https://orcid.org/0009-0006-1476-9031
Figures
Abstract
This study examined the ectoparasites in free-living wild bee colonies in Totoró, Cauca Department, and Valle del Cauca, Colombia. Researchers collected 2116 bee specimens: 620 from Cauca (200 Apis mellifera, 320 Partamona peckolti, and 100 Paratrigona eutaeniata) and 1496 from Valle del Cauca (Dagua, Tocota, Buga, Cali, Pradera), including 1498 A. mellifera and 48 Tetragonisca angustula. Using microscopic and stereoscopic techniques and a special taxonomic key, the study identified the first recorded presence of Leptus (Leptus) alberti n. sp. (Acari: Erythraeidae) in colonies of free-living Africanized A. mellifera and stingless bees, including P. peckolti, P. eutaeniata, and T. angustula in Cauca and Valle del Cauca. This finding updates the reported species for South America. The presence of L. (L.) alberti n. sp. was identified in four sample points in the Totoró-Cauca area, with a 75% parasitic prevalence in free-living bee colonies at three of the four localities, specifically in hives located in the wild forest of Totoró. Two Meliponini species were also identified: one in P. peckolti and another in P. eutaeniata. In Cauca, the prevalence was 5% for A. mellifera and 0.3% for Meliponini. In Valle del Cauca, L. alberti n. sp. was observed in five out of 22 localities, resulting in a 23% prevalence in wild A. mellifera. Additionally, a 4.16% prevalence (2/48) of L. alberti n. sp. was found in T. angustula. Six A. mellifera specimens tested positive for L. (L.) alberti n. sp., as did one P. peckolti and one P. eutaeniata specimen. No other external mites were detected in the collected samples.
Citation: Sanchez-Quilindo BA, Pizo-Barona HL, Benavides Montaño JA (2024) Leptus alberti n. sp. (Trombidiformes: Erythraeidae) parasitizing free-living colonies of Apis mellifera, Partamona peckolti, Paratrigona eutaeniata and Tetragonisca angustula in Totoró and Valle del Cauca, Colombia. PLoS ONE 19(12): e0311409. https://doi.org/10.1371/journal.pone.0311409
Editor: Oriana Rivera-Lozada de Bonilla, Norbert Wiener University, PERU
Received: February 19, 2024; Accepted: September 18, 2024; Published: December 16, 2024
Copyright: © 2024 Sanchez-Quilindo et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All relevant data are within the manuscript.
Funding: This work was supported by the Universidad Nacional de Colombia – Palmira, Valle del Cauca, Colombia. The Office of Research and Extension. Project HERMES Code: 57604, QUIPU: 202010040144. Interdisciplinary Strategic Alliance with the purpose of studying the diversity of mites and parasitic agents associated with Hymenoptera Apidae and formulating strategies for their conservation and sustainability in agricultural and livestock production areas in the Pacific region of Colombia. This project was funded under the National Call for the Promotion of Interdisciplinary Strategic Alliances that integrate the mission processes of the Universidad Nacional de Colombia – Sede Palmira.
Competing interests: The authors have declared that no competing interests exist.
1 Introduction
Both A. mellifera and the Meliponini tribe are permanently exposed to a broad range of parasites and pathogens, including metazoans (nematodes, mites), microbes (viruses, bacteria, protozoans, fungi) and parasitoids [1]. Parasites and pathogens are the major source of stress in free-living and managed bee colonies, causing a series of detrimental effects: physiological damage (pathological lesions), metabolic disruptions, imbalances and impaired physiological functions. They also compromise immunological system, weakening their defense mechanisms and reducing their population [2].
A. mellifera is a honeybee with more than 31 subspecies that was introduced to Latin America in the 17th century, from Africa, Europe, and Western Asia. A. mellifera scutellate, a hybrid, was subsequently introduced in 1978 and 1997 from Venezuela. Today, 13 identified linages of the African bee haplotypes are present in Colombia territory [3–5]. While frequently described as effective pollinators, recent studies have shown that A. mellifera may be less efficient when quantified. Furthermore, the honeybee traditional model displaced native bees and decrease pollination of native wildflowers competing with native floral resources [6,7].
Free-living colonies exist in the wild without direct human involvement. They are essentially self-sufficient, depending on natural resources for sustenance and habitat. In the context of free-living colonies, they can consist of a variety of species, such as wild honeybees and formerly managed honeybees that have become free-living. These categories includes colonies of Africanized A. mellifera (honeybees) and various species of stingless bees.[8]. Since it is challenging to determine whether bees are genuinely wild, descended from colonies that never occupied a beehive, or if they come from free-living colonies that swarmed from a nearby apiary; these bees are denominated as ’free-living’ [8,9].
