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Facultative planktotrophy in the tropical echinoid Clypeaster rosaceus (Linnaeus) and a comparison with obligate planktotrophy in Clypeaster subdepressus (Gray) (Clypeasteroida: Echinoidea)
Abstract
Larval development to metamorphosis and early juvenile growth and survivorship were examined in Clypeaster subdepressus (Gray) and C. rosaceus (Linnaeus). C. subdepressus has an obligatorily planktotrophic larva that metamorphoses after 16 to 28 days at 27°C. The larva of C. rosaceus can, but need not feed prior to metamorphosis, which occurs after 5 to 7 days at 27°C. Feeding by larvae of C. rosaceus does not change the time to metamorphosis but does increase size at metamorphosis, early juvenile growth and may increase juvenile survivorship relative to unfed larvae. Size at metamorphosis increases in larvae of C. rosaceus that feed for several days after they are competent to metamorphose, but there may be a limit to this increase because the condition of the rudiment degenerates after a period of time. The development of C. rosaceus may represent a transition between planktotrophy and lecithotrophy. This intermediate state has advantages for the juvenile stage that are not included in the trade of fecundity against risk to offspring usually considered in life history discussions of developmental mode of marine invertebrates.
... An intermediate pattern known as facultative planktotrophy (Chia, 1974;Emlet, 1986;Vance, 1973a), where larvae are not only capable of feeding in the plankton but can also complete metamorphosis without food, is a rare but persistent mode of development that has been observed at least eight times across several marine invertebrate taxa (Table 1; see also Allen & Pernet, 2007). Facultative planktotrophy is often considered an intermediate mode of development in the evolutionary transition between feeding and nonfeeding larvae, but whether or not intermediate modes can maximize reproductive success over evolutionary timescales is still up for debate (Christiansen & Fenchel, 1979;Levitan, 2000;McEdward, 1997;Vance, 1973aVance, , 1973b. ...
... In facultative planktotrophs, larval feeding resulted in larger juveniles in echinoderms (Allen & Podolsky, 2007;Emlet, 1986;Hart, 1996) and gastropods (Kempf & Hadfield, 1985;Miller, 1993). Juvenile size is an important life history characteristic because larger juveniles tend to exhibit higher survival, growth, reproduction, and longevity across several species (Marshall et al., 2018). ...
... The availability of food for larvae does not always decrease time to metamorphosis in facultative planktotrophs, For example, there was no difference between fed and unfed treatments in the echinoid Clypeaster rosaceus or the gastropods Conus pennaceus and Phestilla sibogae (Emlet, 1986;Kempf & Hadfield, 1985;Perron, 1981). In the ophiuroid Macrophiothtrix rhabdota, planktonic duration was decreased in the presence of food (Allen & Podolsky, 2007). ...
Most marine invertebrate larvae either obligately feed or depend on maternally provided reserves during planktonic development. A small number of species have the capacity to do both, in a mode of development known as facultative planktotrophy. We describe facultative feeding in a larva from the Oregon coast, and identify it as being an undescribed species in the genus Amphiodia, which we refer to as Amphiodia sp. opaque. We quantified the effects of food on larval and juvenile quality by culturing larvae, collected as embryos, with and without microalgal food at 15°C. The resulting juveniles were monitored under conditions of starvation. A cohort of juveniles of larvae caught as plankton was subjected to the same starvation treatment for comparison with our laboratory-reared larvae. We observed benefits to offspring that received food: larvae provided with microalgae developed more quickly and metamorphosed at higher rates. Furthermore, juveniles resulting from fed larvae were larger and were able to avoid starvation for longer after metamorphosis. Our results varied across two experimental years, suggesting that provisions provided by parents vary between populations and years. Juveniles from planktonic larvae exhibited sizes not statistically different from larvae cultured in the absence of food, but died from starvation more quickly.
... There are a handful of intermediate larval types between these two extreme modes, which have proven invaluable for understanding the speed, manner, and order in which developmental changes occur during the evolution of non-feeding forms [26,[28][29][30]. The sea biscuit Clypeaster rosaceus is perhaps the best-studied echinoderm with an intermediate larval type [27,[31][32][33]. Like obligate planktotrophs, including its closely related congener C. subdepressus, C. rosaceus larvae develop through a pluteus larval form with functioning feeding structures [31]. ...
... The sea biscuit Clypeaster rosaceus is perhaps the best-studied echinoderm with an intermediate larval type [27,[31][32][33]. Like obligate planktotrophs, including its closely related congener C. subdepressus, C. rosaceus larvae develop through a pluteus larval form with functioning feeding structures [31]. However, unlike obligately planktotrophic larvae, C. rosaceus larvae develop from large eggs, can complete metamorphosis without feeding [33] and develop in under a week, as opposed to the three weeks C. subdepressus takes [31,34]. ...
... Like obligate planktotrophs, including its closely related congener C. subdepressus, C. rosaceus larvae develop through a pluteus larval form with functioning feeding structures [31]. However, unlike obligately planktotrophic larvae, C. rosaceus larvae develop from large eggs, can complete metamorphosis without feeding [33] and develop in under a week, as opposed to the three weeks C. subdepressus takes [31,34]. Furthermore, C. rosaceus larvae begin forming structures that develop into a juvenile shortly after gastrulation, like species with non-feeding development, but unlike species with obligately feeding larvae that typically do not produce juvenile structures until late larval stages [26]. ...
Background:
Larval developmental patterns are extremely varied both between and within phyla, however the genetic mechanisms leading to this diversification are poorly understood. We assembled and compared the developmental transcriptomes for two sea biscuit species (Echinodermata: Echinoidea) with differing patterns of larval development, to provide a resource for investigating the evolution of alternate life cycles. One species (Clypeaster subdepressus) develops via an obligately feeding larva which metamorphoses 3-4 weeks after fertilization; the other (Clypeaster rosaceus) develops via a rare, intermediate larval type-facultative feeding- and can develop through metamorphosis entirely based on egg provisioning in under one week.
Results:
Overall, the two transcriptomes are highly similar, containing largely orthologous contigs with similar functional annotation. However, we found distinct differences in gene expression patterns between the two species. Larvae from C. rosaceus, the facultative planktotroph, turned genes on at earlier stages and had less differentiation in gene expression between larval stages, whereas, C. subdepressus showed a higher degree of stage-specific gene expression.
Conclusion:
This study is the first genetic analysis of a species with facultatively feeding larvae. Our results are consistent with known developmental differences between the larval types and raise the question of whether earlier onset of developmental genes is a key step in the evolution of a reduced larval period. By publishing a transcriptome for this rare, intermediate, larval type, this study adds developmental breadth to the current genetic resources, which will provide a valuable tool for future research on echinoderm development as well as studies on the evolution of development in general.
... Nonfeeding larvae have evolved from feeding larvae many times within the echinoderms, hemichordates, lophophorates, polychaetes, gastropods, bivalves, crustaceans, and other taxa (Strathmann 1978). Among the echinoids (sea urchins and their relatives) in particular, nonfeeding larvae have evolved at least 15 times (Emlet et al. 1987;Emlet 1990;R. Emlet pers. ...
... comm., 1992). This transition has demographic (McMillan et al. 1992), ecological (Menge 1975;Perron 1981;Emlet 1986), and macroevolutionary (Hansen 1980;Jablonski 1986) consequences. Alterations in development provide the mechanism for many types of morphological evolution (Bonner 1982;Raff and Kaufman 1983;Raff and Raff 1987). ...
... The transition to nonfeeding larval development is poorly understood because the supposed intermediate form (a facultatively feeding larva that is able to feed but develops from such large eggs that it can complete development without food) is rare. One echinoderm (Emlet 1986), four gastropods (Perron 1981;Kempf and Hadfield 1985;Kempf and Todd 1989), a bivalve (Alatalo et al. 1984), and a toad (Crump 1989) are known to develop in this way, and a small number of other species may also develop as facultative feeders (Kempf and Hadfield 1985;Strathmann 1985;Emlet 1986;G. Eckert, pers. ...
Species with large eggs and nonfeeding larvae have evolved many times from ancestors with smaller eggs and feeding larvae in numerous groups of aquatic invertebrates and amphibians. This change in reproductive allocation and larval form is often accompanied by dramatic changes in development. Little is known of this transformation because the intermediate form (a facultatively feeding larva) is rare. Knowledge of facultatively feeding larvae may help explain the conditions under which nonfeeding larvae evolve. Two hypotheses concerning the evolutionary loss of larval feeding are as follows: (1) large eggs evolve before modifications in larval development, and (2) the intermediate form (facultatively feeding larva) is evolutionarily short-lived. I show that larvae of a heart urchin, Brisaster latifrons, are capable of feeding but do not require food to complete larval development. Food for larvae appears to have little effect on larval growth and development. The development, form, and suspension feeding mechanism of these larvae are similar to those of obligate-feeding larvae of other echinoids. Feeding rates of Brisaster larvae are similar to cooccurring, obligate-feeding echinoid larvae but are low relative to the large size of Brisaster larvae. The comparison shows that in Brisaster large egg size, independence from larval food, and relatively low feeding rate have evolved before the heterochronies and modified developmental mechanisms common in nonfeeding echinoid larvae. If it is general, the result suggests that hypotheses concerning the origin of nonfeeding larval development should be based on ecological factors that affect natural selection for large eggs, rather than on the evolution of heterochronies and developmental novelties in particular clades. I also discuss alternative hypotheses concerning the evolutionary persistence of facultative larval feeding as a reproductive strategy. These hypotheses could be tested against a phylogenetic hypothesis.
... Nonfeeding larvae are also considered to be derived from feeding ones. The present diversity of developmental types in a variety of clades reflects the switch to nonfeeding larvae that has occurred independently several times (Strathmann 1974;Emlet 1990). The evolution to non feeding larvae is generally accompanied by a major reduction or loss of the larval structures required for feeding and is also considered to be irreversible ( Strathmann 1974Strathmann , 1978a). ...
... The evolution to non feeding larvae is generally accompanied by a major reduction or loss of the larval structures required for feeding and is also considered to be irreversible ( Strathmann 1974Strathmann , 1978a). In some echinoid lineages, existing intermediate forms between planktotrophic and lecithotrophic larvae (Emlet 1986;Raff 1987;Olson et al. 1993) support this evolutionary scheme of the larval stage in echinoids. However Lacalli (1993), even if his work supports this idea, pointed out that a number of unresolved questions remain and that the alternative hypothesis considering the nonfeeding larvae as primitive (Grave 1903) cannot be excluded. ...
... Stars represent the existence of brooding species in the clade (after Emlet et al. 1987;Raff 1987). of nonpelagic lecithotrophic development. Brood-protecting development occurs in about 20% of total echinoid species and has arisen independently in at least seven clades (Fig. 1, see also Strathmann 1978a;Emlet et al. 1987;Raff 1987). This happened at least three times in antarctic echinoids (Table 1). ...
Marine invertebrates display a great variety of life-history traits and reproductive strategies. In echinoids, four patterns of larval development are generally recognized: planktotrophy, pelagic lecithotrophy, bottom dwelling, and brood protecting. Each broad type of free and protected development is found in all the oceans, but comparisons of the principal reproductive modes between different geographic regions have shown that they are not equally distributed. Frequency of pelagic development (planktotrophic and lecithotrophic) decreases from equator to Antarctic, where brood protecting becomes dominant. Numerous theories have been proposed to explain the richness of nonpelagic development in most marine invertebrates within the Southern Ocean. These theories can be grouped into three categories: (1) larval survival, where selection acts on larval; (2) energy allocation; and (3) dispersal. All of them consider the adaptative significance of brood protecting as the key to the success of this strategy in the Antarctic. However, the adaptative significance of brooding and the evolutionary success of this strategy in the Antarctic must be considered as two separate questions. To consider the problem at an evolutionary level, we have examined the consequences of different reproductive strategies on the genetic structure of species and on the long-term evolution of the clade. We examine this problem in the case of echinoids, a clade particularly well suited to addressing this question. In echinoids, the reduction of larval-stage duration is associated with a decrease in gene flow and consequently in the geographical scale of genetic differentiation. This allows us to reconsider the high-speciation-rate model, which leads to an increase in the number of low-dispersal species (isolation by distance). This model, previously tested by means of fossils is not satisfactory in living echinoids. Thus, the model is rebuilt with the addition of differential extinction rate between planktotrophic and brooding species in relation with the climatic history of the Antarctic.
... Можно предположить, что известные у иглокожих экзотрофные личинки с коротким периодом развития [72] развиваются из ооцитов с повышенным содержанием запасных веществ, демонстрируя начальный этап приобретения эндотрофии. Следующим этапом является факультативная планктотрофия, известная, например, у морских ежей Clypeaster rosaceus и Brisaster latifrons и голожаберного моллюска Phestilla sibogae [35,49,63,88,134,196,200]. Самки из атлантической популяции полихеты Streblospio benedicti формируют два типа яиц (мелкие и крупные), из которых развиваются планктотрофные и факультативные планктотрофные личинки соответственно. ...
... также [198,200]). Другой взгляд на таких личинок рассматривается в работах Эмлета [49], МакЭдварда [101] и Аллена и Перне [13]. Так или иначе, но с того момента, когда количество предоставляемых материнским организмом веществ и энергии стало полностью обеспечивать потребности развивающейся личинки, необходимость в структурах, обеспечивающих ее автономное питание (поимку пищевых частиц и их переваривание), отпала (см. ...
... Другим объяснением, является предположение, что их редкость связана с относительной непродолжительностью «эволюционного существования»: они либо должны дать начало непитающейся личинке, либо вымереть [200]. Напротив, Эмлет [49] считает, что факультативно планктотрофные личинки могут быть эволюционно стабильными, поскольку они способны пользоваться «бонусами», предоставляемыми обоими вариантами строения и физиологии (подробно обсуждается в работе Харта [63]). Так или иначе, именно факультативная планктотрофия (которая, по данным ряда исследователей, распространена шире, чем считается) показывает, каким образом осуществлялся переход от одного состояния к другому [13,49,88,101]. ...
The review addresses hypotheses on the transition from planktotrophic to lecithotrophic larvae in different groups of marine invertebrates. Using gymnolaemate bryozoans as an example, a sequence of events that could accompany this transition has been reconstructed to show that changes in oogenesis are likely to be of major importance. An association between the acquisition of non-feeding larva and the origin of brooding in Gymnolaemata is suggested. It is proposed that numerous independent origins of lecithotrophy occured in this group. The extrinsic factors and environmental background of the Upper Cretaceous radiation of the gymnolaemate order Cheilostomata are discussed.
