Exploring the Diversity and Abundance of Necrophagous Flies in Tabriz City, Northwest of Iran: Implications for Medical and Health Importance

doi:10.21203/rs.3.rs-3148018/v1

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Exploring the Diversity and Abundance of Necrophagous Flies in Tabriz City, Northwest of Iran: Implications for Medical and Health Importance

https://doi.org/10.21203/rs.3.rs-3148018/v1

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Background: Flies are of medical importance and cause problems by transmitting mechanically various pathogens to human and animals and myiasis. This study was performed to determine the diversity and abundance of medically important flies in Tabriz city, Northwest of Iran.

Methods: Adult flies and their larvae trapping was conducted on a monthly basis from July to October 2021. Then, the trapped flies were identified morphologically using valid identification keys. Simpson index, Shannon index, Jackknife Procedure, Margalef index, Menhinick index, Camargo, Modified Nee, and Smith and Wilson indexes were calculated to determine species diversity and species richness and species evenness as well as species biodiversity of flies. Also, the rare or dominant species was estimated by Rarity richness index.

Results: In this study, totally 17 species flies including Musca domestica, Muscina stabulans, Phaonia spp., Hydrotaea spp., Musca autumnalis, Lucilia sericata, Chrysomya albiceps, Calliphora vicina, Sarcophaga africa, Sarcophaga variegata, Sarcophaga argyrostoma, Sarcophaga aegyptica, Sarcophaga sp., Sarcophaga lehmanni, Sarcophaga (Liosarcophaga) spp., Fannia sp., and Anthomyia sp. from five families (Muscidae, Calliphoridae, Sarcophagidae, Fanniidae, and Anthomyiidae) were identified. According to the bootstrapping method, Simpson index and Shannon index were 0.792 and 2.638, respectively and the number of common species was estimated to be 6.22 at the 95% confidence level. The highest species diversity was related to Sarcophagidae family and the lowest of that was related to Muscidae family by Shannon index. Musca autumnalisand M. domestica species were recognized as the rare species and the dominant species, respectively.

Conclusions: The highest number of fly species (14) were caught in August and September, and the lowest number of species (9) in October. Due to the medical and health importance of flies, it is recommended to take measures to control population of these insects.

Biodiversity

Fauna

Fly

Species richness

Tabriz

Diptera is one of the largest orders of insects which include about 10% of the world's biodiversity. There are more than 125000 identified and described species of flies in the world. About 2500 species belong to Sarcophagidae family, 1500 to Calliphoridae, 5000 to Muscidae, and 285 to fanniidae (Brown 2005; Pape 1996). Most of them are beneficial for plant pollination, biological control, decomposition, and treatment of diabetic wounds (maggot therapy). On the other hand, about 11 thousand species can cause problems for humans and animals through the transmission of various pathogens such as bacteria, fungi, nematodes and viruses, as well as by causing myiasis (Dehghan et al, 2021; Howell 2003; Grassberger et al, 2013). Thus, flies have medical, veterinary, and economic importance. Moreover, flies like Sarcophagidae and Calliphoridae has forensically importance (Fantio et al, 2022; Fremdt and Amendt 2014; Rena et al, 2018).

Myiasis is the infestation of humans and vertebrate animals with fly larvae, which feed on the host’s necrotic or living tissue. According to the type of attacked tissue, myiasis is classified. The larvae may attack their hosts through wounds and through the natural cavities of body including the mouth, ears, eyes, nose, and genitourinary tract (Akbarzadeh et al, 2018). Sarcophagidae, Calliphoridae, Muscidae and Oestridae are the most important families that cause human myiasis (Bernhardt et al, 2019; Nasser et al, 2021).

Biodiversity deals with the basic principles of various species, genetics, and ecosystem which can be investigate with three concepts of Alpha (α), Beta (β), and Gamma (γ). Alpha diversity is described as the mean diversity of species in different communities or habitats within a local scale. Beta diversity measures the variation in taxonomic composition among habitats, in order word; it is the linkage between local alpha diversity and regional gamma diversity. Gamma diversity is the total variation of a habitat (Levin 2013; Fontana et al, 2020).

