The solitary cold-water scleractinian C. huinayensis is described here as a brooder. Although reproduction in scleractinian CWCs is still poorly known, no other temperate species has yet been described to brood larvae. The solitary temperate CWC D. dianthus12, as well as the temperate colonial CWC D. pertusum8,10,38, M. oculata8,10 and O. varicosa9 reproduce by broadcast spawning. Brooding has only been reported in subpolar and polar solitary CWCs from the Southern Ocean17,18.
Although quantitative data on the number of larvae released in the four Southern Ocean brooders are lacking, a potential number of larvae released per polyp can be inferred from their maximum fecundity (Table 1). C. huinayensis appears to be in the lower range of larvae production (6.5 ± 11.4 month-1 larvae), when compared its larval size (750–1080 µm length) with Balanophyllia malouinensis larvae (> 600 µm, Table 1).
Thorson’s rule43,44 states that organisms at higher latitudes tend to produce larger and fewer offspring and are frequently brooders. However, the brooding C. huinayensis appears to defy this rule, as it occurs at mid-latitudes (36° and 48.5° S33,45). Though the phylogeography of C. huinayensis is not yet clear, six other solitary species of the genus Caryophyllia are endemic to Antarctica46, suggesting that the genus may have originated in the Southern Ocean, with the mid-latitude distribution of C. huinayensis making the downstream end dispersal via the cold Humboldt Current branching off the Southern Ocean. In our case, Thorson’s rule does not seem to be a good predictor of the macroevolutionary patterns and reproductive mode in Caryophyllia.
A better explanation can be inferred from Kerr et al.47. Their phylogenetic study on scleractinians revealed that the change from spawning to brooding (or vice versa) is based on the sexuality of the corals (i.e., gonochoric or hermaphroditic) and not on latitudinal distribution. The main pathway is from gonochoric spawners to gonochoric brooders, then to hermaphroditic brooders, and finally hermaphroditic spawning, which is the dominant reproductive mode in shallow-water corals.
The results of our study indicate that C. huinayensis reproduces throughout the year, albeit with large temporal variations in the number of larvae released. However, the fluctuations were not seasonal. This may be due to the fact that the aquarium for this experiment lacked external timing signals (zeitgebers) usually found in the field, i.e., there were no fluctuations e.g., in water temperature, food frequency, food quality, or salinity, which might otherwise have synchronized the corals’ internal clock. Although, it is not yet known if the local C. huinayensis population exhibits seasonality in their larval release, the lack of larvae in April 2021 could also be due to poor internal fertilisation success based on the quality and/or quantity of sperm released (which was never observed).
If there is no seasonal release of larvae from the natural coral population, this may indicate that rapid recolonisation is possible throughout the year following a disturbance. Substrate alterations are usually observed in the Patagonian fjord region, where strong physical disturbances such as landslides occur48, due to precipitation and earthquakes49. Also, hypoxia events (< 2 ml l-1) caused by pulses and subsequent degradation of terrestrial and marine organic matter (e.g., phytoplankton blooms)50,51 are common in the fjords51, negatively impacting the benthic life, but promoting new available space for settlement. These events may be exacerbated in time and space by salmon farming activities, as bacterial respiration during the degrading of uneaten food pellets or salmon faeces52, decreasing the oxygen concentration and thus reduces the likelihood that recolonisation can take place at a natural rate after hypoxic events.
On the one hand, brooding in C. huinayensis with subsequent release of well-developed larvae throughout the year has the advantage of rapid settlement, reducing the likelihood of drift to unfavourable locations and die-off21. On the other hand, a high dispersal potential has a positive effect, as larvae can spread to new habitats with better conditions. Therefore, stable and suitable environmental conditions at a site, with occasional disturbances that expose substrates are favorable for brooder with short larval dispersal, as has been shown for C. huinayensis. However, if environmental conditions vary, longer-dispersed larvae may have an advantage. Different reproductive approaches were observed in two brooding tropical Agarcia-species from a reef off Curaçao, where A. humilis—which occurs in shallow waters subject to physical and biological disturbance—has many small larvae throughout the year. In contrast, A. agaricites that thrives in deeper and less disturbed areas, has few but large larvae, which are released only in spring/summer20. While the low fecundity and narrow time window for reproduction limit the species’ capacity to colonise new available substrate, the disadvantage is compensated by the larger size and, hence, long-lasting energy reserves of the larvae, promoting higher dispersal.
As access to natural CWC populations is difficult and the release of offspring can rarely be observed, it is difficult to establish a link between reproduction and environmental cues. However, Maier et al.53 conducted a transplantation experiment with D. pertusum at Nakken reef, Norway, determining that gametogenesis is supported by lipids obtained during spring, profiting from increased phyto- and zooplankton abundance at this time. The coral then rebuilt the tissue reserves in autumn, probably related to the spawning season (late January to early March)38.
