Paulina Selvakumaraswamy

Temperature, but not pH, compromises sea urchin fertilization and early development under near-future climate change scenarios

Global warming is causing ocean warming and acidification. The distribution of Heliocidaris erythrogramma coincides with the eastern Australia climate change hot spot, where disproportionate warming makes marine biota particularly vulnerable to climate change. In keeping with near-future climate change scenarios, we determined the interactive effects of warming and acidification on fertilization and development of this echinoid. Experimental treatments (20–26°C, pH 7.6–8.2) were tested in all combinations for the ‘business-as-usual’ scenario, with 20°C/pH 8.2 being ambient. Percentage of fertilization was high (>89%) across all treatments. There was no difference in percentage of normal development in any pH treatment. In elevated temperature conditions, +4°C reduced cleavage by 40 per cent and +6°C by a further 20 per cent. Normal gastrulation fell below 4 per cent at +6°C. At 26°C, development was impaired. As the first study of interactive effects of temperature and pH on sea urchin development, we confirm the thermotolerance and pH resilience of fertilization and embryogenesis within predicted climate change scenarios, with negative effects at upper limits of ocean warming. Our findings place single stressor studies in context and emphasize the need for experiments that address ocean warming and acidification concurrently. Although ocean acidification research has focused on impaired calcification, embryos may not reach the skeletogenic stage in a warm ocean.

Unshelled abalone and corrupted urchins: development of marine calcifiers in a changing ocean

The most fragile skeletons produced by benthic marine calcifiers are those that larvae and juveniles make to support their bodies. Ocean warming, acidification, decreased carbonate saturation and their interactive effects are likely to impair skeletogenesis. Failure to produce skeleton in a changing ocean has negative implications for a diversity of marine species. We examined the interactive effects of warming and acidification on an abalone (Haliotis coccoradiata) and a sea urchin (Heliocidaris erythrogramma) reared from fertilization in temperature and pH/pCO2 treatments in a climatically and regionally relevant setting. Exposure of ectodermal (abalone) and mesodermal (echinoid) calcifying systems to warming (+2°C to 4°C) and acidification (pH 7.6–7.8) resulted in unshelled larvae and abnormal juveniles. Haliotis development was most sensitive with no interaction between stressors. For Heliocidaris, the percentage of normal juveniles decreased in response to both stressors, although a +2°C warming diminished the negative effect of low pH. The number of spines produced decreased with increasing acidification/pCO2, and the interactive effect between stressors indicated that a +2°C warming reduced the negative effects of low pH. At +4°C, the developmental thermal tolerance was breached. Our results show that projected near-future climate change will have deleterious effects on development with differences in vulnerability in the two species.

Sea urchin fertilization in a warm, acidified and high pCO2 ocean across a range of sperm densities

Marine invertebrate gametes are being spawned into an ocean simultaneously warming, acidifying and increasing in pCO(2). Decreased pH/increased pCO(2) narcotizes sperm indicating that acidification may impair fertilization, exacerbating problems of sperm limitation, with dire implications for marine life. In contrast, increased temperature may have a stimulatory effect, enhancing fertilization. We investigated effects of ocean change on sea urchin fertilization across a range of sperm densities. We address two predictions: (1) low pH/increased pCO(2) reduces fertilization at low sperm density and (2) increased temperature enhances fertilization, buffering negative effects of acidification and increased pCO(2). Neither prediction was supported. Fertilization was only affected by sperm density. Increased acidification and pCO(2) did not reduce fertilization even at low sperm density and increased temperature did not enhance fertilization. It is important to identify where vulnerabilities lie across life histories and our results indicate that sea urchin fertilization is robust to climate change stressors. However, developmental stages may be vulnerable to ocean change.

Reproduction and development of the freshwater clam Corbicula australis in southeast Australia

The freshwater clam Corbicula australis is an important component of the macrobiota of the river systems of southeast Australia. Reproduction of two populations of this clam in the Nepean River at Douglas Park and Menangle was investigated to document the gametogenic cycle, larval morphology and to determine when they incubate embryos. C. australis is a simultaneous hermaphrodite and broods its young in the inner demibranchs. The gonads are ovotestes with oogenic and spermatogenic regions in each ascinus. The sperm are biflagellate, a condition unique in the Bivalvia to clonal corbiculids. Gametogenesis was continuous and did not exhibit a seasonal pattern. In contrast, spawning and incubation of embryos was limited to the warmer months of the year. Embryos were present in the gills from October to May. C. australis develops through a modified veliger larva with a vestigially ciliated velum which is not used for swimming or particle capture. The velum is covered by microvilli and it is suggested that the velar epithelium may be specialised for nutrient uptake in the marsupial environment. C. australis produces several clutches each year and the young are released as advanced juveniles with a well-developed foot. Reproductive output differed between the two populations. This was in part due to the larger size of the clams from Menangle and may also reflect the enhanced productivity at this site. The suite of life history traits exhibited by C. australis: hermaphroditism, potential for self-fertilization/androgenesis, brooding progeny to the crawl-away juvenile stage and a high reproductive output, provide for rapid colonization and population growth in this clam which typically inhabits disturbance prone sandy lotic habitats.

