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Article

First Coprological Survey of Semiferal Goat (Capra hircus) Parasites in Relation to Environmental Factors on the Island of Socotra, Yemen

by
Lucie Maděrová
1,*,
Jan Šipoš
1,
Petr Maděra
2,*,
David Modrý
3,
Barbora Červená
4 and
Josef Suchomel
1
1
Department of Zoology, Fisheries, Hydrobiology and Apiculture, Mendel University in Brno, Zemědělská 1, 61300 Brno, Czech Republic
2
Department of Forest Botany, Dendrology and Geobiocoenology, Mendel University in Brno, Zemědělská 1, 61300 Brno, Czech Republic
3
Department of Parasitology, Masaryk University, Kamenice, 62500 Brno, Czech Republic
4
Department of Pathological Morphology and Parasitology, University of Veterinary Sciences, Palackého třída, 61200 Brno, Czech Republic
*
Authors to whom correspondence should be addressed.
Agriculture 2025, 15(5), 475; https://doi.org/10.3390/agriculture15050475
Submission received: 5 December 2024 / Revised: 13 February 2025 / Accepted: 17 February 2025 / Published: 22 February 2025
(This article belongs to the Section Farm Animal Production)
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Abstract

:
Parasites play a significant role in biodiversity, yet research on these organisms remains limited, particularly in tropical and subtropical regions. Parasites are also an essential aspect of domestic animal husbandry, and their prevalence depends on various factors, such as husbandry conditions and the environment. However, no studies have been conducted on parasites affecting domestic animals on Socotra Island. This study aimed to investigate parasites in selected goat populations on the island using intravital fecal diagnosis. A total of 406 samples from adult goats across different locations (lowlands and highlands) and seasons (dry and rainy) were collected, fixed in 10% formalin, and transported to the Czech Republic for coprological examination using flotation and ether sedimentation methods. Statistical analyses, including partial canonical correspondence analysis (pCCA), the Monte Carlo permutation test, and the chi-squared test, revealed a high prevalence of gastrointestinal parasite infections, with 89% of goats infected. Eimeria spp. had the highest prevalence (76%). Co-infection was common, with 55.9% of goats infected with multiple parasites. Seasonality influenced parasitism, with other Protostrongylidae, Muellerius spp., and Trichuris spp. predominating during the rainy season, and Eimeria spp. and gastrointestinal strongylids predominating during the dry season. This first study on Socotra Island, Yemen, provides crucial insights into effective intervention strategies for controlling goat parasite infections.

1. Introduction

The Socotra Archipelago, situated about 380 km south of Ras Fartak on the Gulf of Aden and roughly 230 km east of Cape Guardafui in Somalia, is famous for its unique plant and animal species [1]. In 1966, the goat population was estimated to be around 19,000 [2]. This number increased dramatically to 220,000 by 1999 [3]. The most recent census indicates that Socotra now hosts 480,000 goats [4].
These goats, believed to have been introduced alongside the first farmers, exhibit a remarkable variety of colors and patterns and roam freely across all ecosystems, including mountainous regions and the capital city, as part of a system of free grazing [3,5]. Prior to the 1950s, the dominant form of livestock management was nomadic pastoralism. This practice involved moving animals to regions with adequate rainfall and grasslands, utilizing a system of rotating grazing areas. However, in the aftermath of World War II, many pastoral communities began to adopt a more settled lifestyle. This shift resulted in a transition from nomadic pastoralism to a system of unrestricted grazing. The change was primarily attributed to a substantial increase in goat populations, which made effective pasture rotation challenging [3]. Traditional pastoralism continues to serve as a primary source of income for the island’s inhabitants [6].
However, the large number of domestic ruminants, particularly goats [7], presents several significant challenges, including the threat of disease transmission [8]. Parasitism is a crucial issue affecting small ruminant production on Socotra, just as it does globally. The free grazing system on Socotra makes goats highly susceptible to a wide array of helminth infections [9]. Gastrointestinal parasites, which include nematodes, trematodes, cestodes, and protozoa (coccidia) [10], can cause diseases that diminish the health and productivity of animals [11,12], manifesting as symptoms such as a rough, dull coat; weakness; diarrhea; tail rubbing; bottle jaw; loss of appetite; and weight loss [13]. In addition, parasites are especially detrimental, with decreased production levels, potentially increased mortality, and substantial financial losses [14].
Despite global recognition of these challenges, there is a notable gap in the literature regarding the parasitofauna of Socotra. To date, only one study has investigated parasites on the island, identifying species such as Haemogregarina spp., Sarcocystis spp., and Eimeria spp., which primarily infect reptiles [15]. The only livestock-related parasite reported is the viviparous midge of the family Oestridae, which can cause serious infections in both livestock and humans [5].
This study aims to provide a comprehensive overview of the parasitofauna affecting domestic goats, the most commonly kept livestock species on Socotra. This study contributes to a better understanding of the management strategies needed to protect goat populations and, by extension, the livelihoods of the Socotri people.

2. Materials and Methods

2.1. Study Area

This research was conducted on Socotra Island, situated in the northwestern Indian Ocean between 12.19°–12.42° N latitude and 53.18°–54.32° E longitude. As part of the Republic of Yemen, Socotra covers an area of 3600 km2 [6]. A large proportion of the island’s surface area (48%) is below 400 m above sea level and classified as lowland. The lower highlands, with elevations ranging from 400 to 700 m, account for 43.5% of the island’s surface area [16]. The island’s population is estimated to be 100,000, subject to seasonal fluctuations. The exact figure remains uncertain due to the absence of a census in Socotra [4]. Socotra’s climate is heavily influenced by the East African–Indian monsoon system, characterized by a biannual migrating intertropical convergence zone that shifts between its northern hemisphere winter position and southern Indian Ocean summer position [17]. The monsoon seasons are divided into two periods: the summer monsoon from May to September, and the winter monsoon from October to January [17,18]. The mean annual rainfall and temperature, measured in a network of meteorological stations from 2002 to 2006, were 216 mm and 28.9 °C at high altitudes, amounting to 800 mm [17].

2.2. Questionnaire Survey

To gain a basic understanding, a questionnaire survey was conducted on goat management and healthcare. Forty goat owners were selected for the interviews.

2.3. Sampling Method

The analysis was conducted at the Veterinary University in Brno, Czech Republic. A comprehensive account of the fecal samples obtained from goats on the island is presented in Table 1. Topographical names were used in accordance with Bezděk et al. [19]. A total of 406 adult female goat samples were collected for coprological examination in 2021 (March and November) and 2022 (March). Some sites were sampled in both years, but these were not the same animals as they came from different herds. These samples were obtained from two different sites: 183 from the lowlands and 223 from the highlands. Two sets of samples were collected, comprising 100 from the dry season (March 2021) and 100 from the rainy season (November 2021). We did not subject the 2022 (n = 206) samples to seasonal testing because monsoon rain did not occur. Only a few rainfall events occurred during the study period. Morning milking times were used for collection to ensure the freshness of the samples. Samples were collected directly from the rectum using rubber gloves. Excreta from one goat were collected in a glass vial, with five samples from each goat placed in each vial and properly labeled. The pellets were fixed on-site with 10% formalin and stored in a refrigerator until departure for coprological analysis, as there is no laboratory on the island. Because of the island’s high temperatures, often exceeding 30 °C, refrigerated storage was chosen as a precaution to prevent the unwanted evaporation of formalin and potential damage to the samples.

2.4. Parasitological Analyses

Samples were processed in the laboratory within 9 months (2021) and 3 months (2022) after collection in Socotra. The samples were uniformly ground to slurry consistency using a mortar and pestle, resulting in a homogenized mixture. Subsequently, the samples were strained through a sieve and transferred to a 50 mL tube, to which an appropriate amount of water was added. The samples were then centrifuged for 10 min at 2000 rpm. After removing the water, the sediment was resuspended in 15 mL of 10% formalin. Subsequently, the suspension was divided into three 5 mL aliquots. One aliquot was used for flotation analysis, the second aliquot was processed by ether sedimentation analysis, and the remaining aliquot was kept as a backup in case of any errors during the analysis.
The identification and analysis of parasitic stages, such as oocysts, eggs, and larvae, were based on their morphological features and size, following the literature [20].

