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Molecular identification and control studies on Coridius sp. (Hemiptera: Dinidoridae) in Al-Khamra, south of Jeddah, Saudi Arabia

  • Wafa Mohammed Al-Otaibi , Habeeb M. Al-Solami , Abdullah G. Alghamdi ORCID logo , Akram S. Alghamdi , Nahed Ahmed Hussien ORCID logo EMAIL logo , Naser Ahmed Alkenani , Shatha I. Alqurashi , Tariq Saeed Alghamdi , Dina F. Alhashdi and Jazem A. Mahyoub
Published/Copyright: December 30, 2025
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Open Life Sciences
From the journal Open Life Sciences Volume 20 Issue 1

Abstract

Citrullus lanatus is the second most produced vegetable worldwide. Various insects, including the watermelon bug, pose a threat to this crucial crop. This study identifies the watermelon bugs in Jeddah, Saudi Arabia, with a focus on the mitochondrial cytochrome oxidase subunit I gene (mtCOI) locus. It also examines its susceptibility to Imidacloprid and Bifenthrin 10 % pesticides via feeding and topical applications. Moreover, the alcoholic extracts of Rhayza stricta and Juniperus procera were also evaluated as safe alternatives for control. Different Coridius species, including C. janus, C. chinensis, C. brunneus, C. nigriventris, and C. viduatus, four of them were first recorded in Saudi Arabia, highlighting the danger this invasive pest poses to watermelon cultivation. Imidacloprid was the most effective pesticide, with LC50 values of 2.45 and 3.37 ppm, whereas the LC50 values of Bifenthrin 10 % were 4.17 and 4.32 ppm for feeding and topical application, respectively. The resistance ratio for Imidacloprid was 1.37 times higher than that of Bifenthrin 10 %, which had a ratio of 1.04 times, in the feeding method compared to the topical method of application. J. procera extract was more effective, with LC50 values of 256.70 and 206.04 ppm, when administered by feeding and topical application, respectively. In contrast, the LC50 values of R. stricta extract were 556.93 and 651.98 ppm, under the same conditions. The relative resistance ratio of J. procera extract topical application was more effective than J. procera feeding method, R. stricta extract feeding, and topical application by about 1.25, 2.70, and 3.16 folds, respectively. The study emphasizes the importance of conducting bioassays for pesticides before their use in control programs.

Keywords: biological control; Coridius ; Jeddah; molecular identification; mtCOI; Saudi Arabia

1 Introduction

Citrullus lanatus (Thunb.), commonly known as watermelon, is the second most produced vegetable worldwide [1], 2]. Watermelon is a warm-season crop cultivated year-round in the tropics. The leading producers are China (70 million tons), Turkey (4.04 million tons), Iran (3.8 million tons), Brazil (2.08 million tons), and Egypt (1.87 million tons). Worldwide production in 2012 was 95.21 million tons [3]. Although its genetic roots trace back to Africa, watermelon has been cultivated for thousands of years in both Africa and the Middle East. It has spread worldwide through knowledge sharing and trade [4], 5]. Watermelon contains about 92 % water and 6 % sugar by weight, making it a source of vitamin C. [3].

In 2020, Saudi Arabia produced 0.522 Mt (rank 23) from nearly 30,000 ha, achieving an average yield of 22.3 t/ha. The Gulf countries import watermelons from India, Pakistan, Jordan, Myanmar, Egypt, and other countries. However, Saudi Arabia is largely self-sufficient in watermelon production, exporting around 4,000–7,000 tons, about 10 % of its total output, while importing between 3,000 and 5,000 tons [1]. From 2001 to 2019, the area, production, and yield of watermelons in Saudi Arabia increased steadily, influenced by rainfall. Approximately 13 regions contribute to watermelon production in Saudi Arabia, with the Makkah region (including the Jeddah governorate) being the most significant, accounting for about 80 % of the kingdom’s total domestic production [6].

Several insects harm watermelon, an important global crop. Among them is the watermelon bug, scientifically known as Coridius sp. (Heteroptera: Dinidoridae). This species is commonly found in Africa, the Near East, and the Arabian Peninsula. They increase in number under favorable conditions such as humidity, temperature, rainfall, and ample vegetation [7], 8]. Aljedani [9] from Jeddah identifies the control of the watermelon bug (Cordius viduatus) as a significant threat to large-scale production, negatively impacting quality and leading to reduced yields.

Previous studies have documented that insect susceptibility to neonicotinoids depends on dosage, exposure route and species [10]. Exposure to neonicotinoids may kill insects outright or may cause altered behaviors via sublethal effects [11], 12]. Imidacloprid is an artificial chemical pesticide widely used for controlling insect pests in lawn and ornamental sites. It has been shown to effectively control some insects like aphids, mealybugs, and black watermelon bugs, but also negatively affect non-target organisms [13]. Imidacloprid is one of the most widely used neonicotinoid insecticides [14]. It resembles nicotine and acts on nicotinic acetylcholine receptors [15]. Imidacloprid has been considered safer than other insecticides due to its favorable toxicological profile [15]; however, reports of poisoning have increased, causing serious organ damage, including to the heart [16], kidneys, and liver [17], and even death [15], 18]. This has raised concerns about Imidacloprid poisoning [19].

Bifenthrin is a chiral synthetic pyrethroid insecticide commonly used for agricultural and domestic pest control. Its widespread use has led to residual detection in environmental media, residential areas, and biota, posing risks to wildlife and human health. Bifenthrin is highly toxic to aquatic species and mainly contributes to insecticide toxicity in waters. It can also cause sublethal effects on non-target organisms, including developmental, neurobehavioral, oxidative, immune toxicity, and endocrine disruption [20].

