Gregarious larval settlement, a phenomenon in which cues associated with conspecifics induce larval settlement, plays a role in the growth of existing aggregations of many aggregation-forming sessile marine invertebrates. The formation of new aggregations, however, requires larvae to settle in response to other cues. The mechanism underlying this variation in larval settlement responses is unknown for most species with gregarious settlement. In this study we first present evidence that larvae of the serpulid annelid Ficopomatus enigmaticus settle gregariously. In no-choice, still-water experiments, a much higher percentage of larvae settled after 24 h of exposure to conspecific tube than after exposure to mussel shell collected from the same habitat. We then tested the hypothesis that larvae of F. enigmaticus display a genetically determined dimorphism in settlement behavior like that of the serpulid Hydroides dianthus, with most larvae capable of settling only in response to a conspecific cue but a small percentage of larvae capable of settling only in response to a biofilm cue. If this hypothesis is correct, the sum of the percentages of larvae that settle in response to a conspecific cue and those that settle in response to a biofilm cue cannot exceed 100% (since each larva can accept only one of the two cue types throughout its competent period). Our data on F. enigmaticus are not consistent with this prediction, suggesting that individual larvae can respond to multiple types of settlement cues during their competent period. This has significant implications for how frequently larvae can form new aggregations, a topic of special importance for F. enigmaticus and H. dianthus, both of which are well-known invasive species in marine habitats around the globe.

The abilities of sabellariid annelids to regenerate missing anterior or posterior body regions are not well understood. We described regeneration ability in the sabellariid Phragmatopoma californica, carrying out amputations in three locations (the opercular region, the middle of the abdomen, and the posterior of the abdomen) and observing survivorship and regeneration in the resulting body fragments for 6 weeks. Both anterior and posterior regeneration were possible, with fragments missing the head and part of the opercular region regenerating missing anterior structures and fragments missing the posterior part of the abdomen and the cauda regenerating missing posterior structures. The posterior-most body region of sabellariids, the cauda, lacks parapodia and chaetae and is typically described as "apparently unsegmented," which raises questions about where new segments are added during growth. Using light and scanning electron microscopy, we show that caudae of P. californica contain serially repeated septa and lateral blood vessels, suggesting strongly that they are segmented, albeit cryptically. These results clarify previous ambiguity in the literature about the regeneration abilities of sabellariids, which will improve future reconstructions of the evolutionary history of regeneration ability in annelids and help focus new questions on how and where sabellariids add new segments to abdominal and caudal body regions.

Ficopomatus enigmaticus (Fauvel, 1923) is a serpulid annelid known for its invasiveness and its ability to build large reef-like aggregations in warm-temperate mesohaline coastal waters worldwide. Ficopomatus enigmaticus has a characteristic fig-shaped operculum adorned with chitinous, inward-curving spines. The arrangement of the spines on the opercular surface is dimorphic: in some worms, the spines are only arranged around the perimeter, whereas in others, they cover the entire operculum. Here, we examine whether opercular spine arrangement is related to the individual’s mitochondrial cytochrome b (cytb) genotype, sex, or body size. Our data suggests that none of these three characteristics is related to opercular spine arrangement. The underlying causes of the opercular dimorphism are currently unknown. There is no indication that it has any taxonomic significance.

