Over-water dispersal makes terrestrial organisms move from one land mass to another. The capability and probability of this dispersal ecologically relate to the distribution of the creatures across lands and islands and then further evolutionarily influence biogeography and biodiversity [1–3]. Molecular and fossil evidence indicates that organisms may only spread outward between lands by crossing the ocean, rather than using land bridges [2, 4, 5], denoting that over-water dispersal is an important strategy for organisms. In the Anthropocene, although human transportation has become a path to crossing oceans for many introduced species, for a species invading new areas artificially, they could still spread out to adjacent areas naturally [6]. For example, Norway rats, which invaded islands around the world by artificial boats, dispersed to adjacent islands by natural drifting or swimming [7, 8]. Therefore, over-water dispersal not only is important for understanding the distribution of native species but also plays a substantial role in determining the range an invasive species can reach.
Extreme saline environments and crucial water loss are major physical challenges for terrestrial organisms when they are drifting on the ocean [9–11]. High-salinity environments are a stress for organisms. Different species have their own salinity tolerances [11–13]; this variation influences the survival differences among species in marine floating, leading to the variance in ability of oversea dispersal at a species level that further influences the distribution of the species [13, 14]. However, research about the association between this physiological ability and distribution has mainly focused on plants, freshwater animals, and arthropods [e.g. 10, 15, 16]. The dispersal of terrestrial vertebrates is rarely explored. In reptiles, some freshwater and terrestrial species appear in saltwater wetlands or coasts, even surviving there for a long time [17–19], demonstrating that reptiles can tolerate higher salinity environments. Nevertheless, previous studies about salinity tolerance have mostly focused on marine or estuary species [18, 20, 21]. In the few studies on freshwater and terrestrial species, the salinity treatments were usually orally fed or injective [12, 22], whereas treatment with saltwater contact, the most relevant situation faced by a drifting individual, has rarely been conducted in previous literature. Furthermore, none of these studies link salinity tolerance to species distributions. Consequently, this key ability for crossing oceans, the saltwater tolerance of direct water contact and how it relates to distribution, has not been fully elucidated.
Dehydration is the most crucial challenge for organisms drifting on the ocean and the vital factor of saltwater tolerance. In reptiles, water loss occurs primarily through skin in addition to the loss through respiration [23, 24]. The water loss of the skin is related to the adaption to the climate of the habitat environment [25–27], whereby species living in hot and dry habitats lose water slower than those living in cold and wet habitat [27, 28]. In addition, the lower rate of water loss indicates that the species can retain water for a long time, which could delay death from dehydration [29, 30]. Thus, species with lower rates of water loss are more likely to survive a drifting period of over-water dispersal than species that lose water fast. However, the relationship between water loss and survival rate in the context of ocean crossing in vertebrates has rarely been reported.
For most reptiles, there are two different ontogenetic stages to ocean crossing: the individual stage and the egg stage. Currently, ocean crossing at the individual stage has been reported abundantly through swimming, floating, or rafting [1, 31–33]. Compared with large species which can swim for a long distance, floating and rafting are the more likely ways for small reptiles to cross oceans [1, 34]. In geckos, dispersal by natural raft or artificial boats has been suggested in some small species [35, 36]. In Anolis, it can float for a short time on sea water [34] to disperse between islands in their native places [1, 4]. On the other hand, it is probable that over-water dispersal occurs at the egg stage [35, 37]. The saltwater tolerance and water loss of reptile eggs may be majorly determined by the type of eggshell. Reptilian eggs are mainly divided into two types: parchment-shelled eggs and rigid‐shelled eggs [38]. The shell of the former is thinner and less calcareous than that of the latter, resulting in differences in flexibility and permeability of water exchange. Parchment‐shelled eggs are highly sensitive to environmental humidity [39], whereas rigid‐shelled eggs, which have a dense and hard shell, could limit the exchange of water and substance from the environment [40]. Therefore, rigid‐shelled eggs should have higher tolerance to seawater. Some gecko studies have shown that eggs can tolerate sea water well after immersion treatment [41, 42]. For parchment‐shelled eggs, successful incubation after immersion of sea water has only been reported in Anolis sagrei [43].
