https://doi.org/10.22319/rmcp.v16s4.6701

Technical note

Estimation of the frequency of lice collected from water buffalo (Bubalus bubalis) at production units in the state of Veracruz, Mexico

 

Melina Maribel Ojeda Chi ^a

Dora Romero Salas ^b*

Anabel Cruz Romero ^b

Milagros González Hernández ^c

Carolina Cárdenas Amaya ^b

Greta Hanako Rosas Saito ^d

 

^a Universidad Veracruzana. Facultad de Ciencias Biológicas y Agropecuarias. Tuxpan, Veracruz, México.

^b Universidad Veracruzana. Facultad de Medicina Veterinaria y Zootecnia. Veracruz, México. 91710.

^c Universidad Autónoma de San Luis Potosí. Facultad de Agronomía y Veterinaria. San Luis Potosí, SLP, México.

^d Instituto de Ecología. Red de Estudios Moleculares Avanzados. Xalapa, Veracruz, México.

 

*Corresponding author: dromero@uv.mx

 

Abstract:

This research aimed to determine the occurrence of lice in Buffalo Production Units (BPU) in Veracruz, Mexico. Fifty-seven (57) buffaloes of different sexes and ages were inspected in two BPUs located in the municipalities of Cotaxtla and Medellín de Bravo (BPU1 and BPU2). The lice were collected from different regions of the body and preserved in vials with 70 % ethanol for transfer to the laboratory. Taxonomic identification was performed with stereoscopic and scanning electron microscopy. The frequency, abundance, and intensity of lice in each BPU, anatomical region, and developmental stage evaluated were calculated. The overall frequency of lice infestation was 78.9 (CI_95%: 65.7 - 88.2). The frequency for BPU1 and BPU2 was 60 % and 100 %, respectively. Six hundred ten lice were collected from the two BPU and only the louse species Haematopinus tuberculatus was found. The abundance was 610 lice/57 buffaloes in total (10.7) and the intensity was 610 lice/45 infested buffaloes (13.6). The costal region was the place with the highest presence of lice. The nit/egg stage was the most abundant, followed by adult lice and nymphs (78.4 %, 16.1 %, and 5.1 %, respectively). The high frequency of lice in buffaloes at BPU in Veracruz can compromise animal health and meat and milk production in buffalo production systems.

Keywords: Lice, Buffalo, Diseases, Mexico.

 

Received: 04/06/2024

Accepted: 28/02/2025

 

In Mexico, buffalo production is an alternative for meat and milk production due to their high rusticity, docility, and ability to adapt to various ecosystems. However, buffalo can also contract viral, bacterial, fungal, and parasitic diseases^(1,2,3). Ectoparasites are of medical-veterinary importance because they can be vectors of diseases. In buffaloes, Haematopinus tuberculatus, or the sucking louse, is the most common and is present in Europe, Asia, South America, Africa, and Australia⁽⁴⁾. H. tuberculatus causes lesions that produce anorexia, cachexia, and reduced production. While the infestation can be asymptomatic, it causes negative effects on milk production and weight gain in growing animals⁽⁴⁾. Besides, its presence has been associated with the transmission of Anaplasma marginale, Trypanosoma vivax, and Brucella abortus^(5,6). In Mexico, there are reports of the presence of A. marginale in lice collected from buffalo⁽⁷⁾. Additionally, other lice species, such as H. quadripertusus, H. eurysternus, and Linognathus vituli, have been reported in buffalo from Iraq and Pakistan, respectively⁽⁸⁾. Therefore, this work aims to determine the occurrence of lice in water buffalo in buffalo production units in the state of Veracruz.

The study was conducted from January to June 2023 in Buffalo Production Units (BPU) selected with the non-statistical convenience method in the municipalities of Medellín de Bravo (BPU1, N: 27) and Cotaxtla (BPU2, N: 30) in the state of Veracruz. In both units, the animals were of the Murrah breed, of different sexes and ages.

Firstly, the BPU that had animals infested with lice were identified. All animals from each BPU positive for lice were included in the study. The animals were individually inspected from head to tail for lice for two or three minutes, without distinction of sex and age; the presence or absence of ectoparasites and the affected body region were recorded by using specific tables. A positive animal was considered to be one that had at least one louse at any stage of development. The collected specimens were deposited in vials containing 70 % ethanol for conservation and transferred to the Parasitology Laboratory of the Diagnostic Unit of the Torreón del Molino Ranch of the Faculty of Veterinary Medicine and Zootechnics of the Veracruzana University.

