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Characterization of polymorphic microsatellite markers in the brine shrimp Artemia (Branchiopoda, Anostraca)

Surveys were conducted for terrestrial reptiles and amphibians from the Vava’u island group within the Kingdom of Tonga between 12 and 27 February 2014. Reptile surveys were conducted on 13 of the 58 islands within the Vava’u Island group (Figures 3.1 and 3.2, Annex3.1). Six sticky trap transects were sampled on the main island of ‘Uta Vava’u, nine sticky trap transects were sampled on other islands within Vava’u, and reptiles were recorded by visual encounter surveys from an additional three islands.

The survey effort on Vava’u consisted of three techniques when possible (Fisher 2011). The first technique was daytime visual encounter surveys of the habitats around the island, as possible, with capture of animals by hand. The second technique involved setting up sticky trap transects at various habitats and elevations across the islands (Figures 3.3 and 3.4). Each station consisted of three standard sticky mouse traps, one placed on the ground, one placed on a log off the ground, and the third stapled to a tree (about 1.5 m high). These traps were optimally placed out in the afternoon and then collected the next morning so that they would sample diurnal and nocturnal species. The third technique was night visual encounter transects. These were used to provide additional data on geckos and iguanas and were both time and distance constrained surveys. We also recorded the presence of invasive mammal and ant species, including rats, pigs, goats, cats and yellow crazy ants.

For each sticky trap transect, a sampling station was set up every 20 or 30 m along the transect line . At each sampling station the three sticky traps were deployed: one on the ground (G), one on a log (L) above the ground, and one on a tree

(T) approximately 1.5 m off the ground. The locations of the transects were selected to sample the variety of habitats, elevational gradients and vegetation types across Vava’u. Captured lizards were removed from the traps using vegetable oil by rubbing it along their body and peeling them off the trap. Once the lizard had been removed, the location of the sticky trap was recorded and the lizards were identified, weighed (g), measured snout to vent (mm), and either a tissue sample or the whole lizard was collected as a voucher specimen. Rats, rat fur and rat chew marks were recorded from the traps. Yellow crazy ants were also counted from the traps. The traps and flagging were removed at the end of the survey.

Museum vouchers of reptiles were also queried for the Kingdom of Tonga via HerpNet2. org on 14 March 2014 to provide additional information on previous collections from the area.

Figure 3.1. Location of reptile trap lines in Vava’u.

Rapid Biodiversity Assessment of the Vava'u Archipelago, Kingdom of Tonga 33

Figure 3.2. Location of night and day transects in Vava’u.

Figure 3.3. Sticky trap stations (photos byAdam Backlin).

Figure 3.4. Ana Fekau and Saia Fonokalafi assisting installation and sampling of reptile sticky trap stations (photos by Adam Backlin).

Rapid Biodiversity Assessment of the Vava'u Archipelago, Kingdom of Tonga 35

3.4. Results

Overall, 4.2 km of sticky trap transects were sampled. These included 15 transects distributed across the Vava’u island group. These surveys covered a broad variety of habitats and islands across Vava’u, from coastal beaches through Maniltoa forests, secondary forests and mangroves (Figure 3.1). A total of 22.3 km of visual encounter surveys was completed with 15.6 km completed during the day and 6.7 km completed at night (Figure 3.2).

A total of 417 terrestrial reptiles representing 11 lizard species was recorded during this survey (Table 3.1 and Figures 3.5 and 3.6). Six species of skink, one iguana species and four gecko species were detected including the first record of the invasive common house gecko (Hemidactylus frenatus) on Vava’u. No snakes or amphibians were detected. Full results from the reptile survey are presented in Annex 3.1.

During this survey we collected reptile inventories on 13 islands, five of which had no previous reptile information − Kenutu, Maninita, ‘Oto, Taula and ‘Umuna. We collected 29 new island species records for reptiles across the Vava’u Island Group (Table 3.2).

A query of the reptiles from the Kingdom of Tonga from HerpNet2. org on 14 March 2014 revealed 1,413 museum records. Records were located from ten museums: the American Museum of Natural History, NY (AMNH), Bernice P. Bishop Museum, HI (BPBM), the California Academy of Sciences, CA (CAS), Carnegie Museum, PA (CM), Field Museum of Natural History (FMNH), Harvard Museum, MA (MCZ), Osaka Museum of Natural History, Japan (OMNH), San Diego Natural History Museum, CA (SDNHM), Utah Museum of Natural History, UT (UMNH), and the Smithsonian National Museum of Natural History, Washington, DC (USNM). Museum abbreviations follow Leviton et al. (1985). Of the 1,413 records, 1,389 were of terrestrial reptiles. Of those, 200 were terrestrial reptiles from the Vava’u island group representing ten lizard species from seven islands (Table 3.2).

