Fisheries Science 65(1) , 48-56 (1999)

Use of Annual Density Banding to Estimate Longevity

Eijiroh Nishi*1 and Moritaka Nishihira*2 *1Natural History Museum and Instit ute, Chiba, Aoba 955-2, Chuo, Chiba 260-8682, Japan *2Biological Institute , Graduate School of Science, Tohoku University, Sendai 980-8578, Japan (Received June 17, 1998) Growth bands of the colonies of the scleractinian coral Porites collected at Okinawan coral reefs were counted on Soft-X Ray micrographs, and age and growth rates of infaunal non-boring organisms were estimated indirectly from the annual coral-growth rings of the host coral. The organisms include a calcareous-tube polychaete Spirobranchus corniculatus (Grube), a sand-tube sabellariid polychaete, Idanthyrsus sp., a vermetid gastropod Dendropoma maxima Sowerby, a pecten bivalve Pedum spon- dyloideum Gmelin, and a coral barnacle Cantellius sp. The three tubicolous former species showed growth in various directions, and 15 to 20 years (S. corniculatus), 8 years (Idanthyrsus sp.), and 15 years (D. maxima) longevity were reliable estimates in this study. In contrast, the pecten bivalve and the coral barnacle showed lesser longevities, usually less than 7 years, and they grew vertically in almost the same direction as the host coral; thus, their growth rates can be estimated roughly by shell or slit-like hole length in relation to average host coral growth. We present here a new and practical method to esti mate age and longevity of non-boring coral infauna, and we discuss marine organism growth and lon gevity with emphasis on polychaetes.

Key words: coral growth ring, infauna, age estimation , polychaete, Okinawa

A major problem arising during the demographic analy coral skeleton overlying calcareous tubes. Soft X-radio- sis of marine organisms is the choice of parameters to be graphs of slabs cut along the growth axis of many massive measured and analyzed. These parameters must represent corals display alternating dark and light bands which out- a minimum variability for a given age. The best known line the former positions of the outer surface of the colony parameter for a demographic study is a set of size fre (Fig. 1). These dark and light bands represent variations in quency histograms. The growth parameters most often the density at which the skeleton was deposited . A pair of used are dry or fresh weight and body length or width. In bands-high density and low density (e.g., light plus dark tube building organisms, tube weight and size are the best bands)-represent one year's growth.7,14) parameter. The calcareous hard shells of molluscs and In the application of this method to coral infauna , there corals are known to show growth lines in the hard materi are 4 basic assumptions as follows: 1) organisms do not als depending on warm and cold seasons, tidal frequen bore into the coral skeleton , 2) they do not extend their cies, one-day activities, etc. (see Rhods and Lutz1)). These tubes or shells beyond the surface of the coral skeleton , 3) parameters must be manipulated with extreme care and a single individual occupies one tube, shell or hole , and it d with expert techniques. Examination of populations in the oes not move to other tubes , shells or holes, and 4) they field is a best way to study its growth, age and whole life are alive at the time of examination or only recently died. span, but in long-live organisms, this is hard to do. The in- For the last assumption, for example , tubes of Spirobran formation remaining on the hard structure of marine or chus and vermetids were used by crustaceans or small fish ganisms, particularly on soft-bodied worms such as poly after the worms' death.",") The life span of those tubes oc chaetes2-5) allows their life history data to be analyzed in a cupied by hole users could be estimated with age of an laboratory in some cases. original worm plus years (times) utilized by hole-users . Coral growth bands have been known to show annual Although the user of the empty tube or hole does not se. growth and the growth bands can be counted using Soft X- crete calcareous materials any more , the estimation of Rays,6-8) fluorescent-microscope,) and by laser densimet times used by the secondary space user is practically not al, ry.10) The information derived from coral growth bands ap- ways difficult. To know the age of the tube itself , not thf plies to many areas of oceanography, paleontology, worm, the tubes lacking original individual that had secret- etc. 8,11) ed the tube could be useful. Nishi and Nishihira12) demonstrated the method to esti mate the age of a tropical tubicolous polychaete Spirobran Materials and Methods chus corniculatus (described as S. giganteus, its taxonomy, see Nishi13) by counting the annual growth bands in the Over 40 massive coral colonies of Porites lutea with tube

