Physical and biological factors affecting the behaviour and mortality of hydrothermal vent tubeworms (vestimentiferans)

Dee~..~ Rcsea~r.h.Vol. 37. No. I. pp. 1ff5-125.I~JO. Printedin G~at Britain+

0198--01~ 1300 + 0.00 ~) lggOPergamonPresspie.

Physical and biological factors affecting the behaviour and mortality o f hydrothermal vent t u b e w o r m s (vestimentiferans) VERENA TUNNICLIFFE,* JOHN F. GARRETI't a n d H . PAUL JOtINSON~:

(Received 3 April 1989; in revised form 19 July 1989; accepted 18 August 1989) Abstract--Vestimentiferan tubeworms of two hydrothermal vents on Juan de Fuca Ridge, northeast Pacific, were photographed with a time-lapse camera over periods of 1.5 and 26 days and supplemented with video for 25 rain. Current and turbidity measurements were also made. Mortality of the worms was heavy: 44% of the worms studied in the 26-day period were removed by falling sulphate/sulphide spires or died for other reasons. Predation effects are very common among collected specimens and implicate the activities of photographed rat-tail fish and polynoid polychaetes. Time-lag auto-correlations reveal a discernible ~midiurnal and diurnal periodicity in the retraction/extension movements of the vestimentiferan population. However, no direct correlation exists with measures of surrounding currents or suspended particulates that have clear tidal components to their periodicity. Worms in each series were examined individually but no consistent endogenous rhythm could be identified. Worms are sensitive to touch and the approach of predators and exhibit rapid retraction resptmses. Although they do not appear to respond to the second-to-minute scale variations in surrounding fluids, their short-term behaviour is highly variable. Over many days, the retraction/extension profile of each worm is quite constant and perhaps is the expression of a constant mctabolic rate. The two species examined differ substantially, with Ices than half the Ridgeia piscesae being extended at any time compared to 3/4 of the R. phaeophiale i'~pulation. Periods of retraction frequently last more than 30 min which may produce anaerobic conditions within the tube. Uptake of dissolved gases, and thus metabolic rate. is likely affected by both the specific retraction bchaviour and br,'mchial filament loss to predators.

INTRODUCTION

FLUIDS emitted by hydrothermal vents are characterized by high concentrations of dissolved hydrogen sulphide that support two unusual phenomena: deposition of polymetallic sulphides around vent orifices and clustering of vent animals dependent on chemosynthesis of organic carbon. Many vent animals live in close proximity to jets of hot water that rapidly accumulate sulphide and emit turbid clouds of suspended particulates. Fauna endemic to northeast Pacific vents inhabit an environment of active metallic sulphide deposition that has marked effects on the nearby animals (TuNNtCLtFFE and JUNIPER, in press). The dynamic nature of the physical and chemical habitat should be reflected in biotic responses. Vestimentiferan tubeworms can form much of the biomass at hydrothermal vents in the Pacific. Their association with chemosynthetic symbiotic bacteria (CAVANAUGHet al., " Department of Biology, University of Victoria, Victoria, B.C., Canada VSW 2Y2. t Ocean Physics, Institute of Ocean Sciences, Sidney, B.C., Canada V8L 2B2. ~t School of Oceanography, University of Washington, Seattle, WA 98195, U.S.A. 103

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1981; FELBECK,1981) limits this taxon to sulphide-rich habitats such as hot vents and cold seeps. The worms discussed here are placed in a family, Ridgeiidae (JoNEs, 1985), unique to the northeast Pacific spreading ridges. The several vestimentiferan species on Juan de Fuca and Explorer Ridges (T~aC~FrE, 1988) range from 10 to 150 cm in mature length and can form dense clusters around vent fluid flows. The vestimentiferan external morphology is simple: only the obturaculum, which supports the branchial plume for gas exchange, protrudes from the chitinous tube. A muscular vestimentum, or collar, wedges the animal in the tube. The fragile trunk extends down the tube and contains the trophosome, or bacteria-hosting tissues. [See W.NDER LANDand NOR~VANC (1977), JONES (1981) and SO~'HWA~ (1988) for complete morphological descriptions.] The only independent movement they show is extension and retraction of the plume. The vestimentiferan of East Pacific Rise and Galapagos, Riftia, provides a biological model. The vent tubeworm is dependent upon biosynthesis by endosymbionts for which dissolved O2, H2S and CO2 are requirements. These compounds, taken up through the branchial filaments, are stored and transported in the vascular system (CHILDREsset al., 1984). Some diffusion may occur through the tube although the sulphide oxidizing "defence capability" in the epidermis described by POWELLand SOMERO(1983) suggests that sulphide is not assimilated this way. In laboratory measurements, high metabolic rates are regulated down to low oxygen levels and to[erance of anaerobic conditions is substantial: worms survive at least 36 h without oxygen (CmLDR~S et al., 1984). Given these observations, one may expect that behaviour of a tubeworm is strongly regulated by concentrations of compounds required for metabolism. Internal concentrations would depend on environmental conditions influencing uptake and on internal storage and metabolic properties. Two interesting quantities are the time it takes to reduce fully saturated fluids to zero with no further input (i.e. the worm is retracted) and the time required to replenish the stored compounds from zero. The sum of these two times might be the length of an endogenous cycle. CHILDREss et al. (1984) provide measures that indicate stored oxygen in a 100 g Riftia would last 0.56 h (misprinted as 56 min in their paper). There is no similar information for Ridgeia, the northeast Pacific tubeworm, which is two orders of magnitude smaller with one order magnitude fewer branchial lamellae. When the branchial plume is extended, the considerable surface area of the branchial filaments is available for uptake of O2, H2S and CO2 to sustain respiration and chemosynthesis within the worm. Excretion via pores at the base of the obturaculum is also possible. The plume, however, is also exposed to predators and fouling. The action of retraction would serve to dislodge particles and to flush the tube. When retracted in the tube, the animal is relatively safe from predators, but exchange of dissolved gases is reduced. The points outlined above suggest that environmental conditions may influence vestimentiferan behaviour and that endogenous rhythms may be generated by metabolic requirements. Further, observations on in situ behaviour are an essential complement to laboratory measurements. The present study used a time-lapse camera to observed vestimentiferans at two hydrothermal vents on Juan de Fuca Ridge. It presents information on the retraction and extension behaviour of the worms that may aid interpretation of the requirements by, and controls on, the functions of these animals.

