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Metamorphosis of Barnacle Nauplii: Effects of Food Variability and a Comparison with Amphibian Models
Ecology
Abstract
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 maximal size appeared to result when food increased during the intermediate portion of the naupliar phase (when the timing of metamorphosis was plastic). Amphibian models adequately describe the effects of variable food on the size and age at metamorphosis to the cyprid, provided that the model specifies an upper limit to size at metamorphosis when food is enhanced prior to fixation of development rate. In contrast to effects on size and age at metamorphosis, cyprids' lipid concentration (lipid per unit body size) only responded to shifts in food that occurred during the sixth instar. This resulted because shifts in food during the sixth instar affected both cyprids' size and lipid content (lipid per cyprid). Earlier shifts in food greatly affected a cyprid's size, but had little effect on lipid content or lipid concentration. Because the size, age, and lipid reserves of cyprids all have fitness implications, the net effects of food variability are complicated and depend on exactly when the variability occurs. Short-term changes in food encountered after the third instar and before the sixth will alter the length of the naupliar period and the size of cyprids. Variability restricted to the sixth instar will not alter the age at metamorphosis, but will affect the cyprid's size, lipid content, and lipid concentration.
... Larval development of marine benthic invertebrates is controlled by a variety of abiotic and biotic factors, including temperature, maternal investment, and food availability (Pechenik 1987;Przeslawski 2004;Marshall and Keough 2006). Although there is some debate as to which factor most affects larval development (Hoegh-Guldberg and Pearse 1995;Hentschel and Emlet 2000;Bos et al. 2007), there is no doubt that food availability is a key regulator of larval development for most planktotrophic species. Higher nutritional content and greater quantities of larval food are linked to faster growth and developmental rates Przeslawski et al. 2008), accelerated metamorphosis (Hentschel and Emlet 2000), and improved juvenile fitness (Phillips 2002). ...
... Although there is some debate as to which factor most affects larval development (Hoegh-Guldberg and Pearse 1995;Hentschel and Emlet 2000;Bos et al. 2007), there is no doubt that food availability is a key regulator of larval development for most planktotrophic species. Higher nutritional content and greater quantities of larval food are linked to faster growth and developmental rates Przeslawski et al. 2008), accelerated metamorphosis (Hentschel and Emlet 2000), and improved juvenile fitness (Phillips 2002). The timing of larval food pulses can also affect later life stages (Hentschel and Emlet 2000;Phillips 2004). ...
... Higher nutritional content and greater quantities of larval food are linked to faster growth and developmental rates Przeslawski et al. 2008), accelerated metamorphosis (Hentschel and Emlet 2000), and improved juvenile fitness (Phillips 2002). The timing of larval food pulses can also affect later life stages (Hentschel and Emlet 2000;Phillips 2004). Such legacies, in which exposure to environmental conditions during early life stages affects later life stages, are receiving increasing attention in ecological studies (Emlet and Sadro 2006;Padilla and Miner 2006;Pechenik 2006;Gimenez 2010). ...
Knowledge of the abiotic and biotic factors that control the development of marine invertebrate larvae is essential for successful laboratory culture, as well as the understanding of the population dynamics of marine organisms. Food availability is a key regulator of larval fitness, and competition for food may arise if larval densities are high. Here we examine the combined effects of food concentration and larval density on the survivorship, growth, developmental rate and lipid stores of the ecologically- important hard clam Mercenaria mercenaria. We hypothesize that the negative effects of food limitation would be exacerbated at high densities due to an interaction between food quantity and larval density. Contrary to our hypothesis, there was no interaction between these factors on survivorship or developmental rate; significantly reduced survivorship was only detected in the highest density treatment at the end of the experiment (Day 15) with no discernable effects of food availability. There were significant interactions between food and density on growth and lipid stores, but these effects were complex and unexpected, with increased growth and decreased lipid stores at moderate densities (500 larvae / L). Potential explanations for our unexpected results include sufficient food availability, adaptation to food availability, direct interference of larvae with each other, and differential survival of larvae with higher natural fitness at high densities. Our results highlight the complex effects of abiotic and biotic factors on larval development. © 2012 Malacological society of australasia " society for the study of molluscan diversity.
... Researchers using amphibians (Hensley 1993, Leips and Travis 1994, Beck 1997, a barnacle (Hentschel and Emlet 2000), a freshwater copepod (Twombly Manuscript 1996), and a mosquito (Bradshaw and Johnson 1995), have varied food rations for larvae over the course of development to examine the degree to which age and size at metamorphosis are plastic or developmentally fixed. Others have varied the timing of periods of starvation during larval development to examine larval survival (Wehrtmann 1991), metamorphic or pupation success, and initial juvenile size (McEdward andQian 2001, Shafiei et al. 2001). ...
... For a variety of taxa, researchers have examined the effects of variable timing of larval food supply on larval size at metamorphosis; in many cases this trait appears quite plastic. When subjected to an initially low food environment and later switched to high food, larvae of amphibians (Hensley 1993, Leips and Travis 1994, Beck 1997, a mosquito (Bradshaw and Johnson 1995), a freshwater copepod (Twombly 1996), and a barnacle (Hentschel and Emlet 2000) were all able to grow much larger compared to control larvae at constant low food, even when these switches occurred late in larval life. Results from the current study are similar; here, when mussel larvae were exposed to greater amounts of food after an initial period of low food, their overall response was a dramatic increase in both size and lipid storage. ...
... Again, the reduction in lipid storage was particularly dramatic for smaller larvae, which may indicate a mobilization of stored reserves to maximize growth before metamorphosis. In contrast, for the barnacle Balanus glandula, Hentschel and Emlet (2000) found greater plasticity in larval size than lipids, and suggested for barnacles that larger size is more important for fitness in a variable environment than higher lipid concentration. ...
For organisms with complex life cycles, larval history is increasingly being found to influence later juvenile or adult performance; however, most experiments maintain manipulations in the larval environment at a constant level. Here, I assess the effects of constant vs. variable larval food availability on the marine mussel Mytilus galloprovincialis. In the laboratory, I raised larvae in four food concentrations: constant high, constant low, initial low switched to high, and initial high switched to low. After settlement, I outplanted juveniles to the field for two weeks. Changes in food availability affected larval size and lipid stores, and covariance between the two. Losses of juveniles were greater, and juvenile growth was lower, for those that had been reared as larvae in constant low food compared to those reared in constant high larval food. For the switched treatments, losses were greater, and growth was lower, for juveniles that had experienced initial low larval food relative to those that had experienced initial high larval food, regardless of average larval size or lipid stores from the different treatments. Thus, the timing of pulses of larval food may impact dynamics of later stages.
... data). By contrast, laboratory experiments with barnacle larvae (West & Costlow 1987, Hentschel & Emlet 2000 have shown that cyprid size responds strongly to food and temperature conditions experienced at the mid to end of the naupliar phase. This could point to mechanisms related to food quantity and quality (Barnes 1956, Moyse 1963, Ianora et al. 2004, Caldwell 2009, not revealed by patterns of chl a, explaining the regional pattern in cyprid size and nutritional traits. ...
... At the scale of shores and locations, we found decoupled (=uncorrelated) responses of body size and nitrogen vs. carbon content (nitrogen and carbon are proxies for proteins and lipids respectively). Decoupled responses can occur under variable conditions (Phillips 2006), from the balance of favourable food conditions during the feeding stages (which impact body size and all reserves) vs. costs of substratum search during the non-feeding stage (which primarily impact lipid and carbon reserves) (Holland & Walker 1975, Lucas et al. 1979, Harms 1987, West & Costlow 1987, Hentschel & Emlet 2000. The consistent positive response of body size and nitrogen content to coastal openness found in the southern region suggests that conditions at open shores favour naupliar growth. ...
In species with complex life cycles, laboratory studies have shown that variations in the traits of settling larvae can affect post-settlement survival and influence recruitment and benthic- pelagic coupling. However, we still know little about the magnitude and spatial scale of natural trait variation. We studied spatial variation in body size and nutritional reserves (carbon, nitrogen and lipids) of settled cyprids of the barnacle Semibalanus balanoides along the coast of West Scotland. We quantified variation among regions (north vs. south: range ~700 km), locations (~50 km), shores (~10 km) and within shores (~10 m). We also evaluated trait responses to gradients in chlorophyll and shore openness and compared swimming vs. settled cyprids in order to infer the likely influence of costs of substratum search on trait variation. Variability between regions was large, with higher trait values (e.g. carbon cyprid⁻¹: 35 to 50% higher) in the north. Most traits correlated negatively with pelagic chlorophyll a (a proxy for larval/juvenile food availability); this counter-gradient pattern suggests an adaptive role of increased reserves, buffering benthic juveniles from low food availability during the critical early post-settlement period. Body size and nitrogen content correlated positively with shore openness; lower than expected carbon content suggest increased costs of substratum search on open shorelines. Higher nitrogen content but lower percent carbon was found in settled vs. swimming larvae, suggesting costs of sub - stratum search at the time of settlement. Overall, we uncovered the spatial scales at which trait variation, shaped by pelagic processes, can affect post-metamorphic survival, recruitment and benthic-pelagic coupling.
... The final attachment of cyprids occurs after the active selection of a microhabitat (Walters et al. 1999). Since cyprids do not feed, the energetic reserves accumulated during the naupliar stages are important, as demonstrated by Hentschel & Emlet (2000). Energy accumulated during the naupliar stages affects the larva's capacity to locate a substratum and to settle and metamorphose successfully (Jarrett & Pechenik 1997, Miron et al. 2000, Jarrett 2003. ...
... Jarrett & Pechenik (1997) have already observed important differences in the physiological quality of barnacle post-larvae from different cohorts. These physiological variations ob-served among cohorts may have resulted from the influence of several factors, such as variability of nutritional conditions during larval ontogeny (Hentschel & Emlet 2000), effects of delayed settlement on cyprid energy content (Lucas et al. 1979) and/or have a genetic basis (recruitment from different geographic populations or larvae produced from genetically different adults within a single population). ...
... Organisms with complex life cycles often exhibit plasticity in the timing of life history switch points, whether the switch point is colony sexual maturation in eusocial insects (holland et al. 2013), anadromy or other ontogenetic niche shifts in fish (Werner and gilliam 1984;Werner 1986;aubin-horth et al. 2009), or metamorphosis in amphibians and insects. metamorphosis, in particular, has been studied across many taxa for nearly a century (Pruthi 1925;adolph 1931), and a wide variety of organisms demonstrate flexible size at, and timing of, metamorphosis (Werner and gilliam 1984;Werner 1986;hentschel and emlet 2000;Peckarsky et al. 2001;Benard 2004;touchon et al. 2013). some of this plasticity in metamorphosis is adaptive, for example, as a response to larval predation risk or pond drying (newman 1992), whereas some may be the non-adaptive consequence of variation in environmental conditions during the larval period (hentschel and emlet 2000;Juliano et al. 2004;touchon et al. 2013). ...
... metamorphosis, in particular, has been studied across many taxa for nearly a century (Pruthi 1925;adolph 1931), and a wide variety of organisms demonstrate flexible size at, and timing of, metamorphosis (Werner and gilliam 1984;Werner 1986;hentschel and emlet 2000;Peckarsky et al. 2001;Benard 2004;touchon et al. 2013). some of this plasticity in metamorphosis is adaptive, for example, as a response to larval predation risk or pond drying (newman 1992), whereas some may be the non-adaptive consequence of variation in environmental conditions during the larval period (hentschel and emlet 2000;Juliano et al. 2004;touchon et al. 2013). ...
Many prey species face trade-offs in the timing of life history switch points like hatching and metamorphosis. Costs associated with transitioning early depend on the biotic and abiotic conditions found in the subsequent life stage. The red-eyed treefrog, Agalychnis callidryas, faces risks from predators in multiple, successive life stages, and can hatch early in response to mortality threats at the egg stage. Here we tested how the consequences of life history plasticity, specifically early hatching in response to terrestrial egg predators, depend on the assemblage of aquatic larval predators. We predicted that diverse predator assemblages would impose lower total predation pressure than the most effective single predator species and might thereby reduce the costs of hatching early. We then conducted a mesocosm experiment where we crossed hatchling phenotype (early vs. normal hatching) with five larval-predator environments (no predators, either waterbugs, dragonflies, or mosquitofish singly, or all three predator species together). The consequences of hatching early varied across predator treatments, and tended to disappear through time in some predation treatments, notably the waterbug and diverse predator assemblages. We demonstrate that the fitness costs of life history plasticity in an early life stage depend critically on the predator community composition in the next stage.
... The embryos and larvae in laboratory culture are at much greater densities than in nature (1), without the usual complement of other plankton and with differing dissolved organic compounds, light, and motion of water. Food, sometimes interacting with temperature, is known to affect the form, size, and organic composition of larvae and the postlarval juveniles subsequently formed (2,3,4,5,6). Absence of predators in cultures can also limit the range of forms because predators affect form or size of some larvae (7). ...
... 18. No single measure fully represents stage of development because larvae develop with different body proportions or size at stage under different conditions (2,3,4,5,6). Some echinoderm larvae divide or bud to produce dwarfed larvae (7). ...
Larvae of marine invertebrates cultured in the laboratory experience conditions that they do not encounter in nature, but development and survival to metamorphic competence can be obtained in such cultures. This protocol emphasizes simple methods suitable for a wide variety of larvae. Culturing larvae requires seawater of adequate quality and temperature within the tolerated range. Beyond that, feeding larvae require appropriate food, but a few kinds of algae and animals are sufficient as food for diverse larvae. Nontoxic materials include glass, many plastics, hot-melt glue, and some solvents, once evaporated. Cleaners that do not leave toxic residues after rinsing include dilute hydrochloric or acetic acid, sodium hypochlorite (commercial bleach), and ethanol. Materials that can leave toxic residues, such as formaldehyde, glutaraldehyde, detergents, and hand lotions, should be avoided, especially with batch cultures that lack continuously renewed water. Reverse filtration can be used to change water gently at varying frequencies, depending on temperature and the kinds of food that are provided. Bacterial growth can be limited by antibiotics, but antibiotics are often unnecessary. Survival and growth are increased by low concentrations of larvae and stirring of large or dense cultures. One method of stirring large numbers of containers is a rack of motor-driven paddles. Most of the methods and materials are inexpensive and portable. If necessary, a room within a few hours of the sea could be temporarily equipped for larval culture.
... The amount of cyprid energy reserves depends on the naupliar feeding history, specifically on algal food quantity and quality. Studies relating barnacle larval development to algal food availability is usually restricted to food quantity (West and Costlow, 1987; Anil and Kurian, 1996; Qiu and Qian, 1997; Hentschel and Emlet, 2000) while factors related to food quality have been insufficiently addressed. Besides energetic factors, attachment of cyprids is significantly controlled by a temporal component, i.e., the age of cyprids. ...
... Earlier studies have demonstrated a linear relationship between food concentration (e.g., S. costatum) and cyprid energy reserves (West and Costlow, 1988; Hentschel and Emlet, 2000). In this study, a similar effect was observed (seeTable 2). ...
Nauplii batch cultures of Balanus amphitrite were reared with four different diatoms (Skeletonema costatum, Thalassiosira pseudonana, Chaetoceros gracilis, silicate-limited C. gracilis) at three different cells concentrations: 1 × 105, 5 × 105, and 1 × 106 cells ml- 1. The cyprid energy reserves were quantified as the ratio of triacylglycerols (TAG) to DNA. Energy reserves of larvae fed on different diatoms at a concentration of 1 × 106 cells ml- 1 were ranked in the order: silicate-limited C. gracilis>C. gracilis>T. pseudonana>S. costatum. There was a significant linear relationship between the TAG content of the diet and cyprid energy reserves. The effect of cyprid energy reserves on metamorphosis to polystyrene surface in the presence and the absence of conspecific settlement factor (SF) was studied after 12, 24, and 48 h of incubation. A strong positive correlation between energy reserves and percent metamorphosis was observed in the absence of SF (r12 h = 0.88, r24 h = 0.82, r48 h = 0.68, P<0.05). A weak positive correlation was observed in the presence of SF (r12 h = 0.43, r24 h = 0.48, r48 h = 0.50, P<0.05). In both treatments, more than 80% of the cyprids with high energy reserves metamorphosed within 24 h. In contrast, a high proportion of cyprids with low energy reserves metamorphosed in response to SF in 24 h. Our results indicate that discriminatory metamorphic behavior of cyprids is closely linked to their TAG/DNA ratio, a proxy for energy reserve. © 2002 Elsevier Science B.V. All rights reserved.
