Philippe Keith

Amphidromy links a newly documented fish community of continental Australian streams, to oceanic islands of the West Pacific

Background Indo-Pacific high island streams experience extreme hydrological variation, and are characterised by freshwater fish species with an amphidromous life history. Amphidromy is a likely adaptation for colonisation of island streams following stochastic events that lead to local extirpation. In the Wet Tropics of north-eastern Australia, steep coastal mountain streams share similar physical characteristics to island systems. These streams are poorly surveyed, but may provide suitable habitat for amphidromous species. However, due to their ephemeral nature, common non-diadromous freshwater species of continental Australia are unlikely to persist. Consequently, we hypothesise that coastal Wet Tropics streams are faunally more similar, to distant Pacific island communities, than to nearby faunas of large continental rivers. Methods/Principal Findings Surveys of coastal Wet Tropics streams recorded 26 species, 10 of which are first records for Australia, with three species undescribed. This fish community is unique in an Australian context in that it contains mostly amphidromous species, including sicydiine gobies of the genera Sicyopterus, Sicyopus, Smilosicyopus and Stiphodon. Species presence/absence data of coastal Wet Tropics streams were compared to both Wet Tropics river networks and Pacific island faunas. ANOSIM indicated the fish fauna of north-eastern Australian coastal streams were more similar to distant Pacific islands (R = 0.76), than to nearby continental rivers (R = 0.98). Main Conclusions/Significance Coastal Wet Tropics streams are faunally more similar to distant Pacific islands (79% of species shared), than to nearby continental fauna due to two factors. First, coastal Wet Tropics streams lack many non-diadromous freshwater fish which are common in nearby large rivers. Second, many amphidromous species found in coastal Wet Tropics streams and Indo-Pacific islands remain absent from large rivers of the Wet Tropics. The evolutionary and conservation significance of this newly discovered Australian fauna requires clarification in the context of the wider amphidromous fish community of the Pacific.

Involvement of thyroid hormones in the control of larval metamorphosis in Sicyopterus lagocephalus (Teleostei: Gobioidei) at the time of river recruitment

After oceanic migration, post-larvae of the amphidromous Sicyopterus lagocephalus recruit to rivers in Reunion Island. As they enter the river mouth, post-larvae undergo many morphological, physiological and behavioural changes. These drastic changes, which allow them to change feeding regime and to colonise the juvenile and adult freshwater habitat, are defined as metamorphosis. The endocrine control of these changes has never been investigated in Gobioid fish. Here, we investigated whether thyroid hormones (TH) influence metamorphosis in recruiting S.lagocephalus. An analytical study was first performed on a cohort of 2400 fish caught at post-larval stage 1 and maintained for 37 days after capture in a flume tank (fluvarium), which replicates as closely as possible the natural conditions. Biometrical parameters (total and standard lengths, corner of mouth angle, body mass and condition factor) and whole-body thyroxine (T(4)) and triiodothyronine (T(3)) contents were measured on fish, sampled at regular intervals during these 37 days (192 fish). TH levels, measured by radioimmunoassays, were highest when morphological changes, such as the change in the position of the mouth, were most important. An experimental approach was then used to test the effect of the hormonal treatment (T(4) or thiourea, TU, a TH inhibitor) on biometrical parameters of 576 post-larvae. The change in the position of the mouth was significantly accelerated in the T(4)-treated post-larvae, while it was significantly delayed in the TU-treated post-larvae, compared to controls. Our study suggests that S.lagocephalus post-larva undergoes a true metamorphic event under the control of thyroid hormones at the time of its recruitment into the river.

Femtosecond laser ablation ICP-MS measurement of otolith Sr:Ca and Ba:Ca composition reveal differential use of freshwater habitats for three amphidromous Sicyopterus (Teleostei: Gobioidei: Sicydiinae) species

The use of freshwater habitats was examined in three amphidromous goby species of the genus Sicyopterus using otolith microchemistry. Two species were endemic to either New Caledonia or Vanuatu whilst the other was widely distributed. Depositional patterns of strontium (Sr) and barium (Ba) in the otolith of adults were analysed with femtosecond laser ablation inductively coupled plasma mass spectrometry (ICP-MS). The Sr:Ca and Ba:Ca results uncovered three different adult behaviours within the freshwater habitat. Some fishes stayed in elevated locations (square profile); others undertook back-and-forth migrations between higher and lower reaches (up-and-down profile), and finally, others stayed in the lower reaches (constant profile). The consequences of these movements to larval survival or competition for food and territory are discussed. This work brings new knowledge on amphidromous behaviour, and it highlights the necessity of multi-elemental analysis to study amphidromy in freshwater systems.

