Richard B. Emlet

OFFSPRING SIZE AND PERFORMANCE IN VARIABLE ENVIRONMENTS: FIELD STUDIES ON A MARINE SNAIL

This study links offspring size and energetic content to offspring performance (measured as growth and survivorship) in the intertidal gastropod Nucella ostrina and examines the effect of hatching size on performance at different times of year and in contrasting environments. The relationships between individual hatchling size and organic content were compared both within and among clutches of N. ostrina. Hatchling size was positively, significantly, and predictively correlated with hatchling organic content both within and among clutches, demonstrating that hatching size could be reliably used as an indicator of maternal investment. The slope of the relationship between hatchling size and organic content varied between clutches, suggesting intrapopulation variation in embryonic growth geometry. In field outplants, hatching size always had a positive and significant effect on growth, and small hatchlings took approximately one month to reach the initial size of their larger siblings. More large hatchlings than small hatchlings were recovered in every experimental outplant. The effect of hatching size on recovery was not significant in short (9 d) outplants, but recovery of large hatchlings was significantly greater than recovery of small hatchlings in two out of three long-term (36 or 54 d) outplants. Overall recovery was lower in the summer, the long-term outplant in which size did not significantly affect recovery. In experiments testing the relationship between hatching size and survi- vorship in two environments that differed in degree of sun exposure, size significantly and positively affected recovery in the more shaded habitat (with higher overall recovery) but not in the sun-exposed environment. Thus, larger hatching size in N. ostrina results in (1) increased hatchling growth, (2) considerably shortened time to maturity, and (3) higher survivorship. However, the advantage of large hatching size was decreased under more severe environmental conditions, those which resulted in higher overall hatchling mortality. Contrary to predictions, poor environmental conditions may not be more likely to select for large offspring size in intertidal habitats: during periods of high heat stress, mortality may be largely random with respect to size.

OFFSPRING SIZE EFFECTS MEDIATE COMPETITIVE INTERACTIONS IN A COLONIAL MARINE INVERTEBRATE

Over the past 30 years, numerous attempts to understand the relationship between offspring size and fitness have been made, and it has become clear that this critical relationship is strongly affected by environmental heterogeneity. For marine invertebrates, there has been a long-standing interest in the evolution of offspring size, but there have been very few empirical and theoretical examinations of post-metamorphic offspring size effects, and almost none have considered the effect of environmental heterogeneity on the offspring size/fitness relationship. We investigated the post-metamorphic effects of offspring size in the field for the colonial marine invertebrate Botrylloides violaceus. We also examined how the relationship between offspring size and performance was affected by three different types of intraspecific competition. We found strong and persistent effects of offspring size on survival and growth, but these effects depended on the level and type of intraspecific competition. Generally, competition strengthened the advantages of increasing maternal investment. Interestingly, we found that offspring size determined the outcome of competitive interaction: juveniles that had more maternal investment were more likely to encroach on another juveniles territory. This suggests that mothers have the previously unrecognized potential to influence the outcome of competitive interactions in benthic marine invertebrates. We created a simple optimality model, which utilized the data generated from our field experiments, and found that increasing intraspecific competition resulted in an increase in predicted optimal size. Our results suggest that the relationship between offspring size and fitness is highly variable in the marine environment and strongly dependent on the density of conspecifics.

EFFECTS OF EGG SIZE ON POSTLARVAL PERFORMANCE: EXPERIMENTAL EVIDENCE FROM A SEA URCHIN

Many life-history and developmental studies of marine invertebrates assume that eggs of species with nonfeeding larvae are large because they provide materials for rapid development. Using the sea urchin Heliocidaris erythrogramma which has 400 μm eggs and nonfeeding larvae, we removed an acellular, lipid-rich component from the blastula equivalent to ca. 40% of the egg volume and ca. 50% of the organic mass. Experimentally manipulated, reduced-lipid larvae survived well, developed in the usual time (3.5 d), and high percentages of the original numbers metamorphosed into anatomically normal juveniles. Control juveniles were larger at metamorphosis, grew more, and survived longer than siblings that lacked this lipid-rich material. Moderate increases in egg size in species with nonfeeding larvae may enhance postlarval performance significantly and therefore may reflect selection on early juvenile traits. The contrasts of our results and comparable experiments with feeding larvae suggests that egg size may play fundamentally different roles in species with feeding and nonfeeding larvae. The accommodation of materials reserved for the juvenile stage should be considered among hypotheses on evolutionary modification of developmental patterns.