В обзоре анализируются гипотезы о переходе от планктотрофных к лецитотрофным личинкам в различных группах морс-ких беспозвоночных организмов. Последовательность событий перехода реконструирована на примере морских мшанок Gymnolaemata. Приведены свидетельства в пользу того, что в основе отказа от планктотрофии лежит изменение типа оогенеза. Показана связь между потерей способности к питанию у личинок и возникновением вынашивания, выдвинуто пред-положение о неоднократном возникновении лецитотрофии у гимнолемат. Рассмотрены внешние условия, на фоне которых осуществлялась позднемеловая радиация гимнолемного отряда Cheilostomata. Ключевые слова: планктотрофия, лецитотрофия, личинки, эволюция, Bryozoa. The review addresses hypotheses on the transition from planktotrophic to lecithotrophic larvae in different groups of marine invertebrates. Using gymnolaemate bryozoans as an example, a sequence of events that could accompany this transition has been reconstructed to show that changes in oogenesis are likely to be of major importance. An association between the acquisition of non-feeding larva and the origin of brooding in Gymnolaemata is suggested. It is proposed that numerous independent origins of lecithotrophy occured in this group. The extrinsic factors and environmental background of the Upper Cretaceous radiation of the gymnolaemate order Cheilostomata are discussed.
... It is also possible that their apparent rarity (as the consequence of a relatively short evolutionary existence) is because such species either give rise to species with non-feeding larvae or become extinct (Wray and Raff 1991 ). Conversely, Emlet ( 1986 ) thought that facultative planktotrophy may be stable from an evolutionary viewpoint, as such larvae may profi t from the positive attributes of both developmental variants (Emlet et al. 1987 ;Havenhand 1995 ;McEdward 1997 ;Allen and Pernet 2007 ; for a detailed discussion see Hart 1996 ). Wray ( 1996 ) remarked that such larvae are effi cacious only under quite specifi c conditions. ...
... Wray ( 1996 ) remarked that such larvae are effi cacious only under quite specifi c conditions. Whatever the case, it is facultative planktotrophy (which according to some researchers is more common than generally thought) that illustrates the transition from one state to the other (Kempf and Hadfi eld 1985 ;Emlet 1986 ;McEdward 1996McEdward , 1997Allen and Pernet 2007 ). ...
... Among invertebrates, facultative planktotrophy is known in two sea urchins, four gastropods, a bivalve and a polychaete (Perron 1981 ;Alatalo et al. 1984 ;Kempf and Hadfi eld 1985 ;Emlet 1986 ;Kempf and Todd 1989 ;Miller 1993 ;Hart 1996 ;Pernet and McArthur 2006 ;reviewed in Wray and Raff 1991 ;Havenhand 1995 ;Wray 1995a ;Raff 1996 ;Hadfi eld and Strathmann 1996 ). For instance, females of the polychaete Streblospio benedicti (Atlantic population) form two types of eggs (small and large), from which, correspondingly, planktotrophic and facultatively planktotrophic larvae develop. ...
This chapter contains an analysis of the main directions in the evolution of sexual reproduction in bryozoans – changes in modes of oogenesis and fertilization, the transition from plank-totrophy to a non-feeding larva and its consequences, the origin of embryo incubation, and the repeated evolution of matrotrophy and placental analogues. The trends that emerge from this analysis are compared with reproductive analogues in the evolution of the bryozoan order Ctenostomata as well as other marine invertebrate groups (predominantly echino-derms, molluscs and polychaetes). The conditions under which the cheilostomes radiated in the Late Cretaceous are considered in detail, and the consequences of the transitions to new reproductive patterns are analyzed. It is suggested that a shift in oogenesis (reduction in egg number and increase in their size) and parental care can apparently evolve in Cheilostomata sequentially, with a short time lag: oogenesis becomes modifi ed fi rst, with the decrease in the number of offspring compensated soon after by the origin of brooding. Finally, the stages in the evolution of sexual reproduction in other bryozoan groups (classes Phylactolaemata and Stenolaemata) are reconstructed. Keywords Brooding • Evolution • Fertilization • Lecithotrophy • Oogenesis • Placentotrophy • Planktotrophy
... Prediction from equation (5) (from Vance 1973b) with , , , and m = 0.8 p = 70 ഞ = 35 (from Havenhand 1995). Echinoids eggs at a size of 280 mm can C = 1 be facultative feeders (Emlet 1986) and are here considered to have ; the theoretical and empirical scales are adjusted accordingly. Al-s = 1 though different parameter values alter the predicted estimates quantitatively, local optima at 0 and 280 mm ( and 1) are always predicted. ...
... Planktonic mortality (Rumrill 1990), food availability (Strathmann 1987b;Olson and Olson 1989;Fenaux et al. 1994), water temperature (Emlet et al. 1987;Emlet 1995), and fertilization rates (Levitan 1995;Levitan and Petersen 1995) have been shown to influence either development time or the survivorship of eggs and larvae. Below, I model the effect of each of these factors on egg size and compare the sensitivities of the factors over a fivefold range typical of natural variation noted in the field. ...
... Fertilization success was inserted into the model as Variation in Water Temperature. Development time in echinoids is inversely related to water temperature (Emlet et al. 1987;Strathmann 1987b;Emlet 1995). Assuming a Q 10 value of 3 (Emlet 1995), I calculated the adjusted developmental rates (T 2 ) over a range of typical seawater temperatures using the formula ...
Life‐history models for marine invertebrate larvae generally predict a dichotomy in egg size in different species: eggs should be either minimal in size or large enough to support development fully without larval feeding. This prediction is contradicted, however, by the empirical observation of wide, continuous variation in egg size between these extremes. The prediction of dichotomy rests on the assumption of a negative linear relationship between egg size and development time. Here, I present a simple model in which development time is inversely proportional to egg size. Incorporating this relationship into an optimality model produces predictions of intermediate rather than extreme egg size. Modeled variations in mortality, food availability, fertilization rates, and temperature all produce continuous shifts in the value of the intermediate optimal size, in direct contrast to those produced by previous models, which predict shifts between two extreme optima. Empirical data on echinoid egg size and development time strongly support the model's assumption of an inverse proportional relationship between egg size and development time. A composite phylogeny is constructed of the 37 species for which egg size, development time, water temperature, and phylogenetic relatedness are known. Independent contrasts are made of the evolutionary changes in egg size and development time. This analysis indicates that evolutionary shifts in development time are correlated with the inversely proportional shifts in egg size assumed in the model. The assumption of a negative linear relationship used in previous models is rejected. This model provides a potential explanation for intraspecific variation in egg size along environmental gradients, sympatric differences in egg size among species, and biogeographic trends in egg size and development mode across taxa.
... It is also possible that their apparent rarity (as the consequence of a relatively short evolutionary existence) is because such species either give rise to species with non-feeding larvae or become extinct (Wray and Raff 1991 ). Conversely, Emlet ( 1986 ) thought that facultative planktotrophy may be stable from an evolutionary viewpoint, as such larvae may profi t from the positive attributes of both developmental variants (Emlet et al. 1987 ;Havenhand 1995 ;McEdward 1997 ;Allen and Pernet 2007 ; for a detailed discussion see Hart 1996 ). Wray ( 1996 ) remarked that such larvae are effi cacious only under quite specifi c conditions. ...
... Wray ( 1996 ) remarked that such larvae are effi cacious only under quite specifi c conditions. Whatever the case, it is facultative planktotrophy (which according to some researchers is more common than generally thought) that illustrates the transition from one state to the other (Kempf and Hadfi eld 1985 ;Emlet 1986 ;McEdward 1996McEdward , 1997Allen and Pernet 2007 ). ...
... Among invertebrates, facultative planktotrophy is known in two sea urchins, four gastropods, a bivalve and a polychaete (Perron 1981 ;Alatalo et al. 1984 ;Kempf and Hadfi eld 1985 ;Emlet 1986 ;Kempf and Todd 1989 ;Miller 1993 ;Hart 1996 ;Pernet and McArthur 2006 ;reviewed in Wray and Raff 1991 ;Havenhand 1995 ;Wray 1995a ;Raff 1996 ;Hadfi eld and Strathmann 1996 ). For instance, females of the polychaete Streblospio benedicti (Atlantic population) form two types of eggs (small and large), from which, correspondingly, planktotrophic and facultatively planktotrophic larvae develop. ...
Chapter 1 is devoted to reproductive patterns in gymnolaemate bryozoans, especially oogenesis, fertilization and brooding in the order Cheilostomata. Following a brief review of the history of studies on cheilostome reproduction, the cell source, position and development of the gonads, sexual structure of colonies and fertilization are described, followed by a detailed description and comparative analysis of the fi ve major reproductive patterns. Correlations are demonstrated between the type of oogenesis (oligolecithal vs macroleci-thal), ovary structure and type of embryonic incubation (non-placental vs placental). Matrotrophy is far more common in Cheilostomata than previously realized, with placental analogues being associated with the various brood-chamber types. Both incipient and substantial matrotrophy have been recorded. Sexual polymorphism, precocious fertilization, nurse cells, coelomopores and oviposition are described from the literature and new data and their evolution is discussed.
... In addition to planktotrophy and lecithotrophy, some echinoderm species develop through an intermediate developmental mode, facultative planktotrophy (Emlet 1986;Hart 1996). Facultatively planktotrophic larvae can feed, but do not need to, as they can metamorphose solely based on energy provided in their egg. ...
... Facultatively planktotrophic larvae can feed, but do not need to, as they can metamorphose solely based on energy provided in their egg. Larvae that are facultatively planktotrophic develop from an intermediate egg size and exhibit intermediate developmental timing to metamorphosis; however, they retain a pluteus morphology and therefore phenotypically resemble planktotrophic larvae (Emlet 1986;Hart 1996;Wray 1996). Facultatively planktotrophic larvae provide a unique opportunity to examine the order and timing of changes that occur in the evolution of lecithotrophy (Allen and Pernet 2007;Snoke-Smith et al. 2007;Zigler et al. 2008;Collin 2012;Zigler and Raff 2013). ...
... In all three replicate experiments, larvae from each of the four crosses developed into normal echinoplutei (Fig. 2) and were able to metamorphose. As with previous work (Emlet 1986), C. rosaceus larvae metamorphosed in both the presence and absence of food, whereas larvae from C. subdepressus only metamorphosed in cultures containing food. Larvae from both hybrid crosses employed the same developmental mode as their maternal species: hybrids from C. rosaceus eggs (CR Â CS) metamorphosed in both the fed and starved treatments, whereas hybrids from C. subdepressus eggs (CS Â CR) only metamorphosed in the fed treatment (Fig. 3). ...
Life history characteristics play a pervasive role in the ecology and evolution of species. Transitions between feeding and non-feeding larval development have occurred many times in both terrestrial and marine phyla, however we lack a comprehensive understanding of how such shifts occur. The sea biscuits Clypeaster rosaceus and Clypeaster subdepressus employ different life history strategies (facultatively feeding larvae and obligately feeding larvae, respectively) but can hybridize. In this study, we examined the development of hybrid larvae between these two species in order to investigate the inheritance of larval developmental mode. Our results show that both reciprocal hybrid crosses developed via the feeding mode of their maternal species. However, as feeding larvae can obtain both energy and hormones from algal food, we tested how hormones alone affected development by setting up a treatment where we added exogenous thyroid hormone, but no food. In this treatment the offspring of all four crosses (two homospecific and two heterospecific crosses) were able to metamorphose without algal food. Therefore we hypothesize that although hybrid developmental mode was inherited from the maternal species, this result was not solely due to energetic constraints of egg size.
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... A third difficulty lies in the TABLE 2. Crown-group symplesiomorphies in echinoplutei. For a discussion of these characters and the phylogenetic evidence supporting the time of their origin, see Neilsen (1987), Emlet (1988), Strathmann (1988aStrathmann ( , 1989, and Wray (1992). Strathmann et al. 1992). ...
... Other features were acquired within the phylum and are also likely to have been present in the echinoid crown-group ancestor's echinopluteus (Emlet 1988;Strathmann 1988a;Wray 1992). Included are vibratile lobes and a ventrally recurved gut (table 2B). ...
... The phylogenetic distribution of features among extant echinoplutei also provides information regarding the larva of the echinoid crown-group ancestor. Features present in all feeding echinoid larvae but absent from other echinoderm classes are likely to have arisen within the echinoid stem lineage, between the origin of the class and the radiation of the crown group(Emlet 1988; Strathmann 1988a; Wray 1992). Several important aspects of echinopluteus morphology fit this phylogenetic distribution, including anterolateral arm rods and the dorsal arch(table 2C).Other features are present in some but not all echinoids, and are absent from larvae of other classes. ...
The post-Paleozoic radiation of echinoids entailed a rapid diversification not only of adult morphology, but also of larval morphology. The timing, order, and phylogenetic distribution of evolutionary transformations in echinopluteus larvae are reconstructed here under maximum parsimony assumptions from a large neontological data base. Comparisons of larval and adult morphology over congruent time intervals demonstrate that the origin of many orders was accompanied by a suite of synapomorphies in larval morphology that was subsequently conserved. Many details of echinopluteus morphology are therefore of taxonomic significance. That larval morphology has diversified independently of adult morphology indicates that mosaic evolution has occurred within the life cycle and suggests that echinoid larvae and adults can and do respond to selection independently. Taken together, these findings underscore the complex ways in which complex life cycles can evolve. -from Author
... Species with lecithotrophic development typically have a larger maximum egg size, reduced fecundity, abbreviated lar val development, and greater juvenile size at metamor phosis than species with planktotrophic development (Strathmann, 1985;Emlet et al., 1987). Intermediate re productive strategies (e.g., facultative planktotrophy), considered transitional and evolutionarily unstable by some theoretical modelers (Vance, 1973;Christiansen and Fenchel, 1979), are known or implied for several species of echinoids (Strathmann, 1979;Emlet, 1986) but seem to be generally rare among echinoderms. ...
... Phylogenetically proximate echinoderm species that are nearly indistinguishable by morphological criteria of ten occur sympatrically and exhibit contrasting develop mental strategies. With such strong similarities between species, these complexes provide useful systems for reli able analyses of the interrelationship between different reproductive traits (e.g., egg size, larval type, juvenile size) and as such they have been the focus of several in vestigations (Atwood, 1973;Menge, 1975;Lawson-Kerr and Anderson, 1978;Emson and Crump, 1979;Schei blingandLawrence, 1982;Emlet, 1986 pers@comm.). This paper describes differences in reproduction and development between Porania antarctica and Porania sp_ that substantiate Clark's (1962) recommendation of distinct species rankings for the two forms. ...
