MARINE ECOLOGY PROGRESS SERIES Vol. 31: 179-184, 1986 - Published July 7 Mar. Ecol. Prog. Ser.

Life history patterns of the dorid nudibranchs Doridella steinbergae and Corambepacifica

Paul M. Yoshioka

Department of Marine Sciences. University of Puerto Rico, Mayaguez. Puerto Rico 00708, USA

ABSTRACT: Benthic life history traits of 2 ecologically similar nudibranchs, DorideUa steinbergae and Corambepacifica, were determined from laboratory rearing studies and examined in context with r and K selection. Although C. pacifica can produce a greater number of larvae, D. steinbergae has the higher maximum rate of natural increase, r,, due to an earlier age at reproduction. Also, D. steinbergae is more efficient in the acquisition and utihzation of their common prey resource. Thus, a trade-off in r and K attributes does not exist between the 2 nudibranchs. A 'bet-hedging' interpretation, entailing a trade-off between reproductive o.utput and probability of successful reproduction, provides a more suitable explanation of llfe history pattern. Bet-hedging occurs when sibling larvae settle on different kelp blades, thereby averaging out local variations in prey abundances.

INTRODUCTION periods unfavorable to the sunrival of other life stages. Other approaches have concentrated on more general Central features of life history pattern can be sum- patterns of survivorship. For instance, delayed repro- manzed by 3 traits: (1) the total number of offspring an duchon decreases the rate of population decline and organism produces; (2) its age at each reproduction; (3) may be advantageous for species which traditionally ~tsage at death (Mertz 1970). The scope of possible experience long periods of unfavorable conditions combinations of life history tralts are evidently limited (Mertz 1971). Also, delayed and iteroparous reproduc- by trade-offs which prevent the evolution of species tion may be favored for marine fish species under possessing only desirable characteristics, such as high conditions of highly variable juvenile survival (Mur- fecundity, early reproduction, and long life (Law 1979). phy 1968). Specific details of costs and benefits associated with Perhaps the best known theory of life history pattern trade-offs generally involve the interaction of life his- is that of r and K selection (MacArthur & Wilson 1967, tory traits with physiological and populational conse- Pianka 1970, 1974). As derived from the logistic equa- quences involved in the acquisition and utilization of tion, r is defined as the intrinsic rate of natural increase resources. For instance, limited metabolic resources and K, the carrying capacity. Frequently, K is may allow rapid growth rates of individuals at a cost of described in terms of superior competitive ability in delayed reproduction which, in turn, results in reduced the acquisition and utilization of limiting resources population growth rates (e.g. Cole 1954). (e.g. MacArthur & Wilson 1967). Also, K selection is Selective forces underlying trade-offs have often characteristic of equilibrium conditions and r, of been attributed to specific ecological factors. Paine unsaturated environments (Pianka 1974). In essence, (1977) suggested that size-specific predation on smaller selection for r and K is mutually antagonistic and (younger) individuals favors the combination of rapid involves trade-offs between productivity (r) and effi- growth rates and delayed reproduction if individuals ciency of resource utilization (K) (MacArthur & Wilson can thereby attain sizes exceeding the capacity of their 1967). predators. Murdoch (1966) demonstrated that in- A major difficulty of life history pattern studies is creased mortality is associated with reproduction in that alternative interpretations may not be mutually the carabid beetle Agonum and postulated that exclusive and predict similar results. For example, enhanced adult survival resulting from delayed repro- Murphy's (1968) model (termed 'bet-hedging' by duction may enable populations to persist through Stearns 1976) demonstrates that variable juvenile mor-

O Inter-Research/Printed in F. R. Germany 180 Mar. Ecol. Prog. Ser. 31: 179-184, 1986

