Hirudinaria, Whitman, 1886

Jiranuntskul, Putita, Boonporn, Ausadang, Kongrit, Chalita, Panha, Somsak & Jeratthitikul, Ekgachai, 2022, Biodiversity of the Buffalo Leeches Genus (Arhynchobdellida, Hirudinidae) in Southern Thailand Revealed from DNA Barcoding., Zoological Studies 61 (84), pp. 1-14 : 10-11

Biogeography of Hirudinaria leeches in southern

Thailand

The distribution pattern of Hirudinaria leeches in southern Thailand primarily corresponds to geography. However, sparse distribution, low genetic distance, and lack of genetic structure might reflect anthropogenic activity and the ectoparasitic lifestyle of this genus. Introductions of leeches by humans or host animals are not unexpected, as many cases have occurred. Hirudinaria manillensis 2 in the Caribbean, for example, was transported by ship from another continent and adapted to the new environment over centuries ( Sawyer et al. 1998). Ozobranchus jantseanus was introduced to Japan by its host species, a turtle. Although it has low genetic diversity, its populations in Japan are rapidly growing ( Nakano et al. 2017).

Distribution data should be interpreted with caution when considering sequences retrieved from previous studies. As mentioned in Chong et al. (2014), sequences from Malaysia were obtained from both leech farms and natural habitats. Leech culture businesses have been established in many states of Malaysia, as the government and aquaculture institute have promoted leech culture for Malaysian entrepreneurs for a decade. There is documented evidence that some leech farms might rear leeches in natural ponds, and so it is unsurprising that leeches have been released into the natural environment ( The Fish Site 2008; Zulhisyam et al. 2016; List of companies in world wide 2020). Local traders in Thailand said that large quantities of living leeches were collected from northeastern and southern Thailand and directly transported to Malaysia or other regions for aquaculture purposes (personal communications). Therefore, some leech sequences from Malaysia could have originated from Thailand. This was reflected in some odd distribution patterns such as those in H. javanica . In Thailand, this species has only been found in the northeastern region. However, the Malaysian specimen was collected in a natural habitat in Selangor, over 1,000 km from the Thai distribution range (diamond symbols in Fig. 1 ) ( Chong et al. 2014).

In a previous study, H. thailandica was reported in northern, northeastern, and central parts of Thailand ( Jeratthitikul et al. 2020). In this study, we discovered H. thailandica north of 9 degrees latitude in southern Thailand. No specimens of H. thailandica were found further south. This limited distribution range corresponds to the Suratthani-Krabi Line, where multiple marine transgressions occurred in the early/middle Miocene (24–13 million years ago), early Pliocene (5.5–4.5 million years ago), and early Pleistocene (1.5 million years ago) ( Woodruff 2003; Bohlen et al. 2020). Marine water that flooded the lowland along the Suratthani-Krabi Line would have divided the peninsula into two parts: the Tenasserim range in the north and the Nakhon Si Thammarat range in the south ( Fig. 1B ). Therefore, populations on either side of the Suratthani-Krabi seaway were isolated. This distribution pattern was also observed in the genetic structure of other freshwater animals such as the giant freshwater prawn Macrobrachium rosenbergii ( de Bruyn et al. 2005) and the dwarf zipper loach Paracanthocobitis zonalternans species-complex ( Bohlen et al. 2020).

Hirudinaria bpling was first described at Bang Lae, Phang-Nga ( Phillips 2012). This study shows an expansion of the distribution range from previous studies ( Phillips 2012; Jeratthitikul et al. 2020). Hirudinaria bpling is distributed along both eastern and western coasts of southern Thailand, roughly just south of the distribution range of H. thailandica . One specimen was from Chumphon (A78), where it was sympatric with H. thailandica . This individual was likely introduced by host animals or by humans.

Because H. bpling and H. thailandica are sister clades and have low interspecific genetic divergence, they may share a common ancestor. One presumption is that their common ancestor was widely distributed throughout the Thai-Malay peninsula, and when sea level rose, the seaway at the Suratthani-Krabi Line acted as a physical barrier between populations, which led to speciation into the present two species: H. thailandica in the north and H. bpling in the south. In our sampling, H. bpling populations were also found north of the Suratthani-Krabi Line (in Phang-nga and Phuket provinces). These populations might have become established shortly after the sea level fell, reconnecting the peninsula. This is reflected in the absence of structure in the phylogenetic relationship between H. bpling populations from either side of the Suratthani-Krabi Line. A similar situation can be seen in the recent northward expansion of Macrobrachium rosenbergii ( de Bruyn et al. 2005) and the secondary contact of the Paracanthocobitis zonalternans group ( Bohlen et al. 2020).