2.4.1. Fecal Flotation

We conducted our research in accordance with the FLOTAC technique [21]. The formalin tube was mixed and centrifuged for 2 min at 2000 rpm. Subsequently, the supernatant was discarded, and the sediment was resuspended in Sheather’s sugar solution (1000 mL of water, 1.5 kg beet sugar, 10 mL phenol, specific gravity 1.3) to the desired level. The tube was then centrifuged again for 2 min at 2000 rpm. Subsequently, the surface layer of the sample was transferred onto a microscope slide using a modified microbiological loop and prepared for microscopic examination at 20× and 40× magnification.

2.4.2. Ether Sedimentation Technique

This method was selected to search for larger eggs and larvae. Five milliliters of ether was added to the 5 mL formalin aliquot, which was then vigorously shaken and centrifuged for 2 min at 2000 rpm. The supernatant was discarded, and the sediment diluted with a few drops of water was transferred onto a slide using a Pasteur pipette. The whole sediment was examined, and 3–5 slides were typically prepared from one sample. The slides were examined under a light microscope at 10× and 20× magnification.

2.5. Statistical Analysis

In this study, we applied multivariate methods, specifically partial canonical correspondence analysis (pCCA) [22], with sampling year and locality as covariates. We used pCCA to evaluate species composition and distribution across seasons (coded as rainy/dry) and altitudinal zonation (coded as lowland/highland). We used a distinct time interval (i.e., one year) as a categorical explanatory variable to eliminate any potential systematic trends over time that would occur, regardless of the tested variables. To avoid conflating temporal and spatial variability, which could lead to a liberal test, we randomized the records separately within each locality. The temporal correlation between repeated samples from the same locality was addressed by restricting the permutation test. Therefore, we applied the restricted Monte Carlo permutation test, constraining randomization by maintaining the temporal autocorrelation of individual records within each locality through cyclic shifts. The abundance of each species was transformed using decimal logarithms. All constrained axes and the first constrained axis were tested using a restricted Monte Carlo permutation test [23]. The analysis was conducted using the CANOCO 5 software [24]. The analyses described below were performed using the R software (ver. 4.4.0) [25]. In this study, we employed the chi-squared test to analyze parasite frequency distribution across species and assess the uniformity of single and multiple parasitism occurrences in goats.

3. Results and Discussion

3.1. Survey Descriptive Statistics

The following text presents descriptive statistics for the management and healthcare of goats. It is important to note that none of the goats were stabled; they roamed freely on the island, with 100% grazing on natural food year-round. However, they were overfed during milking. Regarding awareness, 87% of respondents stated that they were aware of antiparasitics on Socotra; however, 38% did not use them, resulting in 49% of respondents using antiparasitics on their goats. Additionally, 45% of the respondents reported finding parasites in the bodies of slaughtered goats. Regarding water sources, 86% of goats drank from wadis, 9% from springs, and only 5% from domestic sources. Nevertheless, all goats were watered when called for milking, with 100% receiving water.

