A reappraisal of feeding current systems inferred for spire-bearing brachiopods Miguel O. Manceñido1 and Rémy Gourvennec2 1 Invertebrate Palaeontology Division, La Plata Natural Sciences Museum, Paseo del Bosque s/n, B1900FWA La Plata, Argentina, and CONICET E-mail: mmanceni@fcnym.unlp.edu.ar 2 Université de Bretagne Occidentale, UMR 6538 du CNRS ‘Domaines océaniques’, Paléontologie, Avenue Le Gorgeu C.S. 93837, F29238 Brest, Cedex 3, France E-mail: remy.gourvennec@univ-brest.fr ABSTRACT: Spire-bearing brachiopods formally comprise four different rhynchonelliform orders. A calcified spiral brachidium (presumably supporting a spirolophe when alive) and variable median fold and sulcus (probably aiding separation of incurrent from excurrent flows) are peculiar characteristics they all share. Inferences regarding feeding current systems for these extinct taxa have long remained controversial. Two rival models (the Williams–Ager model and the Rudwick–Vogel model) have been developed, each of which has gained supporters as well as critics over the years. In this present paper they are both contrasted and reassessed on the basis of available evidence, together with a new approach that combines: (a) a morpho-functional analysis applying the plankton net as a suitable seston-collecting paradigm; (b) a review of actualistic data showing that all extant spirolophes are functionally inhalant (irrespective of water entering the valves laterally or not); (c) an evaluation of known outcomes from flume experiments yielding consistent empirical results where gaping shells are oriented transversally and dorsally upcurrent; and (d) a reappraisal of the distributions of certain epizoobionts and endosymbionts revealing compatible patterns. The evidence thus accumulated supports the main conclusion that, in most groups (with laterally tapering spiralia), the inhalant current was located medially with the exhalant currents on either side; only in atrypides (with centrally to dorsally tapering spiralia) does the reverse situation appear to have occurred. KEY WORDS: Athyridida, Atrypida, endosymbionts, epizoobionts, exhalant, functional analysis, inhalant, lophophore, spiralia, Spiriferida, Spiriferinida Spire-bearers comprise several orders of extinct articulate brachiopods, which suffered the effects of several mass extinction crises (most striking, in the late Devonian, late Permian and late Early Jurassic), and have long attracted the attention of palaeontologists and biologists (see, for example, Thompson 1942, pp. 831–832). While currently classified into four rhynchonelliform orders, Atrypida, Athyridida, Spiriferida and Spiriferinida (Copper & Gourvennec 1996; Williams et al. 2002, 2006), they share a number of special characteristics. Chief among these shared features are (a) the possession of spiral calcified brachidia (an evolutionary novelty according to Williams & Hurst 1977), which almost certainly supported a spirolophous lophophore in life, and (b) the variable development of an opposing but complementary median fold and sulcus that presumably served to separate inhalant currents carrying food in suspension from those drawing filtered water out, hence minimising risks of recircu- lation (Orton 1914; Ager 1963, 1968; Rudwick 1970; Fürsich & Hurst 1974; Alexander 1999a). In contrast to living organisms amenable to direct observation, when dealing with extinct marine animals, inferences about their vital functions pose a special challenge (Savazzi 1999). Since functions cannot be directly observed in fossils, one has to rely upon a conscien- tious analysis of their morphology with due regard to all competing interpretations. Alternative models that sought to explain the most likely position of inhalant and exhalant currents for these fossils were proposed in the early 1960s, with Alwyn Williams as one of the leading proponents (Williams 1960; Williams & Wright 1961). The ensuing debate does not yet seem to have been settled, as clear from a recent study (Alexander 1999a, fig. 26.1, pp. 388–389). Thus, the aim of this overview is to offer a fresh reappraisal of the available evi- dence, in order to shed new light on this interesting – though still controversial – issue, including Sir Alwyn’s own insightful contributions. 1. Summary of previous research Prevailing ideas about feeding current systems inferred for extinct spire-bearers developed over the last 47 years may be reduced to two competing theoretical models, which are herein named the Rudwick–Vogel and the Williams–Ager models, respectively (see Table 1). 