Phestilla sibogae, a nudibranch living on corals of the genus
Porites, is rarely found on the reef at Kaneohe Bay, Hawaii, although Porites
compressa is a dominant coral there. This is probably due to massive predation
on juveniles and adults. Such predation pressure would force this species to put
high effort into reproduction. In this work I found that P. sibogae laid eggs
amounting to up to 17% of their body weight each day. Furthermore, based on
a 100% conversion efficiency for ingested coral tissue, 51-78% of the calories
each individual ate daily were channeled into egg production. Photosynthetic
activity of zooxanthellae in the nudibranch's tissue suggests that the algae may
provide some of the energy required by the animal's metabolism

Haramaty, Liti

Pacific Science

ScholarSpace at University of Hawai'i at Manoa

Pacific Science(1991), vol. 45, no. 3: 257-262© 1991 by University of Hawaii Press. All rights reservedReproduction Effort in the Nudibranch Phestilla sihogae:Calorimetric Analysis of Food and Eggs 1LIT! HARAMATy2ABSTRACT: Phestilla sibogae, a nudibranch living on corals of the genusPorites, is rarely found on the reef at Kaneohe Bay, Hawaii, although Poritescompressa is a dominant coral there. This is probably due to massive predationon juveniles and adults. Such predation pressure would force this species to puthigh effort into reproduction. In this work I found that P. sibogae laid eggsamounting to up to 17% of their body weight each day. Furthermore, based ona 100% conversion efficiency for ingested coral tissue, 51-78% of the calorieseach individual ate daily were channeled into egg production. Photosyntheticactivity of zooxanthellae in the nudibranch's tissue suggests that the algae mayprovide some of the energy required by the animal's metabolism.THE NUDIBRANCH Phestilla sibogae Bergh,1905 feeds exclusively on corals of the genusPorites (Harris 1975, Rudman 1981) and isthought to occur throughout the entire Indo-Pacific region (Rudman 1981). At KaneoheBay, Oahu, Hawaii, the nudibranchs arerarely found , although Porites compressa isa dominant coral on the reef (R. A. Kinzie,E. Cox, and C. Hunter, pers. comm.). How-ever , P. sibogae become pests when coloniesof Porites compressa are kept in running sea-water tanks in the absence of predators. Thissuggests that the population of P. sibogae onthe reef is controlled by massive predation.The most obvious protective strategy em-ployed by P. sibogae is camouflage and hid-ing. There are no active defense mechanisms,such as nematocysts, in this species (Rudman1981). These observations support the sugges-tion of Harris (1975) that: "Predation onnudibranchs may be another factor influenc-ing longevity. To grow fast and reproduce asrapidly as possibly before being eaten may befar more important than the availability of thefood source." It is known that the juveniles ofP. sibogae exhibit fast growth (faster than thatof a similar species, Phestilla melanobranchia[Harris 1975]), and that upon reaching matu-rity, growth slows and reproduction (egg-laying) becomes continuous (Harris 1975,Rudman 1981).The animals settle, live, and lay eggs ontheir food source-colonies of Porites. Theyingest and digest both animal tissue and thezooxanthellae present in the coral (Rudman1981). Observations showing zooxanthellae inthe cerata of P. sibogae were reported byKawaguti (1943), Rudman (1982), as well asin the present work. Zooxanthellae mighthave more than one function in the host tissue.They provide protective coloration, could bedigested (Rudman 1981), and if photosynthe-tically active can translocate photosynthesisproducts to the host, as reported for othernudibranch species (Hoegh-Guldberg andHinde 1986, Hoegh-Guldberg et al. 1986,Kempf 1984).In this investigation I first estimated howmuch of the energy derived from eating coraltissue is channeled into reproduction (i.e., eggproduction) on a daily basis (reproductiveeffort) and then examined whether or not thezooxanthellae present in the cerata of the P.sibogae were photosynthetically