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      Long-term spatiotemporal stability and dynamic changes in the haemoparasite community of spiny mice ( Acomys dimidiatus) in four montane wadis in the St. Katherine Protectorate, Sinai, Egypt

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          Abstract

          Background

          Long-term field studies of parasite communities are rare but provide a powerful insight into the ecological processes shaping host-parasite interactions. The aim of our study was to monitor long-term trends in the haemoparasite communities of spiny mice ( Acomys dimidiatus) and to identify the principal factors responsible for changes over a 12 year period.

          Methods

          To this end we sampled four semi-isolated populations of mice ( n = 835) in 2000, 2004, 2008 and 2012 in four dry montane valleys (wadis) located in the Sinai Massif, Egypt.

          Results

          Overall 76.2 % of spiny mice carried at least one of the five haemoparasite genera ( Babesia, Bartonella, Haemobartonella, Hepatozoon, Trypanosoma) recorded in the study. Prevalence of haemoparasites varied significantly between the sites with the highest overall prevalence in Wadi Tlah and the lowest in W. El Arbaein, and this changed significantly with time. In the first two surveys there was little change in prevalence, but by 2008, when the first signs of a deepening drought in the region had become apparent, prevalence began to drift downwards, and by 2012 prevalence had fallen to the lowest values recorded from all four sites over the entire 12-year period. The overall mean species richness was 1.2 ± 0.03, which peaked in 2004 and then dropped by more than 50 % by 2012. Species richness was highest among mice from Wadi Tlah and peaked in age class 2 mice (young adults). Site was the most significant factor affecting the prevalence of individual parasite species, with Trypanosoma acomys and Hepatozoon sp. occurring mainly in two wadis (W. Tlah & W. Gharaba). In four of the five genera recorded in the study we observed a significant drop in prevalence or/and abundance since 2004, the exception being Hepatozoon sp .

          Conclusions

          During the 12-year-long period of study in the Sinai, we observed dynamic changes and possibly even cycles of prevalence and abundance of infections which differed depending on parasite species. Although the exact reasons cannot be identified at this time, we hypothesize that the effects of a 15-year-long scarcity of rainfall in the local environment and a fall in host densities over the period of study may have been responsible for a drop in transmission rates, possibly by a negative impact on vector survival.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s13071-016-1471-z) contains supplementary material, which is available to authorized users.

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          Most cited references41

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          The genus Hepatozoon (Apicomplexa: Adeleina).

          Hemogregarines of the genus Hepatozoon are intraerythrocytic apicomplexan parasites that have been described from all groups of tetrapod vertebrates. Gametogenesis, fertilization, and sporogonic development, which culminates in the formation of polysporocystic oocysts, occur in the gut or hemocoel of a hematophagous arthropod definitive host. Merogonic development occurs in the internal organs of vertebrate hosts after they ingest these infected arthropods. The presence of cystic stages, observed for many Hepatozoon species, increases life cycle complexity and exploits the feeding behavior of vertebrate hosts. The inconsistency of morphological characteristics of these parasites, especially those associated with gamont structure, coupled with low host specificity of the parasites for their invertebrate and vertebrate hosts, have rendered species differentiation difficult. A systematic review of the hemogregarine complex has resulted in the expansion of the genus Hepatozoon to include all members of the genus Haemogregarina that infect amphibians, snakes, lizards, crocodilians, birds, and mammals.
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            Analysis of the 18S rRNA gene sequence of a Hepatozoon detected in two Japanese dogs.