Taiwan and the adjacent islands are currently blocked by the sea (a depth of approximately 70 metres) from the Asian continent. However, the main island of Taiwan and the small islands between Taiwan and China were all connected to the Asian mainland before 1.55 Ma and during the Last Glacial Maximum in 26.5–18 ka, during which the sea level fell 135 metres (Fig. 1G)[44–46]. Therefore, Taiwan and these western islands are continental islands. Terrestrial species could disperse between Taiwan and Asian mainland through the land bridge (Fig. 1G). In contrast, the eastern ocean of Taiwan is drastically deep (a depth of over 1,000 metres) due to the oceanic trench in the nearby eastern coast, preventing the islands east of Taiwan from connecting to any island and mainland historically (Fig. 1G). Thus, the eastern islands are oceanic islands, where the species arrive only by over-water dispersal. Combining these historical contexts of geographic connection across Taiwan and these islands, knowledge of the variation of salinity tolerance among species could demonstrate how the current species distributions were formed.
In this study, we aimed to examine the heterogeneity of saltwater tolerance of small lizard species across Taiwan and the adjacent islands to determine their potential ability of over-water dispersal and then inspect the current distributions of these species and their saltwater tolerance within the context of historical geology. Six small lizard species, specifically four native species and two introduced species, were chosen (Table 1) in this study. The four native species were Plestiodon elegans, existing throughout Taiwan, the western and northern islands, and south-eastern China (Fig. 1A); Eutropis longicaudata, distributed in southern Taiwan, the southern islands, and mainland Southeast Asia (Fig. 1B); Diploderma swinhonis, existing throughout Taiwan, the southern islands, and the Ryukyu Islands (Fig. 1C); and Hemidactylus frenatus, existing throughout Taiwan, all adjacent islands, and almost every island in East and Southeast Asia (Fig. 1D). The two introduced species were Eutropis multifasciata and Anolis sagrei. The former is native to the Philippines and was first discovered in southern Taiwan in 1992 [47]. This species has been found in Green Island since 2008 [48] and in Orchid Island since 2017 (Fig. 1E). A. sagrei from the West Indies was discovered in central Taiwan in 2000 [49] and eastern Taiwan in 2006 [50] but has not been discovered to date in adjacent islands (Fig. 1F). In this study, we performed experiments of seawater immersion on these six species and their eggs to simulate the condition of floating on the ocean. Specifically, we first examined the water loss and the survival rate/incubation rate of these small lizards and their eggs using the immersion experiments to evaluate the possibility of natural cross-ocean dispersal. Second, we inspected the association between these variations in saltwater tolerance and the distributions of these six species with the historical contexts of geographic connection across Taiwan and the adjacent islands. Finally, in addition, we assessed the dispersal risk of the two introduced species for conservation purposes.
Table 1
Distributions of six lizard species in Taiwan and adjacent islands. The distance is the closest distance to Taiwan.
| Taiwan | Penghu | Little Liuqiu Island | Guishan Island | Green Island | Orchid Island | Philippines |
Distance from Taiwan | NA | 47 km, west | 13 km, southwest | 11 km, northeast | 44 km, southeast | 63 km, southeast | 161 km, southeast |
Plestiodon elegans | O | O | O | O | X | X | X |
Eutropis longicaudata | O | X | O | X | O | O | X |
Eutropis multifasciata | O | X | O | X | O | O | O |
Diploderma swinhonis | O | X | O | X | O | O | X |
Hemidactylus frenatus | O | O | O | O | O | O | O |
Anolis sagrei | O | X | X | X | X | X | X |
The direction is the relative position to Taiwan. The character O indicates that this species exists in that location, and the character X indicates no distribution. |