1.1. The Rudwick–Vogel model In a seminal paper, Rudwick (1960a) analysed a variety of spire-bearing fossil brachiopods, reconstructing the lopho- phores as spirolophes with a single row of filaments, and recognised that such a disparity could be accommodated in two groups, which he called the ‘Atrypa-group’ (in which, looking from the cone base up, the lamella of the left spiralium is coiled anti-clockwise) and the ‘Spirifer-group’ (in which the Earth and Environmental Science Transactions of the Royal Society of Edinburgh, 98, 345–356, 2008 (for 2007) � 2008 The Royal Society of Edinburgh. doi:10.1017/S1755691007078462 corresponding lamella of the left spiralium is coiled clockwise). His analysis, in terms of an ideal efficient pumping-filtering system with the mantle cavity divided into separate, well- delimited, inhalant and exhalant chambers (cf. his figs 7–8; Fig. 1A–C), led him to conclude that spirolophes could logically fall into four conceivable categories: two inhalant types, with or without a brachidium, and two exhalant types, with or without a brachidium (which were probably evolved indepen- dently several times in the course of brachiopod evolution). Furthermore, he inferred that the brachidium supported an inhalant spirolophe in the ‘Atrypa-group’, whereas an exhalant one was supported in the ‘Spirifer-group’, and that the circu- lation pattern was the same in both of them. Namely, when alive, the water would have entered the gaping shell from either side, and after bathing the lophophore, emerged antero- centrally via the median deflection. He also speculated that transitions between those types possibly occurred during evo- lution, and that extinction of all taxa having exhalant spirolo- phes could not be attributed to lesser efficiency of the latter. In response to contemporary criticisms (Williams 1960; Williams & Wright 1961), he defended his beliefs and subse- quently reiterated his interpretation several times with little, if any, alteration (Rudwick 1960b, 1965, 1970). Independent support for this model was additionally received from (a) a study by Schumann (1967) of oriented epifaunal elements concentrated along both flanks of an alate spiriferide inter- preted as symbiotic and indicative of two inhalant segments of the commissure on either side of an exhalant dorsal median fold; (b) contributions by Vogel (1975, 1986), who discussed in detail several possible alternatives considering spirolophes with single or double rows of filaments and of exhalant or inhalant type (Vogel 1975, figs 7, 11). He concluded that for the ‘Atrypa-group’ the spiralia would act as inhalants irrespective of whether reconstructed with single or double palisades of Table 1 Synoptic comparison of main alternative models for inferred feeding current systems of spire-bearers Rudwick–Vogel model Williams–Ager model Lophophore: a simple spirolophe (with single row of filaments) Deuterolophe lophophore (bearing double row of filaments) Mantle cavity divided in inhalant and exhalant chambers Mantle cavity divided in inhalant and exhalant chambers Some lophophores functionally inhalant (Atrypa-group), all others exhalant (Spirifer-group) Most lophophores functionally inhalant (atrypids, spiriferids, cyrtinids) and very few exhalant (zygospirids, protozygids), less successful Lophophore inhalant aperture greater than exhalant (at high location) Lophophore action passively taking advantage of ambient currents Supported by uniformitarian generalisation, based on observations of living species then known Supported by flume experiments, performed in a flowing tank with gaping models of fossil shells Supported by certain inferred biotic interactions (e.g. distribution of epizoan Cornulites or embedded Diorygma) Supported by certain inferred biotic interactions (e.g. location of epizoan Aulopora or embedded Burrinjuckia) Inhalant currents placed laterally, and exhalant always central Inhalant current always central, and exhalant ones laterally placed Figure 1 Contrasting previous models for feeding current systems: (A) an atrypide (based on Atrypa reticularis); (B) a spiriferide (based on Spirifer striatus); (C) an athyridide (based on Meristina tumida); (D) an atrypide; (E) a spiriferide; (F) a zygospirid. All cross-sections; inhalant chamber stippled, exhalant chamber blank, arrows denoting water flow; not to same scale. (A)–(C) from Rudwick 1960a; (D)–(F) from Williams & Wright 1961. 346 MIGUEL O. MANCEÑIDO AND RÉMY GOURVENNEC filaments (Vogel 1975, fig. 11), and for the ‘Spirifer-group’ he favoured an interpretation of exhalant spiralia with double palisades of tentacles (Vogel 1975, fig. 7D, 1986, fig. 6), with the water incoming laterally and outgoing antero-medially in both cases. He reasoned that, for operating at advantage, the inhalant area ought to have been greater than the exhalant one, and the runoff, like a chimney, should be located at an elevated position; and (c) independent endorsement of equiva- lent feeding current patterns by Copper (1986, figs 1–10), who provided original reconstructions for several taxa of spire- bearers, including protozygids. This model still finds adherents to the present day (e.g., Pérez-Huerta & Sheldon 2006, fig. 8). 