Larry R. McEdward

Reproductive Strategies of Marine Benthic Invertebrates Revisited: Facultative Feeding by Planktotrophic Larvae

Fecundity‐time models of reproductive strategies in marine invertebrates all predict that reproductive success is maximized only at the extreme levels of investment. Selection should drive egg sizes toward small eggs and planktotrophy or large eggs and lecithotrophy. The existence of two distinct larval types, feeding and nonfeeding, has been taken as confirmation of this prediction and has established the current paradigm for larval ecology. However, comparative and experimental evidence does not support the prediction that egg size is minimized in species with planktotrophic larvae. Recent discoveries have documented the existence of planktotrophs that have intermediate egg sizes, differing degrees of dependence on exogenous food, and differing capacities for facultative feeding. A fecundity‐time model is presented that includes facultative larval feeding by dissociating the onset of feeding capability from the need for exogenous food. The facultative feeding model shows that reproductive success can be maximized at intermediate levels of investment per offspring between the minimum for development and the threshold for lecithotrophy, depending on the amount of food available to larvae and the intensity of planktonic mortality. A continuum of larval strategies is predicted.

Life Cycle Evolution in Asteroids: What is a Larva?

The diversity of larval forms and developmental patterns in asteroid echinoderms has become increasingly apparent over the past 10-15 years. However, the classification of developmental patterns has been ambiguous because the patterns have not been defined as unique sets of ecological and developmental character states. In addition, character states have not been defined consistently. Thus attempts to understand the evolutionary changes in development (e.g., heterochrony and heterotopy in morphogenesis) that underlie larval diversity have been hampered. We propose a multifactor classification of asteroid developmental patterns that uses an explicit set of characters that provide information on habitat (e.g., pelagic or benthic) and mode of nutrition (e.g., feeding or nonfeeding) of the developing young, as well as the type of morphological development (indirect = larval; direct = nonlarval). We conclude that direct development is exceptionally rare. All asteroids whose development has been studied, except Pteraster tesselatus, have the indirect type of development. We also propose definitions of some important terms that have been used inconsistently in the literature (e.g., larva, metamorphosis, indirect development, and direct development). Our definitions take into account the continuous nature of development and the evolutionary diversification of ontogenetic sequences. These definitions are intended to provide a clear conceptual basis for analyzing asteroid life cycle evolution. We argue that the ancestral asteroid life cycle involved pelagic larval development with both bipinnarian and brachiolarian stages. We then present a series of hypotheses for six types of evolutionary transitions in development that can account for the diversity of larval forms and developmental patterns in starfish.

Interspecific relationships between egg size and the level of parental investment per offspring in echinoderms.

The relationship between the size of an egg and its energy content was analyzed using published data for 47 species of echinoderms. Scaling relationships were evaluated for all species, as well as for subsets of the species, based on mode of development. Regressions were calculated using linear, power function, full allometric, and second-order polynomial models. The full allometric model is preferred because it is relatively simple and the most general. Among these species of echinoderms, larger eggs contain more energy. Egg energy content scales isometrically across a wide range of egg sizes both among and within different modes of development. The only exception is among species with feeding larval development, where there does not seem to be a clear scaling relationship. In most cases, the regressions were statistically significant and explained a very large proportion of the variance in energy content. However, there were wide confidence intervals around the estimated regression parameters. In all cases, the predictive power of the regression was poor, requiring large differences in egg size to yield significantly different predictions of energy content. Consequently, egg size is of limited value for the quantitative prediction of egg energy content and should be used with caution in life-history studies.

Body form and skeletal morphometrics during larval development of the sea urchin Lytechinus variegatus Lamarck

Development of the echinopluteus of the subtropical/tropical sea urchin Lytechinus variegatus Lamarck, was studied using quantitative measures of size, shape, and the growth of the larval body and skeleton. Larvae of L. variegatus developed rapidly, attaining metamorphic competence in 9–10 days (depending on diet) at a culture temperature of 26°C. Larvae grew substantially from the initial 2-arm pluteus stage to the fully developed eight-arm pluteus with a juvenile rudiment. Larval length increased 2.8-fold, total arm length (summed over all larval arm pairs) increased 7.3-fold. Ciliated band length (an index of feeding capability) increased 6.8-fold, 76% of the increase was allometric, i.e., due to shape change. An index of shape, the ratio of ciliated band length: body length increased 2.8-fold during development to a maximum value of 13.87. Allometric growth occurred both during the period of arm formation and later during rudiment formation by disproportionate growth of the larval arms. The echinopluteus skeleton of Lytechinus variegatus consists of six separate elements: 2 sets of paired (left and right) elements, the body-postoral-anterolateral rod complex and the posterodorsal rods; and 2 unpaired elements, the dorsal arch and the posterior transverse rod. The skeleton of the main body region (body rods) did not grow after the formation of the initial 2-arm larval stage. Body length and arm length increases were due entirely to elongation of the arm skeleton. Increases in larval circumference and development of various lobes were supported by elongation of the dorsal and ventral transverse rods. Pedicellariae (1–3) developed around day 7 at the posterior of the larva. Juvenile skeletal plates developed in association with the proximal tips of several larval skeletal rods, such as the base of the dorsal arch and the bases of the posterodorsal rods. There are several common features of pluteus larval growth that are shared among species, with different egg sizes, from different orders, and from different geographic regions. The most important similarity is the scaling of feeding structures (ciliated band length) relative to larval body size. Elaboration of the ciliated band is by growth of the larval arms with 60–70% of the band located on the arms. However, there are differences in which arm pairs contribute most to form change and feeding capability. These descriptions and comparisons suggest both similarities and differences in larval growth and form that are functionally important and deserve greater attention from larval ecologists.

