rapid growth of a deep-sea wood-boring bivalve

Pergamon Continental Shelf Research, Vol. 14, No. 12, pp. 1349-1359, 1994

Copyright © 1994 Elsevier Science Ltd Printed in Great Britain. All rights reserved

0278-4343/94 $7.00 + 0.00

Rapid growth of a deep-sea wood-boring bivalve

WILLIAM L . ROMEY,* ROBERT C . B U L L O C K t a n d JOSEPH T . DEALTERIS:~

(Received 8 September 1992; accepted 3 February 1993)

Abstract--The growth of Xylophaga atlantica Richards, a deep-sea wood-boring bivalve, was studied by recovering a 1-year t ime series of oak and pine panels deployed at depths of 100 and 200 m at the edge of the continental shelf, south of Cape Cod. Change in shell height between samples was used to assess growth rate. At the 100 m site, the first individuals to settle grew much faster, on average, than those that settled later in the year on the same panels (0.085 mm day -1 vs 0.031 mm day - l , respectively). The growth rate of the max imum sized individuals was 0.027 mm d a y 1 whereas the modal growth rate was half that at 0.015 mm day 1. The modal growth rate of those recovered from 200 m was much greater at 0.246 m m day 1 and is thought to be due to the warmer average temperatures there. Differences in growth rate due to season, substrate and previous density were also apparent.

I N T R O D U C T I O N

DEEP-SEA organisms live under environmental regimes that are quite different from those in the well-studied seasonally disturbed and productive shallow water zones. As such, there is little reason to expect that life history characteristics, such as growth rates, of deep- sea bivalves would be similar to those of bivalves in shallow waters. The influence of physical and biological factors on the growth rate of deep-sea bivalves is not well studied. This study identifies the base line growth rate for Xylophaga atlantica, a wood-boring bivalve which is a major problem for offshore lobstermen. We also present corroborative evidence for the influence of the substrate, temperature, and crowding on growth. Concurrent studies were used to enumerate settlement ( R o M E Y , 1989; ROMEY et al., 1991) and methods of controlling the wood-borer's damage to wooden lobster traps ( D E A L T E R I S

et al., 1988a,b). GRASSLE and SANDERS (1973) suggested that most deep-sea species grow more slowly

than closely-related species living in shallower waters. Similarly, SMITH and TEAL (1973) hypothesized that deep-sea species would have relatively slow growth rates because of the reduced amount of oxygen in deeper waters. However, these generalizations were based on data from adult-skewed teleost populations, rather than on direct observation of known cohorts. Recent research on growth in Bivalvia from deep-sea v e n t s (TURNER and LUTZ,

* Depar tment of Biology, Colby College, Waterville, ME 04901, U.S.A. t D e p a r t m e n t of Zoology, University of Rhode Island, Kingston, RI 02881, U.S.A. $ Depar tment of Fisheries, Animal and Veterinary Science, University of Rhode Island, Kingston, R I 02881,

U.S .A.

1349

1350 W.L. ROMEY etal.

1984) suggest that deep-sea organisms in these ephemeral habitats may grow and reach sexual maturity more rapidly than related organisms in shallower waters.

Wood-boring bivalves of the sub-family Xylophagainae (family Pholadidae) provided some of the earliest data concerning growth in the deep-sea (TIPPER, 1968; TURNER, 1977; MANN and GALLACER, 1985). These bivalves are able to flourish in deep-sea benthic environments despite the scarcity of planktonic nutrient sources. As in the teredenids (TURNER, 1973; WATERBURY et al., 1983), Xylophaga are probably able to use the cellulose in the plant material through which they bore, via a symbiotic cellulolytic nitrogen-fixing bacteria. Since these organisms can be collected by simply putting out wood panels at a characteristic depth, wood-borers have provided some of the earliest data on deep-sea organisms. Once individuals have burrowed into the wood and begun to grow, they remain in the substrate and can be brought to the surface for examination and returned to the sea floor without apparent damage. They can also be maintained at atmospheric pressure in the laboratory for many months.