1.2. The Williams–Ager model Soon after Rudwick published his scheme, Williams (1960), while welcoming the bold and imaginative approach to infer life habits of extinct groups, expressed some reservations and offered alternative views. He rejected the lophophore restora- tion bearing a single row of filaments, arguing alternatively in favour of a deuterolophe condition. This double row arrange- ment was explicitly inspired by the side arms of the Terebratu- lina plectolophe which retain the generative tips of the lophophore medially. Subsequently, Williams & Wright (1961) further expanded their alternative reconstructions of inferred feeding-current flow within various spire-bearing stocks. They asserted that, in all cases, the inhalant stream would have entered antero-medially and the filtered water would be ejected dorso-laterally or postero-laterally, irrespective of the five fundamental attitudes of the spires recognised by them (Williams & Wright 1961, text-fig. 13; Fig. 1D–F). Therefore, in most groups (e.g. atrypids, spiriferids and cyrtinids) the spiral deuterolophe would have acted as inhalant, whereas exhalant versions would have characterised only very few, evolutionarily less successful ones (like the inwardly pointing cones of zygospirids and planispirals of protozygids). Thereafter, this model was further supported by (a) epizoan distributions on a Devonian spinocyrtiid spiriferoid, Orthos- pirifer iowensis (Owen) (formerly as Spinocyrtia, in Ager 1961), and (b) flume experiments carried out with empty shells of related taxa (Wallace & Ager 1966). With regard to athyridides (both alate as Anathyris, and rounded as Pachyplax), similar conclusions were attained on the basis of epizoan interactions and functional considerations with soft-tissue restored as a deuterolophe (Alvarez & Taylor 1987, text-fig. 2, Alvarez & Brunton 1990, text-fig. 12). Among recent supporters of this model (albeit with certain nuances) one may include Jones (1982), Blight & Blight (1990) and Brice (1991), amongst others. 1.3. Modern analogues Over the years, a number of feeding current experiments have been conducted on living brachiopods in aquaria using jets coloured with various innocuous dyes. Genera studied include: Lingula (Chuang 1959; Rudwick 1970), Novocrania [as Crania] (Orton 1914; Rowell 1961; Atkins & Rudwick 1962 ), Magas- ella [as Terebratella] (Rudwick 1962), Notosaria [as Tegulo- rhynchia], Calloria [as Terebratella or Waltonia], Neothyris (Rudwick 1962, 1970) and Megerlina (Savage 1972). These experiments have revealed that, in virtually all extant brachio- pods, adult members of quite different evolutionary stocks (both inarticulates and articulates) maintain a consistent pat- tern of two lateral inhalant currents and a central exhalant one (irrespective of whether the lophophore is a spirolophe or a plectolophe). This fact tends to support the inductive empirical conclusion that such a pattern should have been stable and universal throughout brachiopod evolutionary history. Since the above examples encompass representatives of the three subphyla recognised nowadays (i.e., linguliforms, craniiforms and rhynchonelliforms), it is not surprising that such reason- able assumption was bound to have a marked influence upon the thinking of many contemporaries. By way of corollary, the state of affairs reported in modern books aimed at wider readership sometimes still appears non-committal or controversial. For example, opposite current systems may be simultaneously depicted for the same taxon, or different opinions about flow directions of various taxa are often given as disputed, depending on the authors cited (cf. Roger 1980, Alexander 1999a, b). 2. Morpho-functional analysis An effective methodological approach specifically developed to infer function from structure in fossil organisms (and to help overcome the inherent drawbacks of resorting to uniformitar- ian comparisons alone) is called the paradigm method and its rationale and limitations are well-known in the literature (Rudwick 1964b; Carter 1967; Paul 1975, 1999). It involves a series of successive, logical steps (perception-specification- prediction-evaluation), that are applied to the question under consideration. 2.1. Perception The puzzling structure requiring functional explanation is the calcified spiral brachidium. There is ample consensus that each helical-conoidal spiralium provided a rigid support for an equally shaped spirolophous lophophore, which operated as a filter pump circulation system, but conflicting evidence cur- rently exists as to the most likely positioning of inhalant and exhalant currents during life (cf. section 1 and Table 1). 