The skeleton plays a vital role in the survival of aquatic invertebrates by separating and protecting them from a changing environment. In most of these organisms, calcium carbonate (CaCO3) is the principal constituent of the skeleton, while in others, only a part of the skeleton is calcified, or CaCO3 is integrated into an organic skeleton structure. The average pH of ocean surface waters has increased by 25% in acidity as a result of anthropogenic carbon dioxide (CO2) emissions, which reduces carbonate ions (CO32−) concentration, and saturation states (Ω) of biologically critical CaCO3 minerals like calcite, aragonite, and magnesian calcite (Mg-calcite), the fundamental building blocks for the skeletons of marine invertebrates. In this chapter, we discuss how ocean acidification (OA) affects particular species of benthic calcareous hydroids in order to bridge gaps and understand how these organisms can respond to a growing acidic ocean.
- ocean acidification
Since the arrival of industrialization with the beginning of the British Industrial Revolution in 1750 to now, the accumulative concentration of carbon dioxide (CO2) in the atmosphere through to the year 2019 has increased to 2340 ± 240 gigatonnes of CO2 (GtCO2), of which 25% has been sunk into the ocean [1, 2]. This human-induced sink of CO2 in the ocean produces a chemical phenomenon called ocean acidification (OA) . OA decreases seawater pH, the concentration of carbonate ions (CO32−), and the saturation state (Ω) of the three primary biogenic calcium carbonate (CaCO3) minerals that occur in seawater and in shells and skeletons of calcifying organisms: calcite, aragonite, and magnesian calcite (Mg-calcite) .
Shells and skeletons of calcifying organisms play an essential role in their survival by separating and protecting them from a changing environment, as it happens with calcareous cnidarians [5, 6]. Within the phylum Cnidaria, only 17% of its extant species produce a calcareous skeleton through a process of biological transformation called biomineralization [7, 8]. The biomineralization process involves the selective extraction, transport, and uptake of biominerals from the environment in the function of their abundance and availability for their later incorporation into functional structures under strict biological control .
Of the 17% of the extant cnidarians with a calcareous skeleton, 14% is represented by members of the order Scleractinia (Cnidaria, Anthozoa), while the remaining 3% is made up of species belonging to the superorder “Anthoathecata” (Cnidaria, Hydrozoa) (Figure 1) . In the class Anthozoa, the biomineralization process is the best known and most widely studied, being the opposite for the class Hydrozoa , although they are one of the main components of zoobenthic communities, significant contributors to the building of coral reefs (Figure 2) [10, 11, 12], and also some are essential in pelagic communities due to the presence of a medusa stage .
Calcareous hydroid families with a well-developed benthic polypoid stage are Milleporidae (hydrocorals, “fire corals” or millepores) with 15 species, Hydractiniidae (longhorn hydrozoans) with 4 species, and Stylasteridae (hydrocorals, lace corals, or stylasterids) with 320 species [7, 13]. These three families constitute a polyphyletic group and are commonly grouped as “calcified hydroids,” “calcareous hydrocorals,” or, simply, “hydrocorals”—terms that refer to hydroids that secrete a calcareous skeleton . These calcareous structures can take the form of skeletons composed of individual spicules, spicule aggregates, or massive skeletons , and are responsible for providing protection and ion storage [6, 16, 17].
The calcareous skeleton of the cnidarians is always ectodermal in origin, and its mineralogy is composed exclusively of CaCO3 . In the calcareous species of the class Hydrozoa, their skeletons are composed of calcite, aragonite, or both (Table 1) [9, 19, 20, 21, 22, 23]. Calcite and aragonite are two of the six CaCO3 polymorphs and are the most thermodynamically stable structures deposited extensively as biominerals . In stylasterid species, for instance, the distribution of calcite or aragonite in their skeletons can be as follows: 100% calcite, 100% aragonite, primarily calcite with some aragonite, or primarily aragonite with some calcite . When calcite and aragonite are present at the same time, the two polymorphs always occupy different anatomical sites . Since the natural color of CaCO3 is white , the broad spectrum of colors observed in the calcareous skeletons of hydrocorals is due to the presence of carotenoproteins, symbiotic dinoflagellates of the genus Symbiodinium, or by the presence of microboring or euendolithic microorganisms [25, 26, 27].
|Taxa||Type of skeletogenesis||Principal mineral|
|Family Milleporidae||Modified spherulitic to trabecular|
|Family Hydractiniidae||Spherulitic (with organic lamellae)|
|Family Stylasteridae||Fully spherulitic or modified spherulitic to trabecular|
|Cheiloporidion pulvinatium||Primarily aragonite with some calcite|
|Errina sp.||Primarily calcite with some aragonite|
Phylogenetic analysis supports the independent origins of a calcified skeleton in Hydrozoa [9, 28, 29], and the distribution of CaCO3 polymorphs in their skeletons is considered to have been produced by non-environmental causes . However, the biomineralization process of these organisms is highly variable and strongly affected by environmental factors [30, 31] and substrate .