As a result, using plant-derived pesticides could be a more sustainable way to improve crop production efficiency and reduce food crises while protecting consumer health. These pesticides are affordable, biodegradable, and eco-friendly, and they work in several ways, which suggests they pose less of a risk to humans and the environment. Natural plant products that have insecticidal properties include various types of molecules, such as terpenes, alkaloids, flavonoids, polyphenols, quinones, amides, cyanogenic glucosides, aldehydes, amino acids, saccharides, thiophenes, and polyketides. These compounds play important roles in nature, like repelling insects, attracting them, killing nematodes, fighting fungi, and regulating insect growth, making them a promising source for new pest control agents or biopesticides [21]. Rhazya stricta (Apocynaceae) is a small medicinal shrub found in Saudi Arabia, the UAE, Pakistan, India, and elsewhere [22], 23]. It thrives in sandy soil, characterized by a smooth stem and erect to semi-erect branches. Parts of the plant have antibacterial potential, treat joint infections, cancer, and various skin and stomach diseases [24], 25]. It exhibits larvicidal and growth retarding effects on Culex pipiens [26], 27], Agrotis ipsilon, and Hypera brunneipennis [28]. Its repellent and toxic effects also target the stored grain pests Oryzaephilus surinamensis [29], Trogoderma granarium [30], and Rhyzopertha dominica and T. granarium [31]. Juniperus is a major genus of the Cupressaceae family, with about 70 species worldwide [32]. These species are studied for their antibacterial, antifungal, and insecticidal properties [33], [34], [35], [36], [37]. Juniperus procera is an endangered medicinal tree found in Saudi Arabia; however, an effort is being made to improve its in vitro propagation potential [38]. Juniperus procera is used locally for the treatment of tuberculosis, jaundice [39], intestinal worms, and eye infections, and its wood is resistant to termites and rot [40].

Due to the economic benefits of watermelon and the presence of various insect pests, particularly the watermelon bug, this study aimed to report the molecular diversity of the mitochondrial cytochrome oxidase subunit I gene (mtCOI) loci of watermelon bugs found in Jeddah governorate, Saudi Arabia. Moreover, it evaluated the effectiveness of two chemical pesticides, Imidacloprid (Imidaprid) and Bifenthrin 10 % (Lepostar100 EC), against adult watermelon bugs. Additionally, the study sought to determine the susceptibility of these pests to two types of plant extracts, R. stricta and J. procera, cultivated under local conditions in Saudi Arabia as a safer control method.

2 Materials and methods

2.1 Chemicals and instruments

Chemical pesticides, Imidacloprid (Imidaprid, batch number 17101/89) and Bifenthrin 10 % (Lepostar100 EC, batch number: 82657-04-3), were purchased from a local shop in Jeddah. Ethanol, methanol, and other buffers were obtained from Alfa AesarTM. Deoxyribonucleic acid (DNA) extraction was performed using the MicroElute kit (FAVORGEN BIO CORP, Tawian), with forward and reverse primers targeting COI (Macrogen, Europe), and a 2× master mix (Promega, USA). T100 TM thermal cycler (Bio-Rad, California, Hercules, CA, USA), nanodrop spectrophotometer (MaestroGen, Taiwan), gel documentation system (Vilber Lourmat, France), were used in the present study and sequencing was performed by Macrogen Inc. (Korea).

2.2 Sample collection and rearing

Adults and nymphs of the watermelon bug, Heteroptera: Dinidoridae, were collected in November 2022 from watermelon farms in Al-Khamra, south of Jeddah, Saudi Arabia, a low-altitude region 12 m above sea level [41], at the latitude and longitude as shown in Figure 1 and Table 1. The collected insects were reared and monitored under laboratory conditions at a temperature of 25 ± 2 °C and relative humidity of 60 ± 5 % (Figure 2C and D). The insects were reared in breeding cages (made from muslin, 40 × 40 × 40 cm). This stock colony was maintained with a 14:10 (light: dark) photoperiod throughout the completion of this work. The insect was identified by Professor Dr. Fahd Al-Mikhlafi, Professor of Insect Taxonomy at King Saud University, College of Science, Department of Zoology, Saudi Arabia.

Figure 1: Map showing the watermelon bug sampling locations from Al-Khamra, south of Jeddah, Saudi Arabia.
Figure 1:

Map showing the watermelon bug sampling locations from Al-Khamra, south of Jeddah, Saudi Arabia.

Table 1:

Accession numbers of the present watermelon bugs collected from a Jeddah farm, Saudi Arabia.

Sample number Location Accession numbers Organism
1 Jeddah

21° 14′ 58.3687′′ N

39° 14′ 50.69821′′ E		 LC866666 Coridius janus
2 LC866667 Coridius janus
3 LC866668 Coridius janus
4 LC866669 Coridius janus
5 LC866670 Coridius janus
6 Jeddah

21° 13′ 16.1562′′ N

39° 13′ 48.97884′′ E		 LC866671 Coridius janus
7 LC866672 Coridius janus
8 LC866673 Coridius janus
9 LC866674 Coridius janus
10 LC866675 Coridius janus
11 Jeddah

21° 12′ 42.45696′′ N

39° 12′ 56.34907′′ E		 LC866676 Coridius janus
12 LC866677 Coridius janus
13 LC866678 Coridius janus
14 LC866679 Coridius janus
15 LC866680 Coridius viduatus
16 LC866681 Coridius chinensis
17 Jeddah

21° 7′ 46.28831′′ N

39° 14′ 30.54944′′ E		 LC866682 Coridius nigriventris
18 LC866683 Coridius janus
19 LC866684 Coridius brunneus
20 LC866685 Coridius chinensis
21 LC866686 Coridius janus
22 LC866687 Coridius janus
23 Jeddah

21° 7′ 44.16272′′ N

39° 14′ 23.48131′′ E		 LC866688 Coridius brunneus
24 LC866689 Coridius chinensis
25 LC866690 Coridius chinensis
26 LC866691 Coridius janus
27 LC866692 Coridius chinensis
28 LC866693 Coridius janus

  1. Grey-shaded values refer to Coridius species other than C. janus, recorded in small numbers.

Figure 2: Adults and nymphs of the watermelon bug were collected from an infected farm in Jeddah (A & B) and kept in aluminum cages (40 × 40 × 40 cm) under laboratory conditions (C & D).
Figure 2:

Adults and nymphs of the watermelon bug were collected from an infected farm in Jeddah (A & B) and kept in aluminum cages (40 × 40 × 40 cm) under laboratory conditions (C & D).

2.3 Molecular definition of black watermelon bug by using mtCOI gene

The deoxyribonucleic acid (DNA) was extracted from 28 watermelon bug samples according to Al-Otaibi et al. [42], 43]. Briefly, samples were homogenized, then treated with proteinase K. Next, the DNA was precipitated using 97 % ethanol and purified with silica gel spin columns. The DNA was finally dissolved in 50 μL of deionized water and stored at 4 °C for later use.