... The (Emlet, 1986). A similar mode of develop ment (i.e., facultative planktotrophy) is suggested for echinoplutei ofthe spatangoid Brisasterlatjfrons(Strath mann, 1979) and judging from some egg sizes reported by Emlet et aL (1987) may occur in several other echi noids (e.g., Sterechinus agassizi, Brisasterfragilis). ...
Reproduction and development were mark edly different in two morphologically similar asteroids of the genus Porania that occur in shallow waters of Mc Murdo Sound, Antarctica. Adults ofthe recognized spe cies, Porania antarctica (Perrier, 1894), are large @ = 70 mm) and have genital pores that are situated ab orally on the disc; females broadcast spawn large num bers (3â€"4 x l0@)ofbuoyant eggs that measure 0.55 mm and develop into unusual, yolky planktotrophic larvae. In contrast, adults of the undescribedPorania sp. are considerably smaller (R@ = 30 mm) and their genital pores are located orally on the disc. Female fecundity is low (100â€"3 10 eggs);the few eggs produced measure 0.55 mm, are heavier than seawater, and develop into demer sal lecithotrophic larvae. These differences conform to general patterns reported for echinoderms with divergent types of reproduction. However, other differences con tradict established trends; specifically, P. antarctica with planktotrophic development has a shorter embryonic and larval phase (65 days vs. 78 days) and a larger juve nile size at metamorphosis (0.8 vs. 0.6 mm) than Porania sp., which has lecithotrophic development. The repro duction ofP. antarctica incorporates advantages of both planktotrophic and lecithotrophic strategies and may be particularly well-suited for environmental conditions in
... A few species, mostly of gastropod molluscs and echinoid echinoderms, have larvae that do not fit cleanly into the two nutritional strategies that characterize most larvae, feeding development and nonfeeding development. Sorne examples include: Adalaria proxima, (Thompson, 1958;Kempf and Todd, 1989), Phestilla sibogae (Kempf and Hadfield, 1985), and Conus pennaceus (Perron, 1981;Kohn and Perron, 1994) among the molluscs, a clypeasteroid Clypeaster rosaceus (Emlet, 1986), and Brisaster latifrons (Strathmann, 1978b;Hart, in press), and other spatangoids. The common feature of these species is that their larvae can capture and utilize exogenous particulate food but do not need to feed to complete development to metamorphosis. ...
... The differences between facultative planktotrophs and obligate nonfeeding lecithotrophs are egg size and larval morphology. In facultative planktotrophs, larval morphology is very 315 ENERGETIC STRATEGIES AMONG ECHINOID LARVAE similar to that of obligate feeding larvae and nutritional requirements are very similar to those of obligate nonfeeding larvae (Emlet, 1986;Strathmann, 1987;Kempf and Hadfield, 1985;Kempf and Todd, 1989;Hart, in press). Facultative planktotrophs have been seen as intermediate between strict feeding and nonfeeding larval types because of the unusual association of these two traits. ...
... 1). It is important to note that the time to metamorphosis and juvenile size data from previous studies differed substantially from ours (Arbacia [Harvey, 1956], Lytechinus [Mazur and Miller, 1971], Clypeaster subdepressus [Emlet, 1986]). These studies were carried out under various temperature and culturing regimes, used different species and combinations of food organisms, and probably lacked a common determinant for timing of the induction of metamorphosis. ...
Our current work investigates a major ecological transition in echinoderm life cycles: the evolution from planktotrophic to lecithotrophic larval development. We have discovered a wide range of feeding requirements among subtropical echinoid larvae. Differences in maternal investment determine how much external food is required to build the larval body and subsequently the juvenile rudiment. There appears to be a continuum of nutritional strategies between extreme obligate planktotrophy and functional lecithotrophy (i.e. facultative planktotrophy). We suggest that the ecological boundary between planktotrophy and lecithotrophy is easily crossed and that unlike morphological changes, ecological transitions, are readily reversible.
... Thorson (1950), who defined the terms planktotrophic and lecithotrophic, also referred to the development of a shortlived planktotrophic larva that was able to feed on the plankton, but did not need food to complete its development. This type of development, called facultative planktotrophy, is considered rare (Emlet, 1986;McEdward, 1997). In echinoderms, it has so far been documented in two echinoids [Clypeaster rosaceus (Emlet, 1986) and ...
... This type of development, called facultative planktotrophy, is considered rare (Emlet, 1986;McEdward, 1997). In echinoderms, it has so far been documented in two echinoids [Clypeaster rosaceus (Emlet, 1986) and ...
... Echinoid larvae provide a good example to illustrate this point. The correlation between ecological traits and developmental modes has been extensively studied among echinoids (31,46,122,137). Echinoid pluteus larvae with complex shapes and convoluted ciliated bands are usually defined as planktotrophic, as they remain in the water column for extended periods of time and feed on microalgae. ...
... However, in multiple echinoid lineages, convergent evolution has favored a transition from planktotrophy to lecithotrophy. In the clypeasteroid Clypeaster rosaceus and the spatangoid Brisaster latifrons, development follows the same trajectory as typical planktotrophic species and exhibits a stage morphologically similar to the pluteus larvae, but they do not need to feed to reach metamorphosis (31,46). The clypeasteroid Peronella japonica and the cidaroid Phyllacanthus imperialis extend larval arms like regular plutei but do not form a functional digestive tract and rely on maternal nutrient provisions for their development (96,97). ...
The goal of comparative developmental biology is identifying mechanistic differences in embryonic development between different taxa and how these evolutionary changes have led to morphological and organizational differences in adult body plans. Much of this work has focused on direct-developing species in which the adult forms straight from the embryo and embryonic modifications have direct effects on the adult. However, most animal lineages are defined by indirect development, in which the embryo gives rise to a larval body plan and the adult forms by transformation of the larva. Historically, much of our understanding of complex life cycles is viewed through the lenses of ecology and zoology. In this review, we discuss the importance of establishing developmental rather than morphological or ecological criteria for defining developmental mode and explicitly considering the evolutionary implications of incorporating complex life cycles into broad developmental comparisons of embryos across metazoans.
Expected final online publication date for the Annual Review of Genetics, Volume 57 is November 2023. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
... We studied larvae of seven species of common sea urchins from the Caribbean: the cidaroid Eucidaris tribuloides (Lamarck, 1816); the echinometrids Echinometra viridis A. Agassiz, 1863 and Echinometra lucunter (Linnaeus, 1758); the toxopneustids Lytechinus williamsi Chesher, 1968 andTripneustes ventricosus (Lamarck, 1816); and the clypeasteroids Clypeaster rosaceus (Linnaeus, 1758) and Clypeaster subdepressus (Gray, 1825). These all develop through an obligatory planktotrophic larval stage, except for C. rosaceus, which produces larger eggs that develop into facultative feeding larvae (Schroeder, 1981;Emlet, 1986;Sewell and Young, 1999;Wolcott and Messing, 2005;Vellutini and Migotto, 2010;McAlister and Moran, 2013). There is either little or no published information on larval thermal tolerance for any of these species, except for E. lucunter (Sewell and Young, 1999), although some information on the thermal tolerance of earlier developmental stages is available for three others (Cameron et al., 1985). ...
... All species showed sustained growth in all three aspects of morphology during the six days of the experiment, except for Clypeaster rosaceus, in which growth more or less ceased after day 4, after which some reduction in size was evident (Figs. 3, 4). This species is a facultative planktotroph, which can metamorphose after 5-7 days (Emlet, 1986); therefore, a reduction in arm length and larval body size was not unexpected. ...
In species with complex life cycles, early developmental stages are often less thermally tolerant than adults, suggesting that they are key to predicting organismal response to environmental warming. Here we document the optimal and lethal temperatures of larval sea urchins, and we use those to calculate the warming tolerance and the thermal safety margin of early larval stages of seven tropical species. Larvae of Echinometra viridis, Echinometra lucunter, Lytechinus williamsi, Eucidaris tribuloides, Tripneustes ventricosus, Clypeaster rosaceus, and Clypeaster subdepressus were reared at 26, 28, 30, 32, and 34 7C for 6 days. The temperatures at which statistically significant reductions in larval performance are evident are generally the same temperatures at which statistically significant reductions in larval survival were detected, showing that the optimal temperature is very close to the lethal temperature. The two Echinometra species had significantly higher thermal tolerance than the other species, with some surviving culture temperatures of 34 7C and showing minimal impacts on growth and survival at 32 7C. In the other species, larval growth and survival were depressed at and above 30 or 32 7C. Overall, these larvae have lower warming tolerances (1 to 5 7C) and smaller thermal safety margins (23 to 3 7C) than adults. Survival differences among treatments were evident by the first sampling on day 2, and survival at the highest temperatures increased when embryos were exposed to warming after spending the first 24 hours at ambient temperature. This suggests that the first days of development are more sensitive to thermal stress than are later larval stages.
... Mean lengths ofother measured larval arms (postorals and preorals) also decreased more with the enhanced ration, but not significantly (P > 0.05). The arms become shorter in more advanced eight-armed plutei that are approaching metamorphosis (Emlet, 1986b;Highsmith and Emlet, 1986). Thus the abruptly enhanced ration rapidly moved the eight-armed larvae toward metamorphosis both through increases in the echinus rudiment and stomach and through decreases in lengths of larval arms. ...
... Feeding by many ofthe small fishes depends on prey size and mouth size, and a failed attack would cause little or no damage to a larva. Emlet (1983) found that the fenestrated skeletal rods of pluteus arms were overdesigned for support ofthe arms against the currents generated by their cilia, and overdesign for body support suggests a function in defense against predators. Greater allocation to larval defenses may bring greater benefits in survival relative to costs in growth when low food supplies extend the larval period. ...
Preexisting developmental plasticity in feeding larvae may contribute to the evolutionary transition from development with a feeding larva to nonfeeding larval development. Differences in timing of development of larval and juvenile structures (heterochronic shifts) and differences in the size of the larval body (shifts in allocation) were produced in sea urchin larvae exposed to different amounts of food in the laboratory and in the field. The changes in larval form in response to food appear to be adaptive, with increased allocation of growth to the larval apparatus for catching food when food is scarce and earlier allocation to juvenile structures when food is abundant. This phenotypic plasticity among full siblings is similar in direction to the heterochronic evolutionary changes in species that have greater nutrient reserves within the ova and do not depend on particulate planktonic food. This similarity suggests that developmental plasticity that is adaptive for feeding larvae also contributes to correlated and adaptive evolutionary changes in the transition to nonfeeding larval development. If endogenous food supplies have the same effect on morphogenesis as exogenous food supplies, then changes in genes that act during oogenesis to affect nutrient stores may be sufficient to produce correlated adaptive changes in larval development.
... Birkeland, Chia and Strathmann, 1971), and sorne both (e.g. Kempf and Hadfield, 1985;Emlet, 1986). Still, focus has tended to be on extreme examples, such as ocean-crossing teleplanic larvae, leaving us with our earlier notions that most invertebrates are relative] y fixed in various life history parameters. ...
... In P. sibogae, the !arval stage may be considerably extended when larvae feed and an obligate metamorphic eue is absent. Facultative planktotrophy has also been recorded in an echinoid, Clypeaster rosaceus (Emlet, 1986), and it seems likely that other examples might be found if biologists attempting to rear invertebrate larvae exposed otherwise "lecithotrophic larvae" to varions cultured phytoplanktors. Facultative planktotrophy bestows significant flexibility on species where it occurs, allowing larvae to metamorphose soon after hatching, thus potentially reeruiting to nearby adult populations, or to persist in the plankton longer, leading to broad species dispersal. ...
Nearly all aspects of the life histories of individual marine- invertebrate species are characterized by ranges of sizes, seasonal variation, and functional flexibility and phenotypic plasticity in response to varying environmental conditions; that is, they are highly polytypic. Four major areas of polytypy are considered: (1) breeding seasons and cycles vary greatly in time and duration with latitude and from year to year; (2) egg and larval sizes, while showing both genetic and stochastic variability in all species, are often also flexible responses to adult and larval nutrition; (3) modes of development are variable within a number of single species, often reflecting egg-size differences between populations, or even as a result of hatching age of siblings from a single egg mass; and (4) duration of the pelagic larval phase, both before and after the onset of metamorphic competence. Planktotrophic larvae show plastic responses to phytoplankton abundance in their morphologies, and most larvae are flexible in their age at metamorphosis because this complex process requires a more- or-less specialized substratum to induce it for most invertebrate species. New data are presented that provide additional examples of broad flexibility of sibling lecithotrophic larvae to hatch and settle at greatly differing ages. Larvae of the patelloidean gastropod Lottia pelta settled from 8 to 28 days after fertilization, and those of the fissurelloidean Diodora aspera hatched over a three week period from 7 to 30 days post- fertilization; larval settlement had a similarly broad range. Even the planktotrophic- lecithotrophic dichotomy breaks down as increasing numbers of species are found to produce larvae that can metamorphose without feeding (i.e. lecithotrophy), or feed and greatly extend their larval durations (planktotrophy) in the absence of suitable settlement substrata. Invertebrate groups with rigidly canalized life histories are noted to be components of the fouling community, and it is conjectured that an evolutionary history on floating substrata canalized their life histories toward high inbreeding tolerance, often selfing, and brief pelagic larval durations. We note that most life-history theory has considered extremes and major modes in invertebrate development, and suffers from lack of attention to the abundance of polytypic life-history traits as evolutionary survival mechanisms at the species level. We conclude that response flexibility and plasticity increase both survivorship and fecundity of individuals, while life-history variability increases the likelihood of recruitment across populations and persistence over geological time. More data are needed on the ranges of scalar characters and flexible responses in marine- invertebrate life histories to rigorously evaluate their contributions to evolutionary success.
... For many taxa, there is a major life-history trade off between production of many small, nutrient-poor eggs in high-fecundity species with feeding larvae and production of fewer large, nutrient-rich eggs in low-fecundity species with non-feeding larvae, although facultative feeding larvae are being discovered (e.g. Thorson 1950, Vance 1973, Emlet 1986, Emlet et al. 1987, Jaeckle 1995, McEdward & Miner 2001, Villinski et al. 2002, Falkner et al. 2006, Allen & Pernet 2007, Moran & McAlister 2009. ...
