61 Zoonotic infections in soil of recreational areas Neotropical Helminthology, Vol. 18, Nº1, jan - jun 2024 Neotropical Helminthology Neotropical Helminthology, 2024, vol. 18 (1), 61-77 ORIGINAL ARTICLE / ARTÍCULO ORIGINAL DIVERSITY OF METAZOAN ENDOPARASITES ASSOCIATED WITH LIZARDS (SQUAMATA, LACERTILIA) IN THREE PROTECTED AREAS AND THEIR SURROUNDING ZONES IN NORTHEASTERN BRAZILDIVERSIDAD DE ENDOPARÁSITOS METAZOARIOS ASOCIADOS A LAGARTIJAS (SQUAMATA, LACERTILIA) EN TRES UNIDADES DE CONSERVACIÓN Y ÁREAS ALEDAÑAS EN EL NORDESTE DE BRASIL Elvis Franklin Fernandes de Carvalho 1* , Ana Carolina Brasileiro 1 & Robson Waldemar Ávila 1 ISSN Versión Impresa 2218-6425 ISSN Versión Electrónica 1995-1403 DOI: https://dx.doi.org/10.62429/rnh20241811740 Este artículo es publicado por la revista Neotropical Helminthology de la Facultad de Ciencias Naturales y Matemática, Universidad Nacional Federico Villarreal, Lima, Perú auspiciado por la Asociación Peruana de Helmintología e Invertebrados Af nes (APHIA). Este es un artículo de acceso abierto, distribuido bajo los términos de la licencia Creative Commons Atribución 4.0 Internacional (CC BY 4.0) [https:// creativecommons.org/licenses/by/4.0/deed.es] que permite el uso, distribución y reproducción en cualquier medio, siempre que la obra original sea debidamente citada de su fuente original. ABSTRACT T e Neotropical region har bors a rich reptile biodiversity, especially lizards. However, research on parasite richness in Brazilian lizards still has many gaps. Parasites play a crucial role in ecosystems, and accurate studies are necessary to describe their richness and species composition. Habitat fragmentation caused by human activities threatens biodiversity, including parasites. In this context, protected areas play a fundamental role in biodiversity conservation. We aim to describe the diversity of metazoan endoparasites (helminths and pentastomids) in lizards within three protected areas in Northeast Brazil: Aiuaba Ecological Station (Caatinga), Sete Cidades National Park (Cerrado), and Ubajara National Park (Highland marsh and Caatinga), including surrounding areas. We collected 690 lizards representing 23 species. We recorded 34 parasite taxa, including nematodes (28), trematodes (2), cestodes (2), acanthocephalans (1), and pentastomids (1). Among them, we recorded parasites commonly associated with lizards, such as Strongyluris oscari , and rare parasites, such as Brevimulticaecum sp. and Typhlonema sp. We also observed the presence of trematodes exclusively in highland marsh areas. T is study contributes to understanding lizard parasitism in the Neotropical region, presenting 21 new infection records. Additionally, it suggests that trematodes may be related to environmental humidity, emphasizing the importance of faunal surveys for parasite diversity. Keywords : faunal survey – Helminths – Pentastomida 1 Programa de Pós-Graduação em Ecologia e Recursos Naturais, Departamento de Biologia, Campus do Pici, Universidade Federal do Ceará, Fortaleza - CE, CEP 60440-900, Brasil.* Corresponding author: elvis_f c@hotmail.comElvis Franklin Fernandes de Carvalho: https://orcid.org/0000-0002-6604-6154Ana Carolina Brasileiro: https://orcid.org/0000-0002-5929-941XRobson Waldemar Ávila: https://orcid.org/0000-0003-3641-8321
62 Fernandes de Carvalho et al. Neotropical Helminthology, Vol. 18, Nº1, jan - jun 2024 RESUMEN La región Neotropical alberga una rica biodiversidad de reptiles, especialmente lagartijas. Sin embargo, la investigación sobre la riqueza de parásitos en lagartijas brasileñas todavía tiene muchas lagunas. Los parásitos desempeñan un papel crucial en los ecosistemas, y son necesarios estudios precisos para describir su riqueza y composición de especies. La fragmentación del hábitat causada por actividades humanas amenaza la biodiversidad, incluidos los parásitos. En este contexto, las áreas protegidas desempeñan un papel fundamental en la conservación de la biodiversidad. Nuestro objetivo es describir la diversidad de endoparásitos metazoarios (helmintos y pentastomátidos) en lagartijas dentro de tres áreas protegidas en el noreste de Brasil: la Estación Ecológica de Aiuaba (Caatinga), el Parque Nacional de Sete Cidades (Cerrado) y el Parque Nacional de Ubajara (Brejo de altitud y Caatinga), incluidas las áreas circundantes. Recolectamos 690 lagartijas representando 23 especies. Registramos 34 taxones de parásitos, incluyendo nematodos (28), trematodos (2), cestodos (2), acantocéfalos (1) y pentastomátidos (1). Entre ellos, registramos parásitos comúnmente asociados con lagartijas, como Strongyluris oscari , y parásitos raros, como Brevimulticaecum sp. y Typhlonema sp. También observamos la presencia de trematodos