Experimental taphoneomy shows the feasibility of fossil embryos

The recent discovery of apparent fossils of embryos contemporaneous with the earliest animal remains may provide vital insights into the metazoan radiation. However, although the putative fossil remains are similar to modern marine animal embryos or larvae, their simple geometric forms also resemble other organic and inorganic structures. The potential for fossilization of animals at such developmental stages and the taphonomic processes that might affect preservation before mineralization have not been examined. Here, we report experimental taphonomy of marine embryos and larvae similar in size and inferred cleavage mode to presumptive fossil embryos. Under conditions that prevent autolysis, embryos within the fertilization envelope can be preserved with good morphology for sufficiently long periods for mineralization to occur. The reported fossil record exhibits size bias, but we show that embryo size is unlikely to be a major factor in preservation. Under some conditions of death, fossilized remains will not accurately reflect the cell structure of the living organism. Although embryos within the fertilization envelope have high preservation potential, primary larvae have negligible preservation potential. Thus the paleo-embryological record may have strong biases on developmental stages preserved. Our data provide a predictive basis for interpreting the fossil record to unravel the evolution of ontogeny in the origin of metazoans

Fertile fathoms: Deep reproductive refugia for threatened shallow corals

The persistence of natural metapopulations may depend on subpopulations that exist at the edges of species ranges, removed from anthropogenic stress. Mesophotic coral ecosystems (30–150 m) are buffered from disturbance by depth and distance, and are potentially massive reservoirs of coral diversity and fecundity; yet we know little about the reproductive capabilities of their constituent species and the potential for these marginal environments to influence patterns of coral reef persistence. We investigated the reproductive performance of the threatened depth-generalist coral Orbicella faveolata over the extent of its vertical range to assess mesophotic contributions to regional larval pools. Over equal habitat area, mesophotic coral populations were found to produce over an order of magnitude more eggs than nearby shallow populations. Positive changes with depth in both population abundance and polyp fecundity contributed to this discrepancy. Relative larval pool contributions of deeper living corals will likely increase as shallow habitats further degrade due to climate change and local habitat degradation. This is a compelling example of the potential for marginal habitat to be critical to metapopulation persistence as reproductive refugia

The relative contribution of dinoflagellate photosynthesis and stored lipids to the survivorship of symbiotic larvae of the reef-building corals

The long-distance dispersal of larvae provides important linkages between populations of reef-building corals and is a critical part of coral biology. Some coral planulae have symbiotic dinoflagellates (Symbiodinium spp.) that probably provide energy in addition to the lipids provisioned within the egg. However, our understanding of the influence of symbionts on the energy metabolism and survivorship of planulae remains limited. This study examines the relative roles of symbiotic dinoflagellate photosynthesis and stored lipid content in the survivorship of the developing stages of the corals Pocillopora damicornis and Montipora digitata. We found that survivorship decreased under dark conditions (i.e. no photosynthetic activity) for P. damicornis and M. digitata at 31 and 22 days after release/spawning, respectively. The lipid content of P. damicornis and M. digitata planulae showed a significant decrease, at a higher rate, under dark conditions, when compared with light conditions. When converted to energy equivalents, the available energy provided by the depletion of lipids could account for 41.9 and 84.7% of larval metabolism for P. damicornis (by day 31) and 38.4 and 90.1% for M. digitata (by day 21) under light and dark conditions, respectively. This finding indicates that not all energy requirements of the larvae are met by lipids: energy is also sourced from the photosynthetic activities of the symbiotic dinoflagellates within these larvae, especially under light conditions. In addition, the amounts of three main lipid classes (wax esters, triglycerides, and phospholipids) decreased throughout the experiment in the planulae of both species, with the wax ester content decreasing more rapidly under dark conditions than under light conditions. The observations that the planulae of both species derive considerable amounts of energy from wax esters, and that symbiotic dinoflagellates enable larvae to use their stores at lower rates, suggested that symbiotic dinoflagellates have the potential to extend larval life under light conditions

Rapid declines in metabolism explain extended coral larval longevity

Lecithotrophic, or non-feeding, marine invertebrate larvae generally have shorter pelagic larval durations (PLDs) than planktotrophic larvae. However, non-feeding larvae of scleractinian corals have PLDs far exceeding those of feeding larvae of other organisms and predictions of PLD based on energy reserves and metabolic rates, raising questions about how such longevity is achieved. Here, we measured temporal changes in metabolic rates and total lipid content of non-feeding larvae of four species of reef corals to determine whether changes in energy utilization through time contribute to extended larval durations. The temporal dynamics of both metabolic rates and lipid content were highly consistent among species. Prior to fertilization, metabolic rates were low (2.73–8.63 nmol O2 larva⁻¹ h⁻¹) before rapidly increasing to a peak during embryogenesis and early development 1–2 days after spawning. Metabolic rates remained high until shortly after larvae first became competent to metamorphose and then declined by up to two orders of magnitude to levels at or below rates seen in unfertilized eggs over the following week. Larvae remained in this state of low metabolic activity for up to 2 months. Consistent with temporal patterns in metabolic rates, depletion of lipids was extremely rapid during early development and then slowed dramatically from 1 week onward. Despite the very low metabolic rates in these species, larvae continued to swim and retained competence for at least 2 months. The capacity of non-feeding coral larvae to enter a state of low metabolism soon after becoming competent to metamorphose significantly extends dispersal potential, thereby accruing advantages typically associated with planktotrophy, notably enhanced population connectivity