Hydrothermal vent tubeworms

105

STUDY SITES

The time-lapse camera was deployed twice in July 1986 by submersible on Axial Seamount, Juan de Fuca Ridge (Fig. 1). The venting area (ASHES vent field) at 45°55'N, 130°03'W has a few sulphide chimneys and extensive diffuse venting (HAMMOND, 1990). The target vent ("Mushroom Vent") has a sulphide core about 1.5 m high and 1.5 x 2.0 m across (Fig. 2). Numerous venting anhydrite spires form around the top, the maximum temperature of which was measured as 315°C. Another camera deployment occurred on Endeavour Segment of Juan de Fuca Ridge in September of 1984. The vent field at 47°57'N, 129°06'W has large accumulations of polymetallic sulphides (K~OSTON et al., 1984). The vent at which the camera was deployed had a sulphide core a few decimetres high with maximum temperatures measured at 56°C (JOHNSON and TU[~"~ICLIFFE,1985). METHODS

Camera

Most information for this study is obtained through camera documentation (Table 1). The time-lapse camera (Photosea, San Diego) comprised a controller, a 150 W-s electronic flash and a camera with a 250-frame capacity in which Ektachrome 200 slide film was used. The system was deployed by Alvin and Pbces IV submersibles; Table 1 gives the deployment information for each experiment. Video was taken from a submersible stationary ! m from the vent and included about 300 worms around a hot water spire. This sequence gives information on dynamic worm behaviour and their responses to predators. The time-lapse camera (TLC) was deployed for two experiments about 2.5 m from the vent, photographing the entire mound; observation position was nearly the same each time. The 1-day observation period began on the morning of 19 July, but only the photographs taken after the submersible left the vent field were used. During the 26-day run, began 29 July, the strobe misfired occasionally, giving blank --

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Fig. I. Map indicating sites at which the time-lapse camera was placed on Juan de Fuca Ridge west of the British Columbia/Washington coasts. Endeavour Segment site is at 2230 m depths: Axial Seamount site is at 1545 m depth.

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Table 1. Data collection techniques at Juan de Fuca Ridge hot vents including observation periods, instrument type ( TLC = time-lapse camera), number of images and intervals at which images were acquired during each experiment Time scale

Instrument

Data

Interval

Site

Dates

Video TLC TLC TLC

Close-up 260 frames 201 frames 170 frames

Continuous 6 rain 2.5 h 42 rain

Axial Axial Axial Endeavour

18 Jul. 1986 i9 Jul. 1986 29 Jul.-23 Aug. 1986 2-6 Sop. 1984

25 rain 24 h 26 days 5 days

slides; the malfunction disappeared after 15 days. For this deployment, the camera was attached to a nearby mooring and retrieved by acoustic recall 4 weeks later. Video and 1day observations were executed to determine if the longer-term experiments could accurately resolve worm behaviour. During the Endeavour 5-day deployment the camera sat about 1.5 m from the vent, but misalignment allowed a view of only the tops of both the worms and a sulphide mound; Fig. 1 of JOHNSON and TUNrqZCLt~'E(1985) illustrates the field of view. Data collection

Photographs were examined for gross vent changes and for presence of predators. To gather information on the nature and causes of worm movements, a group of worms was examined in each photographic series. Worms were chosen on the basis of their visibility without regard to their subsequent fate (Figs 2 and 3). In every photograph of a series, the same selected worm was scored as extended or retracted. This information was used to calculate the fraction of the determinable population extended in each slide. Turbidity variations and current shifts made position determinations in some photographs impossible. Table 2 indicates the resolution for each time-series. The mooring to which the camera was attached also supported a current meter located 20 m above the bottom and about 15 m southeast of the photographed vent. The data from that study are presented in full elsewhere (CANNON and PASmNSt~I, in press). Our velocity information comes from smoothed time-series plots of north and east current components which were hand digitized at camera firing times for the 26-day experiment and at hourly intervals for the l-day experiment; resolution was 0.5 cm s-t. Table 2. Observations on vestimentiferan behaviour. For each camera deployment, the same tubeworms were examined in each photographic frame and the branchial plume was scored as extended (or partially extended) or retracted. The mean number o f wortns extended in each frame is presented Deployment

25-min

l-day

26-day

5-day

Species

Ridgeia piscesae

Ridgeia piscesae

Ridgeia piscesae

Ridgeia phaeophiale

No. of worms

27

24

15-211"

24

Total no. of observations

Continuous

5668

3427

4080

Percent unresolvable

0

1.2

2.1

2.3

Mean % extended

45.5"t"

48.7

46.9

73.5

S.D.

39.2

14.9

13.2

7.4

• Number varied due to disappearance of some worms during study. i" For the short duration of the video sequence eight worms never emerged, but collections and T L C observations indicate that the probability of empty tubes is very low.

Hydrothermal vent tubeworms

Fig. 2. View of Mushr(~>m Vent as photographed by time-lapse camera during the l-day series. Vcstimentifcran is Ridgeia piscesae. Water temperature measured at star was 283°C. Numbered arrows indicate some individual worm plumes that were scored as retracted or expanded; all worms used were in this vicinity, Elapsed time of this image is 9.2 h. The fish is probably the macrourid Coryphaenoides acrolepis. Prints are made from colour transparencies of much greater clarity.