2.2. Specification The functional paradigm (i.e. the structure capable of fulfilling a certain function with maximal efficiency under natural limitations) postulated herein is the plankton net, a man-made conical tool devised for efficiently collecting microorganisms from the water (Manceñido 2003, 2005; Fig. 2A), that is an improvement of the funnel model proposed by Copper (1986). An alternative paradigm, namely a multilaminar flat filter, as considered by Vogel (1975, fig. 7B) has already been discarded as improbable by him because work would be concentrated upon the tip of the lophophore (i.e., its smallest and most delicate part). Besides, it is difficult to envisage how lophophore tentacles of each whorl would manage to remain stiffly flat under water flow, and thus it need not be further discussed here. 2.3. Predictions 2.3.1. As is familiar to marine biologists and limnologists engaged in sampling, the plankton net collects when it is pulled through the water mass, establishing an internal flow from base (mouth) to apex (i.e. water is filtered apically from the interior to the exterior of the cone). 2.3.2. With regard to the overall shape of the net itself, the smaller the apical angle of the cone, the greater the relative acceleration of the water flow inside. 2.3.3. Conversely to 2.3.1, when the net is subjected to conditions of inverted flow (by pulling it from its apex), the effect obtained is utterly inappropriate for optimising capture of microorganisms; in fact, it is the standard procedure for rinsing the net. Perhaps, in brachiopods, this might be a rare FEEDING CURRENT SYSTEMS OF SPIRE-BEARING BRACHIOPODS 347 but comparable mechanism for rejecting pseudofaeces occa- sionally reported in certain living species (Rudwick 1962, 1965). 2.4. Evaluation and interpretation The morphological range observed in the analysed structure (spiral brachidia) closely fits with the tested paradigm (plank- ton net), implying self-evident advantages for a suspension- feeder. Thus, viewed as an efficient seston-collecting organ, it is easy to envisage each spirolophe (of the pair) operating like a static, semi-rigid, plankton net forming integral elements of a larger pump-filter system (compare Figs 2A, 6A–C). Like the conical plankton net, the collecting capacity of such a spirolo- phe would be a function of the total surface area of each spiral brachium (as correctly ascertained by Rudwick 1960a, 1962, 1970; Fürsich & Hurst 1974). In the same vein, further enlargement of the filtering area of such a lophophore would be achieved by increasing the number of whorls in each spiralium, with concomitant lengthening of the spirolophe brachial axes (Gourvennec 1989, p. 204). Another predictable consequence of this paradigm would be that, if located in an inhalant sector, the bases of the cones should become gradually wider (like a bell) and with their marginal edges more distant; whereas an exhalant sector should be associated with convergence and narrowing down of the cones, in a nozzle-like fashion. A fast survey reveals that when the shape is known with sufficient detail, the former condition appears in coincidence with the median fold and sulcus of most spire-bearers, save for the atrypides (cf. Cooper & Grant 1976; Williams et al. 2002, 2006). Other paradigms may conflict with the present one. For instance, the role of the zigzag commissural deflections in some brachiopods and bivalves is controversial. Rudwick (1964a, 1970), using the paradigm method, concluded that this feature was a protective one, but Carter (1968) suggested a hydro- dynamic role (vertical spatial spread) for the inhalant and exhalant currents. The latter author emphasised the impor- tance of these structures for the exhalant flux rejecting waste particles. Adopting the paradigm of the plankton net, the role of the zigzag slits in the Spirifer-group s.l. and athyridides (i.e., spire-bearers with the base of the spiralium oriented medially) would be to assist with distributing inhalant currents over the entire basal area of the cone. The higher the median deflection (ideally as high as the base of the cone, which is generally observed), the more efficient the intake. The development of this deflection is often accompanied by a widening of the distance between the two cones (Figure 6B) that is related to an allometric broadening of the sinus/fold, resulting in an onto- genetic increase in length of the median (inhalant) segment of the commissure at the expense of the lateral (exhalant) ones. The length of the median linguiform extension may be longer than that of the lateral commissures in (sub)frontal view, giving an inhalant surface greater than the exhalant one. The weakening (or obsolescence) of the sinus-bounding ribs during ontogeny in some genera with highly developed sinus/fold (Acrospirifer, Paraspirifer, Spinocyrtia, etc.) tends to confirm this viewpoint. Incidentally, a further role of the zigzag deflec- tions reported by many authors following Rudwick (1970), namely, an increase of the area of aperture for any given gap, has proven to be wrong (Gourvennec, 1989, fig. 116) and cannot be invoked in the reconstruction of inhalant/exhalant currents. Thus the mechanical effect of the development of a median plication is consistent with the paradigm proposed here. As emphasised by Jones (1982), the location of the inhalant and exhalant currents in the Rudwick–Vogel model may cause the undesirable effect of accumulating faeces around the shell Figure 2 (A) Plankton net (being towed from right to left), to match Figure 6B, each cone should be rotated almost 90( in opposite directions; (B) Flume experiment with empty valves of Orthospirifer iowensis, anterior zenithal view, ambient flow from top to bottom, hatched arrow inhalant, blank arrows exhalant currents observed (from Wallace & Ager 1966); (C) Professor Bøggild drinking beer defying the law of gravity (from Teichert 1976). 348 MIGUEL O. MANCEÑIDO AND RÉMY GOURVENNEC and particularly in the assumed inhalant (lateral) region close to the substrate. Some authors have discussed this problem and invoked morphologic adaptations or changes increasing the efficiency of exhalant currents, among them the develop- ment of the fold (‘chimney effect’) or the more closely spaced spines in Uncinulus (Westbroek et al. 1980). In the Williams– Ager model, structures such as the extensive alae developed in some spiriferides (Eleutherokomma, Mucrospirifer, etc.) may have functioned similarly to optimise separation of inhalant and exhalant currents. This may be accompanied by a reduc- tion of the degree of crestal protection (sensu Rudwick 1964a), and thus a decrease in the number and/or weakening of the lateral ribs in relation with the development of the alae. 3. Further evidence from other sources 3.1. Actualistic evidence As pointed out in section 1.3, the actualistic assumption that inhalant currents should always enter from the sides while the exhalant jet should exit antero-medially has been an influential obstacle to alternative views. For instance, Ager (1963) reluc- tantly had to reverse the arrows in his original drawing of figure 3.10.C, due to a reviewer’s criticism (Ager 1968). How- ever, two decades later, cleverly designed experimental studies on Discradisca strigata by LaBarbera (1985) yielded interesting results, whose wider implications deserve to be explored more fully. Using a mixture of sea-water and milk released from a pipette, he was able to demonstrate that, at least in one living inarticulate (a discinoid linguliform, in modern systematic terms), the feeding-current pattern shows anterocentral intake at a frontal point funnelled by its long anterior setae, com- bined with two eddying outlets located at either side, guarded by shorter setae (LaBarbera 1985, fig. 2; see also Emig 1997, fig. 411.1). Although not specifically stated, such observations challenge the above mentioned assumption, and, contrary to previous expectations (Rowell 1961; Rudwick 1965), the actual situation resembles more closely Rowell’s (1961) fig. 2b, rather than his fig. 2c. Thus, what we learn from living brachiopods is that, while most operate with their exhalant stream located anterocentrally, some others have their inhalant stream at that location. Furthermore, since all known extant spirolophes (albeit unsupported by brachidia) function as inhalant cones, one may infer that extinct ones, supported by spiralia, may have likewise functioned as inhalant cones. A similar funnelling effect characterises water flow not only through extant spirolophes, but also through trocholophes, schizolophes and individual portions of plectolophes (cf. Rudwick 1962), thus undermining the weak contention that ontogenetic reversal from medially inhalant to laterally inhalant current flow can occur in the same living species (Fagerstrom 1996, p. 1396; Alexander 1999a, p. 389). 3.2. Flume experiments As mentioned above (section 1.2.b), the first to apply flume experiments to modelled valves of fossil spire-bearing brachio- pods in an attempt to solve this question were Wallace & Ager (1966, fig. 1; also Fig. 2B). They placed in a flowing tank conjoined, empty, but slightly gaping shells, resting in their presumed (and now generally admitted) life position (lying on the ventral interarea, with the commissural plane subvertical, and the dorsal valve somewhat tilted towards the current), and recorded in film the ‘behaviour’ of a stained jet. Their results showed that the dyed jet consistently entered via the median fold and exited in small eddies along the postero-lateral segments of the commissure. From this they