Benjamin G. Miner

Size correction: comparing morphological traits among populations and environments

Morphological relationships change with overall body size and body size often varies among populations. Therefore, quantitative analyses of individual traits from organisms in different populations or environments (e.g., in studies of phenotypic plasticity) often adjust for differences in body size to isolate changes in allometry. Most studies of among population variation in morphology either (1) use analysis of covariance (ANCOVA) with a univariate measure of body size as the covariate, or (2) compare residuals from ordinary least squares regression of each trait against body size or the first principal component of the pooled data (shearing). However, both approaches are problematic. ANCOVA depends on assumptions (small variance in the covariate) that are frequently violated in this context. Residuals analysis assumes that scaling relationships within groups are equal, but this assumption is rarely tested. Furthermore, scaling relationships obtained from pooled data typically mischaracterize within-group scaling relationships. We discuss potential biases imposed by the application of ANCOVA and residuals analysis for quantifying morphological differences, and elaborate and demonstrate a more effective alternative: common principal components analysis combined with Burnaby’s back-projection method.

Densovirus associated with sea-star wasting disease and mass mortality

Significance Sea stars inhabiting the Northeast Pacific Coast have recently experienced an extensive outbreak of wasting disease, leading to their degradation and disappearance from many coastal areas. In this paper, we present evidence that the cause of the disease is transmissible from disease-affected animals to apparently healthy individuals, that the disease-causing agent is a virus-sized microorganism, and that the best candidate viral taxon, the sea star-associated densovirus (SSaDV), is in greater abundance in diseased than in healthy sea stars. Populations of at least 20 asteroid species on the Northeast Pacific Coast have recently experienced an extensive outbreak of sea-star (asteroid) wasting disease (SSWD). The disease leads to behavioral changes, lesions, loss of turgor, limb autotomy, and death characterized by rapid degradation (“melting”). Here, we present evidence from experimental challenge studies and field observations that link the mass mortalities to a densovirus (Parvoviridae). Virus-sized material (i.e., <0.2 μm) from symptomatic tissues that was inoculated into asymptomatic asteroids consistently resulted in SSWD signs whereas animals receiving heat-killed (i.e., control) virus-sized inoculum remained asymptomatic. Viral metagenomic investigations revealed the sea star-associated densovirus (SSaDV) as the most likely candidate virus associated with tissues from symptomatic asteroids. Quantification of SSaDV during transmission trials indicated that progression of SSWD paralleled increased SSaDV load. In field surveys, SSaDV loads were more abundant in symptomatic than in asymptomatic asteroids. SSaDV could be detected in plankton, sediments and in nonasteroid echinoderms, providing a possible mechanism for viral spread. SSaDV was detected in museum specimens of asteroids from 1942, suggesting that it has been present on the North American Pacific Coast for at least 72 y. SSaDV is therefore the most promising candidate disease agent responsible for asteroid mass mortality.

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.

Should I stay or should I go: predator- and conspecific-induced hatching in a marine snail

Predator-induced hatching plasticity has been demonstrated in many species of amphibians. However, animals from other clades (e.g., marine species of molluscs and annelids) also place their embryos in capsules or gelatinous masses and might also exhibit hatching plasticity to predators. To date there is no evidence of predator-induced hatching plasticity from any marine species or a major clade of bilateria animals, the Lophotrochozoa. We studied predator-induced hatching plasticity of Nucella lamellosa, a carnivorous marine snail that deposits embryos in capsules. We used two experiments to investigate the effects of two types of predator, crabs and isopods, on developing embryos. In the first experiment, we quantified proportion of hatched embryos from capsules through time exposed to water-borne chemicals of crabs and isopods. Crabs delayed time-to-hatching, and the effects of predators were additive. In the second experiment, we quantified proportion of hatched embryos from capsules through time, developmental stage, and size of embryos in capsules exposed to water-borne chemicals of crabs and conspecifics. With this experiment, we wanted to answer: (1) whether a delay in hatching corresponded to embryos developing slower, and (2) whether the general products of metabolic waste from organisms can delay hatching. We unexpectedly observed that adult conspecific snails accelerated hatching but not developmental rate—the few past studies on the effects of conspecifics have all demonstrated that conspecifics delay time-to-hatching and rate of development. The results were also inconsistent with metabolic waste in general causing a delay in hatching, although the effect of conspecifics does weaken this inference. This study demonstrates that predators delay time-to-hatching in a marine mollusc, and suggests that predator-induced hatching plasticity is widespread among animals and likely evolved multiple times within the bilateria. In addition, conspecifics accelerated time-to-hatching in a marine mollusc, which suggests that conspecifics, like predators, might commonly influence when embryos hatch.

