Shallow gas seeps in the Golfo Dulce, South Pacific of Costa Rica: geological, physicochemical, and biological characterization

doi:10.21203/rs.3.rs-3631742/v1

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Shallow gas seeps in the Golfo Dulce, South Pacific of Costa Rica: geological, physicochemical, and biological characterization

https://doi.org/10.21203/rs.3.rs-3631742/v1

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Methane is a greenhouse gas with a heat absorption capacity 25 times greater than CO₂, potentially playing a significant role at the atmospheric level. Thus there is a growing interest about studying the diversity and ecology of habitats that are important contributors of this gas to the atmosphere. This research aims to carry out a geological, physicochemical, and biological description of a superficial gas seepage in the tropical waters of the Golfo Dulce in Costa Rica. To study this environment underwater visual censuses of fish and bottom cover were conducted, along with collection of water samples for nutrient analysis, and gas to determine the composition of emissions. In addition, rock samples were collected to determine the geological origin and the associated cryptofauna. The seeps are composed of 49.5% methane and the rock that makes up the platform is sandstone from the Charco Azul Group. The bottom cover is dominated by sand (20%), hydrozoans (18%), and 12% of the «other» category. A total of 18 species of fish were found, and wrasses (Labridae) were the dominant group. Regarding cryptofauna, a total of 93 taxa were recorded. This study presents a new report of the ghost shrimp Biffarius for the Eastern Tropical Pacific. This ecosystem presents unique features because it is a shallow, highly diverse place, with a structure of the biological community different from what it is known for the Pacific coast of Costa Rica and the region. Knowing the above, it is recommended to establish conservation strategies.

Methane seep

macrofauna

biodiversity

benthic communities

coastal habitats

tropical like-fjord

Biogenic methane (CH₄) in the atmosphere is mainly derived from microbial mineralization under strictly anaerobic conditions (Wang et al. 1996), and can be oxidized in terrestrial, aquatic, or atmospheric zones to produce carbon dioxide (CO₂) (Wigley and Schimel 2000). There is a growing concern about the rising levels of atmospheric methane in the last decades, as it has been recognized as a critical greenhouse gas due to its 25-fold thermal absorption capacity compared to CO₂ (Ramaswamy 2001; Fletcher and Schaefer 2019; Scoones 2023). Despite the increasing research on the natural and anthropogenic pathways of global CH₄, measuring this gas still poses significant challenges. Comparisons between studies usually present uncertainties since different data sources and methodologies are used, and some of these have proven to underestimate CH₄ levels (Saynes et al. 2016; Wolf et al. 2017).

Regarding the natural sources of methane, wetlands are considered among the largest contributors representing over 20% of global annual emissions, while other contributions occur through transport from the Earth’s crust, as in volcanic eruptions and biological processes in aquatic ecosystems (Wang et al. 1996). The open ocean contributes little to natural emissions (Rhee et al. 2009; Change 2013). Other studies have estimated that coastal areas and the continental shelf could contribute about 50 % of the naturally occurring methane in the atmophere (Etiope and Klusman 2002; Etiope et al. 2008). Marine sediments can store large amounts of biogenic methane, releasing it as bubbles that dissolve in the water, producing high methane concentrations at the sea bottom (Mau et al. 2007; Schneider von Deimling et al. 2011). Marine seepages are one of the ocean's main reservoirs and sources of methane (Fujikura et al. 1999; Domack et al. 2005; Leifer et al. 2006; Dando 2010).

Descriptive and ecological studies on methane seeps have been increasing in recent years, showing remarkable specificities according to its location and environmental conditions, with a growing interest of the community in these habitats (Childress et al. 1986; MacAvoy et al. 2005; Levin and Mendoza 2007; Macavoy et al. 2008; Thurber et al. 2010; Levin et al. 2015, 2017).) A common characteristic of many species living in rich methane environments is their potential to use methane as a carbon source mainly through chemosymbiotic relationships (Thurber et al. 2010).