The mitochondrial cytochrome oxidase subunit I gene (mtCOI) region was targeted for amplification via polymerase chain reaction (PCR) using forward primer (LCO1490, 5′-GGTCAACAAATCATAAAGATATTGG-3′) and reverse primer (HC02198, 5′-TAAACTTCAGGGTGACCAAAAAATC-3′) [44]. The PCR mixture (20 μL) was prepared with: 1 μL (100 ng/μL) extracted DNA, 7 μL sterile water, 1 μL forward primer, 1 μL reverse primer, and 10 μL of 2× master mix (Promega, USA) in a 0.2 mL PCR Eppendorf tube to amplify a 700 base pair (bp) fragment from COI. The amplification involved 35 cycles with the following steps: 95 °C for 60 s, 40 °C for 60 s, and 72 °C for 90 s, followed by a final extension at 72 °C for 7 min in a T100 TM thermal cycler (Bio-Rad, California, Hercules, CA, USA). PCR products were verified by electrophoresis on a 1.5 % agarose gel stained with ethidium bromide.

PCR products were sequenced using the Sanger method [45]. The resulting data underwent preprocessing, including quality checks and trimming, using Geneious software version 2024.0.5 [46], which is specifically designed for molecular biology tasks. Further, it was submitted to the DNA Data Bank of Japan (DDBJ) (https://www.ddbj.nig.ac.jp/index-e.html) for accession numbers as mentioned in Table 1. The nucleotide sequences of the present isolates were aligned using the COI loci of other isolates with accession numbers, geographic locations, and descriptions, as per the National Center for Biotechnology Information (NCBI) GenBank database (Table 2). The alignment algorithm had three parameters related to gap costs: gap open cost (10), gap extension cost (1), and end gap cost (same as others). The analysis was carried out using CLC Genomics Workbench Version 24.0.2 from QIAGEN Aarhus A/S (digitalinsights.qiagen.com/). Additionally, a BLAST comparison was done between two or more sequences for specific isolates using the Basic Local Alignment Search Tool (BLAST) (https://blast.ncbi.nlm.nih.gov/) [47]. A phylogenetic tree was drawn using the Maximum Likelihood (ML), based on the Tamura-Nei model, by molecular evolutionary genetics analysis version 6.0 (MEGA6), according to Tamura et al. [48].

Table 2:

Reference numbers in the GenBank (NCBI) for the most compatible samples with the study sample.

Accession Description Geographic location names Organism
GU247486 Coridius janus isolate B110 cytochrome oxidase subunit I-like (COI) gene, partial sequence; mitochondrial India Coridius janus
MG838348 Coridius janus voucher PESM110 cytochrome oxidase subunit 1 (COI) gene, partial cds; mitochondrial India Coridius janus
MT765072 Coridius janus isolate H1 cytochrome c oxidase subunit I (COX1) gene, partial cds; mitochondrial India Coridius janus
JQ387600 Coridius nigriventris cytochrome oxidase subunit 1 gene, partial cds; mitochondrial China Coridius nigriventris
JQ387599 Coridius chinensis cytochrome oxidase subunit 1 gene, partial cds; mitochondrial China Coridius chinensis
HQ333535 Coridius sp. ST-2011 voucher B290 cytochrome oxidase subunit I (COI) gene, partial cds; mitochondrial. India Coridius sp.
OR228916 Coridius janus isolate JED_1 cytochrome c oxidase subunit I (COX1) gene, partial cds; mitochondrial Jeddah, Saudi Arabia Coridius janus

2.4 Conventional compounds tested

The efficiency of two types of pesticides used in controlling agricultural pests in Jeddah was evaluated (Table 3).

Table 3:

The chemical properties of the studied insecticides.

Active ingredient Insecticide trade name Usage rate Chemical group Chemical structure and CAS
Imidacloprid (20 % SL) Imidaprid (batch number 17101/89) 100 ml/100 l Neonicotinoid is an insecticide that contains contact, stomach, and systemic activity and is used against a wide range of insects on many crops [49].

[50]
Bifenthrin (w/v) 10 %. Lepostar100 EC (batch number: 82657-04-3) 40 ml/100 l A pyrethroid is a non-systemic pesticide with contact and stomach action, used against many insects on many crops [51].

[52]

  1. CAS Registry Numbers of chemicals appear in bold.

2.5 Non-conventional compounds tested

In this study, the efficiency of two types of plant extracts (R. stricta and J. procera) (Figure 3A and B) collected from the city of Al-Baha was evaluated by Dr. Najeeb Al-Saghir, assistant professor of classification of flowering plants at Al-Baha University. The leaves (1 kg from each) were rinsed in tap water, then with distilled water to remove dust, and dried at room temperature. Dried leaves were ground in an electric grinder to obtain a fine powder. This was followed by extracting the samples with methanol (1:3) and evaporating them using a rotary evaporator to obtain the crude extract for each sample according to Mahyoub [53]. Plant leaves were washed, dried in the shade at room temperature, and prepared for extraction. Fresh leaves (40–60 g) were finely ground and loaded into a 250 ml glass stoppered Soxhlet apparatus. Methanol (200 ml) was added to the round-bottomed flask, and the extraction was conducted for 6 h. The extracts were then concentrated using a rotary evaporator to form a semi-dry material. The extracted components were stored at −10 °C until needed for testing against selected insect stages. Stock solutions of each plant extract were prepared by adding 1 ml of the extract to 99 ml of distilled water containing 0.5 % triton X-100 [54]. From these stock solutions, concentrations of 1, 2, 3, 4, and 5 ppm were prepared in distilled water.

Figure 3: Rhazya stricta (A) and Juniperus procera. (B) were used in the present study.
Figure 3:

Rhazya stricta (A) and Juniperus procera. (B) were used in the present study.

2.6 Evaluation of some conventional and non-conventional insecticides against Coridius janus

Bioassay tests were carried out on randomly selected third-instar male and female nymphs. Five replicates were used, each with 20 nymphs.

2.6.1 Topical application bioassay method

The method of Wang et al. [55], with some modifications, was used to estimate the sensitivity of C. janus adults. A 0.5 μL of the selected pesticide (Imidacloprid and Bifenthrin 10 %) or methanolic plant extracts (R. stricta and J. procera) concentrations was applied to the dorsal side of the bug’s thorax using a Hamilton syringe held in a manual micro-applicator (Hamilton Co., Reno, NV) as a topical treatment application. Different concentrations were used for the topical application of Imidacloprid and Bifenthrin at 1–5 ppm, while methanolic plant extracts of R. stricta ranged from 200 to 1,400 ppm and J. procera from 100 to 1,000 ppm. The tested concentrations were distributed on the dorsal side of the thorax; five replicates for each concentration were used, where each replicate contained 20 adult insects. In addition, five replicates of insects treated with water only are used as controls. The insects were placed in Petri dishes containing untreated watermelon leaves after treatment, and each insect was treated separately. The percentage of mortality (%) was recorded after 24 h of treatment.