Species Diversity is the number and relative abundance of species found within a particular biological community or ecosystem. Species Richness and Evenness are two components of Species Diversity. Species Richness is the number of species present in an area and Species Evenness describes the relative abundance of each species (Levin 2013; Magurran 2004).

There are some articles related to arthropods biodiversity (Abedi-Astaneh et al, 2015; Arzamani et al, 2018; Davari et al, 2018; Jahanifard et al, 2014; Khoobdel et al, 2013; Mozaffari et al, 2020; Halide et al, 2017). A study by Koobdel et al showed that the fly diversity and abundance in the Iranian triple islands in Persian Gulf are high especially in early spring and autumn (Khoobdel et al. 2013). In the conducted studies in North Khorasan and Qom Provinces, Simpson index and Shannon–Wiener index were used to estimate species diversity, Margalef index and Menhinick index were used to estimate species richness, and also Shannon evenness index and Buzas and Gibson’s evenness index for species evenness (Arzamani et al, 2018 ;Mozaffari et al, 2020). Based on the review article on medical important flies, it was found that 102 species in 9 families were reported in Iran during 1977–2017 (Akbarzadeh et al, 2018).

Realizing biodiversity and species diversity of necrophagous flies and determining their distribution is necessary to prevent transmission of the diseases caused by flies and also, to use the control methods of population of these insects. This study was conducted due to the lack of accurate information about the fauna, species diversity, and biodiversity of medical important flies in Tabriz city, Northwest of Iran.

Study area

This cross-sectional study was done from July to October 2021 in the different areas of Tabriz city, in East Azerbaijan Province, Iran. This mountainous city is 245 km2 wide and located at a height of 1300 m above sea level in plain areas and 2100 m in mountainous areas between 38°2' N latitude and 46°25' E longitude (Fig. 1). Clarifying of its climate, Tabriz has mild summers and cold winters with heavy snowfall and subfreezing temperatures.

Study design

Different areas of Tabriz city were randomly selected and adult flies and their larvae trapping was conducted on a monthly basis. The geographic coordinates of the sampling areas were recorded to prepare the map distribution of the species of flies using the GIS software.

Fly collection and identification

Adult modified traps with chicken liver as bait were used to attract adult flies and capture them. These traps were placed early morning and picked up late evening. Furthermore, the larvae stages of flies were collected from chicken liver placed in open plastic in the environment (Dehghan et al. 2020) and adults attracted to bait were caught by hand net.
The trapped adult flies and larvae were transferred to the laboratory and adults were mounted. Also, most of the larvae of flies were stored in 70% alcohol, and to confirm the larvae identification and investigate the characters of their adult stage, some of them were transferred in the insectarium and reared. The species of the trapped adults and larvae were identified morphologically using valid identification keys (Akbarzadeh et al, 2015; Grisales et al, 2016; Grzywacz et al, 2017; Jones et al, 2019; Malaithong et al, 2019; Marshall et al, 2011; Richet et al, 2011; Whitmore et al, 2020).

Data analysis

Species diversity was estimated using Simpson and Shannon indexes. The Jackknife Procedure, Margalef and Menhinick indexes were calculated to estimate species richness and also, Camargo, Modified Nee, Simpson, and Smith and Wilson indexes were used for species evenness (distribution uniformity). Plus, the rare or dominant species was determined by Rarity richness index.

The fauna of flies in Tabriz city

Totally, 2192 flies (17 species) were collected from different areas of Tabriz city. The trapped flies belonged to five families including Muscidae, Calliphoridae, Sarcophagidae, Fanniidae, and Anthomyiidae (Table 1). An overall, Musca domestica species (629) was the most abundant during this study in different areas of the city, followed by Chrysomya albiceps (535) and Lucilia sericata (515), respectively. The largest numbers of flies were observed in August.