Wood-borer growth rates have been enumerated in a number of ways. Most common among these is to measure the increase in burrow length (DONS, 1940; SANTHAKUMARAN and SNELI, 1984) or shell height (NAIR and SARASWATHY, 1971; NORMAN, 1977). Other measures include: number of shell ridges (MILLER, 1922; CLAPP, 1925); body length (NAIR and SARASWATHV, 1971); and wet or dry-weight (NAIR and SARASWATnV, 1971). Variation in growth rates may be due to a variety of factors, most importantly: genetics, length of growing season, temperature, substrate qualities and inter- and intraspecific (e.g. crowding) interactions.

The objective of this study was to determine the in situ growth rate of the bivalve X. atlantica and characterize its variability. Cohort analysis was used to follow age classes of X. atlantica observed in bottom-deployed panels collected at regular time intervals. Growth rates based on the maximum, median and mode height of shells were compared.

MATERIALS AND METHODS

Vinyl-coated metal racks each holding 12 oak and 12 pine panels measuring 20 cm high × 8 cm wide × 2 cm deep, were placed at two sites at the edge of the Continental Shelf south of Cape Cod ]Fig. l(b): 40°21'N, 70°23'W) on 12 August 1987. The depth at Site 1 and Site 2 was 100 and 200 m, respectively. Racks were deployed by co-operating fishermen who incorporated them into regularly fished trawls of wire mesh lobster racks. Construction of the racks allowed a space of 0.5 to 2.0 cm between panels so that all parts of the substrate were available to settling larvae. [For further details concerning the rack design see ROMEY et al. (1991).] At regular intervals fishermen brought the racks to the surface, removed one oak and one pine panel, and returned the remaining panels to the sea floor. Retrieved panels were placed in on-board circulating sea water tanks, and then transferred to coolers on shore and transported to the chilled (14°C) running sea water tanks at the University of Rhode Island's Graduate School of Oceanography and were maintained in running sea water in order to observe the activity of the siphons. Entire panels were preserved in 70% ethyl alcohol within several days of their return. At a later time, individuals were dissected from the preserved panel by using a knife to chip away the wood. In order to insure that recently settled individuals were not overlooked, a binocular dissecting microscope was used throughout the extraction process. Whole X. atlantica were removed until at least 80 individuals had been obtained from each panel, or until no

Rapid growth of a deep-sea wood-boring bivalve 1351

(a)

(b)

1 0 0 ~ i / ~ S i l e ~

I / ~ ~ - ~ o o o ~ _ ~ o o o ~

3 9 * ~ i i • , - / '3000~ 72* 71" 70* 69*

Fig. 1. (a) S.E.M. of an empty Xylophaga atlantica shell. Note the grooved anterior used to bore through the wood. The foot would protrude from a permanent opening from the anterior ("a") and attach to the substrate. The siphons would extend well beyond the posterior ("p") of the shell. The shell's height was the measurement between the umbo ("u") and the ventral margin ("vm"). (b)

Study Sites 1 and 2 off southeastern New England, U.S.A. Depth contours are in m.


Table 1. The maximum ("Max"), mean, and mode shell height for each sample. "Day" is the elapsed number of days from when the rack of panels was first deployed on 12 August 1987. "Panel" is the number of panels that were available for analysis. "N" is the total number of individuals taken from the wood. Growth rates were calculated by taking the difference in the last two reported height values and dividing by the difference in the number of days. The

growth rate for the first panel is an estimate (see text for the method of calculating age-O)

Study Panel Height (mm) Growth (mm day-i) site type Day Panel N Max Mean Mode Max Mean Mode

1 Oak 41 1 8 0.5 0.5 0.25 0.012 0.011 0.006 68 1 18 1.6 0.6 0.25 0.040 0.003 0.000

131 2 91 5.2 1.8 1.25 0.057 0.020 0.015 276 1 84 8.6 3.0 3.25 0.023 0.008 0.013 313 1 86 7.7 3.7 3.75 0.000 0.018 0.013

Pine 41 1 10 0.5 0.4 0.25 0.012 0.009 0.006 68 1 20 1.5 0.4 0.25 0.037 0.000 0.000

131 2 109 6.9 2.8 2.25 0.085 0.037 0.031 276 2 174 7.7 3.6 3.25 0.005 0.005 0.006 313 1 35 7.7 4.6 4.50 0.000 0.027 0.033