Tropical and temperate freshwater amphidromy: a comparison between life history characteristics of Sicydiinae, ayu, sculpins and galaxiids

Amphidromy is a distinctive form of diadromy, but differences in the life histories of tropical and temperate amphidromous fishes suggest that there are two types of freshwater amphidromy. The life histories of Sicydiinae gobies, ayu (Plecoglossus altivelis), Japanese sculpins (Cottus) and galaxiids (Galaxiidae), suggest that the Sicydiinae are representatives of tropical freshwater amphidromy, whereas ayu, sculpins and galaxiids are representatives of temperate freshwater amphidromy. The Sicydiine larval stage may be required to occur in the ocean for all species, but ayu, sculpins and galaxiids have landlocked or fluvial forms with larvae that do not need to enter the ocean for larval feeding and growth. This suggests that Sicydiine larvae have a high oceanic dependency whereas ayu, sculpins and galaxiid larvae have a low oceanic dependency. Freshwater amphidromous fish in tropical and temperate zones appear to have developed two different strategies in the evolution of their life histories. It is likely that the evolutionary direction of the larval stage of tropical amphidromy is to remain in the sea and that of temperate amphidromy is towards having the ability to remain in freshwater if needed. Tropical and temperate amphidromy appear to be biologically informative categories and evaluations of this hypothesis will facilitate better understanding of the various forms of amphidromy in the future.

Otolith shape analysis for three Sicyopterus (Teleostei: Gobioidei: Sicydiinae) species from New Caledonia and Vanuatu

Otolith shape analysis has been used in a number of studies as an inexpensive and powerful method for categorising fish in individual stocks. Elliptical Fourier analysis was used on three different amphidromous Sicyopterus species. Sicyopterus lagocephalus is a widespread species while the other two have a limited distribution area, Sicyopterus aiensis being endemic to Vanuatu, and Sicyopterus sarasini to New Caledonia. Both endemics live in sympatry with the widespread species. The otolith shape of all fish sampled was a clear species differentiator, thereby demonstrating that otolith shape is species-specific. At an intraspecific level there are different river populations within samples from Vanuatu, indicating a western group and an eastern “central” group.These results are congruent both for the endemic species, S. aiensis and for the cosmopolitan species. Finally, we found that, for S. lagocephalus, the cosmopolitan species, New Caledonian samples are close to western Vanuatu samples, the latter two being well differentiated from the eastern “central” Vanuatu samples. The explanation for these results may lay either in the influence of environmental factors on the otolith shape, or in the influence of common early life history thus reflecting genetic factors, or a combination of both.

Threatened fishes of the world: Sicyopterus sarasini Weber & de Beaufort, 1915 (Gobiidae)

Common name: “Sicyoptere de Sarasin” or “Lochon”. Conservation status: critically endangered. Identification: D1 VI, D2 I + 10, A I + 10, C 11–14, P 17–19, LL 45–65. Maximum standard length: 15 cm (Watson et al. 2000) (Illustration by Clara Lord). Distribution: Endemic to New Caledonia. Inventories between 1995 and 2000 by MNHN found it in 17 catchment areas in South Province (Marquet et al. 2003); February 2007 inventory found it only in four (Kwatea, Trou Bleu, Nera and Barendeu Rivers). Abundance: Largely relictual. Best-preserved populations in Trou Bleu and Barendeu Rivers. “Cote Oubliee” populations suspected in good health. Habitat and ecology: Strictly lives in rivers with peridotite beds, in clear, well-oxygenated water (current speed 30–80 cm·s) 20–40 cm deep, on pebbles or rocks; adheres to substrate with sucker-like pelvic fins. Scrapes diatoms and algal food off substrate (Marquet et al. 2003). Reproduction: Amphidromous. Spawns in rivers. River current carries planktonic larvae to sea. Several months later, they return to rivers where they metamorphose into juveniles (Keith 2003), and climb up waterfalls with their sucker, colonising upper streams. Threats: River physical deterioration and water pollution from nickel mining and deforestation. Silt deposits on rocks prevent algal growth, eliminating predominant food source; also prevents fish adhesion to rocks, thus decreasing access to headwater habitats and spawning ground availability. Conservation actions: No legal protection or conservation activity. Conservation recommendations: Inventory and monitoring of remaining stock. Study Environ Biol Fish (2008) 83:169–170 DOI 10.1007/s10641-007-9311-9

The genus Cotylopus (Teleostei: Gobioidei) endemic to the rivers of islands of the Indian Ocean with description of a new species from Mayotte (Comoros)

Cotylopus rubripinnis, new species, is described on the basis of nine specimens collected from the Island of Mayotte (Comoros), Indian Ocean. Cotylopus rubripinnis differs from the only other known species in the genus (C. acutipinnis Guichenot, 1863) in usually having fewer scales in lateral (LS), transverse back (TRB), transverse forward (TRF), and zigzag series (ZZ), and in having pectoral, dorsal and caudal fins reddish. The genus was previously only known from the Mascarene Islands (Réunion and Mauritius). The discovery of a second species for that rare and endemic genus 1400 km farther to the north‐west in the Indian Ocean is discussed.

