Epizoan ecology and interactions in the Devonian of Spain

Palaeogeography, Palaeoclimatology, Palaeoecology, 61 (1987): 17 31 Elsevier Science Publishers B.V., Amsterdam -- Printed in The Netherlands

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EPIZOAN ECOLOGY AND INTERACTIONS IN THE DEVONIAN OF SPAIN FERNANDO ALVAREZ and PAUL D. TAYLOR Departmento de Paleontologia, Universidad de Oviedo, Oviedo (Spain) Department of Palaeontology, British Museum (Natural History), London SW7 5BD (Great Britain) (Received May 6, 1986; revised and accepted Janury 27, 1987)

Abstract Alvarez, F. and Taylor, P. D., 1987. Epizoan ecology and interactions in the Devonian of Spain. Palaeogeogr., Palaeoclimatol., Palaeoecol., 61: 17-31. Shells of the brachiopod Anathyris phalaena (Phillips) from the Rafieces Group (Emsian) of NW Spain are frequently encrusted by epizoans including Aulopora, Hederella, Spirorbis and trepostome bryozoans. Aulopora is preferentially distributed on dorsal valves, and all of the epizoans occur in greater densities on the median parts of the brachiopod shells. The unusual growth pattern of Aulopora colonies implies synchronous growth of the coral and the host brachiopod. The epizoans are interpreted as symbionts of living brachiopods which were able to survive for a short time after death of their hosts. Competition for living space on the brachiopod shells is indicated by epizoan overgrowths and fouling. Anathyris was one of several spire-bearing brachiopods which supported a symbiotic fauna of epizoans during Devonian times. The frequency worldwide of brachiopod encrustation evidently declines markedly into the later part of the Palaeozoic.

Introduction E v i d e n c e for biotic i n t e r a c t i o n (Tervesz and McCall,, 1983) is not easily o b t a i n a b l e in fossil m a t e r i a l . T h e r e are often m a j o r difficulties in a s c e r t a i n i n g w h e t h e r the s u p p o s e d l y i n t e r a c t ing o r g a n i s m s a c t u a l l y lived at the s a m e t i m e and in the s a m e place. P r o b l e m s of i n t e r p r e t a tion are, h o w e v e r , m i n i m i s e d in c e r t a i n sessile i n v e r t e b r a t e s w h i c h r e t a i n t h e i r o r i g i n a l spatial l o c a t i o n s a f t e r death. N o t a b l y , epizoans c e m e n t e d to the shells of host o r g a n i s m s p r o v i d e an o p p o r t u n i t y to s t u d y possible host epizoan and e p i z o a n - e p i z o a n i n t e r a c t i o n s . T h e s e i n t e r a c t i o n s m a y give i n s i g h t s into the a u t e c o l o g y of h o s t s and epizoans (e.g. Ager, 1961; S c h u m a n n , 1967; Spjeldnaes, 1984), a n d the ecological s t r u c t u r e of h a r d s u b s t r a t u m 0031-0182/87/$03.50

c o m m u n i t i e s (e.g. T a y l o r , 1979, 1984; Liddell and Brett, 1982). T h e Rafieces G r o u p (Lower D e v o n i a n ; Emsian Stage) of A s t u r i a s , N W S p a i n h a s long b e e n k n o w n for its rich, diverse and wellp r e s e r v e d f a u n a s (De V e r n e u i l and D ' A r c h i a c , 1845; G a r c i a - A l c a l d e and Alvarez, 1976). In p a r t i c u l a r , the locality of Ferrofies h a s yielded e x c e l l e n t e x a m p l e s of the b r a c h i o p o d A n a t h y ris p h a l a e n a (Phillips), m a n y of w h i c h are e n c r u s t e d by v a r i o u s epizoans. The p r i n c i p a l aim of this s t u d y is to describe the d i s t r i b u t i o n of these epizoans on the b r a c h i o p o d s , and t h e i r m u t u a l r e l a t i o n s h i p s and possible life interactions. A c o m p a r i s o n is m a d e with p r e v i o u s l y described epizoans of D e v o n i a n b r a c h i o p o d s , and the fossil r e c o r d of e n c r u s t a t i o n of brachiopod shells is r e v i e w e d briefly.

:U 1987 Elsevier Science Publishers B.V.