active.MATERIALS AND METHODSAt the Hawaii Institute of Marine Biology(on Coconut Island, in Kaneohe Bay, Oahu),2571 This paper is contribution no. 849 from the HawaiiInstitute of Marine Biology. Manuscript accepted 15Sep-tember 1990.2 Department of Life Sciences, Bar-I1an University,Ramat-Gan, Israel 52100.258P. sibogae establish populations on coloniesof Porites compressa kept in running seawatertanks. Observations and experiments weredone on animals collected from thesepopulations.Experiments were run in running seawaterchambers, 1.5 liters in volume . Two chamberswere used, each containing two individuals ofP. sibogae and a piece of living Porites com-pressa. The animals used were of differentsizes, ranging on average from 1847 mg to3546 mg in total mass for pairs in each experi-ment. Once every 24 hr the animals were takenfrom the chamber, placed on a filter for 30 secto let the water drain, weighed, and putback in the chamber.The eggs laid during thepreceding 24-hr period were collected, andthe surface area of the coral eaten was mea-sured by marking the area on a transparentplastic film, cutting it out , and weighing it.The area was then calculated from a calibra-tion of plastic film pieces of known area andweight.For determination of the caloric content ofthe coral, tissue was removed from freshlycollected colonies using a Water Pik washingdevice (Johannes & Wiebe 1970). Distilledwater was used with the Water Pik to obtaina sample as free ofsalt as possible. The volumeof homogenate collected from a known sur-face area of coral was recorded. The homog-enate was frozen , freeze-dried, and weighed.Weight ofdry tissue per square centimeter wascalculated. Dried tissue was used to determineash content (500°C for 3 hr [Paine 1971]).Pellets of dry homogenate weighing 6.57-8.11 mg were used for calorimetric analysis.The eggs, collected each day, were rinsedwith distilled water, placed on a piece of filterpaper for 10 min to let the water drain, andweighed for wet mass. Additional eggs, col-lected from the reservoir of animals, were usedto establish the caloric content of the eggs.The eggs were rinsed , dried , and weighed forwet mass as described . Freeze-dried eggs wereused for dry mass and ash content (after com-bustion for 3 hr at 500°C) measurements.Pellets weighing 4.38-18.11 mg were used incalorimetry.Caloric values for eggs and coral tissue weredetermined using a Phillipson microbombPACIFIC SCIENCE, Volume 45, July 1991calorimeter (Phillipson 1964). Samples ofcoral tissue were high in ash content, as re-ported in previous investigations (Glynn andKrupp 1986, Richmond 1987). Eggs wereunexpectedly high in ash content. Similar re-sults have been reported by Todd (1979) forspawn samples ofnudibranchs. Because of thehigh ash contents, an endothermy correctionfactor of 0.14 cal/rng ash was applied (Paine1966; see also Todd 1979). Respiration of theanimals first in the dark and then in the light(45 /lE m- 2 S-I) was measured with an oxygenprobe (Strathkelvin Instruments) in a 225-mlchamber containing filtered (through 0.5-/lmfilter) water and using one animal at a time.RESULTSThe results of four experiments are sum-marized in Table 1. The average mass of eggslaid daily ranged from 157.5 mg to 571.3 mgand was correlated to animal mass (r = 0.78).The ratio between body mass and eggs massranged from 0.17 in experiment 3 to 0.08 inexperiment 4. This ratio was the same in ex-periments 1,2, and 3 (P = .05, SNK test) , butit was significantly lower (P = .05) in experi-ment 4. The area of coral eaten daily by thenudibranch pairs ranged from 2.7 cm' (ex-periment I, day 4) to 12.7 cm2 (experiment 3,day 1). There was no correlation betweenanimal weight and area of coral eaten (r =0.18). Calculations of the caloric contents ofeggs were based on the calorimetric analysi sof eggs collected from the reservoir of animalsand resulted in a factor of 6.22 ± 1.2 cal /mgdry mass. The caloric area specific contentof Porites compressa was determined to be69.5 ± 7.53 cal/em", The ratio between cal-ories eaten