tality results in attributes associated with K selection, species level, a group rearing of newly settled veligers and variable adult mortality in the attributes of r selec- was used to estimate growth and feeding rates of tion. Differences between alternative approaches are smaller individuals. not tnvial with respect to the underlying selective Total body length and the number of zooids eaten mechanisms. Murphy (1968) emphasized the variabil- and egg masses were laid were recorded when the ity of mortahty, irrespective of the source, while r and food supply was changed. Both DondeLla steinbergae K selection is based on the more restrictive premise and Corambe pacifica feed by rasping through the that competition in terms of population growth rates frontal membrane and sucking out the contents of (e.g. Cole 1954, Lewontin 1965) or efficiency (Mac- Membranipora membranacea zooids (e.g. McBeth Arthur & Wilson 1967, Pianka 1974) represents the 1968). Feeding rates were thus based on counts of appropriate selective framework. Unfortunately, tests empty zooids before and after the addtion of nudi- to distinguish between alternatives are usually lacking branchs. Controls showed negligible loss of zooids (Steams 1977). over the time intervals involved. The number of eggs In this report I examine the life history patterns of 2 laid were based on subsample counts of egg masses. dorid nudibranchs, Dondella steinbergae Lance and Laboratory experiments examining the relative Corambe pacrfica MacFarland & O'Donoghue. These efficiencies of the nudibranchs in the acquisition and nudibranchs are very similar in physical appearance utilization of zooids involved only pre-reproductive and commonly CO-occur in the Macrocystis pynfera (L.) indviduals. D. steinbergae ranged in size from 0.35 to kelp canopy feeding on their only known prey, the 0.42 cm and C. pacifica from 0.60 to 0.73 cm. Equal bryozoan Membranipora membranacea (L.)(MacFar- numbers of both species were placed in test containers land & O'Donoghue 1929, Lance 1962, McBeth 1968, with algal blades heavily encrusted with approxi- Seed 1976, Yoshioka 1982a. Harvell 1984). M. mem- mately 19 200 M. membranacea zooids. Food was not branacea population sizes may vary by more than an changed in the course of the experiment. The number order of magnitude in 2 wk and range from less than 1 of nudibranchs placed in each container ranged from 4 to more than 1000 colonies per kelp blade seasonally (a pair of each species) to 32 (16 of each species). (Yoshioka 1982b). These features suggest that prey resources span the spectrum from overabundance to severe Limitation, thereby providing the requisites RESULTS necessary for selection based on population growth rates (r) and competitive efficiency (K). Life hstory features of Doridella steinbergae and I present laboratory rearing data of the benthic life Corambe paciflca based on the rearing studies are stages of the nudibranchs and interpret the results in given in Table 1. Several differences between the context of r and K selection. Evaluation of r selection is species are apparent. C. pacifica grows larger and based on a formal demographic definition of the max- displays higher size-specific and Lifetime consumption imum intrinsic rate of natural increase, r,, and K selec- rates of zooids. For instance, in the 0.2 to 0.42 cm size tion on several measures of the efficiency of resource class C. pacifica consumes an average of 55 zooids per acquisition and uuzation. I then test whether a trade- day compared to 27 for D. steinbergae. Reproduction off between r and K exists between Dondella steinber- begins about 17 and 26 d after settlement for D. stein- gae and Corambe pacifica. Finally, I compare the bergae and C. pacifica, respectively. No differences merits of r and K selection and bet-hedging in the were noted in the size and appearance of individual ecology of the nudibranchs. eggs (approximately 70 pm in diameter) and newly hatched veligers (shell lengths: 130 pm) indicating no differential investment in energy per larva between METHODS the two species. Bickell & Chia (1979) give sirmlar measurements for D. steinbergae. Although the total Field-collected specimens of DondeJJa steinbergae number of egg masses laid by the 2 species are not and Coramba pacifica were reared in the laboratory at statistically different (10 for C. pacifica versus 10.5 for 13.5"C. Freshly collected algal blades heavily D. pacifica), lifetime reproduction by C. pacifica is encrusted with Mernbranipora membranacea were higher because of the larger number of eggs per egg added in excess as food every 1 to 2 d when the mass, 2550 + 596 (95 % C.I., n = 8) compared to 1135 seawater medium was changed. Because both nudi- + 250 (n = 7)for D. steinbergae. branchs are hermaphroditic cross fertilizers, con- In the laboratory no mortality was observed prior to specific pairs of larger and similar-sized individuals reproduction and all individuals succumbed after were kept in each test container. Also, because nu&- reproductive periods of about 8 d for Dondella stein- branchs less than 0.2 cm could not be identified to the bergae and 17 d for Corambe pacifica. A notable fea- Yoshioka: Llfe history of dorid nudibranchs 181

Table 1 Dondella stevlbergae and Corambe paafica Reproduchon zooid consumphon, and durahon of vanous sue classes n = # palrs of D stelnbergae and C panfica each ' group reanng of 4 Dondella and 5 Corambe, ' ' maxlmum sizes of D stelnbergae and C pacdica 95% C1 based on pairs Probabillhes based on the t-test NS = not significant at 0 05 level

Size class n Duration P # Zooids consumed P # Egg masses laid p (cm) (d) Doridella Corambe Dondella Corambe Dor~della Corambe

