BULLETIN OF MARINE SCIENCE, 39(2): 145-161, 1986 LARVAL INVERTEBRATE WORKSHOP
INTRODUCTION TO THE INVERTEBRATE LARVAL BIOLOGY WORKSHOP: A BRIEF BACKGROUND
R. Andrew Cameron
The larvae of benthic marine invertebrates are puzzling creatures. They are usually minute, yet they are anatomically complex. They remain obscure among the more numerous holoplanktonic animals with whom they live, yet they play a visibly important role in benthic population dynamics. Because small and obscure larvae seldom reveal either their origins, destinations or hour-by-hour activities, they represent the life phase that is least understood in invertebrate life patterns. To replace missing data, overly simple assumptions have been used in models of community ecology and population biology. Lack of information on larval dispersal, larval nutrition and predation and the role of larvae in life history strategies is particularly apparent. Productive research into larval lives and processes continues to accumulate and for our purposes here can be divided into four areas: (1) dispersal, (2) settlement and metamorphosis, (3) life history ecology and (4) evolution.
Dispersal That the larval stage is the dispersal phase of benthic marine invertebrate life cycles is undeniable (see Scheltema this volume for review). However, only a few of the larger decapod larvae can swim faster than ocean currents and thus take an active role in their horizontal distribution (Mileikovsky, 1973). Larvae have been characterized as passively transported particles at the mercy of the currents in which they find themselves. In the Kiel Bight, the larvae of most polychaetes and echinoderms do not make significant vertical migrations, nor do they pass the discontinuity layers (Banse, 1955; 1956). Hydrographic mechanisms alone can explain the greater abundance of larvae around tropical islands or reefs and within atoll lagoons (Boden, 1952; Johnson, 1954; Hamner and Hauri, 1982). Horizontal discontinuities such as surface slicks, generated by internal waves (Fu and Holt, 1982), contain higher abundances of larvae and other plankton (Zeldis and Jillett, 1982; Shanks, 1983). But larvae unable to swim against currents can still control their movement by changing vertical position in a water column with currents which move in different directions. This principle is best illustrated by the retention of larvae in estuaries which possess a net seaward flow. The retention of larvae in estuaries may be a passive phenomenon akin to the retention of fine sediments (Korringa, 1952; DeWolff, 1974), but it is more likely that biological adaptations increase the probability of retention. For example, the larvae of some decapod species which are highly dependent on estuarine conditions were found only in the land-ward moving lower water strata while larvae of species not restricted to estuaries were found throughout the water column (Sandifer, 1975). The behaviors by which larvae actively participate in their transport are just now being described. Larvae could respond to numerous environmental cues to regulate their swim- ming activity. Thorson (1964) concluded that light is the main cue to swimming behavior and that changing responses to light can explain the observed ontogenetic differences in vertical distribution. The directional responses of crab larvae depend on light intensity, light adaptation, temperature, salinity and polarization. All crab
145 146 BULLETIN OF MARINE SCIENCE, VOL. 39, NO.2, 1986 larvae are sensitive to green light which maximally penetrates coastal waters (Forward and Cronin, 1978), while crabs from high intertidal habitats have high sensitivity to ultraviolet light (Forward and Cronin, 1979). Phyllosoma larvae of the lobster, Panu/irus longipes, exhibit additional maxima at 470 nm and 615 nm, probably because they are also adapted to oceanic waters with maximum transparency at 400-500 nm (Ritz, 1972). In general, all crab zoeal stages are photopositive (Forward and Costlow, 1974; Sulkin, 1975), while megalopas may be either photopositive (Sulkin, 1975; Bigford, 1979) or indifferent (Forward and Costlow, 1974). The larvae of the crab, Rhithropanopeus harrisii, exhibit complex vertical migration at four zoeal stages so that they would remain in the strata of least net flow thereby reducing their longitudinal transport (Cronin, 1982). Evi- dence for an endogenous rhythm in these behaviors also exists (Cronin and For- ward, 1979). It is not clear whether negative phototaxis or increased sinking rate is the mechanism by which larvae ready to settle seek the sea floor. For example, cyprids, but