18 Materials and methods A total of 36 specimens of Anathyris phalaena (Phillips) were studied from the Verneuil Collection housed at the Departement des Sciences de la Terre, Universit~ de Lyon 1 (France). These specimens were collected during the last century from Ferrofies (Asturias, NW Spain) in argillaceous limestones of the Rafieces Group (Lower Devonian; Emsian) (see Garcia-Alcalde and Alvarez, 1976, for complete description). A further six specimens collected recently from the same locality have also been utilized. Specimens prefixed ~'EM" are from the Verneuil Collection; specimens prefixed "DPO" are lodged in the Departamento de Paleontologia, Universidad de Oviedo. Most of the specimens studied have been weathered to some degree and are relatively free of matrix. Brief boiling in a mild detergent and careful brushing helped to eliminate the remaining matrix. Afterwards the specimens were carefully examined using a binocular microscope and some were selected for study using an SEM equipped with an environmental chamber capable of accommodating large, uncoated specimens (Taylor, 1986). The Ferrofies brachiopod assemblage apparently belongs to Benthic Assemblage 2-3 of Boucot (1984). Anathyris phalaena constitutes approximately 19% of the total brachiopod fauna and at least 44% of recently recovered specimens of A. phalaena have been encrusted by epizoans. The abundance of individual epizoans was deiermined by recording the number of brachi30

25

20 m m

20

25

30

opods bearing each epizoan. "Biomass" abundance and distributional pattern were also quantified using a method modified from one used by Kesling etal. (1980). Dorsal and ventral valves of the brachiopods were in turn divided into convenient radial sectors, corresponding to morphological features of the shells, which were subdivided into concentric zones from the umbo outwards (Fig.l). This enabled a total of 16 grid areas to be defined. The number of epizoans present on each of these grid areas was recorded. From these data it was possible to quantify the total number of grid areas occupied by each of the epizoan species, giving a rough "biomass" estimate, and the distribution of epizoan species over the shell surface. It must be emphasized, however, that the grid areas are not all of equivalent surface area; simple comparison of epizoan occupancy figures for each grid area cannot be used as a reliable indicator of the density of encrustation on different parts of the shells.

Brachiopod ecology Detailed study of sedimentary facies in which Anathyris is found (C. Vera, pers. comm., 1985) and the degree of preservation of the accompanying fauna (Alvarez and Brime, 1982) indicates that Anathyris inhabited a range of microhabitats in protected zones of muddy bottoms in a shallow littoral platform of moderate currents with some wave influence. Argillaceous samples from Ferrofies analysed by X-ray diffraction are mostly kaolinite with minor amounts of illite, illite-smectite mixed 30

l

A

C

B

C'

25

20ram

20

~

/

\

25

30

l

l

~

C

B

A'

C'

Fig.1.Gridsystemusedfor recordinglocationofepizoanson the twovalvesof Anathyris phalaena (Phillips).

19

layers and chlorite. This mineral suite indicates a restricted environment very close to the shoreline (Hayes, 1963; Parham, 1966; Alvarez and Brime, 1982; Gindy, 1983). The large cardinal area, the posterior thickening of the adult shells, the presence of a clear pedicle opening and the fact that the encrusting fauna occurs on both valves, suggests that Anathyris lived umbo down with its large cardinal area over the muddy substrate of the sea floor (possibly with the beak slightly buried), anchored using a functional pedicle to some bioclasts or shell debris, the lateral commissure subperpendicular to the sedi ment-water interface, and the anterior margin facing upwards into clear waters. On single bedding planes at other localities at the same stratigraphical horizon as Ferrofies several specimens of Anathyris have been found preserved in this apparent life position. However,

the effects of depositional compaction and slight tectonic deformation preclude accurate determination of the original angle between the lateral commissure and the sediment surface. If the tendency postulated by several authors (Hurst, 1974; Palmer and Fiirsich, 1974; Kesling etal., 1980) for Spirorbis to occupy upper surfaces is accepted, this would imply a life position subperpendicular to the sea floor with the dorsal valve (which bears fewer Spirorbis) slightly closer to the sediment (Fig.2). The position of inhalant and exhalant current flow in Anathyris, as in other spirebearing brachiopods, is still open to debate (see Ager, 1961; Wallace and Ager, 1966; Rudwick, 1970; Chatterton, 1975; Pitrat and Rogers, 1978; Jones, 1982; Brunton, 1984; LaBarbera, 1985). Although there is little direct evidence, a quiet water environment would favour the presence

incurremt halant"~ . "b~!.~ ~!:,!~i..i~.~...

iilexhalant . : !...'""".-i""i.'::.. ,..~.!':,'.!"L.'..'.'."...'"::-":' .'.!' :''I:I''"

il -

~

..........

-

z',~:V}~,j~

"

:

Fig.2. Inferred life position of Anathyris phalaena (Phillips), showing the suggested arrangement of feeding currents, viewed ventrally (A), dorsally (B), laterally (C), anterio-laterally (D) and obliquely (E).