exclusivamente en áreas de brejo de altitud. Este estudio contribuye a comprender el parasitismo en lagartijas en la región Neotropical, presentando 21 nuevos registros de infección. Además, sugiere que los trematodos pueden estar relacionados con la humedad ambiental, enfatizando la importancia de los estudios faunísticos para la diversidad de parásitos. Palabras clave : Helmintos– levantamiento faunístico – Pentastomida INTRODUCTION Te Neotropical region is one of the most biodiverse on the planet, with Brazil being a biodiversity hotspot whiting ecosystems supporting a vast array of plant and animal species, many of which are endemic (Myers et al. , 2000; Zachos & Habel, 2011; Antonelli, 2022). It harbors the third-largest richness of reptile species globally, and the Northeast region is the second richest in the country, hosting 413 species and subspecies, including 137 lizard species (Squamata, Lacertilia) (Guedes et al ., 2023). However, only 56 lizard species in the region (approximately 40%) have been investigated in parasitological studies (Lacerda et al. , 2023).Considering that parasites are important components of ecosystems and exhibit great diversity (Poulin & Morand, 2000), taxonomic studies, geographic distribution analyses, and host interaction investigations are crucial (Poulin & Mouillot, 2003; Bozick & Real, 2015). To better explore this diversity, accurate identifcations are essential to avoid underestimating parasite richness (Poulin, 2019). Tus, with the application of modern microscopy techniques, faunal surveys contribute to redescriptions and the discovery of new species (Macedo et al. , 2023). However, there is an estimated 75,000 to 300,000 species of helminths parasitizing vertebrates, and up to 33% of these may be at risk of extinction (Dobson et al. , 2008; Carlson et al. , 2017).Among the primary threats to biodiversity are human activities, with habitat fragmentation caused by agricultural practices afecting organisms from microorganisms to large vertebrates (Ellis et al. , 2010; Christian, 2023). Tis fragmentation can lead to both immediate species loss and subsequent extinctions, impacting species distribution patterns and community composition due to environmental changes (Krauss et al. , 2010). For parasitic helminths, these disturbances can infuence the structure and composition of communities, with factors such as abundance, prevalence, and intensity susceptible to interference (Cardoso et al. , 2016; Carlson et al. , 2017; Portela et al ., 2020).In this context, protected areas play a crucial role in species preservation, serving as biodiversity refuges (Llorente-Culebras et al. , 2021; Li et al. , 2022). Tese areas can act as repositories of taxonomic, genetic, and functional diversity for the surrounding areas. Terefore, investigating the biodiversity associated with conservation areas and their surroundings can provide valuable insights into local biodiversity. In Brazil, fully protected areas are a primary means of biodiversity conservation, including national parks, ecological stations, natural monuments, and wildlife refuges. In the Northeastern region, there are 26 fully protected areas covering diferent types of native vegetation, such as Caatinga, Cerrado, and Highland marshes.
63 Metazoan Endoparasite Diversity in Lizards in Northeastern Brazil Neotropical Helminthology, Vol. 18, Nº1, jan - jun 2024 Considering this, studies conducted in protected areas and their surroundings, encompassing faunal surveys, including parasitological assessments, are valuable, as they can unveil rich biodiversity. Tese studies are also signifcant for reinforcing the importance of protected areas in safeguarding native species and their ecological relationships. Te objective of this study was to describe the richness of metazoan endoparasite species (helminths and Pentastomida) associated with lizards in three protected areas and their surrounding zones in Brazilian northeast. MATERIAL AND METHODS Study areas Field sampling comprised three protected areas (PAs) in northeastern Brazil and their surroundings (Fig. 1). Te Aiuaba Ecological Station (AES), covering an area of 11,746.60 ha, is situated in the southern part of the state of Ceará in the municipality of Aiuaba (6°36’ to 6°44’ S - 40°07’ to 40°19’ W). Tis area features a hot-semiarid tropical climate, an average annual rainfall of 568.4 mm, and an average temperature ranging from 24 to 26°C. Te predominant vegetation in the ecological station is caatinga stricto sensu, with its interior well-preserved, encompassing 81% of its total area covered by conserved vegetation (Araújo et al. , 2017).Te Sete Cidades National Park (SCNP, 4°06’58.8”S 41°43’41.8”W), located in the