2. Skeletogenesis and OA
The biomineralization process is practically unknown to calcareous hydroids. Sorauf  summarizes some hypotheses about the biomineralization process of some Hydrozoa, and there has been no review about it to date. The basic structure is of the spherulitic growth of a principal mineral controlled by organic substrates to form pillars in which the spherulites are in part compartmentalized by a skeletal organic matrix (SOM), which forms an irregular matrix with compartments but does not form sheaths for individual crystal growth. In the class Hydrozoa exist three types of skeletogenesis, and the principal minerals involved are the CaCO3 polymorphs aragonite or calcite (Table 1) [19, 20, 21, 22].
In addition to biomineralization, CaCO3 plays a significant role as second messenger to control exocytosis, cortical reactions in eggs, and muscle contraction . In some hydractinids, CaCO3 is required for larval motility , induction of metamorphosis , and secretion of adhesive material during the latter .
The biocrystallization, such as sclerotization, is derived from the ectoderm, which produces a SOM that controls the spacing of nucleation sites and limits the size or shape of spherulites [21, 36]. The organic secretions may be composed of peptides, proteins, proteoglycans, lipids, and polysaccharides, which, as a whole, are known as the template for mineralization [21, 37]. It is known that this template is involved in most, if not all, stages of biomineral formation, from transport, through nucleation and growth, to structure stabilization (Figure 3) .
According to an analysis of SOM homologs in cnidarians, including Hydrozoa, several proteins related to biomineralization were identified . Extracellular adhesion proteins and carbonic anhydrases homologs were the most common proteins found (e.g., in Millepora alcicornis, Millepora complanata, and Millepora squarrosa). Homolog proteins include enzymes such as peptidase-1 and peptidase-2 as well as acidic proteins like SAARP-1, SAARP-2, acidic SOMP, CARP4, CARP5, Integrin-like and two SAARP-like proteins; those proteins are involved in calcite formation . Two galaxin ortholog proteins (Galaxin and Galaxin-2)  have been fully characterized by the calcifying matrix of scleractinian corals . More interestingly, carbonic anhydrases, which are known to precipitate CaCO3 in different calcareous organisms , have been identified in Hydrozoa species, CruCA-4, and Putative CA . Finally, in contrast to scleractinian corals, Hydrozoa species did not show small cysteine-rich proteins (SCRiPs) , whose function in corals is still unclear.
In some calcareous hydroids, a progressive capability to produce a similar SOM to that of scleractinian corals has been observed, with individual control of crystal growth . Also, the calcification process of stylasterid and millepore species has been compared with that of scleractinian corals . This calcification process includes uptake and transport of materials, production of organic secretion, the formation of tissue cavities where calcification may take place, and the deposition of CaCO3; these processes may be influenced differently by environmental conditions, and be affected by OA [43, 44].
About the biochemical process underlying the response of hydrocoral M. alcicornis in acidified waters, it has been found that the calcification process in the hydrocoral was not affected by a wide range of seawater pH (8.1–7.5) under experimental conditions . Besides, is mentioned that the Ca-ATPase plays an essential role in the biomineralization as maintenance a steady-state net calcification rate in the hydrocoral, especially under scenarios of moderate (pH 7.8) and intermediate (pH 7.5) acidification of seawater, but under a scenario of severe acidification (pH 7.2) of seawater, the hydrocoral is not able to maintain a steady-state net calcification rate . On the other hand, physiologically, the exposure to seawater acidification induces oxidative stress with consequent oxidative damage to lipids and proteins, which could compromise hydrocoral health . However, a reduction in the calcification process was not observed in Millepora platyphylla despite having been exposed to OA conditions .
Some effects in other calcareous organisms, for instance, anthozoans, sea urchins, and mollusks by OA are: slowdown of their calcification rates; changes in gene expression consistent with metabolic suppression; increased oxidative stress; potential effect on symbiotic zooxanthellae; decrease in matrix proteins; reduction of carbonic anhydrase protein; increased calcite growth; structural disorientation of calcite crystals; fragile skeletons that reduce protection from predators and changing environments, affect the expression of the gene encoding Ca-ATPase enzymes and the enzymatic activity itself [30, 44, 47, 48, 49].
OA not only affects the skeleton of the calcareous hydroids, but it can also affect the other phases of its life cycle, for instance, the medusa stage of millepores, since it has been recently recorded that cubomedusae suffer from higher mortality when subjected to OA conditions (pH 7.5) .