20 of a median inhalant and lateral exhalant currents. This ar r an ge m ent would have allowed Anathyris to extract food particles from clear water above the muddy bottom surface and eject waste material far from the i nha l a nt current area (see Jones, 1982 for discussion). An anteromedial inhalant c ur r e nt stream may also explain the consistent position of the protocorallite of Aulopora colonies on the median depression of the fold of the dorsal valve (Fig.3.d) if, as Pitrat and Rogers (1978) supposed in a similar case, the coral planula was carried to this place of a t t a c h m e n t in the feeding cu r r en t of the brachiopod.

T a x o n o m i c composition of the epizoans The epizoans divide into two well-defined groups according to their abundance. Aulopora, Hederella spp., Spirorbis and trepostome bryozoans are present on the majority of encrusted Anathyris shells, whereas the remaining epizoans are recorded from less than 10% of the shells. This distribution is almost certainly explained, at least in part, by preservational factors. All of the common epizoans are relatively robust forms, whereas many of the r a rer epizoans (notably Ascodictyon) are small, delicate forms. Areas o f b r a c h i o p o d shell preserving good details of ornament also tend to preserve the r ar er epizoans. Preservational problems together with taxonomic difficulties (many of the epizoans have simple external morphologies and belong to groups in which systematic studies are scarce) limit the level to wh'ich the epizoans can be identified. Therefore, no attempt has been made to determine species identities or to subdivide fully the major taxonomic entities present; any such procedure would merely lend a spurious impression of precision.

The following taxa were recognised: (1) Aulopora sp. This tabulate coral (Fig.3.a, d; Fig.4a, c) is visually the dominant epizoan. The simple, tubular corallites are arranged in uniserial chains with a characteristic growth pattern which is described below. The protocorallite tapers proximally and is about 2.9 mm long by 1.3 mm wide, with an aperture 0.9 mm in transverse diameter. Most of the later corallites have a sharp, right-angled bend and range up to 6 mm in length with a width of 1.6mm and an aperture 1.1-1.5mm in transverse diameter. (2) Hederella spp. Several species of Hederella encrust Anathyris (Fig.3.c, d; Fig.4.d, e). However, colonies tend to be too incomplete to reveal their overall budding patterns, and the dimensions of the zooecia are astogenetically very variable. Therefore no attempt has been made to recognize species. HedereUa colonies have long, tubular zooecia, usually somewhat vermiform, ornamented by faint transverse annulations. The zooecia apparently bud from the sides of a stolon. They range from 0.35 mm in width in the smallest colonies, to 0.59 mm in the largest. Although Hederella is traditionally classified as a cyclostome bryozoan (e.g. Bassler, 1939), budding pattern, wall structure and zooecial dimensions suggest t hat the genus is incorrectly assigned and may not be a bryozoan. (3) Spirorbis sp. The involute spiral tubes of Spirorbis (Fig.3.a, b; Fig.4.f) range up to 4.5 mm in width and are ornamented by slight ridges transverse to growth direction. Similar worm tubes are a common element of encrusting faunas from the Silurian and Devonian. They are assumed to have been constructed by a polychaete annelid like the living Spirorbis. However, in view of the morphological simplicity of these tubes it may be unwise to accept

Fig.3. Epizoicfauna on Anathyrisphalaena (Phillips) from the RafiecesGroup (Emsian) of Ferrofies,NW Spain. All are x 1.8. a. Dorsal view of EM 20101 showing Aulopora corallites concentrated along the brachiopod commissure, Spirorbis and a sheet-like trepostome; b. Ventral view of EM 20102 showing numerous Spirorbis; c. Ventral view of EM 20103with a large HedereUa overgrowing a trepostome; d. EM 20104, dorsal view showing a colony of Aulopora commencing growth from a protocorallite situated in the median depression on the fold of the brachiopod and producing long branches growing outwards towards the two lateral margins of the brachiopod.

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Fig.4. Scanning electron micrographs of epizoans on Anathyris phalaena (Phillips) from the Rafieces Group (Emsian) of Ferrofies, NW Spain. Back-scattered electron images of uncoated specimens, a. Protocorallite (left) and early budded corallites ofAulopora, DPO 112134, x 10. b. Curved corallites from a lateral branch ofAulopora, EM 20104, x 12. c. Abraded Aulopora corallite overgrowing monotrypid trepostome, EM 20101, × 14. d. Hederella overgrowing monotrypid trepostome, EM 20103, ×9. e. Hederella on brachiopod ventral valve, EM 20106, x 9. f. Spirorbis on brachiopod ventral valve, EM 20102, x 9.