... Plasticity in growth and development rate influences the timing of metamorphosis and subsequent age and size at metamorphosis across a wide range of taxa [e.g. insects (Nylin, Wickman & Wiklund 1989; Bradshaw & Johnson 1995; Blanckenhorn 1998; Gotthard 1998; Lounibos 2001; Danks 2006), crustaceans (Twombly 1996; Hentschel & Emlet 2000), fish (Reznick 1990) and amphibians (Wilbur & Collins 1973; Wilbur 1980; Pfennig, Mabry & Orange 1991; Rowe & Ludwig 1991; Newman 1992; Morey & Reznick 2004; Rudolf & Rodel 2007)]. In general, body size is positively correlated with survival and fecundity, although a larger size often requires additional time for growth, and results in an older age at metamorphosis (Roff 1992; Stearns *Correspondence and present address: Department of Zoology, Oregon State University, 3029 Cordley Hall, Corvallis, OR 97331, USA. ...
... Plasticity in growth and development rate influences the timing of metamorphosis and subsequent age and size at metamorphosis across a wide range of taxa [e.g. insects (Nylin, Wickman & Wiklund 1989; Bradshaw & Johnson 1995; Blanckenhorn 1998; Gotthard 1998; Lounibos 2001; Danks 2006), crustaceans (Twombly 1996; Hentschel & Emlet 2000), fish (Reznick 1990) and amphibians (Wilbur & Collins 1973; Wilbur 1980; Pfennig, Mabry & Orange 1991; Rowe & Ludwig 1991; Newman 1992; Morey & Reznick 2004; Rudolf & Rodel 2007)] . In general, body size is positively correlated with survival and fecundity, although a larger size often requires additional time for growth, and results in an older age at metamorphosis (Roff 1992; Stearns 1992). ...
Summary 1. Phenotypic plasticity may allow an organism to respond to temporally variable opportunities for growth and risks of mortality. However, life-history theory assumes that there are often trade-offs between the benefits afforded by plasticity in one trait and the consequences of that plasticity on other traits that affect fitness. In organisms with a complex life cycle, trade-offs may occur between larval and post-metamorphic traits. 2. Many amphibians metamorphose in temporary ponds, and may accelerate larval development to avoid mortality when a pond desiccates. A younger age at metamorphosis often results in reduced body size, but may also facilitate a trade-off with physiological traits that are linked to fitness in the adult stage. 3. We investigated a potential trade-off between desiccation-driven acceleration of development rate and immune system responsiveness in a species that breeds exclusively in temporary ponds. We exposed Rana sylvatica (wood frog) tadpoles to four possible desiccation regimes and then assayed the cell-mediated immune response to a standardized foreign antigen, phytohaemagglutinin (PHA), injected 3 weeks after metamorphosis. We also quantified total leucocyte numbers from haematological smears to obtain a secondary measure of individual immunological condition. 4. Animals exposed to desiccation had shorter development times, weaker cellular immune system responses to PHA and lower total leucocyte numbers than animals from control groups. Both measures of immune response showed a decrease with increasing severity of the desiccation treatment. 5. It is currently unclear whether the observed depression in immune response is transient or permanent. However, even temporary periods of immune system suppression shortly after meta- morphosis may lead to greater susceptibility to opportunistic pathogens or parasites.
... As a consequence, juveniles originating from old cyprids have lower energy reserves and show depressed growth compared to those of young cyprids (Pechenik et al. 1993; Jarrett and Pechenik 1997; Thiyagarajan et al. 2003). Apart from their age, the quality and quantity of algal food available to nauplii affect the accumulation of energy reserves in cyprids (West and Costlow 1988; Hentschel and Emlet 2000; Thiyagarajan et al. 2002). Generally, juveniles obtained from larvae fed high quality and/or quantity of algal food have higher energy reserves than juveniles obtained from larvae fed low quality and/or quantity. ...
... As a consequence, juveniles originating from old cyprids have lower energy reserves and show depressed growth compared to those of young cyprids (Pechenik et al. 1993;Jarrett and Pechenik 1997;Thiyagarajan et al. 2003). Apart from their age, the quality and quantity of algal food available to nauplii affect the accumulation of energy reserves in cyprids ( West and Costlow 1988;Hentschel and Emlet 2000;Thiyagarajan et al. 2002). Generally, juveniles obtained from larvae fed high quality and/or quantity of algal food have higher energy reserves than juveniles obtained from larvae fed low quality and/or quantity. ...
The energetic cost of metamorphosis in cyprids of the barnacle Balanus amphitrite Darwin was estimated by quantification of lipid, carbohydrate and protein contents. About 38–58% (4–5mJ individual–1) of cypris energy reserves were used during metamorphosis. Lipids accounted for 55–65%, proteins for 34–44% and carbohydrates for <2% of the energy used. Juveniles obtained from larvae fed 106cells ml–1 of Chaetoceros gracilis were bigger (carapace length: 560–616m) and contained more energy (5.560.10mJ juvenile–1) than their counterparts (carapace length: 420–462m; energy content: 2.490.20mJ juvenile–1) obtained from larvae fed 104cells ml–1. At water temperatures of 30C and 24C and food concentrations of 104 and 102cells ml–1 (3:1 mixture of C. gracilis and Isochrysis galbana) as well as under field conditions (26.93.1C and 2.20.8g chlorophylla l–1), juveniles obtained from larvae fed the high food concentration grew faster than juveniles obtained from larvae fed low food concentration until 5days post-metamorphosis. Laboratory experiments revealed a combined effect of early juvenile energy content, temperature and food concentration on growth until 5days post-metamorphosis. After 10days post-metamorphosis, the influence of the early juvenile energy content on growth became negligible. Overall, our results indicate that the energy content at metamorphosis is of critical importance for initial growth of juvenile barnacles and emphasize the dependency of the physiological performance of early juvenile barnacles on the larval exposure to food.
... In all barnacles, the cyprid is a non-feeding larva specialized for settlement, and its survival relies on the amount of nutrients accumulated during the preceding naupliar phase or, if these are also non-feeding, handed over from the egg (Hentschel & Emlet, 2000, Thiyagarajan et al., 2002. This obviously entails that a finite amount of energy is available for accomplishing the entire sequence of the F I G U R E 7 (a) Average distance of antennular step in the wide and close searching behaviors of Wanella milleporae (wide-n = 5, closen = 10, Welch unpaired t-test, p < .001). ...
Symbiosis is increasingly recognized as being an important component in marine systems, and many such relationships are initiated when free-swimming larvae of one partner settle and become sedentary on a host partner. Therefore, several crucial questions emerge such as the larva's mechanism of locating a host, selection of substratum and finally settlement on the surface of its future partner. Here, we investigated these mechanisms by studying how larvae of the fire coral-associated barnacle Wanella milleporae move, settle and establish symbiosis with their host, Millepora tenera. Cyprids of W. milleporae possess a pair of specialized antennules with bell-shaped attachment discs that enable them to explore and settle superficially on the hostile surface of the fire coral. Intriguingly, the stinging polyps of the fire coral remain in their respective pores when the cyprids explore the fire coral surface. Even when cyprids come into contact with the nematocysts on the extended stinging polyps during the exploratory phase, no immobilization effects against the cyprids were observed. The exploratory phase of Wanella cyprids can be divided into a sequence of wide searching (large step length and high walking speed), close searching (small step length and low speed) and inspection behavior, eventually resulting in permanent settlement and metamorphosis. After settlement, xenogeneic interactions occur between the fire coral and the newly metamorphosed juvenile barnacle. This involved tissue necrosis and regeneration in the fire coral host, leading to a callus ring structure around the juvenile barnacle, enhancing survival rate after settlement. The complex exploratory and settlement patterns and interactions documented here represent a breakthrough in coral reef symbiosis studies to show how invertebrates start symbiosis with fire corals.
... Besides ambient flow, suspension feeders are also dependent on the abundance of food particles in their environment to fuel their growth, reproduction, and early development (Hentschel & Emlet, 2000;Anil et al., 2001;Desai & Anil, 2004). Unlike flow, little is known about how food availability generally affects suspension-feeding behavior, although specific examples of particle dependent behavioral shifts have been documented. ...
Barnacles are sessile suspension feeders whose feeding efficiency and behavior is largely determined by the movement of water through their environment. Barnacles expend energy to feed actively in environments with low flow velocity, whereas they may feed passively at higher flow velocities, which is more efficient than active feeding. Many intertidal barnacles have been shown to switch between active and passive feeding modes as water velocities change, but little is known about the behavior of epibiotic species attached to mobile hosts, which are exposed to more consistent feeding currents. To assess the response of epibiotic barnacles to flow, laboratory-reared sea-turtle barnacles, Chelonibia testudinaria (Linnaeus, 1758), were subjected to a wide range of water velocities in both the presence and absence of food particles. Their behaviors were video-recorded and categorized using an automated behavior recognition algorithm compiled in R. Individuals of C. testudinaria only displayed passive feeding behavior, but did not feed at lowest test velocities. This species fed most at flow velocities between 25 cm s–1 and 40 cm s–1 (linear mixed effects model, F = 19.30, P < 0.001), a range that correlates well with the average swimming speed of two common host species, the loggerhead and green sea turtles, on which C. testudinaria resides. Chelonibia testudinaria displayed longer average feeding durations when food particles were absent than when food was abundant (linear mixed effects model, F = 11.76, P = 0.001), a result that is in line with the expectations of optimal foraging theory for suspension-feeding invertebrates. Lack of active feeding in this species may have evolved following the establishment of its epibiotic nature and may make this obligate epibiotic species entirely reliant on its hosts’ movements to provide a feeding current. This is the only barnacle species known to not facultatively switch between active and passive feeding modes.
... Similar effects have been found in the estuarine crab Neohelice granulata Giménez et al., 2004), in this case based on an extension of the larval phase through an additional zoeal stage. Compensatory effects of a prolonged development have been found in early crustacean larvae exposed to inadequate food conditions (Anger & Spindler 1987;Hentschel & Emlet, 2000), and partial compensation has been found under chronic but moderate food limitation at low temperatures (Torres & Giménez 2020). ...
In coastal areas with estuarine influence, exposure to hypo-osmotic conditions may affect larval survival, development and growth. Most knowledge about effects of reduced salinity on coastal organisms is based on keeping individuals under constant conditions in the laboratory. By contrast, little is known about the effects of more realistic situations where organisms are exposed to low salinity over short time scales. Such environmental short-term fluctuations are expected to increase due to climate change. Here, we experimentally evaluated the sublethal effects of both short-term and continuous exposure to moderately reduced salinities (salinity 20 and 25; compared to seawater, salinity 32) in larvae of European lobster Homarus gammarus. Total body dry mass and biochemical composition (measured as: protein and lipid contents) were measured as response variables in Mysis stages I to III. Short-term effects of low salinity were quantified in a group of larvae kept in seawater from hatching until the time of transfer to the test salinities. After ca. 40 % of each moult cycle in seawater (determined in preliminary experiments for Mysis I, II and III), larvae were assigned to a seawater control or reduced salinities lasting for 16 h (i.e. until ca. 50 % of the time spent within the moulting cycle). Effects of continuous exposure to low salinity were quantified when larvae were exposed to the different salinities from hatching, until they reached ca. 50 % of the successive moulting stage. Surprisingly, in the Mysis II and III stages, short-term exposure to low salinity had much stronger effects on accumulation of reserves than the continuous exposure. Such effects were manifested mostly as limited accumulation, or even losses, in the lipid content as compared to reductions in the amount of protein accumulated. The most sensitive stage to exposure to low salinity was the Mysis III; by contrast in Mysis I such effects were relative weak (not always significant). Chronic exposure to low salinity also led to an increase in developmental time especially at the advanced stages. Our results highlight the importance of quantifying effects of environmental fluctuations at different time scales in order to better understand how organisms cope with realistic environmental change in the coastal zones. For H. gammarus, our results suggest that larvae respond adaptively to low salinity by maintaining protein levels at expenses of reductions in lipid accumulation and by extending the developmental time, but the capacity to elicit a fully compensatory response varies ontogenetically.
... Therefore, the growth of tadpoles is affected both by physical factors (e.g., temperature and dissolved oxygen) and by food availability and density of tadpoles (Wilbur and Collins, 1973;McDiarmid and Altig, 1999;Wells, 2007). This pattern has been applied commonly in studies of metamorphosis of amphibians, but it has been very influential in studies of other species as well, including fishes (Reznick, 1990), barnacles (Hentschel and Emlet, 2000), copepods (Twombly, 1996), and insects (Bradshaw and Johnson, 1995;Peckarsky et al., 2001). ...
Little is known about many aspects of the tadpole ecology of Quasipaa verrucospinosa (Bourret, 1937), whereas this species has also been classified as Near Threatened (NT) due to habitat change and degradation, loss of forest and stream habitats and overexploitation. We conducted experiments in the field and collected tadpole data to estimate survival rates, growth rates, and age at metamorphosis. The average number of tadpoles per clutch was 518, the average survival ratio at the final stage of metamorphosis was 80%, and the total time to metamorphosis averaged 55.8 days. Multiple regression results for possible effects of water temperature, dissolved oxygen, and pH values on survival rates and the total time of tadpole metamorphosis were significant among localities. Water temperature and dissolved oxygen, but not pH values, were negatively associated with the survival ratio and metamorphosis time of tadpoles. At the beginning stage of metamorphosis (41-42), tadpoles had an average body weight of 2.7 g, a snout-vent length (SVL) of 24.8 mm, a tail length of 40.5 mm, and a total length of 65.3 mm. The process of metamorphosis is completed in stage 46, at which juvenile frogs had a mean body weight of 2.3 g and a mean SVL of 25.8 mm. We used a two-way multivariate analysis of variance to examine the effects of year and site factors on the variance in morphological measurements and body weightes of tadpoles. This analysis revealed that body sizes of tadpoles varied significantly among years, sites, and by site-year interaction. Water temperature and dissolved oxygen have major impacts on rates of growth, timing of metamorphosis, and body size of tadpoles at metamorphosis.
... Ces travaux, de nombreuses fois cités par la suite, qui suggéraient l'importance du comportement des larves en voie de sédentarisation dans la dynamique de recrutement, m'ont poussé à développer des approches 'éco-étho-physiologiques' pour comprendre les mécanismes de sélection de l'habitat par les larves d'invertébrés. Pechenik et al. 1998, Hentschel & Emlet 2000. Plus précisément, la capacité de la larve à localiser un substrat, à se fixer puis à se métamorphoser découle de l'énergie stockée principalement sous forme de lipides (Jarret & Pechenik 1997, Miron et al. 2000, Jarret 2003. ...
HABILITATION À DIRIGER DES RECHERCHES : Fonctionnement des écosystèmes benthiques soumis aux pressions anthropiques à différentes échelles d'espace et de temps
... Lipid physiological indices for invertebrate larvae can be determined by coloration of neutral lipids with the dye Nile red, followed by quantification using image analysis to calculate lipid surface relative to total larval surface (Castell and Mann, 1994;Hentschel and Emlet, 2000;Kheder et al., 2010). In cypris larvae, the transparent carapace makes it easy to visualize the conspicuous lipid droplets (triacylglycerol, TAG), the main larval energetic reserves (Tremblay et al., 2007). ...
Marine invertebrates inhabiting low-latitude shores are exposed to both extremely hot and highly variable conditions. Further changes in habitat temperature may pose a risk to these populations. In this study, we examined the early life stage response of foundation species from subtropical and tropical latitudes to changes in the thermal habitat. We manipulated the color of settling surfaces for barnacle species that occupy the same ecological niche, Chthamalus bisinuatus (southeastern coast of Brazil), and Chthamalus proteus (northwestern coast of Panama). Using an in situ experimental approach, we assessed: 1) the combined effects of temperature and other abiotic parameters, and 2) the significance of larval and early juvenile traits in determining post-settlement performance for the first three days of benthic life. We found that the biological outcomes differed for the two species, according to the local thermal regime experienced. C. bisinuatus juveniles responded positively to higher temperatures, through a positive interaction between larval energetic condition, post-metamorphic size and temperature on their initial growth. Conversely, C. proteus juveniles grew slower at higher temperatures, although a positive effect of size at settlement was found. Continuous air-and sea-surface temperature measurements revealed that the tropical chthamalids experienced temperatures ≈6 °C higher than their subtropical congeners, as well as harsher thermal conditions during aerial exposure. This suggests that manipulated temperatures likely exceeded the tolerance of the Caribbean population, already living on the edge of their thermal threshold. Our findings contribute to the understanding of the factors underpinning the critical post-settlement events that drive patterns of abundance and distribution of barnacles in low-latitude systems.