It has been reported that in shallow cold methane seeps (less than 100 m), a chemosymbiont community does not develop like in deep-sea methane seeps (Savvichev et al. 2004; Levin 2005). Some of the most renowned organisms associated with deep-sea methane seeps are Bathymodiolus mussels, siboglonid tubeworms, vesicomyd clams, provannid gastropods, alvinocarid shrimps, kiwa crabs, and galatheid squat lobsters (Childress et al. 1986; Macavoy et al. 2008; Levin et al. 2012). However, Vedenin et al. (2020) reported the presence of species typical of reducing environments in shallow cold methane seeps, such as siblogloinid worms and thiasirid bivalves.

Golfo Dulce, located in the southern Pacific of Costa Rica, has characteristics that can favor the presence of shallow-water biogenic methane emissions, such as 1) low availability of oxygen due to water circulation patterns, 2) high availability of nutrients, and 3) steep slopes that produce abrupt changes in depth despite the proximity to the coast (Quesada-Alpízar and Cortés 2006). In 2012, shallow gas emissions were observed and studied in Golfo Dulce (Wild et al. 2015). This study aims to describe the geological, physicochemical, and biological attributes of the shallow methane seepage found in this gulf. Our objectives are: 1) describing the origin and composition of the minerals of the rocky platform present at the shallow methane seepage, 2) characterizing the physicochemical parameters of the water column in the areas surrounding the shallow methane seep, and 3) determining the biological assemblage associated with the shallow methane seep.

Study site

Golfo Dulce (08°40' N; 83°20' W) is an embayment of approximately 50 km length and 10–15 km width, with an area of ~ 700 km² (Dean 1997; Quirós 2003) (Fig. 1a). This gulf has been referred as a “tropical like-fjord” because its geomorphological and bathymetric characteristics resemble that of a fjord (Hebbeln and Cortés 2001): depth at the inner area is ~ 200 m deep and only ~ 75 m at the mouth. This results in circulation patterns that drive the oxygen, nutrient, and temperature in Golfo Dulce similarly to a fjord (Acuña-González et al. 2006; Morales-Ramírez and Nowaczyk 2006; Svendsen et al. 2006). For example, the average temperature is 30°C in the surface and 14°C at the deepest area (Richards et al. 1971) which also presents anoxic conditions (Ferdelman et al. 2006). Golfo Dulce was declared a Responsible Marine Fishing Area in 2010 (Salas et al. 2012).

Here in 2012, Wild et al. (2015) observed gas emissions from a shallow carbonate platform (Fig. 1a, b). This site is a shallow platform at 10 m depth, presenting cold gas emissions which were composed > 85% methane, with a carbonate platform of 100 m² rising 2 m above the surrounding soft-sediment bottom. The gas emissions had temperatures ranging from 28°C to 31°C, which places them closer to cold seeps than hydrothermal vents (Wild et al. 2015). The signature of the δ13C carbon isotopic analysis resulted from -47‰ to །51‰, indicating that it originates from the anaerobic oxidation of methane and the biogenic and autogenic formation of carbonates (Wild et al. 2015). The biological and physicochemical attributes of this type of cold methane emissions of biogenic origin have been described worldwide (Naehr et al. 2000; Judd and Hovland 2007; Pierre et al. 2014).

Sampling design

Sampling was carried out on March 28, 2019, and February 13, 2020, using SCUBA. Five steel rods were spaced 6 m apart on the carbonate platform marking the start of six survey transects (Fig. 1c). A 50 m tape measure was placed parallel to the shoreline at the beginning of each survey transect. All five transects were used for bottom cover censuses, and three for fish surveys. Each transect was divided in three sections: 0 to 10, 20 m to 30 m, and 40 m to 50 m (Fig. 1c). There is a gradient of proximity to the coast between the survey transects, where transect 1 is the closest and shallowest, and 5 is the farthest and deepest.

To determine the geological origin of the rocks in the platform, two blocks of rocks (~ 15 cm in radius) were collected during each visit. After a visual inspection, the rocks with the least bioerosion were selected to obtain the most compact solid rock for analysis. After collection, the living organisms were removed in the laboratory using tweezers, and the rock samples were washed with soap and water and dried in the open air for 48 hours (Alfaro et al. 2018). To describe and identify the rocks, thin sections were cut and observed with a petrographic microscope to count and identify the minerals that make up the rocks. This analysis was conducted in the Petrography Laboratory of the Escuela Centroamericana de Geología of the Universidad de Costa Rica (UCR).