state of Piauí, between the municipalities of Piracuruca and Brasileira, in a Cerrado stricto sensu area, covers approximately 6,221 ha. It experiences a tropical semi humid dry climate, with an average annual precipitation ranging from 1,300 mm to 1,500 mm and an annual average temperature of 28.8°C, with minimums of 23.2°C and maximums of 36.0°C according National Institute of Meteorology (Castro & Costa, 2007; INMET, 2024). Ubajara National Park (UNP, 3°50’31.2”S 40°54’00.5”W), also in the state of Ceará, is in an area that encompasses zones of caatinga stricto sensu and relictual moist forest Figure 1. Schematic map illustrating protected areas with highlighted sample points in yellow. Legend: SCNP: Sete Cidades National Park, UNP: Ubajara National Park, and AES: Aiuaba Ecological Station.zones, also known as highland marsh. Te park covers 6,288 ha and is situated in the northwest portion of the state of Ceará in the Ibiapaba Plateau, spanning three
64 Fernandes de Carvalho et al. Neotropical Helminthology, Vol. 18, Nº1, jan - jun 2024 municipalities: Frecheirinha, Tianguá, and Ubajara. Te annual rainfall reaches 1,483.5 mm, with average temperatures ranging between 24 and 26°C. Sample design and host collection Lizard sampling were conducted from 2018 to 2020, covering both dry and rainy seasons, except in 2020 when collections were exclusively performed during the rainy period. During the expeditions, visual encounter surveys were carried out, exploring all possible microhabitats used by lizards (Bernarde, 2012). Hosts were manually collected during daytime from 8:00 to 17:00. Te total sample efort in hours amounted to 1,110 h, calculated by summing the number of hours in the feld multiplied by the number of researchers conducting searches on each expedition. Te distribution of sampling points followed the methodology of Brasileiro et al. (2023). Te lizards were euthanized following the ethical procedures of the Federal Council of Veterinary Medicine – CFMV (2013) with lidocaine hydrochloride 60 mg/kg, preserved in 70% ethanol, and subsequently cataloged in the Herpetological Collection of the Federal University of Ceará. Collection and Processing of Parasites After necropsy with a longitudinal anteroposterior ventral incision, the hosts had their coelomic cavity, lungs, stomach, intestines, and accessory organs of the digestive system examined for parasites. When hosts were necropsied fresh and parasites were found, they were fxed in boiling 70% ethanol and preserved in the same solution for subsequent analyses. Due to the number of collected hosts, some could not be necropsied immediately after collection and were fxed as described earlier. In these cases, necropsies were subsequently conducted, and the parasites were stored in 70% ethanol.Te nematodes, acanthocephalans, and Pentastomida collected were clarifed using a lactic acid solution (Andrade, 2000). Platyhelminths were colored using the carmine technique (Amato & Amato, 2010), diaphanized with eugenol oil, and mounted on temporary slides for taxonomic identifcation. Identifcation was based on the observation, counting, and morphometry of taxonomic characters according to relevant literature (Araújo & Gandra, 1941; Lucker, 1943; Rêgo & Ibáñez, 1965; Rego, 1983; Vicente et al. , 1993; Almeida et al ., 2008; Anderson et al. , 2009; Bursey et al. , 2010; Fernades & Kohn, 2014; Pereira et al. , 2017; Vieira et al. , 2020; De Sousa et al. , 2022). Parasitological descriptors of mean abundance, infection range, and infection intensity followed by standard error, and prevalence in percentage was calculated according to Bush et al. (1997). After identifcation, all parasites were deposited in the Parasitological Collection of the Federal University of Ceará Ethics aspects: All procedures used in this work follow the ethical standards of the relevant national and institutional guides on the care and use of laboratory animals. Collection permit Instituto Chico Mendes de Conservação da Biodiversidade - ICMBio (process n° 68 031–1 and n° 72 762) and the Ethics Committee on Animal Use of the Federal University of Ceará (CEUA-UFC) (#CEUA 6314010321). RESULTS A total of 690 hosts were collected, distributed across 23 lizard species, with 237 at Aiuaba Ecological Station (AES, 10 spp.), 239 at Sete Cidades National P\ark (SCNP, 14 spp.), and 214 at Ubajara National Park (UNP, 18 spp.). Among these, parasitic infections were documented in 20 species, except for Copeoglossum nigropunctatum Spix, 1825, Colobosaura modesta Reinhardt and Lütken, 1862, and Vanzosaura multiscutata Amaral, 1933. Regarding hosts, the largest sample size was for Ameivula pyrrhogularis Silva and Avila-Pires, 2013 (AES: 67, SCNP: 60, and