uncritically this taxonomic assignment until a s p e c t s of m o r p h o l o g y s u c h as t u b e m i c r o structure and early growth stages have been studied. (4) T r e p o s t o m e s . M o r e t h a n o n e s p e c i e s of t r e p o s t o m e b r y o z o a n (Fig.3a, c; Fig.4.c, d)

o c c u r s on t h e A n a t h y r i s s h e l l s b u t t h e i r t a x o n o m i c d e t e r m i n a t i o n h a s n o t b e e n att e m p t e d ; a l l a r e t h i n , s h e e t - l i k e c o l o n i e s from w h i c h it is difficult to p r e p a r e t h i n s e c t i o n s which would reveal taxonomically diagnostic f e a t u r e s of i n t e r n a l m o r p h o l o g y . T h e t w o

23

commonest forms are a leioclemid and a monotrypid. The leioclemid has autozooecia with small apertures (c. 0.1mm diameter) indented by acanthostyles and surrounded by smaller polymorphic zooecia (?mesozooecia). Broken bases of narrow cylindrical branches can often be observed arising from the encrusting part of the colony. The monotrypid has simple polygonal autozooecial apertures (c. 0.2 mm diameter), lacks acanthostyles and polymorphic zooecia, and is monticulate. (5) Corynotrypa sp. The runner-like cyclostome bryozoan Corynotrypa is represented by a fragmented colony/colonies of about 32 zooecia. Branch ramifications are lateral, and the parallel-sided zooecia are about 0.5 mm long by 0.2 mm wide. (6) Fistuliporid cystoporate. One poorlypreserved example of a cystoporate bryozoan has been observed. The small disc-shaped colony has zooecia with well-developed lunaria. (7) Holdfasts. A few mound-shaped structures occur which are interpreted as holdfasts, probably of ptilodictyine cryptostome bryozoans. They are about 1 cm in diameter, and have concave slopes ornamented by radial striations. Unfortunately, poor preservation obscures details of the summit and central depression within which the erect part of the colony would have articulated. (8) Ascodictyon sp. Narrow thread-like encrustations, sometimes associated with vesiclelike structures, are identified as Ascodictyon. This genus is traditionally regarded as a ctenostome bryozoan but may be better treated as a problematicum. Ascodictyon is only observed on Anathyris in which shell ornamentation is clearly defined; it has undoubtedly been removed from many other specimens by abrasion. (9) Discs. Enigmatic subcircular discs ranging between 0.4 and 0.6mm in diameter are present on a few brachiopod shells. Some have a slightly raised rim and a faintly granular surface. (10) Petrocrania sp. A single example has been observed of this encrusting inarticulate

brachiopod (see Bassett, 1984). The dorsal valve is slightly conical, about 7 mm in diameter, and has a rugose concentric ornament.

Epizoan distribution Although it is possible to find epizoans fouling the surfaces of other epizoans, most settled on apparently empty areas of brachiopod shell. The four commonest epizoans (Table I) each encrust between 60 and 70% of the study sample of Anathyris. Hederella is the most abundant in terms of the number of brachiopods which it has been observed to encrust. The "success" of each epizoan can also be gauged by the number of grid areas occupied (Table I). Values of grid occupancy for the four common epizoans range from 110 to 194 with the highest value for Aulopora. Whereas epizoans are present on roughly the same number of dorsal as ventral valves (Table II), with the exception of Aulopora, the number of grid areas occupied differs from the two valves (Table III). The total number of grid areas occupied on the dorsal valve is considerably larger than areas occupied on the ventral valve. However, Spirorbis, Hederella and trepostomes each occupy more grid areas on the ventral valve than on the dorsal valve (Table IV). The very marked preference of Aulopora for the dorsal valve outweighs the slight preference of the other common epizoans for the ventral valve. The number of grid areas encrusted appears

TABLE I Frequency of occurrence of epizoans on 40 individuals of

Anathyris phalaena from the Rafieces Group (Emsian) of Ferrofies, NW Spain Specimens encrusted

Spirorbis Hederella Trepostomes

Aulopora

Total no.

%)

29 30 25 24

72 75 63 60

Grid locations occupied

145 183 110 194

24 TABLE II Distribution of epizoans on dorsal and ventral valves of encrusted in the various shell locations

Dorsal valve Ventral valve Dorsal valve only Ventral valve only

Anathyris phalaena. Numbers are the number of brachiopods

Spirorbis

HedereUa

Trepostomes

Aulopora

22 22 6 5

21 25 5 6

19 20 3 7

23 2 21 1

TABLE III Number and percentage of grid areas occupied by epizoans on major parts of each valve of Anathyris phalaena emphasizing differential occupancy of the two valves. Figures in parenthesis are values for the median fold recalculated to the equivalent surface area as the lateral surfaces Dorsal valve

