The ‘stretching modulation of skeletal growth’ is a mechanism allowing corals to preferentially invest calcification resources in thickening the skeleton, thus increasing skeletal density, or accelerating linear extension[5, 23]. The tropical Porites, for example, invests increased calcification at higher temperatures into linear extension[3, 8]. In contrast, the tropical Montastraea annularis invests increased calcification at higher temperatures to construct denser skeletons[5, 23]. In the Mediterranean endemic Balanophyllia europaea, calcification is allocated evenly between increasing skeletal density and linear extension, indicating that the ability to colonize the substratum quickly and the mechanical strength of the skeleton are both important for this species. The temperate L. pruvoti exhibited a response which was similar to the one of M. annularis, in that calcification was positively correlated with skeletal density but not with linear extension. For each 1 mg mm-2 yr-1 of calcification rate variation, skeletal density varied by ~ 1 mg mm-3.
Geometrically calculated skeletal density values in the present work were reasonable with respect to other studies on tropical and temperate species[3, 5, 17, 22]. The computed skeletal density used in this and in previous studies[15, 22] is analogous to the bulk density, which is defined as the skeletal mass divided by the total volume (skeletal matrix volume plus pores volume;). Skeletal matrix volume is further composed by the crystals of CaCO3 and by the intracrystalline organic matrix regulating the crystallization process. Analyses to quantify the porosity in the same samples of the present study show that the variation of bulk density depends on variations of porosity, while the variation in the density of the skeletal framework (micro-density,) is not strong enough to significantly affect bulk density.
The lack of correlations with SST exhibited by the calcification rate and skeletal density in the present study on Leptopsammia pruvoti confirms previous studies on the population density, growth and population structure stability of this species, where the coral parameters were always shown to be unrelated to environmental variables such as solar radiation or SST[15, 16]. For both the linear and power function models, trends of the analyses performed on the full dataset were confirmed by the analyses on the three age-based subsets, indicating that differences in the mean age of the samples in the populations did not bias the results.
The lack of correlation between calcification rate of the azooxanthellate L. pruvoti and SST along the latitudinal gradient is a different response with respect to the similar studies on temperate and tropical zooxanthellate species. For example, calcification rate of the Mediterranean endemic B. europaea is negatively related to SST, while in the tropical Porites and M. annularis it is positively related to SST[3, 5]. However, mid-term studies on Porites highlight a reduction of its calcification rate as SST increases[7, 8], even if a recent long-term analysis of Porites calcification along Australian coasts show no evidence of widespread patterns of decline in calcification rate since 1900. In that analysis, calcification rates at high-latitude reefs were found to be more sensitive to temperature increase than more tropical reefs. Another recent analysis of Porites spp. and Montastraea spp. in the Great Barrier Reef and Mexican Caribbean highlighted a negative response of calcification to increasing SST for both genera, but a higher sensitivity to temperature increase for the former genus, rather than the latter one. This has fundamental consequences in light of future global warming scenarios, since differential reduction of calcification between coral genera could profoundly affect community structure. Our results suggest a higher sensitivity of zooxanthellate species to the variations of temperature, while asymbiotic corals may be more tolerant to temperature variations. The higher sensitivity of symbiotic species may be due to the decrease of photosynthetic performance at higher temperatures, since in zooxanthellate corals calcification is enhanced by photosynthesis, and both processes have temperature optima. Alternatively, a role may be played by the much steeper response of respiration to subtle temperature increases (Q10) than that of photosynthesis, resulting in significant decrease of the residual net photosynthesis and of the energy surplus needed for calcification and other physiological processes. Although the hypothesis of photosynthetic inhibition at high temperatures is intriguing, other environmental parameters may influence coral calcification (pH, total alkalinity, wave exposition, flow rate, etc.). Besides local factors, the apparent insensitivity of L. pruvoti growth to the SST range experienced in the present study may be due either to 1) the lack of zooxanthellate, and thus a lack of inhibition of calcification by the depressed net photosynthesis, or 2) a higher optimal temperature for the calcification of this species with respect to B. europaea, or 3) a coupling between the above two factors, or 4) a sampling area not representative of the species conditions at the collection sites. L. pruvoti distribution area includes also regions outside the Mediterranean Sea, up to the southern coasts of Ireland and UK, where seawater temperature is considerably lower. It is then unlikely that this species has a higher optimal temperature for calcification than the Mediterranean