107

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Fig. 3. Views of Mushroom Vent taken during the 26-d~,y series: the camera is rotated slightly t~ the right compared to Fig. 2. Distance between the black marks on the rope is 50 em. Seeming lack of focus in centre of images is due to hot water refraction. (A) At elapsed time 13 days 10.5 h. spire (star) will gr<~w for another 7(l h before collapsing. Inscribed circle indicates the area measured for transmitted light thus for turbidity levels. Numhered arrows indicate some of the studied worms, (B) At elapsed time 22 days 9..~ h, many of the studied worms have been eliminated hv the Edling spire; numbered arr~ws indicate some surVivors. Two fish arc present ( t , w ~ :IM=I I + ~ J - r

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Hydrothermalvent tubeworms

109

Photograph clarity varied markedly as suspended particulate concentrations changed. Turbidity changes in the Axial 1-day and 26-day sequences were measured in a manner similar to that used in the 5-day deployment (Joru~soN and TtJr~Ntct.iF'~, 1985). Each photographic slide was mounted on a Zeiss microscope equipped with an automatic exposure unit; the same 6.75 m diameter area on each 35 mm slide corresponded to an area in the water column just above the vent (Fig. 3A). Light transmission values were measured with reference to a standard and are comparable between 1- and 26-day measurements; 5-day values, taken with different set-up, are not comparable. Axial Seamount animals were taken from the part of Mushroom Vent beyond the camera's view. Collected vestimentiferans were identified, cut from their tubes and examined for predation damage. The few Endeavour tubeworms available were identified.

Analyses Correlation and regression coefficients were calculated among various combinations of current speed, north and east components of current, turbidity and fraction of worm population extended. After subtracting mean values, time-lag auto- and cross-correlations were computed for the current speed, the north and east components of current, turbidity and the fraction of the worm population extended. For the l-day series, timelag autocorrelations were computed also for the individual worms. Blank slides or nonresolvable values were not used; the actual number of values available for a given lag was used in computing the correlation at that lag. The auto- and cross-correlations were transformed into power spectra using the Biackman-Tukey method, and confidence limits for the spectra and coherences were calculated (OxNES and Er~oolsoN, 1972). Trend removal had no significant effect, but application of a 'Harming' window improved the discrimination of spectral peaks relative to background. A maximum of 35 lags were used for the 26-day series of 245 slides to give reasonable separation between the diurnal, inertial and semidiurnal periods. For each worm, mean and standard deviation of current and turbidity variables were compared between the photographs in which that worm was extended and those in which it was retracted. A t-test examined the significance of differences. Similarly, for 1- and 5day data, the statistics of turbidity, currents and population were compared between photographs in which an extended worm was retracted in the subsequent photograph, and those other photographs in which it was extended. Photographic series were divided into five shorter segments of 50 samples for the 1- and 26-day series and 45 samples for the 5-day series. The fraction (p) of the observations for which each worm was retracted was determined for each segment. The variance of this fraction was estimated as p*(1-p), since the fraction should have a binomial distribution. A t-test determined if the retraction frequencies among the segments were significantly different. The distribution of time periods that worms spent extended and retracted was determined for each experiment and plots made of cumulative time each was extended over the observation period. Individual worm distributions were totalled to produce an overall population distribution. For the 26-day series, which had many gaps in the early part of the record, it was necessary to consider both complete sequences, in which the first and last frames could be definitely determined and incomplete sequences, where different states were observed before and after a gap.

110

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Vent anima~ The Axial vestimentiferan was identified with confidence as Ridgeia piscesae Jones. Samples from this vent included the limpet Lepetodrilus fucensis, three polynoid polychaete species, and three alvinellid polychaete species. The vestimentiferan inhabiting the Endeavour (5-day) site had the stiff gold-coloured tubes and capped obturacula matching JOtqES' (1985) description of Ridgeia phaeophiale. Also visible in photographs of this vent were the same limpet and unidentifiable polynoids.

Vent changes The most striking phenomenon in the Mushroom Vent photographs was the growth and collapse of anhydrite spires from which the hottest water flowed (Figs 2 and 3). The 1-day series revealed growth rates as high as 4 cm h-t while spires in the 26-day series grew up to 45 cm height before collapsing. The spires were fragile and, being formed mostly of sulphate minerals, quickly dissolved after falling. Detailed information will be reported elsewhere. JOHNSONand Tu~,vmcu~E (1985) described the abiotic changes at the 5-day Endeavour vent which include a visit by the submersible Alvin in the second day and the growth rate of an anhydrite spire at 2 cm day-~.

Worm mortality Three observation periods were too short to confirm animal deaths. However, of the total 32 worms studied during the 26-day series, nine disappeared during observation (Fig. 3A,B) and five others stopped emerging and were presumed dead. The field of camera view included six actively venting spires. All collapsed and regrew at least once in 26 days, one doing so six times. Spire chunks falling on nearby vestimentiferans frequently dislodged the worms. The falling spires fragments made an "avalanche" trail down the face of the mound. It was difficult to distinguish individual worms at the base and middle of the mound, but crushing and removal was evident here. Chimney collapse also meant that the location of the exit orifice for hot water changed; one worm never reemerged from its tube after a new outlet opened just below it (no. 19 in Fig. 9c). Three types of mobile animals seemed to eat tubeworms (Table 3). Rat-tail fish are common around both Juan de Fuca vent fields and display no aversion to areas of active Table 3.