2.6.2 Feeding bioassay method

The feeding bioassay was implemented according to Al-Otaibi et al. [56] with some modifications. Accordingly, the same five concentrations of each pesticide/plant extract were prepared in the previous topical application. Watermelon leaves were immersed in pesticide/plant extract (at different concentrations separately) for 30 s, and then left to dry. Each concentration had five replicates, each containing 20 adult insects. Five replicates of the control insects were grown on watermelon leaves treated with water only. Bugs were checked 24 h post-treatment, and the mortality percentage was recorded.

2.7 Statistical analysis

A random design was used to distribute insects and different concentrations of the tested compounds (pesticide/plant extract), calculate mortality % after 24 h of both methods (topical and feeding), and compare them with the control sample. The results are presented as tables of means and standard errors (SE). Laboratory toxicity results (toxicity probit lines (LDP), lethal concentration of 50 % (LC50) and 90 % (LC90) values) were calculated using the LDP Line Program, following Finney’s [57] method, which guided in vitro bio/insecticide toxicity data analysis with software for curve generation and statistical parameter extraction [58], 59]. When a significant treatment effect was observed, means were compared using Fisher’s least significant difference (LSD) test at a p ≤ 0.05.

3 Results

3.1 Molecular definition of watermelon bugs by mtCOI gene

Twenty-eight isolates of watermelon bugs from Jeddah were successfully amplified at 700 bp (Figure 4) and sequenced at the mtCOI gene locus. Their sequences were submitted to DDBJ with different accession numbers, as shown in Table 1. According to the alignment of the present isolates and references found in NCBI Genbank, Table 1 shows that the most abundant species among watermelon bugs found in Jeddah, Saudi Arabia, is C. janus (19 isolates out of 28). The present study has recorded four additional species of Coridius: C. viduatus, C. chinensis, C. nigriventris, and C. brunneus.

Figure 4: Gel electrophoresis of the PCR product = 700 bp, M = low molecular weight DNA marker (100–1,500 bp).
Figure 4:

Gel electrophoresis of the PCR product = 700 bp, M = low molecular weight DNA marker (100–1,500 bp).

By comparing the present Coridius sp. with reference isolates in Table 2, the similarity percentage is the highest against the OR228916 (Jeddah, Saudi Arabia) isolate, ranging from 98.50 % (LC866666) to 78.50 % (LC866691). The present isolates show a significant correspondence to the established reference sequence OR228916 (Jeddah, Saudi Arabia). While the similarity % is lower against other isolates from India or China, ranging from 89.90 % (GU247486 and LC866683) to 74.82 % (LC866689 and JQ387599) (Table 4).

Table 4:

The percentage of similarity between the watermelon bugs of the present study and other global isolates based on BLASTN in NCBI.

The present study isolates % Identical sites Global accession number Country The present study isolates % Identical sites Global accession number Country
LC866666 98.50 % OR228916 Jeddah, Saudi Arabia LC866680 86.79 % HQ333535 India
LC866667 84.60 % OR228916 Jeddah, Saudi Arabia LC866681 76.40 % JQ387599 China
LC866668 83.30 % GU247486 India LC866682 85.70 % JQ387600 China
LC866669 89.10 % MG838348 India LC866683 89.90 % GU247486 India
LC866670 95.20 % OR228916 Jeddah, Saudi Arabia LC866684 81.10 % MG838348 India
LC866671 87.50 % GU247486 MG838348 India LC866685 81.36 % JQ387599 China
LC866672 85.09 % HQ333535 India LC866686 76.60 % MG838348

MT765072		 India
LC866673 88.20 % MT765072 India LC866687 80.89 % HQ333535 India
LC866674 78.92 % HQ333535 India LC866688 82.77 % HQ333535 India
LC866675 89.70 % MT765072 India LC866689 74.82 % JQ387599 China
LC866676 84.80 % HQ333535 India LC866690 83.33 % JQ387599 China
LC866677 83.58 % HQ333535 India LC866691 78.50 % OR228916 Jeddah, Saudi Arabia
LC866678 85.57 % HQ333535 India LC866692 82.51 % JQ387599 China
LC866679 90.10 % OR228916 Jeddah, Saudi Arabia LC866693 79.30 % HQ333535 India

The affinity distance between the present isolates and the references used from (NCBI) and (Bold System) is determined based on a longitudinal scale based on the Tamura-Nei model with 1,000 bootstrap replications in MEGA 7 to build a phylogenetic tree (Figure 5). According to the phylogenetic analysis, the species C. janus was closely related to most of the present isolates (19 isolates out of a total 28 = 68 %), showing a high degree of similarity in DNA sequences. This was followed by other Coridius species with low prevalence among total isolates; C. viduatus (1/28 = 3.6 %), C. nigriventris (1/28 = 3.6 %), C. brunneus (2/28 = 7 %), and C. chinensis (5/28 = 18 %).

Figure 5: Phylogenetic relationships among watermelon bugs collected from Jeddah and the nearest reference isolates found in Genbank.
Figure 5:

Phylogenetic relationships among watermelon bugs collected from Jeddah and the nearest reference isolates found in Genbank.

Figure 6 shows an alignment of DNA sequences from COI of the present isolates and the nearest reference ones. Most of the positions of the present isolates have identical sites with each other and the other GenBank isolates, with a few nucleotide substitutions. A few sequences show significant variations from the consensus DNA sequence. LC866666 is the most similar to the consensus DNA sequence, while LC866677 is the least.

Figure 6: Alignment between the watermelon of the present study and the most closely related reference isolates found in GenBank.
Figure 6:

Alignment between the watermelon of the present study and the most closely related reference isolates found in GenBank.

3.1.1 The bioassay of some conventional and non-conventional insecticides against the watermelon bug

The susceptibility level of watermelon bugs to various conventional and non-conventional insecticides was assessed using two different methods: topical application and feeding. The conventional tested pesticides were Imidacloprid and Bifenthrin 10 %, while the non-conventional tested compounds were the methanolic extract of R. stricta and J. procera leaves.

