Environmental implications of skeletal micro-density and porosity variation in two scleractinian corals

The correlations between skeletal parameters (bulk density, micro-density and porosity), coral age and sea surface temperature were assessed along a latitudinal gradient in the zooxanthellate coral Balanophyllia europaea and in the azooxanthellate coral Leptopsammia pruvoti. In both coral species, the variation of bulk density was more influenced by the variation of porosity than of micro-density. With increasing polyp age, B. europaea formed denser and less porous skeletons while L. pruvoti showed the opposite trend, becoming less dense and more porous. B. europaea skeletons were generally less porous (more dense) than those of L. pruvoti, probably as a consequence of the different habitats colonized by the two species. Increasing temperature had a negative impact on the zooxanthellate species, leading to an increase of porosity. In contrast, micro-density increased with temperature in the azooxanthellate species. It is hypothesized that the increase in porosity with increasing temperatures observed in B. europaea could depend on an attenuation of calcification due to an inhibition of the photosynthetic process at elevated temperatures, while the azooxanthellate species appears more resistant to variations of temperature, highlighting possible differences in the sensitivity/tolerance of these two coral species to temperature changes in face of global climate change.     

Inferred calcification rate of a Mediterranean azooxanthellate coral is uncoupled with sea surface temperature along an 8° latitudinal gradient

Introduction

Correlations between sea surface temperature (SST) and growth parameters of the solitary azooxanthellate Dendrophylliid Leptopsammia pruvoti were assessed along an 8° latitudinal gradient on western Italian coasts (Mediterranean Sea), to check for possible negative effects of increasing temperature as the ones reported for a closely related, sympatric but zooxanthellate species.

Results

Calcification rate was correlated with skeletal density but not with linear extension rate, indicating that calcium carbonate deposition was preferentially allocated to keep a constant skeletal density. Unlike most studies on both temperate and tropical zooxanthellate corals, where calcification rate is strongly related to environmental parameters such as SST, in the present study calcification rate was not correlated with SST.

Conclusions

The lower sensitivity of L. pruvoti to SST with respect to other sympatric zooxanthellate corals, such as Balanophyllia europaea, may rely on the absence of a temperature induced inhibition of photosynthesis, and thus the absence of an inhibition of the calcification process. This study is the first field investigation of the relationship between SST and the three growth parameters of an azooxanthellate coral. Increasing research effort on determining the effects of temperature on biological traits of the poorly studied azooxanthellate scleractinians may help to predict the possible species assemblage shifts that are likely to occur in the immediate future as a consequence of global climatic change.

     

Relationships between growth,population dynamics,and environmental parameters in the solitary non-zooxanthellate scleractinian coral <Emphasis Type="Italic">Caryophyllia</Emphasis><Emphasis Type="Italic">inornata</Emphasis> along a latitudinal gradient in the Mediterranean Sea

The ecology of scleractinian corals may be understood through comparisons between population demographic data and environmental parameters. Growth (growth constant and maximum size) and demographic parameters (population structure stability, instantaneous mortality rate, average age of individuals, percentage of immature individuals, age at maximum biomass, and average age of biomass) of the solitary, non-zooxanthellate, and temperate coral Caryophyllia inornata were investigated at six sites along an 8° latitudinal gradient of temperature and solar radiation (SR) on the western Italian coasts. Growth parameters were homogeneous among populations across the investigated latitudinal range. While demographic parameters were not correlated with depth temperature, populations were progressively less stable and showed a deficiency of young individuals with increasing SR, likely as a result of the lowered energetic resources due to reduced zooplankton availability. These results contrast with data from another Mediterranean non-zooxanthellate solitary coral, Leptopsammia pruvoti, investigated along the same gradient, which shows no correlation between population demography and temperature or SR.     

Relationships between growth,population structure and sea surface temperature in the temperate solitary coral <Emphasis Type="Italic">Balanophyllia europaea</Emphasis> (Scleractinia,Dendrophylliidae)

The demographic characteristics of the solitary zooxanthellate scleractinian Balanophyllia europaea, endemic to the Mediterranean, were determined in six populations, on a latitudinal gradient along the Italian coast, and compared with the mean annual sea surface temperature (SST). Growth rate correlated negatively, and asymptotic length of the individuals positively with SST. With increasing SST, the distributions of age frequencies moved away from a typical steady state structure (i.e., exponential decrease in the frequency of individuals with age), indicating less stable populations and showed a deficiency of individuals in the younger-age classes. These observations suggest that high temperatures are an adverse factor to the B. europaea symbiosis. Using projected increases in seawater temperature, most of the B. europaea populations in the Mediterranean are expected to be close to their thermal limits by 2100 and the populations at that time may support few young individuals. Communicated by Environment Editor Prof. van Woesik.     