Evolution of Diadromy in Fish: Insights from a Tropical Genus (Kuhlia Species)

Diadromous species undergo regular migration between fresh and marine waters. This behavior is found in many species, including fish, mollusks, and crustaceans, some of which are commercially valuable species. Several attempts to trace the evolution of this behavior have been made in Salmonidae and Galaxiidae, but ambiguous phylogenies and multiple character state changes prevented unequivocal conclusions. The Kuhliidae family consists of 12 fish species that inhabit tropical islands in the Indo-Pacific region. The species have marine, partially catadromous, or fully catadromous life histories (i.e., they migrate from rivers to the sea to reproduce). The evolution of migratory behavior was traced on a well-resolved phylogeny. Catadromous Kuhlia species were basal, and partially catadromous and marine species formed derived monophyletic groups. This is, to our knowledge, the first time that a clear origin and polarity for the diadromous character has been demonstrated. We propose that the relative lack of resources in tropical, inshore, marine habitats and the ephemeral and isolated nature of freshwater environments of tropical islands, combined with phenotypic plasticity of migratory traits, play key roles in driving the evolution of diadromy in the Kuhliidae and probably in other groups. This work is an important starting point to understand the role of diadromy in speciation and adaptation in unstable habitats.

Stretched to the limit; can a short pelagic larval duration connect adult populations of an Indo-Pacific diadromous fish (Kuhlia rupestris)?

Freshwater species on tropical islands face localized extinction and the loss of genetic diversity. Their habitats can be ephemeral due to variability in freshwater run‐off and erosion. Even worse, anthropogenic effects on these ecosystems are intense. Most of these species are amphidromous or catadromous (i.e. their life cycle includes a marine larval phase), which buffers them against many of these effects. A long pelagic larval duration (PLD) was thought to be critical to ensure the colonization and persistence in tropical islands, but recent findings indicated that several species with short PLDs are successful in those ecosystems. To test the potential of a short PLD in maintaining genetic connectivity and forestalling extirpation, we studied Kuhlia rupestris, a catadromous fish species with an extensive distribution in the western Pacific and Indian Oceans. Using a combination of molecular genetic markers (13 microsatellite loci and two gene regions from mtDNA) and modelling of larval dispersal, we show that a short PLD constrains genetic connectivity over a wide geographical range. Molecular markers showed that the short PLD did not prevent genetic divergence through evolutionary time and speciation has occurred or is occurring. Modelling of larvae dispersal suggested limited recent connectivity between genetically homogeneous populations across the Coral Sea. However, a short PLD can maintain connectivity on a subocean basin scale. Conservation and management of tropical diadromous species needs to take into account that population connectivity may be more limited than previously suspected in those species.

Contrasting Genetic Structure among Populations of Two Amphidromous Fish Species (Sicydiinae) in the Central West Pacific

Both present-day and past processes can shape connectivity of populations. Pleistocene vicariant events and dispersal have shaped the present distribution and connectivity patterns of aquatic species in the Indo-Pacific region. In particular, the processes that have shaped distribution of amphidromous goby species still remain unknown. Previous studies show that phylogeographic breaks are observed between populations in the Indian and Pacific Oceans where the shallow Sunda shelf constituted a geographical barrier to dispersal, or that the large spans of open ocean that isolate the Hawaiian or Polynesian Islands are also barriers for amphidromous species even though they have great dispersal capacity. Here we assess past and present genetic structure of populations of two amphidromous fish (gobies of the Sicydiinae) that are widely distributed in the Central West Pacific and which have similar pelagic larval durations. We analysed sections of mitochondrial COI, Cytb and nuclear Rhodospine genes in individuals sampled from different locations across their entire known range. Similar to other Sicydiinae fish, intraspecific mtDNA genetic diversity was high for all species (haplotype diversity between 0.9–0.96). Spatial analyses of genetic variation in Sicyopus zosterophorum demonstrated strong isolation across the Torres Strait, which was a geologically intermittent land barrier linking Australia to Papua New Guinea. There was a clear genetic break between the northwestern and the southwestern clusters in Si. zosterophorum (φST = 0.67502 for COI) and coalescent analyses revealed that the two populations split at 306 Kyr BP (95% HPD 79–625 Kyr BP), which is consistent with a Pleistocene separation caused by the Torres Strait barrier. However, this geographical barrier did not seem to affect Sm. fehlmanni. Historical and demographic hypotheses are raised to explain the different patterns of population structure and distribution between these species. Strategies aiming to conserve amphidromous fish should consider the presence of cryptic evolutionary lineages to prevent stock depletion.