In the laboratory,  each development stage  (adults,  nymphs, and eggs)  was clarified with 10 % KOH for 3 to 5 min, following the methodology described by Shakya⁽⁹⁾; subsequently, they were mounted on slides for examination under the stereo microscope. The species of louse was determined through the taxonomic keys developed by Guzmán-Torres and Cano-Santana⁽¹⁰⁾. In addition, a scanning electron microscopy (SEM) was performed in the Advanced Molecular Studies Laboratory of the Institute of Ecology of Xalapa, Veracruz, in order to describe the main morphological characteristics of the lice. As a first step, a washing was carried out using an ultrasonic cleaner (Cole-Parmer 8848), followed by chemical fixation/dehydration with ethanol and xylene and drying using a critical point dryer (Quorum model K850). The specimens were then covered with gold using a metal ionizer (Quorum model Q150R S) for analysis in the field emission SEM (FEI Quanta 250 FEG).

To analyze the information, descriptive statistics were obtained by means of online statistical software (VassarStats: Website for Statistical Computation), which was used to estimate the frequency and 95 % confidence intervals. Frequency was obtained from the number of infested buffaloes/number of buffaloes examined × 100. Mean abundance refers to the total number of lice collected/total number of buffaloes tested. Mean intensity refers to the total number of lice collected/number of buffaloes infested.

In total, all 57 buffaloes from the two BPU were included in the study. Table 1 shows the frequency of animals positive for some stage of lice development. The overall frequency of lice infestation was 78.9 % (45/57). In the BPU1 located in Cotaxtla, there was a frequency of 60.0 % (18/30) and the BPU2 located in Medellín de Bravo presented 100 % (27/27) of infested buffaloes. The mean abundance was 610 lice collected from 57 buffaloes (10.7 lice/buffalo) and the mean intensity was 610 lice collected from 45 infested buffaloes (13.6 lice/buffalo).

 

 

 

Table 1: Frequency of lice found in the BPU in Cotaxtla and Medellín de Bravo

CI= 95 % confidence interval.

 

In total, 610 lice were collected, of which 481 were egg/nits and 129 lice (31 nymphs and 98 adult lice). The only species identified was Haematopinus tuberculatus (Table 2).

 

 

Table 2: Frequency of infestation by nits, nymphs, and adult lice of H. tuberculatus collected in the different body areas of Bubalus bubalis

 

 

 

Figure 1 shows a female H. tuberculatus. This species of louse was characterized by being an apterous insect with a dorsoventrally flattened body. The head was elongated and arrow-shaped and the thoracic area was much wider than it was long (Figure 1A). Likewise, the thoracic area appeared to be fused (Figure 1C)^(5,11). Another characteristic of this louse is that it has the “nail-finger” complex in the tarsal segment, forming a tarsal claw that allows it to attach to the host’s hair (Figure 1B). It also had a sclerotized abdominal segment, forming lateral lobes whose function is to provide rigidity to the abdomen. The genitalia had finger-like projections or gonopods that serve to guide, manipulate, and stick the eggs to the host’s hairs (Figure 1D)⁽¹²⁾.

 

 

 

 

Figure 1: Scanning electron microscopy, H. tuberculatus dorsal (left) and ventral (right) views

A) Arrow-shaped head, B) hook-shaped tibial-tarsal claw, C) thoracic area with fused appearance, D) vulva in the shape of fingers.

 

 

 

In countries where buffalo is a common productive species, lice prevalence of 11.6 % (Brazil)⁽¹³⁾ to 100 % (Iraq and India)⁽⁸⁾ has been informed. In Mexico, there are recent reports of prevalences of 19 to 100 % of H. tuberculatus in adult buffalo and calves in the states of Veracruz and Tabasco, respectively^(7,14). Likewise, only the level of infestation has been reported in buffaloes, with low infestation (1-10 lice) in adult animals and medium infestation (11-25 lice) in calves⁽¹⁴⁾. On the other hand, in cattle, an average intensity of 8 to 36 lice and an average abundance of 36 to 56 lice of the species Linognathus vituli and H. Eurysternus have been informed. In this study, similar results were found with respect to intensity; nevertheless, the abundance found was lower than what has been previously described in cattle (10 lice/buffalo)⁽¹⁵⁾.