not nauplii, of barnacles cease swimming in light (Crisp and Ritz, 1973). Photonegative behavior may be most important at the very moment of settlement because it brings the larvae into cryptic and shaded habitats which could provide protection from silt, predation and other sources of mortality (Buss, 1979). Gravity is the most constant physical factor to which larvae can respond. Cen- trifugation experiments which exclude the effects of buoyancy, dissolved gases and pressure demonstrate direct, active orientation to gravity in larvae of the bryozoan Bugula stolonifera, while those of B. neritina possess some other means of maintaining a vertical orientation (Pires and Woollacott, 1983). Larvae less than 1 mm in length, a size at which viscous forces are more important than inertial ones, generally swim by means of cilia alone while larger larvae, at a size where inertial forces gain importance, can efficiently use muscular activity (Vogel, 1981). The relationship between viscosity and inertia (the Reyn- olds number) incorporates terms for the length oflarvae and the mean swimming velocity. At the low Reynolds numbers larvae experience, larval length not shape is the important morphological parameter. Thus the diverse morphologies of small invertebrate larvae do not improve swimming efficiency per se but rather have developed to place the cilia at efficient positions for swimming and feeding (Strath- mann, 1974b; Emlet, 1983; Chia et al., 1984). MacBride (1914) states that the larval phase of development represents a former condition of the adult in keeping with Haeckel's biogenetic law. Citing larval transparency, small size and specialized swimming structures, Garstang (1922) countered MacBride's ideas and stated that larvae were specially adapted for a planktonic existence. This last view has evolved into the thesis that larval forms are maintained under selection for dispersal. Strathmann (197 4a) pointed out that the spread of sibling larvae could confer short-term advantages to individuals by permitting the larvae to sample a number of independently varying habitats. These ideas were further pursued in a series of models which investigated the effects of scale of dispersal (Palmer and Strathmann, 1981). They showed that at larger scales an asymptote of maximum relative advantage is reached and furthermore, that the asymptote is higher and more slowly approached as increasing environ- mental variance is factored in. More recently Strathmann (1980) has expressed the opinion that no evidence exists to either support or refute the short-term advantage hypothesis. The larval planktonic period can be divided into two parts: a precompetent period before the larva is capable of settling and a competent period during which it is capable of settling if the appropriate environmental cues are encountered. A CAMERON: INTRODUCTION TO INVERTEBRATE WORKSHOP 147 mathematical model using eddy diffusion for larval dispersal predicts that the length of the precompetent and competent larval periods will covary and that the competent period will be equal to or greater than the precompetent period (Jackson and Strathmann, 1981). The scant data on these periods agree with the predictions. One optimization model for the duration of the competent period concerns avail- ability of favorable substrata and the balance of risks of settling at a suboptimal spot or returning to the plankton to search further (Doyle, 1975). Using examples from nudibranch molluscs, Todd and Doyle (1981) propose a settlement-timing hypothesis which states that planktotrophic larval strategies alone are of sufficient length to bridge the period between optimum spawning times and optimum set- tlement times. In subsequent discussions of this idea Hadfield and Switzer-Dunlap (1984) offer the alternate hypothesis that the broad reproductive season and large juvenile size are an adaptation to a variable food supply at settlement. In a theoretical treatment, Istock (1967) makes a case for viewing the larval phase as selected to exploit an alternate food source away from competition with adults. These alternative views propose a variety of selective forces other than dispersal which could account for the maintenance of a larval stage. The difficulty of tracking larval transport renders most conclusions about dis- persal debatable. Until the fate of discrete populations of larvae with known pedigrees can be described in time and space, the investigator is left with only partially reliable estimates on which to base predictions about population dy- namics and life history parameters.