Corresponding address. Eijiroh Nishi, Natural History Museum and Institute, Chiba Aoba 955-2, Chuo , Chiba 260-8682, Japan. Tel: +81-43-222 8689 Fax: +81-43-266-2481 E-mail: [email protected] Age Estimation of Coral Infauna 49

Fig. 1. Sketch of images of coral growth bands and infaunas. Hp, Notaulax sp. (boring sabellid); Sc, Spirobranchus corniculatus; Is, Idanthyrsus sp.: Dm, Dendropoma maxima; Ps, Pedum spondiloidi um; Cs, Cantellius sp.

worms, pecten shells, or coral-barnacles were collected at pears on the surface of the living tissues of coral (Smith"); Sesoko Island and Zampa Cape, Okinawa Island during Figs. 1 and 2A, B). 1994 to 1995. Only non-boring infauna species were stud Idanthyrsus sp. (Sabellariidae) dwells in packed sand- ied. After collection, corals were dried after rinsing with tubes and appear on dead coral colonies and on living mas synthetic detergent; thereafter, they were sliced into 2 to 5 sive colonies23) (Nishi and Kirtley, unpublished data: Figs. mm thick slices (maximum 10 mm thickness) at the por 1 and 2C, D). We studied only those individuals on living tion including the tubes or shells. The sliced plates were massive Porites colonies in the present study. then radiographed under Soft X-Rays (Softex, Hitachi 2) A vermetid gastropod Dendropoma maxima MB3). The exposure was 40 kVp, 3 mA, for 4 to 5 minutes Sowerby is a well known vermetid in coral reef area and (in a slice 3-4 mm thick). The source to subject distance frequently is found in dead and living corals in various was 50 cm. The areas of interest of the soft X-radiographs regions24,25)(Figs. 1 and 2E, F). Vermetids feed by a combi (generalized) is shown in Figs. I and 3 (partly drawn from nation of mucous nets and ctenidial cilia which collect photos of Nishi and Nishihira12)). detritus and other planktonic particles from the water.',) Usually we prepared one or two slices per worm, with a Dendropoma maxima is a solitary species and commonly maximum of 10 per worm, and the slice included the appears on massive coral species.") They are distributed whole or only a part of the tube (Figs. 1 and 3). If the slice on dead and living corals, but only those on living Porites included the whole tube or hole cut longitudinally as were studied. shown in Fig. 3A, the exact growth dates could be deter- 3) A scallop bivalve Bivalves living in scleractinian mined from the settlement to recent years. For pecten corals are also available as materials for age-estimation. bibalves and barnacles, we can cut the slice including its en- Pedum spondyloideum Gmelin attaches to living massive tire hole. If the slice included two openings of the same corals at a very early growth stage and subsequently tube as shown in Fig. 3B, the growth rate between the two becomes completely enclosed within the coral except for openings could be determined accurately. Some slices of its ventral region, which maintains an elliptical opening" tube of tubicolous species, however, contained only one (Figs. I and 2G, H). The growth rates of the coral and the opening clearly cut horizontally, so we could only com- scallop are precisely balanced, and the form of the scallop pare the size of recent tube openings on the coral surface is highly modified by its semi-enclosed existence to prevent with the opening that appeared in the slice. overgrowth by the coral, its upward growth results in an ex tremely elongate shell .21) Life Habits of Coral-Infauna Studied 4) A coral barnacle Some species of coral-associated 1) Tube worms (Polychaetous Annelida) Spirobran barnacle are buried in living colonies with a part of the chus corniculatus (Grube) is well known to be a coral in- shell apparent on the colony surface (Fig. 1 and Figs. 2K, habitant; it presently is in a taxonomically complicated L). Their growth is limited in vertical extent and their state. 13.17)Its life history and ecology have been studied by orifices usually appear on the surface. In Okinawan coral many researchers."-") The larvae settle on the exposed reefs, many species are known to live as coral coral skeleton near the living part of the coral and extend associates .28-30)Among the barnacles, Cantellius sp., which their tubes toward living tissue, then the tube is covered by was investigated in this study, is common in Porites colo the living coral tissues and the tube entrance (aperture) ap- nies (Nishi pers. obs.). The species has different forms in re- 50 Nishi and Nishihira