2 Oak 74 1 12 2.0 1.3 1.75 0.027 0.017 0.023 89 1 41 4.5 2.6 2.25 0.166 0.086 0.033

Pine 74 1 8 2.0 1.3 1.25 0.027 0.017 0.016 89 1 47 5.7 4.0 3.25 0.246 0.180 0.133

Lab Oak 261 1 31 5.0 3,1 3.25 0.019 0.011 0.012 330 1 5 5.5 3.7 2.75 0.007 0.008 0.000

Pine 261 1 43 6.0 3.5 3.25 0.022 0.013 0.012 330 l 6 6.3 5.8 6.25 0.004 0.033 0.043

more could be found. Low recruitment rates during some parts of the year (RoMEY, et al., 1991), meant that equal numbers of organisms were not obtained throughout the study. Extracted individuals were kept in 70% ethyl alcohol or Bouin's solution and measured using a Wild M.8 compound microscope with a drawing tube and stage micrometer. The distance from the umbo to the ventral margin of the valve [= height, Fig. l(a)] was measured to the nearest 0.01 mm.

Historically, wood-borer growth curves have been calculated by a simple regression through the mean or maximum size measurements from a series of samples (TIPPER, 1968; NORMAN, 1977; SANTHAKUMARAN and SNELl, 1984). The complicating factor of newly settling individuals changing the "average" size was usually controlled in shallow water studies by periodically removing newly settled individuals from the experimental panels (NAIR, 1971). However, we wished to find out the growth rate of individuals in wood subjected to continuous recruitment, as they normally would. Size measurements of the individuals in each panel were first separated into 18 classes, as SOKAL and ROHLF (1969) suggest for the optimal analysis of histograms. Each histogram was then percent- transformed and plotted along an x-axis of cumulative time with "day 0" denoting the day that all racks were first deployed at that site.

Growth rates between the initial deployment and the first collection (Table 1) were calculated as if the pediveliger larvae, which are approximately 268 /~m in height (CULLINEY and TURNER, 1976), settled on the deployment date: i.e. day-0 equals age-0. In reality, age-0 for the major cohort [mode of Fig. 2(a) and (b)] was probably between November and December of 1987 (ROMEY et al., 1991). Therefore the initial growth rates reported here are probably slightly underestimated.

1354 w.L. RoMEv et al.

8.75 8.25 7.75 7.25 835

'E 8.25 E 5.75

S.25 4.75 4.25 5.75 5.25 2.75 2.25 1.75 1.25

.75

.25

30 60 90 120 150 180 210 240 270 300 330

Days (from 12 August 1987)

n-8 n-18 n-91 n-84 n-86

[ ]

[]

mmmm

I ] - 2 0 ~ o f N

~9 n n D

~ N [ ] N I

30 60 90 lzo is0 ~s0 z~0 z40 zT0 300 ~30

Fig. 2. Length-frequency diagram showing the number of organisms obtained from oak (a) and pine (b) panels retrieved from Site 1 at a particular collection date. The sample size is indicated at

the top of each histogram. The scale bar is equal to 20% of the percentage-transformed data.

R E S U L T S

Five sets of experimental panels were recovered from Site 1 between 22 September 1987 and 19 June 1988. Only two sets of panels were collected from Site 2 before the racks were lost at sea. The only species of wood-borer found in Site 1 panels was X. atlantica. But at Site 2, an undescribed species of Xylophaga (R. D. TURNER, personal communicat ion) was seen occasionally along with the predominant X. atlantica.

Percentage standardized length-frequency histograms show a continuous distribution of size classes in the later samples from Site 1. New recruits (the smallest size class) continued to colonize the oak panels until at least 22 December but not as late in the year on the pine panels (Fig. 2). The restricted data from Site 2 is only included in Fig. 3 for comparison. Maximum growth occurred before 22 December , followed by slower growth over the next 5 months (Fig. 3). It appears [Fig. 3(c), last two samples] that the average height continues to increase but that the largest individuals did not grow any larger [Fig. 3(a)].

Growth rates varied greatly depending on the time of year, substrate, site and crowding. From the limited Site 2 data it appears that growth at these deeper sites is almost twice as rapid as that from Site 1 (Table 1, Fig. 3). The mean growth rate in Site 2 oak panels was greater than the mean growth rate in pine, although the maxima are higher in pine. Also, growth of X. atlantica at Site 2, was slower in pine than in oak for the first two sampling intervals. However the situation was reversed during the next three sampling intervals, with the growth rate in pine surpassing that of oak (Fig. 3).