... While we speculate here on potential adaptive explanations for the lack of an effect of maternal provisioning on planktonic larval survival, it is important to recognize that this lack of effect could also be the result of a physiological constraint. We did not discriminate here the effects of food supply on different naupliar stages, but other studies on the same species and in the same area suggest that early stages may be more tolerant to food shortage than late-stage nauplii (Freuchet et al., 2015;Barbosa et al., 2016), in accordance to the results obtained by Hentschel & Emlet (2000) on Balanus glandula Darwin. Early nauplii of Chthamalus bisinuatus may endure for up to 5 days without any exogenous food sources in the laboratory (Freuchet et al., 2015), suggesting that larvae released in oligotrophic waters may still survive and reach the cyprid stage if oceanographic conditions improve later on. ...
Understanding the effects of maternal and pelagic resource allocation on larval traits is essential to better understand population dynamics of marine benthic invertebrates. We tested how different levels of food supply to adult barnacles and their feeding larvae (nauplii) might alter survival to the settling cyprid larval stage and cyprid quality. Median development time did not vary, except when both parents and larvae were given a low food supply, which delayed the time to metamorphosis by over 40%. Survival to the cyprid stage was only affected by larval feeding, which doubled in better-fed nauplii. In contrast, cyprid size showed a more complex response, prone to additive effects of maternal and larval provisioning. Moreover, the resulting size-range observed for experimental cyprids (spanning over 70% of the minimum cyprid size) mirrored the variation found in the coastal plankton, suggesting that food supply may exert similar effects in nature. Given that barnacles nearly saturate available habitat under favorable conditions, maternal allocation resulting in enhanced late-stage larval quality may be adaptive since competition for available settling space is likely intense. On the other side, severe resource limitation through embryogenesis and larval development may impose delayed metamorphosis and thus enhanced potential for transport and the colonization of marginal habitats, where intraspecific competition may be lower and larval quality less critical.
... Other things being equal or homogeneous, high phytoplankton availability in coastal waters during larval development can therefore lead to higher recruitment (e.g. Olson & Olson 1989, Cushing 1990, Menge 2000 and high larval physiological quality that should improve post-settlement survival (Jarrett & Pechenik 1997, Hentschel & Emlet 2000, Phillips 2002) as well as overall juvenile condition (Bertness et al. 1991, Menge et al. 1997, Sanford & Menge 2001. All of these factors may result in the maintenance of genetic diversity from the larval pool. ...
Understanding the multiplicity of processes producing genetic patterns in natural populations can shed light on the ecology and evolution of species, and help guide effective management and conservation strategies. Here we investigated the role of environmental, demographic, and geographic factors in shaping the spatial patterns of genetic diversity and differentiation of the intertidal barnacle Notochthamalus scabrosus along the central-northern coast of Chile (28−34° S). We analyzed genetic data from 7 microsatellite loci genotyped for 300 individuals sampled from 10 sites and combined this information with 8 site-specific environmental (4), demographic (2), and geographic (2) variables using least squares linear regressions, generalized linear models, and matrix regression analyses. We found a strong association between the spatially structured genetic diversity of N. scabrosus and patterns of temporal variability in chlorophyll a, and among-site differences in seawater temperature and adult abundance. Our results illustrate that population size, partly driven by recruitment success, can leave a signal on genetic structure of this highly dispersive marine species. The significant effect of temperature and chlorophyll a stresses that local adaptation may be key to understanding the spatial genetic structure of our model species. Hence, the results of this work represent an advance towards understanding the usually complex causal relationships between environmental variables, gene flow, and genetic diversity patterns of coastal populations.
... Earlier studies have shown that larval settlement can be affected by a variety of endogenous factors, including proteins, pheromones, hormones, and neurotransmitters (Pawlik 1992;Yamamoto et al. 1998;Hentschel and Emlet 2000;Fusetani 2004;Qian et al. 2010). More recent transcriptomics and proteomics profiling analyses indicated that several crucial pathways, including Wnt, MAPK, and NO pathways, were involved in the settlement and metamorphosis of B. neritina (Zhang et al. 2010a, b;Wong et al. 2012;Wong et al. 2014). ...
Larval attachment and metamorphosis, also collectively known as settlement, plays an important role in the life history of marine invertebrates with biphasic life cycle. Bugula neritina can settle on any substrate without substrate selection. This complex transformation usually involves an active selection process, while the larval decision to settle is regulated by both exogenous and endogenous factors. This study focuses on the involvement of arginine kinase (AK), an important enzyme that regulates energy metabolism in marine invertebrates, during larval settlement of the bryozoan Bugula neritina. We reveal that AK was highly expressed in the swimming larvae of B. neritina, while its expression was down-regulated post-attachment. When treated with AK inhibitors, the larval settlement rate was significantly decreased. In addition, the immunostaining results indicated that AK was mainly localized to the neuro-muscular cord in swimming larvae. Overall, our results suggest the involvement of AK in regulating larval settlement of B. neritina.
... Improved feeding opportunities afforded by DVM may be crucial to the nauplii of some barnacle species. In another balanid barnacle, greater food availability has been demonstrated to increase the size and lipid reserves of cyprids (Hentschel and Emlet 2000) which in turn metamorphose into juveniles with greater energy stores, faster growth (Thiyagarajan et al. 2003) and higher survival (Thiyagarajan et al. 2005). Additionally, because increased temperature has been shown to accelerate development in both species of chthamalid barnacles that occur in the study area (Venegas et al. 2000), nightly migration into shallower water (which is generally warmer in central Chile where some degree of thermal stratification is common) should shorten the time to competency while minimizing mortality due to visual predators. ...
... Improved feeding opportunities afforded by DVM may be crucial to the nauplii of some barnacle species. In another balanid barnacle, greater food availability has been demonstrated to increase the size and lipid reserves of cyprids (Hentschel and Emlet 2000) which in turn metamorphose into juveniles with greater energy stores, faster growth (Thiyagarajan et al. 2003) and higher survival (Thiyagarajan et al. 2005). Additionally, because increased temperature has been shown to accelerate development in both species of chthamalid barnacles that occur in the study area (Venegas et al. 2000), nightly migration into shallower water (which is generally warmer in central Chile where some degree of thermal stratification is common) should shorten the time to competency while minimizing mortality due to visual predators. ...
The vertical and horizontal distribution of larval stages of the most common intertidal barnacle and mussel species were characterized in near-shore waters of central Chile. Paired day/night cruises were conducted on four spring-summer dates between December 2007 and November 2008, under contrasting wind, wave height, and near-shore stratification conditions. Regardless of variability in oceanographic conditions, the highest abundances of barnacle and mussel larvae were found within 1500 m from shore. Non-uniform vertical distributions were observed for chthamalids, balanids and mussel larvae, but patterns of diel variability differed among them. Chthamalid and balanid nauplii, as well as balanid cyprids were more abundant in the upper 20 m of the water column, while the density of chthamalid cyprids was highest near the bottom. Mussel larvae were only found within 20 m of the surface. The Mean Depth Distribution (MDD) of all nauplii (balanid and chthamalid) and chthamalid cyprids was deeper during day than night, suggesting typical diel vertical migration (DVM), but this difference was statistically significant only for nauplii. Mussels did not show diel differences in vertical distribution. The amplitude of DVM, measured as the difference between daytime and nighttime MDD, decreased with increasing wave height in chthamalid and balanid nauplii, but not with along-shore wind stress. Chthamalid nauplii, and to a lesser extent, balanid nauplii were found below the pycnocline during the day and above at night, suggesting that DVM involves daily crossing of this density barrier. In contrast, cyprids of all barnacle species were distributed across the pycnocline with no clear pattern. The results suggest that barnacle and bivalve larvae may exhibit a variety of behavioral responses to position themselves in the water column despite typically turbulent near-shore waters, and that such behavior varies between species and through ontogeny within species. Moreover, some stages of barnacle larvae perform DVM, but the amplitude decreased with increasing wave height – which may be either a plastic response to environmental cues or merely turbulent mixing impeding the ability of larvae to perform vertical migration.
... Yet, an important aspect of variability has received considerably less attention: that resource levels can vary during an individual's development. Even though there is substantial evidence that variation in food levels during development can affect age and size at maturity (e.g., Leips and Travis 1994;Hentschel and Emlet 2000), we know little about how this variation affects reproductive success and adult survival. ...
Despite a large body of knowledge about the evolution of life histories, we know little about how variable food availability during an individual's development affects its life history. We measured the effects of manipulating food levels during early and late larval development of the mosquito Aedes aegypti on its growth rate, life history and reproductive success. Switching from low to high food led to compensatory growth: individuals grew more rapidly during late larval development and emerged at a size close to that of mosquitoes consistently reared at high food. However, switching to high food had very little effect on longevity, and fecundity and reproductive success were considerably lower than in consistently well-fed mosquitoes. Changing from high to low food led to adults with similar size as in consistently badly nourished mosquitoes, but even lower fecundity and reproductive success. A rapid response of growth to changing resources can thus have unexpected effects in later life and in lifetime reproductive success. More generally, our study emphasizes the importance of varying developmental conditions for the evolutionary pressures underlying life-history evolution.
... They develop through a series of pelagic larval feeding stages, the nauplius, followed by a nonfeeding larval stage, the cyprid, which settles and metamorphoses. Food conditions experienced by nauplius stages determine the amount of reserves available to the cyprids to search for an appropriate settlement site and undergo metamorphosis (West & Costlow 1987, Hentschel & Emlet 2000, Thiyagarajan et al. 2003a. Metamorphosis requires a considerable amount of total available reserves (e.g. ...
One of the central issues in ecology is the identification of processes affecting the population structure and dynamics of species with complex life cycles. In such species, variation in both the number of larvae that enter a population and their phenotype are important drivers of survival and growth after metamorphosis. Larval experience can have strong effects on key postmetamorphic traits, but the temporal scale of such 'trait-mediated effects' may be short, and their magnitude may depend on the environment experienced after metamorphosis. We used an intertidal barnacle to study the long-term consequences of trait-mediated effects under different postmetamorphic conditions by manipulating larval food concentration and monitoring patterns of survival and growth in juveniles at 2 intertidal levels over a 5 mo period. In 2 replicated experiments, higher food levels resulted in increased body size, mass and reserves (measured from elemental composition) in the settling larval stage and increased body size of newly metamorphosed juveniles. In Expt 1, high food concentration reduced juvenile mortality at low intertidal levels, while on the upper intertidal, mortality was high for all larval food concentrations. By contrast, in Expt 2, low larval food concentration decreased juvenile survival at both shore levels. When present, effects were established early (Weeks 1 or 2) and persisted for over 10 wk in Expt 1 and 22 wk in Expt 2. Interactive effects of the larval and juvenile environments can have important implications for population size: trait-mediated effects may persist for long periods, helping to explain patterns of adult abundance.
... As a consequence, juveniles originating from old cyprids have lower energy reserves and show depressed growth compared to those of young cyprids (Pechenik et al. 1993;Jarrett and Pechenik 1997;Thiyagarajan et al. 2003). Apart from their age, the quality and quantity of algal food available to nauplii affect the accumulation of energy reserves in cyprids (West and Costlow 1988;Hentschel and Emlet 2000;Thiyagarajan et al. 2002). Generally, juveniles obtained from larvae fed high quality and/or quantity of algal food have higher energy reserves than juveniles obtained from larvae fed low quality and/or quantity. ...
... While the size and complexity of appendages can affect drag acting on passively sinking larvae (Emlet 1983), appendages with increased surface area are also more effective during swimming behaviour and may counteract the increased sinking velocities of larger individuals (Chia et al. 1984). When combined with their lower densities, older nauplii may be better able to maintain position in the water column, relative to available food supplies, particularly in later stages, where energy intake is important for lipid storage in advance of metamorphosis to the non-feeding cyprid stage (Hentschel and Emlet 2000). This may also promote increased transport and more substantial dispersal away from adult populations during these stages. ...
The installation of marine renewable energy devices (MREDs) is progressing rapidly along many coastlines. It has been suggested that MRED arrays could provide stepping-stones for larval dispersal, mediating species range expansions or invasions. As common members of hard-substrate fouling communities and likely colonisers of MREDs, the larval dispersal processes of barnacles (Cirripedia: Thoracia) in the Firth of Lorn (Scotland) are assessed at scales ranging from mm to 10s – 100s km. At the scale of the organism itself, significant differences in larval mass densities and sinking velocities were observed between species of cirripedes, suggesting that larval physiology and morphology play an important role in water column vertical positioning. The importance of vertical positioning to horizontal transport and dispersal of larvae was identified in field surveys of the horizontal and vertical distributions of cirripede larvae, which revealed the interplay of wind-driven and tidally-oscillating currents in determining transport distances. Numerical simulations of larval dispersal based on a threedimensional hydrodynamic model then demonstrated that larvae with shallower abundance distributions often experienced greater horizontal transport, but that net dispersal distances were often greater for larvae deeper in the water column. Overall, simulated transport and dispersal distances were greatest for particles released at habitats further from the coast, such as MREDs, suggesting that the connectivity of these adult populations may be enhanced.
Together, larval morphology, vertical positioning, and the coastal proximity of adult habitat could serve as useful indicators of larvae capable of reaching nearby newly installed offshore structures. For locations designated for MRED development in the Firth of Lorn, it is suggested that species with dispersal abilities similar to the cirripedes in this study could feasibly use these structures as stepping-stones for dispersal and range expansion, which could have important consequences when fouling communities are comprised of commercially important or invasive species.
... The larval settlement stage of barnacles, the cyprid, does not feed but instead acquires the energy reserves needed to power the search for suitable substratum from its earlier feeding stages (nauplius I-VI) (Lucas et al. 1979, Walker et al. 1987, Thiyagarajan et al. 2002. Consequently, the search period is finite, but its maximum duration is difficult to predict (Hentschel and Emlet 2000). For some species it is known that the cyprid stage can persist for as long as 3-4 wks (Lucas et al. 1979). ...
The barnacle, Chelonibia testudinaria (Linnaeus, 1758), is reported to associate with nearly every species of sea turtle and is particularly common on loggerheads, Caretta caretta (Linnaeus, 1758), with symptoms of Debilitated Turtle Syndrome (DTS). Here, we test recruitment rates of C. testudinaria on various natural and artificial substrata, including carapace from healthy and debilitated loggerheads. In addition, the sizes of individual barnacles were followed through time to estimate early growth rates and to provide attachment duration estimates. Floating racks holding replicate panels of four treatments (DTS turtle carapace scutes, healthy turtle carapace scutes, Plexiglas®, and slate tile) were placed at four independent sites in Charleston County, South Carolina. Panels were monitored for 34–54 d. Our findings indicate that C. testudinaria larvae recruit and grow at significantly higher rates along the open shore vs protected areas, but do not recruit differentially to the four substratum types. Individual barnacle growth was highly variable within and between sites and substratum types; the mean growth rate was 4.28 mm d−1 (95% CI: 3.42–5.14 mm d−1). However, due to the high variability in growth, this value cannot serve as a fine-scale indicator for attachment duration. Further experiments of substratum selection and long-term survival are needed to fully clarify the nature of the barnacle/turtle association.
... Like most thoracican barnacles, B. glandula hatches as a nonfeeding nauplius and develops through five other feeding naupliar instars. As in other nauplii, there is variation in structures and size at a given stage (Branscomb & Vedder 1982;Brown & Roughgarden 1985;Hentschel & Emlet 2000). However, we know of no studies of the extent to which naupliar structures continue to develop in brooded nauplii after they become capable of hatching and swimming or of the effect of prolonged brooding on the morphology of later naupliar stages after hatching. ...
... Genotype specific mortality in barnacle species may result from selective effects preceding or following metamorphosis. The term 'latent effects' has been employed to describe selective pressures that act on the planktonic condition of barnacle nauplii in a way that influences post-settlement fitness (Jarrett & Pechenik 1997, Hentschel & Emlet 2000, Pechenik 2006). ...
Balancing selection has been invoked to explain the apparent maintenance of polymorphisms at the mannose-6-phosphate isomerase (Mpi) and glucose-6-phosphate isomerase (Gpi) loci in a diverse array of organisms. However, in many cases the agents of selective stress and the gram size of environmental heterogeneity necessary to preserve genetic variation remain uncertain. In the barnacle Sennbalanus balanoides, differing selection regimes have been proposed across the species' range. To test whether or not fitness differences segregate with Mpi and Gpi polymorphisms near the southern range limit, barnacles from Narragansett Bay, Rhode Island, were subjected to physiological challenges in the laboratory. Survivorship was measured in barnacles exposed to an orthogonal combination of salinity, thermal and dietary stresses. Cirral length and genotype frequency shifts at Mpi and Gpi were assessed in low salinity treatments. Mortality from thermal stress was greatly enhanced under low salinity. Across all low salinity treatments there was a nonsignificant trend of decreased fitness associated with the Mpi-SS genotype. Cirral length variation was significantly correlated with Mpi genotypes in a pattern consistent with survivorship data.