Table 3.1. Lizard species recorded in Vava’u surveys.

Island

Lau banded iguana Oceania gecko Mourning gecko Pacific slender-toed gecko Common house gecko Oceanic snake-eyed skink Pacific moth skink Undetermined skink White-bellied copper-striped skink Dark-bellied copper- striped skink Tongan robust treeskink1 Polynesian slender treeskink2

Brachylophus fasciatus Gehyra oceanica Lepidodactylus lugubris Nactus palagicus Hemidactylus frenatus Cryptoblepharus poecilopleurus Lipina noctua Emoia cyanura /impar Emoia cyanura Emoia impar Emoia mokolahi1 Emoia tongana2 Total captures per island

‘Uta Vava’u 1 11 3 8 5 - 4 5 21 35 1 5 99

Pangaimotu - - - - - - - 3 6 2 1 - 12

Vaka’eitu - - - - - 1 - - 5 8 - - 14

‘Euakafa - 1 1 - - - - - 10 12 - - 24

A’a - 2 - - - - - - - 3 - - 5

Mafana - 2 - - - - - - 1 1 - - 4

‘Euaiki - - - - - - - - - 17 - - 17

Kulo - 3 - - - - - 1 - - - - 4

Kenutu - 5 8 2 - 17 - 12 38 28 - - 110

Maninita - 19 11 1 - - - - 2 5 - - 38

‘Oto - - - - - 4 - - - 31 - - 35

Taula - 6 - - - - - - 2 13 - - 21

‘Umuna - 6 3 - - 1 - 10 3 11 - - 34

Total islands occupied

1 55 26 11 5 23 4 31 88 166 2 5 417

1 Formerly Dandy skink, Emoia trossula.

2 Formerly Murphy’s tree skink, Emoia murphyi.

Table 3.2. New island species records in Vava’u.

Island

Lau banded iguana Oceania gecko Mourning gecko Pacific slender-toed gecko Common house gecko Indo-Pacific slender gecko Oceanic snake-eyed skink Pacific moth skink Undetermined skink White-bellied copper-striped skink Dark-bellied copper- striped skink Tongan robust treeskink1 Polynesian slender treeskink2

Brachylophus fasciatus Gehyra oceanica Lepidodactylus lugubris Nactus palagicus Hemidactylus frenatus Hemiphyllodactylus typus Cryptoblepharus poecilopleurus Lipina noctua Emoia cyanura /impar Emoia cyanura Emoia impar Emoia mokolahi1 Emoia tongana2 Total species/ island

‘Uta Vava’u BR, GR BR, G,

2 Formerly Murphy’s tree skink, Emoia murphyi.

BR = BIORAP (2014), G =Gill (1990), GR = Gill and Rinke (1990), M = museum record, S = Steadman et al. (1999), ZG = Zug and Gill (1997), UV = unverified.

Rapid Biodiversity Assessment of the Vava'u Archipelago, Kingdom of Tonga 37

Figure3.5. Emoia tongana, the largest lizard on the right, and E. cyanura/impar, the two smaller blue tailed lizards, captured on a sticky trap (photo by Adam Backlin).

Figure 3.6. Juvenile Emoia tongana captured on a sticky trap (photo byAdam Backlin).

3.5. Discussion

The BIORAP in 2014 was the most recent assessment of reptiles in the Vava’u Island Group since the Steadman et al. (1999) expedition in 1993 and 1995−1996. All but 30 of the 200 museum specimens from Vava’u were collected since 1985. This indicates that very little was known about the reptiles in Vava’u 30 years ago and since that time only a few collecting expeditions have occurred.

In the past 18 years, little has changed within the reptile community across the Vava’u island group. On our surveys in 2014 we detected all known species of terrestrial reptiles except one, the Indo-Pacific slender gecko (Hemiphyllodactylus typus). This species is known from only one specimen collected in 1993 (USNM 333617). This is a small cryptic gecko that is not easily captured on sticky traps. It likely still occurs within Vava’u at low densities. We were able to detect one additional reptile not documented from Vava’u, the invasive common house gecko (Hemidactylus frenatus). This is a newly established invasive species arriving within the last 18 years. It is readily detectable on the walls and ceilings of structures and was very common throughout Neiafu. We did not detect this species outside of Neiafu and it was also absent from Mounga Talau which is less than 1 km from structures in Neiafu. This species is continuing to spread throughout the Pacific Basin, as previously suggested by Case et al. (1994), and is not a surprising finding. Biosecurity measures could be implemented to try to limit its movement to all the remaining populated areas of Vava’u.