E E

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9 -

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DAYS F R O M S T A R T

Fig. 3. The maximum (a), mode (b) and median (c) height of a particular X. atlantica sample plotted with respect to days from the start of the experiment, 12 August 1987. Data points were

obtained from Table 1.

Given the low sample sizes of our study, we were unable to assess the variability in growth within a particular site. We calculated an average growth rate by adjusting for the apparent age of the maximum and mode size classes (Fig. 4) and plotting this against height of the shell. The average size from Site 1 oak samples revealed the most clearly defined cohort.

The date when the first organisms settled on the new panels was estimated by interpolation from Fig. 2 to be the 20th day of the study. For the mode cohort, the average

1356 w . L . ROMEY et al.

Fig. 4.

A E

.l- k -

O ,,=, ..J

[ ]

O Maximum Cohort

• Mode Cohort g o

30 60 90 120 150 180 210 240 270 300

AGE OF INDIVIDUALS (days)

The relationship between cohort shell height and age for individuals taken from the Site 1 oak panels. Age-0 was found by interpolation (see text).

day of settlement was estimated to be on the 68th day of the study (also by interpolation). The linear regression for these data (assuming the y-intercept = 0) is: height = 0.027 x age (r 2 = 0.91). For the mode cohort the regression is: height = 0.015 x age (r 2 = 0.96).

DISCUSSION

Opportunistic organisms are characterized by rapid growth and attainment of sexual maturity, high fecundity and high dispersal rates (TURNER, 1973). This type of life history is characteristic of organisms which rely on spatially and temporally unpredictable resources. Opportunism may also be an advantage in adapting to new environments more quickly (HOAGLAND and TURNER, 1981). Although Xylophaga was the first recorded opportunistic species in the deep-sea (e.g. TURNER, 1973), the discovery of a diverse fauna surrounding the abyssal thermal vents and seeps suggests that there may be other opportunistic bivalves utilizing spatially separated, short-lived resources (e.g. TURNER and LUTZ, 1984).

The present study assesses the variability of growth rates of the deep-sea wood-borer X. atlantica in a substrate subjected to continuous recruitment throughout the year. The factors responsible for intraspecific variation in our study can be attributed to a variety of factors including innate differences, as well as physical and biological factors in the environment. Although the variability in seasonal and individual growth has been documented in several species of teredinid wood-borers (NAIR and 8ARASWATI-IY, 1971), the variability of growth in Xylophaga has not previously been studied.

During the 330-day sampling period, the largest individuals followed a typical S-shaped growth pattern. Physical crowding may account for some of the decline in growth of the largest individuals towards the end of the study. Although this species can reach as much as 15 mm in height (TURNER, 1973), the largest specimen retrieved in our study was 8.6 mm. The wood in the last two samples collected was so disintegrated that the thin veneer of


wood crumbled at the lightest touch. It was also apparent that many of the largest individuals ran out of wood and had fallen out of the panels. This loss may explain the apparent decrease in observed height of the maximum-sized individuals [Fig. 3(a)]. Some of the largest shells in these samples were empty, the bivalves within having succumbed to predators, perhaps. This may account for the fact that borers growing in oak, a denser wood, reached a larger maximum size than those growing in pine [Fig. 3(a)].

Wood-boring molluscs typically show the same S-shaped growth curve seen in this study [Fig. 3(a)] in which an initial rapid growth phase levels off to an asymptotic maximum (DONS, 1940; TURNER, 1956; NORMAN, 1977; SANTHAKUMARAN and SNELI, 1984). The rapid growth phase may be an adaptation allowing the primary colonizers to establish them- selves prior to the arrival of other organisms (HOAGLAND and TURNER, 1981). The asymptote probably occurs when individuals reach adulthood and divert their energy from growth into gamete production.

It is important to compare various methods for determining growth rates from length- frequency data. Basing growth rates on the mean, maximum, or mode of length frequency diagrams may produce a variety of different estimates for growth. Most authors have used the mean rate. However, in this study, modal size was the most useful statistic for estimating growth in this type of sampling because it identifies the peak of a cohort. The mode becomes its own natural marker within a frequency distribution, and can be easily detected in subsequent samples. Although the heights of the maximum-sized individuals also identify a traceable group in the series, this group will be the first to be affected by stunting due to crowding. Thus, the mean height of a sample, used in most studies, can be heavily biased by the maximum.