Lifetime totals

ture observed during the rearing study was low varia- the benthic life stage. With these criteria, reproductive b&ty in the size (age) of first reproduction; without output would be dependent upon the efficiency at exception D. steinbergae and C. pacifica began repro- whch zooids are acquired and uthzed. In terms of duction upon reaching threshold sizes of 0.42 and 0.73 resource uthzation, Dondella steinbergae is the more cm, respectively. efficient species in egg production in relative to zooid Age-specific reproductive rates of DondeUa stein- consumption whether these ratios are determined over bergae and Corarnbe pacifica can be used to calculate the entire benthic lifespan or limited to the reproduc- the maximum intrinsic rate of natural increase, r,, tive period. For instance, averaged over the entire defined by the Lotka-Euler equation: lifespan, D. steinbergae produces 14.6 eggs per zooid consumed compared to 2.4 for C. pacifica. The ability to acquire Mernbranipora rnernbranacea where 1, = age-specific survivorship which I assumed zooids is potentially affected by behavioral interac- to be 1.0 until reproduction ceases. Age-specific birth tions between individuals as well as the ability to rate, m,, would .be expressed by the number of eggs locate dispersed prey. The former consideration evi- laid per day. For simplicity and lack of evidence to the dently does not play an important role since no inter- contrary, I assumed that reproduction proceeds at a or intraspecific interactions (exclusive of copulation) constant rate for mature individuals with D. steinber- were observed in the laboratory, indicating that com- gae and C. pacjfica producing 1528 and 1430 eggs per petition for limited resources would occur by exploita- day, respectively. Individual age, X, would lnclude tion rather than interference mechanisms. Thus, the hme spent as eggs and vehgers in addition to the post successful acquisition of zooid resources would prob- settlement times measured in the laboratory. Egg ably be related simply to the abhty to locate zooids. In masses of both nudibranchs take 6 to 7 d to hatch this respect the most striking behavioral difference (Yoshioka 1973). D. steinbergae veligers spend a observed between the nudibranchs was the constant minimum of 25 to 26 d in the plankton (Bickell et al. activity of DorideLla steinbergae compared to Corarnbe 1981). I also assumed this value for C. pacifica, based pacifica. This feature is reflected by characteristic on the similar egg and veliger sizes of both species. feeding patterns of the nudibranchs; zooids eaten by D. Thus, C. pacifica and D. steinbergae would be a steinbergae are dispersed haphazardly within M. minimum of 57 and 48 d old, respectively, when repro- rnernbranacea colonies (McBeth 1968), while C. duction begins. pacifica leaves large contiguous patches of empty Despite its lower fecundity, DondeUa steinbergae zooids (MacFarland & O'Donoghue 1929). has a higher r, than Corarnbepacifica, 0.181 compared The preceding comparisons inhcate that Dondella to 0.159 d-l, respectively. steinbergae would reproduce more successfully under A major difficulty of r and K selection is that K conditions of Limited zooid resources. To verify ths cannot be expressed in terms of life history conclusion, I put various desities of both species in phenomena, and as a result r and K attributes cannot containers with similar-sized sections of algal blades be compared directly (Stearns 1977). I attempted to encrusted with Mernbranlpora rnernbranacea. Prey measure K attributes of the nudibranchs by assuming density per ranged from sufficient to that (1) Mernbranipora rnernbranacea zooids represent severely limiting based on the lifetime requirements of the appropriate limiting resource and (2) reproductive both species. In general, reproduction per individual output is the best measure of individual success during for both species decreased with increasing nudibranch 182 Mar. Ecol. Prog. Ser. 31. 179-184, 1986

Table 2. Doridella steinbergae (D. S.) and Corambe pacifica (C. p). Number of egg masses laid per individual during competition experiment; totals and ratios

Number of Days Total Ratio Nudibranchs 0- 1 1-4 4-10 10-18 D. S. : C. p. D. s. : C p. D. S. : C. p D. S. : C p. D S.. C. p. D. S : C. p. D. S.. C, p.