... The physiological state, or condition, of marine organisms appears to vary greatly through space and time due to variability in environmental conditions such as temperature and food supply (McCormick & Molony 1993, Kerrigan 1996, Hentschel & Emlet 2000, and this variation may have significant demographic consequences. Elevated nutritional condition, for example, has positive implications for survival of seabirds (Perez et al. 2006), growth in barnacles (Thiyagarajan et al. 2005), and swimming endurance (Stobutzki 1997), offspring quality (McCormick 2003), and sur-vival (Booth & Hixon 1999) in fishes. ...
Variation in individual performance and condition of marine organisms can influence larval supply and the outcome of post-settlement processes. The broad applicability of these patterns among systems and under different environmental conditions, however, remains relatively unknown. We determined whether nutritional condition would affect the survival of recently settled recruits of a temperate reef fish, the blackeye goby, and whether refuge availability would modify the importance of condition. Recruits were fed high or low food rations in the laboratory for 15 d, after which pairs of high-and low-ration fish were marked and placed on standardized plots of rock rubble in the field. Plots were monitored daily to determine mortality over 12 d. To examine the combined effects of condition and refuge availability, pairs of fish were placed on plots of high, medium, or low amounts of refuge. Laboratory experiments examined the effect of condition on burst swimming speed to elucidate the mechanisms underlying the observed patterns of survival. On standardized plots, fish fed low rations experienced higher mortality than fish fed high rations. When refuge was manipulated, low-ration fish experienced higher mortality than high-ration fish at higher levels of refuge. Surprisingly, higher mortality was observed for high-ration fish on low-refuge plots, possibly due to differences in risk-prone behavior. A reduction in the overall probability of mortality resulted in an unanticipated dampening of the importance of condition for survival. Our results indicate that the ecology of individuals, mediated by environmental conditions, is an important constituent in the population demography of reef fishes.
... Field studies have shown that abundance of phytoplankton and POM can regulate the growth, overall size and distribution of adult filter feeders in soft and hard-bottom habitats (Page & Hubbard 1987, Grebmeier et al. 1988, Duggins et al. 1989, Smaal & Van Stralen 1990, Bertness et al. 1991, Leichter et al. 1998, Sanford & Menge 2000. In addition, higher phytoplankton concentrations can lead to increased development and survival rates of larvae (Barnes 1956, Hentschel & Emlet 2000. However, except for research conducted in estuarine and fjord systems (e.g. ...
Phytoplankton and particulate organic matter constitute the primary food source for adult filter-feeders, as well as for larval stages of many benthic and pelagic organisms. The structure and dynamics of nearshore benthic communities may be associated with variation in nearshore primary production. However, we know little about the scales of variability in phytoplankton in nearshore waters along open coasts, or about their causes. To characterize spatial and temporal patterns of chl a concentration, we conducted 2.5 yr of daily, shore-based monitoring at 3 sites separated by 10s of km within an upwelling region in central Chile. We found that: (1) peaks in chl a concentration were typically short-lived, persisting no longer than 4 d, (2) blooms occurred in spring to early summer months at all sites, but also during autumn months at 1 site (Las Cruces), and (3) the intensity and frequency of blooms were consistently different among sites; highest concentrations were at Las Cruces, lower at El Quisco, and the lowest at Quintay. Analyses of wind data and surface temperature, and inspection of Advanced Very High Resolution Radiometer (AVHRR) satellite images, suggested that among-site differences were due, at least in part, to alongshore variation in upwelling intensity and the formation of warm-water pockets or upwelling shadows in sections of the coast, such as Las Cruces. In contrast to the spatial pattern described offshore and over larger spatial scales, chl a concentrations were significantly lower at the coldest site, Quintay, located at the core of an upwelling center (Pta. Curaumilla), than at the warmer site of Las Cruces, which lies downstream from upwelling. Day-to-day variation in chl a levels during spring at Las Cruces seems related to the alongshore intrusion of waters upwelled upstream. Overall, the pattern observed at our 3 sites, together with previous studies at other upwelling systems, suggests that sections of the coast around 15 to 20 km downstream (equatorward) from upwelling centers could exhibit consistently higher phytoplankton concentrations than sites located in front of upwelling centers, generating a source-sink type of geographic pattern of nearshore nutrients and phytoplankton along the coast.
... I calculated proportional area of lipid content as the ratio of lipid area: larval area for each individual, and means were calculated for each larval food concentration. These methods have been recently validated for barnacle larvae by Hentschel and Emlet (2000), who found that lipid content determined using image analysis of Nile Red stained larvae correlated well with lipid content determined using biochemical extraction methods. ...
The potential for long-lasting effects of larval experience on early juvenile stages is growing in recognition as an important aspect of the ecology of organisms with complex life cycles. For marine species, most studies of recruitment have focused on the numbers of settlers that arrive to a site, largely ignoring the potential variability in larval condition or quality and how such variability may influence the likelihood of recruitment success. In this study, I investigated the effect of larval nutritional history on early juvenile performance, and whether these effects are mediated by conditions in the juvenile habitat for the marine mussel Mytilus galloprovincialis. I raised larvae in the laboratory under different food concentrations. Larvae raised with the highest food concentrations were significantly larger in size at metamorphosis and had higher proportional lipid content at metamorphosis than those from lower food concentrations. Half of the newly metamor- phosed juveniles were outplanted into intertidal and subtidal habitats for 2 wk. The other half were maintained in the laboratory at two different juvenile rations for up to 20 d. Juveniles raised with high larval food had higher juvenile growth rates and attained larger juvenile sizes than those from lower larval food in all cases. There was a significant positive relationship between size at metamorphosis and juvenile growth for juveniles maintained in the laboratory. Early juvenile growth rates did not change over time (between 10 and 20 d post-metamorphosis). Juveniles raised in higher juvenile rations had elevated growth rates and attained larger final sizes after 20 d than juveniles from low juvenile rations across all sizes at metamorphosis. For juveniles in the field, there was no effect of tidal height on growth for 2 wk post-metamorphosis. Field conditions were more favorable than laboratory conditions for juvenile growth, yet even these more favorable conditions did not compensate for the effects of larval nutritional history on early juvenile growth. Losses of juveniles from both the field and the laboratory were higher for those that had been raised in lower larval food conditions than for those that had been raised in higher larval
... Juvenile energy has not been quantitatively modelled to assess potential influences on life-history evolution for marine invertebrates but has been qualitatively considered multiple times (e.g. Strathmann, 1977; Eckert, 1995; Hentschel, 1999; Hentschel and Emlet, 2000; Phillips, 2002). ...
Life-history models to investigate the larva-juvenile transition in benthic invertebrates have primarily been static models that focus on the larval portion of the process. Here we develop a dynamic optimization model to quantify the roles of (1) habitat quality, (2) habitat distribution and (3) maternal investment in the successful settlement of hypothetical lecithotrophic marine invertebrate larvae. In particular, we focused on the roles of these variables in the proportion of larvae settling successfully, their post-settlement state, and their post-settlement fitness (state plus habitat settled in). We evaluated the fitness consequences of larvae making one of two decisions: (1) searching for 'better habitats' and thus staying pelagic in order to settle at a later time, or (2) settling to the benthos and acquiring some measure of future fitness, pending successful settlement. Our results suggest that habitat distributions have a substantial impact on the proportion and state of larvae that settle to specific habitat qualities (and thus fitness) but little impact on the total number of larvae that settle. Maternal investment had the strongest positive effect on post-settlement state where more maternal investment generally resulted in more energy-rich settlers. Increases in maternal investment above the initial minimum resulted in diminishing returns in terms of successful larval settlement or the distribution of settlers in better habitat qualities. We discuss our results in light of the current debate on marine reserve designs.
... Larval quality is controlled by many factors, including maternal investment, genetics, and environmental conditions. Viability of early stage larvae is often directly related to the energetic content and size of eggs (Marshall & Keough 2007), whereas the fitness of later larval stages is often mediated by quantity and quality of food (Hentschel & Emlet 2000, Wacker & von Elert 2002, Bos et al. 2007). In addition to food composition, other environmental conditions regulate invertebrate larval development, particularly temperature (Hoegh-Guldberg & Pearse 1995, O'Connor et al. 2007. ...
Larval size and developmental rate can vary tremendously within and among cohorts because of genetics, environment, and maternal investment. This natural variation in larvae may have effects that span multiple life stages. Here we investigate the effects of larval size and developmental stage on the subsequent life stages of the commercially and ecologically important clam Mercenaria mercenaria. Fifteen days after fertilization, we divided larvae into two groups based on their developmental stage (umbonal or pediveliger) and recorded survival, size, and developmental stage of individuals over the next 4 months. Results revealed that after four months larvae that had only reached the umbonal stage by Day 15 were significantly smaller than those that had reached the pediveliger stage. These smaller and less developed larvae were less successful than the larger and more developed larvae across late larval and juvenile stages. In particular, smaller and less developed larvae were less likely to metamorphose, required more time to metamorphosis, and had lower survival and growth rates. These results suggest that natural variation in larval size and developmental rate can affect recruitment in a variety of ways: (1) Increased time to metamorphosis may increase the cost to larvae via predation or exposure to environmental stress, (2) Decreased proportion of larvae able to metamorphose may directly reduce the number of settlers, and (3) Decreased growth and survival rates for juveniles may reduce the number of new recruits. We also discuss the persistence of natural variation in larval size and developmental rate in light of the observed negative effects associated with smaller and less-developed larvae.
... Naupliar cultures raised using di¡erent food concentrations have been reported to a¡ect the amount of energy reserves in cyprids (West & Costlow, 1987;Hentschel & Emlet, 2000). Cyprids like other invertebrate larvae derive their energy from stored lipids. ...
The influence of food concentrations (0.5, 1 and 2×105 cells ml−1) and temperatures (20 and 30°C) on the survival, development, organic carbon and nitrogen content of Balanus
albicostatus
larvae was evaluated. The effect of food concentration on the subsequent ageing and metamorphosis of cypris larva was also determined. At lower food concentration and temperature, naupliar development duration was prolonged and the rate of metamorphosis of nauplius to cyprid was low. The rearing food concentration affected organic carbon and nitrogen content of the nauplii, which was also reflected in non-feeding cyprids. A decrease in the carbon content was observed with cyprid ageing at 5°C. Metamorphosis was higher in 8-d aged cyprids when compared to 2-d aged cyprids, and was positively influenced by the natural biofilm.
... In free-living organisms, larval size often indicates quality; big larvae grew in better conditions or were better adapted to the prevailing conditions (Hentschel and Emlet 2000, Morey and Reznick 2000, Phillips 2002, Altwegg and Reyer 2003, De Block and Stoks 2005. Having acquired more resources, large larvae have more energy to allocate to the various functions necessary for survival and reproduction in the adult habitat (Van Noordwijk and de Jong 1986, Reznick et al. 2000). ...
In organisms with complex life cycles, fitness often increases with body size at the transition from larva to adult. The translation of larval size into fitness, however, can depend on the source of size variation, with size, per se, not always increasing adult success. In parasitic worms, many factors influence larval growth, but little is known about the consequences of this growth variation. We examined how the size of the tapeworm Schistocephalus solidus in its copepod first intermediate host affects infection success and growth in the stickleback second host. Moreover, we assessed whether the conspicuous growth variation caused by copepod size is fitness-relevant. Using larvae of the same age, we found that larger worms had a substantially higher infection probability and they tended to still be slightly larger after several months of growth in fish. However, big larvae from bigger copepods did not have higher fitness, suggesting that being large relative to the host, but not necessarily large in general, is important. These findings clarify some aspects of the life history strategy of S. solidus (e.g. why there is a flat ontogenetic reaction norm across copepod stages), but also raise questions (e.g. why growth costs have been hard to document). More generally, our results indicate that larval size can correlate with fitness in helminths, but that not all size variation is predictive of success in the next host.
... In accordance with previous investigations, di¡erent food concentration used in larval cultures clearly a¡ected the amount of energy reserve in cyprids (West & Costlow, 1988;Hentschel & Emlet, 2000). At algal food concentrations below 10 4 cells ml 71 , nauplii did not metamorphose into cyprids (data not shown). ...
The nauplii of Balanus amphitrite (Cirripedia: Thoracica) were cultured on a daily diet of Chaetoceros gracilis at different concentrations. Both young (zero-day old) and aged (six-day old) cyprids were subject to attachment assays, followed by studies of juvenile growth and survival for two weeks under laboratory conditions. The TAG/DNA ratio of cyprid increased in the following order of food concentrations: 106 > 104 > 104 cells ml-1. More than 70% of cyprids metamorphosed in the presence of conspecific settlement factor, irrespective of their TAG/DNA ratio. The juvenile growth and survival in young cyprids surpassed that of the aged cyprids. The TAG/DNA ratio had no significant effect on juvenile growth and survival in both young and aged cyprids. The negative effect of delayed metamorphosis on juvenile growth and survival appeared to be independent of the TAG/DNA ratio.
... Intertidal barnacles as conspicuous, widely distributed, and ecologically important species have served to study the eVects of environmental factors, e.g., temperature, salinity, food type and concentration, light (e.g., Crisp and Ritz 1973; Harms 1984; Holm 1990; Konya and Miki 1994; Anil et al. 1995 Anil et al. , 2001 Anil and Kurian 1996; Qian 1997, 1999; Hentschel and Emlet 2000; Thiyagarajan et al. 2002a; Nasrolahi et al. 2007), and more recently global warming and ocean acidiWcation (Findlay et al. 2008; Hung et al. 2008; Findlay et al. 2009; McDonald et al. 2009; Wong et al., in press) on larval development and settlement success. Much of this progress on what is frequently considered the most sensitive life history phase is facilitated because barnacle larvae can be easily reared under controlled conditions (Thiyagarajan et al. 2000). ...
The fate of key species, such as the barnacle Amphibalanus improvisus, in the course of global change is of particular interest since any change in their abundance and/or performance may entail
community-wide effects. In the fluctuating Western Baltic, species typically experience a broad range of environmental conditions,
which may preselect them to better cope with climate change. In this study, we examined the sensitivity of two crucial ontogenetic
phases (naupliar, cypris) of the barnacle toward a range of temperature (12, 20, and 28°C) and salinity (5, 15, and 30 psu)
combinations. Under all salinity treatments, nauplii developed faster at intermediate and high temperatures. Cyprid metamorphosis
success, in contrast, was interactively impacted by temperature and salinity. Survival of nauplii decreased with increasing
salinity under all temperature treatments. Highest settlement rates occurred at the intermediate temperature and salinity
combination, i.e., 20°C and 15 psu. Settlement success of “naive” cyprids, i.e., when nauplii were raised in the absence of
stress (20°C/15 psu), was less impacted by stressful temperature/salinity combinations than that of cyprids with a stress
history. Here, settlement success was highest at 30 psu particularly at low and high temperatures. Surprisingly, larval survival
was not highest under the conditions typical for the Kiel Fjord at the season of peak settlement (20°C/15 psu). The proportion
of nauplii that ultimately transformed to attached juveniles was, however, highest under these “home” conditions. Overall,
only particularly stressful combinations of temperature and salinity substantially reduced larval performance and development.
Given more time for adaptation, the relatively smooth climate shifts predicted will probably not dramatically affect this
species.
Significance
Why most—but not all—organisms mature earlier in better growth conditions remains a mystery. Theory suggest that a solution may lie in the existence and evolution of critical size thresholds during development. The threshold model makes two unique predictions on the evolution of reaction norms between species and the effect of food reductions within species. We test this model experimentally using five damselfly species aligned along an ephemeral–permanent gradient, finding strong support for each prediction. Permanent habitats favor large thresholds and early maturation in better conditions, whereas ephemeral habitats favor small thresholds producing the rarer pattern with delayed maturation. The evolution of developmental thresholds is critical for understanding natural and human-induced variation in age and size at maturity.
