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Prevalence and intensity of gastrointestinal parasites in the vulnerable spur-thighed tortoise (Testudo graeca) from the central-western of Morocco

Authors:
El Hassan El Mouden at Cadi Ayyad University
El Hassan El Mouden
El-Mustapha Laghzaoui
El-Mustapha Laghzaoui
Omar Amahmid at Regional Centre for Careers of Education and Training, CRMEF Marrakesh / University Cadi Ayyad, Faculty of Sciences Semlalia (Associate Researcher) - Marrakesh, Morocco.
Omar Amahmid
  • Regional Centre for Careers of Education and Training, CRMEF Marrakesh / University Cadi Ayyad, Faculty of Sciences Semlalia (Associate Researcher) - Marrakesh, Morocco.
Abdelaziz Abbad at Cadi Ayyad University
Abdelaziz Abbad
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Abstract and Figures

This study was undertaken to determine the prevalence and intensity of gastrointestinal parasites in wild Testudo graeca tortoises in Morocco. A total of 102 tortoises sampled in two arid areas: Central Jbilets Mountains (CJM) and Sidi Kaouki Forest (SKF) were macroscopically examined and subjected to qualitative (flotation and Baermann techniques) and quantitative (McMaster technique) microscopic examinations. The identified gastrointestinal parasites belong to two nematode families (Pharyngodonidae and Ascarididae) and three protozoa families (Balantidiidae, Eimeriidae and Entamoebidae). 92.1% of tortoises were determined to harbor one or more parasite types. Oxyurid adults were the most frequently encountered with a prevalence of 22.7% and 72.4% in CJM and SKF, respectively. Nematode eggs were found in almost all individuals of both populations studied. The prevalence of protozoa was 9.1% and 3.4% in CJM and SKF, respectively. Oxyurid adults showed the highest intensity in SKF (36.5 ± 30.2) whereas, ascarid adults are absent in CJM. Statistical analysis showed that the prevalence of infection by ascarids was significantly higher in adults than in juveniles. The intensity of infection by ascarid and oxyurid eggs differed significantly between sexes and localities, respectively. Our results showed a difference of infection between the two localities, which could be in relation with habitat quality. SKF is affected by both agriculture and overgrazing. In addition, the tortoises from this locality are active for a large part of the year, which increases their chance of encountering the parasites.
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Basic and Applied Herpetology 35 (2021) 000-000
DOI: http://dx.doi.org/10.11160/bah.194
CITE THIS ARTICLE AS “IN PRESS”
Prevalence and intensity of gastrointestinal parasites in
the vulnerable spur-thighed tortoise (
Testudo graeca)
from the central-western of Morocco
El-Mustapha Laghzaoui1, Omar Amahmid1,2, Abdelaziz Abbad3, El Hassan El Mouden1*
1Laboratory of Water, Biodiversity and Climatic Change, Faculty of Sciences, Semlalia, Cadi Ayyad Univer-
sity, Marrakech, Morocco.
2Department of Life and Earth Sciences, Biology and Geology Research Units, Regional Centre for Careers
in Education and Training CRMEF-Marrakech, Marrakesh 40 000, Morocco.
3Laboratory of Microbial Biotechnologies, Agrosciences and Environment, Faculty of Sciences Semlalia,
Cadi Ayyad University, Marrakech, Morocco.
*Correspondence: E-mail: elmouden@uca.ac.ma
Received: 30 June 2020; returned for review: 02 December 2020; accepted 14 January 2021.
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

-  Te stud o graeca

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      -
     
et alet al
  -   
-
     
et al

 et al  
LAGHZAOUI ET AL.
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    
      
 
       

et
al  
    
     

    
 et al    etal
etaletal
etal
-

  
  
   et al  
-et al
    
    
T. graeca

   
   
etal
     
  

 
-et al 
      

     


    

    
      
     
et al
et al
    
-
     
 - et al  
    

et al.
 et al et al
et al.
   
  et al  
 et al -
et al

- , ;  et
al.   et al  
et al   et al  
      

    
   et al 


    
 -T. graeca  
      
     
     
      
 -    


Study areas
      
      
      

GASTROINTESTINAL PARASITES IN TESTUDO GRAECA
3
       
       
        

       
    
      
 Ziziphus lo tus
Retama mo nosp erm a
    
     
     
      
  et al.    et
alet al
     
   
    et al
  
    
    
     
   et al   
     
 Argania spino sa

     Ch am aero p s
humilis  
      
  
     
 
     
     
T. grae ca 

LAGHZAOUI ET AL.
4
     et al.