2:2 2.0 :2.0 1.5:1.5 2.5 :3.0 0.0: 1.0 6.0: 7.5 0.80 4:4 1.5 : 0.8 1.8: 1.0 3.0:2.0 2.0 : 0.0 8.3 : 3.8 2.20 8:8 0.9 : 0.3 1.4 : 0.5 1.6:0.8 1.1 :0.1 5.0: 1.6 3.08 16: 16 1.6:0.3 1.9:0.4 0.9: 0.4 0.0 : 0.1 4.4: 1.1 3.94

density indicating the effects of resource limitation higher population growth rate if prey resources are (Table 2). More importantly, D. steinbergae laid a always overabundant and would produce proportion- comparatively greater number of egg masses than ally more offspring if resources were always limiting. Corambe pacifica with increasing nudibranch density Since D. steinbergae is the superior species at both (p = 0.04, l-tailed, exact probability test) conflrming extremes of resource availability, the exclusion of the prediction of greater reproductive success under Corambe pacifica would appear imminent. conditions of resource limitation. An alternative interpretation of the life history pat- terns of the nudibranchs can be formulated from the perspective of coexistence: (1) How can differences in DISCUSSION life history pattern account for their coexistence? (2) What are the selective forces and trade-offs implied The theory of rand K selection may appear appropri- thereby? An essential ingredient of coexistence is the ate for Doridella steinbergae and Corambe pacifica interaction between the complex life cycles of the because both species possess a suite of life history nudibranchs and the dynamics of their prey. Mem- traits and ecological correlates characteristic of r selec- branipora membranacea populations exhibit large tion (Pianka 1974). These include: (1) rapid growth, (2) short-term (biweekly) fluctuations in size with early reproduction. (3) many small offspring, (4) small densities sufficient to support the successful growth body size, (5) short lifespan, (6) occurrence in an uncer- and reproduction of the nudibranchs occurring at tain environment (Yoshioka 1982b), (7) variable and episodic intervals (Yoshioka 1982b). Doridella stein- nonequilibrium population sizes (Yoshioka unpubl.), bergae and Corambe pacifica have adapted to these (8) frequent recolonizations (Yoshioka 1982a). How- conditions by settling only in instances of high prey ever, counter to theoretical expectation, D. steinbergae densities, suggesting that veligers can delay settle- has a higher r, and is more efficient in the acquisition ment and wait in the plankton for proper settling and utilization of prey resources, and consequently a conditions (Yoshioka 1982a, unpubl.). The resulting trade-off does not exist between population growth implication of a planktonic 'seed bank' (Harper 1977) rates (r) and efficiency (K).The higher r, of D. steinber- is supported by field experiments. Large numbers of gae, despite lower fecundity, is attributable to the both nudibranchs can be induced to settle out if heav- ovewhelming role of the age of first reproduction in ily encrusted algal blades are placed in the field, even determining population growth rate (Cole 1954, during periods when both species are absent in kelp Lewontin 1965). Also, because the greater fecundity of beds due to low M. membranacea abundances C. pacifica probably results from its greater size which, (Yoshioka 1982a). In concordance, Bickell et al. (1981) in turn, requires longer development times, r and K have demonstrated that the settlement of D. steinber- selection cannot explain the trade-off between fecun- gae can be delayed for 25 d past the attanment of dity and development time. Furthermore, r and K may metamorphic competence. be even positively correlated in these nudibranchs. Egg The preceding observations indicate that early production relative to zooid consumption (efficiency) reproduction in the benthic life stage of Doridella probably increases with shorter deveIopmenta1 periods steinbergae is offset by a corresponding increase in because proportionately more metabolic energy may be time spent in the plankton awaiting proper settling required for non-reproductive metabolic processes (as conditions. As a result, the effective generation times maintenance) with longer developmental periods. of the nudibranchs would be equivalent and deter- A major consequence of these considerations is that r mined by temporal features of the prey population and K selection cannot account for the coexistence of rather than endogenous developmental rates. The net the nudlbranchs. Doridella steinbergae would have a effect can be simply demonstrated by the relation: Yoshioka: Life histol -y of dorid nudibranchs 183