UNP: 36), and Tropidurus hispidus Spix, 1825 (AES: 67, SCNP: 49, and UNP: 66), which are also the species with the highest recorded parasitic richness (Table 1).Te total abundance of parasite individuals was 21,289.00. Specifc-level identifcation was not possible in some cases due to the difculty in visualizing important morphological characters or due to the ontogenetic developmental stage. In these cases, a more conservative approach was adopted, and a higher taxonomic level was recorded. Terefore, the richness of recorded parasite taxa in this study was 34 taxonomic groups (24 at the specifc level, seven at the genus level, two at the family level, and one at the phylum level), with 11 for AES, 24 for SCNP, and 25 for UNP (Table 1).From the records made in this study, 21 are new infection records for the host species. Sete Cidades National Park (SCNP) had the highest number of new records (13), followed by Ubajara National Park (UNP) with seven and Aiuaba Ecological Station (AES) with one (Table 1). For Ameivula pyrrhogularis, six new records were documented, fve in SCNP ( Brevimulticaecum sp., Capillaria freitaslenti Araujo & Gandra, 1941, Cruzia lauroi Vieira et al ., 2020, Falcaustra sp., Spinicauda
65 Metazoan Endoparasite Diversity in Lizards in Northeastern Brazil Neotropical Helminthology, Vol. 18, Nº1, jan - jun 2024 spinicauda Olfers, 1819 and one in UNP ( Pharyngodon travassosi Pereira, 1935), making it the host species with the highest number of new records. In the UNP, a single individual of Typhlonema sp. infecting Norops fuscoauratus d’Orbigny, 1837, was recorded. Tis was also the only area where the trematodes Mesocoelium monas Rudolphi, 1819, and Paradistomum parvissimum Travassos, 1918, were registered, occurring only at collection points within the protected area and infecting Coleodactylus meridionalis Boulenger, 1888, Norops fuscoauratus , Enyalius bibronii , Tropidurus hispidus , and Tropidurus semitaeniatus Spix, 1825. Host specie s NParasite taxonAMA ± SEAPP%MII ±SELife cycleAiuaba Ecological Station Ameivula pyrrhogularis Silva & Avila-Pires, 201367 Acanthocephala Unidentifed Cystacanth2–21.49–M Cestoda Oochoristica travassosi Rêgo & Ibáñez, 19651–11.59–H Nematoda Pharyngodon cesarpintoi Pereira, 193569310.34±3.65 1–16538.8026.65±8.55M Strongyluris oscari Travassos, 192321–1–202.99–M Gymnodactylus geckoides Spix, 182515 Nematoda Parapharyngodon largitor Alho & Rodrigues, 1963231.53±0.491–553.332.87±0.58M Hemidactylus agrius Vanzolini, 19781Not parasitized Hemidactylus brasilianus Amaral, 193517 Nematoda Parapharyngodon alvarengai Freitas, 19571–10.06–M Skrjabinellazia galliardi Chabaud, 1973*1–10.06–H Spauligodon oxkutzcabiensis Chitwood, 193894–22–7211.76–M Lygodactylus klugei Smith, Martin & Swain, 19778 Nematoda Spauligodon oxkutzcabiensis 1–116,77–M Table 1. Helminths and Pentastomida associated with lizards (Squamata, Lacertilia) in Aiuaba Ecological Station, Sete Cidades National Park, Ubajara National Park and their surroundings, including the number of examined hosts (N) and parasite taxa, along with total abundance (A), mean abundance (MA) ± standard error (SE), infection range (IR), prevalence in percentage (P%), mean infection intensity (MII) ± standard error (SE), and the life cycle of the parasite, whether monoxenous (M) or heteroxenous (H). New parasitism records are indicated with “*”. (Continued Table 1)
66 Fernandes de Carvalho et al. Neotropical Helminthology, Vol. 18, Nº1, jan - jun 2024 Phyllopezus pollicaris Spix, 182513 Nematoda Pharyngodon cesarpintoi 24–247,69–M Spauligodon oxkutzcabiensis 25919.92±7.475–9669.2328.78±9.44M Tropidurus hispidus Spix, 182574 Acanthocephala Unidentifed cystacanth3–31.35–H Cestoda Oochoristica travassosi 30.04±0.0214.051±0H Nematoda Ascarididae1–11.35–MCosmocercidae1–11.35–M Parapharyngodon largitor 971.31±0.311–1537.843.46±0.62M Pharyngodon cesarpintoi 9–1–82.70–M P hysaloptera lutzi Cristofaro, Guimarães & Rodrigues, 1976 2072.78±0.511–1656.764.92±0.75H Skrjabinellazia galliardi 3–31.35 –H Strongyluris oscari 550.74±0.301–1516.214.48±1.48M Tropidurus jaguaribanus Passos, Lima & Borges-Nojosa, 201115 Acanthocephala Unidentifed cystacanth1–16.67–H Nematoda Parapharyngodon largitor 382.53±1.625–232012.67±5.36M Physaloptera lutzi 352.33±1.911–2933.337±5.50H Strongyluris oscari 785.2±2.302–294013±4.10M Vanzosaura multiscutata Amaral, 19334Not parasitized Sete Cidades National ParkHost speciesNParasite taxonAAM ± EPAPP%IM±EPLife cycle Ameiva ameiva Linnaeus, 17585 Nematoda Capillaria freitaslenti Araujo & Gandra, 194118–1820–M Spinicauda spinicauda Olfers, 1819*3–320–M Parapharyngodon sceleratus Travassos, 1923 * 1–120–M Ameivula pyrrhogularis 60 Acanthocephala Unidentifed cystacanth280.46±0.291–168.205.6±2.91H (Continued Table 1)(Continued Table 1)