3.2. Overall Results

Among the 406 goats analyzed, 363 (89%) were infected with one or more taxa of gastrointestinal parasites. These findings align with those of Koinari et al. [26], who reported an infection rate of 89% in Papua New Guinea, which align with the results of Chikweto et al. [27] (98% in Grenada, West Indies), Eke et al. [28] (75% in Niger State, Nigeria), Singh et al. [29] (67% in Mathura, India), and Raza et al. [30] (78% in the Cholistan Desert, Pakistan). Figure 1 illustrates the prevalence of detected parasites, with Eimeria spp. occurring most frequently with 309 (76%) ( χ 2 = 671.8 , p < 0.001), followed by gastrointestinal strongylids with 182 (45%) ( χ 2 = 671.8 , p < 0.001), Trichuris spp. with 116 (29%) ( χ 2 = 671.8 , p < 0.001), Strongyloides sp. with 26 (6%) ( χ 2 = 671.8 , p < 0.001), Muellerius spp., with the lowest prevalence at 9 (2%) ( χ 2 = 671.8 , p < 0.001), and other undetermined Protostrongylidae with 7 (2%) ( χ 2 = 671.8 , p < 0.001).
Table 2 presents a comprehensive classification of the various parasitic species examined in this study, categorizing them by their routes of infection.
The most prevalent parasites in the examined goats were Eimeria spp., with oocysts detected in more than 75% of the animals. The prevalence of Eimeria spp. in goats ranges from less than 20%, reported from Papua New Guinea [26], to values exceeding 80% or even 90% in Ethiopia, Malaysia, Iran, Egypt, and Northern Jordan [32,33,34,35,36].
If we compare the prevalence of Eimeria spp. with that in the other countries mentioned above, we can assume that they have a higher prevalence due to higher rainfall and animal breeding practices. Socotra is drier than Malaysia and some areas of Ethiopia. The mean annual rainfall and temperature, measured in a network of meteorological stations from 2002 to 2006, were 216 mm and 28.9 °C at high altitudes, amounting to 800 mm [17]. In Malaysia, rainfall ranges between 2000 and 3000 mm and can reach up to 4000 mm in mountainous regions. In Ethiopia, it ranges from 200 mm in dry areas to 1500 mm in mountainous regions. Lower humidity outside the monsoon season limits the spread of Eimeria. Socotra has free-range goat farming, often with lower stocking densities than intensively farmed countries, which may reduce the risk of parasite transmission. Specifically, in Western Iran, Etsay et al. [33] reported that a higher prevalence might be associated with immunity levels and variations in management practices. The low prevalence of Eimeria spp. in a study by Koinari et al. [26] in Papua New Guinea may be attributed to differences in methodologies used for parasite identification. A simple flotation procedure was used in that study.
The infection can cause clinical coccidiosis, which is the most prevalent enteric illness affecting goats, according to a study conducted by Kaur et al. [37]. This condition, caused by coccidian parasites, can result in high mortality rates and reduced milk, hair, or meat production, as reported by Agyei et al. [38]. The risk of clinical disease is higher in young animals and is often associated with a high density of animals and/or poor hygiene [39].
Gastrointestinal strongylids constituted a significant proportion of parasites, accounting for 45% of instances. This is comparable to the findings in other regions, with prevalence rates ranging from 33% in India and 49.5% in Ethiopia to 57% in South Africa [40,41,42]. Similar results could be explained by the prevalence of extensive goat farming in all three regions. The animals graze in open pastures, which reduces their exposure to feces, a primary source of reinfection. However, some studies have reported much higher prevalence rates of 90% in Kenya and 89% in Grenada [27,43]. Socotra is characterized by an arid to semiarid climate, with annual rainfall ranging between 200 and 800 mm, which is significantly less than that in tropical areas such as Kenya, where high humidity and frequent rainfall create ideal conditions for strongylid eggs to sporulate and survive in the environment. Chikweto et al. [27] reported that the high prevalence may be due to resistance to anthelmintic drugs, the type of grazing system used, and the level of education of farmers. These parasites can cause various health problems, including diarrhea, anemia, hypoproteinemia, stunted growth, and even death in severe cases [20].
Trichuris spp. are another group of parasites identified in the samples. The prevalence of Trichuris spp. in the examined goats was 29%. This aligns with some studies, such as those reporting 30% in South Africa and 35% in Pakistan [42,44]. However, most studies have reported lower prevalence rates. The prevalence of Trichuris spp. in goats ranges from 0.47% in India [40] to 12%, which is similar to findings in regions such as Malaysia, Papua New Guinea, Nigeria, and Kenya [26,28,43,45]. These parasites can cause enteritis, diarrhea, and weight loss in infected animals [46]. Socotra, South Africa, and Pakistan exhibit similar climatic conditions, suggesting that the comparable prevalence is attributable to analogous environmental factors. In India, Dixit et al. [40] reported that the decreasing trend in the overall prevalence of gastrointestinal helminths is associated with a declining trend in the mean minimum relative humidity. In regions such as Nigeria and Kenya, it is prevalent for goats to graze alongside other livestock, including sheep, cattle, or poultry. Mixed husbandry practices may facilitate the proliferation of other parasite species that are predominant in a given environment, thereby limiting the dissemination of Trichuris spp. The low prevalence of Trichuris spp. in goats in areas characterized by high rainfall, such as Papua New Guinea and Malaysia, may be attributed to the potential washing out of eggs from the soil. Additionally, these regions feature abundant vegetation, allowing goats to graze on shrubs, trees, and elevated vegetation. Consequently, if goats have limited contact with contaminated soil, the risk of infection is reduced.
The prevalence of Strongyloides sp. in the examined goats was relatively low, at 6%. This is lower than what has been reported in most other regions. The prevalence of Strongyloides sp. in goats ranges from as low as 1% in India to as high as 45.6% in Malaysia [40,45]. Other studies have reported values between 5% and 36% in regions such as Ethiopia, Nigeria, South Africa, Kenya, Egypt, and Papua New Guinea [26,27,28,41,42,43,47,48]. The lower prevalence of Strongyloides sp. on Socotra may be attributed to the arid climate and intense solar radiation, which diminishes the survival of infectious stages. Conversely, in humid regions such as Malaysia and Papua New Guinea, consistent moisture and favorable temperatures facilitate a higher prevalence of this parasite. In areas characterized by moderate temperatures and regular precipitation such as South Africa or Egypt, larvae may exhibit prolonged survival, potentially resulting in increased prevalence. Clinical symptoms caused by Strongyloides sp. can vary widely and may include intermittent diarrhea, dehydration, anorexia, weight loss, tooth grinding, foaming at the mouth, anemia, and even neurological signs, such as ataxia, wide stance, stupor, and nystagmus [49].
Larvae of Mullerius capillaris (Muellerius sp.) were found at a prevalence rate of 2%. This is lower than what has been reported in most other regions. The prevalence of Mullerius capillaris in goats varies widely, from as low as 6.5% in Egypt to as high as 93% in the Czech Republic [48,50]. Other studies have reported prevalence rates ranging between 12% and 64% in countries such as Bangladesh, the United States, northeastern Ethiopia, and Iraq [51,52,53,54,55]. The larvae of Muellerius sp., which utilize terrestrial gastropods as intermediate hosts, require a moist environment to complete their life cycle. The arid conditions of Socotra likely restrict the abundance of gastropods and larval survival in the environment. In regions with higher prevalence rates, such as the Czech Republic (93%) [50] or Bangladesh (64%) [52], moderate temperatures and regular precipitation provide optimal conditions for gastropod survival and larval development. For instance, the Czech Republic exhibits a temperate climate and adequate moisture to sustain an intermediate host population, facilitating a high prevalence of this parasite. This nematode infects the lungs and releases its larvae through sputum and stool. Transmission to animals occurs when secondary hosts, such as slugs or snails, are accidentally consumed by goats and sheep [51].
The least abundant parasites were other Protostrongylidae that could not be determined to the genus level, with an overall prevalence of only 2%. This low prevalence is consistent with other studies, which have reported rates of 2% in Mongolia and 4% in Iraq [55,56]. Socotra and Iraq have similar climatic conditions in terms of temperature and rainfall, so it is likely that this weather effect correlates with the prevalence of the parasites. The dry season and high temperatures likely prevent the massive spread of these parasites. Similarly, in Mongolia, despite the markedly different climatic characteristics (continental climate with extreme winter frosts and short, relatively humid summers), seasonal variations also limit the spread of these parasites. The combination of unfavorable conditions in these three regions (Socotra, Iraq, and Mongolia) likely hinders the widespread and long-term survival of Protostrongylidae parasites, as reflected by the low prevalence rates in all cases. These parasites inhabit the lungs but are not considered major pathogens and have relatively minor economic importance compared to other helminth parasites in goats. Pneumonic signs are rarely observed in association with Protostrongylidae infection [31].
Based on the aforementioned discussion, it can be concluded that goats on Socotra Island exhibit a lower prevalence of several parasite species, with the exception of Trichuris spp., compared to findings from other studies. This phenomenon can primarily be attributed to a combination of environmental, climatic, and management factors. As reported by Maděrová et al. [57], surveyed farmers of Socotra identified diseases as one of the most common causes of non-slaughter mortalities. Therefore, there is an urgent need for disease identification and control to ensure the health of both humans and animals. Our research contributes to this goal by providing new insights into the presence of parasites in goats on Socotra, bringing us closer to a deeper understanding of health risks and prevention options. In particular, hygiene should be maintained in areas with higher concentrations of animals as there is the greatest risk of parasite transmission, particularly at watering places during the dry season.
The majority of positive cases were double infections, with 180 (44%) ( χ 2 = 394 ,   13 , p < 0.001), and single infections, with 136 (33%) ( χ 2 = 394 ,   13 , p < 0.001). In addition, no infections were observed in 43 cases (11%) ( χ 2 = 394 ,   13 , p < 0.001), triple infections were observed in 36 cases (9%) ( χ 2 = 394 ,   13 , p < 0.001), quadruple infections were observed in 10 cases (2%) ( χ 2 = 394 ,   13 , p < 0.001), and there was one case of a quintuple infection (0.2%) ( χ 2 = 394 ,   13 , p < 0.001) (see Figure 2).
It is noteworthy that the majority of the samples, accounting for 55.9%, displayed co-infection with multiple parasites, with some goats experiencing up to five infections. This high parasite density underscores the importance of understanding mixed infections, as they can have severe consequences, including host mortality [58]. Co-infections were examined in a study conducted by Ghimire in Kathmandu, Nepal [59]. The study found that 100% of the samples contained more than two parasites, with some samples showing seven infections. Similarly, a study by Cai et al. [60] found that 91.5% of the samples had more than one parasite, with many samples from Jiangsu, Shaanxi, and Hunan in China showing five infections.
Therefore, Socotra has a lower prevalence of multiple parasite co-infections compared to the aforementioned areas in China and Nepal. This difference may be due to differences in climatic conditions, specifically the amount of rainfall. Although Nepal and the provinces mentioned in China have high annual rainfall, Socotra is significantly drier. The lower rainfall in Socotra limits environmental humidity, which is crucial for the survival and development of free-living parasites, which may explain the lower co-infection rates.