Colombia is home to over 600 bee species, both in natural and agricultural systems [10]. Include A. mellifera and stingless bees of the Meliponini tribe (Apidae). There are currently 120 documented stingless bee species in country, including 44 in 175 active meliponaries as of 2020 [11]. The Valle del Cauca and Cauca have 71 species, 18 genera; among them, we can find Nannotrigona mellaria [12–14], P. peckolti, and T. angustula [13], which had not been previously reported in this Department. Nevertheless, Paratrigona eutaeniata has been identified in the Departments of Cundinamarca, Boyacá, Santander, but not in Cauca and Valle del Cauca [15].
A. mellifera in Colombia faces threats, such as Varroa destructor, Aethina tumida Murray (Coleoptera: Nitidulidae), Acaropis woodi (1.2% prevalence) and Nosema spp., (5.1% prevalence) [5,16,17] as well as several viruses [18]. There are few studies on free-living colonies of A. mellifera or stingless bees; nonetheless, important advances have been implemented in Brazil through the identification of seven novel eukaryotic viruses in high abundance in unhealthy M. quadrifasciata. [19].
Recently, Leptus spp in a Meliponini tribe in Argentina [20]. Mites of the genus L. alberti n.sp can transmit bacteria, to their host while feeding, which can induce death [21]. Due to the globalization of beekeeping and the importation of genetic material, such as A. mellifera specimens and other bees, mites have appeared in endemic bees, negatively affecting bee biodiversity in Colombia [22]. It is important to be aware that any new mite-bee association, under suitable conditions, can become a threat to these bees [23]. The objective of this study was to determine the presence of parasitic mites in wild bee populations in the municipality of Totoró (Cauca) and other localities of the Valle del Cauca. This can help to evaluate the potential threat that new parasites may pose to the beekeeping community in the region.
2 Materials and methods
2.1 Ethics statement
This does not involve participation of specimens’ tissues, vertebrate animals or embryos. Approval for the study was granted by the Ethical Committee Board of the Faculty of Universidad Nacional de Colombia Palmira, letter number 20689, during a meeting held on April 20, 2023. The study falls under the project titled "Interdisciplinary Strategic Alliance aimed at investigating the diversity of mites and parasitic agents associated with Hymenoptera Apidae and devising strategies for their conservation and sustainability in agricultural and livestock production areas in the Pacific region of Colombia." Community clarification sessions were carried out in Cauca and Valle del Cauca to elucidate the project’s objectives and study protocol. Prior to sample collection, consent was obtained from the communities. Additionally, written consent was from the owners before collecting bee samples.
2.2 Description area
Totoró is a region in Colombia characterized by significant biological and cultural diversity, with temperatures ranging from 0°C to 22°C and a broad range of altitudinal zones, from 2200 to 3800 meters above sea level (Fig 1). Indigenous communities include the Nasas, Polindaras, and Tontotuna [24]. The local inhabitants are primarily engaged in agricultural activities, which involve the utilization of trees for various purposes such as timber, ornamental use, water protection, fruit cultivation, and erosion control. Furthermore, their livelihoods revolve around managing their own seeds in gardens, species selection, planting, exchange, and sale. Additionally, animal husbandry is an integral part of their activities [25]. The Piedra Grande farm, situated in Miraflores village, served as the initial sampling location and spans across 8 hectares, 2 are specifically allocated to the cultivation of Castilla blackberry (Rubus glaucus), tomato (Solanum betaceum), and zucchini (Cucurbita pepo) (Fig 2). Remaining 6 hectares are designated for cattle husbandry and stewardship practices. The wild hive was identified at an approximate distance of 300 meters from the farm entrance, encompassed by a biodiverse array of indigenous plant species (Fig 2). The El Recuerdo farm, situated in the La Palma hamlet, is located at a 45-minute walking distance from the Piedra Grande farm. This agricultural establishment is dedicated to the intensive rearing of Cebuina breed cattle. In addition, the farm features a limited representation of indigenous flora, incorporating specific shrub species and notably showcasing the flourishing of white point grass (Fig 2). During the sampling conducted within Valle del Cauca, positive observations were made regarding the presence of the ectoparasite Leptus spp. The assessments were specifically carried out within apicultural settings, focusing on wild A. mellifera colonies located in Dagua-Tocota, Buga, Pance, Pradera, and the Topacio reserve in Cali. The final sample involved a natural hive hosting Tetragonica angustula.