Predators o f vestimentiferans seen at Juan de Fuca hydrothermal vents. Listed are the observations and sources that support the likelihood of predation activity

Predator

Observations

Source

Macrourid fish

Seen 7 times in 18 h Seen 26 times in 26 days; seen head-down among worms

1-day TLC 26-day TLC

Polynoid polychaete

Found among damaged worms Crawl to worm tops pausing partly inside

Collections Video; 5-day TLC

Majid crab

Observed once Observed feeding on worms Behaviour and stomach samplcs

26-day TLC Submersible TUNmCLWFEand JENSE~ (1987)

Hydrothermal vent tubeworms

111

venting. The Axial time-lapse pictures recorded 33 fish visits, and some fish were seen head-down among worms. Nearly all fish could be positively identified as macrourids, while fin and pattern characteristics were occasionally clear enough to tentatively identify Coryphaenoides acrolepis (Figs 2 and 3B) and Nezumia ?stelgidolepis(D. SrEt~, personal communication). No stomach content analyses or definitive observations are available to confirm predation of vestimentiferans. Close-up views by video and 5-day TLC recorded the actions of polynoid polychaetes; colour differentiation suggested that there were at least two species of the five described by PE'rnBONE (1988). They crawled up the vestimentiferans and stayed partially inserted in the top of the tube for as long as 2 h. One other known predator is the crab Macroregonia macrochira; the legs of one were seen on the last frame of one sequence. A collection of 74 vestimentiferans from the Axial vent was examined for predation damage. Worm sizes ranged from 1 to 15 mm tube diameter. Only one worm appeared untouched while 15 had lost part or all of the obturaculum, 39 had parts of both obturaculum and branchial filaments removed, and 19 had "cropped" filaments and occasionally "scalloped" edges on the vestimentum. Neither live nor preserved worms are damaged in this manner by handling. Some of the "decapitated" worms--probably due to fishmshowed signs of obturaculum regeneration. Polynoids were probably responsible for removing branchial filaments after pushing past the upper obturaculum, which flares to act as a plug. Parasites were not found in the tubes. The Endeavour specimens were not examined systematically before use in another study; however, bald patches that may have resulted from predation were noted. Ridgeia phaeophiale from another vent were examined subsequently; only three of 30 specimens were damaged.

Currents Current speed and direction during the 1- and 26-day studies are presented in Figs 4a, b and 5a, b. During August 1986, the southward current vector dominated and currents did not exceed 20 cm s-t. Spectral analysis of these data shows the presence of diurnal and seimdiurnal signals (see Fig. 6a), confirming the presence of tidal currents on the ridge. Similarly during the 5-day experiment, a weak measure of water movement (photographed worm tube displacement) showed a semidiurnal periodicity (JoHNsoN and TUSrqlCLIF~, 1985). We have no direct measure of variability of flow emanating from the vent.

Turbidity Relative variations in light backscatter (turbidity levels) observed in the photographs are presented in Figs 4e, 5c and 7a; we have no measure of absolute values of suspended particulates nor do we know if our representation is linear. The 1-day data show no large fluctuations; the initial peak is likely due to nearby submersible activity. In contrast, large fluctuations were seen during the 26-day series, a phenomenon also observed from the submersible on different days. A peak is evident in the spectral analysis (Fig. 6b) at 1.9 cpd, the semidiurnal tidal frequency. There is no direct significant correlation between current speed or direction and water turbidity; however, spectral analysis showed a high coherence of turbidity with current speed and north-south component of the current at semidiurnal and diurnal tidal frequencies (Table 4).

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Vestimentiferan population behaviour On the average, less than half the R. piscesae population was extended at any one time (Table 2), an observation that is consistent among the video, 1- and 26-day series. About 3/4 of the R. phaeophiale population was extended at any time and thereby differed significantly from R. piscesae.

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Hydrothermal vent tubeworms

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Table 4. Twenty-six day TLC data set: frequencies with significant coherence between selected variables. Coherences were calculated from time.lag correlations for lags of up to 35 photographs. All frequencies at which the signals contain significant energy 0 % of variance) and at which the coherence between the two signals is significantly different from zero at P < 0.05 are listed Variable A

Variable B

Frequency (cpd)

Coherence

N-current N-current N-current N-current Speed Speed N-current N-current Speed N-current E-current E-current E-current E-current

E-current E-current E-current E-current Turbidity Turbidity Turbidity Turbidity % Worms out % Worms out % Worms out % Worms out % Worms out % Worms out

0.274 0.960 1.509 1.921 0.960 1.921 0.960 1.921 0.960 0.960 0.274 0.960 1.509 1.921

0.614 0.946" 0.894" 0.886" 0.753" 0.674 • 0.777" 0.874* 0.784" 0.705 • 0.898" 0.594 0.817" 0.604

• Those for which P < 0.02. High coherence indicates high correlation between the signals in a specific frequency band. N-current and E-current are the north-south and east-west components of the current while speed is calculated from the north and cast vectors.

116

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a,d.

The frame-to-frame population behaviours for the different TLC series are presented in Figs 4d, 5d and 7b. Our initial analyses were to determine if these data were random or if there was a distinct pattern of coordinated population behaviour. The time-series spectral analysis could resolve no significant peaks in the 1-day data, indicating that there is no evidence for a repeating pattern with a period less than 12 h. In the 26-day spectrum, however, peaks (significantly higher than adjacent low at the 95% level) suggest a cyclic population behaviour at 0.3, 0.9 and 1.8 cpd; the latter two peaks are each somewhat broader and a lower frequency than the peaks associated with the tidal component of the currents (Fig. 6c). No significant correlation was found between current speed and percentage worms extended, but peaks in the population spectrum do show significantly high spectral coherence with the currents (Table 4). No significant relationship between percentage of worms extended and turbidity could be found. Many of the dips in the behaviour curves of Figs 4d and 5d coincide with the presence of fish or the collapse of a nearby spire although not all such disturbances elicited such responses. The effects of disturbance rarely persist beyond one photograph, even in the highfrequency l-day images. The power spectra of the 5-day population behaviour and of turbidity each show one significant peak at a frequency of 0.63 cpd. Coherence between the signals is high (0.841) but not significant at P < 0.05 because of the few degrees of freedom in this short series. As before, there may be evidence of a degree of coordinated extensioa/retraction behaviour but no clear correlation exists with measured variables. The extent to which the worms responded to common external stimuli was examined in the photograph with the Alvin manipulator placed among the studied worms. The 12 closest worms contracted and remained so as Alvin worked the vent in the following photograph; the next frame showed that most worms had re-emerged 10 min after Alvin left the site. Individual worm behaviour