endemic B. europaea, since L. pruvoti lives in much colder seas and deeper waters (up to 70 m depth). Even if any comparison between L. pruvoti and B. europaea must be taken cautiously, since the two species were sampled at different depths (16 m and 6 m, respectively), which may be subject to different thermal regimes throughout the year, the variation of calcification rate among sites, found in L. pruvoti, could be related to particular local conditions unrelated to temperature. Since the present study focused on the influence of SST, we selected sites with similar environmental traits other than SST, but we did not thoroughly analyze all the site characteristics such as nutrients and zooplankton availability or competitive interactions with other organisms, which could all contribute to the observed differences in calcification rate. However, these local differences, while contributing to the variability of calcification rate (this study) and of population dynamics traits, are not strong enough to determine significant variations in population abundance, which is homogeneous across all sites with about 10,000 individuals per square meter. It may be argued that no correlation with SST has been found because the selected sampling area for this study was too small and unrepresentative of the population. However, the same sampling area adequately represents the sites in previous studies on the biometry, growth and population dynamics of the species[15, 16, 22], where trends in the biometric parameters (such as polyp length) with temperature have been found. Moreover, significant differences in calcification rate among sites have actually been found in the present study, but they do not correlate to temperature, and are likely due to local differences in parameters other than temperature. An alternative explanation of the difference in demographic parameters among sites may be related to suspension feeding. In the Mediterranean, the warm summer–fall season is characterized by lower nutrient levels and zooplankton availability than the cool winter–spring season. Corals and several benthic suspension feeding taxa have proved to be stressed by low nutrients and limited zooplankton availability. Different availability of resources among sites may affect calcification rate in L. pruvoti. However, if this was the case, negative effects on calcification rate would be expected in the warmest sites (where the warm season is longer and the zooplankton availability lower, on average). Instead, L. pruvoti calcification seems to be unrelated to SST. The differences in calcification rates and population dynamics traits among sites may be related to other environmental parameters not considered in this study (pH, total alkalinity, wave exposition, flow rate, etc.). Further investigations are thus needed to better constrain the environmental controls on the population dynamics of this species. Moreover, further investigation on the poorly studied azooxanthellate species are needed to differentiate the environmental controls on the growth of symbiotic and asymbiotic corals.
One of the main threats for coral and coral reefs survival is global temperature increase. The speeds of many negative changes to the oceans are near or are tracking the worst-case scenarios from the IPCC and other predictions. Recently, one of the most diverse communities in the Mediterranean Sea, the coralligenous (~1,666 species;), where suspension feeders are dominant, has been strongly affected by several mass mortality events related to high temperatures[32–36]. The zooxanthellate dendrophylliid B. europaea is a Mediterranean endemic species which will likely be negatively affected by seawater warming, since increasing temperature lowers its population abundance, its skeletal density, by increasing its skeletal porosity, and lowers its calcification rate. Moreover, warmer populations are less stable and show a progressive deficiency of young individuals, so that there is concern for the future of this species. These detrimental effects of increasing temperature seem to be related to the symbiosis with zooxanthellae, whose photosynthesis could be depressed at high temperatures causing cascading negative effects on the growth and reproductive traits of B. europaea, although this hypothesis is yet to be tested[15, 18, 22, 37]. L. pruvoti, instead, seems to be tolerant to the same temperature range experienced by B. europaea. In fact, biological traits of the former species have been studied in the same sites and time interval, but none of them is negatively correlated with SST ([15, 16, 18] and present study). Increasing temperature may even favour L. pruvoti, since the corals living in populations characterized by higher SSTs have a higher micro-density, even if this increase in micro-density is not strong enough to cause significant variations of bulk density. However, the limit of temperature increase that will still be tolerable by this species is unknown. Moreover, it should be noted that the results derived from analyses based on latitudinal variations of calcification are not necessarily the same as those derived from time-based analyses. In fact, while calcification may have a positive correlation with SST along a latitudinal gradient, such as in Porites, it may be negatively correlated with the increasing SST recorded in recent years[7, 8], and may fluctuate during the yearly cycle of temperature variation. Thus, any extrapolations of spatial derived data to time resolved predictions has to be taken cautiously.