It illustrates the location of agricultural estates within the municipal boundaries of Totoró, ranging in elevation from 2750 to 2500 m.a.s.l. and distributed across the Departments of Cauca and Valle del Cauca. The mapping was generated using Geographic Information Systems Laboratory (GIS) National University of Colombia Palmira headquarters. (2024) and Created with BioRender.com.
Angucho (Bejaria resinosa) (A); White point grass (Rhynchospora colorata) (B); Achira (Canna indica) (C); Papunga (Bidens pilosa) (D), Tree tomato crops (Solanum betaceum) (E); Floral tree (Meriania nobilis) (F); Zucchini (Cucurbita pepo) (G); purple matico (Aristeguietia lamiifolia) (H); and Mora castilla (Rubus glaucus) (I). Created with BioRender.com.
2.3 Sampling points
The field study focused on six diverse areas within the Departments of Cauca and Valle del Cauca. In the Cauca Department, mites (Trombidiformes: Erythraeidae) were found in the Municipality of Totoró (Lat: 2°30′37″N, Long: 76°24′07″W, Alt: 2750, 14°C, Biological Register ID: H.01.), two sampling point in Miraflores village (Lat: N 2°33′25″, Long: 76°25′21″ W, Alt: 2700 m.a.s.l., 19°C); one sampling in La Palma-Totoró (Lat: 3°32′34″ N, Long: 76°26′26″W, alt: 2481 m.a.s.l., 14°C, ID:H.04); and the last one in Bella Vista-Totoró (Lat: 2°34’36.6" N, longitude: 76°27’20.4" W, Alt: 2500 m.a.s.l., 14°C, ID:H.25). Fig 1 illustrates the sampling locations: in the Valle del Cauca Department, in Dagua-Tocota (Lat: 3°30’28" N, Long: 76°38’55" W, Alt:1520 m.a.s.l. 17°C, ID: H.02.); the Agroecological farm “El Porvenir-Buga” (Lat: 3°50’55.0"N, Long: 76°12’46.0"W, Alt: 2481 m.a.s.l., 19°C ID: H.014.); Natural forest reserve, Topacio. Cali, located at (Lat: 3°19’03.6"N, Long: 76°38’15.2"W, Alt: 2481 m.a.s.l., 14°C ID: H.017.); High Mountain of Pueblito Pance (El Trueno). (Lat: 3°19’03.6"N, Long: -76°38’15.2"W, Alt: 2481 m.a.s.l., 18°C ID: H.018); Villa El Mesón. Pradera (Lat: 3°29’55.9"N, Long: 76°11’23.3"W, Alt: 1869 m.a.s.l., 20°C ID: H.019).
2.4 Study and sample size
The study was conducted from February 2023 to February 2024. In order to calculate the sample size, we used the formula n = E2Z2⋅p⋅(1−p)/E2, where n = sample size Z = Z-score corresponds to the desired confidence level (for 95% confidence, Z ≈ 1.96), p = estimated proportion of the Meliponini species population that is unknown in the area of interest. We used 0.5% for maximum variability with margin of error E. . This study adopted an observational approach, closely examining exposure to parasites within each sample. A representative sample from each location underwent scrutiny at a specific moment and place [26]. We collected a total of 2116 individuals from 25 located points to get enough specimens for analysis. The data was analyzed measuring the prevalence of the disease, and it was calculated (No. of specimens parasitized/Total no. of specimens examined) x 100.
To detect ectoparasites, including Leptus spp, Varroa spp, A. woodi, among other mites, a comprehensive analysis was conducted in the Departments of Cauca and Valle del Cauca. In the first region, a total of 620 individuals from wild hives were processed: 200 A. mellifera and 420 stingless bees. Specifically, 115 P. peckolti were examined in Miraflores-Totoró, 205 in La Palma-Totoró, and 100 P. eutaeniatain in Bellavista-Totoró (Fig 3). In the second Department, the investigation entailed the examination of a total of 1496 individuals derived from both apiaries and wild hives. This cohort comprised 1448 A. mellifera, with the following spatial distribution: 830 specimens in Dagua-Tocota, 366 in the agroecological farm “El Porvenir” located in Buga municipality, 91 samples collected in the High Mountain of Pueblito Pance (El Trueno), and 161 free-living colonies of A. mellifera in Villa El Mesón, Pradera. Additionally, 48 individuals of wild T. angustula underwent scrutiny in Reserva Topacio (Fig 3).