Most behaviour information comes from periodic photographs. The relative frequency, 'p', that a given state (retracted or extended) is observed may be assumed to equal the fraction of time spent in that state. If successive images are statistically independent (no correlation between successive images), the number of images that occur in sequences of exactly 'n' successive images showing the worm in the same state will be (l p)2Rpn. The sequence must be preceded and followed by images showing the other state. The observed numbers of images in sequences of different lengths for the 26and 5-day series agree well with those predicted from this relation, except for a few long sequences discussed below. Predicted average sequence lengths also agree with those observed in the 26-day (1.96 and 1.92 observed "in" and "out" vs 2.11 and 1.90 expected) and 5-day (1.78 and 3.71 observed "in" and "out" vs 1.36 and 3.74 expected) populations. Thus most sequences can be explained as chance groupings of uncorrelated events and therefore contain no information on the length of time actually spent in either state, other than to suggest that these periods must be short relative to the interval between photographs. However, in the 1-day series, the distribution of sequence lengths is quite different from that expected by chance as shown in Fig. 8; these sequences may be interpreted to represent continuous worm behaviour. Two-thirds of the retraction sequences were 24 min or less and 2/3 of the total time retracted (and extended) was spent in sequences shorter than 90 min. Only 2.2% of the 504 retraction sequences in all the worms were longer than 3 h, although these represent 15% of total time retracted. One worm (no. 9) remained retracted for 6.8 h. -

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The longer series do contain long sequences which are unlikely to occur by chance sampling. From a probablistic argument, it appears the worms remain retracted for long periods. For instance, the 5-day series has four retraction sequences of nine frames (6.3 h) which is 267 times more frequent than expected by chance. Single observations of 8.0, 7.4 and 8.4 h are 250, 930 and 3500 times more frequent than expected by chance. In the 26-day series, one 14-frame sequence (35 h for worm no. 15) is 10 times the expected occurrence. Similarly, five sequences of extension span 25 h, these being 10 times the expected occurrence. Video observations indicate vestimentiferans have high tactile sensitivity and retract when touched by debris or other animals such as alvinellids or polynoids. The camera flash elicited no obvious reaction. Length of time extended was highly variable (Fig. 9a); some worms never emerged but one was extended for all but 5 s of the 25 rain period. Retraction was practically instantaneous but re-extension took a mean time of 33.2 s (n = 22; s = 8.0 s). During the 1-day deployment, the fraction of time extended for individual worms ranged from 15% (worm no. 2) to 76% (no. 11) of the observations. In Fig. 9b, the changing slopes of lines representing individual behaviour indicate that worm behaviour is not constant. In fact, division of each worm "history" into five separate segments shows that, for nearly every worm, the slope of at least two intervals are significantly different. Spectra of individual worm behaviour was inspected for periodicity that might be masked when all individuals are considered together. Only one worm shows cyclic behaviour, repeating the retraction/withdrawal sequence every 3.5 h. Some worms show indications of a similar frequency, but most have no significant periodic pattern.

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The 26-day observations verify the high worm-to-worm behaviour variability seen in R.

piscesae at Mushroom Vent (Fig. 9c) although, because of the spire collapse at 16.4 days, only four worms were visible for the entire sequence. Four other worms that apparently died during the study (nos 1, 10, 13 and 23) show the shortest times extended before death. Over this longer time, the retraction frequency of individual worms stays relatively constant; interestingly, there is a statistical difference (P > 0.1) between the initial and final slopes of no. 2 and no. 11 curves---survivors of the spire collapse. Ridgeia phaeophiale shows much lower worm-to-worm variability, with a range from 57 to 84% of the time extended (Fig. 9d). Individual behaviour curves are relatively straight as the amount and disposition of time spent retracted remains constant; the majority of curves shows no significant change in slope over the 4 days. A small orifice venting water at 56°C was located a few centimeters to the left of the worms, but no behavioural gradient with respect to position was apparent. For all time-series studies, differences in turbidity, current and population statistics between the times any one worm is retracted and then extended were examined; we find there are some differences of statistical significance, but there is no consistent pattern, i.e. one worm would be extended in times of highest current and another worm retracted. Similarly, the difference in environmental conditions immediately preceding the beginning of a retraction sequence and for other times when the worms were extended were examined for the I- and 5-day sequences. The differences are not statistically significant, so that there is no evidence for retraction in response to a change in currents, turbidity or the rest of the worm population. DISCUSSION

The rapid spire growth rates that we observe have been noted elsewhere

(IIEKINIANet

al., 1983) and such precipitation of sulphate/sulphide minerals is a common precursor to massive sulphide accumulation (HAYMON and KAS'rNER, 1981). At Mushroom Vent, TUNN[CUF'Fe and JUNWER (in press) recorded nine collapses of spires taller than 10 cm during the 26-day deployment. A subsequent year-long camera deployment at this vent confirmed the frequency and sizes of spire collapse (JoIlNSON and TUNNICLIFFE, 1988). Mass removal of animals by falling chimney fragments may be a normal feature of the vent habitat. Attrition of vestimentiferans by predators is suggested by the frequent appearances of fish in photographs and polynoids in close photographs and collections; such predators are implicated further by the damage observed on the branchial plumes of sampled animals. However, the high level of damage (nearly 100% of individuals examined) at Mushroom Vent is not always seen elsewhere. From the hundreds of vestimentiferans

