Jan A. Pechenik

Larval experience and latent effects—metamorphosis is not a new beginning

For many years ecologists have documented the remarkable within-species variation inherent in natural systems-for example, variability in juvenile growth rates, mortality rates, fecundities, time to reproductive maturity, the outcomes of competitive interactions, and tolerance to pollutants. Over the past 20 years, it has become increasingly apparent that at least some of this variation may reflect differences in embryonic or larval experiences. Such experiences may include delayed metamorphosis, short term starvation, short term salinity stress, or exposure to sublethal concentrations of pollutants or sublethal levels of ultra violet irradiation. Latent effects-effects that have their origins in early development but that are first exhibited in juveniles or adults-have now been documented among gastropods, bivalves, echinoderms, polychaetes, crustaceans, bryozoans, urochordates, and vertebrates. The extent to which latent effects alter ecological outcomes in natural populations in the field, and the mechanisms through which they are mediated are largely unexplored.

Delayed metamorphosis by larvae of benthic marine invertebrates: Does it occur? Is there a price to pay?

Abstract In the laboratory, the swimming larvae of benthic marine invertebrates are generally capable of prolonging their larval period beyond the time that they first become physiologically competent to metamorphose. Larvae seem to differ markedly in their ability to postpone metamorphosis, both interspecifically and intraspecifically. The proportion of this variability that is genetically controlled has not yet been determined; if under genetic control, both pre-competent and competent periods would be subject to selection, although the selective pressures and the physiological or developmental mechanisms through which such pressures might operate remain purely speculative. Limited data strongly suggest that at least a few species delay metamorphosis in the field. The frequency with which they do so, and under what conditions they do so, and for how long, are unexplored questions. Some of these issues can now be explored, with the finding that various inorganic and organic substances can trigger the met...

Influence of delayed metamorphosis on survival and growth of juvenile barnacles Balanus amphitrite

Competent cyprid larvae of the barnacle Balanus amphitrite Darwin were prevented from metamorphosing in the laboratory for 3 or 5 d using three different techniques (holding at low temperature, crowding, and detaining on a silanized surface). We then assessed the effects of prolonging larval life on post-metamorphic growth and survival, in comparison with control individuals that metamorphosed soon after they were competent to do so. Seven experiments were conducted over 2 yr (July 1987 to September 1989). In all experiments (each with six replicates per treatment), postponing larval metamorphosis for 3 or 5 d dramatically depressed postmetamorphic growth rate (P<0.05), although metamorphic success and post-metamorphic survival were not affected (P>0.10). The results suggest that B. amphitrite cyprids deferring their metamorphosis in the field may be less successful in competing for space, at least during the first few weeks of postlarval life.

Attachment of Mytilus edulis L.larvae on algal and byssal filaments is enhanced by water agitation.

Abstract Larvae of the blue mussel Mytilus edulis L. are known to settle preferentially on filamentous substrata, in this study, competent larvae attached by secreting byssal threads onto filamentous red algae, Ceramium rubrum (Hudson) Agardh, Cystoclonium purpureum (Hudson) Batters, and Polysiphonia sp., and byssal threads from conspecific adults, but not onto the glass culture dish. Percent attachment to filamentous substrata in static conditions was low (0–30%). Unexpectedly, culture agitation routinely increased percentage attachment to filaments two- to eight-fold. This effect was not due to an influence of agitation on oxygen concentration, no differences in oxygen concentration of shaken vs. static cultures were detected at the end of the test periods. Water agitation in the absence of filaments did not induce attachment to the glass culture dishes. Elevated potassium (5–20 mM increases in KCl levels) and γ-aminobutyric acid (GABA, 10 −6 -10 −4 M) were also tested for ability to induce settlement or metamorphosis of competent mussel larvae, no induction occurred in up to 48-h exposures. To date, the bivalve M. edulis is the first mollusc reported that is not induced to settle and metamorphose by elevated potassium ion levels.

The relationship between temperature, growth rate, and duration of planktonic life for larvae of the gastropod Crepidula fornicata (L.)