and calories in the eggs rangedfrom 0.78 in experiment 2 to 0.25 in experi-ment 4. Calculation of this ratio assumed thatall coral tissue and zooxanthellae ingestedwere utilized (i.e., assimilation of 100%) . Theratios were not significantly different for ex-periments I to 3, but were significantly lowerin experiment 4 (P = .05, SNK test) .The results for oxygen consumption areshown in Table 2. Oxygen consumptionReproduction Effort in the Nudibranch Phestilla sibogae-HARAMATY 259TABLE 1SUMMARY OF DAILY MEASUREMENTS AND AVERAGES FOR FOUR EXPERIMENTSANIMAL EGGS CORAL EGGS WEIGHT EGGS CALORIESEXP. MASS MASS EATENNO. DAY (mg) (mg) (ern") ANIMAL WEIGHT CORAL CALORIES1 2,508 380 7.3 0.15 0.432 2,471 359 3.6 0.15 0.823 2,209 327 6.1 0.15 0.444 2,323 290 2.7 0.13 0.89Average 2,377.7 339 4.9 0.14 0.65SO 138.0 39.3 2.1 0.01 0.242 1 3,634 577 4.7 0.16 1.022 3,286 514 8.1 0.16 0.533 3,720 673 6.7 0.17 0.78Average 3,546 .7 571 6.5 0.16 0.78SO 229.8 54.7 1.7 0.01 0.243 1 2,196 367 12.7 0.17 0.242 1,990 297 4.1 0.15 0.613 2,130 419 6.1 0.20 0.574 2,174 477 6.0 0.22 0.665 3,090 414 7.2 0.13 0.48Average 2,316 395 7.2 0.17 0.51SO 440 67.2 3.3 0.04 0.164 1 1,828 117 4.1 0.06 0.232 1,867 198 6.3 0.11 0.26Average 1,847 157 5.2 0.08 0.25SO 28 57.3 1.5 0.03 0.02N OTE: Animal mass determined at the beginning of a 24-hr period; eggs mass determined at the end of a 24-hr period. Results arefor pairs of animals in each experiment.TABLE 2RE SULTS OF OXYGEN CONSUMPTION MEAS UREMENTSLight = 45 JlE m ? s -\was significantly lower when measured at45 J1.E m? S-1 than in the dark (P = .02,Mann-Whitney U test) .EXP. NO.2345DARK- 0.073r 2 = 0.79- 0.073r 2 = 0.80-0.021r2 = 0.84- 0.055r 2 = 0.94- 0.025r 2 = 0.68LIGHT- 0.0 19r2 = 0.58-0.037r2 = 0.96- 0.0 15r2 = 0.99-0.017r2 = 0.78-0.013r2 = 0.64DISCUSSIONThe proportion of resources (energy) thatis diverted to reproduction should be in bal-ance with other energy-demanding life activ-ities (metabolism, respiration, growth). Theproportion channeled into reproduction de-pends on the life history of the species and onenvironmental factors (Williams 1966). Ac-cording to Miller (1962), nudibranchs can beseparated into two groups. In the first arespecies that eat seasonal food and grow andreproduce quickly while their food sourcelasts. In the second group are species that eatfood that is abundant throughout the yearand that grow slowly and reproduce season-ally. Phestilla sibogae has characteristics of260both groups. Its food is available in all sea-sons; however, it grows quickly and repro-duces constantly (Harris 1975, Rudman1981). This could result from both evolu-tionary background and environmentalfactors.An important environmental factor in-fluencing life history is predation (Crowl andCovich 1990). Phestilla sibogae is rarely seenon Porites in the field, yet is abundant on thiscoral when kept in predator-free laboratoryseawater tanks. This observation suggestsmassive predation on juveniles and adults inthe field. The reproductive traits mentionedabove for P. sibogae may well be determinedby predation pressure on the adults and thelack of an active defense .Such predation pressure would also in-fluence the quantity of available energy thatis channeled into reproduction. An increase inresources devoted to reproduction would re-sult in decreased growth and survivorship andwould reduce the future potential to repro-duce (Williams 1966). When P. sibogaereaches maturity (as evidenced by the onset ofegg-laying), growth rate slows (Harris 1975,Rudman 1981), and an animal lays an averageof 1.5 egg masses a day for about 100 days(death occurs soon after the egg-laying ceases)(Harris 1975). As shown in the results re-ported here (experiments 1-3), each indi-vidual lays 14-17% of its body weight in eggsdaily . Based on 100% conversion efficiencyfor ingested food, derived from eating coral,51-78% of the energy is channeled into repro-duction on a daily basis . Because this valueis based on 100% conversion efficiency, theactual percentage of ingested energy investedin reproduction must be