Inferred calcification rate of a temperate azooxanthellate caryophylliid coral along a wide latitudinal gradient

Correlations between environmental parameters (depth temperature and solar radiation) and growth parameters (bulk skeletal density, linear extension rate and net calcification rate) of the solitary azooxanthellate coral, Caryophyllia inornata, were investigated along an 8° latitudinal gradient on the western Italian coasts. Net calcification rate correlated positively with both bulk skeletal density and linear extension rate, showing that C. inornata allocates calcification resources evenly to thickening the skeleton and increasing linear growth. Overall, the three growth parameters did not follow gradients in the two environmental parameters, showing a different trend compared to most studies on zooxanthellate corals. However, the results are in agreement with the only previous analysis of an azooxanthellate coral, Leptopsammia pruvoti, studied along the same latitudinal gradient. In a comparison of the response to temperature of all Mediterranean species whose growth has been investigated to date, azooxanthellate corals were more tolerant to temperature increases than zooxanthellate corals.     

The influence of time since introduction on the population growth of introduced species and the consequences for management

Several processes likely act to change the demographic rates of introduced species over time, and this changing demography could influence the optimal management of invasive populations. Optimal management strategies should be derived based on the demography. However, we have a poor understanding of the degree to which the demography of introduced species changes following initial introduction. We used published matrix population models of introduced plant populations to test how population growth rate and elasticity change with time since introduction. We did not find a significant relationship between population growth rate and time since introduction. However, elasticity to stasis increased while elasticity to growth decreased with time since introduction. Broadly, as time since introduction progressed the elasticities of the introduced plant populations became more similar to those that have been reported for native species. These results suggest that the optimal management strategy should be derived incorporating elasticity through time, especially when the time scope of management is long or the available demographic data were obtained in the past.     

Plant Demography and Habitat: A Comparative Approach

Abstract Progress in plant demography will depend upon being able to synthesize a large body of data and this requires a means of comparing populations between sites and species. We have employed a comparative technique using elasticity analysis of stage-projection matrices to partition the contributions of fecundity (F), survival (L) and growth (G) to the finite rate of increase λ. Ordination of populations of 77 perennial herbs and trees in G-L-F space has shown that species segregate in this triangular space according to their life history and habitat. In the present paper we use the correspondence between demographic parameters and habitat revealed by this method to predict how succession and a variety of environmental factors such as grazing and fire are likely to alter the demography of populations and ultimately to change the composition of communities.     

Genetic structure of the deep-sea coral Lophelia pertusa in the northeast Atlantic revealed by microsatellites and internal transcribed spacer sequences

The azooxanthellate scleractinian coral Lophelia pertusa has a near-cosmopolitan distribution, with a main depth distribution between 200 and 1000 m. In the northeast Atlantic it is the main framework-building species, forming deep-sea reefs in the bathyal zone on the continental margin, offshore banks and in Scandinavian fjords. Recent studies have shown that deep-sea reefs are associated with a highly diverse fauna. Such deep-sea communities are subject to increasing impact from deep-water fisheries, against a background of poor knowledge concerning these ecosystems, including the biology and population structure of L. pertusa. To resolve the population structure and to assess the dispersal potential of this deep-sea coral, specific microsatellites markers and ribosomal internal transcribed spacer (ITS) sequences ITS1 and ITS2 were used to investigate 10 different sampling sites, distributed along the European margin and in Scandinavian fjords. Both microsatellite and gene sequence data showed that L. pertusa should not be considered as one panmictic population in the northeast Atlantic but instead forms distinct, offshore and fjord populations. Results also suggest that, if some gene flow is occurring along the continental slope, the recruitment of sexually produced larvae is likely to be strongly local. The microsatellites showed significant levels of inbreeding and revealed that the level of genetic diversity and the contribution of asexual reproduction to the maintenance of the subpopulations were highly variable from site to site. These results are of major importance in the generation of a sustainable management strategy for these diversity-rich deep-sea ecosystems.     