Abstract To determine if a relationship exists between rate of development and ability to delay metamorphosis, larvae of the prosobranch gastropod Crepidula fornicata (L.) were reared at 18 and 24°C in the absence of metamorphosis-inducing cues. Average growth rates were determined directly by periodically subsampling and measuring larvae at both temperatures. Individual growth rates were estimated from size at, and date of, spontaneous metamorphosis. Larvae generally grew more quickly at the higher temperature, in terms of shell length, tissue dry weight, and protein content. Regardless of temperature, most (>95%) larvae eventually metamorphosed spontaneously in clean glass dishes. Rapid growth was associated with an apparently shorter pre-competent period and earlier spontaneous metamorphosis, reflecting increased rates of differentiation. These results suggest a developmental mechanism through which selective pressures may operate to determine dispersal potential in this, and perhaps other species. Specifically, pre-competent and delay periods may be altered through selection for different rates of development. Demonstration of such a mechanism may ultimately increase our ability to predict the potential duration of planktonic existence of planktotrophic marine invertebrate larvae under a variety of environmental circumstances.

Influence of delayed metamorphosis on survival, growth, and reproduction of the marine polychaete Capitella sp. I

Abstract In the absence of an appropriate environmental cue, larvae of benthic marine invertebrates typically delay their metamorphosis. Delaying metamorphosis is considered beneficial in promoting placement of offspring into suitable habitats and likely increasing genetic exchange among populations. However, recent studies suggest that delaying metamorphosis can reduce juvenile fitness in some species, by reducing postmetamorphic survivorship or growth rate. The effects of delayed metamorphosis on survival, growth, and reproduction of the marine polychaete Capitella sp. I were tested. The lecithotropic larvae, which are competent to metamorphose within minutes of their release from the parental brood tube, were forced to delay metamorphosis for up to 216 h at 20°C. We induced metamorphosis at intervals by adding azoic sediment, and then reared the juveniles in the laboratory for up to 4 wk. Although survival was significantly reduced ( P 72h, delaying metamorphosis had no convincing effect on postmetamorphic growth rate (μg tissue· day −1 ), time to first reproductive activity, or fecundity.

Using KCl to determine size at competence for larvae of the marine gastropod Crepidula fornicata (L.)

Competent larvae of the marine gastropod Crepidula fornicata (L.) were induced to metamorphose (i.e., lose the velum) by elevating sea-water [KCl] by 5–50 mM. The response was optimal at 15–20-mM elevations, at which 50% metamorphosis was obtained in ≈1125 μm shell length metamorphosed in response to increased [KCl]. Rearing temperature may affect the size at which larvae of this species become responsive to K+. CaCl2 (20-mM concentration elevations), GABA (4×10−7, 4×10−6 M), and NaCl (10–20-mM concentration elevations) generally failed to trigger metamorphosis. Twenty-mM elevations of [RbCl] and [CsCl] induced 100% metamorphosis but the juveniles were immobile and died after several days. Elevating [KCl] appears to be a reliable way to assess competence and trigger metamorphosis in larvae of C. fornicata.

The effect of starvation on acquisition of competence and post-metamorphic performance in the marine prosobranch gastropod Crepidula fornicata (L.)

The duration of the precompetent period of development determines the obligate dispersal period for larvae of many benthic marine invertebrate species. This study considers the extent to which the onset of metamorphic competence in the gastropod Crepidula fornicata (L.) is controlled by growth rate or the attainment of a critical, threshold size. Precompetent larvae of C. fornicata were starved in filtered seawater for up to 6 days at 25 °C and subsequently tested for competence by 5 h exposures to 20 mM excess K+ in seawater. Control larvae were reared in excess phytoplankton suspension (Isochrysis galbana, clone T-ISO) and tested for metamorphic competence concurrently with starved individuals. Even though larvae stopped growing (and in fact lost up to 37% of their initial ash-free dry weight) after being transferred to filtered seawater, many individuals became competent to metamorphose while being starved. These results suggest an allocation of limited energy stores to differentiation rather than to growth, and clearly indicate that the onset of metamorphic competence is not size-dependent and does not depend on growth for larvae of this species. Metamorphosed juveniles grew more slowly if they had been starved as larvae, indicating a link between larval nutritional experience and post-metamorphic performance.