67 Metazoan Endoparasite Diversity in Lizards in Northeastern Brazil Neotropical Helminthology, Vol. 18, Nº1, jan - jun 2024 Cestoda Oochoristica vanzolinni Rêgo & Rodrigues, 19657–71.64 –H Nematoda Brevimulticaecum sp .* 1–11.64–H Capillaria freitaslenti* 360.59±0.341–188.197.2–3.22M Cruzia lauroi Vieira et al . 2020 5–51.64–H Falcaustra sp .* 5–51.64–H Pharyngodon travassosi Pereira, 1935 * 3115.09±2.641–13211.4744.43–17.77M Piratuba sp . 4–1–33.28– Spinicauda spinicauda* 3–31.64–M Brasilisincus heathi Schmidt & Inger, 19517 Nematoda Oswaldocruzia sp . 2–214.28–M Parapharyngodon sceleratus * 1–114.28–M Strongyloides sp. * 10–1014.28–M Strongyluris oscari *1–114.28–M Colobosaura modesta Reinhardt & Lütken, 18621Not parasitized Hemidactylus agrius 43 Acanthocephala Unidentifed cystacanth30.07±0.0416.981±0H Nematoda Parapharyngodon largitor 160.37±0.161–513.952.67±0.56M Physaloptera lutzi 1–12.33–H Strongyluris oscari *1–12.33 –M Pentastomida Raillietiela mottae Almeida & Lopes, 20081–12.33 –H Hemidactylus mabouia Moreau de Jonnès, 18181 Acanthocephala Unidentifed cystacanth1–1100– Iguana iguana Linnaeus, 17581 Nematoda Alaeuris vogelsangi Lent & Freitas, 194819–19100–M Micrablepharus maximiliani Reinhardt & Lütken, 186214 Acanthocephala Unidentifed cystacanth2–27.14–H Nematoda Physalopteroides venancioi Lent, Freitas & Proença, 1946 * 2–27.14–H (Continued Table 1)(Continued Table 1)
68 Fernandes de Carvalho et al. Neotropical Helminthology, Vol. 18, Nº1, jan - jun 2024 Skrjabinodon campia oae De Sousa, Silva De Oliveira, Morais, Da Silva Pinheiro & Ávila * 60.07±0.07221.422±2M Phyllopezus pollicaris 7 Nematoda Parapharyngodon largitor 71±0.691–542.862.33±0.69M Spauligodon oxkutzcabiensis 446.29±5.172–3742.8614.67±5.17M Polychrus acutiros - tris Spix, 1825 1Not parasitized Tropidurus hispidus 49 Acanthocephala Unidentifed cystacanth2–14.08–H Cestoda Oochoristica travassosi2–22.04–H Nematoda Falcaustra sp . 7–2–54.08–H Parapharyngodon alvarengai 26–7–194.08–M Parapharyngodon largitor 180.37±0.121–318.372±0.24M Parapharyngodon sceleratus 340.70±0.403–1810.206.08±2.85M Physaloptera lutzi 901.84±1.561–5620.419±5.27H Piratuba sp . 5–52.04–H Strongyloides sp . 3–1–24.08–M Strongyluris oscari 701.42±0.441–1330.614.67±1.05M Tropidurus semitaeniatus Spix, 182548 Acanthocephala Unidentifed cystacanth5–1–44.17–H Nematoda Capillaria freitaslenti* 7–3–44.17–M Parapharyngodon alvarengai 410.85±0.462–1810.418.2±2.97M Parapharyngodon largitor 150.31±0.132–410.423±0.32M Parapharyngodon sceleratus 2–22.08–M Physaloptera lutzi 2–22.08–H Physaloptera retusa Rudolphi, 18191–12.08–H Rhabdias sp . 6–62.08–H Strongyluris oscari 220.46±0.151–420.832.2±0.4M Ubajara National ParkHost speciesNParasite taxonAAM ± EPAPP%IM±EPLife cycle Ameiva ameiva 5 Nematoda Cosmocercidae27–2720–M Pharyngodon cesarpintoi 22–2220–M Pharyngodon travassosi 3–320–M Physaloptera lutzi 1–120–H Physaloptera retusa 5–4–520–H Skrjabinellazia galliardi 1–120–H (Continued Table 1)(Continued Table 1)
69 Metazoan Endoparasite Diversity in Lizards in Northeastern Brazil Neotropical Helminthology, Vol. 18, Nº1, jan - jun 2024 Ameivula pyrrhogularis 36 Cestoda Oochoristica travassosi 1–12.78–H Nematoda Pharyngodon cesarpintoi 501.38±0.929–318.3316.67±7.17H Pharyngodon travassosi* 1–12.78–H Brasilisincus heathi 17 Acanthocephala Unidentifed cystacanth14–3–1111.76–H Cestoda Oochoristica vanzolinni 6–65.88–H Nematoda Strongyluris oscari 2–25.88–M Coleodactylus meridionalis Boulenger, 188816 Acanthocephala Unidentifed cystacanth2–112.5–H Trematoda Mesocoelium monas Rudolphi, 181980.50±0.381–618.752.67±1.67H Cestoda Oochoristica vanzolinni 3–36.25–H Copeoglossum arajara Rebouças-Spieker, 19814 Nematoda Rhabdias sp . 1–125–H Physaloptera Lutzi 1–125– Copeoglossum nigropunctatum Spix, 18251Not parasitized Enyalius bibronii Boulenger, 18856 Acanthocephala Unidentifed cystacanth *1–116.64–H Trematoda Mesocoelium monas 145–14516.64–H Nematoda Physaloptera sp .* 1–116.64–H Hemidactylus agrius 18 Acanthocephala Unidentifed cystacanth1–15.56–H Nematoda Parapharyngodon alvarengai 1–15.56–M Parapharyngodon largitor 2–211.11–M Skrjabinellazia galliardi 9–1–716.67H Hemidactylus mabouia 8 Nematoda Parapharyngodon largitor 3–325–M (Continued Table 1)(Continued Table 1)