Settlement and Recruitment Many, if not all, benthic marine invertebrates show both temporal and spatial variation in recruitment. The study of the environmental factors that are the proximate causes for the observed variation has been a perennial activity of marine biologists (Thorson, 1950; Frank, 1975). The reasons for these investigations include practical application to fisheries (Hayman and Tyler, 1980) as well as more theoretical considerations of life-history evolution (Murphy, 1968; Reaka, 1979). Although many investigators have produced plausible models for recruit- ment, enough gaps still exist to ask the fundamental question: What determines recruitment density and its temporal and spatial variation? Because recruitment is one element in a complex life-cycle, it is important to ask how variations in any of the phases affect recruitment. If recruitment is defined as the appearance of the smallest recognizable indi- viduals in a population, then the distribution in time and space of recruiting animals will be influenced by (1) larval availability, (2) substrate selection and metamorphosis, and (3) early juvenile mortality. The interaction of these three elements dictates specific patterns of recruitment. For example, small juvenile red sea urchins in southern California are found under larger adults which protect them from predation (Tegner and Dayton, 1977). Laboratory-reared larvae will settle readily on rocks taken from immediately beneath an urchin as well as from a long distance away, suggesting that early juvenile mortality or migration pro- duces the observed pattern rather than settlement preference (Cameron and Schroeter, 1980). The factors which have been frequently cited as instrumental in shaping the abundances of animals include predation (Paine, 1966), competition for space (Connell, 1975), physical disturbances (Dayton, 1971), and competitive networks (Buss and Jackson, 1979). A common element in many of these constructs is the implicit assumption that the important interactions occur among adult animals 148 BULLETIN OF MARINE SCIENCE, VOL. 39, NO.2, 1986 or, at least, that recruitment is constant in time and space. This view has been challenged recently on philosophical (Dayton, 1979) and empirical (Underwood and Denley, 1982) grounds. These challengers point out that the importance of variation in recruitment has been largely neglected and, there is evidence to suggest that this variation may playa crucial role in the dynamics of communities on hard substrata (Sutherland and Karlson, 1977; Keough, 1983; Underwood and Denley, 1982; Connell, 1985). Enhanced larval abundance in either time or space can result in enhanced recruitment. Even though large populations of sand dollar larvae (Dendraster excentricus) occur annually in Monterey Bay offshore of established sand dollar beds, size frequency measurements in one bed suggest that substantial recruitment only occurred in one of the two years studied (Cameron and Rumrill, 1982). Small-scale local currents probably prevented the transport of larvae onshore during one year. In Panama, peak settlement in the sand dollar, Encope stokesi, occurs during the dry season when strong upwelling enriches coastal waters and causes increased phytoplankton production (Dexter, 1977). Ebert (1983) postu- lates that the correlation between recruitment of the sea urchin, Strongylocentrotus purpuratus, in southern California and upwelling may be a result of increased larval survival even though upwelling should aid in the offshore transport of the larvae. Settlement in invertebrate larvae begins with a sequence of larval behaviors that are essentially the same for many groups (Thorson, 1950; Meadows and Campbell, 1972; Crisp, 1974). Photopositive and/or geonegative larvae become photonegative and/or geopositive (or just sink) to approach suitable surfaces for settlement. Temporary attachment alternates with continued swimming, usually in ever tighter circles, until a preferred site is chosen for metamorphosis. Barnacle cyprids literally walk on their adhesive antennules in the last phases of these searches (Knight-Jones and Crisp, 1953). Many marine invertebrate larvae settle on surfaces filmed by micro-organisms and their extracellular products (Crisp, 1974; Scheltema, 1974; Meadows and Campbell, 1972). In such diverse groups as cnidarians (MUller, 1973), polychaetes (Wilson, 1955), oysters (Cole and Knight-Jones, 1949), bryozoans (Brancato and Woollacott, 1982), and echinoids (Hinegardner, 1969) are found examples of larvae that settle in response to microbial cues. Based on specific sugar inhibitions, a lectin-ligand mechanism has been proposed for the interaction between the polychaete Janua brasiliensis and microbial extracellular products (Kirchman et a1., 1982a; 1982b). The biological interactions are far more subtle and possibly more important than non-biological ones in determining settlement (Scheltema, 1974). Larvae from several taxa of encrusting organisms avoid substrata where there is a high probability of death from overgrowth by competitively dominant forms (Gros- berg, 1981). In the laboratory, the bryozoan Bugula pacifica will delay settlement when presented with extracts of the compound ascidian Diplosoma macdonaldi which will overgrow the bryozoan (Young and Chia, 1981). An arborescent bryo- zoan settles in dense aggregations which were experimentally shown to discourage predation even though individual growth is reduced. This observation prompted the author to suggest that gregarious settlement requires cooperation and is a response to density dependence in the outcome of interference competition (Buss, 1981). Woodin (1976) stated that adult-larval interactions maintain shifts in in- faunal abundance patterns. In dense assemblages, infaunal filter feeders exclude settling larvae which results in sharp boundaries between types of assemblages. This hypothesis is supported by evidence that adult deposit feeding polychaetes CAMERON: INTRODUCTION TO INVERTEBRATE WORKSHOP 149 reduce the survival of larvae (Wilson, 1980; Levin, 1981). On the other hand, high densities of clams in microcosm experiments did not significantly reduce the recruitment of larvae (Maurer, 1983).