    T. graeca 
       

     et al.

Sampling methods

T. graeca 


       
   
et al   
   



     

      

Parasitological analysis
    
      
  
      


   

    
     

     
    
       
   - 


    -
   
      

 
     
     
    
    

   


     
      


   
      
      

      

     
      


     

Statistical analysis
     
    

     
   
     
     
-
GASTROINTESTINAL PARASITES IN TESTUDO GRAECA
5
    
 
    
      
      
       -
    




     

    

   
    




     

      
     


     

     
      
      
     
    
Χ
       
    

 Χ       
     
    
  



      

     
       
     
   
Χ
  Χ        
Χ
   
T. grae ca   

  
 Entamoeba     
  Balantidium   Eimeria 

LAGHZAOUI ET AL.
6


        
        

      
     
      


       
      
   
 ’ᵞ       
     
’ᵞ
      
    
’ᵞ
    
’ᵞ

    Balan-
tidium       
       



Eim e ria
      
Entamoe ba

 

     

      

Entamoe ba

     
Eime riaBalan-
tidium Entamoeba    

 
       
      

        
    
        
        

Balantidium cysts     
Eimeria  
Entamoeba       
 T. g raeca 

GASTROINTESTINAL PARASITES IN TESTUDO GRAECA
7
 
       
      

         
 - - - - - - - -
     
 - - -
            
 - 3250 12 717 - - - - - -
         
  -  - - - - -

Balantidium  
     

Eimeriaoocysts
  
 -
Entamoeba
       
 - - - - -
  T. grae ca  

LAGHZAOUI ET AL.
8


     
     
     
    
   
       
    -


     
      
    
et al. et al

       
    

    T. grae ca   
      

      
 et al.,    
   Tachygo netria den-
tata T. longicollis     T.
seuratiThaparia thapariet al.
     
 

   et al
     
     
     
 

     
   
   et al  -
et al

    et al
 et al.
    
    
    
      
et al
      
  - 
       
       
     
   
et al    

     



et al
      

     
      
     et al
     
      
    
    
   -  
     
   - et al
 
  -

     
     
  
      
      
et al.
GASTROINTESTINAL PARASITES IN TESTUDO GRAECA
9
    
et al
 
  et al.    
     
      
     
      
       
      
     
    
      
 - T. graeca  
 etal    


    
et al
     
    
    
 et al.     



     
      
     
     
et al
et al  -
    -
     
  
et al     
    
    
et
al   Balantidium  

     
et al.    

     et al
 et al 
    
       
   - 
et al
     
Geo chelo ne e le gans
   Balantid ium  
et alEntamoe-
ba 
E. invad e ns
   et al  
     
     
    
  - 
     
Eimeria   
      
      -
  -  
  Eim eria sp.  

       
     
Eimeria sp.     
     
 et alet al.
      
  
     

   
    
      
-et al
 et al     
LAGHZAOUI ET AL.
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     
   
      
    
    
      
       
  et al.    
- et al.  

    
    
     
     
    
      
  
      
     -
et al 
  
      
   et al.  
et al.       
      
   
et al
Acknowledgments
     “ 

   ”  
   
     
-

-
     
Türkiye Parazitoloji Dergisi. 31: 330336.
      
       

 Proceedings of th e Ro yal
Society of London. 269: 16251632.
     
      
     
     

Te stud o grae ca
  
Amphibia-Reptilia. 33: 285296.
-
      
 Testudo graeca graeca 
Manouria. 7: 1718.

    
Journal of Exotic Pet
Medicine. 31: 512.
   Biodémographie et écologie
d’ une population de Testudo graeca graeca
L. 1758 (Chelonia : Testudinidae) dans
l’Arganeraie d’Essaouira (Maroc atlan-
tique) 

      
      
     
    
  Testudo graeca grae-
caAmphibia-Reptilia. 26: 113115.
      