... Species producing small eggs (<150 to 250 µm diameter) have larvae that depend on exogenous resources to reach the juvenile stage, while those with large eggs (> 250 to 300 µm diameter) develop to metamorphosis without feeding (Strathmann 1985, Emlet et al. 1987, Jaeckle 1995. Identification of a few echinoderm species with facultative planktotrophy which have eggs intermediate in size and which can avail themselves of exogenous food, but do not need to feed to achieve the juvenile stage, provides insights into the transition to lecithotrophy (Emlet 1986, Hart 1996, Wray 1996, Allen & Pernet 2007, Allen & Podolsky 2007. This transition appears to have occurred through a facultative feeding larva, a larval form that might not be evolutionarily stable (Wray 1996). ...
For free-spawning marine invertebrates, the egg is the unit of maternal investment in offspring. For many taxa, there is a major life-history trade-off between production of many small, nutrient-poor eggs in high-fecundity species and fewer large, nutrient-rich eggs in low-fecundity species. In echinoderms, the switch from small eggs in species with ancestral-type feeding larvae to large eggs and non-feeding larvae is a significant change with major consequences for larval ecology and juvenile success. In this first comparative study of maternal investment in the Ophiuroidea across species with a range of egg sizes and larval types, the egg protein and lipid content of 4 species with planktotrophic and 6 species with lecithotrophic larvae were characterised. The planktotrophs produced eggs dominated by protein with triacylglycerol as the main energy storage lipid. The switch to lecithotrophy in the Ophiuroidea is associated with an increase in energy storage lipids to produce an energy-dense egg, as is typical of echinoderms with this mode of development. The eggs of the lecithotrophs, however, contained several novel lipid classes not found in ancestral-type ophiuroid eggs. These eggs also differed from those of other echinoderms with lecithotrophic development in the presence of these novel lipids rather than up-scaling of the ancestral maternal provisioning strategy. Our findings support the hypothesis of independent evolution of lecithotrophy multiple times in the Echinodermata. In the Ophiuroidea, this is seen in the evolution of different lipid pro - visioning patterns between species with large eggs.
... Therefore, the diet consumed and the availability of food for adult has the potential to affect egg quality, larval morphometry and the level of larval development. Furthermore, larvae can develop using food reserves from eggs [5], energy reserves are consumed entirely for development larvae [6] [7]. Larvae are organisms that are between the phases after the embryo and juvenile for both invertebrates and vertebrates. ...
Hatchery is the main factor that plays an important role in aquaculture sea urchin Tripneustes gratilla (Linnaeus 1758). The quality of sea urchin egg is determined by the absorption of nutrients that carried throughout the gonad development while the quality of nutrients is very likely influenced by the type of food consuming. This research of substrate types on habitat breeding embryonic development and larval morphometric of sea urchin had been done on October - November 2016 at the laboratory of marine, Research Center for Deep Sea, Indonesia Institute of Sciences, Ambon. The Samples taken from three different habitats comprises Hative Besar, Liang and Suli beach. The purpose of this research is to determine the effects of substrate types on habitat breeding embryonic development and larval morphometric of sea urchin. The method that has been used to determine the morphometric was done by measuring the diameter and height of the shell using a digital caliper and total body weight using a digital scale. To observe embryonic development and larval morphometric done by in vitro fertilization through eggs selection then cultured in petri dish at a density of 10ind/ml. The result of this research is the most dominant quantity of embryonic development (72 hours) indicated by culture vessel from Hative Besar meanwhile the least is indicated by Liang. The greatest larval morphometric is indicated by culture vessel from Hative Besar with length and height of larval body further the larval of culture vessel from Hative Besar shown ossification formation.
... It should be highlighted that most of the lineage founder cells and many tissues are established at the 64-cells stages, well before the appearance of any morphological difference of the later embryo (same result in Matranga, 2005). However, Cleavages and development of embryo and larva of the investigated sea urchin Strongylocentrotuspurpuratus were similar to those reported in other echinoidswith planktotrophic larvae (Emlet, 1986;Vellutini and Migotto, 2010). The developmental timing of hatching blastulae took longer period (08.45 h at 24 • C)than those in Lytechinusvariegatus (6 h at 23 • C) (Strathmann, 1987) andin Clypeastersubdepressus (7 h at 26 • C) (Vellutini and Migotto, 2010). ...
Adults of August (2014) along the northern estruarine of gametes has been carried out by potassium chloride injection using a one ml tuberculin syringe equipped with a 26 or 30 gauge needle. Gentle shaking of the animal anticlockwise 90 minutes of injection aided in gamete shedding. Gently sperm and eggs were mixed with a clean stirring rod. time schedule for different stages has been tabulated. and were placed on glass slides with embedding mixture of PBS / glycerol / DABCO. Immediate viewing and photographing were very small and extremely motile Zygote (3 min. after fertilization) has undergone radial holoblastic cleavage till the blastul (3.50-4.15 hrs. after fertilization).The early blastula had a blastoderm enclosing a central blastocoel (6 hr 20 min. after fertilization). Cilia were developed on the exterior of the blastoderm and gradually this embryonic stage hatc At the animal pole an apical plate was formed in the form of a thickened region of epithelium with a tuft of long cilia while the epithelium at the vegetal pole flattened and thick plate (16hr 45min.. after fertilization). Ingression of primary mesenchyme cells into the blastocoel took place and a new cavity was formed referred to enteron. (19hr 15min. after During the prism stage the embryo took the shape of a rounded pyramid (21 hr 20 min. after fertilization). Pluteus larva with two arms was developed (24hr 30 min. afte larva developed into into eight continued larval developme swimming blastulae were subjected to certain bioactive inducers which had been claimed to induce metamorphosis, involved in signaling systems, serve in neuronal control, control morphogen behavioral reactions or interact with members of several signal transduction proteins pathways under normal physiological conditions. Results of these trails were introduced to One variance (ANOVA) with P < 0.05 and Dunnett's Multi It has been concluded that Acetyl choline 0.5 mM, Serotonine NH4ClNH4Cl and cGMP 1 pluteus larval stage with and NH4Cl 300 µM exereted no role in metamorphosis and antibiotic sea water had negligible effect.
... Support for this relatively long FFP in A. mollis comes from experimental work by Morgan (2008), where there was a divergence in larval size [proposed as an indicator of FFP by Miner et al. (2005) and Byrne et al. (2008b)] between high and low phytoplankton diets in the period between 3 and 7 days. The FFP in planktotrophic echinoids is generally shorter, from 48 to 72 h, but longer FFP are reported in Tripneustes gratilla (Byrne et al. 2008b), in the enhanced planktotroph Encope michelini (Eckert 1995) and the facultative planktotroph Clypeaster rosaceus (Emlet 1986; see also Miner et al. 2005, their Table 3). McEdward (1997) hypothesised that the length of FFP was positively correlated with egg size, and this was supported in the study of 6 tropical sand-dollar species by Miner et al. (2005). ...
Echinoderms are widely used to investigate the relationship between egg size, energy content and larval developmental strategies in marine invertebrates; although there have been few studies on ophiuroids and holothuroids. In this paper, we provide the first detailed biochemical information on egg composition and utilization in the planktotrophic holothuroid, Australostichopus mollis. The egg ultrastructure, protein content (85.1 ng egg−1) and lipid:protein ratio of 0.42 were consistent with those of other planktotrophic echinoderms of similar egg size. However, the lipid content (35.6 ng egg−1) was outside the 95% prediction band for the relationship between egg size and lipid content for echinoderms. Triacylglycerol (TAG) was the main energetic lipid present in the egg, with ca 50% of the TAG being utilized to construct the feeding auricularia; the remaining TAG was estimated to be consumed over 114.8 h (4.8 days) of development. Feeding a microalgal diet during early larval development did not affect the rate of TAG utilization, but increased protein content in the 90-h auricularia. Biochemical information from A. mollis eggs/larvae suggests that TAG might be the ancestral maternally derived energetic lipid in the Echinodermata, but also that there may be different patterns of lipid utilization between different classes.
... From 2009 to 2013, Tara Oceans launched a study of the global ocean ecosystem to sample the plankton of the world's oceans. Both genomics and transcriptomics, in the form of Illumina nextgeneration sequencing, were applied to plankton samples, in combination with oceanographic measurements (e.g., temperature, salinity, nutrients) and obligate planktotrophs (e.g., the echinoid Clypeaste r spp., Emlet, 1986). Marine invertebrate larvae also offer the exciting possibilities of studying hybrid larvae, such as those produced by crosses between planktotrophic and lecithotrophic echinoderms (Raff et al., 1999) and tailed and tail-less ascidian larvae (Swalla and Jeffery, 1996). ...
The diverse phenotypes exhibited by marine invertebrate larvae are the result of complex gene-environment interactions. Recently, technological advances in molecular biology have enabled large-scale -omics approaches, which can provide a global overview of the molecular mechanisms that shape the larval genotype-phenotype landscape. -omics approaches are facilitating our understanding of larval development and life history evolution, larval response to environmental stress, the larval microbiome, larval physiology and feeding, and larval behavior. These large-scale molecular approaches are even more effective when combined with large-scale environmental monitoring and phenotypic measurements. Current -omics approaches to studying larvae can be improved by the addition of functional genetic analyses and the reporting of natural variation in gene expression between individuals and populations. Systems-level approaches that combine multiple -omics techniques will allow us to explore in fine detail the interactions of environmental and genotypic influences on larval phenotype.
... The shape and behavioural repertoire of marine invertebrate larvae reflect requirements for feeding, swimming, navigation, settlement and defence (Emlet 1986;McEdward 1986a, b;Pennington and Strathmann 1990;Sameoto and Metaxas 2008;Chan and Grunbaum 2010). Larval swimming ability and behaviour vary greatly among developmental stages and species and play a key role in dispersal and thus population connectivity (Metaxas and Saunders 2009;Metaxas 2013). ...
... Settling early would thus have expected costs in terms of juvenile growth, competition and/or protection from predation (e.g. [58,59]). We observed that juveniles resulting from turbulence exposure while precompetent were more than 30% smaller than their counterparts who had settled when they had reached competence in the absence of turbulence exposure, three days later. ...
Complex life cycles have evolved independently numerous times in marine animals as well as in disparate algae. Such life histories typically involve a dispersive immature stage followed by settlement and metamorphosis to an adult stage on the sea floor. One commonality among animals exhibiting transitions of this type is that their larvae pass through a 'precompetent' period in which they do not respond to localized settlement cues, before entering a 'competent' period, during which cues can induce settlement. Despite the widespread existence of these two phases, relatively little is known about how larvae transition between them. Moreover, recent studies have blurred the distinction between the phases by demonstrating that fluid turbulence can spark precocious activation of competence. Here, we further investigate this phenomenon by exploring how larval interactions with turbulence change across ontogeny, focusing on offspring of the sand dollar Dendraster excentricus (Eschscholtz). Our data indicate that larvae exhibit increased responsiveness to turbulence as they get older. We also demonstrate a likely cost to precocious competence: the resulting juveniles are smaller. Based upon these findings, we outline a new, testable conception of competence that has the potential to reshape our understanding of larval dispersal and connectivity among marine populations.
... Contrariamente ao verificado para o primeiro estádio de zoé, a disponibilidade do alimento torna-se importante para o desenvolvimento das larvas de L. seticaudata e L. boggessi no estádio de zoé II. Embora, a ausência de alimento não induza mortalidade no estádio inicial de desenvolvimento larvar, devido ao elevado potencial endotrófico destes organismos (Emlet, 1986), a longo prazo os períodos de inanição promovem o aumento da duração do desenvolvimento larvar, um assentamento tardio e assíncrono, traduzindo-se muitas vezes em elevadas mortalidades durante a metamorfose . ...
The Ophiuroidea, the most diverse echinoderm class, exhibits an array of life history patterns and larval forms, the evolution of which is poorly understood. With a robust phylogeny available for the major family, the Ophiocomidae, we undertook an assessment of the evolution of development in these ophiuroids. We spawned 15 species and documented larval development in 14 of these. In total, data on egg size or larval development were available for 27 species across the four recognized genera ( Breviturma , Ophiocoma , Ophiocomella , and Ophiomastix ). Ophiocomids have a bimodal egg size distribution. Species with small eggs ( x̄ = 82 μm diameter, range 55–100 μm diameter) and large eggs ( x̄ = 424 μm diameter, range 335–550 μm diameter) have planktotrophic ophioplutei and lecithotrophic vitellariae, respectively. The advanced ophiopluteus transforms into an armless vitellaria prior to metamorphosis through resorption of the larval arms and rearrangement of the ciliary tracts into series of transverse bands. Thus, the Type II pattern of development (which includes both the ophiopluteus and vitellaria) may be characteristic of the Ophiocomidae. This is not seen in other ophiuroid families. Evolution of nonfeeding (lecithotrophic) development through a vitellaria larva appears to have occurred only once in this family, in the genus Ophiomastix . Several traits appear to be specific to some species or genera, including an ornate fertilization envelope ( Ophiocoma species), the presence of an early barrel‐shaped larva ( Breviturma species), and the presence of vibratile lobes in advanced ophioplutei ( Breviturma , Ophiocomella ). In species with lecithotrophic development, the vitellaria is distinct, with prominent ciliated lobes around the developing juvenile rudiment. Larval form may assist with identification of ophiocomid larvae in plankton samples.
Echinoderms are in habitats in coastal waters because is a biota that can maintain the sustainability and the balance of the coral reef ecosystem. Human activity in utili zing Echinoderms, namely in Echinoidea and Holothuroidea can affect life his life. The purpose of this study was to determine the diversity of phyla Echinoderms class Echinoidea and Holothuroidea at the Harbor Waingapu Old Pier and its use as a medium Biology learning. The research method used is purposive sampling and analyzed using the approach quantitative descriptive with the Shannon diversity index formula Wiener. Echinoderm samples were calculated using the technique quadratic transects with a plot size of 2 x 2 meters are placed perpendicularly in the direction of 50 meters using a plot of 30 plot. Environmental factors measured are temperature, salinity, degrees acidity (pH) and levels of oxygen (DO). Measurements are taken at each observation station. The results showed 11 species Echinoderms are divided into 2 classes, namely Diadema setosum, Diadema savignyi, Tripneustes gratilla, Strongylocentrotus droebachiensis, Echinocardium flavescens, Clypeaster subdepressus, and Mespilia globulus from the class Echinoidea. Holothuria atra, Holothuria scraba, Euapta godeffroyi and Chiridota rigida from the class Holothuroidea. The diversity index obtained includes medium category with a value of H = 1.696.