Fig. 2, Photos of coral infauna. A-B, Spirobranchus corniculatus apertures (A) and tube (B); C-D, Idanthyrsus sp. aperture (C) and section of tube (D); E-F, Dendropoma maxi ma aperture (E) and internal plug (F); G-H, Pedum spondiloidium; J, K, L, Cantellius sp., aperture (J) and section of empty shell (K, L). lation to size; in large-sized forms the shell is depressed completely embedded (Fig. 2L). In Cantellius sp . embed and the base is deep and cylindrical; in small-sized forms ded in massive Porites colonies, the upper surface of the the shell is conical and the base is shallow and cup shaped shell is always exposed, being at the same level as the sur- (Fig. 1, right, and Fig. 2K and L) relative to the general face of the coral (Figs. 1, right and 2J) . Therefore, the age shape of commensal cirripeds stated by Hiro.31,32)As stated of each individual can be estimated by the annual growth by Hiro,321in the initial stage of development, the associ rate of the host coral. ated cirriped has a somewhat conical shell and increases more in breadth than in length, probably to attain its full Results size before being surrounded by the host (Fig. 2K); however, in later stages, the lengthwise growth of the basal Coral Growth part becomes more pronounced, lest the cirriped should be Growth of coral colonies of Porites lutea varied greatly Age Estimation of Coral Infauna 51

Fig. 4. Relationship between tube orifice diameter and years (N=20) in

Fig. 3. Generalized drawing from Soft-X Ray micrographs of coral

A, age since settlement and B, two openings fro the same tube formed several yers apart. st, settlement point; t, tube, s, surface. Scale shows i cm.