Ventral valve

Total number

Ratio DV/VV

Number

Percent

Number

Percent

All areas

381

60.3

251

39.7

632

1.52

Lateral surfaces Near hinge sector Near median fold

262 143 119

41.5 22.6 18.8

166 96 70

26.3 15.2 11.1

428 239 189

1.58 1.49 1.70

Median folds

119(476)

18.8

13.4

204

1.40

85(306)

TABLE IV Number of grid areas occupied by each epizoan on major parts of each valve of

Spirorbis

Hederella

Trepostomes

Anathyris phalaena Aulopora

DV

left AC fold CC' right C'A' Total

32 12 21 65

33 18 28 79

20 13 20 53

57 76 51 184

VV

left AC fold CC' right C'A' Total

26 29 25 80

44 31 29 104

18 21 18 57

3 4 3 10

Ratio DV/VV

left AC fold CC' right C'A' Total

Total specimens encrusted Total grid locations occupied (DV + VV)

1.52 0.41 0.84 0.81

0.75 0.58 0.97 0.76

1.11 0.62 1.11 0.93

19 19 17 18

29

30

25

24

145

183

110

194

25

44

42

40

26

17

5

8

~ 342 314 21 VENTRAL

Fig.5. Occurrences of all epizoans on ventral and dorsal valves of Anathyris phalaena (Phillips). Numbers represent the frequency of grid area occupancy.

larger for shell lateral surfaces than for median surfaces (Table III; Fig.5). However, this pattern of occupancy may be explained simply by the larger surface area of the lateral parts of Anathyris shells. Indeed, when occupancy values are adjusted proportionally to surface area, epizoans become more abundant on the median parts of shells (Table III). Of epizoan occupied grid areas, the ratio of dorsal/ventral valve occupancy is highest on lateral surfaces and lowest on the median fold (Table IV). Spirorbis, Hederella and trepostomes are fairly evenly distributed on the dorsal valve, but on the ventral valve, where they occupy more grid areas, they are more abundant in the median than in the lateral areas. Possibly they were prevented from colonizing the median areas of the dorsal valve by the common presence of Aulopora. Epizoans occur rarely (Fig.5) on the peripheral concentric band of grid areas on either valve. This is explained by the fact that only 25% of the brachiopod population studied was large enough to include peripheral grid areas numbered ~ 8 and 14-16 (Fig.l). In addition these relatively young parts of the brachiopod shell were available for colonization only for a short period of time before brachiopod death.

Brachiopod-epizoan interactions The spatial distribution of epizoans on the host brachiopod shells was dealt with above. Here evidence of life associations and postmortem associations are discussed. It is often difficult to prove a life association between a fossil epizoan and its host. Although the distribution of epizoans may appear to be related to the feeding currents of their host

(e.g. Schumann, 1967), a similar distribution can also often be explained, albeit less convincingly, by the physical hydrodynamic regime established around the host shell after death, or by differences in shell topography and ornamentation. Negative evidence for life association provided by epizoans failing to cross commissures of bivalved hosts can be unreliable; even a slight postmortem gaping of the valves could be sufficient to halt epizoan growth at the commissure, although it is possible that the valves remain tightly closed in some brachiopods after death. The most reliable indicator of a life association is a response in the skeletal growth of the host clearly related to the presence of the epizoan (see Chatterton, 1975). No host responses of this type were identified in the encrusted sample of Anathyris. A second good indicator of life association is an epizoan growth pattern closely related to the growth of the host. Ager (1961) recognized that an abrupt halt in the growth of an epizoan at a growth line on the shell of a brachiopod was indicative of life association. The pattern is explained as the result of the epizoan keeping pace with the growth of the brachiopod shell at the commissure until a traumatic event caused epizoan mortality and simultaneously checked brachiopod growth causing a growth line on the shell. One example has been observed of a leioclemid trepostome spreading across the dorsal valve of Anathyris (specimen DPO 112135) as far as a prominent growth line. The abruptness with which this trepostome is truncated at the growth line is most satisfactorily explained by the effect of a traumatic event on a life association. Growth pattern of the common epizoan