DEVELOPMENTAL MODE AND SPECIES GEOGRAPHIC RANGE IN REGULAR SEA URCHINS (ECHINODERMATA: ECHINOIDEA)

Among marine benthic organisms, the ability to disperse, primarily during the larval stage, is widely thought to influence the extent of species geographic range. Because related species often differ in their modes of larval development (pelagic, feeding larvae; pelagic, nonfeeding larvae; or brooded development), and these can have dramatically different planktonic intervals, the mode of development may influence geographic range. A global survey of 215 regular echinoids shows that species with pelagic, feeding larvae have significantly larger ranges than those with pelagic, nonfeeding larvae, but there is no difference in ranges between species with pelagic, nonfeeding larvae and those with brooded development. These patterns are maintained within the Cidaroida and the Temnopleuroida, which account for the great majority of species with pelagic, nonfeeding development and brooded development. This limited effect of developmental mode on geographic range is found among species occurring predominantly in waters shallower than 100 m. For species occurring deeper than 100 m, there is no significant difference in geographic range related to type of development. The relationship between developmental mode and species range was examined more closely for circa 30 species for which the developmental period was known from laboratory observations. Adjusting the developmental times to a common temperature, 20°C, using realistic values for Q10 from 2.0 to 3.6, showed a highly significant, negative correlation between egg volume and developmental time, indicating the potential for developmental mode to influence the planktonic interval. However, there was no relationship between time in the plankton, estimated from unadjusted developmental times, and extent of species geographic range. These results suggest that developmental mode may influence extent of species geographic ranges indirectly through the consequences of dispersal for gene flow or recovery from disturbance.

Linking stages of life history: How larval quality translates into juvenile performance for an intertidal barnacle (Balanus glandula)

Many marine invertebrates with complex life cycles produce planktonic larvae that experience environmental conditions different from those encountered by adults. Factors such as temperature and food, known to impact the larval period, can also affect larval size and consequently the size of newly settled juveniles. After documenting natural variation in the size of cyprids (the final larval stage) of the barnacle Balanus glandula, we experimentally manipulated temperature and food given to larvae to produce cyprids of differing sizes but within the size range of cyprids found in the field. In a set of trials in which larvae of B. glandula were raised on full or reduced rations in the laboratory and subsequently outplanted into the field as newly metamorphosed juveniles, we explored the effects of larval nutrition and size on juvenile performance. Larvae that received full rations throughout their feeding period produced larger cyprids (with more lipid and protein). These larger cyprids grew faster as juveniles and sometimes survived better in the field than juveniles from larvae that had their food ration reduced in the last feeding instar. For naturally settling barnacles brought into the laboratory within 2 days of settlement and fed, we found that initial juvenile size was a good predictor of juvenile size even after 2 weeks of growth. By manipulating food given to juveniles that were derived from larvae fed either full or reduced rations, we found that larval nutritional effects persisted in juveniles for 2-3 times the period that larvae experienced altered food rations.

MACROEVOLUTIONARY CONSEQUENCES OF DEVELOPMENTAL MODE IN TEMNOPLEURID ECHINOIDS FROM THE TERTIARY OF SOUTHERN AUSTRALIA

Abstract Taxonomic revision and cladistic analysis of a morphological dataset for Australian Tertiary temnopleurids resolve the phylogeny of the group and allow the testing of a series of hypotheses about the evolution of larval development and consequences of changes in development. Australian Tertiary temnopleurids encompass all three major developmental types found in marine invertebrates (planktotrophy, lecithotrophy, and brooding). Planktotrophy is plesiomorphic for this clade, and nonplanktotrophic larval development evolved independently at least three times during the Tertiary. The change to a nonplanktotrophic mode of larval development is unidirectional with no evidence of reversal. In addition, there is no evidence of an ordered transformation series from planktotrophy through planktonic lecithotrophy to brooding. In common with previous studies of other invertebrate groups, analysis of the raw data suggests that nonplanktotrophic taxa within this clade have significantly shorter species longevities, more restricted geographic ranges and higher speciation rates than taxa with planktotrophic development. However, analysis using phylogenetically independent contrasts is unable to confirm that the stratigraphic and geographic patterns are unbiased by the phylogenetic relationships of the included taxa.

METAMORPHOSIS OF BARNACLE NAUPLII: EFFECTS OF FOOD VARIABILITY AND A COMPARISON WITH AMPHIBIAN MODELS

Like many animals, barnacles have a complex life cycle with shifts in both diet and habitat. The life cycle of most barnacles has three distinct phases: (1) a planktotrophic nauplius, (2) a non-feeding, planktonic cyprid that subsists on energy reserves, and (3) a benthic juvenile and adult. We conducted a series of experiments to measure the effects of variable food concentration during the naupliar phase on the age, size, and lipid reserves of Balanus glandula cyprids. When food shifted during only the first ∼25% of the naupliar phase (the first three instars), the initial food level did not affect the timing of metamorphosis to the cyprid. Shifts in food that were restricted to the final ∼40% of the naupliar phase (the sixth instar) also did not affect age at metamorphosis. During the intermediate portion of the naupliar phase, enhanced food decreased the age at metamorphosis, while reduced food lengthened the naupliar phase. Cyprid size generally correlated positively with changes in food, but a maxim...