from 4 to 15 mm yr` (average 9.5 mm, S.D. 2.65, N=50) Fig. 5. Relationship between tube orifice diameter and years (N=8) in among colonies and even within a colony. This variation is mainly by environmental condition around coral colonies which vried in individual colony and in years, and might partly be due to the cutting direction of the colony, be- grew to a stage with a 6 to 9 mm tube opening diameter wi cause the colony might have had grown in various direc thin 12 or 13 years (Fig. 4). The largest worm had a 10 mm tions. Among 40 colonies examined, an ordinary annual orifice diameter in this study, and the worm was estimated growth was 6 to 12 mm (Fig. 3). to had lived more than 15 or 20 years. In field, a maximum of 14 to 15 mm orifice diameter was observed,") thus the Polychaeta Spirobranchus corniculatus longevity of the tropical tube worm is possibly about 30 Examples of growth estimation of Spirobranchus are years in Okinawa. shown in Fig. 4 which shows that the diameter of the open- ing and the number of growth bands between the recent Polychaeta Idanthyrsus sp. tube opening and the opening in the slice. The growth rate Sabellariid polychaete with sand tube (Fig. 2C, D) has was 0.1 to 0.8 mm yr"' in tube-orifice inner diameter an annual growth rate similar as or slightly faster than (average 0.45 mm, S.D. 0.21, N= 100 for 20 worms). Very Spirobranchus, usually being 0 to 1.2 mm yr-1, with an little growth was detected in some worms, while others average of 0.61 mm (S.D. 0.36) in tube-orifice inner di grew fast and attained 5 mm tube-orifice diameter within 6 ameter (N=5: Fig. 5). The largest worm had a tube with years (Fig. 4). Tube orifice diameter is known to be cor- 1.2 mm orifice diameter and over 20 cm length, suggesting related roughly with tube length, which ranged 3 to 20 cm an age of over 8 years. and usually grew to various directions.") Most tube aper tures were directed upper-laterally (Fig. 2A), rarely verti A Vermetid Gastropod cally and completely upward in direction. Some worms Among coral infauna studied, Dendropoma maxima grew with 3 to 5 mm tube opening diamter within 10 years was largest, and it grew faster than the other species (0.2 to from the settlement, and some larger worms which origi 2.5 mm in tube orifice inner diameter yr`', average 0.85 nally had 2 to 4 mm tube opening diameter at 1981 to 1982 mm, S.D. 0.45) and attained an orifice diameter of > 10 52 Nishi and Nishihira mm within 10 years and estimated logevity being 10 to 15 The growth rate was high in the first and second years; it years (Fig. 6). Tubes frequently run on the coral colony has a somewhat conical shell and increased more in surface with the anterior part not buried in living tissues breadth than in length (Fig. 2K), about 1 to 2.5 mm in (Fig. 2E) and the growth rate was inconsistant; this sug orifice diameter was attained in two years, and the growth gests a more rapid linear growth of individual tubes than rate decreased suddenly so that the lengthwise growth of of host coral growth in some cases. the basal part became more pronounced and showed only Some vermetid worms have made internal plugs in tubes 0.25 to 1.0 mm yr-1 (Fig. 8). The observed maximum shell (Fig. 2F) and therefore the tube was frequently partly diameter was 7 mm, and that particular barnacle was possi damaged. In such cases, we could not trace entire tubes. bly older than 5 to 7 years. In 10 coral colonies, 10 barnacle shells completely bu A Scallop Pedum spondyloidium ried into coral skeleton were found, the sizes of which Growth rate of the scallop, Pedum spondyloidium va ranged from 30 to 60 mm in shell height, with a maximum ried from 2 to 8 mm in shell length yr-1 (average 5.5 mm, shell diameter being 4 to 7 mm. Those individuals might S.D. 2.3) and 2 to 10 mm yr-1 in shell width (average 5.8 have died in the 3rd to 7th year after settlement. mm, S.D. 3.1, N=5; Fig. 7). In early stages, it grew rather quickly (3 to 8 mm in maximum shell width yr-1), and the Relationship between Tube or Hole Length and Estimated growth rate decreased to 3 to 6 mm in its later stages (over Age 20 mm width). Maximum shell width was 30 mm, possibly For five species studied here, hole depth or tube lengths indicating over 6 years longevity. were measured and compared to host coral growth. In tube-dwelling polychaetes and the vermetid, tube length va- A Coral Barnacle Cantellius sp. The visible part of the cirriped on the coral surface was very small, although the maximum shell opening diameter >5 mm., and the growth rate yr-1 was 0.25 to 2.5 mm (average 0.96 mm, S.D. 0.53, N=7; Figs. 2K, L, and 8).