      
    
     
Testud o g. grae ca
  Revue d'Ecolo gie
(Terre Vie). 60: 265278.
     
      
GASTROINTESTINAL PARASITES IN TESTUDO GRAECA
11


 Chelonian Conservation and
Biology. 7: 2127.
      
      
   

Te stud o grae ca   
Vie Milieu 56: 4954.
-    
 

     
   - 
Jo urnal o f Eco logy. 106: 2204
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-
-  
 -  
  
    
   
 -  Te stud o
graecaPeer Journal. 126.
      
    
-    Alae uris
seurat
Alaeuris num idica
  Jo urnalParasitolgy. 87:
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      
   Me h d iella
microstoma    Mehdiella
peerae
 Mehdie lla Seurat 
  Fo lia
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      
  
Mehdiella
  

Parasite. 10: 333342.

       
Tachygonetria   
  
     
Zo o system a . 27: 193209.
      
     
    
   Jour-
nal of Herpetological Medicine and Sur-
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
  - 
      
    
    -
 Testudo graeca  
     
VeterinaryParasito-
logy. 187: 491497.
  -  
       
 -
 Testud o graeca  
-PLo S One.
14: 112.
   -
     
Te stud o grae caJournal of Herpeto-
logical Medicine and Surgery. 14: 45.
 -   Flore
fongique cutanée et parasitisme digestif des
tortues terrestres: étude d’une population
composée de Testudo hermannii, T. graeca
et T. horseldii.
      
LAGHZAOUI ET AL.
12

Testudo graeca graeca
      
 Journal of Arid
Environments. 64: 422435.
    - 
        
    
Te stud o graeca 
-  Hyalo mma ae -
gyptium   International
Journal of Acarology. 46: 6365.
     

      
   
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
  
     
Go pherus po lyp he-
mus  
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    
GASTROINTESTINAL PARASITES IN TESTUDO GRAECA
13
      
 Advancesin Research. 8: 1

      
    
     
    
     
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      
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    