Fig. 9. Extension and retraction of individual worms studied in each experiment, x-axis is the elapsed time of the experiment, y-axis is the time a particular worm spends extended. Diagonal line represents 100% elapsed time spent extended in (b), (c) and (d). Individual worms mentioned in text arc designated. (a) 25-rain video observations of Ridgeia piscesae. Eight worms never emerged so lie on the 0 line. (b) l-day TLC observations at Mushroom Vent of Ridgeia piseesae showing high variability in behaviour. (c) 26-day TLC observations at Mushroom Vent of Ridgeia piscesae showing relatively constant slopes over many days. Only three worms were present after the spire collapse at 16 days; other worms became visible and counts were begun at this time. Five worms stopped emerging and were presumed dead. (d) 5-day TLC observations at Endeavour Segment of Ridgeia phaeophiale. Worm no. 8 observations were begun at 23 h.

Hydrothermal vent tubeworms

121

examined for systematic purposes, it appears that R. piscesae tends to sustain the greatest damage and R. phaeophiale the least; vent to vent variations are great. Of the recognized Ridgeia "species" (Turo~ICLIVrE,1988), R. piscesae has the softest tube and usually a bare obtur-acular tip; R. phaeophiale has a pagoda of cuticular caps topping the obturaculum and thus plugging the tube when with- drawn. Defence mechanisms appear minimal, but R. phaeophiale may have some advantage against smaller predators. The deep-sea spider crab that is particularly abundant around the Endeavour vent site obtains part of its diet from vestimentiferans (TuN~aCLn~ and JENSEN, 1987). Intense predation pressure at the 13°N site of East Pacific Rise due to high densities of the vent crab Bythograea (see cover of Oceanologica Acta Vol. Sp. No. 8, 1988) resulted in "decapitated" tubeworms (Tevnia jerichonana) in many of the collected samples at this vent (V. TU~CUrVE, personal observation). Macrourid fish are relatively unspecialized feeders on benthic and pelagic prey, although (McLELLAN, 1977) noted no benthic component to the diet of, C. acrolepis. However, the frequency of this animal's appearance, its observed position among the worms and the total obturaculum removal in many specimens implicates it as a major predator. During the 26-day experiment, 44% of the observed worms apparently died. Although the habitat is highly favourable chemically, it is physically unstable and unpredictable. Susceptibility to mass wasting of chimneys and the lack of any really effective defence mechanisms against predators appear to result in high mortality among the vestimentireran population. Non-fatal effects, such as physical displacement and partial removal of the branchial plume, may substantially decrease the worm's capability to exchange dissolved compounds. Subsequent inability to meet the requirements of symbionts may be a secondary source of mortality. The four worms with lowest slopes in Fig. 9c all apparently died during observation: they may have been in a moribund state due to such factors before their deaths. Worms from this same population that were displaced during sampling rarely were seen extended before their eventual death (unpublished observation). Our small sample implies a mortality rate of 50% of the mature population per month on this mound. Thirteen months after this experiment, in September 1987, Mushroom Vent had far fewer vestimentiferans (TuNNICLI~ and JUNIPER, in press); recruitment success or habitat suitability had changed. Habitat variability, both spatial and temporal, is a documented feature of hydrotherreal vents. JOIINSON et al. (1986, 1988b) demonstrated the variation in dissolved gas concentrations over short distances around vent animals. TUNNICLI~E et al. (1985) and JOHNSON et al. (1988a) presented multiple-hour temperature records at worm vents that were characterized by large and rapid variations occurring over seconds; as temperature variability is a good indicator of O2 and H2S variability, JOHNSON et al. (1988a) emphasized the temporal variability in concentrations of dissolved gases that vestimentiferans must experience. Some features of the vent environment show cyclic variability; water turbidity levels and currents both have strong spectral peaks at tidal frequencies. The source of turbidity is surely suspended sulphide and sulphate particulates; a sediment trap about 10 m from Mushroom Vent measured sedimentation rates significantly higher than those outside the ventfield (R. A. FE~L~', personal communication). We tested the possibility of worm response to particulates after observing substantial quantities of particles among the branchial filaments. Our method of measuring turbidity is flawed as it is dependent upon the direction in which the plume is carried with respect to the camera. However, LAMPrrr