The frequency of infestation of the animal’s body areas was also obtained, and it was found that the costal region was the most frequent, 100 % (45/45), followed by the cervical or neck region with 80 % (36/45) frequency, the scapular region with 42.2 % (19/45) and, to a lesser extent, the ventral,  coccygeal, and auricular regions with 20 % (9/45), 11.1 % (5/45), and 4.4 % (2/45), with significant differences among the different regions (P<0.05).

Chaudhuri and Kumar⁽¹⁶⁾ indicate that the location of H. tuberculatus depends on the stage of development since adult lice are most often found on the back, neck, and hind legs, but not on the head and tail. Nonetheless, other researchers⁽¹⁴⁾ reported the presence of H. tuberculatus in the head region in a BPU of Tabasco.

In relation to the frequency of each stage of development of H. tuberculatus present by region, Table 2 shows that there were high frequencies of eggs/nits and adult stages in the costal, cervical or neck, and scapular regions.

The results of this research are different from those informed in another study⁽¹⁷⁾, where they mention that the  most  infested  region is the tail  (77.7 %)  and less frequently,  the face (22.2 %); likewise, Ojeda-Robertos et al⁽¹⁴⁾ mention that the head, body, and forelimbs were the regions of predilection of the adult phases. The results of this study coincide with those reported by Figueiredo⁽¹⁸⁾, who found the neck area to be the region with the highest frequency.

On the other hand, it is mentioned⁽¹⁸⁾ that adult lice are usually not found where they oviposit their eggs, which coincides with what was found in this work, where nits/eggs were found in the ear and neck regions, whereas the adult stage was found in the ventral and coccygeal regions. It has been reported that the nit/egg phase represents the highest percentage of the development stages present in the animals⁽¹¹⁾, a result similar to that described in this study, where nits/eggs represented 78.8 % of the stages found in the buffaloes evaluated.

This study demonstrated the presence of animals with H. tuberculatus in BPU in the municipalities of Medellín and Cotaxtla, Veracruz. Likewise, there was a higher frequency of lice in the costal and cervical regions.

The information generated in this study highlights the need to control this ectoparasite because it has been associated with the transmission of Anaplasma marginale and Brucella spp^(7,19). In addition, it is necessary to determine what factors are associated with its presence in order to implement control programs with directed designs.

 

Acknowledgements

The authors are grateful for the support provided by each of the BPUs that allowed them to work with their animals.

 

Funding

This research was conducted with funding from the Parasitology Laboratory located at the Torreón del Molino Ranch of the Faculty of Veterinary Medicine and Zootechnics of the Veracruzana University.

 

Conflict of interest

The authors state that they have no conflict of interest.

 

Literature cited:

1.    de la Cruz-Cruz LA, Roldán-Santiago P, Berdugo-Diaz DF, Rodríguez-Florentino R, Berdugo-Gutiérrez JA. Characteristics of buffalo production and research systems in southern Mexico. J Buffalo Sci 2022;11:19–31. https://doi.org/10.6000/1927-520X.2022.11.03.

2.    Cruz L, Roldan P, Maitret E, Zava M. El búfalo de agua Tomo 1: Generalidades y características productivas. Ciudad de México: LID Editorial Mexicana SA de CV. 2021.

3.    Romero SD, Pérez de León AA. Bubalinocultura en México: retos de industria pecuaria naciente. Logros y Desafíos de la Ganadería Doble Propósito, 6ta ed. Maracaibo, VN: Fundación; 2014.

4.    Ahmed WM, Habeeb SM, El Moghazy FM, Hanafi EM. Observation on pediculosis in buffalo-cows with emphasis on its impact on ovarian activity and control by herbal remedies. WASJ 2009;6:1128–1138.

5.    Prasath NB, Latchumikanthan A, Selvaraj J. Velusamy R. Occurrence of Anaplasma bovis in a buffalo calf infested with Haematopinus tuberculatus (Burmeister, 1839): A morphological study. Indian J Vet Pathol 2023;3:237-241.