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14
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
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... All coprological examinations were carried out within 24 h after sampling, according to the protocol described by (Laghzaoui et al. 2021b). The individual fecal samples were macroscopically examined for the possible detection of adult parasites. ...
Enteric parasites in free-living Mediterranean pond turtle (Mauremys leprosa leprosa) in contrasted areas (naturel vs polluted) from central-western of Morocco
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Full-text available
  • Mar 2023
The objective of this study is to assess the occurrence of intestinal parasites in Mediterranean pond turtle Mauremys leprosa leprosa collected from three contrasting environments in Morocco. Stool samples from 92 turtles were examined for parasite detection and enumeration. The identified intestinal parasites belong to helminths (Oxyurids and Ascarid) and protozoa (Entamoebidae). 27.17% of turtles were found to be infected by helminths and/or protozoan parasites. No adult form of these parasites has been detected. Oxyurid and ascarid eggs were found in individuals of populations studied from Oued Ksob (23.07% - 30.76%) and Oued Zat (34.14% - 24.39%), respectively. For protozoa, Entamoeba cysts were common in turtles in Oued Ksob (15.38%), Oued Zat (12.19%) and Oued Tensift (5.26%) localities. Oxyurid eggs showed the highest intensity at Oued Zat reaching 29.30 ± 59.59 EPG, versus 12 ± 0.38 EPG for Ascaris eggs in Oued Ksob. Entamoeba cysts were detected in lower levels with a maximum of 1.66 ± 1.50 CPG, in Oued Zat. The prevalence of turtles eliminating eggs was statistically significant between localities for different parasite groups. This study reports for the first time a parasitological characterization of gastro-intestinal parasites in wild populations of M. leprosa leprosa from contrasting environments, suggesting a relationship between turtles’ infestation and the quality of their living environment.
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Enteric parasites in free-living Mediterranean pond turtle (Mauremys leprosa leprosa) in contrasted areas (natural vs polluted) from central-western of Morocco
Article
Full-text available
  • Mar 2024
  • ENVIRON SCI POLLUT R
The objective of this study is to assess the occurrence of intestinal parasites in Mediterranean pond turtle Mauremys leprosa leprosa collected from three contrasting environments in Morocco. Stool samples from 92 turtles were examined for parasite detection and enumeration. The identified intestinal parasites belong to helminths (oxyurids and ascarid) and protozoa (Entamoebidae). A total of 25 turtles (27.17%) were found to be infected by helminths and/or protozoan parasites. No adult form of these parasites was detected. Eggs of oxyurid and ascarid were detected in individuals of populations studied from Oued Ksob (23.07% and 30.76% of n = 13 turtles) and Oued Zat (34.14% and 24.39% of n = 41 turtles), respectively. For protozoa, Entamoeba cysts were present in turtles in Oued Ksob (15.38% of n = 13 turtles), Oued Zat (12.19% of n = 41 turtles), and Oued Tensift (5.26% of n = 38 turtles) localities. Oxyurid eggs showed the highest intensity at Oued Zat reaching 29.30 ± 59.59 eggs per gram (EPG), versus 12 ± 0.38 EPG for ascaris eggs in Oued Ksob. Entamoeba cysts were detected in lower levels with a maximum of 1.66 ± 1.50 cysts per gram (CPG), in Oued Zat. The prevalence of turtles eliminating eggs was statistically significant between localities for different parasite groups. This study reports for the first time a parasitological characterization of gastrointestinal parasites in wild populations of M. leprosa leprosa from contrasting environments, suggesting a relationship between turtles’ infestation and the quality of their habitat.
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A case of massive infestation of a female Spur-thighed tortoise Testudo graeca by blood-sucking ticks Hyalomma aegyptium (Acari: Ixodidae)
Article
Full-text available
  • Dec 2019
Infestation by ticks affects several vertebrate groups, including tortoises. Testudo species are among chelonian fauna that are infested in their natural habitat by several tick species, with Hyalomma aegyptium as the dominant one. We report a heavy tick infestation found in female T. graeca in May 2018 in Had Draa (Essaouira region, Morocco). The female, with carapace length of 175 mm and body weight of 779.3 g was found to be infested by 288 H. aegyptium in different stages. It was more infested by female ticks than males, and the hind limbs (59.6%) and forelimbs (30.25%) were the most frequent predilection sites of ticks. Our data provide the first record of massive parasitism by H. aegyptium in this vulnerable and threatened tortoise.
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Population density of the spur-thighed tortoise Testudo graeca declines after fire in north-western Africa
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Fire is a key ecological process in several biomes worldwide. Over recent decades, human activities (e.g. rural abandonment, monoculture plantations) and global warming are magnifying the risk of fire, with changes in fire intensity and frequency. Here, we offer the first study that examines the impact of fire on the spur-thighed tortoise Testudo graeca living in a native cork oak forest and pine plantation in north-western Africa. A total of 44 transects (22 burnt and 22 unburnt) were sampled at 8 sites affected by fires of natural cork oak forest and pine plantation with 8 surveys per site in 2015–2017 (264 hours of sampling effort). Tortoise densities were estimated with line-transect distance sampling. The detection probability of tortoises was higher in burnt (0.915) than unburnt (0.474) transects. The density of tortoises was negatively associated with elevation and declined with fire by c. 50% in both forest types. The negative response of T. graeca to fire should be considered in conservation planning of this species in north-western Africa in a future scenario of changes in fire regime.