طی فرایند پروش میگو آلاینده های مختلفی تولید و به همراه پساب از استخرهای پرورش خارج می شود. در این پژوهش تاثیرات سایت پرورش میگو شیف در استان بوشهر بر کیفیت آب خروجی از استخرها و نیز بر برخی از خصوصیات زیستی کشتی چسب Amphibalanus amphitrite و اویستر Saccostrea cucullata که در مجاورت این سایت حضور دارند مورد بررسی قرار گرفت. بر طبق نتایج، فرایند پرورش میگو باعث کاهش کیفیت آب می شود. دما، شوری، نیتروژن کل، فسفر کل، آمونیاک و کلروفیل a در کانال خروجی اختلاف معنی داری با مقادیر ثبت شده برای این فاکتورها در کانال ورودی نشان دادند. میانگین نیتروژن کل (میلی گرم بر لیتر)، فسفر کل (میلی گرم بر لیتر) و کلروفیل a (میکروگرم بر لیتر) در آب ورودی به ترتیب 03/0 ± 78/0، 01/0 ± 07/0 و 76/0 ± 83/11 به ثبت رسید که در ابتدا کانال خروجی به ترتیب به 30/0 ± 57/2، 03/0 ± 20/0 و 33/0 ± 16/17 و در انتهای کانال خروجی به ترتیب به 03/0 ± 38/2، 0/0 ± 15/0 و 68/0 ± 31/16 رسید. تراکم کشتی چسب ها در ابتدای کانال خروجی به طور معنی داری بالاتر از تراکم این گونه در کانال ورودی بود درحالی که تفاوتی بین تراکم اویسترها در ایستگاه های مختلف دیده نشد. با این وجود طول و وزن اویسترها و کشتی چسب های ساکن در کانال خروجی به طور معنی داری بالاتر از افراد هم گونه در کانال ورودی بود. به نظر می رسد افزایش بار مواد آلی در استخرها و در نتیجه در پساب خروجی با افزایش مواد غذایی در دسترس برای این دو گونه ی صافی خوار باعث افزایش تراکم کشتی چسب ها و طول و وزن هر دو گونه در مقایسه با ایستگاه شاهد (کانال ورودی) شده است.
Plethodontid salamanders exhibit biphasic, larval form paedomorphic, and direct developing life cycles. This diversity of developmental strategies exceeds that of any other family of terrestrial vertebrate. Here we compare patterns of larval development among the three divergent lineages of biphasic plethodontids and other salamanders. We discuss how patterns of life-cycle evolution and larval ecology might have produced a wide array of larval life histories. Compared with many other salamanders, most larval plethodontids have relatively slow growth rates and sometimes exceptionally long larval periods (up to 60 mo). Recent phylogenetic analyses of life-cycle evolution indicate that ancestral plethodontids were likely direct developers. If true, then biphasic and paedomorphic lineages might have been independently derived through different developmental mechanisms. Furthermore, biphasic plethodontids largely colonized stream habitats, which tend to have lower productivity than seasonally ephemeral ponds. Consistent with this, plethodontid larvae grow very slowly, and metamorphic timing does not appear to be strongly affected by growth history. On the basis of this, we speculate that feeding schedules and stress hormones might play a comparatively reduced role in governing the timing of metamorphosis of stream-dwelling salamanders, particularly plethodontids.
Morphological and developmental responses of anuran larvae
(Physalaemus albonotatus) to chemical cues from the predators Moenkhausia dichoroura (Characiformes:
Characidae) and Belostoma elongatum (Hemiptera: Belostomatidae). Zoological Studies 50(2): 203-210.
Animals constantly face various predators in diverse environments. The phenotypic changes induced in prey by
different predators may differ quantitatively but not qualitatively, possibly because similar defense strategies are
effective against different predators. Also, species inhabiting more-permanent habitats tend to exhibit defense
strategies that enable them to coexist with potential predators. We examined phenotypic plasticity responses
to different predators. We tested differences in the morphology and growth rates of mewing frog Physalaemus
albonotatus tadpoles raised in the presence of chemical cues from water-bug (Belostoma elongatum) and
fish (Moenkhausia dichroura) in order to determine if this species has generalized or specialized responses to
different predators. The experiment was performed under microcosm conditions, and the experimental design
consisted of 3 treatments: chemical cues from fish and from water-bug, and a control group. Each container
held a single larva in order to obtain independent data for different variables. Each treatment was replicated
30 times, with 90 total experimental units. The main findings were as follows: 1) tadpole morphology was
significantly affected by the presence of predator cues; 2) tadpoles reared with fish cues were significantly larger
than those subjected to the other 2 treatments (water-bug cues and the control), while those reared with waterbug
cues were also larger than the control; and 3) tadpoles exposed to chemical cues of predators exhibited
accelerated growth rates and development stages. Our results suggest that the presence of predaceous fish
and water-bug has a major effect on morphology, growth rate, and development of P. albonotatus tadpoles.
Morphological variables, growth rates, and developmental stages followed the same pattern, and all of these
variables showed increases in tadpoles exposed to chemical cues of predators, possibly because P. albonotatus
larvae develop in temporary and semi-permanent ponds and are able to exploit different habitats, and therefore
their responses to chemical cues from different predators are similar
The effects of algal diet on larval survival and growth of the barnacle Amphibalanusimprovisus was for the first time examined under controlled laboratory conditions. Larvae were obtained by dissecting egg lamellae at later developmental stage out of the adults. Hatched nauplii were reared in 0.6-l glass beakers (200 larvae l-1) on a monoalgal diet of Chaetoceroscalcitrans, Chlorellavulgaris and Scenedesmusquadricauda at 1x105 and 2x105 cells ml-1, under continuous light at 25 ±1°C. The rate of development, survival and size (at Stage V) of the larvae were measured for each diet. The majority of nauplius II larvae (~70%) fed with Cha.calcitrans and Chl.vulgaris developed into cyprids within seven days while those fed with S.quadricauda remained at Stage II. A shorter time interval for Stage II to III was observed in larvae fed with a Chl.vulgaris monoalgal diet than Cha.calcitrans. Larvae fed with Cha.calcitrans had shorter developmental intervals for later larval stages (Stages IV–VI). The highest mortality was observed in the treatment with a monoalgal diet of S.quadricauda, while the highest survival was achieved with a diet of Cha.calcitrans. The mixed diet of Cha.calcitrans, Chl.vulgaris and S.quadricauda resulted in a shorter developmental duration of larval cycle (six days). Both food type and food concentration significantly affected the length and width of the nauplius larvae.
Life histories may show phases of both plasticity and canalization in response to feeding rate. Models for life history canalization and plasticity postulate a threshold for initiation of canalized developmental events. Some models postulate adaptive plasticity, whereas others postulate nonadaptive plasticity that results from environmental modulation of fixed development. These models have been tested by changing feeding rate at various times and determining when timing of life history events becomes unresponsive to those changes. This approach has been criticized because putative thresholds are usually not known. We use an alternative experimental design to test models of reproductive plasticity and canalization, and to estimate thresholds, in the grasshopper Romalea microptera. We develop mathematical models for published verbal models that predict how life history timing changes with feeding rate. Alternative models predict distinct relationships of time to oviposition vs. mean food intake that we test via experimental manipulation of food intake and nonlinear regressions. Regressions yield estimates of both the threshold and the duration of post-threshold development. A model postulating a fixed threshold and canalized post-threshold development provides the best, most parsimonious fit to data for this grass-hopper. Thus, the simplest model, postulating no adaptive variation in development, is supported, a result that is consistent with previous experiments on this system using changing feeding rates. We use the estimate of the threshold (in units of food eaten) and measurements of hemolymph protein content to estimate the threshold in units of physiologically relevant storage. These results elucidate the structure of reproductive plasticity in this system and how this alternative experimental approach can provide testable predictions of developmental thresholds for further experiments on life history plasticity and canalization.
The biological performance of species close to their biogeographic boundaries is of
critical interest in a period of rapid climate change and can inform predictions of future patterns of
distribution. The classic view is that performance attributes (reproduction, growth, survival) will
gradually decline from the centre towards the edge of a species range. A persistent discontinuity in
the distribution of the intertidal barnacle Chthamalus montagui on the central south coast of England
has enabled us to test hypotheses about its performance and recruitment as the range edge is
approached. Although adult density was reduced by over 5 orders of magnitude along a 200 km distance,
there was little evidence of impaired performance at the range edge. There have been fluctuations
in abundance over the last 50 yr at shores approaching the border, which are associated with
changes in temperature and suggest thermal sensitivities. A study of recruitment in C. montagui and
in other intertidal barnacles revealed a region of very low recruitment for all species close to the border
of C. montagui. We propose that reductions in larval supply caused by complex regional hydrography
and suboptimal habitat quality, not adult performance, is most likely responsible for a steep
gradient in recruitment as the border is approached, although possible reductions in larval performance
cannot be totally discounted. The location of ‘low recruitment cells’ caused by oceanographic
processes that obstruct the dispersal of propagules needs to be identified when modelling the rate of
change of biological assemblages and the location and spacing of reserves
An anthropological analysis was conducted on skeletal and dental remains brought to the Galveston County Medical Examiner's office. The skeletal remains were dry, fragmented, and absent of typical fluvial characteristics. During microscopic examination, semitransparent, circular objects were discovered on the dentition, the mandible, tibial plateau, and distal femur. The objects were glycoproteinous adhesions deposited by the acorn barnacle, Balanus improvisus. B. improvisus is an intertidal barnacle found in estuaries in Galveston Bay. Basal diameter of the adhesions on the dentition were significantly smaller than those found on the postcranial bones (p = 0.010), indicating two consecutive cohorts adhered to the bone and dentition. As settlement typically occurs once a year, this would indicate that the remains were in the fluvial environment for at least 375-410 days. It is important in geographic areas that have prevalent fluvial environments that human remains, particularly dentition, are microscopically examined for marine life evidence.
Metamorphosis is a common life-cycle transition in organisms as diverse as amphibians, insects, fishes and crustaceans, and the timing of this transition often affects an individual's fitness. Here, we measured age and size at metamorphosis in laboratory-reared individuals of the freshwater copepod, Diaptomus leptopus, and then followed individuals over their entire life cycle to assess the fitness consequences of variation in age and size at metamorphosis. In 3 separate experiments, individuals were raised in different food conditions: low food (0.2 μg C/ml) switched to high food (0.7 μg C/ml), or high food switched to low food, at several different larval and juvenile stages. Control individuals were reared on high or low food concentrations over their entire life cycles. For each individual, we measured age and size at metamorphosis and age and size at maturity; for females, we also measured total lifetime egg production, longevity, and calculated a composite fitness measure, λ. Statistical analyses showed no significant effects of age or size at metamorphosis on these same traits measured at maturity, or on the fitness components we estimated. The first individuals to mature had the highest total egg production and individual fitness; differences in body size at maturation explained none of the variation observed in fitness components. Our results show that metamorphosis was uncoupled from maturity and from fitness components by growth and development achieved during the juvenile phase of the life cycle, and support the conclusion that fitness consequences of metamorphosis depend fundamentally on the organization of an organism's life cycle. They also suggest that body size plays a different life-history role in these organisms than is recognized in most poikilotherms, and suggest the hypothesis, based on laboratory experiments, that selection may act primarily on juvenile developmental rates in field populations.
The performance of a species can be significantly altered by subtle changes in the physical environmental. The intertidal barnacle Balanus glandula is predominantly an open coast species in the Northeast Pacific. However, B. glandula commonly inhabits estuaries where environmental conditions such as salinity and temperature drastically differ from the open coast. We used survivorship and growth rates as a measure of performance in recently metamorphosed laboratory reared juvenile B. glandula outplanted along an environmental gradient at the mouth, mid-estuarine, and riverine end of the South Slough Estuary, Oregon, USA. Juvenile performance was highly variable over spatial and temporal scales and dependent upon existing environmental conditions. Surprisingly, along this estuarine gradient, juveniles performed better at a mid-estuarine location than at the mouth of the estuary. Typically, the riverine end of the estuary was the least suitable habitat along the estuarine gradient due to high juvenile mortality and a low growth rate. Although seasonally variable, survivorship and growth decreased with height along a vertical intertidal gradient as well. In a reciprocal transplant experiment, populations from both ends of the estuarine gradient displayed similar survivorship and growth rates. Our results demonstrate that the interactions of environmental conditions that vary temporally and spatially along a gradient strongly affect the success of an individual surviving and prospering during the early juvenile period.
Lipid and protein biochemistry of eggs (84μm in diameter), embryos and early larvae of the tropical echinoid Tripneustes gratilla (Linnaeus 1758) were quantified to determine how maternal provisions are used to fuel development of the echinopluteus. The
eggs contained a mean of 30.82ng lipid and 87.32ng protein. Energetic lipids were the major lipid component (55.52% of total
lipid) with the major class being triglyceride (TG: mean 15.9ng, 51.58% of total). Structural lipid was dominated by phospholipid
(PL: mean 11.18ng, 36.26% of total). Early embryogenesis was not a major drain on egg energetic lipid and protein. Development
of the functional feeding larva used ca. 50% of initial egg energetic lipid and most of this was TG. Maternal TG was still
present in the 8-day echinoplutei and it was estimated that this energetic lipid would be depleted in unfed larvae by day
10. There was no change in PL. In a separate experiment lipid biochemistry of rudiment stage larvae and early developing juveniles
were quantified to determine how lipids are used during metamorphosis. Fed larvae accumulated lipid (mean 275.49ng) with
TG and PL being the major energetic and structural lipids, respectively. Larval lipid stores were not appreciably depleted
by metamorphosis and so were available for the early benthic stage juvenile. Juveniles started their benthic existence with
314ng total lipid (TG: mean 46.84ng, 14.9% of total, PL: mean 137.51ng, 43.67% of total). Nile Red histochemistry and histology
showed that the stomach serves as a nutrient storage organ and, that lipid stores accrued by larvae sustain developing juveniles
for up to 4 days post settlement. Triglyceride supported both non-feeding stages of development and the prefeeding larval
and perimetamorphic benthic stage. In this first study of lipid stores in settlement stage echinoderm larvae, we show that
T. gratilla larvae sequester the same major energetic lipid (TG) to support the early juvenile that the female parent provided them to
fuel early development.
Ratios are used by many ecological physiologists to adjust (or scale) data that vary allometrically with body size. We use two sets of real data from our laboratory to illustrate in detail how investigators may be misled by statistical analyses performed on such ratios. The first example concerns the use of ratios to increase the precision of data gathered in planned experiments where body size varies within experimental groups but not among them. The second example concerns the use of ratios to remove confounding effects of body size from studies where animals in one group are larger than those in other groups, as a result either of the experimental manipulation itself or of the procedure for assigning animals to treatment groups. In both of these examples, statistical analyses of ratios lead to conclusions that are inconsistent with impressions gained from visual examinations of data displayed in bivariate plots. In comparison, analyses of covariance lead to conclusions that agree with impressions gaine...
We investigated how changes in food availability during development affected the timing of and body size at metamorphosis in two closely related species of tree frogs that use different larval habitats. We raised tadpoles of Hyla gratiosa (a temporary-pond breeder) and Hyla cinerea (a permanent-pond breeder) at two different temperatures on either constant resources or a regime in which we altered food levels at one of three different times during development. For both species, larval period was affected only by early changes in food level; early increases shortened larval period, and decreases lengthened it. The timing of metamorphosis of Hyla gratiosa showed greater plasticity than that of Hyla cinerea, because of its greater overall response to any food-level change and not because of any difference between species in the duration of the sensitive period. The two species showed comparable levels of plasticity in body size at metamorphosis; increases in food level produced larger body sizes, and decreases produced smaller sizes. However, in contrast to the pattern seen in larval period, later changes in food level had the greatest effect on body size. These results force a reexamination of current ideas about the adaptive significance of plasticity in the timing of metamorphosis in response to food availability in larval anurans. We offer a model of dynamic allocation that accommodates the extant data on this tissue.
The effects of short-term variation in food availability on larval survival and development of the barnacle Balanus amphitrite amphitrite Darwin were studied in the laboratory. We found that 0.5 and 1 d intervals of alternating feeding and starvation did not influence survivorship of stage II nauplii, but lengthened the duration of development by about 40%; survivorship of nauplius II initially starved for 2 and 3 d was >25 % lower than in the continuously fed controls, and larval development was prolonged by >1.5 d. Four-day initial starvation in nauplius II led to 100% larval mortality. Initial starvation also significantly affected feeding time required to complete nauplius II. Although initial starvation in nauplius II affected larval survival and duration of development, those larvae reaching cypris stage all metamorphosed into juveniles. The minimum feeding time required for completion of nauplius II was extended by >8 h for each day of initial starvation, for up to 2 d initial starvation. Feeding time required to complete individual naupliar stages also increased with larval development. Continuous access to food beyond the minimum feeding time shortened the duration of development. Our data suggest that B. amphitrite amphitrite larvae can survive short-term starvation and that such ability may help them overcome a patchy food supply in the field. However, sublethal starvation will lengthen the duration of development, thus increasing exposure to sources of mortality such as predation or misrouting. Since initial starvation in the nauplius II stage did not influence the metamorphic capacity of cyprids in the laboratory, sublethal starvation during larval development should not affect bioassay results.