Habitats of wild bees (Apini) in Miraflores–Totoró. (A); Positioning of P. peckolti Meliponini wild bees on a beach milk tree, P. (Euphorbia laurifolia]) (B); Nest of wild bee specimens (Meliponini) in La Palma (Finca El Recuerdo) (C); Nest of P. peckolti wild bees (Meliponini) in Miraflores–Totoró, (D); Location of a wild hive on a peach tree, Prunus persica, P. peckolti (E); Nest of wild bee specimens P. eutaeniata (Meliponini) in Miraflores, Bellavista village, (F), P. eutaeniata over Persicaria nepalensis (G), Mantico morado, Ipomea purpurea (I), Rubus glaucus (H). Created with BioRender.com.
2.5 Mounting, microscopy, and image analysis
The bees were captured using a wide-mouthed jar containing 70% alcohol. Parasitic larvae of the Trombidiformes: Erythraeidae family were collected from A. mellifera, P. peckolti, P. eutaeniata and T. angustula in Totoró, Cauca, and Valle del Cauca, Pacific of Colombia. The collection was deposited in CEUNP-70 at the Universidad Nacional de Colombia, Palmira campus. The alcohol fixed specimens were slide-mounted in Hoyer’s medium. They were observed using a Leica S8APO stereoscope and both ZEISS PrimoVert and Primo Star AxioCam ICc microscopes. The mites were examined using two microscopy techniques: Phase-contrast microscopy (PCM) and Light microscopy (LM). Taxonomic keys were used for precise and rigorous identification [27–32]. Minimum and maximum values of the morphometric measurements were registered during captures of individuals for which photogrammetric data existed. 11 specimens were studied: H01.P01.I017-SL1, H01.P01.I81-SL1, H01.P01.I093-SL1, H01.P01.I116-SL1, H01,P01.I189-SL1, H01,P01.I189-SL2, H04.P02.I178-SL1, H04.P02.I178-SL2(r), H25.P01.I018-SL1, H18.P02.I036-SL1, and H19.P02.I015-SL1. All measurements are given in micrometers, with the range followed by the mean. The terminology and measurements generally follow Southcott (1992) [27], Haitlinger (2016) [30], Saboori, (2020) [31], and Haitlinger (1991) [32]. This evaluation was carried out in the Parasitology, Immunology, and Infectious Diseases Laboratory (PARINEI), located at the Lab Farm Mario González Aranda, Experimental Center of the Universidad Nacional de Colombia, Palmira Campus, Valle del Cauca.
2.6 Statistical analysis
The statistical analysis was conducted using GraphPad Prism 10 software. Comparisons of samples collected in Cauca and Valle del Cauca for Leptus alberti n. sp. were performed using a one-way analysis of variance (ANOVA), followed by Bonferroni’s multiple comparison post hoc test.
3 Results
We identified the presence of L. (L) alberti n. spp. in four sample points in the area of Totoró-Cauca, within the Department of Cauca (Table 1, see also S1 Fig). In 3 of the 4 localities, parasitic prevalence was 75% in free-living colonies of bee hives. Specifically, three hives located in the wild forest within the municipality of Totoró. We also identified two Meliponini species: one in P. peckolti (Fig 4) and another in P. eutaeniata (Fig 5). The total population, as previously described, included 200 A. mellifera, 320 P. peckolti, and 100 P. eutaeniata.
Infestation by Leptus (L) alberti.n. spp, characterized by a black tegument with brown coloring. The hind legs femur displays a mite attached to the trochanter (A). P. peckolti features a malar mouth with a small lateral tooth and spoon-shapedarea (B), spoon-shaped corbiculae (C), scutellum without a medial notch (D), and a propodeum larger, measuring 1–1.5 times the scutellum’s length; notable hairs present on both ventral and dorsal thoracic areas (E). The wings exhibit a reddish membrane with a pentagon (3-4-5-6-7) (F), with overall dimensions ranging between 5.5 and 6.3 mm [15]. Created with BioRender.com.
Mite attached to the lateral thorax (A); malar with four denticles (B); tibia in a triangular shape (C); ocellus and exposed alveolar areas; yellow clypei and two yellow stains in the shape of an inverse comma, at the lateral orbicular margin from medium ocellus (D); lack of medial notch (E); hexagon-shaped wings (F) [15]. Created with BioRender.com.