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Aulopora is usually linked very closely to that of the host Anathyris. Most of the Aulopora colonies occur on the dorsal valves of Anathy° ris and have their protocorallites located in the median depression on the fold of the brachiopod (Fig.3.d). In 9 examples where the protocorallite (Fig.4.d) could be identified, it was located 7-15 mm (~= 10.3 mm) anterior of the umbo and orientated towards the anterior commissure, parallel to the growth direction of the brachiopod. The first few budded corallites generally have the same orientation as the protocorallite but later corallites are usually aligned in two branches, one on either side of the sulcus, which extend towards the lateral margins of the shell (Fig.3.d). In 11 examples measured, these branches can first be recognized between 11 and 18mm (2=14.3mm) anterior of the umbo. Branch axes are subparallel to growth lines on the brachiopod shell, slightly transgressing younger growth lines towards the margins of the shell. For example, in one specimen (Fig.3.d) a branch comprising 9 corallites is 28 mm in length and transgresses 2 mm of brachiopod growth lines from its origin to the distalmost point at the lateral margins of the brachiopod. The corallites of these branches have an unusual morphology. Instead of being approximately straight like most Aulopora corallites, they have a sharp near 90 ° bend which separates a proximal part from a distal part (Fig.3.d). The proximal parts of the corallites form the axes of the branches, whereas the distal parts are orientated towards the anterior commissure, parallel to the growth direction of the brachiopod. The apertures of the corallites often open along the anterior commissure but sometimes form a row posterior of the commissure though parallel to it. In some examples corallites in branches posterior of the commissure have distallybudded daughter corallites oriented towards the commissure. These daughter corallites occasionally give rise to new branches parallel to the original branches but closer to the commissure. Rarely (Fig.3.a), a row of corallites is observed to diverge from a branch and grow towards the umbo of the shell.

The growth pattern of these Aulopora colonies contrasts with the dichotomously branching colonies which typify most Aulopora (e.g. Sparks et al., 1980, pl. 3, fig.l). This unusual growth pattern is related to simultaneous growth of Aulopora and the host Anathyris. A four-stage growth model (Fig.6) illustrating the development of the Aulopora:Anathyris association shows the inferred sequence of events. The coral planulae either settled selectively in the median depression on the fold of the dorsal valve, or settled in various sites on the brachiopod but only survived and grew in the median depression on the fold of the dorsal valve. The protocorallite grew towards the anterior commissure of the brachiopod and

stage 2

stage Fig.6. Four stage growth model depicting the inferred development of Auloporaon the dorsal valve of a living Anathyrisphalaena.See text for explanation.

27 budded daughter corallites with a similar growth orientation. It is not clear whether the growth of these corallites stopped short of the commissure or whether their apertures reached the commissure. A pair of branches were then initiated which grew towards the two opposite lateral margins of the brachiopod. The growing tips of these branches evidently maintained a constant distance posterior of and close to the commissure. Because the brachiopod shell itself was growing, the branches grew onto progressively younger parts of the shell, gradually transgressing growth lines. In the example given above (Fig.4.d), a branch transgressed 2 mm of brachiopod shell for 28 mm of its own growth, i.e. linear growth rate in the Aulopora colony was about 1 4 x t h a t of the brachiopod. Abrupt bending of the corallites whose proximal parts formed the axes of the branches, re-oriented the growth direction of the corallites towards the commissure. Corallite apertures thus became aligned along the commissure of the host brachiopod. Corallites were apparently able to keep their position at the commissure by growing in length. However, a maximum corallite length seems eventually to have been attained after which the aperture was left posterior of the commissure. New corallites were sometimes budded from the distal ends of these corallites, and in some cases they initiated a second generation of colony branches which grew parallel to the original branches but in a more anterior position. Aulopora colonies with this growth pattern were able to occupy new substratum space as it became available during growth of the brachiopod shell. Although the growth pattern of Aulopora gives clear evidence for a life association with Anathyris, there is a single example (specimen EM 20107) of a colony crossing the commissure of the brachiopod from dorsal to ventral valve. The early growth stages of this particular colony are typical of those inferred to have been life associates, and it seems likely that colony growth continued after death of the brachiopod. Crossing of the commissure has been observed in only one other epizoan, a

monotrypid trepostome (specimen EM 20108). It seems likely that most or all of the epizoans were life associates of Anathyris. Occurrences of Aulopora overgrowing Hederella and both monotrypid and leioclemid trepostomes is evidence for this supposition, given that Aulopora was almost certainly a life associate. The encrusting fauna as a whole is regarded as one which associated with living Anathyris but was able to survive death of the host and continue existence for a short time.

Epizoan-epizoan interactions Encrusting organisms firmly cemented to a hard substratum preserve their original spatial relationships to the substratum and to one another. Overgrowth between the skeletons of different epizoans is frequently observed (e.g. Fig.4.c, d) and can be interpreted in two ways. Firstly, it might be the result of an encounter between two living epizoans in which one of the pair was able to win substratum space by growing onto the surface of the other. Secondly, it might be the result of a living epizoan growing over the surface of a second dead epizoan. Unfortunately, distinguishing unequivocally between the patterns resulting from competitive encounters and sequential colonization is difficult (e.g. see Spjeldnaes, 1984; Taylor, 1984). However, for relatively small, short-lived substrata (e.g. brachiopod shells) it is quite likely that a good proportion of skeletal overgrowths will be the result of competitive interactions between living epizoarts. Forty-one skeletal overgrowths between pairs of epizoan species were recorded from the sample of encrusted Anathyris shells. All of these involved the four commonest epizoans (i.e. Aulopora, Hederella, Spirorbis and trepostomes). Figure 7 gives the results of these overgrowths, and Table V expresses the results for each of the four species in terms of an overgrowth ability index i.e. observed frequency as the overgrowing epizoan relative to total observed encounters. No examples were observed of reciprocal overgrowth in which an