3.1.2 The bioassay of conventional insecticides

The results in Table 5 show that the mortality percentage of bugs treated with Imidacloprid was directly proportional to the concentration, with mortality rates ranging from 10 ± 0.5 % to 73 ± 0.15 % (P = 0.0001) for topical application (LSD = 3.78) and from 10 ± 0.11 % to 90 ± 0.5 % (P = 0.0001) for the feeding method (LSD = 4.66). The linear response ratios also indicate a direct relationship between the tested concentrations and the percentage of insect death. Percent response increases with concentration for both topical (8.1 ± 0.16 to 67.6 ± 0.25 %) and feeding methods (7.8 ± 0.5 to 87.1 ± 0.28 %), with least significant differences (LSD) of 3.52 and 3.98, respectively. Mortality percentage of the control group (bugs treated with water/feed on leaves treated with water) ranges from 0 to 3 bugs in both methods.

Table 5:

Mortality rate of different concentrations of Imidacloprid (Imidaprid 1, 2, 3, 4, and 5 ppm) on Coridius sp. in five time-independent replicates.

Con. (ppm)f Mortality (%) Linear response (%)
Mean ± SE Mean ± SE
Topical application Feeding method Topical application Feeding method
1 10e  ± 0.5 10e  ± 0.11 8.1e  ± 0.16 7.8e  ± 0.5
2 28d  ± 1.25 34d  ± 0.75 27.4d  ± 0.25 37.4d  ± 0.25
3 36c  ± 0.25 60c  ± 0.18 44.7c  ± 0.75 62.6c  ± 0.15
4 58b  ± 0.25 78b  ± 0.27 57.9b  ± 0.22 78.1b  ± 0.11
5 73a  ± 0.15 90a  ± 0.5 67.6a  ± 0.25 87.1a  ± 0.28
LSD 3.78 4.66 3.52 3.98
P-value 0.0001 0.0001 0.0001 0.0001

  1. The same letter within the column shows a non-significant difference according to the least significant difference (LSD). Mortality % of the control group ranges from 0 to 3 bugs in both methods. fThe concentration (in ppm) of pesticide was prepared using Imidaprid (Imidacloprid).

Similarly, in the case of measuring the sensitivity of adult watermelon bugs to Bifenthrin 10 %, it was found that mortality rates ranged between 5 ± 0.1–60 ± 0.22 % for topical treatment and 7 ± 0.0–64 ± 0.7 % through feeding at concentrations ranging between 1 and 5 ppm (Table 6). In addition, the linear response% increases according to concentration for topical (2.8 ± 0.22–57.6 ± 0.5 %) and feeding methods (4.43 ± 0.01–58.57 ± 0.25 %) with LSD of 7.7 and 10.2, respectively. Mortality percentage of the control group (bugs treated with water/feed on leaves treated with water) ranges from 0 to 3 bugs in both methods.

Table 6:

Mortality rate of different concentrations of Bifenthrin (Lepostar 100 EC 1, 2, 3, 4, and 5 ppm) on Coridius sp. in five time-independent replicates.

Con. (ppm) Mortality (%) Linear response (%)
Mean ± SE Mean ± SE
Topical application Feeding method Topical application Feeding method
1 5e  ± 0.1 7e  ± 0.0 2.8e  ± 0.22 4.43e  ± 0.01
2 12d ± 0.5 17d ± 0.12 15.6d ± 0.11 19.00d ± 0.21
3 27c  ± 0.25 27c  ± 0.75 31.6c  ± 0.25 34.70c  ± 0.40
4 49b ± 0.11 49b ± 0.4 46.0b ± 0.15 48.01b ± 0.17
5 60a  ± 0.22 64a  ± 0.7 57.6a  ± 0.5 58.57a  ± 0.25
LSD 5.9 8.5 7.7 10.2
P-value 0.0001 0.0001 0.0001 0.0001

  1. The same letter within the column shows a non-significant difference according to the least significant difference (LSD). Mortality % of the control group ranges from 0 to 3 bugs in both methods. fThe concentration (in ppm) of pesticide was prepared using Lepostar 100 EC (Bifenthrin).

Figure 7 and Table 7 show the toxicity probit lines (LDP) of Imidacloprid and Bifenthrin 10 % and the statistical constants derived from them. In the case of Imidacloprid, the LC50 and LC90 values of the watermelon bugs after treatment at 24 h were 3.37 and 10.24 ppm for the topical application and 2.45 and 5.50 ppm for the feeding, respectively. On the other hand, Bifenthrin 10 % treatment results in the death of 50 % of bugs at 4.32 ppm and 90 % at 11.46 ppm for topical application. In addition, the feeding method results in the death of 50 % of watermelon bugs at 4.17 ppm, while 90 % of them die at 12.20 ppm.

Figure 7: Resistance ratio (RR) that compares the efficacy of Imidacloprid (A) and Bifenthrin 10 %. (B) using the topical and feeding methods.
Figure 7:

Resistance ratio (RR) that compares the efficacy of Imidacloprid (A) and Bifenthrin 10 %. (B) using the topical and feeding methods.

Table 7:

Toxicity index of Imidacloprid (Imidaprid) and Bifenthrin (Lepostar 100 EC) against watermelon bug using topical and feeding methods.

Statistical parameters Imidacloprid Bifenthrin 10 %
Topical application Feeding method RR Topical application Feeding method RR
Slope 2.65 3.65 1.71 3.03 2.75 1.04
(Chi)2 4.9 (7.8)a 2.2 (7.8)a 4.5 (7.8)a 5.7 (7.8)a
p 0.0017 0.0052 0.0021 0.0012
r 0.96 0.99 0.97 0.98
LC50 (ppm) 3.37 2.45 4.32 4.17
LC90 (ppm) 10.24 5.50 11.46 12.20

  1. aTabulated (Chi)2.

According to Table 7, the chi-square values for both tested compounds are lower than 7.8 based on the statistical analysis at three degrees of freedom and a significance level of 0.05. This demonstrates the consistency of the tested strain, showing a strong positive correlation between the tested concentrations and the resulting mortality rates. The correlation strength ranged from 0.96 to 0.99 for Imidacloprid and from 0.97 to 0.98 for Bifenthrin for both topical application and feeding methods, respectively. The resistance ratio (RR) values confirmed that the feeding method was more effective than the topical application by approximately 1.37 and 1.04 folds for Imidacloprid and Bifenthrin, respectively.

The results showed that the Imidacloprid pesticide was more effective against watermelon bugs than Bifenthrin by about 1.28 and 1.70 folds through topical application and feeding, respectively (Figure 8). Overall, the results demonstrated that watermelon bugs showed greater susceptibility to the compounds tested when used for feeding, with Imidacloprid proving to be more effective than Bifenthrin 10 %.