Food limitation stimulates metamorphosis of competent larvae and alters postmetamorphic growth rate in the marine prosobranch gastropod Crepidula fornicata

The effects of food limitation on growth rates and survival of marine invertebrate larvae have been studied for many years. Far less is known about how food limitation during the larval stage influences length of larval life or postmetamorphic performance. This paper documents the effects of food limitation during larval development (1) on how long the larvae ofCrepidula fornicata (L.) can delay metamorphosis in the laboratory after they have become competent to metamorphose and (2) on postmetamorphic growth rate. To assess the magnitude of nutritional stress imposed by different food concentrations, we measured growth rates (as changes in shell length and ash-free dry weight) for larvae reared in either 0.45-μm filtered seawater or at phytoplankton concentrations (Isoehrysis galbana, clone T-ISO) of 1 × l03, 1 × 104, or 1.8 × 105 cells ml−1. Larvae increased both shell length and biomass at 1 × 104 cells ml−1, although significantly more slowly than at the highest food concentration. Larvae did not significantly increase (p > 0.10) mean shell length in filtered seawater or at a phytoplankton concentration of only 1 × 103 cells ml−1, and in fact lost weight under these conditions. To assess the influence of food limitation on the ability of competent individuals to postpone metamorphosis, larvae were first reared to metamorphic competence on a high food concentration ofI. galbana (1.8 × 105 cells ml−1). When at least 80% of subsampled larvae were competent to metamorphose, as assessed by the numbers of indlviduals metamorphosing in response to elevated K+ concentration in seawater, remaining larvae were transferred either to 0.45-μm filtered seawater or to suspensions of reduced phytoplankton concentration (1 × 103, 1 × 104, or 5 × 104 cells ml−1), or were maintained at 1.8 × 105 cells ml−1. All larvae were monitored daily for metamorphosis. Individuals that metamorphosed in each food treatment were transferred to high ration conditions (1.8 × 105 tells ml−1) for four additional days to monitor postmetamorphic growth. Competent larvae responded to all food-limiting conditions by metamorphosing precociously, typically 1 wk or more before larvae metamorphosed when maintained at the highest food ration. Surprisingly, juveniles reared at full ration grew more slowly if they had spent 2 or 3 d under food-limiting conditions as competent larvae. The data show that a rapid decline in phytoplankton concentration during the larval development ofC. fornicata stimulates metamorphosis, foreshortening the larval dispersal period, and may also reduce the ability of postmetamorphic individuals to grow rapidly even when food concentrations increase.

Effects of larval starvation and delayed metamorphosis on juvenile survival and growth of the tube-dwelling polychaete Hydroides elegans (Haswell)

Abstract Competent larvae of the serpulid polychaete, Hydroides elegans (Haswell), were induced to metamorphose by either 10 −4 M 3-isobutyl 1-methylxanthine (IBMX), adult homogenate, or 30 mM excess K + . Treatment with excess K + had adverse effects ( P P >0.1). Metamorphosis was triggered using IBMX in subsequent studies. Competent larvae were forced to delay metamorphosis for up to 12 days by preventing the formation of biofilm in glass beakers. Juvenile growth was assessed by increases in tube length and dry tissue weight. The larvae remained fully responsive to IBMX while delaying metamorphosis up to 11 days but lost the ability to respond to adult homogenates within only 3 days, suggesting that the two chemicals act at different points in the metamorphic pathway and that only part of the pathway degrades as metamorphosis is delayed. Metamorphic responses were not affected by starvation during the competent phase. Delaying metamorphosis significantly reduced juvenile survival whether the larvae were fed or starved. However, there was no apparent effect of starvation on juvenile growth as juveniles developed from the larvae that were starved while delaying metamorphosis grew as fast as those developed from the larvae that were fed during the delay period. Our results suggest that Hydroides elegans cannot delay metamorphosis without measurable adverse effects on juvenile survival and growth.