Spawning during the winter season was observed for the actinia Corynactis sp.54 and suggested for D. dianthus12 and the octocoral Primnoella chilensis55, all from Comau Fjord. This period coincides with the seasonal temperature minimum56 at the sampling depth of C. huinayensis. It is thus conceivable that the change in water temperature initiates gametogenesis, while increasing food availability in early spring fosters the development and release of brooded planulae. The peak of released larvae of in vitro-reared C. huinayensis (June–December 2018, Fig. 2c) matches the reproductive season of D. dianthus and P. chilensis. Although water temperature and food supply were kept constant in our laboratory study, an endogenous clock can be suspected as a pacemaker for reproduction that the adult polyps collected in the field “remembered” but run out of phase due to the lack of an external natural stimulus, which may explain the observed variability in planulation (Fig. 2c).
The swimming behaviour of C. huinayensis larvae in the first days was similar to that of O. varicosa26 from an in vitro experiment, in which the larvae spent two to four days at the water surface and three weeks in the lower water column before metamorphosing. Likewise, D. pertusum larvae remained at the water surface for the first two weeks before bottom-probing 3–5 weeks after fertilization41. Translating the in vitro observations of C. huinayensis larvae to the field, this might indicate that the two days of swimming upwards and being pelagic do not provide much potential for dispersal. However, the strong tidal currents of the photic zone49,57 could significantly increase their dispersal. It should be noted, however, that in Comau Fjord a strong halocline at around 10–15 m depth probably prevents the larvae from swimming up to the brackish surface layer (7–31 salinity)33,58. This however needs to be verified, as larvae of D. pertusum are able to survive at a salinity of 255.
One of the forces governing connectivity between coral populations is thought to be related to the planktonic stage, though not solely based on larvae locomotion. At 1.18 ± 0.4 mm s-1, the swimming velocity of C. huinayensis larvae is within the range of other CWCs (Table 1). The determined swimming speed of C. huinayensis is, however, 1–2 orders of magnitude lower than the tidal current velocities recorded at the vicinity of coral populations in Comau Fjord (5 cm s-1, maximum 15 cm s-1)59. Hence, horizontal dispersal is likely dominated by drift, as in other planktonic larvae, and the range is largely determined by the PLD ended by settlement. Former studies found that larvae released from brooders can settle within hours or a few days60, as the larvae are released at an advanced stage of development and may therefore already be competent to settle. In contrast, the entire larval stage of broadcast spawners occurs in the water column. These contrasting reproductive modes may result in different patterns of larval dispersal. For the broadcast spawners O. varicosa, the PLD is 42 d9, whereas for D. pertusum (where PLD was not yet described) a PLD of eight weeks made the dispersal modelling done by Fox et al.61 match the genetic population structure better than other models, indicating a PLD of eight weeks plausible. Thus, the potential of local settlement of these two species can be considered low due to the relatively long planktonic phase, in contrast to the 8 ± 9.3 d for C. huinayensis. However, studies on both sides of the Atlantic have shown a constrained genetic connectivity in D. pertusum between the two sides. In an investigation near Oslofjord, Norway, Dahl et al.62 showed that restricted connectivity also applies to populations of D. pertusum at a local scale. Likewise, Morrison et al.63 observed significant genetic differences between populations of the Gulf of Mexico and populations of the West and East Atlantic Ocean, though there is high connectivity within the regions. Populations on the European continental margin and in isolated fjords showed moderate levels of gene flow64. A microsatellite study on populations from Comau Fjord found no vertical or horizontal genetic differences and concluded that the local population of D. dianthus is panmictic65,66. Based on the strong tidal current in Comau Fjord, which may transport larvae both vertically and horizontally, and the relatively short planktonic phase of C. huinayensis (8 ± 9.3 d), the population of C. huinayensis may also be panmictic. However, genetic analyses would have to be carried out to elucidate the population structure of the species to be able to assess the degree of connectivity among the populations. Overall, the levels of connectivity between coral populations appears to be the interaction between large-scale currents, local environmental conditions and the species-specific reproductive modes.
When the settlement surfaces in the holding tank were allowed to grow biofilms two weeks before the start of the settlement trial, 48% of the larvae settled within one to three days. In contrast, if the surfaces were not pre-conditioned, the PLD extended up to 28 d with an average of 26.7 ± 2.1 d (n = 4). Although the number of larvae able to extend the PLD in this study is too low to draw any robust conclusions, this could nevertheless indicate that the biofilm plays a role as a cue for settlement in C. huinayensis larvae. This observation is supported by Webster et al.28, indicating that biofilms may outstrip the importance of other settlement cues (e.g., coralline algae) in shallow-water corals from the Great Barrier Reef.