Table 1

The different species of necrophagous flies caught and their abundance in different areas of Tabriz city from July to October 2021.
Family	Species	Months
		July		August		September		October		Total
		No.	%	No.	%	No.	%	No.	%	No.	%
Muscidae	Musca domestica	82	13	125	19.9	402	63.9	20	3.2	629	28.7
	Muscina stabulans	7	9.6	26	35.6	24	32.9	16	21.9	73	3.3
	Phaonia spp.	0	0	0	0	3	100	0	0	3	0.1
	Hydrotaea spp.	0	0	3	50	3	50	0	0	6	0.3
	Musca autumnalis	0	0	1	100	0	0	0	0	1	0.05
Calliphoridae	Lucilia sericata	28	5.4	347	67.4	58	11.3	82	15.9	515	23.5
	Chrysomya albiceps	25	4.7	295	55.1	197	36.8	18	3.4	535	24.4
	Calliphora vicina	2	5.9	21	61.8	7	20.6	4	11.7	34	1.6
Sarcophagidae	Sarcophaga africa	11	17.5	18	28.6	27	42.8	7	11.1	63	2.9
	Sarcophaga variegata	3	14.3	1	4.7	12	57.2	5	23.8	21	0.9
	Sarcophaga argyrostoma	0	0	53	64.6	14	17.1	15	18.3	82	3.8
	Sarcophaga aegyptica	0	0	29	93.5	2	6.5	0	0	31	1.4
	Sarcophaga sp.	2	1.1	91	51.7	62	35.3	21	11.9	176	8
	Sarcophaga (Sarcophaga) lehmanni	1	100	0	0	0	0	0	0	1	0.05
	Sarcophaga (Liosarcophaga) spp.	0	0	1	100	0	0	0	0	1	0.05
Fanniidae	Fannia sp.	14	70	3	15	3	15	0	0	20	0.9
Anthomyiidae	Anthomyia sp.	0	0	0	0	1	100	0	0	1	0.05
Total individuals		175	7.9	1014	46.3	815	37.2	188	8.6	2192	100
Total Captured species		10	58.8	14	82.3	14	82.3	9	52.9	17	100
No.: Number
%: Present

Species richness and species diversity

Based on Jackknife estimation, the species richness with a standard deviation of 1.44 was 20.8 and the expected number of species with 95% confidence was between 16 and 25 species. Using the bootstrapping method, at the 95% confidence level, Simpson index was 0.792 and Shannon index was 2.638, and the number of common species was estimated to be 6.22. Similar to the results of bootstrapping method, based on measures of heterogeneity, Simpson and Shannon indexes and number of common species were calculated 0.792, 2.647 and 6.26, respectively. Also, measures of evenness showed Camargo, Modified Nee, Simpson, and Smith and Wilson indexes were 0.284, 0.081, 0.283 and 0.127, respectively.

Species richness, Shannon, Simpson, Margalef, and Menhinick richness indexes were calculated are shown in Table 2. The highest species diversity was related to Sarcophagidae family and the lowest was related to Muscidae family by Shannon index. However, the species diversity of two families, Calliphoridae and Muscidae, were equal in October. Also, other diversity indexes including Simpson, Margalef, and Menhinick richness indexes showed that Sarcophagidae has the most species diversity during this study (Fig. 2). In addition, based on the rarity index, Musca autumnalis and M. domestica species were recognized as the rare species and the dominant species in Tabriz city, respectively (Fig. 3).

Table 2

Different species diversity indexes of flies, Tabriz city, Iran from July to October 2021.
Index	Formula	months
Index	Formula	July	August	September	October
Specimens (N)	Total number of specimens
Species richness (S)	The number of species	10	14	14	9
Shannon Index	\({\text{H}}^{{\prime }}={?}_{i=1}^{s}pi\text{ln}\left(pi\right)\)	0.709	0.763	0.673	0.773
Simpson Index	\(SI=\frac{{?}_{i=1}^{s}ni (ni-1)}{N (N-1)}\)	0.273	0.229	0.314	0.235
Margalef Richness Index	\(MaRI=\frac{\text{S}-1}{\text{ln}N}\)	1.742	1.878	2.386	1.527
Menhinick Richness Index	\(MeRI=\frac{S}{\sqrt{{?}_{i=1}^{s}ni}}\)	0.755	0.439	0.595	0.656