Constraints on the formation of colonies of the extant azooxanthellate scleractinian coral Dendrophyllia arbuscula

Sentoku, A. & Ezaki, Y. 2011: Constraints on the formation of colonies of the extant azooxanthellate scleractinian coral Dendrophyllia arbuscula. Lethaia, Vol. 45, pp. 62–70. Scleractinia display a variety of growth forms, whether zooxanthellate or azooxanthellate, as the consequence of the combined effects of both intrinsic and extrinsic factors. New modules arise in colonial corals through asexual reproduction, including budding and division. The azooxanthellate, branching dendrophylliid Dendrophyllia arbuscula van der Horst 1922 , is a good species to investigate intrinsic regularities in budding, because: (1) the lateral corallites always occur in the vicinity of four primary septa, excluding the two directive primary septa; (2) the two directive septa in lateral corallites tend to be oriented almost perpendicular to the growth orientation of parental corallites; (3) the lateral corallites grow more‐or‐less diagonally upwards; and (4) these regularities are retained from the axial to the derived lateral corallites during colony growth. Accordingly, a colony of apparently complex dendroid corals is formed according to certain universal rules that apply to successive generations of corallites. The presence of two opposite sectors in which budding do not occur seems to be common to other azooxanthellate scleractinian families. Regularities, other than the orientation of the directive septa, are also commonly found at least in other azooxanthellate dendrophylliid genera. These regularities suggest the presence of strict developmental constraints on the asexual reproduction of the Scleractinia, both extant and extinct. These regularities by azooxanthellate scleractinians, as one of the representative colonial metazoan groups, provide us with fundamental data with which we can understand how colonies are constructed. □Azooxanthellate coral, budding, colony, Dendrophyllia arbuscula, regularity.     

Fine-Scale Skeletal Banding Can Distinguish Symbiotic from Asymbiotic Species among Modern and Fossil Scleractinian Corals

Understanding the evolution of scleractinian corals on geological timescales is key to predict how modern reef ecosystems will react to changing environmental conditions in the future. Important to such efforts has been the development of several skeleton-based criteria to distinguish between the two major ecological groups of scleractinians: zooxanthellates, which live in symbiosis with dinoflagellate algae, and azooxanthellates, which lack endosymbiotic dinoflagellates. Existing criteria are based on overall skeletal morphology and bio/geo-chemical indicators—none of them being particularly robust. Here we explore another skeletal feature, namely fine-scale growth banding, which differs between these two groups of corals. Using various ultra-structural imaging techniques (e.g., TEM, SEM, and NanoSIMS) we have characterized skeletal growth increments, composed of doublets of optically light and dark bands, in a broad selection of extant symbiotic and asymbiotic corals. Skeletons of zooxanthellate corals are characterized by regular growth banding, whereas in skeletons of azooxanthellate corals the growth banding is irregular. Importantly, the regularity of growth bands can be easily quantified with a coefficient of variation obtained by measuring bandwidths on SEM images of polished and etched skeletal surfaces of septa and/or walls. We find that this coefficient of variation (lower values indicate higher regularity) ranges from ~40 to ~90% in azooxanthellate corals and from ~5 to ~15% in symbiotic species. With more than 90% (28 out of 31) of the studied corals conforming to this microstructural criterion, it represents an easy and robust method to discriminate between zooxanthellate and azooxanthellate corals. This microstructural criterion has been applied to the exceptionally preserved skeleton of the Triassic (Norian, ca. 215 Ma) scleractinian Volzeia sp., which contains the first example of regular, fine-scale banding of thickening deposits in a fossil coral of this age. The regularity of its growth banding strongly suggests that the coral was symbiotic with zooxanthellates.     