The feeding larvae of echinoderms take two distinct forms: plutei (echinoids, ophiuroids), which have calcified skeletal rods supporting long, slender arms bearing the ciliated band, and non-plutei (asteroids, holothuroids), where the ciliated band is borne on rounded lobes of tissue that do not contain skeletal rods. Many feeding larvae of echinoderms are known to alter the length of their ciliated bands in response to food ration, with larvae fed low rations producing longer ciliated bands (absolutely or relative to body size) than those fed high rations. Prior work suggests that the structural cost of adding a given length of ciliated band might be lower for plutei than for non-plutei, which might affect the scope for phenotypic plasticity in ciliated band length in the two types of larvae. We tested the hypothesis that plutei support a greater length of ciliated band per unit tissue than non-plutei by comparing the relationships between ciliated band length and protein content of larvae of eight species of echinoderms (four echinoids, one ophiuroid, two asteroids, and one holothuroid) fed the same food rations at two timepoints prior to development of juvenile structures. We found no difference between larval forms in length of ciliated band per unit body protein, at least for larvae reared under relatively high food conditions (6000 cells mL-1 Rhodomonas lens), weakening the hypothesis that certain larval forms might be more prone to plasticity on this basis. We then compared the expression of phenotypic plasticity in ciliated band length at three timepoints prior to development of juvenile structures among seven of those eight species (three echinoids, one ophiuroid, two asteroids, and one holothuroid) exposed to low or high food levels (1000 vs. 6000 cells mL-1 R. lens). This is the first study in which larvae of multiple echinoderm classes were reared in similar conditions and in which ciliated band lengths were estimated in three dimensions for all species. We found no evidence of phenotypic plasticity in ciliated band length at pre-feeding stages in any species, but did observe it in feeding stages of five of the seven species studied, including at least one species from each of the four echinoderm classes that include feeding larvae. Our data provide no indication that larvae of the four classes differ in their scope for phenotypic plasticity in ciliated band length, but do suggest differences between pluteus and non-pluteus larvae in how this plasticity can be expressed. We also examined responses of stomach size and mouth width to the two food treatments, and similarly found no indication that scope for phenotypic plasticity in these metrics differed between pluteus and non-pluteus larvae. Finally, we used our three-dimensional estimates of ciliated band length to evaluate a more easily measured estimate of ciliated band length in bipinnaria and auricularia larvae. Measurements of a tracing of the ciliated band from a two-dimensional image allowed for accurate prediction of ciliated band length as measured in three dimensions in these non-pluteus larvae, a result that validates prior studies that have used this two-dimentional method and will permit future researchers to easily estimate ciliated band length in bipinnaria and auricularia larvae.

BackgroundEchinoid larvae are known to display food-induced phenotypic plasticity, where larvae alter their morphology and physiology to reflect available food levels. The aim of this study was to describe the induction and reversal of morphological and physiological plasticity through the entirety of larval development of the sand dollar Dendraster excentricus.ResultsWhen larvae fed a low algal ration were switched to high food conditions at 10-, 20-, and 30-day post-fertilization, we observed rapid induction of the high-fed phenotype as indicated by decreases in postoral arm length (POAL) as well as changes in assimilation and growth efficiencies. Switched larvae required more time to develop, but due to physiological changes in assimilation efficiency, they expended the same total amount of energy to achieve metamorphic competence as constantly high-fed larvae. These morphological results were also confirmed by tracking individual larvae in separate experiments. When larvae were switched from high to low food conditions, short-armed larvae rapidly experienced significant increases in POAL.ConclusionsThese results establish that plasticity responses in echinoid larvae are both reversible and inducible throughout larval development and result in significant adaptive benefits in terms of energy use. Our single larval experiments facilitate future analyses that can explore the genetic and molecular underpinnings of phenotypic plasticity.

Hydrostatic skeletons, such as an elephant trunk or a squid tentacle, permit the transmission of mechanical work through a soft body. Despite the ubiquity of these structures among animals, we generally do not understand how differences in their morphology affect their ability to transmit muscular work. Therefore, the present study used mathematical modeling, morphometrics, and kinematics to understand the transmission of force and displacement in the tube feet of the juvenile six-rayed star (Leptasterias sp.). An inverse-dynamic analysis revealed that the forces generated by the feet during crawling primarily serve to overcome the submerged weight of the body. These forces were disproportionately generated by the feet at more proximal positions along each ray, which were used more frequently for crawling. Owing to a combination of mechanical advantage and muscle mass, these proximal feet exhibited a greater capacity for force generation than the distal feet. However, the higher displacement advantage of the more elongated distal feet offer a superior ability to extend the feet into the environment. Therefore, the morphology of tube feet demonstrates a gradient in gearing along each ray that compliments their role in behavior.