Functional and Evolutionary Implications of Opposed Bands, Big Mouths, and Extensive Oral Ciliation in Larval Opheliids and Echiurids (Annelida)

Larvae of two annelids, the opheliid Armandia brevis and the echiurid Urechis caupo, captured small particles between opposed prototrochal and metatrochal ciliary bands and also captured large particles with wide ciliated mouths. The body volume of larval A. brevis increased more rapidly than the estimated maximum clearance rate as segments were added. Capture of larger particles by late-stage larvae may compensate for this potentially unfavorable allometry. The existence of larvae that use two feeding mechanisms at once, not previously known in annelids, suggests possible evolutionary routes between larval forms that feed only with opposed bands (e.g., serpulids and oweniids) and those that use complex oral ciliature to feed primarily on large particles (e.g., polynoids and nephtyids). In particular, the metatroch and food groove of opposed-band feeders may have arisen as expansions of oral ciliation in ancestral large-particle feeders; alternatively, extensive oral ciliation in large-particle feeders may have originated as a modification of metatroch and food-groove cilia in ancestral opposed-band feeders.

Legacies in life histories

Complex life-histories are common in nature, have many important biological consequences, and are an important focal area for integrative biology. For organisms with complex life-histories, a legacy is something handed down from an ancestor or previous stage, and can be genetic, nutritional/provisional, experiential, as well as the result of random chance and natural variation in the environment. As we learn more about complex life-histories, it becomes clear that legacies are inexorably linked in the short- and long-term through ecology and evolution. Understanding the consequences and drivers of life-history patterns can therefore only be understood by considering all types of legacies and integrating legacies across the entire life cycle. Larry McEdward was a leader in the field of ecological physiology, and evolutionary ecology of marine invertebrate larvae with complex life-histories. Through his scientific work and publications, devotion to students, colleagues, family, and friends, Larry has left a lasting legacy that will impact the future development of the field of larval ecology and complex life-histories.

Behavioral plasticity in an invaded system: non-native whelks recognize risk from native crabs

Inducible defenses have the potential to affect both invasion success and the structure of invaded communities. However, little is known about the cues used for risk-recognition that influence the expression of inducible defenses in invasive prey, because they involve a novel threat. In laboratory experiments, we investigated behavioral defenses induced by a native crab on two invasive oyster drills (marine whelks Urosalpinx cinerea and Ocinebrina inornata). Both drills hid more often and reduced their feeding rates when they detected predators consuming conspecific prey. Examination of the responses of U. cinerea to specific cue sources (predator kairomones, conspecific alarm cues) indicated that this species had the strongest responses to cues from injured conspecifics, but that it did recognize the novel crab predator. Our observation of native predator (per se) recognition by an invasive marine prey is novel. In addition, we observed that neither species of drill reduced their defensive behavior to reflect predation risk shared by a group of prey. The lack of density dependence in risk-assessment could cause populations of invasive prey to transmit both quantitatively and qualitatively different community effects over the course of an invasion as abundance changes. Together, these findings demonstrate several ways that the risk-assessment strategies could be important in establishment and post-establishment dynamics of invasive prey.

Culture of echinoderm larvae through metamorphosis.