3.3. The Impact of Rainy and Dry Seasons on the Diversity of Parasite Species

Based on the pCCA model, we can conclude that protostrongylids, including Muellerius sp. and other undetermined Protostrongylidae, as well as Trichuris sp., parasitized exclusively during the rainy season, while Eimeria spp. and gastrointestinal strongylids had significantly higher prevalence during the dry season (permutation test of all axes: pseudo-F = 5.1; p = 0.026), as depicted in Figure 3. Tropical regions such as Socotra generally have a heightened incidence of parasitic activity and prevalence during wetter periods, a finding corroborated by several studies [61,62,63,64,65].
In the permanently humid and savanna zones of the tropics, rainfall is the major factor determining the availability and transmission of strongylid nematodes in sheep and goats in natural pastures [66]. In contrast, this research indicates that strongylid parasite infestation poses a greater risk during the dry season, which contradicts the findings of previous studies [61,62,63,64,67,68,69,70,71,72,73]. This discrepancy warrants further scientific inquiry to determine the specific factors that contribute to the increased risk. These factors may include the presence of specific microclimatic conditions during drought, such as soil moisture or the microenvironment around vegetation. The higher prevalence during the dry season may be due to goats ingesting larvae during the rainy season when the wet environment provides favorable conditions for development. The larvae then take approximately one month to reach adulthood. In addition, some parasite species can delay their development, for example, in the mucous membrane of the host, which can affect the timing of their detection. Another important factor is the increased concentration of animals around limited food and water sources during the dry season. This situation increases the risk of environmental contamination with feces, thereby increasing the likelihood of parasite transmission between animals. Owners are more likely to congregate their animals at watering and feeding points during the dry season, resulting in increased contact between animals. In addition, the possibility of interactions between goats and other animals that could serve as reservoirs for parasites should be investigated. As emphasized by Okon et al. [74], understanding seasonal differences in the availability of infective nematode larvae is critical for the epidemiology and control of infections caused by strongylid nematodes.
Eimeria spp. is another parasite that tends to be more prevalent in the dry season. An increased incidence of infections caused by Eimeria spp. during dry periods is commonly observed and can be attributed to several factors. Eimeria spp. oocysts are highly resilient and can survive under dry conditions for extended periods [75]. In addition, drought can cause stress and weaken the immune system of animals, making them more susceptible to infections [76]. During dry periods, the lack of quality grazing may lead to dietary changes [77] that negatively affect the digestive system of animals and increase their vulnerability to parasitic infections [78]. It is also believed that a lack of herbs during the dry season may result in an increased number of oocysts per unit area, as suggested by Wamae et al. [79]. However, several studies have reported a higher prevalence of Eimeria spp. in the rainy season compared to the dry season [62,63,67,72,80,81,82,83,84,85]. Nonetheless, some studies have reported significantly higher oocyst counts during periods of drought than in other periods, as demonstrated by Kusiluka et al. [84].
The parasite Strongyloides sp. has an increased incidence on the island of Socotra, particularly during the dry season. This finding can be compared with the findings of other studies. A study conducted by Nwosu et al. [71] in northeastern Nigeria showed that this parasite species is present in sheep and goats throughout the year irrespective of the season, which was likely due to poor hygiene in the animal husbandry system, particularly of feeders and waterers. While some studies have reported a higher prevalence in the dry season [86], other studies have suggested that the highest prevalence of the parasite occurs in the rainy season [61,63,64,72,73]. This difference suggests that factors influencing parasite prevalence may be complex and dependent on local conditions. In Socotra, there is also more frequent feeding and watering of animals in the dry season than in the rainy season, as suggested by Maděrová et al. [57]. Thus, we can assume that infection may also have originated from poor cleaning of buckets and feeding areas, where parasites may have accumulated.

3.4. Impact of the Interaction Between Season and Relief on Parasite Species Composition

An ordination plot that evaluates the distribution of species as a function of the interaction between season and relief showed three clusters (see Figure 4). Based on the pCCA model, the first cluster was the clearest: Muellerius sp. and other Protostrongylidae, which predominantly parasitized at higher elevations during the rainy season. The second cluster consisted only of Strongyloides sp., which predominantly parasitized at higher elevations during the dry season. The third and least distinct cluster was formed by Eimeria spp., gastrointestinal strongylids, and Trichuris spp.; however, the graph shows a slight shift in the activity of Eimeria spp. and gastrointestinal strongylids toward the lowlands during the dry season (permutation test of all axes: pseudo-F = 4.4, p = 0.04048). Relief as an independent factor had no conclusive effect on species composition.
The results showed that Muellerius spp. and other Protostrongylidae predominantly parasitized at higher altitudes during the rainy season. This finding is consistent with the ecology of these species. Parasites have an indirect life cycle involving intermediate hosts, namely terrestrial gastropods, which are most active and abundant during periods of abundant moisture, that is, during the rainy season. Identifying the specific species of gastropods involved as intermediate hosts is crucial for understanding the transmission cycle and implementing targeted prevention and control measures in livestock. The island of Socotra remains poorly studied, and greater attention should be directed toward identifying these intermediate-host snails. Larvae were detected in droppings in November, with the rainy season beginning in October [17,18]. As the prepatent period for these species lasts 6–10 weeks [10], goats were probably infected at the beginning of this period. This theory is supported by the findings of other scientists, such as Diez et al. [87], who found that the greater prevalence of Muellerius spp. increased with increases in relative humidity and rainfall.
Strongyloides sp. predominantly parasitizes at higher altitudes during the dry season. The higher likelihood of infection with Strongyloides sp. parasites in the highlands may be due to the fact that during the dry season, there are limited water sources in the countryside and animals concentrate in these areas [88]. This increases the concentration of parasites in certain areas where animals spend more time and, therefore, the likelihood of infection, as infective stages can persist there for a long time. The same is true for pastures: in the dry season, there may be less available moist soil, which can lead to higher concentrations of infective larvae in small areas of moist soil, such as near watering holes or in shaded areas where moisture is retained longer. This concentration may lead to greater exposure of animals to parasites [89].
Eimeria spp. and gastrointestinal strongylids infested goats more frequently in lowlands during the dry season. This correlates with the previously described finding that parasite infestation most likely occurs in the lowlands during the dry season (see Figure 3). The dry season also leads to the drying of lagoons, where grass grows and animals concentrate on grazing (see Figure 5). This environment is suitable for oocysts and larvae that seek warmth and large amounts of soil [90].

4. Conclusions

To the best of our knowledge, this is the first report on the prevalence of endoparasites in goats on Socotra Island, Yemen. In addition, Eimeria spp. and gastrointestinal strongylids are the most abundant parasites in goats. A significant proportion of the samples, specifically 55.9%, exhibited concurrent infections with multiple parasites, with some goats harboring as many as five different parasites simultaneously. Notably, protostrongylids, including Muellerius sp. and other undetermined Protostrongylidae, as well as Trichuris sp., were exclusively observed during the rainy season, whereas Eimeria spp. and gastrointestinal strongylids showed significantly higher prevalence in the dry season. This study also revealed interactions between season and relief affecting parasite species composition in the examined ecosystem. These findings demonstrate that certain parasites exhibit distinct patterns of prevalence based on elevation and seasonal changes. Specifically, Muellerius sp. and Protostrongylidae showed a preference for higher elevations during the rainy season, whereas Strongyloides sp. predominated at higher elevations during the dry season. Eimeria spp., gastrointestinal strongylids, and Trichuris spp. exhibited more complex patterns, with a slight shift in activity toward lowland areas during the dry season.
Addressing parasitic infections is crucial for improving the overall well-being and productivity of goats, particularly in regions where goat farming is a key livelihood. Knowledge of gastrointestinal helminth biology and the epidemiological infection patterns caused by these parasites is essential for developing appropriate control strategies, which can help reduce production losses. We recommend raising awareness among farmers in the study area regarding the impact of endoparasites on small ruminants and the importance of effective control measures. Maintaining cleanliness in areas with high animal concentrations should be prioritized to mitigate this risk.

Author Contributions

All authors contributed to this study’s conception and design. Material preparation, data collection, and analysis were performed by L.M., P.M., J.Š., B.Č., D.M. and J.S. The first draft of the manuscript was written by L.M., and all authors commented on previous versions of the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the Franklinia Foundation, Phase 1 (2020-03).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

This study involved a questionnaire survey of farmers and the collection of excrement directly from the rectum of goats. Participants provided verbal informed consent for animal sampling and the related survey questions. The collection of samples was carried out by Lucie Maděrová, who has a professional education in the field of animal protection and welfare, adhering to the regulations and guidelines on animal husbandry and welfare.

Data Availability Statement

The datasets generated and analyzed during this study are not publicly available because this paper has not yet been published. After publication, they will be made available in a publicly accessible repository.

Acknowledgments

The researchers behind this text extend their heartfelt appreciation to their Socotri acquaintances, including friends, guides, drivers, and herd owners from whom samples were gathered, for their generosity and assistance during this study. They express their deepest gratitude to Eng. Salem Hamdiah and Mohammed Amar for their invaluable help with translations during the interviews. Moreover, the researchers are thankful to Martin Štůsek for his feedback throughout this project. They acknowledge that their travel to Socotra was facilitated in part by Mendel University’s support through a long-term international internship (Long-Term Traineeships of MENDELU Doctoral Students Abroad, 2021-03), for which they are sincerely thankful. Finally, the authors express their gratitude to the Environmental Protection Agency (EPA) and local authorities for granting permission to conduct the fieldwork.

Conflicts of Interest

The authors declare they have no known competing financial interest or personal relationships that could have appeared to influence the work reported in this paper.