To collect gas samples, VWR® Storage bottles 200 ml were placed upside-down over the gas emission holes on the platform. Five bottles were collected in 2019 and three in 2020. The chemical composition of the gas was determined by gas chromatography technique using a Thermo Scientific gas chromatograph, model Trace 1300, with a Thermo Scientific TracePLOT TG-Bond MSieve PLOT 30 m, 0.53 mm ID column at the Centro de Investigación en Electroquímica y Energía Química (CELEQ) of the UCR.

For nutrient analysis, a bottom water sample was taken in an amber bottle and kept cold until processed. The nutrients considered for the study were: phosphate, silicate, ammonium, nitrite, and nitrate. A Constant Flow Autoanalyzer (FIA) was used for nutrient determination. The analysis was carried out at Centro de Investigación en Ciencias del Mar y Limnología (CIMAR) of the UCR.

The Point Intercept Technique (PIT) was used to determine the bottom composition (Segal and Castro 2001). A measuring tape was placed along 50 m of the surveying transects in the platform for this technique. The 50 m were divided into 10 m transects (Fig. 1c). The PIT was carried out on five transects (Fig. 1c). On each transect, the type of bottom immediately below the tape each 50 cm was identified and recorded. Bottom cover categories were determined by species for macroalgae and corals; nevertheless, other observed groups were classified into broader groups: sponges (Porifera), hydrozoans, octocorals, turf, and others. In addition, categories such as rock, rubble and sand were included.

The composition of fishes was estimated using a tunnel census, consisting of underwater visual fish surveys 10 m long, 5 m wide, and 5 m high (Alvarado et al. 2015) (Fig. 1c). In three of the five surveying transects (firs, middle, and last transects), three 10 m tunnel surveys were conducted from 0–10 m, 20–30 m, and 40–50 m (Fig. 1c). On census, the fish species were identified, counted, and measured, according to Alvarado et al. (2015). The PIT and fish surveys were carried out only during 2019, since strong currents during 2020 precluded these surveys.

To assess the cryptic fauna associated with the carbonate platform rocks in the gas emission site, five blocks of rock of approximately 15 cm radius were haphazardly collected from different parts of the carbonate platform. Each block was placed in a bag with seawater and sealed. The block was submerged in a seawater solution with magnesium chloride to relax and separate the organisms inhabiting the rock. Then, the rock was carefully examined on a tray with seawater and slowly fragmented with a hammer and chisel, removing the cryptic fauna with tweezers until all the rock fragments were under 1 cm in diameter. All the specimens were preserved in 70% alcohol. The fauna was identified at the lower taxonomic level possible and counted in the laboratory, using regional taxonomic keys: decapods crustaceans (Rathbun 1918, 1930, 1931; Holthuis 1951; Haig 1960; Kim and Abele 1988; Kropp 1989), mollusks (Keen 1971; Skoglund 1992), stomatopods (Salgado-Barragán and Hendrickx 2010), brittle stars (Clark 1940), and polychaetes (Fauchald 1977).

Data analysis

A Permutational Multivariate Analysis of Variance (One-way PERMANOVA) was performed to determine the taxa composition variation along the carbonate platform (transect) position for both bottom cover and fish assemblage. A species accumulation curve (± 95% confidence limits) was estimated using the sample-based rarefaction with Mao's tau method to determine if the sampling recorded the higher possible number of taxa and to estimate the maximum number of taxa present among samples of cryptic fauna among samples. All the analyses were performed using PAST 4.13 (Hammer et al., 2001).

The rock that makes up the platform is a fine greenish-grey sandstone. It has a fine mud matrix of 60% and 40% siliciclastic with highly weathered grains, and the mineralogical characteristics are rarely observable. Of the 60% of the matrix, 35–40% are lithoclasts, 5% feldspars, and both quartz and foraminifera make up less than 1%. The angularity of the rock goes from subrounded to subangular, the contacts between the grains are of the floating type, it does not have sedimentary structures, and it is classified as a sandy, silty clayey rock. Observed grain types and weathering are considered indicators of reworking. In addition, it presents perforations of around 2 cm due to bioturbation. Based on this information, the rocks are classified as highly weathered lithoclasts of volcanic origin, producing scarce plagioclase and highly degraded unrecognizable quartz. The smallest foraminifera are rare. According to the characteristics of the rock and the geographical location, it was determined that it belongs to the Charco Azul Group (Olsson 1942).