Figure 8: Comparison between the treatment methods of pesticides according to the resistance ratio (RR) values.
Figure 8:

Comparison between the treatment methods of pesticides according to the resistance ratio (RR) values.

3.1.3 The bioassay of some plant extracts against the watermelon bugs

The effect of the R. stricta extract against adults of watermelon bugs is illustrated in Table 8. The effective used concentrations of the plant extract (R. stricta) range from 200 to 1,400 ppm. The mortality percentage of the treated insects corresponding to these concentrations ranged from 13 ± 0.01 % to 88 ± 0.15 % for topical application and from 17 ± 0.17 % to 91 ± 0.22 % for the feeding method. The findings indicated a significant direct correlation between the mortality rates and the concentrations applied, as demonstrated by the linear response rate that ranges from 8.90 ± 0.22 to 80.80 ± 0.14 % for topical application and from 12.20 ± 0.25 % to 85.27 ± 0.25 % for feeding.

Table 8:

Mortality rates of different R. stricta extract concentrations on Coridius sp. in five time-independent replicates.

Con. (ppm) Mortality (%) Linear response (%)
Mean ± SE Mean ± SE
Topical application Feeding method Topical application Feeding method
200 13e  ± 0.01 17e  ± 0.17 8.90e  ± 0.22 12.20e  ± 0.25
500 30d  ± 0.11 36d  ± 0.225 38.11d  ± 0.70 45.12d  ± 0.11
800 58c  ± 0.05 63c  ± 0.15 59.21c  ± 0.12 65.98c  ± 0.15
1,100 69 b  ± 0.25 78 b  ± 0.12 72.44 b  ± 0.15 78.05b  ± 0.50
1,400 88a  ± 0.15 91a  ± 0.22 80.80a  ± 0.14 85.27a  ± 0.25
LSD 11.50 13.60 14.80 9.80
P 0.0001 0.0001 0.0001 0.0001

  1. The same letter within the column shows a non-significant difference according to the least significant difference (LSD). Mortality % of the control group ranges from 0 to 3 bugs in both methods.

On the other hand, the concentrations of J. procera extract that were effectively used ranged from 100-1,000 ppm (Table 9). The mortality % of topically treated insects ranged from 25 ± 0.11 % to 91 ± 0.25 % and 30 ± 0.23 %–97 ± 0.05 for the feeding. The increase in concentration led to a significant increase in the mortality rates, as 1,000 ppm concentration was the highest significant, as it led to a linear response rate of 87.10 ± 0.14 % and 92.66 ± 0.37 % with topical application and feeding, respectively.

Table 9:

Mortality rates of different J. procera extract concentrations on Coridius sp. in five time-independent replicates.

Con. (ppm) Mortality (%) Linear response (%)
Mean ± SE Mean ± SE
Topical application Feeding method Topical application Feeding method
100 25e ± 0.11 30d ± 0.23 21.6e ± 0.47 25.31d ± 0.98
300 49d ± 0.15 55c ± 0.19 55.15d ± 0.57 63.50c ± 0.33
500 70c ± 0.22 78b ± 0.25 71.04c ± 0.42 79.24b ± 0.28
800 82b ± 0.75 89a ± 0.01 82.77b ± 0.89 89.37a ± 0.17
1,000 91a ± 0.25 97a ± 0.05 87.10a ± 0.14 92.66a ± 0.37
LSD 18.5 11.2 7.8 9.6
P 0.0001 0.0001 0.0001 0.0001

  1. The same letter within the column shows a non-significant difference according to the least significant difference (LSD). Mortality % of the control group ranges from 0 to 3 bugs in both methods.

According to the statistical analyses of Table 10 and Figure 9, the LC50 of R. stricta extract was equal to 651.98 and 556.93 ppm, while the LC50 of J. procera leaves was 206.04 ppm and 256.70 ppm for topical application and feeding, respectively. By comparing the values of LC50 of watermelon bugs treated with plant extracts, the efficiency of R. stricta through feeding is higher than the topical application by 1.17 folds, while J. procera topical application is higher than feeding method by 1.25 folds.

Table 10:

The toxicity index of R. stricta and J. procera extracts against the watermelon bug using the topical application and feeding method.

Statistical parameters R. stricta J. procera
Topical application Feeding method Topical application Feeding method
Slope 2.62 2.62 2.12 1.92
(Chi)2 6.89 (7.8)a 3.54 (7.8)a 6.18 (7.8)a 3.65 (7.8)a
p 0.0008 0.0061 0.0065 0.0301
r 0.9691 0.9715 0.9678 0.9841
LC50 (ppm) 651.98 556.93 206.04 256.70
LC90 (ppm) 2,007.50 1,718.53 830.76 1,198.05

  1. aTabulated (Chi)2.

Figure 9: Regression lines for R. stricta and J. procera bioassay of watermelon bug using topical application and feeding technique.
Figure 9:

Regression lines for R. stricta and J. procera bioassay of watermelon bug using topical application and feeding technique.

The results show that J. procera extract through topical (contact) application had higher activity against adults of watermelon bugs compared to its feeding method, R. stricta extract feeding, and R. stricta topical (contact) application by about 1.25, 2.70, and 3.16 folds, respectively (Figure 10).

Figure 10: Comparison between LC50 values of the tested plant extracts against adults of watermelon bugs.
Figure 10:

Comparison between LC50 values of the tested plant extracts against adults of watermelon bugs.

4 Discussion

Molecular biology serves as a key classification method for identifying organisms and understanding the relationships among individuals of a species and its subspecies, including the identification of the watermelon bug through DNA barcoding, as noted by Tembe et al. [60]. In the present study, polymerase chain reaction (PCR) results indicated that all samples exhibited the same molecular weight of 700 bases (bp). Furthermore, nucleotide sequencing of watermelon bug samples from Jeddah revealed a genetic relationship with Coridius sp. Among these, C. janus was found to be the most prevalent species, followed by C. chinensis, C. brunneus, C. nigriventris, and C. viduatus. This study represents the molecular-level record of these various species in Saudi Arabia. This poses a significant risk to the cultivation of this essential crop in Saudi Arabia and substantially reduces watermelon yields. This result coincides with the emergence of insect species in Saudi Arabia (not its native area), which accidentally enter from other regions: Rhynchophorus ferrugineus found in three (Jeddah, Makkah, and Taif) [56] and Aedes aegypti in two (Taif and Jeddah) governorates [43].