References

  1. Van Damme, K. Socotra Archipelago. In Encyclopedia of Islands; University of California Press: Berkeley, CA, USA, 2009; Chapter Socotra Archipelago; pp. 846–851. [Google Scholar]
  2. Brown, G. Social and Economic Conditions and Possible Development of Socotra; Technical report, Federal Government Mission Report; Durham University: Durham, UK, 1966. [Google Scholar]
  3. Scholte, P.; Miller, T.; Al-Okaishi, A.; Saed, A. Goats: Part of the Problem or the Solution to Biodiversity Conservation on Socotra? Technical report, IUCN—World Heritage Site evaluation mission to Socotra island; The International Union for Conservation of Nature (IUCN): Gland, Switzerland, 2007. [Google Scholar]
  4. Maděra, P.; Van Damme, K. Socotra Archipelago (Yemen). In Imperiled: The Encyclopedia of Conservation; DellaSala, D.A., Goldstein, M.I., Eds.; Elsevier: Oxford, UK, 2022; pp. 267–281. [Google Scholar] [CrossRef]
  5. Miller, A.G.; Morris, M. Ethnoflora of the Soqotra Archipelago; Royal Botanic Garden Edinburgh: Edinburgh, UK, 2004; OCLC: Ocm56654267. [Google Scholar]
  6. Van Damme, K.; Banfield, L. Past and present human impacts on the biodiversity of Socotra Island (Yemen): Implications for future conservation. Zool. Middle East 2011, 54, 31–88. [Google Scholar] [CrossRef]
  7. Pietsch, D.; Morris, M. Modern and ancient knowledge of conserving soils in Socotra Island, Yemen. In Land Degradation and Desertification: Assessment, Mitigation and Remediation; Springer: Dordrecht, The Netherlands, 2010; pp. 375–386. [Google Scholar]
  8. Herrero, M.; Grace, D.; Njuki, J.; Johnson, N.; Enahoro, D.; Silvestri, S.; Rufino, M.C. The roles of livestock in developing countries. Animal 2013, 7, 3–18. [Google Scholar] [CrossRef] [PubMed]
  9. Abebe, W.; Esayas, G. Survey of ovine and caprine gastro-intestinal helminthosis in eastern part of Ethiopia during the dry season of the year. Rev. Med. Vet. 2001, 152, 379–384. [Google Scholar]
  10. Zajac, A.; Conboy, G.A. Veterinary Clinical Parasitology, 8th ed.; Wiley-Blackwell: Hoboken, NJ, USA, 2012. [Google Scholar]
  11. Sanyal, P. Gastrointestinal parasites and small ruminant production in India. In Proceedings of the ACIAR PROCEEDINGS, Bogor, Indonesia, 22–25 April 1996; pp. 109–112. [Google Scholar]
  12. Maichomo, M.; Kagira, J.; Walker, T. The point prevalence of gastro-intestinal parasites in calves, sheep and goats in Magadi division, south-western Kenya. Onderstepoort J. Vet. Res. 2004, 71, 257–261. [Google Scholar] [CrossRef]
  13. Risso, A.; Kessler, J.; Soriano, V.; Nunes, M.; Machado, G.; Langaro, A.; Rossetto, R.; Zuffo, T.; Dallago, M.; Castro, P.; et al. Influence of Pathological Conditions Caused by Gastrointestinal Parasites Infection on Pregnant Ewe’s Behavior. Acta Sci. Vet. 2015, 43, 1283. [Google Scholar]
  14. Simpson, H. Pathophysiology of abomasal parasitism: Is the host or parasite responsible? Vet. J. 2000, 160, 177–191. [Google Scholar] [CrossRef]
  15. Tomé, B.; Maia, J.; Perera, A.; Carranza, S.; Vasconcelos, R. Parasites in a hotspot: Diversity and specificity patterns of apicomplexans infecting reptiles from the Socotra Archipelago. Parasitology 2021, 148, 42–52. [Google Scholar] [CrossRef]
  16. Brown, G.; Mies, B.A. Vegetation Ecology of Socotra; Number v. 7 in Plant and vegetation; Springer: Dordrecht, The Netherlands, 2012; OCLC: Ocn773671515. [Google Scholar]
  17. Scholte, P.; De Geest, P. The climate of Socotra Island (Yemen): A first-time assessment of the timing of the monsoon wind reversal and its influence on precipitation and vegetation patterns. J. Arid Environ. 2010, 74, 1507–1515. [Google Scholar] [CrossRef]
  18. Kalivodová, H.; Culek, M.; Čermák, M.; Maděra, P.; Habrová, H. Potential importance of Socotra dragon’s blood tree cloud forests and woodlands for capturing horizontal precipitation. Rend. Lincei. Sci. Fis. Nat. 2020, 31, 607–621. [Google Scholar] [CrossRef]
  19. Bezděk, J.; Purchart, L.; Kral, K.; Hula, V. List of local Socotran geographical names used in entomological literature. Acta Entomol. Musei Natl. Pragae 2012, 52, 27–67. [Google Scholar]
  20. Zajac, A.; Conboy, G. Fecal examination for the diagnosis of parasitism. Vet. Clin. Parasitol. 2012, 8, 72–73. [Google Scholar]
  21. Cringoli, G.; Rinaldi, L.; Maurelli, M.P.; Utzinger, J. FLOTAC: New multivalent techniques for qualitative and quantitative copromicroscopic diagnosis of parasites in animals and humans. Nat. Protoc. 2010, 5, 503–515. [Google Scholar] [CrossRef] [PubMed]
  22. Ter Braak, C. Partial canonical correspondence analysis. In Classification and Related Methods of Data Analysis, Proceedings of the First Conference of the International Federation of Classification Societies (IFCS), Aachen, Germany, 29 June–1 July 1987; North-Holland: Amsterdam, The Netherlands, 1988; pp. 551–558. [Google Scholar]
  23. Shipley, B. A permutation procedure for testing the equality of pattern hypotheses across groups involving correlation or covariance matrices. Stat. Comput. 2000, 10, 253–257. [Google Scholar] [CrossRef]
  24. Ter Braak, C.J.; Smilauer, P. CANOCO Reference Manual and CanoDraw for Windows User’s Guide: Software for Canonical Community Ordination, Version 4.5; Technical Report. 2002. Available online: www.canoco.com (accessed on 20 October 2024).
  25. Toffalini, E.; Gambarota, F.; Perugini, A.; Girardi, P.; Tobia, V.; Altoè, G.; Giofrè, D.; Team, P.C.; Feraco, T. Clusters that are not there: An R tutorial and a Shiny app to quantify a priori inferential risks when using clustering methods. Int. J. Psychol. 2024, 59, 1183–1198. [Google Scholar] [CrossRef] [PubMed]
  26. Koinari, M.; Karl, S.; Ryan, U.; Lymbery, A. Infection levels of gastrointestinal parasites in sheep and goats in Papua New Guinea. J. Helminthol. 2013, 87, 409–415. [Google Scholar] [CrossRef] [PubMed]
  27. Chikweto, A.; Tiwari, K.; Bhaiyat, M.I.; Carloni, J.; Pashaian, K.; Pashaian, A.; De Allie, C.; Sharma, R.N. Gastrointestinal parasites in small ruminants from Grenada, West Indies: A coprological survey and a review of necropsy cases. Vet. Parasitol. Reg. Stud. Rep. 2018, 13, 130–134. [Google Scholar] [CrossRef]
  28. Eke, S.; Omalu, I.; Ochaguba, J.; Urama, A.; Hassan, S.; Otuu, C.; Okafor, I. Prevalence of gastrointestinal parasites of sheep and goats slaughtered in Minna Modern Abattoir, Niger State, Nigeria. J. Anim. Sci. Vet. Med. 2019, 4, 65–70. [Google Scholar] [CrossRef]
  29. Singh, V.; Varshney, P.; Dash, S.; Lal, H. Prevalence of gastrointestinal parasites in sheep and goats in and around Mathura, India. Vet. World 2013, 6, 260. [Google Scholar] [CrossRef]
  30. Raza, M.A.; Younas, M.; Schlecht, E. Prevalence of gastrointestinal helminths in pastoral sheep and goat flocks in the Cholistan desert of Pakistan. JAPS J. Anim. Plant Sci. 2014, 24, 127–134. [Google Scholar]
  31. Taylor, M.A.; Coop, R.L.; Wall, R. Veterinary Parasitology, 3rd ed.; Blackwell: Hoboken, NJ, USA, 2007. [Google Scholar]