The gas emission samples were predominantly composed by methane, with an average mass/volume percentage of 53 ± 5% (2019) and 46 ± 5% (2020). The analysis found less than 6% of H₂ and less than 2% of CO₂, but these values are below the detection limit of the methodology used in this study.

Regarding the concentration of nutrients, silicate values ranged from 6.47 to 20.96 µmol l^− 1, while phosphate was not detected in 2019, but in 2020 it was found in a concentration of 0.29 µmol l^− 1 on the surface and 0.32 µmol l^− 1 on the bottom. Nitrate, nitrite, and ammonia were variable (Table 1).

Table 1

Nutrient concentration (mean ± incertitude) at a shallow methane seep in Golfo Dulce, southern Pacific coast of Costa Rica. Minimum detection levels (µmol l^− 1): silicate = 1.63; nitrate = 0.30; nitrate = 0.37; ammonium = 0.36; phosphate = 0.08. nq: not quantifiable.
Year	Sample	Nutriments (µmol l^− 1) ± inc
Year	Sample	Silicate	Nitrate	Nitrite	Ammonium	Phosphate
2019	Surface	20.96 ± 2.33	5.71 ± 0.39	5.03 ± 0.46	3.83 ± 0.46	nq ± 0.12
2020	Surface	8.59 ± 1.83	10.41 ± 0.52	8.18 ± 0.29	1.83 ± 0.41	0.29 ± 0.18
2020	Bottom	6.47 ± 1.85	11.31 ± 0.55	8.67 ± 0.29	1.74 ± 0.41	0.32 ± 0.18

The bottom cover was dominated by sand (20%), hydrozoans (18%), and "others" (12%), mainly including coralline calcareous algae (CCA) and octocoral genera, such as Carijoa, Leptogorgia, and Pacifigorgia. Only 5% of the overall cover was, the order Gelidiales and the genera Dictyota and Halimeda being the most common (Fig. 2). The turf was relatively common in three of the transects. Only one species of reef-forming coral was observed, Porites lobata, with a cover of 1.9%. The colonies of P. lobata present an encrusting growth, and small sphere-shaped colonies were found on the edges of the platform, unattached from the bottom, also called “free-living rolling stones” coral colonies (Scoffin et al. 1985; Riegl et al. 1996).

Significant differences were found between the bottom cover between the different surveying transects (One-way PERMANOVA, F = 4.46; p = 0.0001). The bottom coverage varied among the transects without following a particular gradient, transects 1, 3, 4, and 5 have a similar trend, although with variation among them, and on the other hand, transect two is separated much more by the categories that compose it. The turf contributed the most (20%) to the differences among transects Table S1 (Online Resource 1) but does not show a clear trend between the transects, while the categories sand and cyanobacteria contributed 11.4 and 11.2%, respectively (Online Resource 1). The scleractinian coral P. lobata was only observed in Transect 2 (9.5% cover in transect 2, but only 3.7% overall). The macroalgae was most common in transect 2 (17.5% cover), and this category contributed to 9.4% of the differences between the transects Table S1 (Online Resource 1). Hydrozoans were commonly found in the platform, with a percentage higher than 17% in all transects, except transect 2 (1.6%, Fig. 2), and contributing to 12.5% of the differences Table S1 (Online Resource 1).

Regarding the fish ensemble associated with the gas emission platform, a total of 2,274 individuals were recorded from 18 species. Halichoeres dispilus had the highest abundance (1,170 ind), followed by Thalassoma lucasanum (944 ind) Table S2 (Online Resource 2). These two wrasses made Labridae the most common family, comprising 93% of the total number of fishes. Other species found in lower abundances were: Haemulon steindachneri (3.07%), Chaetodon humeralis (1.20%), Stegastes flavilatus (0.75%), and Suflamen verres (0.75%) (Online Resource 2). Labridae, Pomacentridae, and Serranidae were represented by three species each, followed by Lutjanidae and Chaetodontidae, with two species Table S2 (Online Resource 2).