Alignment of mtCOI indicates that the current isolates exhibit a remarkable degree of genetic similarity with the Coridius sp. isolates from India and China. Jeddah governorate is a significant industrial city on the Red Sea in Saudi Arabia, acting as a crucial gateway for millions of imported products, trade animals, and pilgrims from countries [41], which could inadvertently introduce pests. This discovery is crucial for the classification of these insects and could support efforts to curb their spread. Nonetheless, the few discrepancies identified may offer valuable insights into the genetic variability influencing pest management [43].

Pesticides are a primary method for controlling crop pests; however, many pests have developed resistance to various pesticides, which complicates effective management. Consequently, evaluating pest susceptibility to these chemicals is essential before applying them. This assessment is vital for the success of pest control programs. Many earlier studies have underscored the significance of understanding resistance patterns to enhance management strategies and minimize the likelihood of ineffective pest control. By examining resistance, we can make informed choices regarding pesticide applications and consider alternative approaches when needed [61].

The results showed a difference in the susceptibility levels of watermelon to the tested pesticides, which was evident in the variation of the LC50 % values for the treated adults exposed to these compounds. This disparity is attributed to differences in the mode of action, the composition of the used pesticide, and the dose. These findings align with Aljedani [10], who evaluated the efficiency of Imidacloprid and Azadirachtin against the watermelon bug, C. viduatus. In addition, Al-Dosary et al. [62] highlight the variation in susceptibility levels of red palm weevils in relation to the tested compounds. The pesticides tested were more effective when administered through the feeding method (Imidacloprid LC50 = 2.45 ppm, Bifenthrin LC50 = 4.17 ppm), which involved treating watermelon leaves with specific concentrations. This method showed greater efficacy than topical application (Imidacloprid LC50 = 3.37 ppm, Bifenthrin LC50 = 4.32 ppm), where the pesticide is applied to the insect’s dorsal side. The increased effectiveness of the feeding approach may stem from its ability to deliver the pesticide directly to the insect’s vulnerable areas via both feeding and contact, while topical application only facilitates contact exposure. These findings align with those observed by previous studies [56], 63], 64].

The results showed that the Imidacloprid (LC50 = 2.45 ppm, 3.37 ppm) was more effective compared to Bifenthrin 10 % (LC50 = 4.17 ppm, 4.32 ppm) through feeding and application methods, respectively. This may be due to the chemical group to which the pesticide belongs (Neonicotinoids), which have a lethal effect against insects, as neurotoxins that affect the polarization of neurons. Several studies have reported that insects are highly susceptible to neonicotinoids, with a positive linear response rate, mortality rates occurring at low concentrations, and a significant response rate associated with high mortality rates [11], 12], 65].

Over the past few years, research has shown that pesticide toxicity is causing severe health problems. Exposure to pesticides by parents or during early childhood or adolescence can be linked to various human diseases. At a cellular level, pesticides can trigger epigenetic and genetic changes that pose serious direct or indirect risks. Whether exposure is direct or indirect, it can lead to chronic or acute toxicity. Pesticides also cause a range of health issues, including neurogenic, carcinogenic, and reproductive disorders in humans [66]. Synthetic pyrethroids, like Bifenthrin, cause sodium channels to stay open, leading to hyperexcitation and nerve blockage. Insecticides such as neonicotinoids, including Imidacloprid, bind to the acetylcholine site on the nicotinic acetylcholine receptor (nAChR), causing lethargy and paralysis [67]. The issues from organo synthetic insecticides have led to the adoption of natural products as an alternative pest control method [68], 69]. Generally, these products are less persistent in the environment and safer environmentally and toxicologically than many current organo synthetic pesticides [70]. Beyond lethal effects, botanical insecticides may repel pests, inhibit oviposition, and alter various arthropod pests’ feeding and hormonal systems [71]. These traits enhance the appeal of biopesticides for pest management [72]. Saudi Arabia has a diverse range of flora, including valued medicinal plants like R. stricta and J. procera Hochst, as noted by Elsheikh et al. [73]; Al-Zahrani [74]. The current study demonstrates the effectiveness of R. stricta and J. procera extracts in controlling watermelon bugs, aligning with modern agricultural pest management trends [10].

The results show that there is a differential effect of plant extracts against adult black watermelon bugs. Their toxic effect was found to be dose-dependent. J. procera is more effective on Coridius sp. with an LC50 of 206.04 ppm for topical application and an LC50 of 256.70 ppm for feeding, compared to R. stricta, which has an LC50 of 651.98 ppm for topical application and an LC50 of 556.93 ppm for feeding. This aligns with previous studies indicating that the extracts of Tephrosia vogelii and Moringa oleifera demonstrated effectiveness against insect pests affecting watermelon [75].

Rhazya stricta exhibits toxicity against Coridius sp. due to compounds like glycosides, triterpenes, and alkaloids, which can disrupt physiological processes by inhibiting enzymes such as lipoxygenase and acetylcholinesterase. Studies show that rhazimine from R. stricta inhibits arachidonic acid metabolism [76]. Naz et al. [77] explore the potential of R. stricta as a new sustainable and environmentally friendly method for managing Meloidogyne incognita in tomato crops, offering a cost-effective and low-risk alternative to chemical nematicides. It also demonstrates larvicidal effects against A. aegypti and impacts the growth of C. pipiens [26]. Additionally, its extract has shown effectiveness against agricultural pests like A. ipsilon and Helicoverpa brunneipennis [28], and research by Madkour et al. [29] found high mortality rates in O. surinamensis after exposure to R. stricta extracts.

Juniperus procera, a member of the Cupressaceae family, is recognized for its insecticidal effects [73]. Its methanolic extract is more effective than R. stricta at increasing watermelon bug mortality at lower concentrations. The topical application of J. procera extract demonstrated greater activity against watermelon bug adults than J. procera feeding, R. stricta feeding, and topical application, by approximately 1.25, 2.70, and 3.16 folds, respectively. This is consistent with a previous study by Elsheikh et al. [73], which reported that extracts from J. procera stems significantly impacted the fecundity, fertility, and sterility index of adult female Chrysomya albiceps. Additionally, malformations were observed in the pupae and adults of C. albiceps after larvae were treated with acetone and petroleum ether extracts from J. procera stems.