70 Fernandes de Carvalho et al. Neotropical Helminthology, Vol. 18, Nº1, jan - jun 2024 Physaloptera sp . 1–112.50– Iguana iguana 2 Nematoda Alaeuris vogelsangi 2756–275650–M Capillaria freitaslenti* 1–150–MCosmocercidae18–1850–M Ozolaimus cirratus Linstow, 19061935–193550–M Lygodactylus klugei 1Not parasitized-- Micrablepharus maximiliani 4Not parasitized Norops fuscoauratus d’Orbigny, 183712 Trematoda Mesocoelium monas 13–1–1218.18–H Nematoda Cosmocercidae2–29.09–M Rhabdias sp . 1–19.09–H Typhlonema sp . *1–19.09–M Phyllopezus pollicaris 1 Nematoda Spauligodon oxkutzcabiensis 6–6100– Polychrus acutirostris 2 Nematoda Gynaecometra bahienses Araujo, 197813005–1300550–M Salvator merianae Duméril & Bibron, 18392 Nematoda Cruzia lauroi 46–4650–H Diaphanocephalus galeatus Rudolphi, 1819128–17–111100–M Physaloptera retusa 4–450–H Tropidurus hispidus 66 Acanthocephala Unidentifed cystacanth140.21±0.151–104.554.67±2.73H Trematoda Mesocoelium monas 1–11.52–H Paradistomum parvissimum Travassos, 19185–51.51–H Cestoda Oochoristica travassosi 2–21.52–H Nematoda Oswaldocruzia sp . 240.36±0.161–915.152.04±0.78M Parapharyngodon largitor 1382.09±0.531–2739.395.30±1.10M (Continued Table 1)(Continued Table 1)
71 Metazoan Endoparasite Diversity in Lizards in Northeastern Brazil Neotropical Helminthology, Vol. 18, Nº1, jan - jun 2024 Physaloptera lutzi 1752.65±0.811–4039.396.73±1.79H Rhabdias sp.50.07±0.051–34.541.67±0.67H Spauligodon oxkutzcabiensis 15–151.52–M Strongyluris oscari 410.62±0.301–1715.154.1–1.67M Tropidurus semitaeniatus 38 Acanthocephala Unidentifed cystacanth30.16±0.1012.63–H Trematoda Mesocoelium monas 1–12.63–H Nematoda Parapharyngodon alvarengai 2–25.26 –M Parapharyngodon largitor 6–62.63–M Physaloptera lutzi 1–12.63–H Physalopteroides venancioi* 9–2–95.26 H Skrjabinellazia galliardi 2–22.61–H Strongyluris oscari 751.97±1.231–4321.059.36±4.37M (Continued Table 1) DISCUSSION In this study, 34 taxa of parasites were recorded, including Nematoda, Cestoda, Acanthocephala, and Pentastomida, infecting 20 species of lizards (Squamata, Lacertilia) with 21 new infection records. Aiuaba Ecological Station (AES) is one of the three protected areas studied, where most studies on lizard parasites have been conducted, thus, most of the records from this study had already been reported previously (see Brasileiro & Carvalho, 2023; Lacerda et al., 2023). Among the three protected areas, Sete Cidades National Park (SCNP) is the least represented in the literature regarding studies on lizard parasites. Similarly, Ubajara National Park (UNP) is also underrepresented, with Norops fuscoauratus and Tropidurus hispidus being investigated for parasites in previous studies (Santos-Mesquita et al. , 2020; Brasileiro & Carvalho, 2023). As Protected areas represent the local fauna (Zachos & Habel, 2011), the low number of studies in these areas, coupled with the species of hosts not yet investigated for parasites, contributed to the increasing number of new parasitic records in SCNP and UNP compared to AES. Te AES has been the focus of numerous studies on herpetological fauna and their parasites by research groups from nearby universities such as the Regional University of Cariri (URCA) and the Federal University of Cariri (UFCA). In comparison, SCNP and UNP have been relatively less explored by researchers studying parasites of reptiles and amphibians. However, with the rise in research centered on conservation units, the trend is for biodiversity records in these areas to increase as well, underscoring the importance of these regions for biodiversity protection.With a total of 690 analyzed lizards distributed among 23 host species, the richness of parasites found can be explained by the richness of the hosts, their ecological aspects and also by the sample size, since the sampling efort is related to the richness of the species sampled (Guegan et al. 2007; Poulin, 2019). Hosts with more recorded parasite species, such as T. hispidus , exhibit generalist feeding habits and are well-distributed in the sampling locations (Kolodiuk et al ., 2009). Te combination of these factors contributes to contact with diferent parasite species (Leung & Koprivnikar, 2019).For the species Colobosaura modesta , Copeoglossum nigropunctatum , and Vanzosaura multiscutata , we did not record any parasitic infections in this study. Representatives of the family Gymnophthalmidae are characterized by fossorial and semifossorial habits, and for this reason, they are expected to be parasitized by helminths with heteroxenous life cycles, as discussed by Teixeira et al. (2018). For the family Scincidae, whose representatives exhibit intermediate foraging behavior, a rich parasitic fauna is expected, including both monoxenous and heteroxenous species (Cooper, 1995; Rocha et al. , 2003). In addition, in previous studies that included C. nigropunctatum and V. multiscutata , parasites such as Physaloptera retusa Rudolphi, 1819, and Cosmocercidae, Parapharyngodon alvarengai Freitas, 1957, Pharyngodon cesarpintoi Pereira, 1939, Physaloptera lutzi Cristofaro, Guimarães & Rodrigues, 1976, Spauligodon oxkutzcabiensis Chitwood, 1938, and Skrjabinodon campiaoae De Sousa, Silva De Oliveira, Morais, Da Silva Pinheiro & Ávila, 2022, respectively, were recorded (Araujo-Filho et al. , 2020; Teixeira et al. ,