Metamorphosis The metamorphosis of marine invertebrate larvae consists of a series of changes that prepare a pelagic larval form to take up a benthic life. Metamorphosis may be an abrupt event that occurs over a very short period as is the case of echinoids (Cameron and Hinegardner, 1974) or ascidians (Cloney, 1978) or it may be gradual and best marked by the change of habitat as in some polychaetes (Eckelbarger, 1978). Often these changes occur in response to an environmental cue. The rapid metamorphosis of sea urchins and ascidians results from morpho- genetic movements due to micro filament-mediated cell shape changes. Meta- morphosis in the sea urchin Lytechinus pictus occurs in three steps over 45 min- utes: the larval arms bend to expose the urchin rudiment to the surface, the larval epidermal cells change shape collapsing the tissue onto the presumptive aboral surface, and finally the former lining of the vestibule of the urchin rudiment envelops the collapsed tissue to form the adult epithelium (Cameron and Hine- gardner, 1974; 1978). Metamorphosis in the ascidian tadpole begins with attach- ment by means of the everted adhesive papillae and is rapidly followed with the resorption of the tail (Cloney, 1978). Tail resorption occurs by means of cell- shape changes in the caudal epidermis or notochordal cells depending on the species (Cloney, 1966; 1972). In both of the cases cited, the cell shape changes can be inhibited with Cytochalasin B which interferes with the formation of 50- 70-p.m microfilaments. Metamorphosis can also result from muscular movements coupled with the secretion of adhesive substances and external coats. The attachment and meta- morphosis of the polychaete, Spirorbis spirorbis, begins with the secretion of a mucus by the dorsally situated attachment gland. The larva then rolls over ad- hering to the surface by these secretions. The ventral gland bulge is now directed upward and the primary mucoid tube is derived from it by secretions which flow down over the larvae and the attachment mucus (Nott, 1973). Cellu1arioid chei- lostome bryozoans attach at metamorphosis by secretions of the metasomal sac epithelium which is everted by muscular contraction (Reed and Woollacott, 1982). The newly formed ancestrula becomes covered with a pellicle secreted by the neck cells of the metasomal sac and carried over the body by the coronal cilia (Wool- lacott and Zimmer, 1971). However, the extension of the pallial epithelium and meta somal sac to form the adult epithelium involves microfilament-mediated cell shape changes (Reed and Woollacott, 1983; Lyke et al., 1983). Metamorphosis in opisthobranchs proceeds by muscular contraction and dif- ferential growth in several stages: loss of the velum, shell and opercular detach-, ment, and sinking of the visceral mass into the foot (Bonar and Hadfield, 1974; Harrigan and Alkon, 1978). The velum is not always lost but its dissociated cells form the first post-larval meal, or may be incorporated into the head epithelium (Hadfield, 1978). The shell is cast offby a contraction ofthe larval retractor muscles pulling the visceral mass from the surrounding shell (Bonar, 1978). Detachment from the shell may occur before loss of the velum, but they occur within a few hours of each other (Perron and Turner, 1977). The adult epithelium fOfIJ1Swhen the thickened mantle edge covers the visceral mass (Thompson, 1958) or when the mantle is lost leaving the propodial epidermis over the visceral mass (Bonar, 1978). 150 BULLETIN OF MARINE SCIENCE, VOL. 39, NO.2, 1986
Although the available information is still scant, it appears that larvae carry out the irreversible events of metamorphosis when they sense specific chemical substances associated with their preferred substrate (see Hadfield, this volume, for review). This chemoreception event implies the presence of cellular receptors for the substr~te associated chemicals and some method of integrating signals over the entire larva. The integration of a receptor induced chemical signal by larval nervous elements is less well documented. The evidence falls into two classes: (1) the description oflarval tissues with morphological and physiological attributes of nervous function and (2) the demonstration that altered ionic com- position and purified neurotransmitters can induce metamorphic changes (see Hadfield, this volume, for review). The most complete evidence exists for echi- noids (Cameron and Hinegardner, 1974; Ryberg, 1977; Burke, 1982; Satterlie and Cameron, 1985) and gastropods (Morse et al., 1979; Morse and Morse, 