A boom–bust phylum? Ecological and evolutionary consequences of density variations in echinoderms

Abstract

Abstract. Echinoderms play a key role in structuring many marine ecosystems and are notorious for large population density variations in so-called ''outbreak'' or ''dieoff'' events. In a review of this phenomenon, we assess the causal factors and ecological and evolutionary consequences. We identified 28 species (6 Asteroidea, 8 Echinoidea, 10 Holothuroidea, 4 Ophiuroidea) that exhibit large (more than two population doublings or halvings) population density changes. Three generalized patterns were identified and named for exemplary species:(1) rapid decreases followed by no or slow recovery (Diadema-Paracentrotus Model), (2), rapid increase and apparent stability at a new population density (Amperima-Amphiura Model), and (3) population density fluctuations (Acanthaster-Asterias Model). Echinoderms identified were distributed from the shallow intertidal to the deep sea, and from tropical to temperate regions. In most cases, significant impacts on the respective ecosystems were observed. The most striking similarity among all species identified was possession of the ancestral-type planktotrophic larva. This larval type was significantly overrepresented in species identified within the Asteroidea, Echinoidea, Holothuroidea, and for the combined data set. We suggest three main factors that render a life history with planktotrophic larvae a high-risk-high-gain strategy: (1) a strong nonlinear dependency of larval production on adult densities (Allee effects), (2) a low potential for compensatory feedback mechanisms, and (3) an uncoupling of larval and adult ecology. The alternative (derived) lecithotrophic larva occurs in 68% of recent echinoderm species, suggesting an evolutionary trend toward this larval type. Lecithotrophic development represents a more buffered life history because compensatory feedback between adult densities and larval output is likely to be more efficient. For lecithotrophic developers, direct nutritive coupling from adult to larva to the early benthic juvenile provides a buffer against starvation. Lecithotrophic larvae are independent of the vagaries of planktonic food supply, and their short planktonic duration may promote local recruitment. Anthropogenic influences contributed to the population density variations in most cases, including increased primary productivity through eutrophication or global change, disease, overfishing, and species introductions. We suggest that anthropogenic disturbance, through its influence on the frequency and/or amplitude of echinoderm population density changes, may go beyond present ecosystem impacts and alter future evolutionary trends.

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

“…The data are similar to those obtained in a previous study of H. erythrogramma using a single sperm concentration (10 3 sperm ml -1 ) (Byrne et al, 2009). With regard to prediction #1, the data indicated that near future ocean acidification (to pH 7.6) and increased pCO2 (to 1892 ppm) does not reduce fertilization success even at very low sperm densities (10 sperm per egg).…”

“…This is also the case for bivalve fertilization (Byrne, 2009;Havenhand and Shlegal, 2009; but see Parker et al, 2009). …”

“…Ocean acidification has dire consequences for larvae due to impaired larval calcification and hypercapnia (Clark et al, 2009;Dupont et al, 2008;Kurihara, 2008). However, in areas of strong warming such as southeast Australia, embryos of species like H. erythrogramma that are sensitive to thermal effects (Byrne, 2009;Byrne et al, 2009) may not reach the larval stage in a warm ocean regardless of pH. Developmental failure regardless of the stage affected or stressor(s) involved will cause recruitment failure with flow-on effects to marine ecosystems (Przeslawski et al, 2008).…”

“…Relatively small perturbations in planktonic and recruitment phases can translate to large alterations of adult populations (Uthicke et al, 2009 Table 2 Relationship between sperm concentration and sperm:egg ratios.…”

“…powerplant effluent) indicate that marine fertilization is robust to these stressors (Bay et al, 1993;Carr et al, 2006;Greenwood and Bennett, 1981;Wilson and Hyne, 1997), but recent studies indicate that acidification has a negative effect on fertilization (Havenhand et al, 2008;Kurihara and Shirayama, 2004;Parker et al, 2009). For H. erythrogramma we sought to explain the contrasting results where low pH impaired fertilization in one study (potentially due to reduced sperm motility) (Havenhand et al, 2008), but not in another (Byrne et al, 2009). …”