72 Fernandes de Carvalho et al. Neotropical Helminthology, Vol. 18, Nº1, jan - jun 2024 2020; Sousa et al. , 2022). Te parasites found in the cited studies are commonly associated with lizards (Ávila & Silva, 2010; Lacerda et al. , 2023). For C. modesta , no records of parasitism were found up to the writing of this work. Terefore, we assume that low sample size may have contributed to this result.Sete Cidades National Park (SCNP) had the highest number of new parasitism records. For the state of Piauí, where the park is located, only the species Iguana iguana Linnaeus, 1758, T. hispidus , T. semitaeniatus , and Phyllopezus pollicaris Spix, 1825, had been investigated for parasites in previous studies (Ávila et al. , 2012; Otávio et al. , 2018; Brasileiro & Carvalho, 2023). Most of the species analyzed in SCNP had already been the subject of parasitism studies in other locations in the country; however, the associated species were diferent (Ávila & Silva, 2010; Lacerda et al. , 2023). Tis park is located in a Cerrado stricto sensu area, and this ecoregion is considered an important biodiversity hotspot in Brazil (Zachos & Habel, 2011). Given this, as a rich biodiversity environment, the Cerrado can also harbor a great diversity of parasite species. Additionally, as understudied species are included in research, new data are obtained, and parasites not yet recorded for host species can be discovered.Te species with the highest number of new records was A. pyrrhogularis , the majority of which were parasites with a heteroxenous life cycle. Many parasites with this type of life cycle use arthropods as intermediate hosts (Anderson, 2000) and lizards of the genus Ameivula spp. has a diverse diet, including mainly arthropods and insect larvae, with active foraging habits (Mesquita & Colli, 2003ab). In an environment rich in biodiversity, ecological connections can become more complex, allowing for numerous interactions. Tis complexity may lead to more parasite species utilizing a variety of species as intermediate hosts, thereby increasing their success in reaching their fnal hosts (Poulin, 2014). Tis richness may have contributed to the number of new records in this study area, given that arthropods are part of the diet of several lizard species. Additionally, A. pyrrhogularis had been included in previous research, however, the growing number of new infection records highlights signifcant gaps in our comprehension of lizard parasitism.It was also recorded for A. pyrrhogularis, a specimen of the genus Brevimulticaecum Mozgovoi, 1951, constituting the frst record for lizards. Nematodes of the genus Brevimulticaecum spp. are more commonly associated, in their adult forms, with freshwater fsh and crocodilians. However, records of larval forms have been made in amphibians and a species of snake (Moravec et al., 1994; Anderson, 2000). Studies suggest that the larval forms in amphibians may play a role in the life cycle, aiming for fnal infection in crocodilians (González & Hamann, 2013). Te infection in A. pyrrhogularis may have occurred through the ingestion of a larval form, as this lizard species has a broad diet, including both adult and larval arthropods, and the diet may be directly related to the parasitic fauna (Silva et al. , 2019). It has been documented that parasites of this genus can cause intestinal lesions in defnitive hosts (Cardoso et al. , 2013). With the record of Brevimulticaecum sp. in the sampled locality, a more detailed examination of the biodiversity that may be involved in the life cycle of this parasite becomes important.Te records of Trematoda ( Mesocoelium monas and Paradistomum parvissimum ) were made only in the Ubajara National Park (UNP). Among the three protected areas, UNP has the highest average annual precipitation and the lowest average temperature (1,436.32 mm and 22–26 °C). Environmental conditions may be related to the prevalence of certain groups of parasites (Dybing et al ., 2013). Given this and knowing that trematodes have a heteroxenous life cycle, the presence of parasites with this life cycle in more humid environments may be related to the higher survival of their infective larval forms or eggs (Stromberg, 1997; Dybing et al ., 2013; Bolek et al., 2019). Additionally, their intermediate hosts, commonly arthropods or small mollusks, are also present in more humid environments (Dronen et al. , 2012). Supporting this idea, the literature shows that the presence of reptile-parasitic trematodes is associated with more humid environments, such