1984; Hadfield, 1984; Hadfield and Scheuer, 1986; Hirata and Hadfield, 1986). Although the specifics of morphogenesis are different for each group, the patterns of regu- lation appear similar. Life History Ecology Life history theory attempts to determine the characteristics ofa life cycle which predict survival; or as Stearns (1983) poses the question: "What is the minimal representation of the organism and its interactions with its environment that we must consider to understand evolutionary change?" Students of larval biology have concerned themselves for the most part with parameters such as the envi- ronmental influence on reproduction and mortality, the cost of reproduction and relative costs of different reproductive strategies (see Hines, this volume, for re- view). One example of the influence of the environment on life history traits is the part played by the environment in the timing of reproduction. Spawning in re- sponse to changes in light levels has been documented for cnidarians (Yoshida, 1959), bivalves (Sastry, 1979), and other groups (see Segal, 1970, for review). Temperature change serves as a cue for bivalves (Sastry, 1979) and asteroids (Pearse, 1965). Recently, photoperiod has been shown experimentally to syn- chronize gametogenesis and spawning in polychaetes (Garwood, 1980) and sea stars (Pearse and Eernisse, 1982). The adaptive significance of these responses is most obvious in the case where spawning occurs in response to increased phy- toplankton concentration and the plant cells could serve as food for the larvae (Himmelman, 1975). However, another view is that the major importance ofa singlecue is to promote synchrony of spawning and thereby maximize fertilization. Fecundity is inversely proportional to egg size when compared in groups of closely related species of similar adult size (Thorson, 1946; Coe, 1949; Kohn, 1961). Furthermore, there is a dichotomous distribution of forms into those with small eggs and planktotrophic development and those with large eggs and direct or lecithotrophic development (Thorson, 1950; Mileikovsky, 1971). A number of theories have been put forth to explain these correlations. Vance (1973a; 1973b) presents a model which parallels Thorson's ideas, and attempts to explain the evolution of developmental mode on the basis of optimized reproductive effi- ciency. Christiansen and Fenchel (1979) expanded these ideas to develop a model that predicts evolutionarily stable offspring sizes for a given reproductive effort. The fecundity question is even more complicated because the size is measured in terms of diameter or volume not units of energy. The size of marine invertebrate eggs is not proportional to organic content because small eggs have more con- centrated organic matter than large ones (Turner and Lawrence, 1979). Also, there CAMERON: INTRODUCTION TO INVERTEBRATE WORKSHOP 151
appear to be differences among higher taxa in the minimum size offreely spawned eggs (Strathmann and Vedder, 1977). Direct development and lecithotrophic development are often associated with brooding or encapsulation: life history tactics which protect the embryos for some period of their development. A simple probability model shows that even a short period of encapsulation can reduce overall mortality and that the benefit of en- capsulation is greater at lower mortalities (Pechenik, 1979). In an extension of this model which predicts evolutionarily stable mixed life histories, Caswell (1981) concludes that the cost of encapsulation is the pivotal factor. Both the strength and proportional energy allocation to capsules increase with increasing devel- opment time in 10 species of Hawaiian Conus, and the increasing allocation to capsules as a function of egg size reflects the cost of producing stronger capsules (Perron, 1981). The benefits of encapsulation could include protection from en- vironmental stress and predation. However, predation on encapsulated embryos has been shovynto equal or exceed that on planktonic stages (Brenchley, 1982). Egg capsules may offer protection by reducing the magnitude and rate of the decrease in salinity when exposed to fresh water (Pechenik, 1982). Greater brood care is associated with smaller adult size in some but not all invertebrate taxa. None of the varied hypotheses which account for the association between brooding and adult size fit all the reported cases. Possibly different life history traits in different taxa form the basis for selection of the association (Strathmann and Strathmann, 1982). Although current models of life history tactics assume