Our results may imply that C. huinayensis larvae are able to extend their PLD when, for example, an appropriate substrate is unavailable. Consequently, PLD extension requires either energy stores (lecithotrophic larvae) or feeding (planktotrophic larvae), as shown for D. pertusum larvae. Here, larvae can feed on picoplankton by ciliary feeding or scavenging on mucus strings5. Although feeding of C. huinayensis larvae was not determined in this study, two lines of evidence suggest planktotrophy: the PLD may be long (26.7 ± 2.1 d), suggesting storage-independent development. More importantly, the histological cuts of 25 larvae showed a well-developed oral pore which connects to the pharynx through the gastrovascular cavity opening (Fig. 4), which may indicate a developed gastrovascular system.
Field studies on C. huinayensis from Comau Fjord showed high coral abundance (2211 ± 180 ind. M2) at 25 m water depth on a substrate inclination between 60° and 80°, but no individuals on horizontal substrate surfaces34. This pattern was attributed to sedimentation, where the horizontal seafloor is smothered by inorganic terrigenous particles derived from river run-off33,58 and/or by organic matter from intense salmon farming in Comau Fjord67 (such as fish faeces and uneaten food pellets passing through the salmon cages)68,69. Inclined surfaces, by contrast, are too steep for the sediment to accumulate. Based on the fact that the observations in this study were carried out in sediment-free artificial sea water, this demonstrates that settlement on horizontal surfaces can occur, supporting the assumption that the distribution pattern of C. huinayensis in the field is likely conditioned by sedimentation.
As opposed to most larvae of shallow-water scleractinians, the larvae of C. huinayensis lack photosynthetic endosymbionts, so that they depend entirely on heterotrophy and/or their energy reserves. Anyhow, we observed a similar structuring and timing of tissue and skeletal development in C. huinayensis as in the tropical corals Galaxea fascicularis and Acropora brueggemanni (re-described as Isopora brueggemanni)31,32. Within the first three days after settlement, all three coral species developed four pairs of mesenteries, which reached the stomodaeum, while two pairs did not (Fig. 5d). Moreover, the first endotentacles (2 ± 1.5 d, Fig. 5g) and the second exotentacles (4 ± 2.1 d, Fig. 5i) appeared at the same time and place in all three species. Similarly, the first crystals and crystal structures of the basal plate ring and the endosepta were precipitated (4 ± 2.1 d, Fig. 5i). These similarities suggest that early development in C. huinayensis is highly conserved, whether the energy costs invested during metamorphosis and juvenile growth are covered by internal energy reserves or heterotrophic feeding, or a combination of both. Although no studies have addressed the relationship between internal lipid and protein reserves with growth rate during the early growth stages in CWCs, it has been observed in the facultatively mixotrophic O. varicosa, where deep azooxanthellate colonies, subsisting on both energy reserves and exogenous food, grew at a higher rate than zooxanthellate shallow-water colonies70. This indicates that under certain conditions a heterotrophic diet may be energetically better that a mixotrophic diet.
This study was the first to describe the metamorphosis of a temperate scleractinian cold-water coral, using C. huinayensis as the model species. Our results show a similar ontogenetic timing from planula to juvenile polyp in C. huinayensis as described for tropical corals, suggesting a highly conserved evolutionary mechanism in spite of large environmental (e.g., temperature) differences.
The CWC C. huinayensis showed a peak in larval release in vitro, that coincided with the low temperatures and increased food availability at its site of origin, Comau Fjord, in austral winter. As the released larvae had a developed gastrovascular system, this could indicate a planktotrophic or mixed mode larvae, that may benefit from the increase of phyto- and zooplankton in austral spring. On the other hand, the short PLD may have the advantage of feeding immediately after settlement by offsetting the high energy costs during metamorphosis, allowing a rapid onset of skeletogenesis.
Climate change influences seasonal environmental variability by enhancing water stratification, reducing the depth of the mixed layer and water circulation, which combined, reduces the productivity of phytoplankton and consequently of the zooplankton71. Overall, it can alter the phenology of organisms, i.e., timing of their seasonal activities72. Our study showed that C. huinayensis displays a moderate phenology, which could be a consequence of the lack of environmental variability in the aquarium, indicating the ability of C. huinayensis to acclimatize to new environmental conditions. However, if the phenology of this coral is pronounced in the field, the expected changes in food availability would not match the observations in the aquarium. On the contrary, lower energy uptake could therefore affect reproductive capacities, larval survival, metamorphosis and growth, impairing the connectivity and thus population stability of this species.
Source: Ecology - nature.com