            Partial sequences of the 18S rRNA gene (625 bp) from a Hepatozoon detected in two canine hepatozoonosis cases, one clinical and one subclinical, in Japan were analyzed. Both sequences were identical to each other and they were closely related to the Hepatozoon canis strain found in Israel with 99% (617/625) nucleotide identity. Both Hepatozoon americanum and Hepatozoon catasbianae were distantly related to the Japanese Hepatozoon with 94% (586/625) and 91% (566/625) identities, respectively. In a phylogenetic tree, the Japanese Hepatozoon was most closely related to H. canis from Israel but was significantly different than H. americanum and H. catasbianae. These results suggest that the Hepatozoon detected in the Japanese dogs might be a strain variant of H. canis, but is apparently a different species than H. americanum.
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              A nested PCR for the ssrRNA gene detects Trypanosoma binneyi in the platypus and Trypanosoma sp. in wombats and kangaroos in Australia.

              Trypanosome infections in their natural hosts are frequently difficult to detect by microscopy, and culture methods are unreliable and not suitable for all species of Trypanosoma. A nested PCR strategy for detecting and identifying Trypanosoma species, suitable for detecting both known and unknown trypanosomes, is presented. Thirty-two blood samples from 23 species of Australian birds and mammals were screened by a nested PCR for the presence of Trypanosoma sp. ssrRNA. Three infections were detected, one in an eastern grey kangaroo (Macropus giganteus), one in a common wombat (Vombatus ursinus) and one in a platypus (Ornithorhynchus anatinus). The kangaroo and wombat are new host records for Trypanosoma sp.; the platypus parasite was Trypanosoma hinneyi. The three parasites could be distinguished by restriction fragment length polymorphisms of the amplified fragment of the ssrRNA gene. The kangaroo and wombat parasites were also isolated in a semi-solid blood agar medium. The culture forms of the kangaroo trypanosome had an expanded flagellar sheath in which structures similar to hemidesmosomes were detected by EM. The nested PCR was at least as sensitive as culture, and analysis of the PCR products gave parasite-specific fingerprints. Therefore this method could be suitable for rapidly screening host animals for the presence of trypanosomes and identifying the infecting strain.
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                Author and article information

                Contributors
                muha@biol.uw.edu.pl
                mabed@biol.uw.edu.pl
                emanmohallal@yahoo.com
                e.mierzejewska@biol.uw.edu.pl
                jbehnke@up.poznan.pl
                samy@biomapegypt.org
                francis.gilbert@nottingham.ac.uk
                rwelc@biol.uw.edu.pl
                akloch@biol.uw.edu.pl
                jerzymbehnke@gmail.com
                anabena@biol.uw.edu.pl
                Journal
                Parasit Vectors
                Parasit Vectors
                Parasites & Vectors
                BioMed Central (London )
                1756-3305
                8 April 2016
                8 April 2016
                2016
                : 9
                Affiliations
                [ ]Department of Parasitology, Institute of Zoology, Faculty of Biology, University of Warsaw, 1 Miecznikowa Street, 02-096, Warsaw, Poland
                [ ]Desert Research Center, Cairo, Egypt
                [ ]Department of Forest Phytopathology, Faculty of Forestry, Poznań University of Life Sciences, Poznań, Poland
                [ ]Department of Zoology, Suez Canal University, Ismailia, Egypt
                [ ]Faculty of Medicine & Health Sciences, School of Biology, University of Nottingham, Nottingham, UK
                [ ]Department of Ecology, Institute of Zoology, Faculty of Biology, University of Warsaw, 1 Miecznikowa Street, 02-096, Warsaw, Poland
                Article
                1471
                10.1186/s13071-016-1471-z
                4826546
                27059180
                1e46d097-af4c-4492-8526-59baaaa4eccf
                © Alsarraf et al. 2016

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100004281, Narodowe Centrum Nauki;
                Award ID: OPUS 2011/03/B/NZ6/02090
                Award Recipient :
                Funded by: KBN-BC Young Scientist Program
                Award ID: WAW/342/06
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100004569, Ministerstwo Nauki i Szkolnictwa Wyższego;
                Award ID: 140000/501/86-110101
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2016

                Parasitology
                acomys dimidiatus,acomys russatus, haemoparasites,haemobartonella,bartonella,hepatozoon,trypanosoma,babesia,species-richness,prevalence,abundance,sinai,drought,between year variation

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