that reproductive pa- rameters are free to co-evolve, many taxa exhibit strong allometric constraints which restrict the possible range of variability in reproductive effort relative to body size. Among the Crustacea, studies on reproductive effort in amphipods (Nelson, 1980), barnacles (Hines, 1978; 1979), and others reveal a strong corre- lation between body size and reproductive output. Comparisons of crabs spanning four orders of magnitude in body weight indicate that female body size is the principle determinant of reproductive output and that allometric limitation on space available for yolk accumulation is the main constraint on brood size (Hines, 1982). Considering the relative stability of populations over long time periods and the large fecundities of many marine invertebrates, the mortality of the larval stage must be enormous (Thorson, 1950). Unfortunately, actual estimates are rather rare in the literature. Bivalve larvae in estuaries and crustacean larvae with discrete larval stages have provided the best estimates. Based on known rate of loss from the estuary and decrease in numbers over the time following the spawning peak, Korringa (1941) estimates, depending on temperature, 2.5 to 10% survival to settlement of oyster larvae in Oosterschelde Basin, Netherlands. Survival rates for oyster larvae in Pendrell Sound, British Columbia (Quayle, 1964) and Mer- cenaria larvae in Little Egg Harbor, New Jersey (Carriker, 1961) fall near the lower of Korringa's values. By comparing number oflarvae at each stage and the duration of stage, the mortality of barnacle larvae in Miramichi Estuary, New Brunswick was estimated at 14.5% per day, which agrees closely with calculated rates (Bousfield, 1955). Similar levels of 19.6% per day were obtained for the pink shrimp, Penaeus duodarum, in the Gulf of Mexico (Munro et al., 1968). Extrap- olating from data on reproductive output and recruitment (Sarver, 1979) for the opisthobranch, Aplysia juliana, only 0.002% of the larvae produced survive the 30-day-plus planktonic period. All of these studies and many more not mentioned are plagued by uncertainties related to sampling: are the investigators sure they are always sampling the same larval populations? 152 BULLETIN OF MARINE SCIENCE, VOL. 39, NO.2, 1986
Although predation has long been regarded as a major source of mortality for pelagic larvae, reports of specific predators have only recently appeared. The major plankton predators are hydromedusae, scyphomedusae, siphonophores, cteno- phores, chaetognaths, copepods, euphausids, shrimp and some invertebrate lar- vae. The larva of the polychaete, Magelona, preys exclusively on larval bivalves (Lebour, 1923). This is the only known predator specializing on larvae; most are generalists which may exploit meroplankton seasonally. The setae oftrochophores can function in larval defense against four planktonic predators with different feeding mechanisms (Pennington and Chia, 1984). Hydromedusae and scypho- medusae prey on larvae at least occasionally (Lebour, 1923; Southward, 1955; Thiel, 1964; McCormick, 1969; Zelickman et al., 1969; Spencer, 1975; Larson, 1976) and feeding rates of these cnidarians in dense aggregations measured on copepods or Artemia nauplii are high enough to account for significant reductions in larval populations (Fraser, 1969; Huntley and Hobson, 1978). The clearest case where a predator has significantly affected larval populations is the ctenophore, Mnemiopsis leidyi. These ctenophores, which produce consis- tent annual blooms in some estuaries of eastern North America, eat larval bivalves and gastropods and copepods. When Mnemiopsis was rare in Barnegat Bay, New Jersey, the settlement of Ostrea, Teredo, and Bankia was heavy and poor bivalve settlement occurred when the ctenophore was dense (Nelson, 1925). In a 2-day period when the ctenophore was dense the density of oyster larvae dropped from 608.5 per liter to 0.54 per liter. In contrast, the oyster larvae dropped from 362 per liter to 87'per liter on a comparable day in a year when the ctenophore was rare. In the York River Estuary, the density of annelid and barnacle larvae varied inversely with the ,Mnemiopsis density (Burrell and Van Engel, 1976). Decapod larvae are mostly unaffected by Mnemiopsis (Cronin et al., 1962). Also low food levels are probably a source of larval mortality due to starvation or prolonged planktonic periods which increase the exposure to predation (Thor- son, 1950). The problem of nutrition is compounded by the demonstrated ability of larvae to take up dissolved nutrients (Manahan et al., 1983; de Burgh and Burke, 1983). An important role for nutrition in larval survival is suggested in the case of the asteroid Acanthaster planci which experiences sudden, periodic population increases in the tropical Indo-Pacific (Birkeland and Randall, 1979). These increases follow heavy rains and Birkeland (1982) hypothesizes that runoff provides nutrients causing phytoplankton blooms which enhance the survival of Acanthaster larvae. The increased survival of the larvae results in an outbreak 3 years later. This hypothesis is further supported by quantitative studies of the feeding and nutrition of these larvae which indicate that they cannot survive on the levels of phytoplankton normally found in Great Barrier Reef waters (Lucas, 1982).
Evolution The importance of the larval phase to the distribution and evolutionary history of invertebrates has only recently come to be appreciated by paleontologists (see Strathmann, this volume, for review). Demonstration of the early ontogeny of fossil organisms was long considered elusive, but it is clear that patterns oflarval development can be inferred in well preserved molluscan shells because the ac- cretionary form of growth retains a record of early developmental stages (Lutz and Jablonski, 1981). Elements of the larval skeleton of echinoids are incorporated into the adult plates and the crystal patterns of the adult apical plates in fossil remains can be analyzed to determine trophic mode (Emlet, 1985). CAMERON: INTRODUCTION TO INVERTEBRATE WORKSHOP 153
The role of larval dispersal in species-level evolutionary processes seems well established in the paleobiological literature (Shuto, 1974; Scheltema, 1977; 1978; 1979; Crisp, 1979). Because planktotrophic species can disperse widely, they have broad geographical ranges and local catastrophes are unlikely to eliminate a species over its entire geographical range. Furthermore, larvae from other, persistent populations can replenish populations reduced by local extinction (Jablonski and Lutz, 1983). Consequently, species without planktotrophic larvae tend to be geo- logically short-lived and they are characterized by high extinction rates. Hanson (1978; 1980; 1983) found that Lower Tertiary volutid gastropod species of the Gulf Coast having "planktonic" larvae had a mean species duration of 4.4 million years (MY) while those with "non-planktonic" larvae had a mean duration of 2.2 MY. Furthermore, the geographical ranges of the planktonic species averaged twice those of the non-planktonic ones. Among the Gulfand Atlantic coastal Plain gastropods from the Late Cretaceous, planktotrophic species had a mean duration of approximately 6 MY and a mean geographical range of 1,500 km, while non- planktotrophic ones have only about 3 MY and a mean range of 610 km (Jablonski, 1979a; 1980). However, the degree of environmental tolerance could also playa role in determining extinction rates and ranges (Jackson, 1974; 1977; Jablonski and Valentine, 1981). This factor could be responsible for the lack of a simple, direct relationship between longevity or range and developmental mode in Late Cretaceous bivalves (Jablonski, 1979a). The ability to disperse should also affect speciation rates. Wide dispersal of planktotrophic larvae should maintain gene flow between disjunct populations; in contrast, species with restricted dispersal will tend to have local populations that remain isolated after initial colonization or separation from the parent pop- ulation. Consistent with these predictions are electrophoretic and biochemical studies on living populations in which lower levels of genetic differentiation are exhibited by species with planktotrophic larvae than those with nonplanktonic or nonplanktotrophic ones (Berger, 1973; Gooch, 1975; Ward and Warwick, 1980). However, some planktotrophic species exhibit clinal or geographical dif- ferentiation on a variety of scales. Most authors have attributed this to differential post-settlement mortality rather than a lack of dispersal (Struhsaker, 1968; Mar- cus, 1977; Milkman and Koehn, 1977; Ament, 1979). Furthermore, Scheltema (1977; 1978) has presented a model which suggests that lineages or clades having widely dispersing planktotrophic larvae will produce new species via "punctuated equilibria" (Gould and Eldredge, 1977), when larvae by chance invade newly available, highly suitable habitat, become isolated and rapidly evolve. Barriers to planktonic larval transport are hard to envision; however, the information on larval transport in general is scant. An allopatric speciation