Nile red (NR) is a hydrophobic fluorophore that binds specifically to neutral lipids. We examined the usefulness of NR as a probe for detecting neutral-lipid-storage products in benthic (harpacticoid) copepods. Following a brief (30 min) exposure to NR, lipid droplets, which fluoresce a bright yellow/orange, were clearly visible under epifluorescent illumination. Analysis of fluorescent images was used to determine relative lipid concentrations. The NR procedure was used on copepods subjected to a range of starvation periods. As predicted, detectable lipid reserves decreased with increased starvation period. The sensitivity of the NR procedure makes it a potentially useful tool for comparing relative lipid levels in individual organisms, even where lipid concentrations are near or below the detection limits of conventional analytical methods.
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.
Newly molted (0-d-old) cyprids of the barnacleBalanus amphitrite Darwin were prevented from settling for 0 to 14 d at four different temperatures (25, 20, 15 and 5°C treatments). The effect on settlement success of prolonging the cyprid lifetime was evaluated using a nitrilocellulose membrane assay. In addition, protein extract prepared from these cyprids was analyzed using gel electrophoresis to characterize the effect of age on protein content and composition. Settlement success was significantly affected for larvae aged at 25 (P P P P P P = 0.17), but did enhance the decline in settlement success with age during Phase II (P < 0.001). Gel electrophoresis revealed a significant decline in the quantity of the cyprid storage protein CMP (Cyprid Major Protein) with increasing age at 25, 20 and 15°C, but CMP levels remained constant at 5°C. These results suggest that, upon molting to the cyprid stage, larvae may still require a settlement-competence attainment period. This may be achieved by CMP utilization during Phase I, depletion of which during Phase II may be responsible for reduction in settlement success with cyprid age such that remaining CMP stores can no longer support the production of adult structures following settlement.
The authors extend earlier theory to include explicit time constraints in 3 hypothetical, complex life cycles. Dynamic optimization models are constructed to determine optimal time and mass trajectories for niche shifts. They consider the habitat shift at emergence in mayflies, where reproduction terminates a growth period in the first habitat and is constrained to a season. They consider the habitat shift at metamorphosis in amphibians, where reproduction terminates a growth phase in the 2nd habitat and reproduction is constrained to a single point in time. They then combine the first 2 effects to allow an extended period of reproduction in amphibians. Here optimal time and mass trajectories are determined for the shift from aquatic to terrestrial habitat and the shift from a growth phase to a reproductive phase. Time constraints on complex life histories lead to optimal sizes for niche shifts that vary with time. In time-constrained life histories, any variation in the state of individuals at some time prior to reproduction will be preserved to some degree at reproduction. Optimal switches in habitat use or life history stage should depend not only on state but also on the time that state is achieved. -from Authors
Amphibian larvae exhibit phenotypic plasticity in size at metamorphosis and duration of the larval period. I used Pseudacris crucifer tadpoles to test two models for predicting tadpole age and size at metamorphosis under changing environmental conditions. The Wilbur-Collins model states that metamorphosis is initiated as a function of a tadpole's size and relative growth rate, and predicts that changes in growth rate throughout the larval period affect age and size at metamorphosis. An alternative model, the fixed-rate model, states that age at metamorphosis is fixed early in larval life, and subsequent changes in growth rate will have no effect on the length of the larval period. My results confirm that food supplies affect both age and size at metamorphosis, but developmental rates became fixed at approximately Gosner (1960) stages 35-37. Neither model completely predicted these results. I suggest that the generally accepted Wilbur-Collins model is improved by incorporating a point of fixed developmental timing. Growth trajectories predicted from this modified model fit the results of this study better than trajectories based on either of the original models. The results of this study suggests a constraint that limits the simultaneous optimization of age and size at metamorphosis. 32 refs., 5 figs., 1 tab.
To determine if the onset of intertidal life is a critical time for survival, we examined the fate of newly settled Balanus glandula, an intertidal barnacle, on natural rocky substrata in Barkley Sound, British Columbia, Canada. In total, 552 individual settlers were mapped and followed daily during their first 3 to 5 d after settlement in May 1992 and were then periodically re-examined over a 45 d period. A sharp decline in survivorship occurred during the first day after settlement. For settlers arriving on 16 and 17 May, mortality during the first day after settlement (38.0%) was almost as high as all mortality during the following 44 d (40.1%). Mortality during the first day after settlement was 1.5 to 6.0 times higher than during the second day for settlers arriving on 16, 17 and 18 May. There was no relationship, however, between percent first day mortality and densities of recruits or of grazers (limpets, littorines). The elevated levels of first day mortality were also not consistent with desiccation stress, wave exposure, or size-specific changes in vulnerability. The first moments after settlement may constitute a bottleneck for the survival of barnacles settling in the intertidal zone. For organisms such as B. glanduIa, selective pressures for traits such as time of settlement relative to the tidal cycle, selection of settlement micro-site, and energy reserves at settlement could be most intense during the first day in the benthic habitat.
Many benthic marine invertebrates develop by means of free-living, dispersive larval stages. The presumed advantages of such larvae include the avoidance of competition for resources with adults, temporary reduction of benthic mortality while in the plankton, decreased Likelihood of inbreeding in the next generation, and increased ability to withstand local extinction. However, the direction of evolutionary change appears generally biased toward the loss of larvae in many clades, implying that larvae are somehow disadvantageous. Possible disadvantages include dispersal away from favorable habitat, mismatches between larval and juvenile physiological tolerances, greater susceptibility to environmental stresses, greater susceptibility to predation. and various costs that may be associated with metamorphosing in response to specific chemical cues and postponing metamorphosis in the absence of those cues. Understanding the forces responsible for the present distribution of larval and nan-larval (aplanktonic) development among benthic marine invertebrates. and the potential influence of human activities on the direction of future evolutionary change in reproductive patterns, will require a better understanding of the following issues: the role of macro-evolutionary forces in selecting for or against dispersive larvae; the relative tolerances of encapsulated embryos and free-living larvae to salinity, pollutant, and other environmental stresses; the degree to which egg masses, egg capsules, and brood chambers protect developing embryos from environmental stresses; the relative magnitude of predation by planktonic and benthic predators on both larvae and early juveniles; the way in which larval and juvenile size affect vulnerability to predators; the extent to which encapsulation and brooding protect against predators; the amount of genetic change associated with loss of larvae from invertebrate life cycles and the time required to accomplish that change; and the degree to which continued input of larvae from other populations deters selection against dispersive larvae. The prominence of larval development in modem Life cycles may reflect difficulties in losing larvae from Life cycles more than selection for their retention.
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 (PP>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.
Data support the previously published hypothesis that amphibians should adjust their developmental rates in response to environmental conditions, accomplished by the responses of the differentiation rate to the growth rate. -from Authors
Researchers commonly compute percentages or size-specific indices in an attempt to remove effects of body size from physiological data. Unfortunately, such ratios seldom eliminate the influence of body size on a physiological response and the ratios introduce major (but often unrecognized) problems with respect to statistical analysis and interpretation of the data. Indeed, these shortcomings of ratios frequently lead investigators to arrive at incorrect conclusions in otherwise flawless experiments. A superior alternative to using ratios combines graphical analysis and the analysis of covariance, which is a widely available statistical routine that uses least-squares regression to remove effects of body size from physiological data. Accordingly, we counsel researchers to discontinue forming ratios in an attempt to normalize physiological data for variation in body size and to adopt a reliable alternative. We also advise readers of scientific research not to place great confidence in results of studies that use ratios for scaling.
1. Under standard laboratory rearing conditions, caterpillars of Manduca sexta invariably go through 5 larval instars before pupating.2. Evidence is presented that the head capsule width of a given instar is proportional to the weight that the individual had attained at the time that the molt to that instar occurred. Fifth-instar larvae with a large range of head capsule sizes were produced by temporarily starving 3rd and 4th instars, thus inducing them to molt at subnormal weights.3. Further observations on such larvae revealed that individuals with head capsules wider than 5.1 mm proceeded to pupate at the following molt whereas larvae with smaller head capsules underwent a supernumerary larval molt.4. It was concluded that larvae of Manduca simply continue to grow and molt until they reach or exceed a sharply defined threshold size (corresponding to a head capsule size of 5.1 mm). The instar in which this threshold size is attained is then the final larval instar during which the corpora allata will be...
Simple ratios in which a measurement variable is divided by a size variable are commonly used but known to be inadequate for eliminating size correlations from morphometric data. Deficiencies in the simple ratio can be alleviated by incorporating regression coefficients describing the bivariate relationship between the measurement and size variables. Recommendations have included: 1) subtracting the regression intercept to force the bivariate relationship through the origin (intercept-adjusted ratios); 2) exponentiating either the measurement or the size variable using an allometry coefficient to achieve linearity (allometrically adjusted ratios); or 3) both subtracting the intercept and exponentiating (fully adjusted ratios). These three strategies for deriving size-adjusted ratios imply different data models for describing the bivariate relationship between the measurement and size variables (i.e., the linear, simple allometric, and full allometric models, respectively). Algebraic rearrangement of the equation associated with each data model leads to a correctly formulated adjusted ratio whose expected value is constant (i.e., size correlation is eliminated). Alternatively, simple algebra can be used to derive an expected value function for assessing whether any proposed ratio formula is effective in eliminating size correlations. Some published ratio adjustments were incorrectly formulated as indicated by expected values that remain a function of size after ratio transformation. Regression coefficients incorporated into adjusted ratios must be estimated using least-squares regression of the measurement variable on the size variable. Use of parameters estimated by any other regression technique (e.g., major axis or reduced major axis) results in residual correlations between size and the adjusted measurement variable. Correctly formulated adjusted ratios, whose parameters are estimated by least-squares methods, do control for size correlations. The size-adjusted results are similar to those based on analysis of least-squares residuals from the regression of the measurement on the size variable. However, adjusted ratios introduce size-related changes in distributional characteristics (variances) that differentially alter relationships among animals in different size classes.
A synthetic theory of the ecology of amphibian metamorphosis is founded on the observation that the large variation in length of larval period and body size at metamorphosis typical of a particular species of amphibian cannot be directly explained by differences in dates of hatching or egg sizes. It is proposed that as development proceeds, variation in exponential growth coefficients causes a trend from a normal distribution to a skewed distribution of body sizes. The degree of skewing increases and the median of the distribution decreases with increasing initial densities of populations. The relative advantages of the largest members of a cohort may arise from a variety of mechanisms including the production of growth inhibitors, interference competition, and size-selective feeding behavior. These mechanisms result in a nonnormal distribution of competitive ability, a possible source of the density-dependent competition coefficient found in systems with many species (1).
Zooplankton are commonly frozen at sea in ecological studies when it is impractical to extract lipids immediately from live animals. Analysis of lipids extracted from the copepod Calanus pacificus established that freezing has negligible effects on copepod dry mass, total lipid content, or lipid composition, resulting only in slight changes in free fatty acids. However, storage for 1 yr at -15°C resulted in substantial loss of polar lipids and accumulation of free fatty acids when compared with animals stored at - 80°C. Rapid freezing in liquid nitrogen, followed by maintenance of animals at temperatures below -70°C, is recommended where immediate lipid extraction is not feasible.
Tile allocation of tinle and resources to the conflicting denlands of grOwtll and reproduction has been an important theme in evolutionary explanations for tile diversity of life history patterns among living organisnis (e.g., Gadgil and Bossert, 1970 ; Schaffer, 1974) . In examining tile probleni of 110w this allocation is achieved and adaptively modified under different ecological conditions, studies of organisms with discrete life stages are particularly important, since growth and reproductive phases of the life cycle are often clearly delineated. Further, an ullderstanding of this problem requires the integration of ecological theory witll developmental and physiological considerations. These points are well illustrated by Wilbur and Collins' (1973) attempt to model control of the neuroiioriiional processes underlying developmental plasticity in ampilibians and to account for variation in amphibian life cycles. A salient feature of their model is the role of hypothetical mechanisms which allow larvae to monitor both tlleir rate of growth and body size; information on which the decision to metamorphose is assumed to be based. Although tile existence of such mechanisms in amphibians remains to be demonstrated, there is evidence to suggest that analogous models may be relevant to tile study of adaptation in insect life cycles. Mechanisms which influence development in response to changes ill body size have been described in studies of the blood-sucking bug, Rliodn ins prolixus (\Vigglesworth, 1934; Van der Kloot, 1961 ; Steel and Harmsen, 1971). Molting occurs only after the ingestion of a blood meal, and tilese studies provide strong evidence that distension of the abdonien is detected by stretch receptors wilicil initiate tile molt by triggering the release of brain hormone. Further evidence of size-dependent regulation of insect development has conie from experimentally manipulating growth of larvae of a holonietabolous insect, Manduca sexta. Nij bout and Williams (1974a, b) Ilave shown that 5th-instar larvae molt only' when they attain a size corresponding to a weight of about 5 g. \Vhen this critical size is reaciled, the corpora allata cease to secrete juvenile hormone, initi ating the endocrine events leading to the molt. Tile determination of which molt will lead to a pupa is also apparently made on the basis of size (Nijhout, 1975).
Nauplii of Balanus glandula obtained from gravid adults were cultured in the laboratory. Morphological descriptions and drawings of the six naupliar stages and the cyprid are presented. The nauplii generally followed the typical developmental pattern of Balanus. Total length (mean ± two standard deviations) of the nauplii increased from 271 ± 16 μm at stage I to 745 ± 116 μm at stage VI. All naupliar stages had a trilobed labrum. Setation of the antennule followed the typical balanid pattern through development; beyond stage I both rami of the antenna and mandible had one or two fewer setae than is typical. The patterns of setation were increasingly variable through development. Within stages, the mandibular exopodite was the ramus with the most consistent setation pattern, while the mandibular endopodite had the least consistent setation pattern. For larvae cultured individually in wells of tissue culture plates, the highest daily rate of metamorphosis to the cyprid occurred 11 days postliberation, with 41% cumulative yield. For mass cultures the metamorphosis rate peaked 13-14 days postliberation, with 56% cumulative yield. Cyprids produced in the mass cultures after 11-12 days of growth averaged 690 ± 60 μm in length; new cyprids appearing after 15-20 days of growth averaged 590 ± 40 μm in length.
Variable growth and development were imposed on the pitcher-plant mosquito. Wyeomyia smithii, to test whether the initiation of metamorphosis was determined early in larval life or remained flexible throughout development. Like anurans, larval W. smithii are specialized for a suspension-feeding way of life and they metamorphose into dispersing, reproductive adults. We therefore used models originally formulated in an amphibian context to examine the effects of modified larval growth on the triggering of metamorphosis and then used our results to reexamine metamorphosis in amphibians. Response to enhanced and decreased food regimens showed that larval growth during the first two (of four) instars affected both the time to and mass at metamorphosis. The major effects of developmental inertia are prominent for about one to two instars and then abate, but do not necessarily disappear, with each succeeding instar. Despite evidence for developmental inertia in W. smithii, experiments transferring larvae from high food to starvation show that the physiological commitment to undergo metamorphosis does not take place until the last (fourth) instar and that nonzero growth during the last instar is required to trigger metamorphosis. All amphibian models for the initiation of metamorphosis involve the effects of rates: developmental rate and past or present growth rates. In W. smithii, there is no primacy of developmental rate and low growth rate does not stimulate metamorphosis of larvae having attained the minimum mass required for metamorphosis. An insect-derived model involving the effects of size-specific growth increments is more consistent than any amphibian model with our results in W. smithii. Testing the reciprocal ability of the insect model to predict amphibian metamorphosis is not possible with current data, because no study has considered zero growth in amphibians to identify the transition from growth-dependent to growth-independent development leading to metamorphosis. This transition marks the irrevocable commitment of the organism to an ontogenetic niche shift from an aquatic larva to a terrestrial, dispersing, and reproducing adult. Identifying the proximal causes of this mechanism is fundamental to understanding how flexible growth and ontogeny of complex life cycles have adapted to variable larval environments.