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A Survey of Gopherus polyphemus Intestinal Parasites in South Florida
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Full-text available
  • Dec 2018
Gopherus polyphemus populations are diminishing throughout their range due to urbanization, fragmentation, and poor habitat management. Increased population densities, poor habitat quality, and lack of fire may influence disease transmission. Parasite roles within wild tortoise populations are largely unknown; despite evidence these pathogens may pose significant health risks. This study provides a baseline of gopher tortoise intestinal parasites across South Florida and reports on how varying environmental and tortoise characteristics may affect intestinal parasite species prevalence and approximate loads. Tortoise fecal samples were taken from six tortoise populations across five South Florida sites. Seven species of intestinal parasites were discovered from 123 tortoises. Identified parasites include endohelminths such as cyathostomes, pinworms, ascarids, flukes, and protozoans including Eimeria , Cryptosporidium , and Amoeba species. Significant differences in parasite prevalence and loads were seen between sites, while parasitism among sex, size class, and habitat type remained relatively ubiquitous.
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Occurrence of health-compromising protozoan and helminth infections in tortoises kept as pet animals in Germany
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Full-text available
  • Jun 2018
Background: Exotic reptiles such as tortoises, have become increasingly common domestic pets worldwide and are known to host different gastrointestinal parasites. Some of these parasites bear zoonotic potential. In the present survey, we parasitologically examined tortoise faecal samples (n = 1005) from 19 different species held as pets in private German households and German zoological gardens. Methods: Saline faecal smears were used to generate prevalence data for potentially health-compromising gastrointestinal parasites. In addition, we performed complete parasitological dissections of dead tortoises (n = 49) to estimate endoparasite burdens precisely. Results: Analysed tortoise faecal samples contained a broad spectrum of endoparasites. We detected ten taxa of endoparasites; oxyurid nematodes (e.g. Tachygonetria spp.) were the most prevalent parasites in faecal samples (43.18%), followed by ascarids (Angusticaecum spp.) (0.01%), Hexamita spp. (0.007%), Balantidium spp. (0.007%), trichomonads (0.004%), Strongyloides spp. (0.003%), Entamoeba spp. (0.005%), Hartmanella spp. (0.001%), Blastocystis spp. (0.002%), heterakids (0.001%) and Trimitus spp. (0.001%). Additionally, we investigated dead tortoise individuals (n = 49; of 10 different species) for aetiological diagnosis and estimation of endoparasite burden. Of these individuals, 38 (77.6%) were infected with parasites and 14 (28.6%) of them died most probably due to severe parasitic infection. Oxyurid infections correlated positively with calcium deficiency and metabolic bone disease (MBD) as well as nephrosis/nephritis, mainly occurring in juvenile tortoises (< 5 years of age). Conclusions: The saline faecal smear technique proved to be efficient in detecting different metazoan and protozoan parasite stages in tortoise faeces. The prevalence of oxyurid infections was particularly high. In combination with pathological findings in clinical oxyuridosis obtained from necropsied animals, our findings call for further, detailed investigations on pathogenesis and immunology of oxyurids in pet reptiles. Coprological analyses for parasite detection should be mandatory before tortoises are transferred to a new owner, animal group, or public and private enclosures such as zoos. We advocate for regular health screenings in pet tortoises and, if parasitic infections are diagnosed, adequate medication or alternative hygiene management should be considered to improve and maintain individual and population health.
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Expansion after expansion: Dissecting the phylogeography of the widely distributed spur-thighed tortoise, Testudo graeca (Testudines: Testudinidae)
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Full-text available
  • Jun 2017
  • BIOL J LINN SOC
Studying phylogeographic histories in wide-ranging species provides key insights into those processes shaping current species’ distributions and genetic structuring. In this work, we extend previous sampling and analyse data from three mitochondrial genes to explore in-depth the phylogeography of the spur-thighed tortoise (Testudo graeca), the most widely distributed of Western Palearctic tortoise species. The combination of loci with different evolutionary rates and new fossil data in molecular clock analyses allow us to infer a dual diversification burst of the species, which took place since the Mio-Pliocene for the eastern subspecies and during the Pleistocene for the subspecies distributed in North Africa. The latter seems to correspond to a more or less contemporary diversification burst, which resulted in the current west–east allopatric/parapatric distribution of the North African lineages. In addition to the previously known genetic lineages, a new one was discovered in Libya. Within a more recent framework, we use estimates of genetic diversity and demographic inferences from molecular data to address the origin of three extant Western European populations. The comparison of their current genetic signatures supports the recent introduction of T. graeca into Majorca and Sardinia and an ancient origin of the populations in south-eastern Spain. The fossil history of T. graeca supports our findings from the most comprehensive and unifying phylogeographic study conducted to date for T. graeca. Our work highlights T. graeca as a paradigmatic system for studying phylogeographic processes that act in very different temporal and geographical contexts.