as the coast, wet forests, collection points near water bodies, or aquatic animals (see checklist collection points in Lacerda et al ., 2023). Te presence of these parasites only in preserved areas (collection sites within protected areas) may be a sign of how human activities afect biodiversity. As observed by Brasileiro & Carvalho (2023), agriculture afects the richness and abundance of parasites with heteroxenous life cycles, including trematodes.Another parasite found in Ubajara National Park (UNP) was a specimen of the genus Typhlonema Kreis, 1938. Tis is a genus whose males seem to be unknown except for Typhlonema salomonis Kreis, 1938 (Lucker, 1943). Tey are typically parasites of lizards, and identifcation is performed through females, with one of the main characteristics being the highly muscular vulva in a prebulbar position and the anus at the end of the body, along with eggs having thick shells (Vicente et al ., 1993; Anderson, 2000). In previous studies, they have been
73 Metazoan Endoparasite Diversity in Lizards in Northeastern Brazil Neotropical Helminthology, Vol. 18, Nº1, jan - jun 2024 recorded parasitizing the intestine of lizards in Brazil, but this is the frst record for Norops fuscoauratus (Ávila & Silva, 2010).Tis study contributes to the understanding of parasitism in lizards in the Neotropical region, presenting 21 new infection records and suggesting that the presence of trematodes may be related to environmental humidity. Tus, the importance of faunal surveys for parasite diversity and investigating land use efects on parasite communities should be emphasized. However, it is important to note the limitations of the study, such as underrepresentation of some species due to the method of collection. For example, Gymnophthalmidae would be better represented if pitfall traps were included in our feld collections. Nevertheless, these limitations did not strongly afect our objectives for this work, which are to describe the metazoan endoparasites of lizards in protected areas and their surroundings. ACKNOWLEDGMENTS We thank to the Laboratório de biologia celular e helmintologia “Profa. Dra. Reinalda Marisa” at the Institute of Biological Sciences, Federal University of Pará (UFPA) for their support in identifying some species. We also thank the feld collection teams from the Universidade Estadual Vale do Acaraú-UVA and the Universidade Estadual do Cariri-URCA, as well as the team involved in slide preparation for parasite identifcation at the Núcleo Regional de Ofologia -NUROF/UFC. Funding Tis study was partially funded by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-CAPES (Finance code 001, process n° 88887.501922/2020-00). Te Fundo Brasileiro para Biodiversidade-Funbio, in collaboration with the Instituto Humanize, funded most of the feld activities. Additionally, thanks to the project “Conservação da biodiversidade em nível de paisagem: mudanças climáticas e distúrbios antropogênicos” (CNPQ/ICMBIO/FAPs n° 18/2017 - processo n° 421350/2017-2) for providing funding for initial feldwork. Author contributions: CRediT (Contributor Roles Taxonomy)EFFC = Elvis Franklin Fernandes de Carvalho ACB = Ana Carolina Brasileiro RWA = Robson Waldemar Ávila Conceptualization : EFFC, ACB, RWA Data curation : EFFC, ACB, RWA Formal Analysis : EFFC, RWA Funding acquisition : EFFC, ACB, RWA Investigation : EFFC, RWA Methodology : EFFC, ACB, RWA Project administration : EFFC, ACB, RWA Resources : EFFC, ACB, RWA Software : EFFC Supervision : RWA Validation : EFFC, ACB, RWA Visualization : EFFC, ACB, RWA Writing – original draft : EFFC Writing – review & editing : EFFC, ACB, RWA BIBLIOGRAPHIC REFERENCES Almeida, W., Freire, E., & Lopes, S. (2008). A new species of pentastomida infecting Tropidurus hispidus (Squamata: Tropiduridae) from Caatinga in Northeastern Brazil. Brazilian Journal of Biology , 68 , 199–203. Amato, J.F.R., & Amato, S.B. (2010). Técnicas gerais para coleta e preparação de helmintos endoparasitos de aves’, in S. von Matter et al. (eds) Ornitologia e conservação: ciência aplicada, técnicas de pesquisa e levantamento . 1 st ed. Technical Books, pp. 369–393.Anderson, R.C. (2000). Nematode parasites of vertebrates: their development and transmission . CABI Publishing. Anderson, R.C., Chabaud, A.G., & Willmott, S. (eds) (2009). Keys to the nematode parasites of vertebrates: archival volume , Keys to the nematode parasites of vertebrates: archival volume . UK.Andrade, C.M. (2000). Meios e soluções comumente empregados em laboratórios . Editora Universidade Rural.Antonelli, A. (2022). Te rise and fall of Neotropical biodiversity. Botanical Journal of the Linnean Society , 199, 8–24.
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