lower. In experiment4 the numbers are significantly lower (0.08 ofbody weight and 0.25 of the energy), probablybecause these animals were smaller and stillgrowing faster than larger animals, henceputting more energy into somatic growth.In the present work, reproductive effort isdefined as the percentage of body weight andof food intake put into production of eggsdaily. In other studies the definition is differ-ent and therefore cannot be directly com-pared. Reproductive effort in nudibranchswas calculated by Todd (1979) as the ratioPACIFIC SCIENCE, Volume 45, July 1991between dry weight and caloric content in eggs(produced cumulatively during a long-termexperiment) and the dry body weight and ca-loric content of the active female . Reproduc-tive effort in terms of dry weight was 57.28-99.96% for Onchidoris muricata and 27.2-60.71% for Ada/aria proxima, and in calories,81.85-142.82% and 24.57-54.84% for the re-spective species. DeFreese and Clark (1983)also calculated the ratio between dry weightand caloric content of females' whole bodyand eggs for 11 species of nudibranchs. Theirratio was calculated for one event of egg-laying. The reproductive effort expressed indry weight was 3-36.1 %, while in caloricterms it was 9.1-36.6%. The reproductive ef-fort as defined in this work was found to be14-17% in body mass and 51-78% in calorieschanneled into reproduction daily.Based on these high values , I conclude thatthe environmental conditions on the reef(being under massive predation pressure)force P. sibogae to "reproduce as rapidly aspossible before being eaten" (Harris 1975).While eating coral tissue, the animals ingestzooxanthellae. The algae can be digested(Rudman 1981). Personal observations dur-ing the present work showed that there areapparently living cells of zooxanthellae in thecerata. This has been reported by Kawaguti(1943), Rudman (1982), and Harris (1975).Oxygen consumption measurements show thatconsumption rate is lower in the light than inthe dark, which suggests that the zooxanthellaein the animals are photosynthetically activeand could contribute photosynthesis productsto the nudibranch. Symbiosis between inverte-brates and zooxanthellae where zooxanthellaecontribute to energy intake of the animals bytranslocation of photosynthesis products isknown in different groups. Symbiosis betweenzooxanthellae and nudibranchs has been de-scribed by Kempf (1984), Hoegh-Guldbergand Hinde (1986), Hoegh-Guldberg et al.(1986), Rudman (1982), and others. If P.sibogae get energy by translocation fromzooxanthellae, it means that the ratio betweenenergy intake and energy that goes to repro-duction is not as high as indicated by theresults of the present work, based only onenergy intake from feeding on corals. ThisReproduction Effort in the Nudibranch Phestillasibogae-HARAMATY 261"hidden" way of getting energy could alsoexplain the high variability in the percentageof energy that goes to the eggs (51-78%)(from coral eating alone) and the low correla-tion between body size and area ofcoral eaten.The amount of energy, if any, the animalsget from translocation of photosyntheticproducts is not correlated to the size of theanimal but rather to the characteristics of thealgae population (number, chlorophyll percell) and the amount oflight to which they areexposed. Different concentrations of zoo-xanthellae in different individuals of a nudi-branch species (Pteraeolidia ianthina) havebeen reported by Hoegh-Guldberg and Hinde(1986). In that work it was reported that 25-60% of photosynthetically fixed carbon istranslocated to the animal. It has been shownthat the algae have the same characteristics aszooxanthellae in shade-adapted corals (Fal-kowski and Dubinsky 1981, Porter et al. 1984)that are photosynthetically active in low lightirradiance (Ie in 30-50 JlE m- 2 S-I). If zoo-xanthellae in P. sibogae are shade adapted,they can photosynthesize even when theanimal is hidden under a coral, as dozooxanthellae that live in coral tissue on thebottom side of some corals (unpublished data).The results of this work give some cluesabout the life history of P. sibogae and raisequestions about potential predators, the pres-ence of the nudibranch on the reef, and theimportance of zooxanthellae in the energybudget of P. sibogae.ACKNOWLEDGMENTSI thank R. A. Kinzie III for advice andcomments, Kevin Wyman for helping with thestatistical analysis and critically reading themanuscript, and the staff and summer stu-dents ofHIMB for helping whenever help wasneeded .LITERATURE CITEDCROWL, T. A., and A. P. COVICH. 