Many crustaceans have complex life cycles characterized by a metamorphosis, yet variation in metamorphic traits, and the causes and consequences of this variation, have rarely been examined. Food concentrations were changed during specific larval stages of the freshwater copepod Mesocyclops edax Forbes (Copepoda: Cyclopoida) to examine whether age and size at metamorphosis remain flexible or become fixed during the larval period. Results were compared to predictions of both flexible (the Wilbur-Collins model) and fixed (Leips-Travis model) rate models for the timing of amphibian metamorphosis. Age and size at metamorphosis were variable in all treatments, and age was always more variable than size. Changes in food concentration early in larval development resulted in significant differences in age at metamorphosis among treatments, but changes initiated when 60% of the larval period had passed had no effect on age at metamorphosis. Development appeared to become fixed later in the larval period, before the ultimate larval stage was reached. These results support predictions of the Leips-Travis model. Early changes in food concentrations had significant effects on size at metamorphosis, but changes initiated during the penultimate larval stage (50-60% of larval development) had no effect on metamorph size. Size at metamorphosis in M. edax also appeared to be fixed before the ultimate larval stage was reached. Fixation of size at metamorphosis during development is not predicted by either model and may be unique to organisms with rigid exoskeletons that constrain growth within any stage. Patterns of covariation between age and size at metamorphosis suggest that food conditions early in larval development exert a large effect on metamorphic traits, in contrast to patterns observed in several amphibian species. The Wilbur-Collins model places a fitness premium on delaying metamorphosis to achieve a maximum size, when growth conditions are favorable; it thus may not apply to crustaceans. Selection pressures on the timing of metamorphosis in crustaceans may differ substantially from those identified for amphibians and other organisms. Because of these differences, incorporating crustaceans into studies of metamorphosis will help to clarify the factors affecting this life cycle transition.
Achievement of a critical body size provides the proximate stimulus for the metamorphic molt in Oncopeltus and other hemimetabolous and holometabolous insects. Effects of size-dependent stimuli on metamorphosis vary in detail among different insects, although the adaptive significance of this variation is as yet unknown. The phenomenon is important to life histories where growth rates are highly variable, since it allows larvae to delay eclosion until a prerequisite body size is attained. In Oncopeltus, variation in growth rate occurs where nymphs develop on individual host plants which differ greatly in nutritional quality, depending on the presence or absence of seeds. This variation in growth rates results in marked variation in adult size. The size at which nymphs eclose is determined by opposing selective forces in the adult and larval stages. When growth is slow, nymphs which must attain a larger size exhibit longer developmental times and lower survival to eclosion. However, bugs which eclose at a larger adult size survive longer under starvation conditions, and presumably could disperse for longer periods in search of food sources. This is particularly important for females eclosing on nonfruiting plants, since they must locate a supply of seeds before reproduction can commence.
Amphibians exhibit extreme plasticity in the timing of metamorphosis, and several species have been shown to respond to water availability, accelerating metamor- phosis when their ponds dry. In this study we analyzed the plasticity of the developmental response to water volume reduction in the western spadefoot toad, Scaphiopus hammondii. Also, we attempted to identify the environmental cue(s) that may signal a desiccating larval habitat. We spawned adults in the laboratory and raised tadpoles in aquaria in a controlled environmental chamber. Water levels of aquaria were gradually reduced by removing water at the rate of 0.5-1 L/d; water in control aquaria was similarly disturbed but not removed. Tadpoles subjected to water volume reduction showed significant acceleration of meta- morphosis. The developmental acceleration depended on the rate of reduction of the water level; i.e., tadpoles exhibited a continuum of response. This developmental response did not result from thermal differences between treatments. Furthermore, the response was reversible in that refilling of the aquaria to the starting water level at various times following the onset of volume reduction resulted in restoration of body mass and a tendency to decelerate metamorphosis. Several lines of evidence suggest that the developmental re- sponse is due neither to the concentration of compounds in the water nor to chemical or physical interactions among conspecifics. Rather, the response appears to be related to the reduced swimming volume and perhaps the proximity to the water surface. When the water level is reduced, tadpoles reduce foraging, and food restriction of prometamorphic tadpoles maintained in a constant high water environment accelerated metamorphosis. Spadefoot toad tadpoles are a valuable model system for explaining both the proximate mechanisms (environmental cues and physiological responses) and the ultimate causes for adaptive phenotypic plasticity in amphibian metamorphosis.
Any single method of testing food limitation can be misleading or inconclusive. We therefore used five different tests for food-limited growth of larvae of a sea urchin from the northwest Mediterranean: 1. In both spring and autumn, larvae given a nearly natural ration of food from daily changes of seawater grew and developed more slowly than larvae with the same water enhanced with a cultured alga. 2. Larvae given a nearly natural ration of food developed more slowly in autumn, when concentrations of chlorophyll a and particles in the plankton were lower, than in spring when these indications of food were higher. 3. Larvae given the enhanced ration grew and developed more rapidly than larvae in presumed cohorts in the plankton. 4. In both spring and autumn, larvae in the field had a food-limited form (longer arms and delayed formation of the echinus rudiment) in contrast to larvae given an enhanced ration. 5. Larvae in the autumn plankton had a more food-limited form than larvae in the spring plankton. Results of all five tests indicated food-limited growth in coastal waters in autumn; three indicated food-limited growth in spring. The concentrations of natural food were not unusually low. Food-limited growth suggests that these larvae may commonly feed with maximal or near-maximal clearance rates. If echinoid larval growth is limited by food under these conditions, it is likely that growth of other larval invertebrates is food limited in many coastal waters.
Implicit in past studies of recruitment is the assumption that all new recruits possess the same capacity for juvenile growth, and that observed variation in juvenile growth and survival is due entirely to spatial and temporal variation in food availability, magnitude of physical stresses, and intensity of competition and predation. We set out to determine if daily larval cohorts of the barnacle Semibalanus balanoides differ in mean physiological quality and, therefore, in their potential for recruiting to adult populations. To assess larval physiological quality, we measured the organic content of nonfeeding cyprid larvae attaching on five dates (10-15 d intervals) during the 1995 recruitment season. Juvenile physiological quality was determined by monitoring the growth, under controlled laboratory conditions, of individuals attaching on seven dates (3-15 d intervals) during the same season. Both cyprid organic content and juvenile growth capacity differed significantly among daily cohorts. We suggest that variation in cyprid organic content may explain previous observations of temporal variation in cyprid metamorphic success and early juvenile mortality and further suggest that variation in juvenile growth capacity contributes to differences in recruitment success of daily cohorts.
The biochemical composition of the cyprids of Balanus balanoides is described. The mean total freeze-dried weight per cyprid was 37.7 μg. Mean values, as percentages of total dry weight were 9.2% neutral lipid, 4.8% phospholipid, 0.8% polysaccharide, 2.7% free sugars, 6.8% protein nitrogen, 8.2% total nitrogen, 3.2% chitin and 12.4% ash.
Free-swimming cyprids, prevented from settling for up to 8 weeks at 8°C utilised their neutral lipid (triglyceride) reserves. At the end of this period 90% of the initial neutral lipid reserves were depleted. There was only a slight decrease in the phospholipid, free sugar and nitrogen content of the cyprids, and the polysaccharide content remained comparatively constant.
Many taxa have evolved complex life cycles featuring a dramatic shift in habitat or resource use at metamorphosis. Despite their prevalence and unique characteristics, we understand little about the adaptive properties and evolution of these life histories. I offer a conceptual framework that considers how size-specific growth and mortality rates in both habitats interact with size at metamorphosis to affect lifetime fitness. This model predicts the size at metamorphosis that maximizes fitness, and I use this framework to interpret the wide variation in the life history structure of the amphibians. In particular, I speculate on the adaptive significance of the tadpole stage of the anurans and on the cause of variation in the size at metamorphosis both between and within anuran families. Further, I predict the conditions under which direct development or paedomorphosis will be selected for, and I offer hypotheses on the selective factors that may contribute to the three-stage life history of the newts. Fin...
Larvae of many benthic marine invertebrates can delay metamorphosis in the laboratory. Along the coast of New England, Semibalanus balanoides (Linnaeus) cyprids recruit to adult populations over a period of approximately 8 weeks and it is reasonable to expect the relative number of cyprids delaying metamorphosis to increase as the season progresses. For cyprid larvae of the barnacle S. balanoides, specificity for a chemical metamorphic cue produced by conspecific adults declines in the laboratory during this delay period. If substratum specificity declines with larval age in the field, daily cohorts of cyprids attaching later in the season should exhibit progressively reduced specificity for the conspecific cue. To determine if cyprids attaching later in the recruitment season exhibit reduced substratum specificity compared to earlier attaching cyprids, the rates of cyprid attachment to control substrata (unattractive) and substrata coated with conspecific adult extract (attractive) were examined in the field at Nahant, Massachusetts, USA for two recruitment seasons (Spring 1994 and Spring 1995). Specificity for the conspecific cue varied considerably among daily cohorts of cyprids attaching at different times during both recruitment seasons. In 1994, cyprids attached at significantly greater rates to plates coated with conspecific adult extract than to control plates (P < 0.05) during the first half of the recruitment season but attached to all plates at similar rates during the remainder of the season. In 1995, cohorts of cyprids attaching on different dates also differed in their specificity for the adult cue although the mid-season decline in specificity observed in 1994 did not occur. Because substratum specificity has only been shown in the laboratory to decline with cyprid age, these results are consistent with the interpretation that cyprid larvae of S. balanoides at least periodically delay their metamorphosis in the field. These results also suggest that field tests of putative settlement cues and antifouling compounds must account for variation in substratum specificity exhibited by larvae attaching at different times during the recruitment season.
In experimental designs used by a number of disciplines, raw data are transformed into ratios and statistical analyses are performed on the ratio data. Although the designs themselves may be appropriate, the mathematical properties induced by ratio transformations can produce a loss of sensitivity in statistical tests. Since there are times when such designs must be used, it would be desirable to characterize the circumstances under which the statistical analysis of ratio data is or is not appropriate. To provide such information, a computer simulation approach was used to generate bivariate normal observations X and Y which were analysed using: (1) an analysis of variance ignoring the covariate; (2) an analysis of covariance; (3) an analysis of variance on the ratio Y/X. Comparisons were made between the three models by accumulating the number of rejections (1−β) on critical F-values for each model. Results taken from over a million analyses are discussed for a wide range of specific treatment effects and known correlations between the independent variable X and the dependent variable Y.
Considers evidence for chemical cues that promote or deter the settlement of marine invertebrates, with a particular focus on the isolation and identification of naturally occurring inducers of settlement. Chemoreception by marine invertebrate larvae is discussed, with a review of information on the larval sensory organs involved in the perception of chemical cues and with comparisons of chemoreception by marine and terrestrial invertebrates. -from Author
Semibalanus balanoides was studied on a sheltered New England shore. Recruitment greatly exceeded the capacity of the space to support adults. At low tidal heights, recruits grew rapidly, experienced severe crowding, and rarely survived to reproduce. At higher tidal heights, individuals grew more slowly and were less affected by crowding, and many (c10%) survived to reproduce. At low tidal heights, no recruits survived to reproduce at any density, due to intraspecific crowding, algal overgrowth, and predation. At intermediate tidal heights, lower recruitment decreased intraspecific crowding and increased survivorship, while at high tidal heights, lower recruitment decreased survivorship. In the high intertidal habitat, S. balanoides survivorship was higher on boulders than on rock cobbles due to thermal buffering, and intraspecific crowding decreased rock and barnacle temperatures and facilitated survival. Shading high intertidal cobbles from solar radiation decreased maximum rock and barnacle temperatures, dramatically increased survivorship and eliminated the survivorship advantage of high densities. High recruitment of S. balanoides can lead to massive density-dependent mortality in physically benign habitats, but in physically stressful habitats high recruitment density may buffer individuals from physical stress and facilitate survival. -from Author
Life cycles that incorporate discrete, morphologically distinct phases predominate among animals. One explanation for the abundance and long-term persistence of complex life cycles is that they represent adaptive mechanisms for decoupling the developmental processes that underlie morphological traits of alternative phases, thereby allowing phases to respond independently to different selective forces. Another explanation is that complex life cycles persist due to developmental constraints acting on particular phases; in particular, larvae may represent the conservation of traits of early development while adult traits evolve more freely in response to selection. A role of adaptive decoupling is generally supported by comparative data on the relative extent of morphological evolution of larvae and adults and on the frequency of elimination of phases from complex life cycles. Adaptive decoupling could result from developmental compartmentalization, and within such developmental systems, heterochrony could be a route to the deletion of a life cycle phase. The extent to which complex life cycles represent adaptive mechanisms for severing developmental linkages could be elucidated both by quantitative genetic studies comparing levels of genetic correlation among phase-specific traits and by molecular developmental studies of gene expression in alternative phases.
We report the use of nile red as a rapid and inexpensive method to estimate cellular lipids in three species of Paramecium and in Tetrahymena by the direct application of the dye to living or fixed cells without extraction and purification. Qualitative estimates of the relative changes in the lipid content of cells of varying culture ages were obtained using fluorescence microscopy, while semiquantitative determinations were obtained by measuring the total fluorescence from the emission spectrum (excitation, 535 nm) of fixed cells treated with excess nile red. The relative amounts of neutral (excitation, 488 nm; emission, 540 nm) and polar (excitation, 535 nm; emission, 680 nm) lipids were approximated using fluorescence intensity at these selected spectral conditions to avoid any spill over from each other. The patterns of change with culture age in total lipids in Tetrahymena and in total, neutral and polar lipids in Paramecium obtained using nile red agreed well with published gravimetric data for these ciliates.
A micro-analytical scheme for the determination of protein, total carbohydrate, freereducing substances, total lipid, phospholipid and RNA levels in marine invertebrate larvae is described and discussed. The scheme is designed for use with 1–2 mg dry weight of tissue. Values of 171·0, 15·03, 50·4 and 11·58 μg/mg dry weight of larvae (flesh + shell) are given for the levels of protein, total carbohydrate, total lipid and RNA respectively, in newly released larvae of Ostrea edulis L.
Larval development of the thoracican cirripede Balanus eburneus is invariant, consisting of six naupliar instars and a terminal nonfeeding cypris instar. In order to elucidate determinants of its fixed instar molting pattern we tested the following hypotheses: (1) the rate of morphogenesis is correlated with the rate of molting; (2) the timing of the morphogenetic molt to the cyprid is time (age) dependent; and (3) initiation of the molt to the cyprid is dependent upon the accumulation of a minimum amount of energy reserves. Naupliar food supply was manipulated in order to vary rates of molting and accumulation of energy reserves. Total oil cell volume per larva was used to nondestructively estimate energy reserve level.
Compound eye development and thoracic appendage development during the six naupliar instar were confined to specific phases of the molt cycle. Suspension of the molt cycle resulted in suspension of morphological development. Initiation of the molt to the cyprid was neither time dependent nor a function of larval oil cell volume. However, the rate of passage through the molt cycle increased abruptly in larvae having an oil cell volume greater than 4–6 × 104 μm3. Nauplii entering the final phase of the molt cycle (D2–4) would attempt to complete development to the cyprid irrespective of their oil cell volume. Correlations between cypris oil cell volume and cypris metamorphic success implied that the naupliar oil cell volume “threshold” of 4–6 × 104 μ3 represented the amount of energy reserves needed to complete covert developmental events rendering the cyprid capable of successfully metamorphosing to the juvenile.
These results suggest that molt cycle stage-specific morphogenesis and growth (energy reserve accumulation) are important determinants of the fixed instar molting of B. eburneus larvae. Comparisons with studies of larval crustaceans which vary instar number indicate (1) greater independence between the processes of molting and morphogenesis among species with a variable instar molting pattern and also that (2) growth is an important determinant of each type of molting pattern.
The larvae of the intertidal barnacle Elminius modestus Darwin were reared using six different feeding regimes comprising a large and/or a small flagellate fed to the larvae at different times during the course of their development. The relative value of the feeding regimes was ascertained by using the rate of development, survival, and size attained by the larvae as a measure of success or failure. The best feeding regime was found to be that providing a unialgal diet of the small flagellate initially followed by a unialgal diet of the large flagellate in later stages of development, while the reverse situation gave the worst results. The increase in mesh size of the antennal filter during growth of the nauplii is suggested as a reason for the varying success of feeding regimes employing foods of different sizes during development. This is seen as confirmation of the idea that cirriped nauplii collect their food by means of filtering appendages rather than by localized currents alone.