28 TABLE V Ranked index of skeletal overgrowth ability (wins/encounters) for 41 overgrowth interactions between the 4 common epizoans of Anathyris

phalaena Epizoan

Encounters

Wins

Overgrowth ability index

Trepostomes

25 24 20 13

18 12 7 4

0.72 0.50 0.35 0.31

Hederella Aulopora Spirorbis

tre )ostomes

S

Aulopora

4

1

Spirorbis

Hederella

Fig.7. Skeletal overgrowths observed between the four common epizoans of Anathyris phalaena. Arrows point from the overgrowing towards the overgrown epizoan. Numbers indicate the frequency of observation.

individual of species A overgrew an individual of species B along part of their contact but was overgrown by the individual of species B elsewhere. However, four of the six speciespair encounters include reversal of overgrowth polarity in which certain individuals of species A overgrew individuals of species B but other individuals of species A were overgrown by individuals of species B. Such intransitivity often occurs during spatial competition between living encrusters (e.g. Buss, 1980), but may of course also reflect a non-determinate colonization sequence. However, the overgrowth ability indices match the pattern expected from spatial competition between living epizoans having the morphological characteristics of those present. Trepostome bryozoans with sheet-like colonies budding new zooecia from an encompassing growing edge are likely

to be good competitors for substratum space (see Taylor, 1984). Indeed, the trepostomes encrusting Anathyris have the highest overgrowth ability index. The other epizoans present all grew from localized points on their circumference (branch ends in Aulopora and Hederella, and the tube aperture in Spirorbis). Much of the perimeter of these taxa consists of exoskeleton vulnerable to overgrowth during life. The majority of overgrowths observed in these taxa were flank encounters in which the overgrowing epizoan surmounted the exoskeletal margins of the overgrown epizoan. The poorest spatial competitor of all seems to have been Spirorbis which not only has the smallest body size but is also the only non-colonial organism among the common epizoans. Small body size and a solitary habit are features often found in encrusters with poor competitive abilities (see Jackson, 1977). However, it would be dangerous to draw firm conclusions from the overgrowth ability indices in view of the small number of observed encounters. In addition to these skeletal overgrowths seven samples of fouling were observed. Fouling can be recognized when the origin of growth of one epizoan, representing the site of larval settlement, occurs directly atop the surface of a second epizoan. Like overgrowth, fouling may have occurred while both epizoans were alive or after the death of the epizoan that is being fouled. The seven observed instances of fouling comprise four examples of Spirorbis fouling Hederella, and three examples of Spirorbis fouling trepostomes. The fact that Spir-

29

orbis is frequently found overgrown by colonies of the taxa it may foul rules out the possibility that it is a late stage colonizer settling exclusively on the surface of earlier, dead epizoans. Discussion

The term ~'epizoan" is often applied broadly in palaeoecology to any shell-encrusting animals regardless of whether the host was alive or dead at the time of encrustation. However, neontologists generally restrict usage of epizoan to associations in which the host was alive when encrusted. The encrusting organisms attached to shells of Anathyris show several indications of having been true epizoans which were symbionts of living brachiopods. Evidence of biotic interactions can be recognized between the epizoans and their host Anathyris,, and between epizoans and other epizoans. Principal among these interactions are: (1) Apparent preferential epizoan utilization of the median fold of Anathyris, possibly in response to the position of the inhalant feeding current; (2) Colony growth pattern in Aulopora determined by shell growth in the brachiopod host; (3) Spatial overlap of different epizoans indicative of competitive overgrowth and fouling. The epizoic fauna of Anathyris resembles previously described associations of encrusters on the shells of Devonian spiriferinid brachiopods. Extensive studies (Kesling et al., 1980; Sparks et al., 1980; see also Hoare and Steller, 1967) of Paraspirifer bownockeri from the Middle Devonian of Ohio revealed the presence of 38 different encrusting and boring organisms in a population of 586 brachiopods. Of these putative epizoans, Aulopora, threadlike "ctenostomes", Hederella and Cornulites dominated, and Spirorbis was among the less common of the epizoans. Like the epizoans of Anathyris, those of P. bownockeri were found