1990.Predator-induced life-history shifts in afreshwater snail. Science 247: 949-951.DEFREESE, D. E., and K. B. CLARK. 1983.Analysis of reproduction energetics ofFlorida Opisthobranchia (Mollusca: Gas-tropoda) . Int. J. Invertebr. Reprod. 6: 1-10.FALKOWSKI, P. G., and Z. DUBINSKY. 1981.Light-shade adaptation of Stylophorapistil/ata, a hermatypic coral from the Gulfof Eilat. Nature (London) 289 : 172-174.GLYNN, P. W., and D. A. KRUPP. 1986. Feed-ing biology of a Hawaiian sea star cor-allivore Culcita novaeguineae Muller &Trogchel. J . Exp. Mar. BioI. Ecol. 96: 75-96.HARRIS, L. G. 1975. Studies on the life historyof two coral-eating nudibranchs of thegenus Phestil/a. BioI. Bull. (Woods Hole,Mass.) 149: 539-550.HOEGH-GULDBERG, 0 ., and R . HINDE. 1986.Studies on a nudibranch that containszooxanthellae. 1. Photosynthesis, respira-tion and the translocation of newly fixedcarbon by zooxanthellae in Pteraeolidiaianthina. Proc. R. Soc. London Ser. B228: 493-509.HOEGH-GULDBERG, 0., R. HINDE, and L.MUSCATINE. 1986. Studies on a nudibranchthat contains zooxanthellae. II . Contribu-tion of zooxanthellae to animal respiration(CZAR) in Pteraeolidia ianthina with highand low densities ofzooxanthellae. Proc. R.Soc. London Ser. B 228: 511- 521.JOHANNES, R. E., and W . J. WIEBE. 1970.Method for determination of coral tissuebiomass and composition. Limnol.Oceanogr. 15: 822-824.KAWAGUTI, S. 1943. Notes on Phestil/a sibo-gae with symbiotic zooxanthellae. TaiwanNat. Hist. Mag. 33:241 (in Japanese).KEMPF, S. C. 1984. Symbiosis between thezooxanthellae Symbiodinum microadriati-cum equals Gymnodinum microadricaticumand four species ofnudibranchs. BioI. Bull.(Woods Hole, Mass.) 166(1) : 110-126.MILLER, M. C. 1962. Annual cycles of someManx nudibranchs, with a discussion ofthe problem of migration. J . Anim. Ecol.31 :545-569.PAINE, R. T. 1966. Endothermy in bombcalorymetry. Limnol. Oceanogr. II: 126-129.- --. 1971. The measurement and applica-262tion of the calorie to ecological problems.Annu. Rev. EcoI. Syst. 2 : 145-164.PHILLIPSON, J. 1964. A miniature bomb calo-rimeter for small biological samples. Oikos15(1): 130-139.PORTER, J . W., L. MUSCATINE, Z. DUBINSKY,and P. G. FALKOWSKI. 1984. Primary pro-duction and photoadaptation in light andshade-adapted colonies of the symbioticcoral Stylophora pistil/ata. Proc. R. Soc.London Ser. B 222 : 161 -180.RICHMOND, R. 1987. Energetic relationshipand biogeographical differences amongfecundity, growth and reproduction in thereef coral Pocil/opora damicornis. Bull.Mar. Sci. 411(2): 594-604.PACIFIC SCIENCE, Volume 45, July 1991RUDMAN, W. B. 1981. Further studies onthe anatomy and ecology of opistobranchmolluscs feeding on the scleractinian coralPorites. ZooI. J. Linn. Soc. 71 :373-412.- - -. 1982. The taxonomy and biology offurther aeolidacean and arminacean nudi-branch molluscs with symbiotic zoo-xanthellae. ZooI. J. Linn. Soc. 74 : 147-196.TODD, C. D. 1979. Reproductive energetics oftwo species of dorid nudibranchs withplanktotrophic and lecithotrophic larvalstrategies. Mar. BioI. 53 : 57-68.WILLIAMS, G . C. 1966. Natural selection, thecosts of reproduction, and a refinement ofLack's principle. Am . Nat. 100: 687-690.

Reproduction Effort in the Nudibranch Phestilla sibogae: Calorimetric Analysis of Food and Eggs

http://scholarspace.manoa.hawaii.edu/bitstream/10125/1389/1/v45n3-257-262.pdf

Reproduction Effort in the Nudibranch Phestilla sibogae: Calorimetric Analysis of Food and Eggs

Abstract

Similar works

Full text

Available Versions

ScholarSpace at University of Hawai'i at Manoa