Vestigial Ophiopluteal Structures in the Lecithotrophic Larvae of Ophionereis schayeri (Ophiuroidea)

Evolution of echinoderm development from a feeding to a non-feeding mode can be examined by studying non-feeding larvae with structures that appear to be vestiges derived from a feeding ancestral state. The lecithotrophic larvae of the Australian brittle star Ophionereis schayeri possess such features, and the early development of this species was documented by light and scanning electron microscopy. The embryos undergo irregular cleavage, resulting in the formation of different sized blastomeres, with subsequent development through a wrinkled blastula stage. The lecithotrophic larva of O. schayeri possesses several vestigial ophiopluteal structures, including a continuous ciliated band, a larval gut, and a larval skeleton. The ciliated band is a reduced expression of the continuous ciliated band typical of ophioplutei. The larval gut is a transiently complete system, but an esophageal plug and rapid closure of the blastopore renders it nonfunctional. The larval skeleton, though reduced, consists of four rods corresponding to the body, posterolateral, anterolateral, and postoral rods characteristic of an ophiopluteus. Due to a heterochrony in larval skeletogenesis, the postoral rods develop early and simultaneously with the other rods. Compared with the larvae of other lecithotrophic ophiuroids, the larva of O. schayeri is one of the most reduced ophiopluteal forms reported to date.

Reproductive cycle of two populations of Ophionereis schayeri (Ophiuroidea) in New South Wales

Reproduction of two populations of Ophionereis schayeri (Müller and Troschel) in New South Wales was investigated from November 1991 through January 1993. The reproductive cycle was documented by histological examination of the gonads and by image analysis to determine the oocyte size-frequency distributions. Both populations of O. schayeri were mature in December and January and had a major summer spawning period between January and February. Thereafter, the condition of the gonads exhibited interindividual variability, with asynchronous low-intensity gamete release through August. O. schayeri has the potential to spawn for up to 8 mo of the year. This breeding pattern with synchronous spawning in summer and asynchronous gamete release through winter was similar in both populations. During autumn and winter, the gonads contained developing gametes and advanced gametes ready for spawning. The eggs spawned by O. schayeri during these seasons started their growth during the previous spring vitellogenic period, and continued to grow through summer. Upon reaching full size, they were stored for spawning outside the main breeding period. Spring is marked by increased spermatogenic and vitellogenic activity followed by maturation and spawning. Throughout their development, the oocytes of O. schayeri are surrounded by a follicle consisting of periodic acid-Schiff-positive (PAS+) haemal fluid and PAS+ yolk by the oocytes. In the testes, the haemal sinus projects into the centre of the spermatocyte columns, thus appearing to play a nutritive role in support of both oogenesis and spermatogenesis. Late vitellogenic oocytes of O. schayeri are firmly anchored to the germinal epithelium by an attachment complex consisting of specialised attachment cells and basophilic strands that radiate between the oolemma and the nucleus. Spawning is associated with rupture of the follicles, which remain as prominent, empty U-shaped profiles in the ovaries. O. schayeri produces copious numbers of 200 μm-diam oocytes, suggesting that this species is a broadcast spawner and that it has a modified ophiopluteus or vitellaria larva.

Development of the five primary podia from the coeloms of a sea star larva: homology with the echinoid echinoderms and other deuterostomes

Confocal laser scanning microscopy of larvae of the asteroid Parvulastra exigua was used to investigate the development of the five primary podia from the coeloms in the echinoderm phylum in an approach to the problem of morphological homology in the deuterostome phyla. The development is shown from an early brachiolaria larval stage to a pre-settlement late brachiolaria larval stage. In the early brachiolaria larva, a single enterocoele connected to the archenteron has formed into two lateral coeloms and an anterior coelom. The primary podia form from the coelomic regions on the left side of the brachiolaria larva, while on the right the coelomic regions connect with the exterior through the pore canal and hydropore. The anterior coelom forms the coelom of the brachia. Homology between the primary podia of the asteroid and the echinoid classes of echinoderms is described and extended to coeloms of other deuterostome phyla.