Feeding larvae of echinoderms appear to differ in scope for adaptive developmental plasticity in response to food. Extension of the ciliary band on narrow arms supported by skeletal rods, as in echinoid and ophiuroid larvae, may enable a greater increase in maximum clearance rate per cell added, conferring greater advantages from developing longer ciliary bands when food is scarce. Formation of the juvenile mouth and water vascular system at a new site, as in echinoid and asteroid larvae, permits extensive growth of the juvenile rudiment during larval feeding, with advantages from earlier or more growth of the rudiment when food is abundant. In contrast, plasticity in storage of nutrients is unrelated to the form of the ciliary band or the site of formation of the juvenile's mouth. Feeding larvae (auriculariae) of holothuroids lack arms supported by skeletal rods and formation of the mouth at a new site but as a unique feature store nutrients in hyaline spheres. In this study, more food for auriculariae of Apostichopus californicus resulted in juveniles (pentactulae) with longer and wider bodies and larger hyaline spheres, but effects of food supply on the size of most body parts of auriculariae were small. Auriculariae with more food developed relatively larger stomachs and larger posterior hyaline spheres, indications of greater nutrient storage. Auriculariae with less food developed relatively wider mouths and differed in some exterior dimensions, which might enhance the capture of food. Plasticity is limited in rudiment development and perhaps in structures for feeding, but plasticity in nutrient storage can provide advantageous compromises between duration of growth as a feeding larva and the condition of juveniles formed at metamorphosis.
Introduction: Central America, a narrow strip of land dividing the Atlantic and Pacific oceans, has a high diversity of marine and terrestrial species. Echinoderms are one of the most diverse marine groups with 420 reported species. Objective: To summarize echinoderm research in Central America. Methods: We compiled the literature from SCOPUS, Web of Science, SciELO, Google Scholar, Biodiversity Heritage Library, the Internet Archive and the Smithsonian Library. Results: We found 324 publications dating from 1840 to 2020; the early studies had a strong taxonomic focus, but after the 1970s, ecology, evolution and reproduction gained prominence. Echinoidea is the most studied class (38% of publications) due to its use in evolutionary studies as well as the importance of the genus Diadema in reef ecology and dynamics. Conclusion: We recommend more research on fisheries management, conservation and environmental education; and greater integration of local and international research.
Most marine invertebrate larvae either feed or rely on reserves provisioned by parents to fuel development, but facultative feeders can do both. Food availability and temperature are key environmental drivers of larval performance, but the effects of larval experience on performance later in life are poorly understood in facultative feeders. In particular, the functional relevance of facultative feeding is unclear. One feature to be tested is whether starved larvae can survive to adulthood and reproduce. We evaluated effects of larval temperature and food abundance on performance in a marine harpacticoid copepod, Tisbe sp. In doing so, we report the first example of facultative feeding across the entire larval stage for a copepod. In a series of experiments, larvae were reared with ad libitum food or with no food, and at 2 different temperatures (20 vs. 24°C). We found that higher temperatures shortened development time, and larvae reared at higher temperature tended to be smaller. Larval food consistently improved early performance (survival, development rate and size) in larvae, while starvation consistently decreased survival, increased development time and decreased size at metamorphosis. Nonetheless, a small proportion (3-9.5%, or 30-42.7% with antibiotics) of larvae survived to metamorphosis, could recover from a foodless larval environment, reach maturity and successfully reproduce. We recommend that future studies of facultative feeding consider the impact of larval environments on adult performance and ability to reproduce.
This chapter describes practical methods and key points for using non-camarodont echinoids including cidaroids (Order Cidaroida), clypeasteroids (also known as sand dollars; Order Clypeasteroida), and spatangoids (also known as heart urchins; Order Spatangoida) as experimental subjects for biological studies. The content described here is based on six Japanese species of echinoids (Astriclypeus manni, Clypeaster japonicus, Echinocardium cordatum, Peronella japonica, Prionocidaris baculosa, and Scaphechinus mirabilis). Specific topics addressed in this chapter include the collection and maintenance of adults, embryonic culture, and experimental procedures for micromanipulations, whole mount in situ hybridization, and immunological experiments.
The polychaete Streblospio benedicti is unusual in that several field populations consist of individuals that exhibit either planktotrophic or lecithotrophic larval development. Planktotrophy in this species involves production of many small ova that develop into feeding larvae with a two- to three-week planktonic period. Lecithotrophy involves production of fewer, larger ova that develop into nonfeeding larvae that are brooded longer and have a brief planktonic stage. Reciprocal matings were performed to investigate genetic variance components and the correlation structure of life-history traits associated with planktotrophy and lecithotrophy. Our objective was to better understand persistence of this developmental dichotomy in Streblospio benedicti, and among marine invertebrates in general. Substantial additive genetic variation (75-98% of total) was detected for the following characters at first reproduction: female length; position of the first gametogenic setiger and first brood pouch; ovum diameter; three traits related to fecundity (numbers of ova per ovary, larvae per brood pouch, and larvae per brood); median larval planktonic period and the presence of larval swimming setae; but not for total number of brood pouches; larval length; larval feeding; and larval survivorship. Based on the unusual geographic distribution of development modes in this species, we hypothesize that the developmental traits have evolved in allopatry and have only recently come into contact in North Carolina. The high additive contribution to variance observed for many traits may be inflated due to (a) nonrandom breeding in nature, and (b) examination of only one component of an age-structured population at one time. Nuclear interaction variance and maternal variance accounted for 84% of the total variation in larval survivorship. This observation supports other empirical studies and theoretical predictions that nonadditive components of variance will increase in importance in individual traits that are most closely tied to fitness. A network of life-history trait correlations was observed that defines distinct planktotrophic and lecithotrophic trait complexes. Negative genetic correlations were present between fecundity and egg size, between fecundity and position of the first gametes, and between larval survivorship and median planktonic period. Positive genetic correlations were detected between fecundity and female size at first reproduction and between planktonic period and the presence of swimming setae. Intergenerational product-moment correlations were negative for larval length and fecundity, planktonic period and egg size, female size and larval survivorship, and fecundity and larval survivorship. If the genetic correlation structure observed in the laboratory persists in the field, it may constrain responses of individual characters to directional selection, and indirectly perpetuate the dichotomies associated with planktotrophy and lecithotrophy.
We analyzed phylogenetic relationships among 12 nominal species of starfish in the genera Patiriella and Asterina (Order Valvatida, Family Asterinidae), based on complete sequences for a mitochondrial protein coding gene (cytochrome oxidase subunit I) and five mitochondrial transfer RNA genes (alanine, leucine, asparagine, glutamine, and proline) (1923 bp total). The resulting phylogeny was used to test a series of hypotheses about the evolution of life-history traits. (1) A complex, feeding, planktonic larva is probably ancestral for these starfish, but this is not the most parsimonious reconstruction of ancestral larval states. (2) The feeding larval form was lost at least four times among these species, and three of these losses occurred among members of a single clade. (3) Small adult size evolved before both cases of hermaphroditism and viviparous brooding, but viviparity was not always preceded by an intermediate form of external brooding. (4) An ordered transformation series from feeding planktonic development to viviparous brooding has been predicted for starfish, but we could not find an example of this transformation series. (5) Viviparity evolved recently (< 2 Mya). (6) Both species selection and transformation of lineages may have contributed to the accumulation of species with nonfeeding development among these starfish. (7) Neither Asterina nor Patiriella are monophyletic genera. Larval forms and life-history traits of these starfish have evolved freely under no obvious constraints, contrary to the widely assumed evolutionary conservatism of early development.
I present my recollections of the significance of ideas, discussions and consequences of the 1981 Dahlem conference that attempted to draw together evolutionary and developmental biology, and in the presentation at that conference of the hypothesis that development might contribute novel mechanisms of evolution. I also discuss my approaches in seeking a suitable non-model organism for asking experimental questions about Evo-devo, and in seeking to integrate the disciplines, including paleontology, systematics, and developmental genetics, which coalesced into a distinct science of Evo-devo in the ensuing years.
Among echinoderms, nonfeeding larvae usually are simplified in body shape, have uniform ciliation, and have lost the larval gut. A few species have nonfeeding larvae that express some remnant features of feeding larvae like ciliated bands and larval skeleton or larval arms, but typically their larval mouth never opens and their gut does not function. Still other species have retained the feeding larval form, a functional gut, and can feed, but they do not require food to metamorphose. The present note describes the development of a tropical holothurian, Holothuria mexicana, which hatches as a gastrula that is already generating coelomic structures. A translucent auricularia forms with a mouth that opens but becomes reduced soon thereafter. In form and ciliation this auricularia resembles a feeding larva, but it does not respond to food. A doliolaria forms on day 4 and the pentactula on day 6 post-fertilization. Further study of this larva and that of its closely related congener, Holothuria floridana, is warranted.
Diadema setosum (Leske, 1778), is one of the common echinoids widely distributed in the Indo-West Pacific Ocean, where it occurs from the Red Sea, Persian Gulf and the east coast of Africa to Japan, Australia and Malaysia. To investigate the developmental basis of morphological changes in embryos and larvae, we documented the ontogeny of D. setosum in a controlled laboratory condition at the Institute of Bioscience, Universiti Putra Malaysia, during July-September, 2012. Matured gametes were obtained from the adult individuals and the eggs fertilized at limited sperm concentration (10-5 dilution). The obtained embryos were then reared at 24-25°C. First cleavage (2-cell), 4-cell, 8-cell, 16-cell, 32-cell and multi-cell (Morulla) stages were attained at 01.20, 02.14, 02.44, 03.09, 03.32 and 03.54 h after fertilization, respectively. Blastulae with a mean length of 111.47±1.88 μm (mean±SD) hatched 08.45 h after sperm entry. Gastrula formed 16.36 h post-fertilization and the archenteron extended constantly, while the ectodermal red-pigmented cells migrated synchronously to the apical plate. The pluteus larva started to feed unicellular algae (Chaetoceros calcitrans) in 2 d, grew continuously, and finally attained metamorphic competence within 35 d after fertilization. Induction of metamorphosis took approximately 1 h 30 min from attachment on the substratum to the complete resorption of larval tissues and the development of complete juvenile structure with adult spines, extended tubefeet and well-developed pedicellaria, the whole event usually took place within 1 d post-settlement. The newly formed juvenile (473.16 ± 6.96 μm, n=30) with a complete adult structure then grew on coralline algae to 3-month old juvenile, which represents the "sea urchin seed" for stocking in grow-out culture. This study represents the first successful investigation on embryonic, larval and early juvenile development of D. setosum. The findings would greatly be helpful towards the development of breeding and seed production techniques for aquaculture of sea urchins. © 2015, Iranian Fisheries Research Organization. All rights reserved.
This chapter discusses the cell lineages in larval development and evolution of echinoderms. The embryonic cell lineages of echinoderms contribute to understanding complementary functional and evolutionary aspects of their larval biology. Most marine animals have complex life histories in which the embryo gives rise to a feeding larva distinct from the adult. The sea urchin pluteus larva is a prime example. The early cell lineages of indirect-developing species generate the cells that produce these larval forms. These larvae feed and grow; thus, the eggs that produce them are relatively small. Only a few cell cleavage cycles are needed to produce the requisite cells and initiate larval morphogenesis. Ancient features of echinoderm cell lineages are the following: maternal determination of the animal–vegetal (A–V) axis; a radial pattern of cleavage; equal cell divisions throughout cleavage; determination of the larval dorsal–ventral (D–V) axis during early cleavage; and segregation of determinants into final positions after the third cleavage. Some of these ancient features are highly conserved among echinoderms, and most notably the maternal determination of the A–V axis and its relationship to the first two cleavage planes.
This study evaluated the starvation resistance of the shrimp, Neocaridina davidi during the first and the third juvenile stages (named here
as JI and JIII) by means of the estimation of point-of-no-return (PNR50). Two experiments were conducted with increasing numbers of
days without food and two controls (one with continuous feeding, CF; the other, with continuous starvation, CS). Time to the first molt and
number of molts did not differ among the treatments beginning at JI or JIII. Nevertheless, longer periods of starvation influenced growth
and survival of juveniles beginning the starvation as JI, but these effects were not observed in JIII. The estimated values of PNR50 for JI
and JIII were 16.15 ± 0.31 and 9.44 ± 0.26 days, respectively. The early stages of the life cycle are more tolerant to starvation than other
decapods previously studied. Such ability indicates a great potential of this species for aquaculture.
The evolution of life cycles involves transitions between discrete states in one or more of the characters that comprise a developmental pattern. In this paper, we examine three of the major life cycle characters and the states for these characters. Using examples from echinoderms, we discuss the evolutionary transitions that have occurred in the type of morphogenesis, developmental habitat, and mode of nutrition during development. We evaluate the functional requirements associated with these transitions to infer the likelihood (frequency or rapidity) of change in a given character and of biases in the polarity of character state transitions. Using comparisons of closely related species, we evaluate the change between states in one character for dependence on the state of, or correlated changes in, other characters. Based on our analysis of congeneric species that differ in developmental habitat, we conclude that the transition between pelagic and benthic development is an ecological change that is independent of changes in morphogenesis and should be reversible. In contrast, the transition from feeding to nonfeeding development has been considered to be irreversible because it involves marked changes in larval morphology. We re-examine the transition between different modes of larval nutrition in light of recent studies that show that there exists a continuum of nutritional strategies between planktotrophy and lecithotrophy. This continuum is largely determined by variation in maternal investment and does not involve alterations in larval morphology. We suggest that the boundary between planktotrophy and lecithotrophy is frequently crossed and that this transition is reversible. Ecological changes represent the crossing of a functional threshold. Only after crossing the threshold, do larvae experience qualitatively different selective pressures that can lead to subsequent changes in morphology and development. Two different changes have occurred in the type of morphogenesis: the simplification of larval morphology that is associated with obligate (nonfeeding) lecithotrophy and the loss of the larval body plan in the evolution from indirect to direct development. It is the modification of morphology independent of the ecological changes that requires alterations in developmental processes, constrains evolutionary options, imposes irreversibility, and establishes the discrete nature of larval patterns in marine invertebrates.