Effects of temperature and rainfall variation on population structure and sexual dimorphism across the geographical range of a dioecious species

The effects of climate (precipitation and temperature) on sexual dimorphism and population structure were analysed along a broad-scale environmental gradient covering the distributional range of the endemic dioecious species Corema album, along the west coast of the Iberian Peninsula. We aimed to assess distribution constraints and sex-related differences in demography and size associated with higher reproductive investment in females. Nine populations were chosen from across the geographic range of C. album and ten 10 × 10 m plots were established (10 m apart) along a 200-m transect. All male, female and non-reproductive shrubs were quantified within each plot and plant size, photosynthetic layer, height, sex ratio, population density and structure, and spatial segregation of sexes, under environmental conditions ranging from temperate to Mediterranean climate, were recorded and analysed. Increased aridity was related to lower population density and less structured populations, indicating an effect of higher temperature and lower precipitation on regeneration. Sexual dimorphism was influenced by climate, with size differences between sexes varying with aridity. However, demographic differences between sexes reflected in sex ratio deviations or the occurrence of spatial segregation were unrelated to any climatic variable, suggesting the existence of compensatory mechanisms that may counterbalance the higher reproductive effort of female plants. The results show the vulnerability of this endemic species to the increase in aridity expected in the southernmost limit of the biogeographical area due to global climate change, and demonstrate the importance of broad scale studies in the assessment of sexual dimorphism.     

Modes of regeneration and adaptation to soft‐bottom substrates of the free‐living solitary scleractinian Deltocyathoides orientalis

Scleractinian corals adapt to various substrate conditions with a variety of growth morphologies and modes of life. The azooxanthellate solitary scleractinian Deltocyathoides orientalis exhibits slightly flattened, bowl‐shaped corallites. This study describes in detail the modes of skeletal regeneration after fragmentation in association with exquisitely adaptive strategies of the corals for life on soft substrates. Larger fragments of individuals retaining almost two‐thirds to five‐sixths of the original skeletal area inherit the densely dilated, lower central skeleton, so as to keep a stable life position on soft substrates and regenerate the lost parts promptly. Even highly fragmented individuals preserving less than 10% of the original skeleton still regenerate and repair. Fragmented individuals with almost one‐sixth to one‐third original skeleton actively maintain a posture with the oral disc upward using movements of remaining tentacles. Damaged and missing soft tissues are then efficiently regenerated to form a mouth and gastrovascular cavity near the new centre of the corallum. Every regenerated individual reuses skeleton and soft tissues, and is capable of burrowing before the completion of growth morphology. The mode of regeneration characteristic of D. orientalis is thus effective and adaptive for maintenance of a stable life position on soft substrates for this solitary scleractinian. As fragmentation in deeper‐water, soft‐bottom settings is likely due to predation rather than turbulence, the rapid corallum regeneration and burrowing strategy may both represent adaptive strategies for life on soft substrates and exploitation of new niches, such as an infaunal mode of life, in a predator‐rich environment.     

Evaluating within‐population variability in behavior and demography for the adaptive potential of a dispersal‐limited species to climate change

Multiple pathways exist for species to respond to changing climates. However, responses of dispersal‐limited species will be more strongly tied to ability to adapt within existing populations as rates of environmental change will likely exceed movement rates. Here, we assess adaptive capacity in Plethodon cinereus, a dispersal‐limited woodland salamander. We quantify plasticity in behavior and variation in demography to observed variation in environmental variables over a 5‐year period. We found strong evidence that temperature and rainfall influence P. cinereus surface presence, indicating changes in climate are likely to affect seasonal activity patterns. We also found that warmer summer temperatures reduced individual growth rates into the autumn, which is likely to have negative demographic consequences. Reduced growth rates may delay reproductive maturity and lead to reductions in size‐specific fecundity, potentially reducing population‐level persistence. To better understand within‐population variability in responses, we examined differences between two common color morphs. Previous evidence suggests that the color polymorphism may be linked to physiological differences in heat and moisture tolerance. We found only moderate support for morph‐specific differences for the relationship between individual growth and temperature. Measuring environmental sensitivity to climatic variability is the first step in predicting species' responses to climate change. Our results suggest phenological shifts and changes in growth rates are likely responses under scenarios where further warming occurs, and we discuss possible adaptive strategies for resulting selective pressures.     