NEEDLER and NEEDLER (1940) noted a positive correlation between water temperature and growth rate of the shipworm, Teredo navalis. Although specific data on temperature for our study sites was not available, nearby surveys (BERG et al., 1987; HOUGHTON el al., 1988) report that bottom temperatures near Site 1 fluctuate from 14°C in late November to 5°C in February. At locations near to Site 2 they found the temperature to be more stable, ranging from 10 to 12°C over the year. Therefore, it appears that the average temperature is higher in the deeper regions. This, in itself, may be enough to explain why these organisms grow faster in the deeper regions; they may be able to grow faster at a constant moderate temperature than one which fluctuates seasonally.

Mean and mode values [Fig. 3(b) and (c)] did not reach an asymptote in our samples and these groups continued to increase in size in the last two samples when the temperature would have been rising (HOUGHTON et al., 1988). In comparison, the growth of the maximum-sized individuals did not increase during this period of warming.

Initial settlement preferences probably account for the difference in mean height between pine and oak experimental panels. There was more recruitment on the rougher oak than on pine in this study (ROMEY, 1989). Yet those who have settled on the pine are able to rasp a greater volume of wood per unit effort, because of the different densities of the wood (TIPPER, 1968, for X. washingtona). Therefore, they are able to grow faster than those in the oak. It seems that there would be a preference for pine, but it appears that an individual's choice is more closely correlated to the surface texture than the type of wood encountered (RoMEY, 1989). This makes sense when in fact, opportunistic species are not usually in a position to make a choice, and must exploit the first food source they find.

Variation in Xylophagainae growth rates due to depth has been previously observed (TIPPER, 1968; SANTHAKUMARAN and SNELI, 1984) but rarely has growth rate and depth

1358 w . L . ROMEY et al.

b e e n c o r r e l a t e d w i t h t e m p e r a t u r e a n d t y p e o f s u b s t r a t e . TIPPER (1968) f o u n d t h a t

X. washingtona a t 1000 m g r e w a t less t h a n h a l f t h e r a t e ( 3 1 . 5 - 4 2 . 9 % ) t h a n t h o s e a t 200 m

a t s i m i l a r t e m p e r a t u r e s . I f t h e s a m p l e s in t h e p r e s e n t s t u d y f r o m S i t e 2 h a d n o t b e e n

d i s c o n t i n u e d a b e t t e r p i c t u r e o f g r o w t h r a t e w i t h r e s p e c t to d e p t h w o u l d h a v e b e e n

o b t a i n e d . H o w e v e r , d a t a f r o m t h e f i rs t t w o s a m p l e s s u g g e s t s t h a t g r o w t h m a y b e m o r e

r a p i d a t d e e p e r s i tes .

Acknowledgements--Support for this project was provided by the Rhode Island Sea Grant Program, the College of Resource Development, Agricultural Experiment Station and the College of Arts and Sciences, Department of Zoology at the University of Rhode Island. We thank T. DeWitt and an anonymous referee for valuable comments on the manuscript. The authors gratefully acknowledge the assistance of Captain Paul Bennett and the crew of the F.V. Heddy Brenna, and Captain AI Eagles and the crew of the F.V. Catherine Anne. The F.V. Reliance and all her crew were lost in November 1987 while tending traps and collecting samples for this study. Deepest sympathies are extended to the families of the captain and crew. This paper is contribution number 2853 of the Agricultural Experiment Station, College of Resource Development, University of Rhode Island.

R E F E R E N C E S

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CLAPP W. F. (1925) Notes on the stenomorphic form of the shipworm. Transactions of the Academy of Science, St. Louis, 25, 81-89.

CULLINEY J. L. and R. D. TURNER (1976) Larval development of the deep-water wood boring bivalve, Xylophaga atlantica Richards (Mollusca, Bivalvia, Pholadidae). Ophelia, 15,149-161.

DEALTERIS J. T., R. C. BULLOCK and W. L. ROMEY (1988a) Trap worms: a critical problem for the offshore lobster industry. Maritimes, 32, 14-15.