We analyzed phylogenetic relationships among 12 nominal species of starfish in the genera Patiriella and Asterina (Order Valvatida, Family Asterinidae), based on complete sequences for a mitochondrial protein coding gene (cytochrome oxidase subunit I) and five mitochondrial transfer RNA genes (alanine, leucine, asparagine, glutamine, and proline) (1923 bp total). The resulting phylogeny was used to test a series of hypotheses about the evolution of life-history traits. (1) A complex, feeding, planktonic larva is probably ancestral for these starfish, but this is not the most parsimonious reconstruction of ancestral larval states. (2) The feeding larval form was lost at least four times among these species, and three of these losses occurred among members of a single clade. (3) Small adult size evolved before both cases of hermaphroditism and viviparous brooding, but viviparity was not always preceded by an intermediate form of external brooding. (4) An ordered transformation series from feeding planktonic development to viviparous brooding has been predicted for starfish, but we could not find an example of this transformation series. (5) Viviparity evolved recently (< 2 Mya). (6) Both species selection and transformation of lineages may have contributed to the accumulation of species with nonfeeding development among these starfish. (7) Neither Asterina nor Patiriella are monophyletic genera. Larval forms and life-history traits of these starfish have evolved freely under no obvious constraints, contrary to the widely assumed evolutionary conservatism of early development.
Species with large eggs and nonfeeding larvae have evolved many times from ancestors with smaller eggs and feeding larvae in numerous groups of aquatic invertebrates and amphibians. This change in reproductive allocation and larval form is often accompanied by dramatic changes in development. Little is known of this transformation because the intermediate form (a facultatively feeding larva) is rare. Knowledge of facultatively feeding larvae may help explain the conditions under which nonfeeding larvae evolve. Two hypotheses concerning the evolutionary loss of larval feeding are as follows: (1) large eggs evolve before modifications in larval development, and (2) the intermediate form (facultatively feeding larva) is evolutionarily short-lived. I show that larvae of a heart urchin, Brisaster latifrons, are capable of feeding but do not require food to complete larval development. Food for larvae appears to have little effect on larval growth and development. The development, form, and suspension feeding mechanism of these larvae are similar to those of obligate-feeding larvae of other echinoids. Feeding rates of Brisaster larvae are similar to cooccurring, obligate-feeding echinoid larvae but are low relative to the large size of Brisaster larvae. The comparison shows that in Brisaster large egg size, independence from larval food, and relatively low feeding rate have evolved before the heterochronies and modified developmental mechanisms common in nonfeeding echinoid larvae. If it is general, the result suggests that hypotheses concerning the origin of nonfeeding larval development should be based on ecological factors that affect natural selection for large eggs, rather than on the evolution of heterochronies and developmental novelties in particular clades. I also discuss alternative hypotheses concerning the evolutionary persistence of facultative larval feeding as a reproductive strategy. These hypotheses could be tested against a phylogenetic hypothesis.
The polychaete Streblospio benedicti is unusual in that several field populations consist of individuals that exhibit either planktotrophic or lecithotrophic larval development. Planktotrophy in this species involves production of many small ova that develop into feeding larvae with a two- to three-week planktonic period. Lecithotrophy involves production of fewer, larger ova that develop into nonfeeding larvae that are brooded longer and have a brief planktonic stage. Reciprocal matings were performed to investigate genetic variance components and the correlation structure of life-history traits associated with planktotrophy and lecithotrophy. Our objective was to better understand persistence of this developmental dichotomy in Streblospio benedicti, and among marine invertebrates in general. Substantial additive genetic variation (75-98% of total) was detected for the following characters at first reproduction: female length; position of the first gametogenic setiger and first brood pouch; ovum diameter; three traits related to fecundity (numbers of ova per ovary, larvae per brood pouch, and larvae per brood); median larval planktonic period and the presence of larval swimming setae; but not for total number of brood pouches; larval length; larval feeding; and larval survivorship. Based on the unusual geographic distribution of development modes in this species, we hypothesize that the developmental traits have evolved in allopatry and have only recently come into contact in North Carolina. The high additive contribution to variance observed for many traits may be inflated due to (a) nonrandom breeding in nature, and (b) examination of only one component of an age-structured population at one time. Nuclear interaction variance and maternal variance accounted for 84% of the total variation in larval survivorship. This observation supports other empirical studies and theoretical predictions that nonadditive components of variance will increase in importance in individual traits that are most closely tied to fitness. A network of life-history trait correlations was observed that defines distinct planktotrophic and lecithotrophic trait complexes. Negative genetic correlations were present between fecundity and egg size, between fecundity and position of the first gametes, and between larval survivorship and median planktonic period. Positive genetic correlations were detected between fecundity and female size at first reproduction and between planktonic period and the presence of swimming setae. Intergenerational product-moment correlations were negative for larval length and fecundity, planktonic period and egg size, female size and larval survivorship, and fecundity and larval survivorship. If the genetic correlation structure observed in the laboratory persists in the field, it may constrain responses of individual characters to directional selection, and indirectly perpetuate the dichotomies associated with planktotrophy and lecithotrophy.
The morphology of marine invertebrate larvae influences population maintenance and connectivity through functional consequences for swimming, feeding, dispersal and settlement. Sea urchin echinoplutei approximate one of two forms: multi-armed larvae with arms at high elevation angles or two-armed larvae with arms at low elevation angles. According to the hydromechanical model of Grünbaum and Strathmann in J Mar Res 61:659–691 (2003), these morphologies convey either high swimming speed and weight-carrying capacity (few arms at low angles) or high stability in shear (many arms at high angles). This dichotomy, as exemplified by the multi- and two-armed larvae of Heliocidaris tuberculata and Centrostephanus rodgersii, respectively, was investigated to assess model predictions with regard to the angle of elevation of the arms. It was hypothesised that this angle differs in the two forms, multi-armed with high angles (>60°) and two-armed with low angles (H. tuberculata and C. rodgersii, respectively. The angle of elevation of the outermost arms was also determined from images of 37 additional species of echinoplutei to examine trends in arm angle and change as larvae develop. Multi-armed larvae exhibited a 3°–16° decrease in postoral arm angle from the 2–4 to 6–8 arm stage. In general, multi-armed larvae had higher arm angles than two-armed larvae and, arm angles decreased with growth in both larval forms.
Normal reproductive charateristics in echinoderms include non-maternal nutritions with a planktonic feeding developmental state, sexual reproduction with gonochorism, seasonal reproduction, and no protection of young by secondary metabolites. Deviant reproductive characteristics include maternal nutrition of the developmental stage that may be planktonic, demersal, or brooded; hermaphroditic sexual reproduction; intermittent or continuous low-level reproduction; protection of young by secondary metabolites; and asexual reproduction. We tested the hypothesis that stress, which causes a decrease in capacity for production, was a factor responsible for deviant reproductive characteristics by comparing taxa from the subphylum to species levels. In the examples used, deviant reproduction occurred in the taxa for which stress could be predicted. Although other factors undoubtably affect reproductive characteristics, the analysis indicates that stress must be considered an important one.
Egg size is a correlate of larval evolution in marine embryos. Comparing species with different egg sizes that develop via similar larvae reveals the flexibility and the constraints underlying larval forms. Clypeaster rosaceus is an echinoid that develops via a facultatively planktotrophic pluteus larva. Unlike most echinoids that develop via plutei, C. rosaceus (1) has a larger egg, with a correspondingly smaller ratio of surface area to volume, and (2) forms a large left coelom early in development. Given these characteristics, we predicted underlying changes in the allocation of embryonic tissues to germ layers. With a low surface-to-volume ratio, the C. rosaceus pluteus likely requires relatively less ectoderm than a typical pluteus, whereas the early formation of a large left coelom likely requires relatively more mesoderm than a typical pluteus. We tested this hypothesis by examining the cell lineage of C. rosaceus. We found that the boundary between ectoderm and endoderm in C. rosaceus has shifted relative to echinoids with more typical planktotrophic plutei and extends to or above the third cleavage plane at the equator of the embryo. This indicates a smaller proportional allocation to ectoderm and a larger proportional allocation to endomesoderm compared to echinoids with smaller egg sizes. On the basis of this observation, we develop a new model for the transition from obligate planktotrophy to lecithotrophy. We argue that species with larger eggs may allocate proportionally more tissue to structures selected for accelerated development. In the case of C. rosaceus, the larval cell lineage apportions more cells to endomesoderm and less to ectoderm due to the smaller surface-to-volume ratio of its larger eggs and the early formation of a large left coelom.
This chapter describes the diversity of larval stages and the patterns of development in echinoids. Most echinoids, including all but one of the edible species, are free-spawners that produce vast numbers of small, yolk-poor eggs that develop into planktonic, feeding larvae known as echinoplutei. This chapter also gives a walkthrough over the ecological challenges that echinoplutei face, and the physiological, morphological, developmental, and behavioral solutions that are utilized to respond to the problems. Tables showing the life cycle patterns and developmental character states in echinoids and the Egg characteristics of echinoids are also documented in this chapter. Other factors such as fertilization ecology, feeding mechanisms, phenotypic plasticity, and evolution of nonfeeding larvae are also well studied in this chapter. Many aspects of the basic biology and ecology of larvae, such as nutritional requirements, environmental tolerances, disease resistance, settlement preferences, dispersal ecology, and population dynamics, which are particularly important for aquaculture and commercial harvesting, remain very poorly known.
Veliger larvae ofthe coral-eating nudibranch Phestilla sibogae can metamorphose 3â€"4 days after hatching in the absence of any external food source. If deprived of a settlement stimulus, starved larvae survived as long as 30 days, but had lost meta morphic competence several days before starvation death. Fed larvae survived more than 42 days and retained metamorphic competence for as long as 42 days. Feeding by these potentially lecithotrophic larvae extended the duration of survivorship by at least 28% and the duration of the competent period by as much as 90%. There is evidence from light and electron microscopy for both digestion and uptake of phy toplankton in the larval gut. The ability to extend a brieflecithotrophic larval existence by planktotrophy may explain the wide spread distribution ofthis species in the tropical Indo-Pacific Ocean.
The tiger lucine Codakia orbicularis is a large edible clam being investigated as a mariculture candidate in the Bahamas Islands. Gonad development and spawning seasons were assessed by monthly sampling of C. orbicularis from Grand Bahama Island, Bahamas and Key Biscayne, Florida. Histological examination of clams showed most of the populations sampled to be ripe between April and November. Natural spawning probably occurs May to October. Codakia orbicularis is dioecious, seldom responding to standard spawning techniques, including physical and chemical stimuli. Artificial fertilization by carefully stripping gonads produced 15-20% viable embryos. Eggs are 108-112 μm in diameter and are singularly encased in a thick capsular membrane. Following fertilization, the gastrula, trochophore and early veliger stages develop within the capsular membrane. Upon hatching, planktonic veligers range from 150-174 μm in shell length and develop to the pediveliger stage in approximately 12 days at 24°C. Metamorphosis occurs approximately 16 days after fertilization. Larval development within the superfamily Lucinacea is characterized by formation of a gelatinous capsule. The long planktonic development and facultative planktotrophy of C. orbicularis is unusual for lecithotrophic bivalve larvae. Larvae of C. orbicularis and other lucinids may also derive nutrition from chemosynthetic bacteria located within their tissues, as reported for adults.
A simple model of the evolution of reproductive patterns in marine benthic invertebrates is presented. The aim is to discuss the dichotomous distribution of forms into those which produce a large number of small eggs with planktotrophic development, and those which produce a small number of large eggs with direct or lecithotrophic development. The fecundity of adult individuals is assumed to be inversely proportional to egg size, and the mortality of planktonic larvae is assumed to be density independent and size dependent. The growth of planktonic larvae is assumed to be sigmoid with metamorphosis occurring at a given size. The model concludes that there are at most two evolutionarily stable egg sizes. Depending on larval growth rate and death rate, the metamorphosis size, a smaller egg size, or both may be evolutionarily stable. The predictions of the model are compared to patterns observed in nature. Illustrative data are supplied mainly from prosobranch molluscs.
The sea-urchin egg completes reduction division within the ovary (Fig. 7.1 [1–2]). The unfertilized egg is a spherical cell about 90μm in diameter, surrounded by a transparent jelly coat about 30μm thick. The refractive index of the jelly coat is the same as that of seawater, making it invisible by ordinary microscope. In a suspension of India ink, however, it remains transparent because the ink particles do not penetrate it. It is easily stained with vital stains such as Janus green. Spermatozoa pass through the jelly coat at any point and enter the egg surface wherever they happen to reach it. The jelly is composed of polysaccharide and has a strong agglutinating effect on sperm, but its role in fertilization has not been fully explained. Even when the jelly coat is removed by seawater acidified at pH 5, fertilization and egg development proceed normally.
Two quite different sorts of selection could favor export of offspring from estuaries: (1) animals which spread offspring over several estuaries increase relative to non-spreaders in the population when favorability of estuaries varies independently; (2) animals which export offspring from an estuary during the larval stage increase relative to non-exporters in the population when survival or growth of larvae is greater outside the estuary. Adaptation to local conditions and the occurrence of homing in many life histories are indirect evidence against the first hypothesis. Conclusions are premature, but predictions are that (1) varying favorability among estuaries rarely favors the spread or dispersal of larvae among estuaries, (2) waters outside estuaries are often safer for larvae than waters inside estuaries, and (3) when there is selection for export of larvae from estuaries, it is selection for migration to areas more favorable to larval development rather than dispersal. In this view, the large scale spread of offspring is an accidental though important consequence of a long planktonic period; the spread of offspring confers no short term advantage.
Dendraster excentricus larvae capable of metamorphosis presented with various substrates show a significant preference for adult-associated sand. Adult D. excentricus produce a chemical cue, possibly a small peptide that is sequestered by some component in the sand and that is stable for at least 7 wk. Thus, larval settlement occurs within or adjacent to existing sand dollar beds which often contain several hundred adults per square metre. Survival of newly metamorphosed D. excentricus is significantly reduced by an extremely abundant, tube-building predator, Leptochelia dubia (Crustacea: Tanaidacea). Tanaidacean and possibly other micropredators, however, are excluded from sand dollar beds by the reworking activities of adult sand dollars. Thus, preferential settlement of D. excentricus larvae near adults of the species should result in increased larval and juvenile survival. -from Author
Egg diameters (mm) of the asteroids Diplasterias meridionalis, Anas ferias perrieri, and Anasterias rupicola and of the echinoid Abatus cordatus were 2.79, 1.75, 1.37 and 1.34, respectively. The levels (% dry wt) of soluble protein/insoluble protein/lipid/carbohydrate were 44: 15: 36: 0.4, 29: 31: 35: 0.9, 37: 28: 26:1.0, and 33:29: 35:2.1, respectively. The calories/egg were 38, 9.45 ± 1.75, 4.69, 3.70 ± 0.98, respectively. Brooded, A. perrieri (1.46 mg dry wt/individual, R = 1.47 mm) had 7.85 ± 1.5 cal/ind. Brooded, A. cordatus (1.76 mg dry wt/ind, length = 2.02 mm) had 4.17 ± 0.06 cal/ind. There was little change in the amount of organic material during development in either species, but the amount of ash increased 5-fold in A. perrieri and 13-fold in A. cordatus. The significance of the large eggs may be in the production of a large juvenile, and not in the provision of a large amount of energy for development.
