3rd (Oct–Dec) 13 26.5 68 1862 14 4th (Jan–March) 9 21.4 68 948 7

Discussion

Environmental temperature plays an im- Cockroaches were not more noticeable in cold portant role in determining the ability of an or- months in third and fourth trimester but prob- ganism to survive in a given habitat. If an or- ably they have physical and behavioral adap- ganism is able to survive in extreme temper- tation which helps them to withstand in ex- ature (during winter or summer) it will in- treme low temperature on land. This study creases their likelihood to colonize that habi- coincides with the findings of Snoddy and tat. When an organism experience high or low Appel (2008) who conducted a survey in temperature in their environment they pro- Southern and Georgia to determine duce certain proteins called “heat shock pro- the extent B. asahinai had expanded its range teins (HSP)” in their cells which allows recov- Northward from Florida. They concluded that ery on a cellular level. These HSP are found visual and bucket sample population began in many organisms from bacteria to mam- increasing in late May and reached their zen- mals (Lutterschmidt and Hutchison 1997). ith in late August or early September. Organisms have the ability to increase or The present study found indoor species of decrease their core temperature in response cockroaches including German and Turke- to environmental temperatures (Slabber et al. stan cockroach were more prominent in bed- 2007). Certain , such as , have rooms, kitchen, stores, hospital wards, office the ability to acclimate to their environmen- stores and rooms adjacent to canteen. Their tal temperature (Hu and Appel 2004). Since high prevalence in these areas can be related cockroaches are closely related to termites, to ideal shady, enriched food and cool envi- they should have the tendency to acclimatize ronment which is more favorable to increase to their environment. Previous studies have their population. Other outdoor species Amer- shown a positive correlation between the tem- ican and Oriental cockroaches are outdoor perature sensitivity of many includ- species and found near to sanitary pipes, wash- ing cockroaches and their environmental tem- rooms, filthy habitat, adjacent gardens of perature (Tsuji and Mizumo 1973, Appel et houses, sewerage pipes and kitchen exit pipe al. 1983, Slabber et al. 2007). where plenty food is available. Late nymphs In this study, cockroache’s species distri- and adults were more numerable in collection bution was observed almost all around the year site where fewer females were captured. En- though environmental temperature may effect vironmental conditions like temperature and on distribution of some outdoor species. Cock- humidity also do affect the life cycle and roaches are highly adapted for diverse land developmental stages of cockroaches. Find- environment especially dry harsh environment. ings of our study are also in conformity to

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Lee et al. (2003) who found that houses were tification of potential american cockroach most commonly infested with B. germanica (Periplaneta americana) Allergens. Iran followed by apartments and villas. The infes- J Public Health. 39(3): 109–115. tation rate of the cockroaches was related to Akinjogunlaa OJ, Odeyemib AT, Udoinyangc the residential types. EP (2012) Cockroaches (Periplaneta americana and Blattella germanica): res- Conclusion ervoirs of multidrug resistant (MDR) bacteria in Uyo, Akwa Ibom State. Sci Most of the urban areas in district Lahore J Bio Sci. 1: 19–30. especially human dwellings are infested with Al-Bayati NA, Al-Ubaidi AS, Al-Ubaidi IK cockroach population. Their presence in hu- (2011) Risks associated with cockroach man associated environment and species abun- Periplaneta americana as a transmitter dance pose them a critical threat for human of pathogen agents. Diyala J Med. 1: health and indicate poor infrastructure of 91–97. sanitary and waste disposal. The infestation Alesho NA (1997) Synathropic cockroaches rate of different species depends on avail- of Russia. Proc Inter Coll Social Insects. ability of food sources, sanitary and climatic 34: 45–50. conditions. Cockroach infestation can be con- Al-Marjani MF, Jafere FN, Abdul Hussain trolled with knowledge about their biology MT, Mezeal EA, Sahtte ZA, Hamza AH, and behavior, attention to sanitation and ef- Shanuor KJ, Asmaeal MH (2008) Study fective use of commercial insecticides. of ß-lactamases producing enterobac- teria isolated from german cockroach (Blatella germanica) in hospitals. Diala Acknowledgements J. 29: 1–10. Appel AG, Reierson DA, Rust MK (1983) The present work is a part of PhD re- Comparative water relations and tem- search of the first author. We are gratefully perature sensitivity of cockroaches. acknowledge the financial support provided Comp Biochem Physiol. 74: 357–361. by the Higher Education Commission, Is- Bonnefoy X, Kampen H, Sweeney K (2008) lamabad, Pakistan and facilitation provided Cockroaches. In Public health signifi- by Entomology lab, Department of Zoology, cance of urban pests. World Health Lahore College For Women University, La- Organization. Regional office for Eu- hore for this research. We are also thankful rope, Scherfigsvej 8. DK-2100 Copen- to Urban Pest Management Team for field hagon, Denmark, pp. 53-84. collection and technical assistance during Boyer S, Rivault C (2004) Interspecific com- sampling. The authors declare that there is petition among urban cockroach Spe- no conflict of interests. cies. Entomol Exp Appl. 113: 15–23. Chamavit P, Sahaisook P, Niamnuy N (2011) References The majority of cockroaches from the Samutprakarn province of Thailand are Abul Hab J (1980) A list of arthropoda of carriers of parasitic organisms. EXCLI medical and veterinary importance rec- J. 10: 218–222. orded from Iraq. Bull Biol Res Cent. Choate PM (2009) A Dichotomous Key for 12(1): 9–40. the Identification of the Cockroach Fauna Ahmed A, Minhas K, Namood-e-Sahar, Aftab (Insecta: Blattaria) of Florida. Depart- O, Sher Khan F (2010) In silico iden- ment of Entomology and Nematology, 256 http://jad.tums.ac.ir Published Online: May 27, 2017 J Arthropod-Borne Dis, June 2017, 11(2): 249–259 H Memona et al.: Species Diversity and …

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