The results showed no significant differences in the fish assemblage composition associated with the surveying transects (One-way PERMANOVA, F = 1.267; p = 0.2699). One species, H. dispilus, contributed to 50.5% of the differences between surveying transects, followed by 37.9% from T. lucassanum, while all other fish species contributed < 15% Table S3 (Online Resource 3).

The cryptic fauna associated with the rocks included 403 individuals considering data from 2019 and 2020, distributed in 92 taxa (species and morphospecies), 47 families, 21 orders, seven classes, and six phyla Table S4 (Online Resource 4). The phylum with the highest representation of individuals was Arthropoda, with 39% of the relative abundance, followed by Annelida with 32%, and Mollusca with 24%. The most abundant families were Mytilidae (16%), Alpheidae (15%), Porcellanidae (10%), (8%), and Eunicidae (8%). The average (± SD) of the number of taxa per rock was 17.20 ± 10.59. No significant differences were detected between the sampling years (One-way PERMANOVA, F = 0.5315, p = 0.8376). In 2019, 60 taxa were found, and in 2020 a total of 57 taxa, 25 of which are shared between both years Table S4 (Online Resource 4). The ghost shrimp genus Biffarius is reported as a new record for the Eastern Tropical Pacific.

The species accumulation curve computed for the ten rock samples has a steep slope not reaching an asymptote (Fig. 3). The rarefaction curves computed for each rock sample suggest that the overall diversity of cryptic fauna was lowest in CH4-10 and the highest were CH4-03.

In Golfo Dulce, the marine coastal and pelagic ecosystems have been relatively well studied in the last decades, including coral reefs, rocky bottoms, mangroves, and seagrasses (Quesada-Alpízar and Cortés 2006; Palacios-Martínez 2015; Chacón-Chaverri et al. 2015). Despite the report of these shallow methane emissions in Golfo Dulce (Wild et al. 2015), there is a knowledge gap on the ecological characteristics that remains to be studied. Other methane emissions have been studied in Costa Rican waters in offshore deep locations (Karaca et al. 2012, Levin et al. 2012, Krause et al. 2014, Levin et al. 2015; McCowin et al. 2020; Rouse and Kupriyanova 2021). In the convergent margin off the coastline of Costa Rica, there is an advection of fluids highly loaded with methane, up to 90 % in gas volume, which causes the formation of cold seeps (Krause et al. 2014). Among the environments tht have been described are extrusions and mud volcanoes on the Nicoya Peninsula, cold methane emissions near Quepos Slide (≈ 400 m) (Karaca et al. 2012), and hydrothermal windows off Parrita (≈ 1900 m), Quepos (999 to 1900 m) and Jacó Scar (1817 m) (Levin et al. 2012, 2015; McCowin et al. 2020; Rouse and Kupriyanova 2021).

During our study, we found a methane saturation of 49.5% in Burbujas site, in contrast to the > 85% reported by Wild et al. (2015). The composition of gas emissions from the seabed can be highly variable depending on various factors, such as telluric movements (Li et al. 2021; Yang et al. 2021). Golfo Dulce is a geologically active site (Malzer and Fiebig 2008), thus it is expected that there will be variations. However, these differences in the amount of methane in the gas can have implications for biological communities, so it is important to regularly monitor this site.

On the other hand, very low oxygen saturations were reported near the bottom of our study site, even below the detection limit, which was 0.5 µM, as opposed to the water column, which is highly oxygen-loaded (Wild et al. 2015). In the Gulf, it has been reported that below 30 m depth, dissolved oxygen has values of less than 10 % (Vargas-Zamora et al. 2021); in the study site it is lower despite being shallower, this is due to the seepage of gases. It is known that in the internal part of the gulf, there is a rapid decrease in oxygen, and this pattern also occurs with nitrates and in a similar way with nitrites (Thamdrup et al. 1996; Acuña-González et al. 2006; Quesada-Alpízar and Cortés 2006).