We employed taxonomic keys in the Neotropical regions [27,30–32].
In Cauca, a prevalence of 5% was noted for A. mellifera and 0.3% for Meliponini. In Valle del Cauca, L. alberti n. spp. was observed in five out of 22 localities, resulting in a prevalence of 23% in wild A. mellifera (H.02, H14,H18,H19). Notably, a prevalence of 4.16% (2/48) of L. alberti n. spp. was identified in T. angustula (codes H.17.P01.I009H, H17.P02.I010). Six A. mellifera specimens from the collected material tested positive for Leptus (L) alberti n.sp spp., (SL) (codes H01.P01.I017, H01.P01.I044, H01.P01.I081, H01.P01.I093, H01.P01.I116, H01.P01.I189). Additionally, one P. peckolti specimen was identified as positive (code H.04.P02.I178), as well as a P. eutaeniata (code H.25.P01.I018). Varroa, Euvarroa, and other external mites were not observed in the collected samples.
The specimens utilized for the classification of Leptus spp. were obtained from free-living colonies of A. mellifera in Totoró, Cauca (H01.P01.I017-SL1, H01.P01.I81-SL1, H01.P01.I093-SL1, H01.P01.I116-SL1, H01,P01.I189-SL1; H01,P01.I189-SL2); from P. peckolti (H04.P02.I178-SL1; H04.P02.I178-SL2.r); from P. eutaeniata (H25.P01.I018-SL1); from feral wild bees in “El Meson” (Palmira, Valle del Cauca) (H19.P02.I015-SL1); and from the high mountain of Pueblito Pance “El Trueno”, Valle del Cauca (H18.P02.I036-SL1), Tables 1 and 2, (Fig 6). No significant difference among populations of L. (L) alberti n. spp in Cauca and Valle del Cauca (S1 Fig). Varroa, Euvarroa, and other external mites were not detected in the collected samples. The mites were systematically identified and cataloged with corresponding codes, as presented in Tables 1 and 2, and (Fig 6).
Specimens were collected from free-living colonies of A. mellifera (H.01.P01.I189), P. peckolti (H.04.P02.I178) and P. eutaeniata (H.25.P01.I018). The collected material underwent microscopic examination at 20X, 40X, and 100X magnifications: (H.01.P01.I189-SL, H.01.P01.I189-SL2, H.04.P02.I178-SL1, H.25.P01.I018-SL1). Scutum without such setae (subgenus Leptus), Setae PL on scutum (A); wide shield without cuticular lines, moderately chitinized, with slight porosity but without striae (stippling), equilateral triangle shape (A); Palp genu with one or two setae, palp femur with only one Se (B), Palp genu with one seta (B), Between coxae I and II two sternale, between coxae II-III not more than four setae (C), AL shorter than PL, ciliate (5D), Genu III without solenidia (E), Genu I with one solenidion (F), Tibia III with one solenidion (G), Dorsum of the idiosome with about 48 ciliated setae (H), Genu II without solenidia (I), Ti III < 400 (J), Ti III< 190 (J), AW > 66 (K), AW > 88 (K), Circular eyes, 16.47 μm wide, on small oval or pyriform ocular sclerites (K), Tibia I with two specialized setae (L), Striated tarsus I (M), (N), (Ñ), naked hypostomala, with two hypostomal setae (O), PW 120, Ti I 122, anterior border of scutum almost straight (A). Created with BioRender.com.
4 Discussion
Over 240 species belonging to the genus Leptus Latreille, 1796 have been documented in their larval stage, inhabiting various species; However, the larvae predominantly infest arthropods, with a preference for Araneae, Coleoptera, Diptera, Hemiptera, Lepidoptera, Opiliones, and Orthoptera [33]. The majority of the reports rely on descriptions of the larvae [34], and just four species are described by the NCBI: Leptus ignotus, Leptus tridentatus, Leptus oudemansi and Leptus sidorchukae [35]. More than 54 species of Leptus have been described in the America continent (North, Central and South), at least 32 species for South America [28,30,32,36,37] (Table 3). Here, we report the first record in Colombia of a mite species closely related to L. alberti n.spp., which is part of the Trombidiformes order, Prostigmata suborder, anystina infraorder. For the Leptus (L), there are two previous additional reports in Colombia. The first report of Leptus olafi in Colombia, Panamá and Venezuela was in 1991 [32]; in addition to Leptus stefani in Colombia [32,38].