The feeding larvae of many echinoids develop long postoral arms relative to body length when food is sparse but relatively short postoral arms when food is abundant, a response thought to adaptively adjust feeding capability. However, in an important recent study, larvae of Dendraster excentricus exhibited this food-conditioned plasticity only when reared at a high density typical of laboratory cultures; when reared at a lower density more representative of larval densities in nature, they did not exhibit this plastic response. This finding suggests that laboratory results cannot be easily extended to make inferences about phenotypic plasticity in nature. We replicated this study and extended it to an even lower larval culture density and to a second species, Lytechinus pictus . Larvae of D. excentricus developed longer arms adjusted for body length when fed the lower of 2 food rations at all culture densities, though differences were only marginally significant at the lower culture density in one experiment. Larvae of L. pictus tended to develop longer arms adjusted for body length at lower food rations, though differences only approached statistical significance at the highest culture density in one experiment. For both species, contrasts between food rations almost always showed an inverse relationship between postoral arm length and stomach length, consistent with prior work demonstrating trade-offs in investment in these 2 features characteristic of phenotypic plasticity. These results suggest that the feeding larvae of echinoids may exhibit food-conditioned plasticity of postoral arm length even at low natural densities.

Growth and development of planktotrophic larvae are dependent on food availability within a nutritionally heterogeneous ocean. Insufficient food can reduce growth and delay metamorphosis, thereby decreasing survival and recruitment. Phenotypic plasticity allows an organism to adjust its phenotype (morphological, physiological, biochemical) to its environment. Planktotrophic echinoid larvae with low food grow longer arms to increase feeding capacity and with high food grow shorter arms to allocate more resources to faster development of other structures. In this study, we investigated if food-induced plasticity in the Pacific sand dollar, Dendraster excentricus, also involved the regulation of digestive enzyme activities during pre-feeding and early feeding larval stages. We measured protein-specific activities of protein, lipid, and carbohydrate digestive enzymes at 33 h postfertilization (HPF; pre-feeding stages) and 96 HPF (feeding stages) to examine if algal presence influenced enzyme rates at these stages and if there was an interaction between pre-feeding stage and feeding stage algal presence. While all enzymes studied increased activities during development, there was no significant effect of pre-feeding algae levels on pre-feeding digestive enzyme activities for all three types of enzymes studied. Furthermore, there was no interaction between larval feeding status (pre-feeding vs. feeding stage) and the presence of algal food. Evidence of food-induced plasticity was observed during the 96 HPF feeding stage for esterase (lipid digestion) and amylase (carbohydrate digestion). Both enzymes exhibited an increase in protein specific rates similar to 1.6-times greater for larvae reared with algae than for those reared without algae. Protease activities were similar for fed and unfed larvae. The differential responses to food during the larval stage likely reflect the initial biochemical composition of the egg, the composition of algal food, and the unique use of each substrate to sustain larval growth and development. Our results demonstrate a multidimensional food-induced biochemical plasticity response of larvae to their feeding environment which includes discrete temporal windows of sensitivity and different enzyme class-specific responses.

Rates of development of the feeding larvae of marine invertebrates may often be limited by inadequate food, extending the length of the larval period and increasing overall larval mortality. A better understanding of the frequency and importance of this phenomenon requires knowledge of the food concentration below which larvae are limited, and above which they are not, as well as estimates of how strongly food supply affects length of the planktonic period. We addressed these issues using larvae of the sand dollar Dendraster excentricus as a model and chl a concentration as a metric of food abundance. We reared larvae in natural seawater collected from coastal southern California (USA), as well as in reduced and supplemented food treatments created from this natural seawater, 6 times from 2017 to 2019 to take advantage of temporal variation in chl a concentration. Larvae showed morphological responses indicative of low food in nature in only 1 of 6 experiments and showed delayed time to 50% metamorphic competence in 2 of 6 experiments. Larvae appeared to be food limited below chl a concentrations of ~2.4-3.0 µg l -1 , but developed at maximal rates at higher food concentrations. Low natural food supplies delayed time to 50% competence by up to 1.25 d. An 11 yr record of chl a concentration in waters of coastal southern California suggests that larvae of D. excentricus are likely food limited in developmental rate throughout much of the year except for late winter to late spring.