Effect of population size on the prospect of species survival

Many recent studies have demonstrated a negative effect of small population size on single plant traits. However, not much is known about the actual consequences of reduced plant performance on the long-term prospect of species survival. I studied the effect of population size on population growth rate and survival probability in the rare perennial herbScorzonera hispanica occurring in fragmented grasslands. Its performance was measured using several traits related to reproduction in 21 populations ranging in size from 3 to 2475 plants. These data were then connected with data on full demography of the species from three of the studied populations. Two different matrix models differing in the number of transitions based on measurements in the populations differing in size were used to explore the relationship between population size and population growth rate. Both matrix models showed that despite the decline in seed production in small populations, population growth rate is never significantly different from one, and the populations could thus be expected to survive in the long run. Calculations of extinction probabilities that take into account demographic and environmental stochasticity, however, showed that populations below 100 flowering individuals have a high probability to become extinct. This demonstrates that demographic and environmental stochasticity is an important driver of the fate of small populations in this system. This study demonstrates that estimation of population growth rate can provide new insights into the effect of population size on population growth and survival. It also shows how matrix models enable the combination various pieces of information about the single populations into one overall measure, and may provide a useful tool for the standardization of studies on the effects of population size on population performance.     

Vulnerability of wild American ginseng to an extreme early spring temperature fluctuation

Frost events in natural plant populations can have dramatic demographic consequences. For many plant species, spring emergence occurs when probability of damaging frost is low. Climate change, however, may alter weather patterns such that the environmental cues signaling spring emergence no longer coincide with periods of low frost risk, rendering plant populations susceptible to damaging frost events more frequently than in the past. In 2007, a spring freeze occurred in the eastern United States after a period of unusually warm temperatures. We took advantage of a long-term demographic dataset for American ginseng (Panax quinquefolius L.) to examine among and within population patterns of frost damage, as well as the effects of the frost on ginseng demography. Higher temperatures prior to the frost event increased the probability and extent of frost damage at the population level. Within populations, large plants tended to be damaged more frequently than smaller plants. Survival, growth, and reproduction were reduced in frost-damaged plants compared to undamaged plants in the year of the frost event, and negative effects on growth and reproduction persisted the following year. For plants such as ginseng, increases in frost frequency will negatively impact population growth, and likely have serious ramifications for long-term population viability.     

Extinction and recovery patterns of scleractinian corals at the Cretaceous-Tertiary boundary

The extinction and recovery of scleractinian corals at the Cretaceous-Tertiary (K-T) boundary was analyzed based on a global database of taxonomically revised late Campanian to Paleocene coral collections. In contrast to earlier statements, our results indicate that extinction rates of corals were only moderate in comparison to other marine invertebrates. We have calculated a 30% extinction rate for Maastrichtian coral genera occurring in more than one stratigraphic stage and more than one geographic region. Reverse rarefaction suggests that some 45% of all coral species became extinct. Photosymbiotic (zooxanthellate) corals were significantly more affected by the extinction than azooxanthellate corals; colonial forms were hit harder than solitary forms, and among colonial forms an elevated integration of corallites raised extinction risk. Abundance, as measured by the number of taxonomic occurrences, had apparently no influence on survivorship, but a wide geographic distribution significantly reduced extinction risk. As in bivalves and echinoids neither species richness within genera nor larval type had an effect on survivorship. An indistinct latitudinal gradient is visible in the extinction, but this is exclusively due to a higher proportion of extinction-resistant azooxanthellate corals in higher-latitude assemblages. No significant geographic hotspot could be recognized, neither in overall extinction rates nor in the extinction of endemic clades.More clades than previously recognized passed through the K-T boundary only to become extinct within the Danian. These failed survivors were apparently limited to regions outside the Americas. Recovery as defined by the proportional increase of newly evolved genera, was more rapid for zooxanthellate corals than previously assumed and less uniform geographically than the extinction. Although newly evolved Danian azooxanthellate genera were significantly more common than new zooxanthellate genera, the difference nearly disappeared by the late Paleocene suggesting a more rapid recovery of zooxanthellate corals in comparison to previous analyses. New Paleocene genera were apparently concentrated in low latitudes, suggesting that the tropics formed a source of evolutionary novelty in the recovery phase.     

A Comprehensive Phylogenetic Analysis of the Scleractinia (Cnidaria,Anthozoa) Based on Mitochondrial CO1 Sequence Data

Background

Classical morphological taxonomy places the approximately 1400 recognized species of Scleractinia (hard corals) into 27 families, but many aspects of coral evolution remain unclear despite the application of molecular phylogenetic methods. In part, this may be a consequence of such studies focusing on the reef-building (shallow water and zooxanthellate) Scleractinia, and largely ignoring the large number of deep-sea species. To better understand broad patterns of coral evolution, we generated molecular data for a broad and representative range of deep sea scleractinians collected off New Caledonia and Australia during the last decade, and conducted the most comprehensive molecular phylogenetic analysis to date of the order Scleractinia.