  32. Verma, R.; Sharma, D.K.; Paul, S.; Gururaj, K.; Dige, M.; Saxena, V.K.; Rout, P.K.; Bhusan, S.; Banerjee, P. Epidemiology of common gastrointestinal parasitic infections in goats reared in semi-arid region of India. J. Anim. Res. 2018, 8, 39–45. [Google Scholar]
  33. Etsay, K.; Megbey, S.; Yohannes, H. Prevalence of sheep and goat coccidiosis in different districts of Tigray region, Ethiopia. Niger. J. Anim. Sci. 2020, 22, 61–69. [Google Scholar]
  34. Hashemnia, M.; Rezaei, F.; Chalechale, A. Prevalence, intensity, and pathological lesions of Eimeria infection in goats in western Iran. Comp. Clin. Pathol. 2015, 24, 805–810. [Google Scholar] [CrossRef]
  35. Abo-Shehada, M.N.; Abo-Farieha, H.A. Prevalence of Eimeria species among goats in northern Jordan. Small Rumin. Res. 2003, 49, 109–113. [Google Scholar] [CrossRef]
  36. Hassanen, E.A.; Anter, R.G.; El-Neshwy, W.M.; Elsohaby, I. Prevalence and phylogenetic analysis of Eimeria species in sheep and goats in Sharkia Governorate, Egypt. Pak. Vet. J. 2020, 40, 437–442. [Google Scholar] [CrossRef] [PubMed]
  37. Kaur, S.; Singla, L.; Sandhu, B.; Bal, M.; Kaur, P. Coccidiosis in goats: Pathological observations on intestinal developmental stages and anticoccidial efficacy of amprolim. Indian J. Anim. Res. 2019, 53, 245–249. [Google Scholar] [CrossRef]
  38. Agyei, A.; Odonkor, M.; Osei-Somuah, A. Concurrence of Eimeria and helminth parasitic infections in West African Dwarf kids in Ghana. Small Rumin. Res. 2004, 51, 29–35. [Google Scholar] [CrossRef]
  39. Lim, J.J.; Kim, D.H.; Lee, J.J.; Kim, D.G.; Kim, S.H.; Min, W.; Chang, H.H.; Rhee, M.H.; Kim, S. Prevalence of Lawsonia Intracellularis, Salmonella Spp. Eimeria Spp. Healthy Diarrheic Pet Rabbit. J. Vet. Med Sci. 2012, 74, 263–265. [Google Scholar] [PubMed]
  40. Dixit, A.K.; Das, G.; Baghel, R.P.S. Gastrointestinal helminthosis: Prevalence and associated determinants in goats of Jabalpur, India. J. Parasit. Dis. 2017, 41, 414–416. [Google Scholar] [CrossRef] [PubMed]
  41. Terefe, D.; Demissie, D.; Beyene, D.; Haile, S. A prevalence study of internal parasites infecting Boer goats at Adami Tulu agricultural research center, Ethiopia. J. Vet. Med. Anim. Health 2012, 4, 12–16. [Google Scholar]
  42. Mpofu, T.J.; Nephawe, K.A.; Mtileni, B. Prevalence of gastrointestinal parasites in communal goats from different agro-ecological zones of South Africa. Vet. World 2020, 13, 26. [Google Scholar] [CrossRef] [PubMed]
  43. Njuki, P.; Kagira, J.; Mhoma, R. Prevalence and intensity of endoparasites in small ruminants kept by farmers in Kisumu Municipality, Kenya. Livest. Res. Rural. Dev. 2009, 21, 11. [Google Scholar]
  44. Gadahi, J.; Arshed, M.; Ali, Q.; Javaid, S.; Shah, S. Prevalence of gastrointestinal parasites of sheep and goat in and around Rawalpindi and Islamabad, Pakistan. Vet. World 2009, 2, 51. [Google Scholar]
  45. Yusof, A.M.; Isa, M.L.M. Prevalence of gastrointestinal nematodiasis and coccidiosis in goats from three selected farms in Terengganu, Malaysia. Asian Pac. J. Trop. Biomed. 2016, 6, 735–739. [Google Scholar] [CrossRef]
  46. Soulsby, E.J. Helminths, Arthropods and Protozoa of Domesticated Animals, 6th ed.; Baillière Tindall & Cassell: Arlington, VA, USA, 1968. [Google Scholar]
  47. Manfredi, M.T.; Di Cerbo, A.R.; Zanzani, S.; Stradiotto, K. Breeding management in goat farms of Lombardy, northern Italy: Risk factors connected to gastrointestinal parasites. Small Rumin. Res. 2010, 88, 113–118. [Google Scholar] [CrossRef]
  48. Osman, F. Incidence of internal parasites of desert goats in New Valley, Egypt. Assiut Vet. Med. J. 2009, 55, 1–10. [Google Scholar]
  49. Pienaar, J.; Basson, P.; Du Plessis, J.; Collins, H.M.; Naude, T.; Boyazoglu, P.; Reyers, F.; Pienaar, W.; Boomker, J.D.F. Experimental studies with Strongyloides papillosus in goats. Onderstepoort J. Vet. Res. 1999, 66, 191–235. [Google Scholar] [PubMed]
  50. Kyriánová, I.A.; Vadlejch, J.; Kopeckỳ, O.; Langrová, I. Seasonal dynamics of endoparasitic infections at an organic goat farm and the impact of detected infections on milk production. Parasitol. Res. 2017, 116, 3211–3219. [Google Scholar] [CrossRef] [PubMed]
  51. Lopez, A.; Martinson, S.A. Respiratory system, mediastinum, and pleurae. Pathol. Basis Vet. Dis. 2017, 471–560.e1. [Google Scholar] [CrossRef]
  52. Islam, K.; Taimur, M. Helminthic and protozoan internal parasitic infections in free ranging small ruminants of Bangladesh. Slov. Vet. Res. 2008, 45, 67–72. [Google Scholar]
  53. Ashraf, M.; Nepote, K. Prevalence of gastrointestinal nematodes, coccidia and lungworms in Maryland dairy goats. Small Rumin. Res. 1990, 3, 291–298. [Google Scholar] [CrossRef]
  54. Béjar González, J.P.; Díaz, P.; Pérez, A.; Prieto, A.; Panadero Fontán, R.; Fernández, G.; López Lastra, C.; Díez Baños, P.; Morrondo Valdeolmillos, P. Infecciones por nematodos broncopulmonares en ganado caprino en la comunidad gallega. In Proceedings of the XXXIX Congreso Nacional de la Sociedad Española de Ovinotecnia y Caprinotecnia: XV Congreso Internacional, Teruel, Spain, 17–19 September 2014; pp. 406–411. [Google Scholar]
  55. Hussain, K. Epidemiological and Therapeutical Study of Internal Parasites Infestation in Native Goats in Mosul Region. Ph.D. Thesis, College of Veterinary Medicine, University of Mosul, Mosul, Iraq, 2005. [Google Scholar]
  56. Shakun, J.D.; Burns, S.J.; Fleitmann, D.; Kramers, J.; Matter, A.; Al-Subary, A. A high-resolution, absolute-dated deglacial speleothem record of Indian Ocean climate from Socotra Island, Yemen. Earth Planet. Sci. Lett. 2007, 259, 442–456. [Google Scholar] [CrossRef]
  57. Maděrová, L.; Šipoš, J.; Maděra, P.; Suchomel, J. Socioeconomic importance of the semi-feral goat population for smallholders on the island of Socotra. Trop. Anim. Health Prod. 2024, 57, 1–20. [Google Scholar] [CrossRef] [PubMed]
  58. Maity, M.; Vineetha, S.; Sahoo, M.; Nandi, A.; Sardana, S. Mixed intestinal parasitic infection in kid: A case report. Explor. Anim. Med. Res. 2018, 8, 120–122. [Google Scholar]
  59. Ghimire, T.R.; Bhattarai, N. A survey of gastrointestinal parasites of goats in a goat market in Kathmandu, Nepal. J. Parasit. Dis. 2019, 43, 686–695. [Google Scholar] [CrossRef] [PubMed]
  60. Cai, W.; Cheng, C.; Feng, Q.; Ma, Y.; Hua, E.; Jiang, S.; Hou, Z.; Liu, D.; Yang, A.; Cheng, D.; et al. Prevalence and risk factors associated with gastrointestinal parasites in goats (Capra Hircus) Sheep (Ovis Aries) Three Prov. China. Front. Microbiol. 2023, 14, 1287835. [Google Scholar] [CrossRef] [PubMed]
  61. Nwosu, C.; Ogunrinade, A.; Fagbemi, B. Prevalence and seasonal changes in the gastro-intestinal helminths of Nigerian goats. J. Helminthol. 1996, 70, 329–333. [Google Scholar] [CrossRef] [PubMed]
  62. Pandey, V.; Ndao, M.; Kumar, V. Seasonal prevalence of gastrointestinal nematodes in communal land goats from the highveld of Zimbabwe. Vet. Parasitol. 1994, 51, 241–248. [Google Scholar] [CrossRef] [PubMed]