Nervous System Development in Feeding and Nonfeeding Asteroid Larvae and the Early Juvenile

Larval and juvenile nervous systems (NS) of three asterinid sea stars with contrasting feeding and nonfeeding modes of development were characterized using the echinoderm-specific synaptotagmin antibody. In the feeding bipinnaria and brachiolaria larvae of Patiriella regularis, the species with ancestral-type development, an extensive NS was associated with the ciliary bands (CBs) and attachment complex. Lecithotrophic planktonic (Meridastra calcar) and benthic (Parvulastra exigua) brachiolariae lacked CBs and the associated NS, but had an extensive NS in the attachment complex. The similarity in the distribution and morphology of synaptotagmin immunoreactive neurons and the anatomy of the NS in the attachment complex of these closely related sea stars suggests conservation of neurogenesis in settlement-stage larvae regardless of larval feeding mode. Nerve cells were prominent on the brachia of all three species. In advanced brachiolariae the larval nervous system was localized to the adhesive disc as the larval body resorbed during metamorphosis. The structures and tissues that contained larval neurons degenerated during metamorphosis. There was no evidence that the larval NS persists through metamorphosis. In juvenile development, synaptotagmin IR was first evident in the NS of the tube feet. As the central nervous system developed, synaptotagmin IR reflected the histological organization of the adult NS. The juvenile NS formed de novo with a temporal lapse between histogenesis and synaptotagmin IR. We evaluated the ontogeny of NS organization in the change in body plan from the bilateral larva to the radial juvenile.

Longevity and larval development among southern bell frogs (Litoria raniformis) in the Coleambally Irrigation Area - implications for conservation of an endangered frog.

Context. With the flow of many of the world’s rivers regulated such that water can be diverted for agriculture and human consumption, basic ecological information on the current status of key biota in significant floodplain wetlands and their response following inundation is needed. The maintenance of natural habitat to ensure amphibian survival is gaining increasing recognition, given the ongoing decline of anuran populations. Information on longevity, time required to emerge from the water and to reach sexual maturity, all provide important information about the required timing, frequency and duration of environmental water allocations to ensure successful recruitment among populations of southern bell frogs (Litoria raniformis Keferstein, 1867). Aims. The aims of this research were to establish the longevity of southern bell frogs in the Coleambally Irrigation Area (CIA) in the Riverina region of New South Wales, Australia, and to evaluate the capacity for southern bell frog tadpoles to survive and successfully metamorphose following an extended overwintering period. Methods. Skeletochronology studies were carried out using toe-clips taken from adult and juvenile frogs captured in irrigation channels and rice fields over two rice-growing seasons. For the metamorphosis assay, southern bell frog tadpoles were held back in their development by low temperatures and low food allocation for 290 days, before temperatures and food allocation were increased adequately to allow metamorphosis to occur. Key results. The study indicated that skeletochronological examination of toe-bones was a useful technique for establishing the age structure of southern bell frogs in this region. The oldest animals in the population were found to be 4–5 years old, although the majority of frogs were typically 2–3 years old. Also, the metamorphosis assay indicated that successful metamorphosis was the exception rather than the rule if tadpole development was held back by low food ration and low temperatures. Conclusions. If southern bell frogs reach sexual maturity only after 2 years, and the oldest animals observed in the field are 4 or 5 years old, then there is a very narrow window of opportunity – two to three seasons – for each individual to successfully breed. Implications. The implications for environmental flow management are that habitats for key species identified for protection such as the endangered southern bell frog will need water every 1–2 years to enable each cohort to breed and maintain the wild populations. The extent of the environmental flows needs to be adequate to ensure that water persists long enough for critical biological events such as anuran metamorphosis to occur during the spring and summer months.

The Larval Apical Organ in the Holothuroid Chiridota gigas (Apodida): Inferences on Evolution of the Ambulacrarian Larval Nervous System

Within the deuterostomes, the similarity of the dipleurula-type larvae of echinoderms (auricularia, bipinnaria) and hemichordates (tornaria) is striking. Here we describe the serotonergic system of the auricularia larvae of the apodid sea cucumber Chiridota gigas to broaden the comparison of the dipleurula-type larval nervous system in the Holothuroidea. This larva has a simple serotonergic nervous system largely composed of the apical organ. The apical organ is a concentration of cells and fibers along, and spanning between, the portions of the ciliary band that traverse the larval apex. Bipolar and multipolar cells give rise to fibers that connect the bands. In contrast to other echinoderm larvae, this larva does not develop serotonergic cells around the mouth. The similar topology and structure of the apical organ of the auricularia and the tornaria suggests that the serotonergic apical organ of the Ambulacraria (Echinodermata Hemichordata) may have originated as a group of nerve cell bodies and fibers that developed in association with ciliary band sectors at the