We did not detect any snakes or amphibians during this survey. We searched for the Pacific tree boa (Candoia bibroni) during our night time visual encounter surveys as there is a single museum record from the Kingdom of Tonga with no further locality data from 1906 (USNM 56211). This species also occurs in nearby Fiji and Samoa (Zug 2013). We spoke with numerous villagers regarding their knowledge of this species and no one we spoke with had ever seen or known of a large snake in Vava’u. We also conducted searches for the invasive Brahminy blindsnake (Ramphotyphlops braminus), mainly in Neiafu. This is a small, wormlike snake that is also known as the ‘flower pot snake’ as it has been transported across the Pacific in the soil of nursery plants (Zug 2013). We did not detect any blindsnakes during our searches. Additionally we did not detect any amphibians. No amphibians have ever been detected on Vava’u. Our surveys aimed to confirm that no invasive amphibians have established recently. The most likely invasive amphibian species would be the cane toad (Rhinella marina).

The Lau banded iguana (Brachylophus fasciatus) is classified as endangered by the IUCN. The only museum specimens from Vava’u were collected in 1969 (Gill 1990). We conducted day and night time visual encounter surveys for the iguana across Vava’u. Although this iguana is diurnal, night surveys are 10 times more likely to detect iguanas compared to day time observations (Harlow and Biciloa 2005). We collected one iguana in the village of Leimatu’a which was from elsewhere (the original capture location was never ascertained) and recently brought to this location (Figure 3.7). In speaking with the local villagers, many were aware of the iguanas and had seen them at some point in their lifetime. Occasionally, locals keep them as pets or sell them. In the areas we surveyed the iguanas, if still present, are at low densities. There may be areas on Vava’u that we did not survey that support large populations of iguanas, but none of the surveys in the 1980s or 1990s detected it. Most of the forest habitats the iguanas require are highly fragmented, manipulated or converted, restricting their ability to access other suitable forest patches. Cat predation seems to be one of the biggest threats to the species in its native range.

Zug (2013) and others (Steadman et al. 2002; Pregill and Steadman 2004) describe the Tongan Lau banded iguana as introduced from Fiji shortly after human colonisation of Tonga. Archaeological studies of the Ha’apai island group of Tonga revealed an extinct species of iguana (Brachylophus gibbonsi) that disappeared less than one century after human colonisation (c. 2,850 years ago; Steadman et al. 2002). Not a single bone of B. fasciatus has been found in any fossil record in Tonga while there is a fossil record of B. fasciatus in Fiji (Pregill and Steadman, 2014). It is likely that B. fasciatus was translocated from Fiji approximately 500 years ago to Tonga as a food source (Pregill and Steadman 2004). Further genetic evaluation of the iguanas is recommended to fully resolve their historic distribution (Keogh et al. 2008).

In the short time we were working on Vava’u, there were two separate documented translocations of iguanas. One was the iguana we ultimately captured in the village of Leimatu’a that had been collected from the forest. We were told that two iguanas had been captured, but one died shortly after translocation. The other translocation was an iguana captured on Pangaimotu, near a vanilla farm. A man named Bien came into possession of this iguana and released it on Mafana where he runs an eco-tourist camp. Movement of this species is of concern since we do not know the source of the iguanas or the size of the population. Outreach about reporting the native iguana and not moving them between islands is important.

Rapid Biodiversity Assessment of the Vava'u Archipelago, Kingdom of Tonga 39

There is also concern that other species, such as the invasive green iguana (Iguana iguana) that is present in Fiji, might be brought to Tonga. In Fiji, movement of the green iguana is leading to major concerns about economic impacts of this species, such as food security issues.

Invasive species are a major threat to the herpeto fauna of Vava’u and elsewhere. Invasive reptiles and amphibians can outcompete and displace native species (Case et al. 1994; Cole et al. 2005; Fisher 2011), and they can also introduce new parasites (Hanley et al. 1995) and diseases. There is also concern over invasive animals such as rats, pigs, goats and ants.