Size and energy content of eggs from echinoderms with pelagic lecithotrophic development

Abstract Mean egg energy content (J · egg −1 ) was significantly and positivelycorrelated with mean egg volume among seven species of holothuroid and asteroid echinoderms with pelagic lecithotrophic (non-feeding) larval development. However, there were not consistent intraspecific relationships between egg size and energy content. Mean egg energy concentration (J · μl −1 ) was variable but was not significantly correlated with egg volume, in contrast to the negative correlation reported for species with planktotrophic (feeding) larvae. Egg energy concentrations in species with pelagic lecithotrophic larvae are similar to those in species with benthic lecithotrophic development (brooding) and significantly greater than in species with pelagic planktotrophic larvae.

Effects of delayed settlement on survival, growth, and reproduction in the spionid polychaete, Polydora ligni

Summary Larvae of the spionid polychaete, Polydora ligni Webster 1879, were forced to delay settlement and metamorphosis for 6 days by withholding suitable substrata. Daily mortality was 2.5% during the competent period of larval development. Starvation increased mortality to 5.4% per day. A high percentage of the control (nondelayed) and fed, delayed larvae metamorphosed (70–81%) and the newly metamorphosed juveniles were the same size in these 2 groups. However, delay combined with starvation greatly reduced metamorphic success (to 15%) and juvenile size. Delay (with feeding) significantly decreased somatic and reproductive growth of post-metamorphic juveniles compared to the nondelayed control group. Costs of delayed settlement and metamorphosis could partially offset the advantages of extending the larval period for benthic habitat selection.

Echinoid larval ecology

This chapter describes the diversity of larval stages and the patterns of development in echinoids. Most echinoids, including all but one of the edible species, are free-spawners that produce vast numbers of small, yolk-poor eggs that develop into planktonic, feeding larvae known as echinoplutei. This chapter also gives a walkthrough over the ecological challenges that echinoplutei face, and the physiological, morphological, developmental, and behavioral solutions that are utilized to respond to the problems. Tables showing the life cycle patterns and developmental character states in echinoids and the Egg characteristics of echinoids are also documented in this chapter. Other factors such as fertilization ecology, feeding mechanisms, phenotypic plasticity, and evolution of nonfeeding larvae are also well studied in this chapter. Many aspects of the basic biology and ecology of larvae, such as nutritional requirements, environmental tolerances, disease resistance, settlement preferences, dispersal ecology, and population dynamics, which are particularly important for aquaculture and commercial harvesting, remain very poorly known.

Effects of the duration and timing of starvation during larval life on the metamorphosis and initial juvenile size of the polychaete Hydroides elegans (Haswell)

The larvae of the polychaete Hydroides elegans were exposed to different feeding schedules to evaluate the effects of starvation on metamorphosis and initial juvenile volume. The timing of starvation (early or late in development) and the total number of days of feeding (3, 5 or 8 days) at 24 degrees C had significant effects on the percentage of larvae that successfully completed metamorphosis and on the volume of the post-metamorphic juveniles. However, the duration of starvation (2, 4, 6 or 8 days) did not influence metamorphosis or juvenile volume. For larvae that had fed for 3 or 5 days, those that were starved at the beginning of development had a higher percentage of successful metamorphosis and produced larger juveniles compared with those starved after an initial 3-day feeding period. Larvae that had been allowed to feed for a total of 8 days were not affected by the timing of starvation. The percentage metamorphosis was lower in larvae that had fed for 3 days (16%), but was not significantly different between those that fed for 5 days (47%) compared to 8 days (47%). However, juvenile volume increased with the number of days of feeding from 0.95 nl after 3 days to 1.35 nl after 5 days, to 1.91 nl after 8 days of feeding. Discontinuous feeding reduced the proportion of larvae undergoing metamorphosis and juvenile volume compared to larvae continuously fed for only 5 days, but had no effect on larvae that fed for 8 days. The larvae of this extremely successful fouling species are remarkably tolerant of starvation and seem to require approximately 5 days of continuous feeding to achieve high levels of metamorphic success and large initial juvenile volume.

CYPHONAUTES' CILIARY SIEVE BREAKS A BIOLOGICAL RULE OF INFERENCE

Biologists routinely assume that a mechanism demonstrated in one organism will be found in others in which form, function, ancestry, and physical parameters are similar. These criteria failed to predict the feeding mechanism of the cyphonautes larva of bryozoans. Larval and adult bryozoans feed with cilia similar in size and distribution, with similar current velocities, and similar Reynolds numbers. Nevertheless, the larvae filter particles with a sieve of stationary cilia whereas the adults respond to individual particles with an induced local reversal of ciliary beat and concentrate particles without filtration. The larvas ciliary sieve is doubly unexpected because it requires a ciliary stiffness at the maximum recorded for cilia.

Morphology and Development of a Unique Type of Pelagic Larva in the Starfish Pteraster tesselatus (Echinodermata: Asteroidea)

Several unusual features characterize the morphology of the pelagic larva of the starfish Pteraster tesselatus and its metamorphosis into the juvenile stage: (1) morphogenesis of the supradorsal membrane during metamorphosis by fusion of 15 lobes on the aboral region of the body; (2) absence of brachiolar arms and attachment disk; (3) heterochronic acceleration of development in the water vascular system, and use of podia for attachment to the substratum at settlement; (4) radial (rather than bilateral) symmetry of the larva; and (5) congruent larval and adult axes of symmetry, and a transverse orientation of the adult rudiment within the larva. Collectively, these features demonstrate that P. tesselatus has a highly derived mode of development and a larva that is unique among the asteroid echinoderms. In contrast to the current interpretation of this larva as a modified pelagic brachiolaria, I suggest that the unusual larva of Pteraster represents an example of an apparently rare evolutionary transition in animal development: the re-evolution of pelagic larval development from benthic brooding.