Regarding the concentrations of nutrients, we found low values for phosphate compared to previous reports for Golfo Dulce, where it increases around 80 m deep (Morales-Ramírez et al. 2015). Silicate had lower concentrations at the bottom than the surface during this study, in agreement with previous findings in Golfo Dulce (Morales-Ramírez et al. 2015). Similar to Morales-Ramírez et al. (2015), no clear trends were found for nitrites and nitrates.

From the analysis of the rock composition, it can be interpreted that the gas emission platform is mainly integrated by a sandstone belonging to the Charco Azul Group in its Paleogene section. Charco Azul rose above the sea and later began to sink, which allowed the formation to undergo a transgression process (Kriz 1990). Charco Azul is of interest within this area because the first gold concentrations of the Golfo Dulce have been found in its basal sediments (Kriz 1990). Fossil organisms of the families Naticidae, Buccinidae, Muricidae, Cancellariidae, Melongenidae, and Terebridae have been found in the Charco Azul group (Aguilar et al. 2010). In our study, only the family Muricidae was present.

The Golfo Dulce is in a geologically active region where the Cocos tectonic plate is subducting under the Caribbean plate. Therefore, in the geological history of the area where the Golfo Dulce is located, telluric movements have actively participated in its formation (Fischer 1980; Kriz 1990). The tectonic activity associated with this area has caused the collapse of crustal blocks and subsequent flooding, thus forming a deep basin with characteristics that cause unique ecosystems (Córdoba and Vargas 1996; Hebbeln et al. 1996). These and other characteristics such as 1) low oxygen availability due to water circulation patterns, 2) it is a nutrient-rich environment, and 3) steep slopes that produce abrupt changes in depth despite proximity to the coast (Quesada-Alpízar and Cortés 2006) favor the development of this type of gas-emitting ecosystem.

The groups conforming the bottom were similar to those reported in the rocky and coral reefs in Golfo Dulce and nearby areas (Alvarado et al. 2015); however, the composition is conspicuously different. Coastal habitats along the Pacific of Costa Rica do not harbor such high abundances of hydrozoans (Alvarado et al. 2015). The composition of some organisms, such as polychaetes, bivalves, sponges, octocorals, and hydrozoans, resembles the communities described in deep areas with methane emissions (Levin et al. 2015; Vedenin et al. 2020; Dueñas et al. 2021). It has been mentioned in previous works that these processes related to hydrocarbon emissions promote the establishment of chemosymbiotic communities (Hilário and Cunha 2008; Oliver et al. 2011).

The microbiota associated with seeps is influenced by various factors, including: the type of fluids that come out, the geomorphological characteristics of the site, and the available substrate, among others, and this in turn has an impact on the chemosymbiotic community that is established in the place. The best known chemosymbiont organisms in these systems are filter feeders, including bivalves, ophiuroids, polychaetes, and hydrozoans (Rodrigues et al. 2008, 2011a, b, 2012). These organisms benefit from the high availability of bacteria and organic matter associated with filtration (Cordes et al. 2010). At the Burbujas site, evidence of the existence of a chemosymbiotic community of hydrozoans and sponges was found. However, research efforts must be increased to find out if it really is, studies on the microbiota, the species that compose it, the filtration rate, and the dynamics of this community.

Turf is the category that contributed the most in terms of differences between transects; in transect one, there was no presence; in transect 2, 3% was found, and in transect 3, the intermediate depth transect, turf predominated with 43%. These differences in coverage percentages in the categories of macroalgae, P. lobata, and turf between transects could be a response to the differences in light penetration or the amount of sediment present in the water.

In the studied platform, only transect 2 had a relatively high cover of macroalgae (i.e. Gelidiales, Dictyota, Halimeda) and the presence of reef-forming corals (Porites lobata). The coral colonies had an encrusting type of growth, and “free-living colonies” or "rolling stones" were found at the edges of the patch.