Fig. 8. Relationship between shell opening width and years (N= 15) in

Fig. 6. Relationship between tube orifice diameter and years (N=10) in

Fig. 9. Relationship between tube or hole length and estimated a ges in

For correlations of each species as follows; Spirobranchus , Y =2.87x-6.52, R2=0 .723, N= 10; Dendropoma =2 , Y .64x-8.15, R2=0.519, N=5; Cantellius , Y=0.854+0.206, R Fig. 7. Relationship between shell width and years (N=8) in Pedum 2 =0.991, N=12; Pedum , Y= 1.092x-0.321, R2=0.962, N=5; Idan. thyrsus, Y=2.692x-9.25, R2=0 .971, N=5. Age Estimation of Coral Infauna 53 ried in individual tubes and by species, their growth was 10.5 years",* although Gruet37) estimated the age as 3-5 clearly inconsistent (Fig. 9). In contrast, hole depths of pec years in the same species. The values of life span of Poly ten and coral barnacle were clearly correlated with esti chaeta ranged from 2 to 3 months in small worms such as mated ages (Fig. 9) and thus with host coral growth rate. It Spirorbis and 8 to 12 years in larger worms such as terebel seems that hole depths for the pecten and the coral barna lids, large serpulids, and others (Table 1). The body size of cle show a value similar to that of the host coral growth, Spirobranchus and Idanthyrsus are smaller than that of although the holes of Pedum were frequently depressed other species with nearly the same age (Table 1). For exam (Fig. 2G, H) and exact growth rate may be difficult to esti ple, Terebellidae showed a longevity of 5 to 7 years at over mate only from growth of host coral. 10 cm body length,) commensal scale worm also had a lon gevity of 4 to less than 10 years at over 10 cm body Discussion length.") Nephtyidae and Lumbrineridae polychaetes are well known to show an exact correlation between growth ring We estimated the average age of calcareous and sand- on chitinous jaws and ages .3,39-41)Nephtys with 5 to 8 years tube dwelling polychaetes of 5 to 8 mm tube orifice di life cycle has a body with 5 to 10 cm length, as in ameter to be 5 to 10 years old (Figs. 4 and 5). These worms Spirobranchus and Idanthyrsus. in this study. Up to now, had a body length 5 to 10 cm (for size distribution of S. cor the longest life span among marine annelids is known for niculatus, see Nishi & Kikuchi")). In the present study, a Spirobranchus polycerus on West Indies coral reefs (prob- maximum of 20 years in Spirobranchus, and 8 years in ably 12 years estimated by host coral growth bands, Idanthyrsus can be taken as the best estimate of life span; Marsden4)) except for our previous work and Smith's the estimated maximum longevity of Spirobranchus is one work on S. giganteus (over 20 years) or S. corniculatus of the longest among marine annelids reported in the litera (over 20 years)."') ture (Table 1). The longevity of Sabellariidae is 3-10 In coral barnacles, Hiro32) suggested that the age of years,") with the maximum known in Sabellaria alveolata as coral barnacles can be roughly estimated by the annual