the trade-off between fecundity and the age of repro- duction. Doridella could easily match the reproductive where R. = net reproductive potential; T = environ- outout of Corambe by reproducing over a longer time mentally determined generation time which would be span. In other words, the ideal strategy appears to be equivalent for both species in a given situation. Given reproduction as early and as long as possible. The equivalent generation times, coexistence would be death of all nudibranchs after a short period of repro- dependent upon an environmental regime in which duction (typifying the classical Type I survivorship the relative advantages of both D, steinbergae (repro- curve) indicates the presence of physiological trade- ductive efficiency) and Corambe pacifica (fecundity) offs between fecundity and development time which can be expressed. This is evidently the case. Variations preclude this possibhty. in the relative abundance of prey range from less than 50 to more than 100 000 zooids per nudibranch on Acknowledgements. G. Breckon, D. Harvell. G. Owen, R. individual kelp blades at a given time (Yoshioka un- Strathmann, and an anonymous reviewer read and improved previous drafts of this manuscript. Partial support during the publ.). Based on the rearing data, these values span the preparation of this manuscript was provided by the Marine spectrum from no, to partial, to complete reproduction Ecology Division of the Center for Energy and Environment by the nudibranchs. Consequently, reproduction (Ro)of Research, Mayaquez, Puerto Rico. either D. steinbergae or C. pacifica would be greater depending upon the relative abundance of prey. It LITERATURE CITED should be noted that, counter to a simplifying assump- tion, C. pacifica would have the shorter larval develop- Bickell, L. R., Chia, F. S. (1979). Organogenesis and his- mental period under these conditions. However, r togenesis in the planktotrophic vehger of DorideUa stein- bergae (Opistobranchia: Nudbranchia). Mar. Biol. 52: selection based on innate developmental processes 291-313 would still represent the inappropriate mechanism. Bickell, L. R., Chia, F. S., Crawford, B. J. (1981). Mor- Schaal & Leverich (1981) give a similar argument for phogenesis of the digestive system during metamorphosis annual plants where the age of reproduction has little of the nudibranch Doridella steinbergae (): Conversion from phytoplanktivore to carnivore. Mar. Biol. effect on r because of exogenous (seasonal) factors. 62: 1-16 Ths scenario of coexistence is readily amenable to a Cole, L. C. (1954).The population consequences of hfe history 'bet-hedging' interpretation of life history pattern. Bet- phenomena. Q. Rev. Biol. 29: 103-137 hedying would occur in the larval life phase when Cohen, D. (1966). Optimizing reproduction in a randomly planktonic dispersal results in sibling veligers settling varying environment. J. theor. Biol. 12: 119-129 Harper, J. L. (1977). Population biology of plants. Academic on different kelp blades, thereby 'averaging out' spa- Press, London tial variations in reproductive success. Variations in Harvell, C. D. (1984). Predator-induced defense in a marine the germination of desert plant seeds within a given bryozoan. Science 224: 2357-1359 seed set (Cohen 1966) represents a similar example of Lance. J. R. (1962). A new Stiliger and a new Corambella pre-reproductive bet-hedging set in a temporal con- (: Opistobranchia) from the N.W. Pacific. Veliger 5: 33-38 text. Bet-hedging provides a satisfactory explanation Law, R. (1979). Ecological determinants in the evolution of for the trade-off between fecundity and developn~ent life histories. In: Anderson, R. M,, Turner, B. D., Taylor, L. time as well as the low variability observed in the age R. (ed.) Population dynamics. Blackwell, London, p. (size) of first reproduction. I have demonstrated else- 81-103 Lewontin, R. C. (1965). Selechon for colonizing abhty. In: where (Yoshioka unpubl.) that the availabihty of food Baker, H. G., Stebbins, G. K. (ed.)The genetics of coloniz- on kelp blades becomes more uncertain with time ing species. Academic Press, New York, p. 79-94 (nudibranch age). Thus, the larger reproductive output MacArthur, R. H., Wilson, E. 0. (1967). The theory of island of Corambe pacifica associated with its longer de- biogeography. Princeton Univ. Press, Princeton MacFarland, F. M,, O'Donoghue, C. H. (1929). A new species velopmental period would be incurred at a cost of in- of Corambe from the Pacific Coast of North America. Proc. creased variability in reproductive success. Similarly, if Cahf. Acad. Sci., ser. 4. 18: 1-27 low variability is indicative of high selective pressure McBeth, J. W. (1968). Feeding behavior of CorambeUa stein- (Lewontin 1965), then it can be inferred that the bergae. Veliger 11: 145-146 benthic life stage is under strong selective pressure to Mertz, D. B. (1970). Life-histories and ecological genetics. In: Connell, J. H., Mertz, D. B., Murdoch. W. W. (ed.) Ecology reproduce as quickly as possible (within the life history and ecological genetics. Harger and Row, New York, p. framework of the nudibranchs) in order to reduce vari- 1-3 ations in reproductive success. (In contrast, the ineffec- Mertz, D. B. (1971). Life history phenomena in increasing and tiveness of early reproduction in determining popula- decreasing populations. In: Patil. G. P.. Pielou. E. C., Waters, W. E. (ed.) Statistical ecology. Vol. 2. Penn. State tion growth rates invalidates r selection as the approp- Univ. Press, University Park, p. 361-399 riate mechanism.) Murdoch, W. W. (1966). Population stability and life history Physiological constraints may ultimately underlie phenomena. 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