to be distributed preferentially on the dorsal valve. Pitrat and Rogers (1978) described the epizoans of Spinocyrtia clintoni from the Devonian Traverse Group of Michigan. A number of 200 out of 280 brachiopods were found to be encrusted, and the epizoans were identified as Spirorbis, Cornulites, Paleschara (probably a trepostome bryozoan), Hederella and Aulocystis. The auloporid coral Aulocystis showed a strong preference for dorsal valves whereas the other epizoans were more often encountered on ventral valves. The growth pattern of Aulocystis illustrated by Pitrat and Rogers (1978, textfig.l.F) is extremely similar to that of the Aulopora colonies which encrust Anathyris. Over 300 specimens of Spinocyrtia iowensis from the Upper Devonian of Iowa were studied by Ager (1961) who found about 90% of them to be encrusted. The four main epizoans present were Aulopora, ~'Palaescara", Hederella and Spirorbis. Ager found evidence for life association with the host brachiopod in the occurrence of abrupt terminations of bryozoan colonies at growth lines on the brachiopod shells. A preference was shown by the epizoans for the dorsal valve and for the median fold of the brachiopods. Several other studies of encrusters on Devonian brachiopods (Shou-Hsin, 1959; Schumann, 1967; Thayer, 1974; Anderson and Dimitricopoulos, 1980; Gekker, 1983 and references therein) involve a similar range of encrusting animals, often with some indication of life association. During Devonian times, spiriferinids, and to a lesser extent other brachiopods, frequently supported epizoic faunas of suspension feeders dominated by auloporid corals, Hederella, trepostome bryozoans, Cornulites and Spirorbis. The literature contains relatively few descriptions of encrusters on bra.chiopod shells of either pre- or post-Devonian age. Notable among studies of encrusters of brachiopods not from the Devonian are: Richards (1972) for the Ordovician; Hurst (1974), Watkins (1981) and Spjeldnaes (1984) for the Silurian; Michalik (1977) for the Triassic; and Brookfield (1973) for the Jurassic. Epizoic associations have also

30

been described on living brachiopods by Rudwick (1962), Zumwalt and Delaca (1980), Hammond (1984) and D'Hondt (1984). Ager (1967, p. 170) remarked: "It is a curious sidelight of brachiopod history that though symbiotic associates [epizoans] are very common on the shells of Palaeozoic brachiopods, especially in the Devonian, they are extremely rare in the fossil record after the end of that era". Personal experience supports Ager's view except that epizoans of brachiopods seemingly become uncommon immediately after the Devonian. Indeed, the paucity of encrusters on Carboniferous and Permian brachiopods (e.g. Cooper and Grant, 1976) is particularly striking. The epizoans characteristic of Devonian brachiopods are generally not specific to particular species of brachiopod (e.g. Thayer, 1974) and can be encountered encrusting a variety of organic and inorganic substrata (e.g. Baird and Brett, 1983). There is no indication that these encrusters were dependent upon brachiopods for their taxonomic survival. Although HedereUa, encrusting auloporids, Cornulites, Spirorbis and adnate lamellar trepostomes all range upwards into the Carboniferous they become less common on brachiopods and all types of hard substrata of Carboniferous and Permian age. Possibly the late Devonian mass extinction (Frasnian-Famennian), known to have been especially harsh on suspension feeding benthos (McGhee, 1982), was important in reducing the abundance and diversity of epizoans. Encrusting associations on Mesozoic-Recent brachiopods and other hard substrata have an entirely different taxonomic composition. They consist mainly of Serpula s.l., cyclostome and, from the late Cretaceous onwards, cheilostome bryozoans, sponges, oysters, foraminifera and thecidean brachiopods. Fossil examples rarely (cf. Taylor, 1980) reveal clear evidence of life association with their brachiopod hosts. However, studies of present day brachiopods show that associations may often be symbiotic. The shells of brachiopods represent an easily

defined category of substrata which has been utilized by a variety of suspension-feeding encrusters since Ordovician times. The emerging pattern of varying abundance of encrusters on fossil brachiopods through geological time requires further study and explanation.

Acknowledgements C. Brime, Departamento de Cristalografia y Mineralogia, Universidad de Oviedo, is thanked for X-raying samples and for discussing the results. We are grateful to C. H. C. Brunton, British Museum (Natural History) for helpful discussions on brachiopod ecology and for giving his comments on the manuscript, and to A. Prieur, D~partement des Sciences de la Terre, de l'Universit~ de Lyon 1, for the loan of specimens in his care, and D. Claugher and the staff of the Electron Microscope and Photographic Units of the British Museum (Natural History) for all the facilities placed at our disposal. F. A. grateful acknowledges financial support from the British Council.

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