Summary1. In analysing the ecological conditions of an animal population we have above all to focus our attention upon the most sensitive stages within the life cycle of the animal, that is, the period of breeding and larval development.2. Most animal populations on the sea bottom maintain the qualitatively composition of the species composing them, over long periods of time, though the individual species use quite different modes of reproduction and development. This shows that species producing a large number of eggs have a larger wastage of eggs and larvae than those with only a few eggs. The wastage of eggs in the sea is much larger than on the land and in fresh water.3. In the invertebrate populations on the level sea bottom, large fluctuations in numbers from year to year indicate species with a long pelagic larval life, while a more or less constant occurrence indicates species with a very short pelagic life or a non-pelagic development.4. In most marine invertebrates which shed their eggs and sperm freely in the water, either (a) the males are the first to spawn, thus stimulating the females to shed their eggs, or (b) an ‘epidemic spawning’ of a whole population takes place within a few hours. Both methods greatly favour the possibility of fertilization of the eggs spawned and show that the heavy wastage of eggs and larvae takes place after fertilization, during the free swimming pelagic life.5. Embryos with a non-pelagic development may originate (a) from large yolky eggs, in which case all the hatching young of the same species will be at the same stage of development, or (b) from small eggs which during their development feed on nurse eggs, when the individual embryos of the same species may vary enormously in size at the stage of hatching.6. Three types of pelagic larvae are known: (a) Lecithotrophic larvae, originating from large yolky eggs spawned in small numbers by the individual mother animals; they are independent of the plankton as a source of food although growing during pelagic life, are absent from high arctic seas but constitute about 1o% of the species with pelagic larvae in all other seas, (b) The planktotrophic larvae with a long pelagic life, originating from small eggs spawned in huge numbers by the individual mother animal; they feed from, and grow in, the plankton, constituting less than 5% of high arctic bottom invertebrates, 55–65% of the species in boreal seas, and 8o-85 % of the tropical species, (c) The planktotrophic larvae with a short pelagic life having the same size and organization at the moment of hatching and at the moment of settling; these constitute about 5% of the species in all Recent seas.7. To find out the factors which cause the enormous waste of eggs and larvae, we thus have to study those forms (constituting 7o% of all species of bottom invertebrates in Recent seas) which have a long planktotrophic pelagic life, as only species reproducing in this way have really large numbers of eggs.8. The food requirements of the planktotrophic pelagic larvae are much greater than those of the adult animals at the bottom. The adaptability of the larvae to poor food conditions seems, nevertheless, to be greater than hitherto believed. The significance of starvation seems mainly to be an indirect one: poor food conditions cause slow growth, prolong larval life, and give the enemies a longer interval of time to attack and eat the larvae.9. At the temperatures to which they are normally exposed, northern as well as tropical larvae seem on an average to spend a similar time (about 3 weeks) in the plankton. The length of the pelagic life of the individual species may, however, vary significantly in nature. In the Sound (Denmark) the larvae are never exposed to temperatures outside the range which they are able to endure. The wastage caused by temperature, like that due to starvation, seems mainly to be an indirect one: low temperatures postpone growth and metamorphosis, and give the enemies a longer time to feed on the larvae.1o. When a larva feeding on a pure algal diet metamorphoses into a carnivorous bottom stage, a ‘physiological revolution’ occurs and a huge waste of larvae might be expected. Experiments have, however, shown that this is not the case.11. Young pelagic larvae are photopositive and crowd near the surface; larvae about to metamorphose are photonegative. Larval polychaetes, echinoderms, and presumably also prosobranchs, may prolong their pelagic life for days or weeks until they find a suitable substratum. Forced towards the bottom by their photonegativity and transported by currents over wide bottom areas, testing the substratum at intervals, their chance of finding a suitable place for settling is much better than hitherto believed.12. Continuous currents from the continental shelf towards the open ocean may transport larvae from the coast to the deep sea where they will perish. Such conditions may (for instance in the Gulf of Guinea) deeply influence the composition of the fauna, while in other areas (European western coast, southern California) they seem to be only of small significance.13. The toll levied by enemies appears to be the most essential source of waste among the larvae. A list of such enemies, comprising other pelagic larvae, holoplank-tonic animals and bottom animals, is given on p. 2o. A medium-sized Mytilus edulis, filtering 1–4 1. of water per hour, may retain and kill about 100,000 pelagic lamellibranch larvae in 24 hr. during the maximum breeding season in a Danish fjord.14. Species reproducing in a vegetative way, by fission, laceration, budding, etc., might be expected to have good chances of competition in such areas where conditions for sexual reproduction are unfavourable. Nevertheless, they only supply a rather small percentage of the animal populations of all Recent seas, probably because their intensity of reproduction is low and because they are unable to spread to new areas. Most forms reproducing in a vegetative way have sexual reproduction as well.15. Pelagic development is nearly or totally suspended in the deep sea, and is restricted to the shelf faunas. In the arctic and antarctic seas pelagic development is nearly or totally suppressed, even in the shelf faunas, but starting from here the percentage of forms with pelagic larvae gradually increases as we pass into warmer water, reaching its summit on the tropic shelves.16. In order to survive in high arctic areas a planktotrophic, pelagic larva has to complete its development from hatching to metamorphosis within I–I ½ months (i.e. the period during which phytoplankton production takes place) at a temperature below 2–4o C. Most larvae, that is in 95% of the species, are unable to do so and have a non-pelagic development, but if a pelagic larva is able to develop under these severe conditions the planktotrophic pelagic life seems to afford good opportunities even in the Arctic. Thus the 5 % of arctic invertebrates reproducing in this way comprise several of the species which quantitatively are most common within the area.17. The antarctic shore fauna has poor conditions similar to those of the Arctic. The longest continuous periods of phytoplankton production are 2 and 3 weeks respectively, and pelagic larvae have, in order to survive, to complete their development within this short space of time at a temperature between 1 and 4o C. Accordingly, non-pelagic development is the rule, but most arctic species are able to support their non-pelagic development by means of much smaller eggs than the antarctic species, where brood protection and viviparity is dominant. The antarctic fauna has apparently had a longer time to develop its tendency to abandon a pelagic life. The greater the size of the individual born, the smaller its relative food requirements and the better its chance of competing under poor food conditions.18. The relatively few data on reproduction in deep sea invertebrates point to a non-pelagic development. The larvae of such forms, in order to develop through a planktotrophic pelagic stage, would have to rise by the aid of their own locomotory organs through a water column 2000–4000 m. high or more (often with counteracting currents) to the food producing surface layer, and to cover the same distance when descending to metamorphose and settle.19. The ecological features common to the deep sea, the arctic and the antarctic seas, which enable the same animals to live and to reproduce there, contribute to explain the ‘equatorial submergence’ of many arctic and antarctic coastal forms.20. In the tropical coastal zones where the percentage of species with pelagic larvae reaches its maximum, the production of food for the larvae takes place much more continuously than in temperate and arctic seas, because light conditions enable the phytoplankton to assimilate all the year round. The tropical species of marine invertebrates breed (in contrast to temperate and arctic species) within such different seasons that their larval stock, taken as a whole, is more or less equally distributed in the plankton all the year round. This makes the competition in the plankton less keen.21. The fact that a mode of reproduction and development, well fit for an arctic area, is unfit in a temperate or tropical area of the sea is probably one of the main reasons for the restricted distribution of species.22. In most groups of marine invertebrates the individual species have only one mode of reproduction and development, which accordingly restricts their area of distribution. In the polychaetes, however, the individual species often show an astonishing lability in their mode of reproduction and development which enables them to compete in wide areas of the sea. Thus, out of the Western European species of polychaetes, 28-4% have been found also in the Indian Ocean, and 18%, at least, along the Californian coast, while the corresponding number of Western European echinoderms, prosobranchs and lamellibranchs found also in the Indian Ocean and California amounts to less than 2%.23. The pelagic or non-pelagic development of marine prosobranchs has proved to be a very fine ‘barometer’ for ecological conditions. Recent observations, still not elaborated, seem to indicate that the shape of the top whorls, the apex, of the adult shells of prosobranchs may show whether the species in question has a pelagic or a non-pelagic development. This discovery may also give us valuable information about the larval development in fossil species, and help us to form an idea about ecological conditions in sea areas from earlier geological periods.
We present several models concerning the short term consequences of spreading offspring in varying environments. Our goal is to determine what patterns of spatial and temporal variation yield an advantage to increasing scale of dispersal. Of necessity, the models are somewhat artificial but we feel they are a reasonable approximation of and hence generalizable to natural systems. With these models we examine consequences of dispersal arising from environmental variation: increased environmental variance, different degrees of spatial and temporal correlation, some arbitrary spatial patterns of favorability and finally some patterns derived from long-term, large-scale weather data collected along a contiguous stretch of coastline from southern Oregon to northern Washington (USA). We examine the costs and benefits of increasing sclae of dispersal in both density dependent and density independent models.
Several conclusions may be drawn from the results of these models. In the absence of any spatial or temporal order to favorability (where favorability is directly proportional to either fitness or carrying capacity) increasing scale of spread produces a higher tate of population increase. At larger scales, though, an asymptote of maximum relative advantage is approached, so each added increment of spread has a smaller contribution to fitness. This asymptote is higher and the approach to it relatively slower with increasing environmental variance. For a given environmental variance, increasing spatial correlation results in a slower approach to the same asymptote. In density independent models, increasing temporal correlation of fitness selects against increased dispersal if expected differences between sites are sufficiently great relative to variation within sites; but in this instance, density dependence yields a somewhat different result: dispersers have a refuge at sites of low carrying capacity or sites lacking non-dispersers. Finally, optimum intermediate scales of dispersal can occur where differences in expected fitness increase with increasing distance from the parental site, such as in a gradient, but where the environmental variation at a given site is fairly large relative to differences in expected fitness between adjacent sites.
The foregoing results are extended for the following predictions. When greater longevity in a resistant phase of the life cycle reduces temporal variation in survival and fecundity, increased generation time should decrease the benefits of spreading offspring in an environment that would otherwise favor spread and could either increase or decrease the costs of spreading offspring in an environment selecting against spread. We speculate that if large scale patterns of varying survival and fecundity are similar to the variation in the physical environment which we examined with weather data, there should be little or no short term advantage to large scale spread of offspring (on the order of 50 kilometers or more) because expected differences increase and seldom if ever decrease with increasing distance between sites.
This suggests that feeding larvae of benthic invertebrates with their concomitant long planktonic period, receive little if any advantage from increased scale of dispersal, and consequently that the advantages to planktotrophy over lecithotrophy must lie in other life history aspects, such as the ability to produce a greater number of smaller eggs.
We tested the hypothesis that larval size in the acorn barnacle Balanus eburneus Gould (Cirripedia Thoracica) varies in relation to food availability. In March–November 1980, and March–July 1981, larvae were obtained from adult Balanus eburneus collected in the Newport River, North Carolina, USA. Carapace length and width of larvae reared at three different food concentrations were measured. Mean naupliar instar size was independent of food concentration. Mean size of the cypris instar increased with increasing food level. Greater cypris size could be attributed to increased food reserves in the preceding naupliar stage, and was coinciden with inmarked increase in metamorphic success. Variation in instar size remained constant or declined during naupliar development, but increased sharply at the molt to the cyprid. Naupliar size regulation involved: (1) conservation of a molt increment specific for each naupliar-naupliar molt, (2) an inverse relationship between premolt size and the molt increment during the first five naupliar instars, and (3) an increase in the precision of the molt increment at the molt to the sixth naupliar instar. Experimental evidence implies that size regulation in Balanus eburneus limits variation about a fixed final naupliar size (e.g. volume). Measurement of naupliar size, accumulated energy reserves, survival and development time, and cypris metamorphic success indicated that naupliar cuticular growth is the most conservative feature of larval development. The data suggest that maximum naupliar size is limited by escalating metabolic costs during development, while minimum naupliar size is limited by size-related feeding effectiveness.
Analysis of biochemical components and measurements of oxygen consumption rates of cypris larvae of Balanus balanoides (L.) maintained in the laboratory at 10C for up to 5 weeks after capture shows that lipid is the primary energy reserve, although later protein is utilised. Initially, the cyprids swim freely with an oxygen consumption rate of ca. 3710-3 l O2 h-1 cyprid-1, but within a few days the rate falls to ca. 2110-3 l O2 h-1 cyprid-1 when they cease swimming and explore the substratum. The cost of metamorphosis was calculated both from the loss of biochemical components and oxygen consumption rates during metamorphosis; the values were 2.810-2 and 3.210-2 cal cyprid-1, respectively. A budget was collated from the data on respiration and biochemical composition, whereby the energy per cyprid was partitioned into that required for essential structural components (6.810-2 cal), that needed for metamorphosis (3.010-2 cal) and an excess available for swimming and exploring, which in the batches studied was about 5.010-2 cal. This excess is mainly derived from the utilisation of lipid reserves and is used up usually 2 1/2 to 4 weeks after capture. During these measurements, samples of cyprids were taken at weekly intervals to test the rate of settlement and success of metamorphosis. The results showed that they lose their competence to metamorphose successfully approximately at the same time (3 to 4 weeks) that the energy supply for swimming and exploration is used up.
In prior studies, critical points have been found in the interaction between exogenous (food) and endogenous (hormonal) control of the larval development of decapod crustaceans. One of them was termed “point of reserve saturation” (PRS). If it has been passed under conditions of sufficient availability of food, decapod larvae may complete their moulting cycle and develop, independent of food, to the next instar. In the present investigation the PRS and the moulting cycle were studied simultaneously in first instar larvae of nine decapod species belonging to eight families and four higher taxa (Caridea, Macrura, Anomura, and Brachyura). The experimental results suggest that the PRS was in general near the transition between stages C and D0 of Drach's classification system, independent of the species, instar duration, and temperature. When temperature was kept constant throughout the experiment, the critical point was reached after one third to one half of total time of first instar development. If postmoult and intermoult (stages A–C) were prolonged by lower initial temperature, the PRS was delayed but found again near the transition. If starvation began before the PRS, the reserves accumulated from food did not allow successful development to the second instar. Depending on the time of initial feeding, the moulting cycle was arrested at one of the two following critical points
(i) Varied origins of larval forms and metamorphoses are indicated by comparisons among extant animals. (ii) Size-specific and stage-specific constraints on survival and growth may result in distinctive larval traits, but to explain larval origins, size- or stage-specific advantages must be extrapolated to ancient environments and ancestral traits. Adaptations for habitat selection or dispersal do not account for evolution of long precompetent periods of larval feeding and growth or for larvae in holoplanktonic life histories. (iii) Transverse bands of cilia on ridges or posterior edges of larvae meet a common functional requirement for propulsion, are expected to be convergently similar, and may have arisen numerous times. (iv) Biases imposed by ancestral larval or juvenile traits might result in convergent similarity of derived larval traits with a result resembling homology. (v) Some extant feeding larvae persist with unusually simple structures or low performance. These larvae suggest possible intermediate steps in the evolution of feeding larvae. (vi) Direction of evolutionary transitions of larval traits are indicated by distribution of traits within clades and by vestigial structures. Feeding larval stages have been lost often and gained rarely. (vii) Most types of feeding larvae evolved at most once, are in clades that diverged early, and are therefore of ancient origin. Other evidences of antiquity are fossil traces of larval molluscs and brachiopods from the Ordovician and fossils of crustacean nauplii from the Upper Cambrian. (viii) Inferred combinations of ancestral traits can differ from combinations known from extant descendants. Examples are external fertilization combined with a feeding larva or small adult size. (ix) In some clades, feeding larval forms that originated earlier may be associated with small parental investment per offspring. (x) Unreliable rules for evolutionary inferences include the assumptions that primitive traits are correlated in extant animals, that evolution proceeds from simple to complex structures, that earlier stages in development are more conservative, and that structures that develop earlier evolved earlier.
On Oregon coastal rocky shores, filter-feeders were relatively abundant and macrophytes were relatively scarce at Strawberry Hill, whereas opposite abundance patterns occurred at Boiler Bay. To determine whether nearshore oceanographic differences were associated with these patterns, we made shore-based measurements of nutrient and Chl a concentrations. We used a three-level nested design to identify ecologically appropriate sampling scales: “site” (10s of km), “bench” nested within site (100s of m), and “location” nested within bench (10s of m). Nutrients varied inconsistently but Chl a was consistently higher at Strawberry Hill. For Chl a, site explained ~70% of the variance, whereas bench and location explained <20%. For nutrients, site and bench explained most of the variance, but neither was consistently more important. The data tentatively suggest that nutrient levels are weakly related to the between-site ecological differences. In addition to the between-site differences, Chl a changed seasonally, with maximum levels in summer. For nutrients, temporal changes were more complex, with highest levels tending to occur in late summer and autumn. No nutrient, however, was scarce enough at either site to limit phytoplankton growth, with the possible exception of nitrate in June. These results were consistent with the hypothesis that nearshore phytoplankton standing stock, a bottom-up factor, could underlie differences in rocky intertidal community structure. National Science Foundation grants OCE92-17459 to B.A.M., and P.A.W. and P.T.S. Andrew W. Mellon Foundation grants to B.A.M. and J. Lubchenco. Fellowship from John Simon Guggenheim Memorial Foundation (B.A.M.).