  63. Das, M.; Laha, R.; Goswami, A. Gastrointestinal parasitism of goats in hilly region of Meghalaya, India. Vet. World 2017, 10, 81. [Google Scholar] [CrossRef] [PubMed]
  64. Lata, K.; Das, G.; Kumbhakar, N.; Saiyam, R. Prevalence of gastrointestinal parasites of goats in and around Jabalpur, Madhya Pradesh. Indian J. Vet. Sci. Biotechnol. 2017, 13, 21–25. [Google Scholar] [CrossRef]
  65. Dappawar, M.; Khillare, B.; Narladkar, B.; Bhangale, G. Prevalence of gastrointestinal parasites in small ruminants in Udgir area of Marathwada. J. Entomol. Zool. Stud 2018, 6, 672–676. [Google Scholar]
  66. Ogunsusi, R. Pasture infectivity with trichostrongylid larvae in the northern Guinea Savanna of Nigeria. Res. Vet. Sci. 1979, 26, 320–323. [Google Scholar] [CrossRef] [PubMed]
  67. Anene, B.; Onyekwodiri, E.; Chime, A.; Anika, S. Gastrointestinal parasites in sheep and goats of southeastern Nigeria. Small Rumin. Res. 1994, 13, 187–192. [Google Scholar] [CrossRef]
  68. Hossain, M.M. Prevalence of Gastrointestinal Parasitic Infections in Sheep of Subarnachar Upazilla in Noakhali District of Bangladesh. Ph.D. Thesis, University of Dhaka, Dhaka, Bangladesh, 2017. [Google Scholar]
  69. Vercruysse, J. A survey of seasonal changes in nematode faecal egg count levels of sheep and goats in Senegal. Vet. Parasitol. 1983, 13, 239–244. [Google Scholar] [CrossRef] [PubMed]
  70. Sissay, M.M.; Uggla, A.; Waller, P.J. Prevalence and seasonal incidence of larval and adult cestode infections of sheep and goats in eastern Ethiopia. Trop. Anim. Health Prod. 2008, 40, 387–394. [Google Scholar] [CrossRef] [PubMed]
  71. Nwosu, C.; Madu, P.; Richards, W. Prevalence and seasonal changes in the population of gastrointestinal nematodes of small ruminants in the semi-arid zone of north-eastern Nigeria. Vet. Parasitol. 2007, 144, 118–124. [Google Scholar] [CrossRef] [PubMed]
  72. Gebeyehu, E.; Seo, M.; Jung, B.; Byun, J.; Oem, J.; Kim, H.; Kwak, D. Prevalence of gastrointestinal parasites in Korean native goats (Capra Hircus Aegagrus). J. Anim. Plant Sci. 2013, 23, 986–989. [Google Scholar]
  73. Gana, J.; Makun, H.; Chiezey, N.; Tekdek, L. Epidemiological study on abomasal nematodes in slaughtered small ruminants raised in the guinea savannah zone of Nigeria. Sokoto J. Vet. Sci. 2015, 13, 26–33. [Google Scholar] [CrossRef]
  74. Okon, E.; Enyenihi, U. Development and survival of Haemonchus contortus larvae on pastures in Ibadan. Trop. Anim. Health Prod. 1977, 9, 7–10. [Google Scholar] [CrossRef]
  75. Foreyt, W.J. Coccidiosis and cryptosporidiosis in sheep and goats. Vet. Clin. N. Am. Food Anim. Pract. 1990, 6, 655–670. [Google Scholar] [CrossRef]
  76. Castanheira, M.; Paiva, S.R.; Louvandini, H.; Landim, A.; Fiorvanti, M.C.S.; Dallago, B.S.; Correa, P.S.; McManus, C. Use of heat tolerance traits in discriminating between groups of sheep in central Brazil. Trop. Anim. Health Prod. 2010, 42, 1821–1828. [Google Scholar] [CrossRef] [PubMed]
  77. Bebe, B.; Udo, H.; Thorpe, W. Characteristics of feeding and breeding practices for intensification of smallholder dairy systems in the Kenya highlands. Livest. Res. Rural. Dev. 2008, 20, 1–13. [Google Scholar]
  78. Aguirre-García, M.M.; Rojas-Bernabé, A.; Gómez-García, A.P.; Escalona-Montaño, A.R. TLR-mediated host immune response to parasitic infectious diseases. In Toll-Like Receptors; IntechOpen: London, UK, 2020. [Google Scholar]
  79. Wamae, L.; Ihiga, M. Seasonal faecal egg count changes in Kenyan goats through a one-year period. Bull. Anim. Health Prod. Afr. 1990, 38, 1–4. [Google Scholar]
  80. Khan, M.; Rehman, T.; Iqbal, Z.; Sajid, M.; Ahmad, M.; Riaz, M. Prevalence and associated risk factors of Eimeria in sheep of Punjab, Pakistan. World Acad. Sci. Eng. Technol. 2011, 5, 334–338. [Google Scholar]
  81. Sorathiya, L.; Fulsoundar, A.; Rao, T.; Kumar, N. Prevalence and risk factors for gastrointestinal parasitism in traditionally maintained goat flocks of South Gujarat. J. Parasit. Dis. 2017, 41, 137–141. [Google Scholar] [CrossRef] [PubMed]
  82. Rehman, T.; Khan, M.; Sajid, M.; Iqbal, Z.; Javid, M.; Riaz, M.; Ahmad, M. Epidemiology of Eimeria and associated risk factors in goats of district Toba Tek Singh, Pakistan. Indian J. Anim. Sci. 2012, 82, 282. [Google Scholar]
  83. Sharma, D.K.; Agrawal, N.; Mandal, A.; Nigam, P.; Bhushan, S. Coccidia and gastrointestinal nematode infections in semi-intensively managed Jakhrana goats of semi-arid region of India. Trop. Subtrop. Agroecosyst. 2009, 11, 135–139. [Google Scholar]
  84. Kusiluka, L.; Kambarage, D.; Harrison, L.; Daborn, C.; Matthewman, R. Prevalence and seasonal patterns of coccidial infections in goats in two ecoclimatic areas in Morogoro, Tanzania. Small Rumin. Res. 1998, 30, 85–91. [Google Scholar] [CrossRef]
  85. Zvinorova, P.; Halimani, T.; Muchadeyi, F.; Matika, O.; Riggio, V.; Dzama, K. Prevalence and risk factors of gastrointestinal parasitic infections in goats in low-input low-output farming systems in Zimbabwe. Small Rumin. Res. 2016, 143, 75–83. [Google Scholar] [CrossRef]
  86. Ndlela, S.; Mkwanazi, M.; Chimonyo, M. Relationship between faecal egg count and health status in Nguni goats reared on semi-arid rangelands. Trop. Anim. Health Prod. 2023, 55, 138. [Google Scholar] [CrossRef] [PubMed]
  87. Díez-Baños, P.; Morrondo-Pelayo, P.; Feijoo-Penela, A.; Carrillo-González, B.; López-Sández, C. Relationship between the excretion of protostrongylid larvae in sheep in North-west Spain and climatic conditions. J. Helminthol. 1994, 68, 197–201. [Google Scholar] [CrossRef] [PubMed]
  88. Sutherland, K.; Ndlovu, M.; Pérez-Rodríguez, A. Use of artificial waterholes by animals in the southern region of the Kruger National Park, South Africa. Afr. J. Wildl. Res. 2018, 48, 1–14. [Google Scholar] [CrossRef]
  89. Titcomb, G.; Mantas, J.N.; Hulke, J.; Rodriguez, I.; Branch, D.; Young, H. Water sources aggregate parasites with increasing effects in more arid conditions. Nat. Commun. 2021, 12, 7066. [Google Scholar] [CrossRef] [PubMed]
  90. Bellard, C.; Genovesi, P.; Jeschke, J.M. Global patterns in threats to vertebrates by biological invasions. Proc. R. Soc. B Biol. Sci. 2016, 283, 20152454. [Google Scholar] [CrossRef] [PubMed]
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Figure 1. Frequency of occurrence of individual parasite species in goats on Socotra. The graph displays the prevalence of various parasite species found in feral goat populations on Socotra Island, represented as a percentage of the total number of detected parasites. Each bar indicates the relative frequency of each species.
Figure 1. Frequency of occurrence of individual parasite species in goats on Socotra. The graph displays the prevalence of various parasite species found in feral goat populations on Socotra Island, represented as a percentage of the total number of detected parasites. Each bar indicates the relative frequency of each species.
