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Anchialine cave ecology

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Abstract

"Anchialine" was defined at the 1984 International Symposium on the Biology of Marine Caves as habitats that "consist of bodies of haline waters, usually with a restricted exposure to open air, always with more or less extensive subterranean connections to the sea, and showing noticeable marine as well as terrestrial influences." Such anchialine pools occur in both uplifed reef limestone and irregular porous lava flows. The water in these pools varies in salinity from nearly fresh to fully marine. Both salinity and degree of connection to the sea control the nature of the biota. Pools close to the sea contain typical marine species, while those farther inland have fewer but more unusual species.
... The anchialine macrofauna is dominated by multiple lineages of strikingly red-pigmented, cave-adapted, euryhaline caridean shrimps (Holthuis, 1963;Maciolek, 1983;Becking et al., 2011). Anchialine shrimps exhibit a suite of characters typical of cave-restricted crustaceans, such as reduced eyes, elongated appendages, and either depigmentation or red coloration (Holthuis, 1963;Maciolek, 1983, Iliffe, 2000. Such adaptations, particularly red coloration, are also typical of deep-sea crustaceans, and indeed cavernicolous species are hypothesized to have had deep-sea origins (Iliffe, 2000). ...
... Anchialine shrimps exhibit a suite of characters typical of cave-restricted crustaceans, such as reduced eyes, elongated appendages, and either depigmentation or red coloration (Holthuis, 1963;Maciolek, 1983, Iliffe, 2000. Such adaptations, particularly red coloration, are also typical of deep-sea crustaceans, and indeed cavernicolous species are hypothesized to have had deep-sea origins (Iliffe, 2000). ...
... Anchialine pools are distributed on tropical karstic shorelines and irregular porous lava flows (Holthuis, 1973;Maciolek, 1983;Iliffe, 2000;Becking et al., 2011). A significant number of anchialine shrimps have correspondingly broad, yet apparently highly disjunct distributions (e.g., Holthuis, 1963;Smith & Williams, 1981;Maciolek, 1983). ...
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Article
We document the current status of the enigmatic bright-red anchialine shrimps in Tiniguiban Islet in the western Visayas region of the Philippines. A second epigeal anchialine pool was discovered in nearby Hinlaran Islet, and two shrimp species were recorded in the pools, the large barbouriid Parhippolyte uveae Borradaile, 1900 as previously reported and a much smaller atyid Antecaridina lauensis (Edmondson, 1935). The shrimps move in and out of the pools with tidal fluctuations, since both pools completely dry out at low tide. The shrimps remain very abundant in Tiniguiban despite extensive modifications made by its owners and an apparent decrease in dissolved oxygen levels. Magico-religious beliefs regarding these unusual red shrimps persist, yet a subtle shift in values is noted, particularly with the growing popularity of the Tiniguiban pool with local tourists. Further modernization and coastal development may rapidly threaten these rare shrimp populations. Our study provides baseline data for systematic study and future protection of these rare pools and their shrimps that uniquely dwell at the interface of cave and marine habitats.
... Anchialine caves are subterranean aquatic habitats situated inland from the coast and containing tidally fluctuating brackish or marine waters (Sket, 1996;Iliffe, 2000;Iliffe & Kornicker, 2009). They occur as pools or flooded tunnels in karstic limestone caves or in volcanic lava tubes. ...
... In addition to numerous taxonomic articles on anchialine cave crustaceans, a variety of books, book chapters, and journal articles over the years have covered numerous associated topics in anchialine research. Examples of recent work includes anchialine ecology (Sket, 1996;Iliffe, 2000), biodiversity , morphology (Mejía-Ortíz et al., 2013), physiology (Bishop & Iliffe, 2012), biogeography (Jurado-Rivera et al., 2017), molecular phylogeny (von Reumont et al., 2012), food web and chemosynthesis (Brankovits et al., 2017), brain and nervous system (Stegner et al., 2015), reproduction (Kubrakiewicz et al., 2012), larval development (Olesen et al., 2014), conservation (Mercado-Salas et al., 2013), and collection (Watling, 2016 for miscellaneous groups; Yager, 2016 for remipedes; and Ng, 2017 for decapods). All such studies have required cave divers for specimen collection. ...
... Research has been supported by multiple grants from the US National Science Foundation, National Oceanic and Atmospheric Administration, National Geographic Society, and others. This article is dedicated to the memory of collaborating taxonomists Thomas Bowman (1918-1995, Jan Stock (1931-1997), Mihai Băcescu (1908-1999, Raymond Manning (1934-2000, Brian Kensley (1944Kensley ( -2004, and Lazare Botosaneanu (1927Botosaneanu ( -2012, as well as cave divers Sheck Exley (1949-1994), Rob Palmer (1952-1997), Rob Parker (1962-1997), Wes Skiles (1958-2010), and Agnes Milowka (1981-2011, all of the latter tragically perishing in diving accidents. Without their support, these investigations would never have been possible. ...