In this study, totally 17 species flies including M. domestica, Muscina stabulans, Phaonia spp., Hydrotaea spp., M. autumnalis, L. sericata, Ch. albiceps, Calliphora vicina, Sarcophaga africa, Sarcophaga variegata, Sarcophaga argyrostoma, Sarcophaga aegyptica, Sarcophaga sp., Sarcophaga lehmanni, Sarcophaga (Liosarcophaga) spp., Fannia sp., and Anthomyia sp. that are of medical importance were identified in different areas of Tabriz city in East Azerbaijan province. The captured flies from four families including Muscidae, Calliphoridae, Sarcophagidae, and Fanniidae that are considered as the most important synanthropic flies are able to mechanically transmit various pathogens such as viruses (Human enterovirus C, Coxsackievirus, infectious hepatitis), bacteria (Chlamydia chlamydia, Shigella spp., Vibrio cholerae, typhoid, paratyphoid (Salmonella), Streptococcus and staphylococcus), rickettsia (Coxilla burneti), parasites such as Entamoeba, Giardia, nematodes and also the eggs of some cestodes to humans and animals (Dehghan et al, 2021; Goddard 2016; Grassberger et al, 2013; Howell 2003). In addition, the larvae of many synanthropic flies can act as obligate or optional parasites and cause myiasis in humans or animals (Bernhardt et al, 2019; Nasser et al, 2021). However, these flies play a significant role in maggot therapy (like L. sericata) and forensic medicine (like S. africa) (Dehghan et al, 2021; Fantio et al, 2022).

Despite the medical and veterinary importance of flies, unfortunately, few studies have been conducted on the fauna and diversity of flies in Iran, especially in East Azerbaijan province. In the study conducted by Halide et al (2017) in the city of Ankara, which has similar weather conditions to the city of Tabriz, C. vicina, Calliphora vomitoria, L. sericata, Lucilia richardsi, M. domestica, M. stabulans, family Sarcophagidae were identified and C. vicina species was seen during all seasons (Halide et al, 2017). This study (Halide et al, 2017) showed that C. vicina is able to continue living and laying eggs even at low temperatures (6.74 ± 5.00°C in March and 1.00 ± 4.18°C in December). In a study on the subfamily Calliphorinae in East Azerbaijan and West Azerbaijan provinces in the northern west of Iran, six species including Bellardia pandia, Bellardia viarum, Bellardia vulgaris, C. vicina, C. vomitoria, Cynomya mortuorum were identified and all species were reported from different areas of East Azerbaijan province (Modarresi et al, 2019). In the conducted study by Khoobdel in the Iranian Triple Islands in the Persian Gulf, 10 species of flies including L. sericata, Chrsomyia megacephala, Ch. albiceps, C. vicina, S. aegyptica, S. africa, Wohlfartia magnifica, Passeromyia species, M. stabulans and M. domestica were collected and this study confirmed that the most abundance and diversity of flies in the studied areas is in early spring and fall (Khoobdel et al, 2013). In current study, the highest number of fly species (14) were caught in August and September, and the lowest number of species (9) in October (Table 1). Similar to our study, in the studies conducted in Sari (Haghi et al, 2017) and Juybar (Motevalli Haghi et al, 2021), cities in north of Iran, different species of Muscidae, Calliphoridae and Sarcophagidae families were identified, and M. domestica species was introduced as the dominant species.

Based on the results of biodiversity indexes (Shannon-Wiener, Simpson Dominance, Simpson Diversity and Margalef Species Richness Index), the highest species diversity and density of flies was seen in June while the lowest was in January 2015 in Ankara (Halide et al, 2017). The result of our study showed that Shannon Index is 2.647 based on the measures of heterogeneity. Therefore, species diversity of flies (S = 17 and H'= 2.647) in Tabriz city is more than the species diversity Ankara (S = 7) (Halide et al, 2017) and other areas of Iran such as Juybar city (S = 7 and H'= 1.005) (Motevalli Haghi et al, 2021), central Iran (S = 13 and H'= 1.87) (Mozaffari et al, 2020) and Abadan county (S = 3 and H'= 0.67) (Davari et al, 2018). In addition, that is determined that there are low differences between species richness and diversity indexes in four months. However, Margalef Richness Index showed that the highest and lowest species richness is in September and October, respectively (Table 2). Various factors such as space of the sampling area, climatic condition, height and vegetation of the study area can affect the results of the investigation of species richness and diversity in the area. The vast area with suitable climatic conditions and topography has a positive effect on the establishment and increase of the population of different species of flies, and as a result, species richness and diversity naturally increases (Motevalli Haghi et al, 2021; Mozaffari et al, 2020).