A possible explanation for this phenomenon is that the platform is exposed to strong currents; in such conditions, when a new colony is being formed and is not entirely attached to the substrate, it may be subject to constant movement, which may result in colonies of sphere-shaped coral (Riegl et al. 1996; Kersting et al. 2017). It has also been mentioned that this form of growth in spheres can be promoted by biological action, whether they are burrowing invertebrates or fish (Glynn 1974). This form of growth and the relationship between coral morphology and methane emissions will be studied in more detail in future work since both factors mentioned above (bioerosion and currents) are present at the study site, as well as the physicochemical conditions. They are not optimal due to gas emissions and may have an influence. The morphology of the coral colonies present in an ecosystem can influence both the fish community and the structural organisms and cryptofauna present in them.

The fish assemblage associated with the platform was similar across all the transects despite the differences observed in the bottom cover composition. Some reef fishes are highly mobile, with home ranges over 1 ha (Zeller 1997), larger than the ~ 100 m² of platform assessed in this study; however, some species of wrasses have relatively small (~ 10 m²) home range sizes (Jones 2005). The predominance of small wrasses such as T. lucassanum coincides with Giraldo et al. (2001) results for healthy reefs on Gorgona Island, Colombian Pacific, as well as deteriorated reefs at Bahía Culebra, Pacific coast of Costa Rica (Arias-Godínez et al. 2019), and it is usually an abundant species even after the ecosystem is disturbed (Juárez-Hernández and Tapia 2018). This same genus has also been reported to be more abundant in other Caribbean reef environments (Jaxion-Harm et al. 2012). It should be noted that Giraldo et al. (2001) conclude that the abundance of T. lucassanum does not depend on the substrate cover but rather on the availability of food and the social structure.

The predominant families of cryptofauna in Burbujas were: Mytilidae, Alpheidae, Porcellanidae, Eunicidae, and Aspidosiphonidae; they tend to be dominant also among the cryptofauna associated with dead corals (Santos et al. 2012) and may be present in live corals, but not in large abundances. The abundances of Porcellanidae and Alpheidae found on this platform were similar to those reported for Golfo Dulce (Vargas and Vargas-Zamora 2020). In the Annelida phylum, all the reported families have been found in assemblages of species associated with deteriorated corals, mainly the families: Eunicidae, Syllidae, Oenonidae, and Serpulidae, in the same way in the Ophiuroidea class in the case of the species Ophiotrix rudis, Ophiotrix spiculata, Ophiactis savignyi, Ophiactis simplex and Ophiocoma aethiops (Salas-Moya et al. 2021).

This similarity may be related to the morphology of the precipitated carbonates to build the rock, which may resemble a deteriorated coral structure with many perforations, which increase the habitable surface. The surface area is proportionally related to the abundance found in a substrate (Nelson et al. 2016). The rubble or deteriorated coral structure has been considered a less restrictive space than living coral for opportunistic or generalist organisms (Enochs et al. 2011; Nelson et al. 2016). Cryptofauna is considered the most diverse group in coral reefs, and in climate change scenarios, it is very important to know the structure and functioning of these little-known organisms that play such various ecological roles (Enochs 2012; Enochs and Manzello 2012; Nelson et al. 2016), such cold seeps like Burbujas can be model ecosystems to visualize possible future scenarios of carbonated ecosystems.

The geological analysis of the rocks suggested high levels of bioerosion, also supported by the presence of bioeroding organisms in the cryptic fauna associated with the rocks, such as Leiosolenus mussels (Mytilidae), callianassids and alpheids shrimps with burrowing behavior, and nuculanid clams. The mussels of the genus Leiosolenus were the most common taxa in the rocks from the gas emission platform. This genus is also abundant in live and deteriorated scleractinian corals, where they play an important role as bioeroders (Hoeksema et al. 2022, Salas-Moya et al. 2021). On the other hand, in other cold methane emissions, mollusks have been reported, mainly bivalves, crustaceans, and annelids; however, the species vary according to their location and depth.

A new report for the country was found in this research, the callianassid shrimp of the genus Biffarius, which has four species, three known for the Atlantic Ocean and one for the Indo-Pacific (DecaNet 2023). Unfortunately, in this research, only one individual was found, so more should be collected to know more details about the identity of the species. In the case of the species Chaetopleura cf. roddai is a chiton that was reported from revised specimens from the collection of the Museo de Zoología of the UCR (Schwabe and Wehrtmann 2009), and this would be a new report since then.