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Anchialine caves are inland, salinity stratified, submerged caves in limestone or volcanic basalt, whereas marine caves are located offshore, completely beneath the seafloor. These caves contain a remarkable biodiversity, with numerous, new higher taxa being recorded in recent decades. While some faunas are Tethyan relicts with highly anomalous distributions, others have relatives inhabiting the deep sea. Cave diving is an essential tool for investigating these wholly submerged environments. As an option to standard open circuit scuba, closed circuit rebreathers provide extended dive time and minimize disturbances to the animal life. Collection techniques involve the use of plankton nets, individual vials, suction bottles, and baited traps. Preservatives include ethanol, RNA-later or special fixatives, depending upon their ultimate purpose.
... The water exchange of anchialine caves with other marine habitats is severely restricted, resulting in the relatively independent environments and special physical-chemical parameters in these caves (Iliffe and Kornicker, 2009;Pakes, 2013;Pérez-Moreno et al., 2016). Little or no photosynthetic oxygen production, stratified water columns and restricted vertical mixing contribute to the anoxic or micro-oxic environment and hydrogen sulfide in anchialine caves (Iliffe, 2000;Seymour et al., 2007;Becking et al., 2011;Gonzalez et al., 2011). ...
... The unique abiotic factors such as dissolved oxygen (DO) concentration, water stratification and temperature in anchialine caves make them natural laboratories for studying marine biodiversity and biological adaptation and evolution. A number of studies on the phytoplankton, zooplankton and benthos in anchialine caves have been performed (Iliffe, 2000(Iliffe, , 2004Bishop et al., 2004;Gerovasileiou et al., 2016), resulting in the description of numerous new species and cognitions previously unknown to science (Iliffe, 2002;Pérez-Moreno et al., 2016). Yager (1981) isolated four new individuals, namely, Remipedia (new class), Speleonectidae (new family), Speleonectes (new genus) and Speleonectes lucayensis (new species) from Lucayan Cavern on Grand Bahama Island, Bahamas. ...
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Article
The Sansha Yongle Blue Hole is the deepest blue hole in the world and exhibits unique environmental characteristics. In this paper, Illumina sequencing and qPCR analysis were conducted to obtain the microbial information in this special ecosystem. The results showed that the richness and diversity of bacterial communities in the hole was greater than those of archaeal communities, and bacterial and archaeal communities were dominated by Proteobacteria and Euryarchaeota, respectively. Temperature and nitrate concentration significantly contributed to the heterogeneous distribution of major bacterial clades; salinity explained most variations of the archaeal communities, but not significant. A sudden increase of bacterial 16S rRNA, archaeal 16S rRNA, ANAMMOX 16S rRNA, nirS and dsrB gene was noticed from 90 to 100 m in the hole probably due to more phytoplankton at this depth. Sulfur oxidation and nitrate reduction were the most abundant predicted ecological functions in the hole, while lots of archaea were predicted to be involved in aerobic ammonia oxidation and methanogenesis. The co-occurrence network analysis illustrated that a synergistic effect between sulfate reduction and sulfur oxidation, and between nitrogen fixation and denitrification, a certain degree of coupling between sulfur and nitrogen cycle was also observed in the hole. The comparisons of bacterial and archaeal communities between the hole and other caves in the world (or other areas of the South China Sea) suggest that similar conditions are hypothesized to give rise to similar microbial communities, and environmental conditions may contribute significantly to the bacterial and archaeal communities.
... Despite their broad range of habitats and environmental tolerance, the presence of polynoids in anchialine caves is exceptional. Only Gesiella jameensis (Hartmann-Schröder, 1974), known only from a lava tube and adjacent crevicular habitats on Lanzarote (Canary Islands), and Pelagomacellicephala iliffei Pettibone, 1985, described from anchialine caves of the Caicos and Great Bahama Bank in the Caribbean (Hartmann-Schröder, 1974;Pettibone, 1985;Gonzalez et al., 2017), are known to occur in this highly demanding environment, characterized by total darkness, lack of photosynthesis, limited exposure to atmospheric oxygen and reduced organic nutrient cycling (Iliffe, 2000). Both taxa share several features presumed to be adaptations to the cave environment, such as swimming habits and presence of long dorsal parapodial cirri (Gonzalez et al., 2018b(Gonzalez et al., , 2021. ...