6.    Dyonisio GHS, Batista HR, da Silva RE, de Freitas ARC, de Oliveira CJ, de Oliveira MIB, et al. Molecular diagnosis and prevalence of Trypanosoma vivax (Trypanosomatida: Trypanosomatidae) in buffaloes and ectoparasites in the Brazilian Amazon Region. J Med Entomol 2021;1:403-407. https://doi.org/10.1093/jme/tjaa145.

7.    Hernández-Velasco A, Sánchez-Montes S, Romero-Salas D, Cruz-Romero A, Jiménez-Hernández J.A, Becker I, Aguilar-Domínguez M, Pérez de León AA. First record of natural infection with Anaplasma marginale in sucking lice infesting the water buffalo (Bubalus bubalis) in Mexico. Parasitol Res 2020;11:3853-3856. https://doi.org/10.1007/s00436-020-06772-7.

8.    AL-Lahaibi BY, AL-Taee AF. Detection of some species of lice and ticks infestation on local buffalo in Mosul city. Iraqui J Vet Sci 2018;2:43-50 10.33899/ijvs.2019.153876.

9.    Shakya M, Kaveri KG, Jamra S, Singh M, Fular A, Agrawal V, Jatav GP, Jayraw AK, Kumar S. Detection of deltamethrin, cypermethrin and flumethrin efficacy against buffalo lice-Haematopinus tuberculatus. Trop Anim Health Prod 2022;18;1:66. doi: 10.1007/s11250-022-03063-4. PMID: 35041093.

10. Guzmán-Torres M, Cano-Santana Z. Actualización del listado de piojos (Insecta: Phthiraptera) de México: distribución, riqueza, grado de especificidad y pediculosis humana. RMB. 2022.

11. Egri, B. Louse infestation of ruminants. Bovine science—a key to sustainable development. Sadashiv SO, Sharangouda JP, editors. Intechopen limit; 2018:79-88.

12. Reeves WL, Lloyd JE. Louse F, Keds B. Flies (Hippoboscoidea): in Mullen GLD. Medical veterinary entomology. USA: Academic Press; 2018.

13. Batista HR, Sarturi C, Stelmachtchuk FN, Rocha OD, Caroprezo MA, Gennari SA, et al. Prevalence and risk factors associated with ectoparasite infestation of buffaloes in an Amazonian ecosystem. Parasites Vectors 2018;11:335  https://doi.org/10.1186/s13071-018-2917-2.

14. Ojeda-Robertos NF, Peralta-Torres JA, López-Hernández KG, Chay-Canul AJ, Ojeda-Chi MM, Rodríguez-Vivas RI. Pediculosis por Haematopinus tuberculatus en búfalos de agua (Bubalus bubalis). Ecosistemas Recur Agropecuarios 2022;3:e3283.

15. Hornok S, Hofmann-Lehmann R, Fernández de Mera IG, Meli ML, Elek V, Hajtós I, Répási A, et al. Survey on blood-sucking lice (Phthiraptera: Anoplura) of ruminants and pigs with molecular detection of Anaplasma and Rickettsia spp, Vet Parasitol 2010;3–4:355-358, https://doi.org/10.1016/j.vetpar.2010.09.003.

16. Chaudhuri RP, Kumar P. The life history and habits of the buffalo louse, Haematopinus tuberculatus (Burmeister) Lucas. Indian J Vet Sci 1961;31:275-287. 

17. Cardona-Zuluaga EA, Ruiz JD, Berdugo JA, Rojas-Gutierrez S, Gómez-Montoya N.  Niveles de infestación y distribución de Haematopinus tuberculatus en búfalos de agua (Bubalus bubalis) de dos fincas del departamento de Córdoba,      Colombia. 2015.

18. Figueiredo M, Silva D, Manrique W, Guerra R. Infestación y distribución de Haematopinus tuberculatus en Bubalinos De São Luís, Estado Do Maranhão, Brasil. The Biologist 2020;1 https://doi.org/10.24039/rtb2013111437.

19. Neglia G, Veneziano V, De Carlo E, Galiero G, Borriello G, Francillo M, Campanile G, et al. Detection of Brucella abortus DNA and RNA in different stages of development of the sucking louse Haematopinus tuberculatus. BMC Vet Res 2013;9:23. https://doi.org/10.1186/1746-6148-9-236.