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Figure 2. Frequency of co-infection occurrences in goats on Socotra. The graph illustrates the distribution of various co-infections observed among the feral goat populations on Socotra Island. Each bar indicates the absolute frequency of occurrence of each type of co-infection. None = no infections; single = one infection; double = two infections; triple = three infections; quadruple = four infections; quintuple = five infections.
Figure 2. Frequency of co-infection occurrences in goats on Socotra. The graph illustrates the distribution of various co-infections observed among the feral goat populations on Socotra Island. Each bar indicates the absolute frequency of occurrence of each type of co-infection. None = no infections; single = one infection; double = two infections; triple = three infections; quadruple = four infections; quintuple = five infections.
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Figure 3. Impact of seasonality on parasite species composition. Partial canonical correspondence analysis (pCCA), with sampling year and locality as covariates, showed the association between the distribution of parasite taxa and season. The significance of the ordination axes was tested using a restricted Monte Carlo permutation test, in which randomization was constrained by maintaining the temporal autocorrelation of individual records through separate cyclic shifts within each locality. The analysis of species abbreviations revealed a partial variation of 1.03867. Explanatory variables accounted for 3.01% of the total variation, with an adjusted explained variation of 2.42%.
Figure 3. Impact of seasonality on parasite species composition. Partial canonical correspondence analysis (pCCA), with sampling year and locality as covariates, showed the association between the distribution of parasite taxa and season. The significance of the ordination axes was tested using a restricted Monte Carlo permutation test, in which randomization was constrained by maintaining the temporal autocorrelation of individual records through separate cyclic shifts within each locality. The analysis of species abbreviations revealed a partial variation of 1.03867. Explanatory variables accounted for 3.01% of the total variation, with an adjusted explained variation of 2.42%.
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Figure 4. Impact of relief and seasonality on parasite species composition. Partial canonical correspondence analysis (pCCA) with sampling year and locality as covariates showed the distribution of parasite taxa in relation to the combination of seasonality and altitude. The significance of the ordination axes was tested using a restricted Monte Carlo permutation test, in which randomization was constrained by maintaining the temporal autocorrelation of individual records through separate cyclic shifts within each locality. The analysis of species abbreviations revealed a partial variation of 1.03867. Explanatory variables accounted for 5.12% of the total variation, with an adjusted explained variation of 3.97%.
Figure 4. Impact of relief and seasonality on parasite species composition. Partial canonical correspondence analysis (pCCA) with sampling year and locality as covariates showed the distribution of parasite taxa in relation to the combination of seasonality and altitude. The significance of the ordination axes was tested using a restricted Monte Carlo permutation test, in which randomization was constrained by maintaining the temporal autocorrelation of individual records through separate cyclic shifts within each locality. The analysis of species abbreviations revealed a partial variation of 1.03867. Explanatory variables accounted for 5.12% of the total variation, with an adjusted explained variation of 3.97%.
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Figure 5. Dry lagoons during the dry season on Socotra. Photo by Lucie Maděrová, Socotra, 2021.
Figure 5. Dry lagoons during the dry season on Socotra. Photo by Lucie Maděrová, Socotra, 2021.
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Table 1. Information on excreta samples collected from goats on Socotra Island, Yemen.
Table 1. Information on excreta samples collected from goats on Socotra Island, Yemen.
Number of GoatsYearLocationReliefSeason
402021Shibonhighlanddry
52021Firmihinhighlanddry
52021Ayhefthighlanddry
392021Shatalowlanddry
112021Erhinolowlanddry
262021Shibonhighlandrainy
242021Ayhefthighlandrainy
152021Homehilhighlandrainy
352021Shatalowlandrainy
292022Shibonhighland-
162022Firmihinhighland-
82022Momihighland-
102022Máalehhighland-
132022Matáarasmhighland-
42022Ganegheneytenhighland-
282022De notitlowland-
82022Hadibolowland-
192022Terbeklowland-
162022Dirhamlowland-
272022Takeslowland-
72022Homehilhighland-
212022Ayhefthighland-
Table 2. Parasites grouped based on their routes of infection [10,31].
Table 2. Parasites grouped based on their routes of infection [10,31].
ParasiteRoutes of InfectionDetails
Eimeria spp.Food-borne/EnvironmentInfection occurs via ingestion of sporulated oocysts from contaminated food, water, or surfaces.
StrongylidsSoil-transmittedLarvae penetrate the skin or are ingested from contaminated soil or pastures.
Trichuris spp.Soil-transmittedEggs are ingested from contaminated soil, vegetation, or water.
Strongyloides sp.Soil-transmittedInfective larvae penetrate the skin or are ingested; moisture facilitates survival.
Muellerius spp.Vector-borne (gastropods)Infection involves ingestion of terrestrial gastropods hosting larvae.
ProtostrongylidaeVector-borne (gastropods)Requires ingestion of gastropods (slugs or snails) as intermediate hosts.
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Maděrová, L.; Šipoš, J.; Maděra, P.; Modrý, D.; Červená, B.; Suchomel, J. First Coprological Survey of Semiferal Goat (Capra hircus) Parasites in Relation to Environmental Factors on the Island of Socotra, Yemen. Agriculture 2025, 15, 475. https://doi.org/10.3390/agriculture15050475

AMA Style

Maděrová L, Šipoš J, Maděra P, Modrý D, Červená B, Suchomel J. First Coprological Survey of Semiferal Goat (Capra hircus) Parasites in Relation to Environmental Factors on the Island of Socotra, Yemen. Agriculture. 2025; 15(5):475. https://doi.org/10.3390/agriculture15050475

Chicago/Turabian Style

Maděrová, Lucie, Jan Šipoš, Petr Maděra, David Modrý, Barbora Červená, and Josef Suchomel. 2025. "First Coprological Survey of Semiferal Goat (Capra hircus) Parasites in Relation to Environmental Factors on the Island of Socotra, Yemen" Agriculture 15, no. 5: 475. https://doi.org/10.3390/agriculture15050475

APA Style

Maděrová, L., Šipoš, J., Maděra, P., Modrý, D., Červená, B., & Suchomel, J. (2025). First Coprological Survey of Semiferal Goat (Capra hircus) Parasites in Relation to Environmental Factors on the Island of Socotra, Yemen. Agriculture, 15(5), 475. https://doi.org/10.3390/agriculture15050475

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