3. Implications, threats, and consequences of OA
The response of hydrocorals to the changes they face in their environment remains unknown, especially how they are affected by anthropogenic activities such as the increase in the concentration of CO2 in the atmosphere, causing an increase in sea surface temperature (SST) and a decrease in seawater pH. The chemistry of OA is better understood from their implications for calcifying marine fauna and their hosts or associations. Skeletons of hydrocorals and longhorn hydrozoans are known to host abundant and diverse symbiotic organisms, for instance, with photosynthetic dinoflagellates (generally referred to as zooxanthellae), and maintain associations with micro and macroboring organisms, and grazers. The microboring organisms (MIO) include cyanobacteria, green and red algae, fungi, and lichens . The macroboring organisms (MAO) comprise ascidians and sponges , while in the grazers encompass echinoderms, mollusks, polychaeta, crustaceans, and fish [42, 52].
Of the three families of extant calcareous hydroids, only “fire corals” have a symbiotic relationship with zooxanthellae . The zooxanthellae are essential for the “fire corals” to achieve their calcification process, keep their rate of calcification constant, as well as speed up a calcareous deposition in the function of the environmental conditions . Loss of this association from hydrocoral tissue is responsible for the white color observed, aptly named bleaching . When “fire corals” experiment stress occurs bleaching, or the paling zooxanthellate decline and the concentration of pigments within the zooxanthellae fall, where each zooxanthella may lose 50–80% of its photosynthetic pigments . The stress can be induced by a plethora of factors, singly or in combination, and among them we have: anomalously low and high temperature, solar radiation, subaerial exposure, sedimentation, freshwater dilution, inorganic nutrients, high concentrations of xenobiotics, presence of pathogens such as protozoan and bacterium, OA, among others [54, 55]. Recently, it has been observed that hydrocorals can select their symbionts zooxanthellae, depending on environmental conditions, which can confer an advantage on how to face ongoing human-driven climate change .
The mechanism underlying the observed bleaching response was not explicitly investigated, some hypotheses are that changes in seawater chemistry influence bleaching thresholds by altering the functioning of the carbon-concentrating mechanism (CCM), photoprotective mechanisms (such as photorespiration for instance), or direct impacts of acidosis; therefore, the acidification effects on coral bleaching are uncertain and review of other aspects, for instance, levels of the other abiotic factors such as light and nutrients, photoacclimation and photoprotection responses, molecular genetics, as well as studies that imply the understanding of integral processes about host-algae are recommended to understand the role that zooxanthellae may play in the ability of corals to cope with these anthropogenic changes in the ocean [53, 57, 58].
The MIO distribution within the skeletons occurs through contact with the substrate of settlement as MIO already colonizes it, and their colonization occurs early in the development of the corals and expands at slower rates than the hydrocoral growth . Since stylasterid corals do not host zooxanthellae, such an arrangement may be beneficial throughout the life of the coral, despite some losses to its skeleton density due to dissolution by MIO; moreover, the boring microflora within corals have a mutualistic relationship, helping corals survive better during bleaching events, because these MIO may satisfy the nitrogen quantities required by live hydrocorals for their balanced growth, also considering that MIO are the major primary producers and agents of microbioerosion dissolving large quantities of CaCO3 with a potential in buffering seawater .
Micro and macrobioerosion under undisturbed natural conditions are essential mechanisms in CaCO3 recycling; however, these bioerosion processes can proceed faster if OA weakens the substrate, also facilitating in this way the bioerosion by grazers . Furthermore, OA does not affect the siliceous sponges as directly as other marine taxa, which are heavily dependent on CaCO3 at various life history stages like cnidarians, mollusks, and many crustaceans species with tiny pelagic larval forms . These siliceous sponges represent a threat when settling on calcareous substrates by the process of weakening the skeleton by their bioeroder action; nevertheless, thermal stress appears to weaken calcifiers more strongly than bioeroding sponges .
Other impacts include shifts in competitive interactions with non-reef builders such as macroalgae, sponges, soft corals, ascidians, and corallimorpharians; the competition impacts the recruitment, growth, and mortality of coral organisms .
This review of current literature concerning the effects of OA on hydrocorals and longhorn hydrozoans and their proposed mechanisms shows that targets are numerous, and therefore it is difficult today to give a conclusion. Besides, several of the findings correspond to anthozoans and specific areas or under laboratory or modeling conditions. On the other hand, it has been shown that each species has a different response, some are more sensitive than others, and some show strategies to survive under conditions of anthropogenic climate change. As proposed by Luz , further studies that use metabolomics and proteomics techniques are necessary to help identify different response pathways in hydrocorals exposed to acidic conditions.
This work was supported by Medusozoa Mexico (
Conflict of interest
The authors declare no conflict of interest.