Methodology

Partial (595 bp) sequences of the mitochondrial cytochrome oxidase subunit 1 (CO1) gene were determined for 65 deep-sea (azooxanthellate) scleractinians and 11 shallow-water species. These new data were aligned with 158 published sequences, generating a 234 taxon dataset representing 25 of the 27 currently recognized scleractinian families.

Principal Findings/Conclusions

There was a striking discrepancy between the taxonomic validity of coral families consisting predominantly of deep-sea or shallow-water species. Most families composed predominantly of deep-sea azooxanthellate species were monophyletic in both maximum likelihood and Bayesian analyses but, by contrast (and consistent with previous studies), most families composed predominantly of shallow-water zooxanthellate taxa were polyphyletic, although Acroporidae, Poritidae, Pocilloporidae, and Fungiidae were exceptions to this general pattern. One factor contributing to this inconsistency may be the greater environmental stability of deep-sea environments, effectively removing taxonomic “noise” contributed by phenotypic plasticity. Our phylogenetic analyses imply that the most basal extant scleractinians are azooxanthellate solitary corals from deep-water, their divergence predating that of the robust and complex corals. Deep-sea corals are likely to be critical to understanding anthozoan evolution and the origins of the Scleractinia.     

Evaluating the consequences of habitat fragmentation: a case study in the common forest herb Trillium camschatcense

The effects of habitat fragmentation on remnant plant populations have rarely been studied extensively using a single species. We have attempted to quantify the effects of forest fragmentation (primarily that of population size) on populations of Trillium camschatcense, a representative spring herb in the Tokachi plain of Hokkaido, Japan. In this region, intensive agricultural development over the past 100 years has divided once-large, continuous populations of this species into small, isolated fragments. Small populations generally produced fewer seeds than large populations, although this result differed between years. The level of seed production is unlikely to explain demographic structures based on life-history stages. Instead, the stage structure was better explained by population size, seedling recruitment being limited in smaller populations. This could be associated with edge effects because the stage structure in small populations corresponded well to that observed in forest edges, where altered microclimatic conditions strongly limit seedling recruitment. Small populations also experienced stochastic loss of rare alleles at allozyme loci as well as biparental inbreeding. Although one consequence of these changes is reduced fertility, the long-term effects on population growth can be controversial in long-lived forest herbs, since the negative effect on fertility may vary across years, and population growth rate may not be sensitive to changes in fertility. Further studies of long-term demography will reveal whether and how habitat fragmentation could limit population growth of remnant populations more than a century after fragmentation.     

Quantifying how fine-grained environmental heterogeneity and genetic variation affect demography in an annual plant population

The ability of plant species to colonize new habitats and persist in changing environments depends on their ability to respond plastically to environmental variation and on the presence of genetic variation, thus allowing adaptation to new conditions. For invasive species in particular, the relationship between phenotypic trait expression, demography, and the quantitative genetic variation that is available to respond to selection are likely to be important determinants of the successful establishment and persistence of populations. However, the magnitude and sources of individual demographic variation in exotic plant populations remain poorly understood. How important is plasticity versus adaptability in populations of invasive species? Among environmental factors, is temperature, soil nutrients, or competition most influential, and at what scales and life stages do they affect the plants? To investigate these questions we planted seeds of the exotic annual plant Erodium brachycarpum into typical pasture habitat in a spatially nested design. Seeds were drawn from 30 inbred lines to enable quantification of genetic effects. Despite a positive population growth rate, a few plants (0.1?%) produced >50?% of the seeds, suggesting a low effective population size. Emergence and early growth varied by genotype, but as in previous studies on native plants, environmental effects greatly exceeded genetic effects, and survival was unrelated to genotype. Environmental influences shifted from microscale soil compaction and litter depth at emergence through to larger-scale soil nutrient gradients during growth and to competition during later survival and seed production. Temperature had no effect. Most demographic rates were positively correlated, but emergence was negatively correlated with other rates.