122

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(1985) detected deep-sea sediment suspension at tidal frequencies using a similar method. Our analyses could not discriminate the causes of turbidity variations: resuspension by tidal currents, rotation of the vent plume or fluctuations in particulate output from the vent. Rhythmic patterns in invertebrate behaviour are well-documented, particularly those associated with respiratory and feeding activities such as in polychaetes (WELLS, 1959; WEBER, 1978). Cycles in environmental conditions---light or tides--may directly induce rhythms or these exogenous patterns may become entrained in genetically controlled behaviour (SOU~ERGER, 1962). In our longer experiments, there is some coordinated activity of the worm population: spectral peaks occurring near the diurnal (5- and 26-day experiments) and semidiurnal (26-day experiment) frequencies suggest a direct response, perhaps to the flux of dissolved Oe and H2S in the current velocities changing with the tides or perhaps merely to physical displacement. The hypothesis that the worms respond to high levels of suspended particulates cannot be supported with our data. In general, none of our tests clearly indicate a strong interaction between the worms and the environmental parameters measured; either the stimuli are weak or other factors are more important. There was no coordinated activity at high frequencies in either the video or the l-day data that would indicate a response to rapid chemical fluctuations affecting the whole population. The lack of correlation between proximal, simultaneous temperature measurements found by JOHNSON et al. (1988a) suggests that spatial heterogeneity is high enough that neighbouring worms may not be experiencing the same water envelope. The possibility that response to such conditions can be visualized is not obvious, as H2S and Oe are almost mutually exclusive in water; worms would have to remain extended to bridge variations in levels of both. We had anticipated, however, that there might be a period during the tidal cycle in which the mixing of vent and bottom waters would provide optimal conditions for chemosynthesis. In considering the behaviour of worms separately, we tested the hypothesis that an endogenous rhythm was present--a rhythm that did not respond directly to external stimuli and thus would not coincide among the worms. The l-day data give a faint indication that there could be an endogenous periodic cycle in some worms but it remains equivocal. Randomly occurring stimuli such as predators or plume fouling may mask any clear internally driven patterns. The worms are highly sensitive to tactile stimuli, but the retraction response is transitory. Re-emergence soon after disruption by particles, other animals or the submersible indicates they do not have a long "memory". A characteristic of the worm behaviour profiles is the variability among worms. If retraction/extension behaviour is a reflection of metabolism, this observation is not surprising in view of the variability in metabolic rates measured by FIStlER et al. (1988) among Riftia individuals. Examining frequency, and duration of branchial plume retractions in terms of metabolic demands raises some interesting points. Firstly, short-term temporal variations of dissolved gases that may be present (JOHNSONet al., 1988a) do not elicit a visible behavioural response. Secondly, dissolved compound uptake can be modified extensively by predators that reduce the branchial area; to compensate, a greater extension time is required which may explain some of the variability seen in Fig. 9. Thirdly, the average time that these worms spend retracted is quite short and within the 0.56 h that CHILDRESSet al. (1984) calculate as the limit of stored oxygen in Riftia fluids. However, some worms do show a considerable capacity for what must be anaerobic conditions by remaining retracted in their tubes beyond this time. If the few

Hydrothermal vent tubeworrns

123

long sequences of retraction that we observe are real (fortuitous sampling is statistically improbable), they represent a sustained capacity for limited gas exchange. Finally, the relative constancy of individual behaviour patterns over many days suggests a constant metabolic demand, the level of which varies among worms. Partial plume loss and position relative to H 2 S flow may explain some of this worm-to-worm variation. However, differences in growth or reproductive state may also be important; the gradual change over 26 days for the worms surviving the spire collapse may represent a change in growth or in dissolved gas access. The observation that the two species have substantially different behavioural profiles requires further investigation. The possibility that the disparity was induced by different vent conditions cannot be eliminated. An observation that needs better substantiation is that R. phaeophiale is often found in feeble hydrothermal flows and R. piscesae is in highvolume flows (V. TUWNICLIFFE, personal observation); different species, therefore, would be expected to have different adaptations. The greater morphological protection from predators that R. phaeophiale shows may induce a less "timid" behaviour and thus it spends more time extended. The primary defence of R. piscesae may be a behavioural one with greater sensitivity to vibration or touch. In view of these observations, it would be of interest to determine if there is a substantial difference in metabolic rates between the species or in factors such as growth or reproductive rate that would affect the population survival. CONCLUSIONS

The hydrothermal vent habitat is noted for a transient and hostile nature while abundantly supplying a single substance, dissolved sulphide, that sustains its high biomass. Despite their extensive adaptations, the vestimentiferan tubeworms studied here suffer high attrition from chronic substratum collapse and from predators; probability of long-term adult survival appears low. Although current and particulate levels are cyclic and predictable, the worms show no resolvable reaction to these variations, but their response to tactile stimuli is immediate. The consistency of their behaviour over many days implies a constant metabolic requirement that is specific to each individual. Ridgeia piscesae has few defences against predation and its behaviour may be strongly adapted to avoidance. Despite favourable supply of dissolved sulphide, the population is retracted half the time. The likelihood of complete or partial plume loss may outweigh the advantages of maximizing uptake. Meanwhile, functions such as physiological "housekeeping" and tube-building can be conducted while contracted. Finally, there appears to be no advantage to encoding a behavioural rhythm in a habitat which, while presenting some cyclic phenomena, harbours frequent, and often fatal, disruptions. Acknowledgements--This work would not have been possible without the field support by the pilots of PiscesIV and Alvin and, partly, the NOAA Vents Program. Monetary support came from the Universities of Victoria and Washington, from Energy Mines and Resources Canada and from NSERC Canada. We are particularly indebted to C. Miller, A. Fisher and K. Wilson for their aid in data collection. Commentaries by Drs A. and E. Southward and a reviewer were particularly useful. We thank IFREMER, France, for computer facilities. REFERENCES CANNON G. A. and D . J . PASHINSKI. Circulation near Axial Seamount, Juan de Fuca Ridge. Journal of Geophysical Research, in press.