For the Hirudinaria manillensis complex, previous studies reported that H. manillensis 1 was abundant in northeastern Thailand and was also found in one location in central Thailand ( Tubtimon et al. 2014; Jeratthitikul et al. 2020). In this study, we found H. manillensis 1 in two locations along the eastern coast of southern Thailand, and in one location on the western coast. In the two locations on the eastern coast, H. manillensis 1 was sympatric with H. bpling . Hirudinaria manillensis 1 specimens from all regions were clustered together in phylogenetic trees with no obvious structure, indicating that they are from a single continuous origin. This species was possibly transported to different regions through the buffalo trade ( GIAHS 2021). In summary, H. manillensis 1 is abundant in northeastern Thailand and sparsely found in the central and southern parts of Thailand. Thus, it could be presumed that the natural range of this species was in the northeast and eventually expanded as the leeches were introduced to other regions.

Although the distribution ranges of H. manillensis 1 and H. manillensis 3 in southern Thailand were adjacent, their ranges did not overlap and codistribution was not found. Furthermore, H. manillensis 3 was not sympatric with other Hirudinaria species. It was found in two locations on the east coast of the Thai-Malay peninsula, in Phatthalung and Songkhla provinces. Sequences from Vietnam (GQ368747-8) were also clustered in the H. manillensis 3 lineage. Leeches from these regions might have been united during glacial periods in the Pleistocene (21,000 –13,000 years ago) ( Voris 2000; Sathiamurthy and Voris 2006; de Bruyn et al. 2013). During glacial periods, sea level was 60–110 m lower than the present day. The area that currently exists as the Gulf of Thailand was exposed as a landmass called the Sunda Shelf. On the Sunda Shelf, the Siam paleo-drainage was the main river system connecting freshwater bodies in Thailand, Cambodia, and Vietnam. This connection could have led to dispersal and gene flow of freshwater taxa across the Sunda Shelf. Hirudinaria manillensis 3 might have migrated throughout the Siam paleo-drainage. Evidence of this was represented by the shallow divergence in phylogeny between H. manillensis 3 from southern Thailand and Vietnam ( Figs. 3 , S 1 , S 2 ). The similarity of freshwater animals between the Thai-Malay peninsula and Indochina also has been reported in other works, e.g., the river catfish Hemibagrus nemurus ( Dodson et al. 1995) , the silver barb Barbodes gonionotus ( McConnell 2004) , the Mekong mud snake Enhydris subtaeniata ( Lukoschek et al. 2011) , the blue panchax killifish Aplocheilus panchax ( Beck et al. 2017) and the tire track eel Mastacembelus favus ( Jamaluddin et al. 2019) . Furthermore, the distribution of H. manillensis 3 in southern Thailand is limited to the east coast. This could be due to the presence of the Nakhon Si Thammarat range, which runs north-south along the middle of the Thai-Malay peninsula. Hirudinaria manillensis 3 might be unable to cross this mountain range to the west coast of the Thai-Malay peninsula.

Figures

Fig. 1. Map showing sampling localities of buffalo leeches genus Hirudinaria in (A) Asia and (B) southern Thailand. Dotted lines indicate hypothetical fauna transition zones in southern Thailand: Isthmus of Kra and Surat Thani-Krabi Line.

Fig. 3. BEAST ultrametric tree of buffalo leeches genus Hirudinaria. Leeches from southern Thailand are highlighted in bold. Numbers on nodes are bootstrap values from ML tree generated by IQ-TREE, Bayesian posterior probability from BI tree generated by MrBayes, and from ultrametric tree generated by BEAST, respectively. Black bars indicate morphological identification (MORPHO) and delineated OTUs suggested by four species delimitation approaches (GMYC, bPTP, BIN, and ABGD). Grey bars indicate samples that were not available for morphological identification.

Fig. 2. External morphology of living Hirudinaria leeches from southern Thailand. (A) dorsal and (B) ventral sides of H. bpling from Satun Province (C) dorsal and (D) ventral sides of H. manillensis 3 from Songkhla Province. Scale bar = 1 cm.