A model of larval dispersal of coastal benthic invertebrates is proposed: Eddy mixing spreads larvae in the onshore-offshore direction during the period before competence to settle and continues to take larvae both onshore and offshore after they are competent to settle; predators kill larvae during both precompetent and competent periods. Distribution of larval stages of several species are consistent with the model. The model correctly predicts (1) increased competent period with increased precompetent period in comparisons among species, and (2) a competent period greater or equal to the precompetent period. The model predicts a decrease in the ratio of competent to precompetent period as precompetent period increases, which is not apparent in available data. Also, some observed competent periods are longer than those predicted by the model. Reasons for these departures from predictions are suggested. The model differs from previous optimization or maximization models for planktonic larvae by including onshore-offshore mixing and therby linking selection on the precompetent and competent periods.
Embryos deep within gelatinous egg masses of the cephalaspidean gastropod Melanochlamysdiomedea (Bergh) and the nereid polychaete Nereis vexillosa Grube develop more slowly than embryos near the surface of the egg mass. The onset of asynchronous development in egg masses of Melanochlamysdiomedea is earlier at some field sites than others. Asynchrony in egg masses of M. diomedea is especially pronounced in still water in the laboratory, and synchrony is greater and hatching completed earlier when the egg mass is divided. Development is synchronous in the thin gelatinous egg ribbons of the cephalaspidean Haminoea vesicula (Gould) from the same field sites and habitat as the thicker and asynchronously developing spheroidal egg masses of Melanochlamys diomedea. Form and size of egg masses affect rates of development, but this effect has not been included in models of life history adaptations.
Sparse and conflicting evidence concerning the mechanism and nature of developmental torsion and detorsion in the Opisthobranchia rendered necessary a full re-examination of these problems. Many contemporary general works either state or imply that during ontogeny opisthobranchs undergo 180° torsion (being identical with diotocardian prosobranchs in this respect) which is reversed in an unknown manner at some later stage of development. This theory is based on the work of Pelseneer (1911); the more detailed work of Saunders & Poole (1910) on Aplysia conflicts with Pelseneer’s views, but nevertheless these views have found wide currency. For this study, a species of dorid nudibranch, Adalaria proxima , was selected, for certain singular features of its biology rendered it possible to rear small populations through the com plete life cycle in the laboratory. A. proxima has an annual life cycle, the adults in nature dying after spawning, and their place being taken by the new generation of juvenile dorids. Death after spawning is correlated not with exhaustion of the germ cells, but with exhaustion of the food reserves built up in the pre-sexual phases of the life cycle. The species feeds mainly on an encrusting polyzoan, Electra pilosa , the dorid buccal pump playing an important part in the feeding mechanism . The spawn of Adalaria proxima shows the typical features characteristic of the egg masses of northern benthic invertebrates. The eggs are large, the number of eggs produced is small, the embryo hatches at a relatively advanced stage after a protracted em bryonic period. The early cleavage stages follow in all important respects the sequence and arrangement found in all dextrally organized gastropods. Gastrulation takes place by epiboly and the veliger form is rapidly assumed. Torsion in Adalaria is pushed back so far into development that it is no longer recognizable as a mechanical process. All the organs, as they become recognizable in sectioned postgastrulae, are arranged in the post-torsional positions, although the process of torsion has been halted far short of the full 180° found in living Diotocardia. The appearance of eyes, the development of the propodium and the structural and histological changes undergone by the mantle fold approximately 3 weeks after oviposition mark a departure from the pattern of embryonic development found in other species of dorid nudibranchs (Thompson 1957). Most of the organ systems are relatively greatly advanced in the hatching larva o Adalaria . The enlargement of the left midgut diverticulum brings about a slight rotation (continued during pelagic life) of the stomach; this is a process which is independent of torsion and was mentioned by Saunders & Poole, who, however, placed a slightly different interpretation upon it. Both dextral and sinistral components are present in the relations between the visceral and cephalopedal parts of the embryonic and larval body, but there can be no doubt that the dorids are truly dextral organisms. A complex arrangement of embryonic body cavities is present; it seems clear that the ‘coelom’ of Aplysia (Saunders & Poole 1910) corresponds to the inner perivisceral cavity of Adalaria , and that the term coelom in this connexion is a misnomer. The pelagic phase is divided into two distinct stages, during the first of which the larvae swim upwards, this behaviour being reversed at the start of the second stage. Searching behaviour characterizes the second stage alone, the selection of a suitable substrate for settlement being governed by an elaborate and highly specific sensory mechanism. Metamorphosis will only occur on a live colony of the encrusting polyzoan Electra pilosa . The cephalopedal ciliary apparatus directs a feeding current into the mouth; normal further development will, however, take place even in sterile sea-water. The larval shell is a hyperstrophic one. Retraction of the larval body is brought about by the larval retractor muscle aided in a co-ordinatory capacity by contraction of muscular elements of the inner perivisceral membrane and of the cephalopedal subepidermal muscle complex. Metamorphosis involves drastic changes, but no change in basic orientation. Detorsion and reversal of visceral flexure are brought about in two stages as the mantle fold first becomes inverted and then spreads over the dorsal surface of the post-larva. The widely stated view that the dorsal integument of the adult dorid is the product o f the evolutionary enclosure of the shell by epipodial folds is contradicted by the embryological evidence. The larval retractor muscle disappears and the muscle complex of the adult is derived from the larval subepidermal muscle complex. The perivisceral cavities are obliterated and the adult haemocoel is derived from the larval cephalopedal subepidermal blastocoelic spaces. Calcareous spicules are laid down in the mantle. Concentration and fusion of the nerve ganglia result in a symmetrical arrangement, the embryonic system having shown traces of the ancestral streptoneury. A discussion of the nature of torsion in opisthobranchs almost entirely disagrees with the views of Pelseneer (1911). All the available evidence implies that torsion in opisthobranchs is greatly modified and never approaches the full 180° twisting found in living Diotocardia. It is not, of course, suggested that Pelseneer’s basic conclusion, that the prosobranchiate condition is ancestral to the opisthobranchiate, is in need of revision. Torsion in lying as it does at the extreme opposite end of the scale from the Diotocardia, is greatly modified and is no longer recognizable as a mechanical process ; torsion in Adalaria does not occur for the same reasons as were important to the ancestral veliger, for in the dorids the larval mantle cavity does not serve to accommodate the head during retraction. The Suggestion is made that the usual manner of referring to torsion during development as involving a movement of the pallial complex from a posterior to an anterior position, is inaccurate and results from any attempt to describe ontogenetical torsion from the study of the adult gastropod alone. Finally, attention is drawn to the paradox that, although the dorid nudibranchs are the most highly evolved gastropods living (speaking in terms of gross structure), the com plex evolutionary steps which have led to the dorid have resulted in a secondary return, in many respects, to the original condition. In the adult dorid, only unimportant traces remain of the three most important steps in the structural evolution of the gastropods, visceral flexure, torsion, and bilateral asymmetry.
A theory of habitat selection is developed which, although fairly general in form, is intended to apply with some realism to the settlement behavior of planktonic larvae of marine organisms. It is assumed that different substrates represent different habitats and that the environment can be heterogenous on two scales of distance: (1) a "fine grained" heterogeneity in which larvae are exposed to a homogeneous mixture of substrate types during the settlement period, and (2) a "course grained" heterogeneity in which the composition of the mixture varies from place to place. The objective is to predict whether settlement will occur on both substrates in the fine grained mixtures or only on one--in other words, whether larvae will exhibit habitat preference. Settlement behavior is treated as an absorbing Markov chain in which the transition probabilities are the probability on encountering a substrate, the probability of metamorphosing on it, the probability of adult survival and the probability of death in th...
Following the discovery by Hans Driesch ( 1891 ) , tha@in sea urchins an isolated blastomere of the two-cell stage can develop into an hapnonic larva, much work has.been done on this subject. However, since the majority of experiments in the past have been concerned with the developmental capacity only as far as the pluteus stage, emphasis in the present investigation was place4 on the aspect of meta morphosing capacity. The inadequacy of past experiments is due to the difficulty of rearing plutei to metamorphosis in the majority of $ea urchin species, which, fortunately, can be obviated in the sand dollar Peronella japonica Mortensen. In this species metamorphosis is completed in the course of three or four days. Peronella is found in great numbers on the sandy b4ttom of a shallow lagoon in the neighborhood of the Misaki Marine Biological Station, and the breeding season extends from the latter part of June to September@ The main developmental features of this animal have @een worked out by Mor tensen (1921), but some new points were noticed by thq authors. In the present paper, the results obtained by operative experiments, an@ points regarding normal development which have a direct concern with the description of the experiments will be reported. I. DEVELOPMENT OF THE WHOLE J@ARVA Egg. The egg, about 300 @
Larvae of all seven species of echinoids occurring in coastal waters from southern British Columbia to central California have been reared through metamorphosis. Larvae of Dendraster excentricus, Brisaster latifrons, and Strongylocentrotus franciscanus can be distinguished from all others by skeletal traits alone. Living larvae of Strongylocentrotus droebachiensis and Strongylocentrotus purpuratus can be distinguished from all others by color of pigment spots combined with skeletal differences. Larvae of Allocentrotus fragilis and Strongylocentrotus pallidus have similar skeletons and pigment spots of the same color, so it is difficult to identify specimens even if they are alive. A key is provided for identification of echinoplutei.Development of Brisaster latifrons is similar to that of Brisaster fragilis in the Atlantic. The development is unusual for echinoderms in that large eggs develop into large feeding larvae with a long pelagic period. Moreover, the juveniles formed at metamorphosis have about the same diameter as juveniles of echinoids with much smaller eggs but similar pelagic periods.
Larvae of Alpheus heterochaelis from North Carolina hatch from large eggs as advanced zoeae, usually moult three times, and exhibit almost no linear growth during a short (4 days at 25°c) larval development. Stage I lasts 6 hours at most and is sometimes skipped; III lasts about twice as long as II. Individuals simultaneously exhibiting characteristics of Stage III and the postlarva were occasionally seen. The three zoeal stages and postlarva are described in detail and illustrated. Stages in embryonic and juvenile development and the hatching process are briefly described. An ‘extended’ pattern of larval development, characteristic of most alpheid species, is described in a general way, and the ‘abbreviated’ development of A. heterochaelis compared to it. At hatching, A. heterochaelis larvae bear rudimentary pereiopods and pleopods; other structures are at the same level of development in both patterns, but subsequent morphogenesis is faster in A. heterochaelis. Larval development of Synalpheus spp., some of which exhibit extreme abbreviation or direct development, is briefly described with reference to the A. heterochaelis pattern.
To test the robustness of earlier models of reproduction in marine benthic invertebrates, additional models whose assumptions differ from the earlier ones are constructed and analyzed. The primary difference is the introduction of the possibility of starvation by feeding planktonic larvae. The introduction of starvation changes none of the qualitative conclusions of the earlier models: only completely planktotrophic and completely lecithotrophic larvae can exhibit maximum reproductive efficiency; in any one environment one mode is likely to be more efficient than the other, and in some environments the evolutionary stability of both forms is possible. These conclusions concern both developmental patterns with planktonic and with benthic prefeeding development. The degree of a larva's susceptibility to starvation affects relative efficiency of planktotrophic and lecithotrophic development. Larvae which can withstand only short periods of food deprivation during the feeding phase are more likely to evolve lecithotrophy than larvae which can survive longer periods. This starvation effect is probably more pronounced in forms with planktonic prefeeding development.
1. Modes of larval development play important roles in the ecology, biogeography, and evolution of marine benthic organisms. Studies of the larval ecology of fossil organisms can contribute greatly to our understanding of such roles by allowing us to race effects on evolutionary time scales.
2. Modes of development can be inferred for well preserved molluscan fossils because the size of the initial larval shell (Protoconch I in gastropods, Prodissoconch I in bivalves) reflects egg size. Other morphological criteria are also available, and a comparative approach based on related taxa with known development may be the most reliable method. By combining larval and adult traits, it is possible to recognize modes of larval development in at least some fossil bryozoans, brachiopods, and echinoderms as well.
(a) Planktotrophic larvae arise from small eggs, are released in enormous numbers with little parental investment per offspring, and suffer tremendous mortality during and shortly after a planktic existence. These larvae feed on the plankton during development, and are commonly capable of a prolonged free-swimming existence, and thus wide dispersal.
(b) Nonplanktotrophic larvae (which include both planktic lecithotrophic forms and ‘direct developers’) generally arise from large eggs, with relatively few young produced per parent. Relative to planktotrophic larvae, nonplanktotrophic larvae generally receive greater parental investment per larva, and larval mortality is generally lower. These larvae rely on yolk for nutrition during development, and planktic durations are generally much briefer than for species with planktotrophic larvae, so that dispersal capability is considerably less. Energetic investment per egg is generally higher than in planktotrophs, but as there are lower fecundities as well it is difficult to generalize about the total energetic cost of one mode of reproduction against the other.
3. Owing to the high dispersal capability of planktotrophic larvae, it has been suggested that species with such larvae will be geographically widespread, geologically long-ranging, and exhibit low speciation and extinction rates. Species with nonplanktotrophic larvae will tend to be geographically more restricted, geologically short-ranging, and exhibit high speciation and extinction rates (again, as a consequence of their characteristically low larval dispersal capabilities).
4. Recognition of differential dispersal capabilities can play a role in paleobiogeo-graphic analyses. Concurrent study of the distribution of groups with contrasting modes of development will permit testing of hypotheses concerning timing, magnitudes and frequencies of migration and vicariance events.
5. Larval types are not randomly distributed in the oceans, but relationships with other aspects of the organisms' biology and habitats are very complex. Mode of development varies with:
(a) Ecology. A simple r–––K model of adaptive strategies is clearly insufficient to explain the observed relationships: while many ‘equilibrium’ species have nonplanktotrophic larvae, and organisms living in less prdictable environments often have planktotrophic larvae, some of the most opportunistic marine species have nonplanktotrophic larvae. Nonetheless, planktotrophic development seems most suited for exploitation of patchy but widespread habitats.