Present study confirmed that forensically important species including C. vicina, L. sericata, Ch. albiceps, S. africa, S. variegata, and S. argyrostoma that cause myiasis exist in Tabriz city. The geographic zone has a main influence on the species of arthropods and the sequence of their appearance on a corpse. For example, forensically important species of Sarcophagidae were commonly seen on indoor corpses, which it could be due to their special biological characters (Baz et al, 2015; Fremdt and Amendt 2014; Matuszewski et al, 2016; Szpila et al, 2015). Sarcophaga africa, S. subvicina and S. variegata species lives in human living environments and these species are known as indicators of urban habitats in summer and S. albiceps as an indicator of rural habitats in Frankfurt (Fremdt and Amendt 2014). Also, some species of flesh flies such as S. africa, S. argyrostoma usually were found on indoor corpses (Rena et al, 2018). So, it can be argued that the diversity and abundance of species of flies in a region is strongly related to their biological characters and habitat preferences (Fremdt and Amendt 2014; Rena et al, 2018; Szpila et al, 2015). It is necessary to mention that six species (L. sericata, Ch. albiceps, S. africa, S. variegata, and S. argyrostoma) out of these species were caught from the area of specialized dermatological hospital. Several cases of nasal myiasis due to Ch. albiceps were reported from hospitals in Bangladesh (Delwar et al, 2021). However, open wounds are more likely to be infested by larvae of flies in the hospitals. Skin injuries or wounds not only raise the chances of being infested by flies causing myiasis, but also may result in infections with bacteria that are resistant to antimicrobial treatments when flies first come into contact with the wound (Ranjbar et al, 2016; Schaumburg et al, 2016). Based on a review by Bernhardt et al (2019), only two cases of nosocomial myiasis caused by larvae of S. africa from South Europe (Dutto and Bertero 2011; Dutto et al, 2013) have been officially reported in the last 20 years.

The fly fauna in Tabriz city had a high species richness and diversity and often included some of the most medically important species. The highest and lowest number of fly species and specimens were caught in August and October, respectively. Also, the most species diversity was related to Sarcophagidae family by all of the species richness and diversity indexes. The high biodiversity of medically important flies in this city can cause health problems for pepole. Therefore, it is recommended to use measures to prevent the epidemic of diseases transmitted by flies as well as myiasis especially around the studied hospital.

Acknowledgements

The authors are grateful for the support of the Infectious and Tropical Research Center in providing financial resources for this project.

Funding

This study received financial support from Infectious and Tropical Diseases Research Center, Tabriz University of Medical Sciences, Iran.

Availability of data and materials

All data on which this article is based are included within the article.

Authors' contributions

Sara Doosti and Madineh Abbasi conceived the original idea. Behrooz Naghili Hokmabad, Ahad Bazmani helped supervise the project. Sahar Azarmi wrote the manuscript with support from Kamran Akbarzadeh and Madineh Abbasi and Mostafa Farmani carried out the implementation. Omid Dehghan performed the species richness, species diversity analytic. All authors discussed the results and contributed to the final manuscript.

Ethical consideration

The ethics committee at Tabriz University of Medical Sciences (Ethics Code: IR.TBZMED.VCR.REC.1399.405) approved this protocol.

Consent for publication

Not applicable

Competing interests

The authors declare that they have no competing interests.

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Editorial decision: Major revisions
14 Dec, 2023
Reviewers agreed at journal
24 Aug, 2023
Reviewers invited by journal
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10 Jul, 2023
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06 Jul, 2023

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Exploring the Diversity and Abundance of Necrophagous Flies in Tabriz City, Northwest of Iran: Implications for Medical and Health Importance

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Version 1

Abstract

Figures

Introduction

Materials and methods

Study area

Study design

Fly collection and identification

Data analysis

Results

The fauna of flies in Tabriz city

Species richness and species diversity

Discussion

Conclusions

Declarations

References

Supplementary Files

Status:

Version 1