The presence of Leptus in wild A. mellifera and P. peckolti, P. eutaeniata and T. angustula is relevant considering that this mite may be detected in the gut and muscle-tissue of Leptus (Leptus sayi, 15,4% prevalence; Leptus lomani, 14.3% prevalence) [21]. Future studies are required to identify whether L. alberti is infected with spiroplasmas and the effect or role on host interaction (female and males) in other populations.
Although there have been previous reports of L. olafi and L. stefani in Colombia, this is the first documentation of a new species L. alberti n.sp parasitizing bees in Colombia. In parallel, Leptus spp., has been observed parasitizing stingless bees (Apidae:Meliponini) in Argentina [20]. A. mellifera Africanized honey bees have also been detected with Leptus spp in 26 (87%) of 30 study colonies. [23]. Flechtman et al. (1980) [56] reported in Lima, Peru, fourteen Leptus sp. larvae that were collected from honeybees, A. mellifera L. These larvae were attached to the intersegmental membranes of abdominal tergites and sternites. This is an old association that comes from the Eocene, as tests from ambar fossils suggest [54–56].
Different factors potentially influence the association between L. alberti and P. peckolti, including the nesting habitat, characterized by locations in holes within walls or proximity to termite colonies. These habitats are typically situated in tropical forests and anthropogenic areas along the Pacific coast and Andean valleys, spanning elevations between 10 and 2,850 meters above sea level [13]. The nesting preferences of P. peckolti possibly expose them to a higher risk of encountering these parasites, which could contribute to the observed findings.
The identification of Leptus spp. in free-living colonies of A. mellifera, P. peckolti, P. eutaeniata, and T. angustula in the wild is likely attributed to the limited human intervention in these ecosystems, facilitating the discernment of these bee populations. The absence of Leptus spp. in regions where A. mellifera is actively managed by beekeepers implies a discernible pattern. Investigations are imperative to elucidate the specific role of Leptus spp. as potential vectors of diseases in free-living colonies, thereby contributing to a more nuanced understanding of the dynamics governing these interactions.
Comparative morphology remains a constant approach to species identification [57–59]; However, Leptus species in South America need to be redescribed since the currently available information is insufficient. New drawings and meristic data are also needed.
There is a low number of examined specimens and a high dependence on metric data to separate species. In the case of L. alberti, there are metric data of limited value. This classification uses mostly non-metric characters of published descriptions for differentiation of L. alberti from other possible species. Cryptic species are phylogenetically closely related that exhibit no unambiguous morphological differences. In order to readily allow their distinction, an integrative taxonomic approach with additional evidence (Behaviour, physiology, ecology) is required, in addition to DNA barcoding methods that help to understand these findings.
5 Conclusions
This study represents the primary complete morphometric documentation of a mite L. alberti n. spp. in free-living colonies of A. mellifera, as well as in other free-living species such as P. peckolti, P. eutaeniata, and T. angustula within the Cauca and Valle del Cauca Departments. This discovery contributes novel insights to the existing understanding of Leptus species in South America, thereby enriching the catalog of documented species in the region. Furthermore, the study underscores the imperative for future investigations aimed at ascertaining whether L. alberti is infected with Spiroplasmas and delving into the potential effects or roles in host interactions. Given the dynamic nature of arthropod associations, it is crucial to explore and elucidate the multifaceted roles and impacts of these interactions in diverse ecosystems. Future studies require an integrative taxonomic approach with additional evidence.
Supporting information
S1 Fig. Leptus alberti n. sp. Comparison Cauca and Valle populations.
https://doi.org/10.1371/journal.pone.0311409.s001
(PDF)
Acknowledgments
We would like to thank the inhabitants of Totoró–Cauca and Valle del Cauca for helping us collect the specimens used in this study. Special acknowledgement to Alexander Sanchez Mosquera and Carlos E. Agudelo M who let us collect some samples. We are also grateful to all the Team of Parasitology immunology and Infectious Disease Group. We express our sincere gratitude to Professor Nora Cristina Mesa Cobo for academic support. Thank you so much to all the PLOS ONE reviewers that help to improve the quality of this manuscript. Daniel Fernando Vasco for writing assistance, and to Alfredo Rivera Peralta for teaching assistance in sample preparation for archiving in the collection at the entomology museum CEUNP70 of the Palmira campus. We also thank the academic peers for critical suggestions to improve the quality of the manuscript.
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