The species accumulation curve suggests that further sampling will result in a higher number of species recorded in this rare habitat. Future studies can explore the diversity using different methodologies and other ecological processes, seasonality, and long-term relationship between the methane emissions and the biological assemblage associated. For example, future studies can observe the influence of the changes in gas emission rates or composition with the dominance of structural taxa, such as sponges, octocorals, and hydrozoans. The present study did not sample mobile macroinvertebrates due to strong current conditions. Thus, more research on this platform is needed for a more integral assessment of the biological ensemble.

Golfo Dulce harbors a higher biological diversity compared to the Gulf of Nicoya, despite presenting lower productivity due to its diversity of habitats (mudflats, estuaries, mangroves, rocky reefs, coral reefs, deep anoxic areas, etc.) within a smaller area (Morales-Ramírez et al. 2015; Vargas-Zamora et al. 2019, Vargas and Vargas-Zamora 2020). It is difficult to compare it with other cold seeps because the known research’s use very different methodologies and because of the depth at which they are found. However, the same groups of organisms have been reported in the biodiversity research’s (Grupe et al. 2015; Levin et al. 2017).

In the case of Burbujas, methane-derived authigenic carbonates precipitate throughout the seep, as occurs in other seeps (Bohrmann et al. 1998; Hovland et al. 2005). This characteristic causes a more heterogeneous seabed habitat in contrast to the soft bottoms of deep waters (Rex 2003). Cold seeps tend to have less diversity than the surrounding ecosystems but with more exclusive fauna, and they also host facultative organisms from the surrounding systems (Levin 2005; Levin et al. 2016).

Aquatic environments with methane emissions are often related to future climate change scenarios. It should be noted that methane, being soluble in water, has the capacity to replace dissolved oxygen, which causes anoxic bottoms near the gas outlets (Schmale et al. 2005). All these characteristics modify the standard water quality parameters and directly influence the organisms that inhabit these systems, thus creating unique ecosystems susceptible to variations.

Studies such as this one are fundamental for conserving ecosystems such as shallow methane seeps, which are specific, diverse, and little known worldwide. These environments are fragile and vulnerable; therefore, some authors have suggested their imminent protection (Rowden et al. 2016; Pereira et al. 2021). Unfortunately, methane seeps are often neglected due to a lack of knowledge, budget for their study, or political interest.

Acknowledgments: We thank the Escuela de Biología, the Centro de Investigación en Ciencias del Mar y Limnología (CIMAR), the Centro de Investigación en Biodiversidad y Ecología Tropical (CIBET) specifically the Museo de Zoología, the Centro de Investigación en Electroquímica y Energía Química (CELEQ), the Laboratorio de Paleontología y Colección de fósiles of the Escuela Centroamericana de Geología, and Laboratorio Interdisciplinario de Osa in Golfo Dulce, all from the Universidad de Costa Rica (UCR) for the logistical support to carry out this work. In addition, we are grateful for the taxonomic and laboratory support of Fiorella Vasquez, Leonardo Chacón, Jeffrey Sibaja, Guaria Cárdenas, Thais Ramírez, Rodney Mora, Eddy Gómez, Roberto Urcuyo, Juan Guillermo Sagot, Mario Espinoza, and Celeste Sánchez.

Funding: This study was funded by Vicerrectoría de Investigación of Universidad de Costa Rica.

Compliance with Ethical Standards: The authors declare that they have no conflict of interest and the work was carried out under the required ethical standards. No animal testing was performed during this study.

Sampling and field studies: All necessary permits for sampling and observational field studies have been obtained by the authors from the competent authorities and are mentioned in the acknowledgements, if applicable. The study is compliant with CBD and Nagoya protocols.

Data availability: The authors declare that the data supporting the findings of this study are available within the paper and its Supplementary Information files. Should any raw data files be needed in another format they are available from the corresponding author upon reasonable request.

Author Contribution Statement: CSM, JCAS, CFG, JJAB conceived and designed research and performed field surveys. CSM and RV performed taxonomic identifications. CSM and JCAS carried out the statistical analysis. All authors wrote, edited, read and approved the manuscript.

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Shallow gas seeps in the Golfo Dulce, South Pacific of Costa Rica: geological, physicochemical, and biological characterization

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