The nonfeeding planktonic larvae of marine invertebrates typically lack larval feeding structures. One puzzling exception to this generalization is the annelid clade Sabellidae, in which nonfeeding larvae possess ciliary bands (specifically, food groove and metatroch) that, to the best of our knowledge, have no function other than in feeding. Nishi and Yamasu (1992b, Bulletin of the College of Sciences, University of the Ryukyus, 54, 107-121) published a scanning electron micrograph showing that nonfeeding larvae of the serpulid annelid Salmacina dysteri also possess food groove and metatrochal cilia. Here I demonstrate that nonfeeding larvae of Salmacina tribranchiata also bear ciliary bands identifiable as food groove and metatroch by position. High-speed video of ciliary beat patterns shows that, together with the prototrochal cilia, these bands function in an opposed band system. The presence of feeding structures in nonfeeding annelid larvae is thus more widely distributed than previously recognized. The presence of feeding structures may make evolutionary transitions to planktotrophy more likely, and may underlie an inferred origin of larval feeding in the common ancestor of one of the two major clades of serpulid annelids, Serpulinae.

The California salt marsh snail Melampus olivaceus , a species from southern California, has established a thriving population in the Elkhorn Slough estuary (Monterey Bay), hundreds of kilometers north of where it is long-established and regularly found. Since the late 1800s this high littoral zone salt marsh snail has occasionally been reported in central California, but only as isolated individuals or shells. We first observed a few individuals of M. olivaceus in Elkhorn Slough in 2013, and the species is now abundant and reproducing throughout the estuary in Salicornia pacifica (pickleweed) marshes. We also document for the first time that this species has a planktonic, feeding larva. Salt marsh snails may have been transported northward as planktonic larvae during periodic El Niño warm water events. Such transport has been reported for other species, but what makes this case unusual is the persistence, reproduction and abundance of the snail following transport.

Because of their lifestyles, abundance, and feeding habits, infaunal marine deposit feeders have a significant impact on the ocean floor. As these animals also ingest microorganisms associated with their sediment and seawater diet, their digestive tract usually contains a diverse array of bacteria. However, while most of these microorganisms are transients, some may become part of a resident gut microbiome, in particular when sheltered from the main flow of digesta in specialized gut compartments. Here, we provide an in-depth analysis of the structure and contents of the intestinal caecum (IC), a hindgut diverticulum found exclusively in schizasterid heart urchins (Echinoidea: Spatangoida: Schizasteridae). Based on specimens of Brisaster townsendi, in addition to various other schizasterid taxa, our structural characterization of the IC shows that the organ is a highly specialized gut compartment with unique structural properties. Next generation sequencing shows that the IC contains a microbial population composed predominantly of Bacteroidales, Desulfobacterales, and Spirochaetales. The microbiome of this gut compartment is significantly different in composition and lower in diversity than the microbial population in the sediment-filled main digestive tract. Inferences on the function and evolution of the IC and its microbiome suggest that this symbiosis plays a distinct role in host nutrition and that it evolved at least 66 million years ago during the final phase of the Mesozoic.

In 1989, Donald Reish hosted the 3rd International Polychaete Conference (IPC3) in Long Beach, on the campus of California State University Long Beach. In 2015 he asked one of us (Bruno Pernet) if it might be possible to bring IPC13 back to Long Beach, thirty years later. Bruno assembled a planning committee consisting of himself and Christine Whitcraft (CSU Long Beach), Kirk Fitzhugh and Leslie Harris (Natural History Museum of Los Angeles County), and Larry Lovell (Dancing Coyote Environmental). The committee’s proposal was accepted at the International Polychaetology Association (IPA) general meeting in Wales in 2016, and the planning committee morphed into an organizational committee!