(b) Latitude. At shelf depths, planktotrophy is predominant in the tropics, and decreases sharply at high latitudes.
(c) Depth. Incidence of planktotrophy decreases with depth across the continental shelf, at least in some taxa. Beyond the shelf, many deep-sea organisms are nonplanktotrophic (e.g. most bivalves, peracarid crustaceans), but planktotrophic development appears to be present in other groups (prosobranch gastropods, ophiuroids, and bivalves inhabiting transient habitats such as sunken wood and hydrothermal vents).
These trends in developmental types will be accompanied by trends in evolutionary rates and patterns as outlined above. The study of larval ecology by paleobiologists will yield insights into the processes that gave rise to ancient evolutionary and biogeographic patterns, and will permit the development and testing of hypotheses on the origins of the patterns observed in modern seas.
Gametogenesis was studied histologically in the deep-sea species Pourtalesia jeffreysi (Wyville Thomson), P. miranda (A. Agassiz) and Echinosigra phiale (Wyville Thomson) collected during 1973–1983 from various positions at depths of 1 040 to 2 921 m in the Rockall Trough. The gonads are small and no synchrony in terms of the stage of gametogenic development was evident in females of the latter two species collected at different times of the year, indicating nonseasonal breeding. Males appear to be ripe at all times of the year. Follicle cells were well developed around the developing oocytes. Both the size range of the yolky ripe eggs (173 to 357 m diam) and potential fecundity within the range of 1 000 to 4 000 oocytes per individual, are indicative of an abbreviated, indirect, lecithotrophic mode of development occurring in all three species. Pourtalesiid postlarvae occurred also in fine-meshed trawl hauls, and their morphology is described. It was not possible to distinguish between P. miranda and E. phiale at sizes
The distribution of various types of larval development among marine bottom invertebrates has been discussed on the basis of ecological evidence by Thorson (1936, 1946, 1950, 1952) and Mileikovsky (1961b, 1965). The information at hand is reviewed anew in this paper and is re-evaluated in the light of modern pertinent literature. The interrelationships between certain larval types and their distribution are not as rigid and direct as originally assumed. This can be proved even by the copy book example of the distribution of the various forms of development among species of the coastal gastropod genus Littorina. Especially among species with wide distributional areas, local populations may exhibit greater diversity in larval types than has previously been thought. Different types of larval development have now become known to exist in different populations of opisthobranch gastropods and lamellibranchs, i.e., in invertebrate groups in which such variability had been ruled out by Thorson. Variability in the type of larval development within given species — as a function of geographical, seasonal and other environmental parameters —is also more common in other marine bottom invertebrates than formerly considered. Marine bottom invertebrates are characterized not only by the 3 main different types of larval development proposed by Thorson (pelagic, direct, viviparous), but also by a fourth type: demersal (free non-pelagic) development. This fourth type occurs at all water depths and in all geographic zones of the oceans. The most important of the 4 types is pelagic (planktotrophic) development. Thorson's rule (decrease in numbers of species possessing pelagic development from the Equator towards the Poles, and from shallow-shelf waters to greater oceanic depths) is well substantiated by new data. However, one correction is necessary: pelagic development is not completely absent in the abyssal zone, as was proposed by Thorson (1950, and later), but is represented in it by at least several species belonging to various groups of invertebrates, and is also fairly common in the bathyal zone. A detailed analysis of the distributional pattern of the different types of development of marine bottom invertebrates must further take into consideration asexual reproduction with all its different modifications. Asexual reproduction in benthonic invertebrates is ecologically significant because of its common occurrence in nature; in numerous species it is also important as a biological supplement to sexual reproduction. The vast majority of species inhabiting the shallow-shelf zone and, partly, the higher levels of the slope zone of ocean areas located roughly between the polar circles, reveals development by means of planktotrophic larval stages. In the highest latitudes and on the slopes to abyssal depths—characterized by low water temperatures, scarcity of food, increasing hydrostatic pressure and other environmental peculiarities—other types of larval development prevail and, progressively, replace pelagic development with increasing latitude or depth. The distributional patterns of the various types of development among marine bottom invertebrates form one of the most important factors determining the basic distributional dynamics of the whole benthos in all oceans, both in the geological past and at the present time.
The time interval over which growth rates are measured modifies the observed growth rates in non-linear growth curves. Growth rates obtained from a sigmoid curve such as the logistic growth equation may appear as if they were derived from the non-sigmoid von Bertalanffy growth equation when the small stage is not represented in the hypothetical growth observation. The inflection point of a sigmoid curve may be underestimated in noninstantaneous growth rate data when they are plotted on a graph against the initial sizes. This problem is significant for marine macro-benthos, whose growth is likely to be sigmoid and initiates mostly at microscopic sizes, when the popular von Bertalanffy growth equation is fitted to the observed growth rate data. Even when the von Bertalanffy growth equation appears to represent the observed growth rates adequately, extrapolation of the equation toward the smaller stage may require an independent investigation.
A method of estimating the length of the exponential growth phase is developed by solving a difference equation derived from the regression of growth increments on the initial sizes. This method facilitates quick assessments of the juvenile lifespan of animals, e.g. the coral-reef asteroid Culcita novaeguineae, which grow exponentially with very low growth rates. The juvenile life span of C. novaeguineae was estimated to be about 2 years from metamorphosis to transformation into the pin-cushion form.
In 7 species of echinoderms, 2 species of polychaetes, and 1 species of oyster with feeding larvae, larger eggs were found to contain more organic matter. Although organic matter per egg increases with egg diameter or volume, it is not proportionate to egg volume, because small eggs have more concentrated organic matter than larger eggs. There appear to be differences among higher taxa in the minimum size of freely spawned eggs. These differences could result from different relationships between mortality and reduced egg size arising from differences between larval feeding mechanisms or differences in size at metamorphosis. An egg has more than five times the organic matter of a diatom of the same size and is thus a bigger meal for suspension feeders.
Feeding mechanisms, rejection mechanisms, and feeding rates of planktotrophic echinoderm larvae of 15 species of four classes have been compared; larvae of 12 species were cultured from fertilization through metamorphosis.The currents created by the ciliated and adoral bands and the mechanisms of removing algae from suspension are similar in the larvae of all four classes. The major differences in feeding are related to the density of cilia in the circumoral field and the differences in overall configuration which distinguish the auricularia and the bipinnaria from the larvae of the pluteus type.In all the larvae the cilia of the ciliated band produce a water current away from the circumoral field. The posteriorly directed components of these currents result in forward swimming. During feeding, particles are retained at the inner side of the ciliated band but water is passed over the band. Particles are transported toward the mouth by water currents, by cilia of the circumoral field, and probably by cilia of the ciliated band. There is little exchange of water in the buccal cavity. Distribution of epidermal secretory cells varies with species.The larvae can cease feeding by directing particles over the ciliated band.Particles can be ejected from the buccal cavity by ciliary reversal and from the esophagus by contraction of esophageal muscles. These types of rejection are often aided by contractions of other muscles in varying combinations. The sets of muscles aiding rejection differ among the classes. The echinoplutei and ophioplutei frequently reverse the ciliary beat along most of the ciliated band to aid such rejection.The auricularia (Parastichopus), ophiopluteus (Ophiopholis), and echinopluteus (Brisaster, Dendraster, Allocentrotus, Strongylocentrotus) can move backwards by reversing the beat of all or most of the ciliated band. The bipinnaria (Luidia, Patiria, Evasterias, Pisaster, Pycnopodia) were not observed to reverse beat but turn by muscular contractions.Particles are sorted in the gut. The rate of passage through the gut is determined largely by the rate of passage from upper to lower stomach. The larvae ingested Sephadex spheres of diameters slightly less than the diameter of the esophagus. The larvae ate rods (Ditylum) longer than 100 or 200μ depending on the stage and species of larva. In Ophiopholis and Strongylocentrotus the presence of Ditylum interfered with feeding on smaller cells.Most fully developed larvae cleared suspensions of Amphidinium at rates of 3 to 4 μl/min and probably clear Cricosphaera and some other particles at twice this rate. Fully developed Luidia larvae cleared Amphidinium at 9 μl/min. The clearance rate is roughly proportional to the length of the ciliated band. The clearance and ingestion rates vary with concentration of food as in other suspension feeders.Questions are raised concerning the larval nervous system, the evolution of clearance rates, and ways in which each larval type may be suited to the development of juveniles of its class.
This is a book review by A. W. F. Edwards (published in Biometrics, 31(2) 229-230) of my books Biometry (by Sokal and Rohlf) and Statistical Tables (by Rohlf and Sokal) both published in 1981.
1. With the possible exception of inarticulate brachiopods, members of the oligomera (brachiopods, ectoprocts, phoronids, hemichordates, echinoderms) do not reacquire a planktotrophic larval phase once it is lost. The feeding larval stages of inarticulate brachiopods, echinoderms, and ectoprocts evolved in the Ordovician at the latest and probably originated much earlier. 2. For functional reasons, larval feeding mechanisms are more readily lost than gained in the oligomera. Loss of obligate larval planktotrophy is accompanied by an extensive loss of larval structures used in feeding. 3. Feeding larvae are unknown from several classes and orders of the oligomera: articulate brachiopods, cyclostome ectoprocts, pterobranch hemichordates, crinoids, phrynophiurid ophiuroids, and dendrochirote holothuroids. Comparison of adult and larval morphology in these and related taxa shows that the ancestors of most of these taxa had a feeding larval stage. 4. Members of the spiralia (annelids, echiuroids, sipunculids, molluscs, entoprocts) probably also lose mechanisms for larval feeding more readily than they are acquired, but new types of feeding free-swimming larval stages have evolved several times in the annelids and at least once each in the sipunculids and molluscs. Gastropods may retain flexibility in reacquiring planktotrophic larvae because encapsulated or lecithotrophic larvae often retain the structures used in feeding. 5. Differences in flexibility in reacquiring a free-swimming feeding larval stage are associated with the original type of larval feeding mechanism, degree of reorganization at metamorphosis, adult structure, and possibly egg capsules with extraembryonic nutritive material. No single explanation can account for all instances of reacquisition of larval planktotrophy. 6. In most phyla eggs range to smaller sizes among species with the original larval feeding mechanism than among species with secondarily acquired larval feeding mechanisms based on formerly juvenile structures. Secondarily acquired larval planktotrophy may not be as effective in permitting reduced egg size and hence greater fecundity.
The planktotrophic larvae of Conus lividus, C. quercinus, C. flavidus, C. striatus, and C. marmoreus were reared through metamorphosis in the laboratory and were described and figured . Minimum planktonic periods of these species were found to be 50, 30, 23, 20, and 10 days, respectively. The lecithotrophic larvae of C. pennaceus metamorphosed within 24 hours of escape from their egg capsules. Early post-hatching growth rate s of planktotrophic veligers were related to hatching size and the developmental state of the velum at hat ching. In C. pennaceus, metamorphosis was induced by the presence of a biological film. Substratum texture had no effect on rates of metamorphosis. The lecithotrophic larvae of C. pennaceus were observed to ingest unicellular algae. Experiments showed that this facultative feeding may improve the survival of C. pennaceus when the larval period is artificially prolonged.
During an investigation into the functional morphology and habits of Pandora inaequivalis (Allen, 1954; Allen & Allen, 1955), successful artificial fertilization of the eggs was carried out and the larvae reared past metamorphosis to the dissoconch stage. As nothing is known of its development, nor that of any other member of the suborder Anomalodesmata, it seems desirable to describe the development and relate it to the habits of the adult. The adults of P. inaequivalvis, on the Brittany coast, are local in their distribution and occur in sheltered sandy bays where they lie at or very close to the surface of the sand at low-water mark. The problem of maintaining each population would seem to depend on some means of limiting the dispersal of the young. Such a limitation was found to occur.
Methods P. inaequivalvis is a hermaphrodite bivalve, the testis and ovary maturing at about the same time. The eggs and sperm are shed directly into the sea.
Echinoderm larval ecology viewed from the egg Studies on the early development ofArachnoidesplacenta
- R B Emlet
- L R Mcedward
- R R Strathmann
EMLET, R. B., L. R. MCEDWARD & R. R. STRATHMANN, in press. Echinoderm larval ecology viewed from the egg. In, Echinoderm studies, Vol. II, edited by M. Jangoux & J.M. Lawrence, Balkema Press, Rotterdam. FELICIANO, A.T., 1933. Studies on the early development ofArachnoidesplacenta. Univ. Philippines Bull. Nat. Appl. Sci., Vol. 3, pp. 413-432.
Flexibility in larval life history patterns TheAmericanArbaciaandothersea urchins
- M G Hadfield
- E B Harvey
HADFIELD, M.G., 1972. Flexibility in larval life history patterns. Am. Zool., Vol. 12, p. 721. HARVEY,E.B., 1956. TheAmericanArbaciaandothersea urchins. Princetonuniversity Press, Princeton,N.J., 298 pp.
The metamorphosis of partial larvae of Peronella japonica Mortensen, a sand dollar Notes on the development of some Japanese echinoids, with special reference to the structure of the larval body
- K Okazaki
- K Dan
- Richard B Emlet Onoda
OKAZAKI, K. & K. DAN, 1954. The metamorphosis of partial larvae of Peronella japonica Mortensen, a sand dollar. Biol. Bull. (Woods Hole, Mass.), Vol. 106, pp. 83-99. RICHARD B. EMLET ONODA, K., 1938. Notes on the development of some Japanese echinoids, with special reference to the structure of the larval body. Report II. Jpn. J. Zool., Vol. 8, pp. l-13.
Egg-volume and fertilization membrane
- Snyder
SNYDER, C.D., 1925. Egg-volume and fertilization membrane. Biol. Bull. (Woods Hole, Mass.), Vol. 49, pp. 54-60.
Echinodermata, scientific results of the trawling expedition of HMCS “Thetis”
- Clark
Reproductive strategies of bivalve mollusks from deep sea hydrothermal vents and intertidal sulfide rich environments
- Berg
Studies on the early development of Arachnoides placenta
- Feliciano
Flexibility in larval life history patterns
- Hadfield
Eine neue Spatangidlarve von der Westküste Norwegens
- Runnström
Development, metamorphosis, and substrate selection of larvae of the sand dollar Mellita quinquesperforata (Leske, 1778)
- Caldwell
Estimating growth parameters from growth rate data: problems with marine sedentary invertebrates
- Yamaguchi