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CAVANAUGH C. M., S . G . G A R D ~ R , M. L. JONES, H . W . JANNASCH and J . B . WATERBURY (1981) Prokaryotic cells in the hydrothermal vent tube worm Riftia pachyptila Jones: possible chemoautotrophic symbionts. Science, 213, 340-342. CmLDKESSJ. J., A. J. Am, and C. R. FISHER(1984) M¢tabofic and blood characteristics of the hydrothermal vent tube-worm Riftia pachyptila. Marine Biology, 83. 109-124. FELBECK H. (1981) CO2 fixation in the hydrothermal vent tube worm, Riftia pachyptila Jones. Physiological Zoology, 58, 272-281. FISHER C. R., J. J. CHILI)KEYS. A. J. ARI', J. M. BROOKS, D. DISTEL, J. A. FAVUZZI, S. A. MACKO, A. NEWTON, M. A. POWELL, G. N. SOMEROand T. SOTO (1988) Physiology, morphology, and composition of Riftia pachyptila at Rose Garden in 1985. Deep-Sea Research, 35, 1745-1757. HAMMOND S. R. (1990) Relationships between lava types, sea-floor morphology and the occurrence of hydrothermal venting in the ASHES vent field of Axial Volcano. Journal of Geophysical Research, in press. HA~,4ON R. M. and M. KASTNER(1981) Hot spring deposits on the East Pacific Rise at 21°N: preliminary description of mineralogy and genesis. Earth and Planetary Science Letters, $3, 363-381. HEKINIAN R., J. FRANCHETEAU, V. RENARD, R. D. BALLARD, P. CHOUKROUNE, J. L. CHEMINEE, F. ALBAREDE,J. F. MINSTER,J. L. CHARLOU,J. C. MARTYand J. BOULEGUE(1983) Intense hydrothermal activity at the axis of the East Pacific Rise near 13°N: submersible witnesses the growth of sulfide chimney. Marine Geophysical Research, 6, 1-14. JOHNSON H. P. and V. TUNNICLIV'FE(1985) Time-series measurements of hydrothermal activity on northern Juan de Fuca Ridge. Geophysical Research Letters, 12, 685--688. JOHNSON H. P. and V. TUNNXCLIFFE(1988) Time-lapse photography of a hydrothermal system: a successful one-year deployment. EOS, 69. 1025--1026. JOHNSON K. S., C. L. BEEtILER. C. M. SAKAMOTO-ARNOLDand J. J. CHILDREYS(1986) In situ measurements of chemical distribution in a deep-sea hydrothermal vent field. Science, 231, 1139--I 141. JOtINSON K. S., J. J. CHILDRESS and C. L. BEEIILER (1988a) Short-term temperature variability in the Rose Garden hydrothermal vent field: an unstable deep-sea environment. Deep-Sea Research, 35, 1711-1721. JOIINSON K. S., J. J. CIIILDREYS, R. R. [IEYSI.ER, C. M. SAKAMOTO-ARNOLDand C. L. BEEtlLER (1988b) Chemical and biological interactions in the Rose Garden hydrothermal vent field, Galapagos spreading center. Deep-Sea Research, 35, 1723-1744. JONES M. L. (1981) Riftia pachyptila, new genus, new species, the vcstimentiferan worm from the Galapagos Rift geothermal vents (Pogonophora). Proceedings of the Biological Society of Washington, 93, 1295-1313. JONt.-S M. L. (1985) On the Vcstimcntifera, new phylum: six new species, and other taxa, from hydrothcrmal vents and elsewhere. Bulletin o[ the Biological Society of Washington, 6, 117-158. KXNGS~rONM. J., J. R. DI'LANEYand [1. P. JOIINSON(1984) Sulfide deposits from the Juan de Fuca Ridge at 47°57'N. Proceedings of the Oceans '83, Vol. 2, Marine Technological Society, pp. 811-815. LAiPrrr R. S. (1985) Evidence for the seasonal deposition of detritus to the deep-sea floor and its subsequent rcsuspension. Deep-Sea Research, 32, 885-897. LAND (VAN DVR) J. and A. NORREVANG(1977) Structure and relationships of Lamellibrachia (Annelida, Vcstimentifera). Kongelige Danske Videnskabernes Selskab, Biologiske Skrifler, 21, 1-104. McLELLAN T. (1977) Feeding strategies of the maerourids. Deep-Sea Research, 24, 1019-1036. OrNES R. A. and L. D. ENOCHSON(1972) Digital time series analysis. John Wiley, New York, 467 pp. PE'rrmoNE M. tl. (1988) New species and new records of scaled polychaetes (Polychaeta: Polynoidae) from hydrothermal vents of the northeast Pacific, Explorer and Juan de Fuca Ridges. Proceedings of the Biological Society of Washington, 101, 192-208. POWELI. M. A. and G. N. SOMERO (1983) Blood components prevent sulfide poisoning of respiration of the hydrothermal vent tube worm Riftia pachyptila. Science, 219, 297-299. SOLLBERGERA. (1962) General properties of biological rhythms. Annals of the New York Academy of Science, 98, 757-774. SOtrnIWARD E. C. (1988) Development of the gut and segmentation of newly settled stages of Ridgeia (Vestimentifera): implications for relationship between Vestimentifera and Pogonophora. Journal of the Marine Biological Association of the United Kingdom, 68, 465-487. TUNNICLIFFEV. (1988) Biogeography and evolution of hydrothermal-vent fauna in the eastern Pacific Ocean. Proceedings of the Royal Society of London, B233, 347-366. TUNNICLIV"FEV. and R. G. JENSEN (1987) Distribution and behaviour of the spider crab Macroregonia macrochira Sakai (Braehyura) around the hydrothermal vents of the northeast Pacific. Canadian Journal of Zoology, 65, 2443-2449. TUNNICLIFI:EV. and S. K. JUNIPER. Dynamic character of the hydrothermal vent habitat and the nature of sulphide chimney fauna. Progress in Oceanography, in press.

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TtYSNlCL~-E V., S. K. JUNIPER and M. E. DE BURGH (1985) The hydrothermal vent community on Axial Seamount, Juan de Fuca Ridge. In: The hydrothermal vents of the eastern Pacific Ocean: an overview, M. JONES, editor, Bulletin of the Biological Socie~ of Washington, 6, 453-464. WEBER R. E. (1978) Respiration. In: Physiology ofannelids, P. J. MILL, editor, Academic Press, New York, pp. 369-392. WF1 rx G. P. (1959) Worm autobiographies. Scientific American. 200, 132-145.