Article
A remarkable new genus and species of scale worm (Annelida: Polynoidae) was found on the bottom sediments of an anchialine cave on the island of Mallorca (Balearic Islands, western Mediterranean). Specimens reach up to 2 cm long, lack eyes and body pigmentation except for a few scattered minute speckles and show enlarged parapodia and sensorial appendages. A red brain is visible through the translucent tegument. Morphological features resemble those of Eulagiscinae, currently comprising eight species in three genera. Phylogenetic analyses of mitochondrial and nuclear DNA sequences are not conclusive on the position of the new taxon but affinity to Eulagiscinae is not ruled out, particularly when taxa with missing data or non-homologous insertion sites are excluded from the analyses. Pollentia perezi gen. & sp. nov. is characterized by a unique set of morphological features: 13 pairs of dorsal elytra; a single type of notochaetae (stout, with spinous rows and pointed tip); and two types of neurochaetae (superior flattened, spinous with tridentate tip; inferior shorter and thinner, lanceolate and pectinate). Some characteristics, such as the long parapodial appendages and swimming habits, are shared with other cave scale worms. However, the new taxon is not closely related to the other two known cave-dwelling polynoids.
... The Crystal and Wonderland Cave sections of the Walsingham System ( Figure 1C) are off the main flow channels where circulation patterns are restricted. Their residence times are much longer, with the phreatic zone consisting of very clear, slowly moving or stagnant waters with a lower surface salinity [14]. Caves with greater water transport, e.g., Palm Cave System ( Figure 1D), have surface waters only slightly diluted and reach normal marine salinity (35-36 ppt) below 1 m depths. ...
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Article
Bermuda is an Eocene age volcanic island in the western North Atlantic, entirely capped by Pleistocene eolian limestone. The oldest and most highly karstified limestone is a 2 km2 outcrop of the Walsingham Formation containing most of the island’s 150+ caves. Extensive networks of submerged cave passageways, flooded by saltwater, extend under the island. In the early 1980s, cave divers initially discovered an exceptionally rich and diverse anchialine community inhabiting deeper sections of the caves. The fauna inhabiting caves in theWalsingham Tract consists of 78 described species of cave-dwelling invertebrates, including 63 stygobionts and 15 stygophiles. Thus, it represents one of the world’s top hotspots of subterranean biodiversity. Of the anchialine fauna, 65 of the 78 species are endemic to Bermuda, while 66 of the 78 are crustaceans. The majority of the cave species are limited in their distribution to just one or only a few adjacent caves. Due to Bermuda’s high population density, water pollution, construction, limestone quarries, and trash dumping produce severe pressures on cave fauna and groundwater health. Consequently, the IUCN Red List includes 25 of Bermuda’s stygobiont species as critically endangered.
... Most marine blue holes in the world belong to the offshore blue hole which are wholly submerged beneath the seafloor. Some of blue holes can exchange water with the open sea by tides [1], while the exchange between some blue holes and the open seas is limited, resulting in the relatively stable internal environment and unique physical-chemical characteristics, such as a strong thermo-halocline, a highly stratified water column, and thick anoxic and hydrogen sulfide-rich layers [2][3][4][5][6][7][8]. ...
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Article
We report an Illumina high-throughput sequencing protocol of eukaryotic microbes in the world’s deepest marine blue hole, Sansha Yongle Blue Hole, Xisha, South China Sea. The variable V9 region of small subunit (SSU) rDNA, was sequenced using this approach from the waters of blue hole and outer reef slope. 917,771 unique eukaryotic 18S rRNA gene sequences and 6093 operational taxonomic units (OTUs) were identified. Significant differences in the eukaryotic composition were observed between the blue hole and outer reef slope, and the richness in the blue hole was much higher than that in the outer reef slope. The richness and diversity of eukaryotes in the blue hole were both lowest at 60 m and highest at 100 m depth. Eukaryotic microalgae assemblages dominated by Dinophyceae were the most abundant in the 10–20 m water column in the hole. Fauna was the main group at and below a depth of 60 m, where Araneae and Cyclopoida were dominant in the 60 m and 80 m water layer, respectively. There was a large number of Entoprocta at a depth of 180 m in the hole, where little oxygen was detected. Turbidity and nitrite concentration had a significant effect on the eukaryote community structure (p < 0.01).
... Interest in the biodiversity of anchialine NOTES 294 caves has increased in recent years as more sites are explored and new species are discovered (Iliffe 2000). The fauna appears to be dominated by crustaceans and many anchialine species show high levels of endemism (Iliffe 1992). ...
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Article
Macrobrachium carcinus is reported for the first time from the Cayman Islands. Specimens were collected on multiple occasions from an unusual habitat for this species – an anchialine cave. It is likely the cave was colonized by M. carcinus larvae via movement through subterranean karst tunnels from the sea inland to the cave entrance. Because only juveniles were collected, it is uncertain whether reproduction is occurring in this cave. However, it is possible M. carcinus may continue to colonize this and other similar caves, and sustained populations may eventually become established on Grand Cayman.