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Protozoa and protozoal infections in chelonians
Article
  • Jun 2019
  • J EXOT PET MED
Protozoa are common findings in chelonian practice, but the impact of many species on the animals’ health status is still inadequately known and understood. The present work aims to provide clinical, diagnostic and therapeutic updates on the main protozoan species that can infect turtles and tortoises: it covers many genera across amoebas (Entamoebidae), flagellates (Tritrichomonadida, Diplomonadida), ciliates (Ciliophora), cryptosporidia (Cryptosporidiidae), coccidia (Eimeriidae, Sarcocystiidae, Haemogregarinidae, Hepatozoidae, Karyolysidae), haemosporidians (Haemoproteidae), piroplasms (Piroplasmida) and trypanosomes (Trypanosomatidae). Brief biological and morphological features, epidemiology, diagnostic techniques, clinical behavior and pathological lesions are described. In order to avoid repetitions, therapy is presented and discussed as a self-standing paragraph at the end of the review.
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Effect of distance to edge and edge interaction on seedling regeneration and biotic damage in tropical rain forest fragments: A long-term experiment
Article
  • May 2018
In forest fragments, edge effects can influence forest regeneration, but little is known about how edge effects influence seedling performance and the interaction between seedlings and their natural enemies over time. In central Amazonia, we recorded survival and growth (in height and leaf number) and damage by insect herbivores and leaf‐fungal pathogens of Chrysophyllum pomiferum (Sapotaceae) seedlings that were exposed to different numbers of edges and to different distances from the forest edge. Grown seedlings were transplanted into one‐square‐metre plots within 1‐ha blocks located in the centre (no edge), the edge (one edge), and the corner (two edges), and at different distances from the edge towards the interior (i.e., 20, 40, 60, 80, and 100 m) of two rectangular fragments (10‐ and 100‐ha in size). Plots were visited once every 2 months for 1 year (1992–1993) and thereafter every 2 years for almost 8 years (1993–2001). Overall, results showed that seedling survival, height, leaf number, and biotic damage varied over time with the presence of nearby edges and with the distance from the edge. Survival was lower in fragment edges and corners than in centres. Increase in height was similar for all positions within the 100‐ha fragment, whereas in the 10‐ha fragment seedling height had a greater increase at the edge and corner than in the centre. Furthermore, survival increased with distance from the edge as did leaf number, whereas height showed a lower increase closer to the edge than farther away. Regarding biotic damage, for both fragments herbivory was greater at the centres and decreased with edge proximity over time, whereas leaf‐fungal damage was greater at the corners than in the edges and increased significantly over time. Biotic damage was correlated with seedling size. Small seedlings were more susceptible to fungal attack, whereas larger seedlings were so to herbivores. Synthesis . This study demonstrated that despite stochastic environmental factors seedling survival, growth, and biotic damage by herbivores and fungal pathogens varied with the level of edge exposure and proximity, which may threaten forest regeneration in the long term.
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Nematode-Associated Aural Abscess in a Mediterranean Tortoise, Testudo graeca
Article
  • Jan 2004
A thirty year old Mediterranean tortoise, Testudo graeca , was presented with a unilateral aural swelling. At surgery a nematode was removed along with casseonecrotic material.
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Internal and External Parasitic Infections of Pet Reptiles in Italy
Article
  • Dec 2016
In captive reptiles, parasites may represent a serious health and management problem for both the reptiles and their human caretakers (zoonotic parasites). In the present study, the prevalence of ecto- and endoparasitic infections and the clinical signs associated with these parasites were determined in pet reptiles living in Italy. To accomplish these aims, fecal samples collected from 120 captive reptiles representing 27 different species, including 63 household pet and 57 pet store reptiles, were analyzed macroscopically and microscopically for the isolation and identification of endoparasites. In addition, the reptiles, along with their terrariums and water containers, were also examined for ectoparasitic arthropods. Recovered arthropods were preserved in 80% ethanol and evaluated microscopically. Overall, 72.5% of the examined reptiles were found to be positive for parasites, with prevalence rates of 45% and of 27.5% for endo- and ectoparasites, respectively. Pet shop animals were more likel...
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