DEALTERIS J. T., R. C. BULLOCK and W. L ROMEY (1988b) Alternative treatments to prevent the biodeterioration of offshore wood lobster traps by the wood-boring bivalve, Xylophaga atlantica. Journal of Shellfish Research, 7,445-451.

DoNs C. (1940) Marine boreorganismer. If. Vekst og voksemate hos Teredo megotara. Det Kongelige Norskc Videnskabers Selskab Forhandlinger, 12, 141-144.

GRASSLE J. F. and H. L. SANDERS (1973) Life histories and the role of disturbance. Deep-Sea Research, 20,643- 659.

HOAGLAND K. E. and R. D. TURNER (1981) Evolution and adaptive radiation of wood-boring bivalves (Pholadacea). Malacologia, 21, 111-148.

HOUGHTON R. W., F. AIKMAN III and W. Ou (1988) Shelf-slope frontal structure and cross-shelf exchange at the New England shelf-break. Continental Shelf Research, 8, 687-710.

MANN R. and S. H. GALLAGER (1985) Growth morphometry and biochemical composition of the young wood boring molluscs Teredo navalis L., Bankia gouldi (Bartsch), and Nototeredo knoxi (Bartsch) (Bivalvia: Teredinidae). Journal of Experimental Marine Biology and Ecology, 85, 229-251.

MILLER R. C. (1922) Variations in the shell of Teredo navalis in San Fransisco Bay. University of Califi)rnia Publications in Zoology, 22,293-328.

NA1R N. B. and N. SARASWATHY (1971) The biology of wood-boring teredinid molluscs. Advances in Marine Biology, 9, 335-509.

NEEDLER A. W. H. and A. B. NEEDLER (1940) Growth of young shipworms (Teredo navalis) in Malpeque Bay. Journal of the Fisheries Research Board of Canada, 5, 8-10.

NORMAN E. (1977) The geographical distribution and the growth of the wood-boring molluscs Teredo navalis L., Psiloteredo megotara (Hanley) and Xylophaga dorsalis (Turton) on the Swedish West Coast. Ophelia, 16, 233-250.

ROMEY W. L. (1989) Recruitment and growth of Xylophaga atlantica. Master's Thesis, University of Rhode Island, Kingston, 113 pp.

ROMEY W. L., K. M. CASTRO, J. T. DEALTER1S and R. C. BULLOCK (1991) Recruitment in the deep-sea wood- boring bivalve Xylophaga atlantica (Richards). The Veliger, 34, 14-20.


SANTHAKUMARAN L. N. and J. A. SNELl (1984) Studies on marine fouling and wood-boring organisms of the Trondheimsfjord (Western Norway). Gunneria, 48, 1-36.

SMITH K. L. and J. M. TEAL (1973) Deep-sea benthic community respiration: an in situ study at 1850 metres. Science, 179,282-283.

SOKAL R. R. and F. J. ROHLF (1969) Biometry, W. E. Freeman and Company, San Francisco, 776 pp. TIPPER R. C. (1968) Ecological aspects of two wood-boring molluscs from the continental terrace off Oregon.

Dissertation Abstracts, 29B, 1453. TURNER R. D. (1956) Notes on Xylophaga atlantica Bartsch and on the genus. Nautilus, 70, 10-12. TURNER R. D. (1973) Wood-boring bivalves, opportunistic species in the deep sea. Science, 180, 1377-1379. TURNER R. D. (1977) Wood, mollusks, and the deep-sea food chains. Bulletin of the American Malacological

Union for 1977, 13-19. TURNER R. D. (1984) An overview of research on marine borers: past progress and future direction. In: Marine

Biodeterioration: an interdisciplinary study, Proceedings for the Symposium on Marine Biodeterioration, J. D. COSTLOW and R. C. TIPPER, editors, Uniformed Services University of Health Sciences, pp. 1-23.

TURNER R. D. and R. A. LUTZ (1984) Growth and distribution of mollusks at deep-sea vents and seeps. Oceanus, 27, 54-62.

WATERBURY J. B., C. B. CALLOWAY and R. D. TURNER (1983) A cellulolytic nitrogen-fixing bacterium cultured from the gland of Deshayes in shipworms (Bivalvia: Teredinidae). Science, 221, 1401-1403.

rapid growth of a deep-sea wood-boring bivalve

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