Table 1. Age of polychaetes studied by growth line on rigid structures, population dynamics and rearing experiments 54 Nishi and Nishihira growth rate of the coral (p. 410). He cited the growth data tubes might remain small and short for some years. of Ma 41)and estimated barnacle ages of at least 5 years in Although calcareous tube worms extend their tubes in vari individuals associated with Favia speciosa in Tanabe Bay, ous directions and in various amounts according to the en Pacific side of central Honshu, Japan. This value is similar vironmental conditions, they can regulate the growth rate to that of our study although this value might vary accord- of their tubes by changing the tube wall thickness,") and ing to host coral growth rate, as suggested by Hiro.32) thus the tube construction work might require a high meta In pecten shells, a less long life is attained on the coral bolic cost. colony in comparison with other Pecten shells.44) In this By counting annual growth bands, we can age and esti study, we analyzed small to middle sized Pedum shells be- mate the growth rate of coral infauna. However, we prob- cause of the difficulty of collection, and maximum sizes of ably cannot estimate a reliable longevity only by this about 8 cm height and 5 cm width (Nishi, pers. obs. in method. That is because empty holes or tubes on coral 1995). Their maximum longevity might be about 10 years colonies are usually used by hole dwellers, including crusta at Okinawa. ceans and fishes. Nishi52) noted the occurrence of empty How can the coral associated polychaetes live so long? tubes of Spirobranchus fully buried in coral skeletons, the Marsden42) noted that the longer life span of S. giganteus tube mouth being not apparent on the coral surface. Even than S. polycerus is probably due to the host coral stabil for such a tube embedded in the coral skeleton, there is no ity; S. giganteus live on longer lived massive coral colo reason to consider that the worm died and that the coral nies, whereas S. polycerus lives on ephemeral plate-like had overgrown the tube. To know the correct longevity of coral colonies. The sedentary polychaetes on living coral coral infauna, the desirable method may be rapid collec colonies possibly cannot live longer than the host coral tion of the coral colony and preparation of cut slabs or colonies. Massive Porites colonies sometimes reach over 5 fixation for further manipulation of age-estimation of m in diameter in Okinawan coral reef (Nishihira, pers. corals and worms. obs.) and Potts et al.") eeestimatedover 500 yearsssage in In contrast to the tube-dwelling species, organisms dwell- large Porites colonies. Spirobranchus and Idanthyrsus ing in the slit-like hole or simple tubes like coral barnacles probably attain a long life by colonizing the long-lived, sta have more easily estimated ages and growth, because their ble coral colony. growth direction is nearly the same as that of the host Why do the coral-associated tube worms have a rela coral, and growth amounts of the associates also nearly tively small body even though they have long life cycles? same as that of the host coral (see results). This shows that One reasonable explanation is great cost for the construc they are obligate coral-dwellers on living tissues. Obligate tion of the thick calcareous or tough sand tubes among living coral-dwellers can regulate their growth to coincide coral colonies. Spirobracnchus tube-wall s are very thick with that of the host coral, but others need not do this. (over 1 mm), with a rigid keel, and sometimes deposit a cal Tubicolous species may possibly regulate their growth careous partition on the posterior part of the tube12); the direction and amount of tube growth.") The tubes of Den tube construction is very tough as shown in Ficopoma dropoma and Idanthyrsus rarely or frequently appeared to tus.46) surpass the host coral growth and are found partly unco Calcareous materials are produced anteriorly on the vered by living coral tissues. tube lip for growth and posteriorly to protect against or We applied the method given by Nishi and Nishihira") ganisms coming into tubes or to plug holes made by boring to five marine animals in this study, and this method is sug organisms. Spirobranchus and Dendropoma tubes rarely gested also to be applicable to other coral infauna. For a have posterior tabula or packing structures (in Dendropo mollusca, Magilus antiquus Montfort, also living in coral ma, see Fig. 2F; for Spirobranchus, Lommerzhiem47); mass, the method seems useful, as suggested by Nishi.53} Nishi and Nishihira12)). Producing large amount of calcare We examined this species tentatively only for a single ous materials on the posterior side and potential danger individual; although we cannot obtain fresh materials in from invading organisms into tubes probably causes slow- living corals, its age is possibly in excess of 5 years in an in- er growth of the coral infauna, especially of tube-dwelling dividual with over 10 cm calcareous part length (calcare species. ous siphon) deposited in nearly 8 cm depth below the coral Coral infauna probably preferentially select host corals surface. that are stable and which therefore protect the infauna Whether the organism concerned is a boring species or from predation. Scott48)confirmed that coral associates, in not is probably judged by the shape of the holes or tubes. cluding boring organisms, occur commonly in the com- Boring organisms usually make vertical straight or com mon (abundant), less aggressive corals with smaller poly plex long tubes or holes, other tubes or holes usually ta ps; and the relative abundance of the corals appears to be pered posteriorly (Fig. 1, comparing Notaulax and other stable over time. Some coral infauna are species specific on tubes or holes). host coral species (e.g., for Spirobranchus, Dai and Yan49); Nishi and Kikuchi33); review of host and associates, Pat- Acknowledgments We are grateful to Dr. James C . Tyler, Smithonian Institution, for his linguistic correction of the manuscript ton"); Scott48)). Spirobranchus prefers living coral, and com , Mr K. Asami, Chib petitively subordinate species .41)We can add a new idea a University, for identifying coral barnacle, and anonymous referees that Spirobranchus and Idanthyrsus probably select those for their useful comments. This study was supported partially by Grant- in-Aid from Japan Ministry of Education host corals which have nearly the same growth rate as that , Science, Sports and Culture (Creative Basic Research Program, DIVER). of the polychaetes. If tubicolous polychaete settle on rap- idly growing species, tubes may not be so tough. In con trast, if they settle on slowly growing coral colonies, their Age Estimation of Coral Infauna 55

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