mechanism for limpets has been proposed in which warming trends allow latitudinal range extension into warm water embayments where populations become isolated during later cooling periods (Murphy, 1978). Patterns oflarval development have been considered to be highly conservative and, indeed, have been used as characters in phylogenetic hypotheses at higher taxonomic levels (deBeer, 1958; Jagersten, 1972). As evolutionary patterns in marine invertebrates become better understood, it is clear that developmental histories have undergone considerable change and that larval stages have been as subject to natural selection as adult stages. Jagersten (1972) argued that plank- totrophy is the primitive condition in many phyla and that the common ancestor of these phyla must have had a planktotrophic larval stage. However, numerous groups within these phyla have independently adopted nonplanktotrophic life patterns. In the case of neogastropods, Jablonski (1979a; 1979b) suggested that selection for nonplanktotrophy may be a means of increasing speciation rates 154 BULLETIN OF MARINE SCIENCE, VOL. 39, NO.2, 1986 during adaptive radiation. There are striking differences in functional morphology between planktotrophic and nonplanktotrophic echinoderm larvae and Strath- mann (1978a; 1978b) has suggested that it might be impossible for an echinoderm lineage to regain complex larval feeding mechanisms once they are lost. For example, crinoids are exclusively lecithotrophic, although they inhabit shallow tropical and temperate seas where species from other groups possess plankto- trophic larvae. It is possible that this developmental pattern resulted from the Permo- Triassic extinctions, selectively or by chance excluding lineages with plank- totrophic larvae. The elimination of over 90% of the invertebrate species at this boundary renders this suggestion quite plausible (Raup, 1979). The simple relationship between species longevity over evolutionary time and larval feeding mode holds true during times of background extinction. However, mass extinction episodes result in changes in species composition that are neither random cullings of species nor intensifications of the background extinction pat- tern (reviewed in Jablonski, 1986). The change in species numbers at major extinction events has, in one case (the end-Permian event), involved a differential loss of planktic species and, in another (the end of the Cretaceous), been propor- tionately equal with respect to developmental mode. The traits that enhance survivorship during background extinction regimes may have little effect during mass extinction episodes. Indeed, mass extinctions may reduce the predominance of species-rich clades selected during more gradual background extinction regimes.
Workshop At Friday Harbor Laboratories of the University of Washington, investigators met from 27 to 31 March 1985 to discuss current research on invertebrate larvae and to address some of the questions mentioned above. Although the participants work in a variety of fields in biology, including population genetics, paleontology, ecology, developmental biology and invertebrate zoology, the common thread throughout was an interest in the larval forms of invertebrate animals and how they contribute to an understanding of the biology of the life pattern to which they belong. The meeting was evenly divided between presented papers and open discussions that followed the paper sessions. The sessions were divided into four sub-topics (dispersal, settlement and recruitment, life histories and evolution) which served to conveniently organize the four days of meetings although con- siderable overlap existed 'between areas. The proceedings of this workshop follow.
This enterprise is very much the product of a collaboration by the members of the Organizing Committee: Drs. Hadfield, Hines, Scheltema and Strathmann and 1. Without their advice, patience and labor, it would not have occurred. I thank Friday Harbor Laboratories and its Director, Dr. D. Willows, for graciously providing a venue for the event. Dr. R. Strathmann, Associate Director, Friday Harbor Laboratories, handled local logistical arrangements. The Office of Naval Research provided funds in support of communications and publication costs. And lastly, I would like to thank the investigators who participated in the workshop and contributed to these proceedings.
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DATEACCEPTED: May 29, 1986.
ADDRESS: Division of Biology 156-29. California Institute of Technology, Pasadena, California 91125.