Salih et al. [78] and Al-Zahrani [79] identified various phytochemical compounds in J. procera, including glycosides/aglycones, ferruginol, phenanthrene, and n-hexadecanoic acid, which are associated with other phenolic compounds. The essential oil and extract that contain ferruginol and phenanthrene exhibit an antifeedant effect on the red clover borer Hylastinus obscurus (Coleoptera: Curculionidae). This explains why the topical application of J. procera extract has greater activity against watermelon bug adults than the feeding method, due to its antifeedant potential. In addition, J. procera demonstrates insect antirepellent activity against other insects such as Anopheles arabiensis, which shows significant contact effects, as reported by Karunamoorthi et al. [80].

4.1 Limitations of the study

1. Controlled Conditions: The experiments took place under laboratory settings, which may not accurately reflect field conditions. Factors such as temperature, humidity, and interactions with other organisms were not considered, potentially affecting the effectiveness of the extracts in natural environments. 2. Chemical Analysis of Extracts: The chemical makeup of the R. stricta and J. procera extracts was not examined. Differences in extraction methods could alter the active compounds, impacting the observed mortality rates. 3. Application Techniques: The study evaluated different application methods (topical versus feeding) separately, but did not explore the potential combined or synergistic effects of using both methods together. 4. Long-term Impact: The research did not investigate the long-term effectiveness of these extracts. Future work should assess residual activity over time and their effects on ecosystems and non-target organisms. 5. Resistance Potential: The possibility that pests could develop resistance to the plant extracts over time was not explored, which is important for understanding the sustainability of these control methods. 6. Sample Size and Replicates: The number of replicates and sample sizes might be limited, affecting the statistical power of the results. A larger sample size could provide more robust conclusions about the genetic diversity, susceptibility, and resistance of Coridius sp. to the tested treatments. By recognizing these limitations, future research can target these gaps to better understand the effectiveness and practical use of plant extracts in pest management.

5 Conclusions and recommendations

Different species of Coridius were recorded in Saudi Arabia for the first time, indicating that this insect is an invasive pest in the Saudi environment. This situation necessitates field studies to monitor its seasonal activity under the climatic conditions of Saudi Arabia and to identify its vital enemies. The results showed that the pesticide Imidacloprid had a stronger effect against the watermelon bug, Coridius sp, highlighting the variation in pesticide efficiency. We recommend conducting biological evaluation experiments for pesticides before their application and developing a comprehensive database about them for reference in planning control programs and making informed decisions regarding pesticide use. The study demonstrated that local plant extracts were effective, particularly those from J. procera. This study suggests isolating the components of this plant to obtain the pure active ingredient and prepare it as a commercial formulation. Enhancing the control of these insects by using insecticides derived from natural sources, which are eco-friendly.

Corresponding author: Nahed Ahmed Hussien, Biology Department, College of Science, Taif University, Taif 21944, Saudi Arabia, E-mail:

Acknowledgments

The authors would like to acknowledge the Deanship of Graduate Studies and Scientific Research, Taif University for funding this work.

  1. Funding information: The authors would like to acknowledge the Deanship of Graduate Studies and Scientific Research, Taif University for funding this work.

  2. Author contribution: Wafa Mohammed Al-Otaibi: Conceptualization, Investigation, Data curation, review & editing; Habeeb M. Al-Solami: Methodology; Abdullah G. Alghamdi: Methodology; Akram S. Alghamdi: Validation; Nahed Ahmed Hussien: Software, Validation, Data curation, Writing – original draft, review & editing; Naser Ahmed Alkenani: Methodology; Shatha I. Alqurashi: Conceptualization; Tariq Saeed Alghamdi: Conceptualization; Dina F. Alhashdi: Conceptualization; Jazem A. Mahyoub: Investigation, Methodology, Data curation, Writing – original draft, review & editing. All the authors accept the final version of the article.

  3. Conflict of interest: Authors state no conflict of interest.

  4. Data availability statement: The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Received: 2025-07-02
Accepted: 2025-10-26
Published Online: 2025-12-30

© 2025 the author(s), published by De Gruyter, Berlin/Boston

This work is licensed under the Creative Commons Attribution 4.0 International License.

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  205. Using plant electrical signals of water hyacinth (Eichhornia crassipes) for water pollution monitoring
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  228. Preparation and characterization of lemongrass oil nanoemulsion: Antimicrobial, antibiofilm, antioxidant, and anticancer activities
  229. Fluorescent detection of sialic acid–binding lectins using functionalized quantum dots in ELISA format
  230. Smart tectorigenin-loaded ZnO hydrogel nanocomposites for targeted wound healing: synthesis, characterization, and biological evaluation
  231. Corrigendum
  232. Corrigendum to “Utilization of convolutional neural networks to analyze microscopic images for high-throughput screening of mesenchymal stem cells”
  233. Corrigendum to “Effects of Ire1 gene on virulence and pathogenicity of Candida albicans”
  234. Retraction
  235. Retraction of “Down-regulation of miR-539 indicates poor prognosis in patients with pancreatic cancer”
https://doi.org/10.1515/biol-2025-1219
Keywords for this article
biological control; Coridius; Jeddah; molecular identification; mtCOI; Saudi Arabia
Creative Commons
BY 4.0

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  223. Bioengineering and Biotechnology
  224. Impact of hyaluronic acid-modified hafnium metalorganic frameworks containing rhynchophylline on Alzheimer’s disease
  225. Emerging patterns in nanoparticle-based therapeutic approaches for rheumatoid arthritis: A comprehensive bibliometric and visual analysis spanning two decades
  226. Application of CRISPR/Cas gene editing for infectious disease control in poultry
  227. Preparation of hafnium nitride-coated titanium implants by magnetron sputtering technology and evaluation of their antibacterial properties and biocompatibility
  228. Preparation and characterization of lemongrass oil nanoemulsion: Antimicrobial, antibiofilm, antioxidant, and anticancer activities
  229. Fluorescent detection of sialic acid–binding lectins using functionalized quantum dots in ELISA format
  230. Smart tectorigenin-loaded ZnO hydrogel nanocomposites for targeted wound healing: synthesis, characterization, and biological evaluation
  231. Corrigendum
  232. Corrigendum to “Utilization of convolutional neural networks to analyze microscopic images for high-throughput screening of mesenchymal stem cells”
  233. Corrigendum to “Effects of Ire1 gene on virulence and pathogenicity of Candida albicans”
  234. Retraction
  235. Retraction of “Down-regulation of miR-539 indicates poor prognosis in patients with pancreatic cancer”
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