Development of newly metamorphosed juvenile sea urchins (Strongylocentrotus franciscanus and S. purpuratus): morphology, the effects of temperature and larval food ration, and a method for determining age

Abstract Following metamorphosis, juveniles of marine benthic invertebrates continue to develop traits that allow them to function and survive in their (new) non-pelagic environment. The sensitivity of juvenile development to environmental conditions or larval quality, such as nutritional condition, are not well understood. This study presents descriptions of trait development that allow species identification of newly metamorphosed juvenile sea urchins Strongylocentrotus franciscanus and S. purpuratus . Following metamorphosis, these two species were distinguishable for at least 3 weeks by different patterns of coronal and aboral pedicellariae. Temperature studies, conducted at three environmentally relevant levels (8, 11, and 14°C) show that developmental rates varied, but the order in which structures formed and became functional in the first 2 weeks after metamorphosis were not affected by temperature. Juvenile feeding begins 9 days after metamorphosis at 14°C and after other traits have developed. Based on suites of traits, we identified juvenile stages and quantified effects of temperature on rate of development (stage day −1 ) with nonparametric regression and with a temperature coefficient, Q 10 . Additional laboratory studies on S. purpuratus show that larval food ration strongly affects the rate of juvenile trait development prior to and after the onset of feeding by juveniles. Comparisons of size of juvenile rudiments and size at metamorphosis between larvae reared in the laboratory at two food levels and wild-caught larvae and juveniles from coastal Oregon (USA) indicate those from the field were well fed and developed at rapid rates. The above information was used to develop a procedure for aging field caught juveniles (≤2 weeks after metamorphosis), provided their thermal history is known. This procedure can be adapted for other invertebrates that acquire traits in an orderly fashion and can be used, in addition to sampling-intensive surveys, to investigate recruitment dynamics in benthic populations.

Energy Use During the Development of a Lecithotrophic and a Planktotrophic Echinoid

The energy required for development was measured in two closely related echinoids with differing modes of development. Heliocidaris tuberculata hatches from a 95-{mu}m egg (~0.1 {mu}g dry organic mass) and develops via a planktotrophic larva over 21-30 days into a juvenile (5.3-7.5 {mu}g). H. erythrogramma hatches from a ~400 {mu}m egg (11.6-19.0 {mu}g) and develops over 3.5-4 days via a lecithotrophic larva into a juvenile with a mass not detectably different from that of the egg. Oxygen consumption increased exponentially in H. tuberculata and peaked at about 200-500 pmol indiv-1 h-1, whereas the oxygen consumption of H. erythrogramma increased rapidly, reaching a plateau at about 800 pmol indiv-1 h-1 on the second day. Metabolic energy expenditure for development to metamorphosis was twofold higher for H. tuberculata (52-60 mJ indiv-1) than for H. erythrogramma (26-35 mJ indiv-1). The interspecific comparison suggests that about half the metabolic expenditure for planktotrophic development goes toward building and operating the larval feeding apparatus and that the return on this investment is 400%-600% over the larval period. When the energy equivalents of the organic masses of the juveniles are included, the energy for constructing a juvenile on a per mass basis is essentially the same for both species (cf. H. tuberculata: 37-42 mJ {mu}g-1; H. erythrogramma: 34-36 mJ {mu}g-1) and implies the absence of developmentally based energetic barriers or benefits to changes in modes of development. Substantial amounts of metabolically inactive material may be present in embryos with nonfeeding development and should be considered in physiological measurements and comparisons.

Phylogeny and evolution of developmental mode in temnopleurid echinoids

The phylogenetic relationships of 24 nominal species of temnopleurid echinoid were established using molecular and morphological data sets. The analysis combined sequence data from mitochondrial 16S rRNA and cytochrome c oxidase subunit I genes and the nuclear 18S-like small subunit rRNA gene with morphological data concerning coronal, lantern, spine, and pedicellarial traits. All four data sets contain similar phylogenetic information, although each provides support at a different taxonomic level. Two data congruence tests (Templetons test and the incongruence length difference test) suggested no significant heterogeneity between the data sets, and all data were combined in a total evidence analysis. The resulting well-resolved phylogeny suggests that Microcyphus, Amblypneustes, and Holopneustes are not monophyletic genera, and that Temnopleurus (Temnopleurus) and Temnopleurus (Toreumatica) are not closely related and should not be regarded as subgenera. In contrast to previous morphological analyses, Mespilia is found to be more closely related to Temnotrema and Toreumatica than it is to Microcyphus. The phylogeny was used to test a series of hypotheses about the evolution of developmental patterns. All species of Amblypneustes, Holopneustes, and Microcyphus are lecithotrophic, and many of these taxa are restricted to southern Australia. Planktotrophy is the ancestral condition for the temnopleurids, and the 11 instances of lecithotrophic nonplanktotrophy in this clade can be accounted for by a single developmental transition that occurred an estimated 4.4-7.4 million years ago, apparently before the migration of Microcyphus to southern Australia. The switch to a nonplanktotrophic mode of development is unidirectional with no evidence of reversals.