Rats are voracious predators and readily eat geckos and skinks. We recorded rats at almost every sampling station on Kenutu and ‘Umuna Islands. Pigs and goats are destructive to habitat and vegetation. Pigs dig up the ground and are likely disrupting iguana nests and eating their eggs. Invasive ants such as the yellow crazy ant (Anoplolepis gracilipes) are already widespread across Vava’u and have been implicated in major losses of biodiversity on other island systems (Smith et al. 2012; Fisher et al. 2012). ‘Euaiki had much greater densities of yellow crazy ants than elsewhere across Vava’u although they were detected at most sampling areas in lower densities. Fisher et al. (2012) found no overlap between three large skink species and invasive ants on Savai’i (Samoa). The invasive ants have invaded all areas of Savai’I below 900 m. These three large skink species are now only found above 900 m where the ants have been unable to colonise.

We compiled all the available data for reptiles from the Vava’u island group and present it in Table 3.2. This table includes work from recent expeditions (Gill 1990; Gill and Rinke 1990; Zug and Gill 1997; Steadman et al. 1999; and this study) and records obtained from ten museums dating back to 1899. There is information available for reptiles from 22 of the 58 islands within Vava’u representing 12 species of lizard. From this data it appears that many of these species are widespread across Vava’u, including Emoia cyanura, E. impar, Cryptoblepharus poecilopleurus, Lipina noctua, Gehyra oceanica, Lepidodactylus lugubris and Nactus pelagicus. Other species appear to be more common on the larger islands or may simply have not been detected on other islands they occupy. Clearly the main island ‘Uta Vava’u has the highest diversity with all known species being detected. This is the only island where three species have been detected− Brachylophus fasciatus, Hemidactylus frenatus and Hemiphyllodactylus typus. For the Lau banded iguana (B. fasciatus), we know that there is a recently translocated individual on Mafana and it was captured from Pangaimotu so this species is likely more widespread than the data represent. The common house gecko (H. frenatus) is an aggressive invasive that will likely spread to other islands. It likely arrived in Vava’u within the last 20 years and may already be present on other islands. The Indo-Pacific slender gecko (H. typus) is also a recent arrival to Vava’u. This is a small cryptic gecko that can be difficult to detect. It may be more widespread and species specific surveys may help to better understand its distribution on Vava’u. The Tongan robust treeskink (Emoia mokolahi) is endemic to Tonga and is widespread across the archipelago from Vava’u to Eua. This species likely occurs on more than five of the islands within Vava’u. Likewise the Polynesian slender treeskink (Emoia tongana) occurs from Vava’u south through the Ha’apai island group and north into Futuna and Samoa. This species is also likely more widespread in Vava’u than our data suggest. Since these last two species can be difficult to detect, all three sampling techniques need to be utilised since they have low detection generally, so that the distribution of the species can be better defined.

3.6. Conservation recommendations

The reptile community in Vava’u has remained mostly intact despite almost 3,000 years of human occupation. To ensure the persistence of these species into the future we outline several recommendations here.

The main island of ‘Uta Vava’u has the most reptile diversity compared to the other islands in this group and is the highest priority island for reptile conservation in Vava’u. This island’s forests are highly fragmented except on the steepest slopes.

We recommend creating management areas that would allow for large intact sections of forest and also linking of forest patches. We also recommend inventories of invasive species across the islands that will provide baseline data to initiate conservation actions working towards control, removal and biosecurity protocol development.

The Lau banded iguana (Brachylophus fasciatus – Figure 3.7) is the only reptile from Vava’u that has a classification on the IUCN Red List. It is classified as endangered, with a decreasing population trend. It is persisting on Vava’u but almost nothing is known about this species in Tonga. Iguana specific surveys should be conducted across the Vava’u island group to understand their current distribution and abundance. This information is required to make informed management decisions on proposed locations of forest management areas or where restoration projects should occur. Compiling a checklist of iguana occupied islands is important as many of the islands have more intact forests than the main island.

These islands could serve as refugia populations in the event of a catastrophic loss of the species within Vava’u, the rest of Tonga, or Fiji.

Figure 3.7. Lau banded iguana (Brachylophus fasciatus) captured in the village of Leimatu’a (photo by Adam Backlin).

Rapid Biodiversity Assessment of the Vava'u Archipelago, Kingdom of Tonga 41

3.7. References

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Cole, N. C., Jones, C. G. and Harris, S. 2005. The need for enemy-free space: the impact of an invasive gecko on island endemics. Biological Conservation 125:

467−474.

Fisher, R. N. 2011. Considering native and exotic

terrestrial reptiles in island invasive species eradication programmes in the Tropical Pacific. Pp. 51−55 in Veitch, C. R., Clout, M. N. and Towns, D. R. (eds), Island invasives: eradication and management. Gland, Switzerland:IUCN.

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(eds.), Rapid Biodiversity assessment of Upland Savai’I, Samoa. Apia, Samoa: SPREP.

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