Publisher Summary This chapter outlines general methods for culturing larval food (unicellular algae), for caring and feeding larvae, and for inducing metamorphosis. The materials used for culturing algae and larvae are culture vessels, one or more aquarium air pumps, along with flexible plastic tubing, valves, connectors, and sea water. A critical component of success in rearing echinoderm larvae is low larval density. Another critical component of success in rearing echinoderm larvae is keeping cultures free of contamination. The most common problems are molds, bacteria, and ciliate protozoans. To lower the risks of contamination, culture larvae at low density should not be overfed with algae; algal cultures should themselves not be contaminated prior to feeding. Salt water (SW) is changed every 2 or 3 days (more often to optimize developmental rates, less often to save labor). SW is changed immediately if cultures become contaminated at least once per day thereafter for several days. Following SW changes, larvae are transferred to clean culture vessels to minimize the risk of contamination. Few echinoderm larvae will readily undergo settlement and metamorphosis in a clean glass culture jar, even when fully competent to do so. The chapter discusses a variety of methods used to induce metamorphosis.

Estimation and interpretation of egg provisioning in marine invertebrates

Per-offspring maternal investment is an integral part of life-history theory. To understand the evolution of per-offspring maternal investment in marine invertebrates, a number of mathematical models have been developed. These models examine how selection affects the proportion of maternally derived egg energy used to produce a newly metamorphosed juvenile (s) and make predictions about the distribution of s in nature. However, there are very few published values of s and therefore it is difficult to evaluate how well these models match nature. We present several equations to empirically estimate values of s for any group of marine invertebrate, and use data from echinoderms to compare the different equations. The calculations that directly estimate s require information on the amount of egg energy, juvenile energy, and energy metabolized during development. Currently, there are few data available for directly estimating s, and thus generating distributions of s derived from direct estimates is not possible. Furthermore, the direct estimations of s are informative for planktotrophy but not for lecithotrophy. We have developed an equation that can be used to directly estimate s for lecithotrophs. The calculations to indirectly estimate s only require egg energy or egg size for the species in question and the value of s and egg energy or size for a reference species. This reference species replaces the need to measure juvenile energy and energy metabolized during larval development. Because egg energy or size is currently available for many species, the indirect estimates will be useful for generating distributions of s, and will allow comparisons with models. Although these indirect methods are good for generating distributions of s, they do not provide reliable estimates of s for any particular species. Estimating values of s to compare models is a critical gap in our current evaluations of marine invertebrate life-history models.

Egg Energetics for the Facultative Planktotroph Clypeaster rosaceus (Echinodermata: Echinoidea), Revisited

The sand dollar Clypeaster rosaceus has an unusual reproductive strategy known as facultative planktotrophy. The egg energy previously reported by Emlet (1) forC. rosaceus is low, and because it is used to estimate values of an important parameter in marine invertebrate life-history models (s), we remeasured the egg energy content. Our measurement of egg energy content was approximately 2-fold greater than Emlet’s (0.11 0.014 SD joules (J) egg 1 vs. 0.047 0.007 SD J egg 1 ) with no difference in egg diameter (274 4.38 SDm vs. 280 7.67 SDm). This result is unlikely to be due to temporal or spatial variation among populations of C. rosaceus. Given the improved technique used to measure egg energy content, an egg energy density (J ml 1 ) more consistent with other observations, and the improved fit of egg sizevs. egg energy regressions for echinoderm planktotrophs, we conclude that our estimate is more accurate. In addition, we detected small annual variation (10%) in egg energy content between females sampled during 2000 and 2001. Facultative planktotrophy is intermediate between the two common types of echinoid larval development: planktotrophy and lecithotrophy (1). Planktotrophic larvae develop from small, energy-poor eggs and require exogenous food to complete development and metamorphosis. In contrast, lecithotrophic larvae develop from large, energy-rich eggs and can complete development without feeding. Although rare, facultative planktotrophs such as Clypeaster rosaceus may represent an important transition in the evolution of marine invertebrate life-history strategies (2, 3). Models of the evolution of larval strategies in marine invertebrates characterize reproductive strategies in terms of the level of egg provisioning (s) (4). These models evaluate the trade-off between fecundity and mortality as a function of s, and assume that selection acts on this character. It is therefore important to estimate values of s for numerous species to compare the natural distribution of s with model results. An informative method for calculating values of s requires comparing egg energy content against a reference species that is near the boundary between planktotrophy and lecithotrophy (5). Clypeaster rosaceus has a level of egg