The good, the bad and the ugly: Emys trinacris, Placobdella costata and Haemogregarina stepanowi in Sicily (Testudines, Annelida and Apicomplexa)

Abstract

Endemic Sicilian pond turtles Emys trinacris Fritz, Fattizzo, Guicking, Tripepi, Pennisi, Lenk, Joger et Wink were examined for the presence of haemogregarine parasites. The presence of haemogregarines, occurring mainly in the microgametocyte stage (13.2 ± 0.12 μm in length and 6.4 ± 0.52 μm in width), was observed in approximately 9% of the sampled E. trinacris. Based on the observed morphology and on the sequencing of nuclear 18S rDNA, we identified the parasite as Haemogregarina stepanowi Danilewsky, 1885. Morphometric study of uninfected and infected red blood cells has shown that H. stepanowi induces different changes in erythrocyte shape depending on the infective stage. The differential count of leukocytes in specimens infected with H. stepanowi showed no significant difference compared with healthy specimens. However, considering the health problems which might be induced by H. stepanowi in the closely related European pond turtle Emys orbicularis (Linneaus), monitoring of the health status of the infected Sicilian populations of E. trinacris is desirable. The restricted distribution of populations of Emys infected with haemogregarines in Sicily is quite puzzling and the possible human-mediated introduction of the parasite in Sicily is briefly discussed.

Haemogregarina podocnemis sp. nov.: description of a new species of Haemogregarina Danilewsky 1885 (Adeleina: Haemogregarinaidae) in free-living and captive yellow-spotted river turtles Podocnemis unifilis (Testudines: Podocnemididae) from Brazil

“…There are no sequences of Haemogregarina species from Brazilian turtles deposited in GenBank. The sequences available are from H. stepanowi (Dvoráková et al 2013;Ozvegy et al 2015;Arizza et al 2016), H. pellegrini (Dvoráková et al 2015), H. balli (Barta et al 2012), and H. sacaliae (Dvoráková et al 2015) obtained in different countries. Other sequences available in GenBank identified the genus Haemogregarina only.…”

Molecular detection of hemogregarines and haemosporidians in Brazilian free-living testudines

“…In this study, the capture of P. expansa coincided with the end of the dry season and the beginning of the rainy season, which would explain the absence of leeches in the sampled animals. Leeches are incriminated vectors of hemogregarines among aquatic reptiles ( Brites and Rantin, 2004 , Jacobson, 2007 , Dvořáková et al, 2014 , Dvořáková et al, 2015 , Arizza et al, 2016 ).…”

“…(Hepatozoidae) ( Soares et al, 2017 ) and Haemogregarina spp. (Haemogregarinidae) ( Jakes et al, 2001 , Telford et al, 2009 , Davis and Sterrett, 2011 , Pineda-Catalan et al, 2013 , Rossow et al, 2013 , Dvořáková et al, 2014 , Dvořáková et al, 2015 , Picelli et al, 2015 , Arizza et al, 2016 , Rakhshandehroo et al, 2016 )]. With regard to haemosporidians, while Haemoproteus spp.…”

“…Molecular investigations of hemogregarines in testudines are mainly based on the 18S ribosomal RNA gene ( Wozniak et al, 1994 ). Phylogenetic inferences of hemogregarines have already been made based on biological samples of testudines and vectors ( Harris et al, 2013 , Dvořáková et al, 2014 , Dvořáková et al, 2015 , Kvičerová et al, 2014 , Arizza et al, 2016 , Rakhshandehroo et al, 2016 ). For instance, Hemolivia spp.…”

“…Haemogregarina spp. were characterized molecularly from blood samples from freshwater turtles in Canada ( Barta et al, 2012 ), the Middle East (Turkey, Syria, and Iran) ( Dvořáková et al, 2014 , Rakhshandehroo et al, 2016 ), North Africa (Morocco, Algeria) ( Dvořáková et al, 2014 ), Southeast Asia (Vietnam, Indonesia, Thailand, and China) ( Dvořáková et al, 2015 ), and Europe (Bulgaria and Italy) ( Dvořáková et al, 2014 , Arizza et al, 2016 ). In South America, DNA from hemogregarines have been detected by PCR in blood samples from captive freshwater turtles [Geoffroy's side-necked turtle (Chelidae: Phrynops geoffroanus ) and the Giant Amazon turtle (Podocnemididae: Podocnemis expansa )] in Brazil ( Pessoa et al, 2016 ) and molecularly characterized from blood samples of wild Scorpion Mud turtles ( Kinosternon scorpioides ) in the Brazilian Amazon ( Soares et al, 2017 ).…”