... Blue holes are sinkholes: vertical, water-filled karst features open to the surface (Mylroie et al., 1995). Inland blue holes of the Bahamas are anchialine caves (Iliffe, 2000), landlocked bodies of water with subterranean connections to the ocean containing meromictic water columns with an upper freshwater lens separated from a lower saltwater column by a stable halocline (Seymour et al., 2007;Gonzalez et al., 2011). Each blue hole displays distinct geochemical traits, making them unique natural laboratories that allow exploring the limits of photosynthesis and the interplay between biotic and abiotic sulfur cycling. ...
... Blue holes are sinkholes: vertical, water-filled karst features open to the surface (Mylroie et al., 1995). Inland blue holes of the Bahamas are anchialine caves (Iliffe, 2000), landlocked bodies of water with subterranean connections to the ocean containing meromictic water columns with an upper freshwater lens separated from a lower saltwater column by a stable halocline (Seymour et al., 2007;Gonzalez et al., 2011). Each blue hole displays distinct geochemical traits, making them unique natural laboratories that allow exploring the limits of photosynthesis and the interplay between biotic and abiotic sulfur cycling. ...
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Article
We report extremely low-light-adapted anoxygenic photosynthesis in a thick microbial mat in Magical Blue Hole, Abaco Island, The Bahamas. Sulfur cycling was reduced by iron oxides and organic carbon limitation. The mat grows below the halocline/oxycline at 30 m depth on the walls of the flooded sinkhole. In situ irradiance at the mat surface on a sunny December day was between 0.021 and 0.084 μmol photons m-2 s-1, and UV light (<400 nm) was the most abundant part of the spectrum followed by green wavelengths (475–530 nm). We measured a light-dependent carbon uptake rate of 14.5 nmol C cm-2 d-1. A 16S rRNA clone library of the green surface mat layer was dominated (74%) by a cluster (>97% sequence identity) of clones affiliated with Prosthecochloris, a genus within the green sulfur bacteria (GSB), which are obligate anoxygenic phototrophs. Typical photopigments of brown-colored GSB, bacteriochlorophyll e and (β-)isorenieratene, were abundant in mat samples and their absorption properties are well-adapted to harvest light in the available green and possibly even UV-A spectra. Sulfide from the water column (3–6 μmol L-1) was the main source of sulfide to the mat as sulfate reduction rates in the mats were very low (undetectable-99.2 nmol cm-3 d-1). The anoxic water column was oligotrophic and low in dissolved organic carbon (175–228 μmol L-1). High concentrations of pyrite (FeS2; 1–47 μmol cm-3) together with low microbial process rates (sulfate reduction, CO2 fixation) indicate that the mats function as net sulfide sinks mainly by abiotic processes. We suggest that abundant Fe(III) (4.3–22.2 μmol cm-3) is the major source of oxidizing power in the mat, and that abiotic Fe-S-reactions play the main role in pyrite formation. Limitation of sulfate reduction by low organic carbon availability along with the presence of abundant sulfide-scavenging iron oxides considerably slowed down sulfur cycling in these mats.
Chapter
The anchialine ecosystem is comprised of land-locked habitats of mixohaline (i.e., salinity of 0.5–30 ppt) water with simultaneous subterranean connections to the ocean and groundwater aquifers that occupy basins of varying geologic origins. Anchialine habitats are ephemeral features (natural senescence can begin in as little as 100 years); while originally formed in young lava flows or ancient limestone reefs, they eventually experience senescence as they gradually fill in over-time with sand, silt, and sediment from abiotic and biotic sources. These habitats are distributed throughout the globe but the largest concentration occurs in the Hawaiian Islands, with over 700 documented habitats being home to a number of unique plants and animals. The biota of the Hawaiian anchialine ecosystem can be characterized by eight shrimp and one crab species, many of which are considered endemic. Very little is known about this ecosystem and its elusive biota and threats to these unique habitats may mean we never get the chance; it is estimated that already more than 90% of Hawaiʻi's anchialine habitats have been lost or degraded by anthropogenic activities. While direct destruction of Hawaiian anchialine habitats from coastal development has eased significantly in recent years due to increased legal protections, major threats still include reduced water quality from runoff or dumping, overharvesting for the aquarium trade, and global climate change. Besides coastal development, invasive species remains one of the greatest threats to anchialine habitats in the islands. For example, alien predators have invaded over 95% of habitats in West Hawaiʻi and have the ability to significantly impact endemic shrimp populations. Invasive plants can also alter nutrient availability and extraneous detritus can lead to accelerated senescence of habitats. Despite these significant challenges, multiple organizations, groups, and individuals have dedicated themselves to helping restore this threatened ecosystem in the Hawaiian Islands and protecting it for future generations.
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