concluded that, given the hydrodynamic properties of the peculiar shell mor- phology (with alate flanks and strongly uniplicate anterior commissure) under water flow, in life these brachiopods would have benefited from passive feeding under ambient flow carry- ing food in suspension, and thus the most efficient internal current system would have been inhalant at the median fold/sulcus and exhalant at the side extremities (hence circulat- ing through the spiral cones from base to apex). Resorting to the absurd, the opposite condition has been figuratively com- pared to a man trying to drink beer from a glass while standing on his head (Ager 1968, p. 163). Years ago, when one of the authors (MOM) pointed out to the late Professor Ager that the palaeontological literature does record one specimen of Homo sapiens capable of drinking beer from a bottle while upside- down (see Teichert 1976, pp. 7–8; Fig. 2C), he promptly replied that it was rather ‘the exception that confirms the rule’, as our digestive system is undoubtedly not adapted to work against gravity, but to feed (and drink) taking advantage of it. In terms of energy expenditure, a potential objection could be raised to the Williams–Ager model since it would not be optimal, particularly for alate spiriferides, because some par- ticles would have to be transported initially in the food groove to the distal part of the spiralium and subsequently back to the mouth (thus passing topologically twice over the same place), unless the distal part of the spirolophe was not operational. In this respect, the Rudwick–Vogel model would be relatively more efficient and consistent with the principle of minimal scaling. Nevertheless, it is worth noting that this aspect is not critical, since some living brachiopods such as Megerlina have been observed to feed intermittently (implying higher energetic cost) rather than continuously (Savage 1972). Similarly, among the different methods used by suspension-feeders for the capture of particles, the ‘ciliary upstream collection’ present in the brachiopods (Riisgård & Larsen 2000) is not a model for optimising energetic efficiency. More recently, noting that Wallace and Ager had docu- mented a single orientation, further similar experiments were carried out, testing gaping models of Paraspirifer bownockeri with their commissural planes in nine different attitudes rela- tive to the ambient flow and to the surface of a medium- grained sand substrate (cf. Alexander 1999a, fig. 26.20). The results yielded by this more comprehensive set of experimental tests with dyed unidirectional currents (7–10 cm/s) revealed that out of the nine different conceivable orientations, most of them failed to efficiently separate incurrent flow from exhalent flow. The only two orientations that proved feasible for producing effective separation, were (a) with the commissural plane across and the dorsal anterior facing, or inclined into, the current, in which case the water enters anteromedially and exits laterally without mixing (i.e. same orientation illustrated by Wallace & Ager 1966), and (b) with the commissural plane vertical and parallel to the current, such an arrangement facilitating lateral intake on the side that faces upcurrent (something self-evident), as well as on the lee-side downcurrent (due to eddies with large radius of curvature), whereas the water sweeping over the central fold creates a low pressure region which favours a median flow exiting away without mixing. Such an outcome was taken as furnishing inconclusive evidence of flow direction between the valves, inasmuch as opposite feeding-current patterns would result depending on the orientation of the spiriferide shells. To deal with that seemingly contradictory situation, it should be borne in mind that option (a) implies a spirolophe acting like a collecting plankton net (section 2.3.1), whilst in (b) it would act as a net being rinsed (section 2.3.3). FEEDING CURRENT SYSTEMS OF SPIRE-BEARING BRACHIOPODS 349 In addition, one can take into consideration that evidence from commensal epibionts (cf. next section 3.3.1), preferen- tially and symmetrically distributed over the dorsal valve, combined with findings in its presumed life-position, led Ager (1961, text-fig. 2) to conclude that it should have faced upstream (cf. also Vogel 1975, fig. 8; Grant 1981, p. 128; Gourvennec 1989, p. 202–203; Fagerstrom 1996, p. 1400–1401, fig. 4). Summing up, orientation (a) is more likely, whereas orientation (b) preferred by Kesling et al. (1980, text-fig. 3) and Sparks et al. (1980, text-fig. 4) is unlikely, based on Alexander’s flume experiment results (Alexander, 1999a, fig. 26.20.H). 3.3. Interactions with other organisms The value of analysing biotic interactions among fossil (and living) organisms has long been recognised in classical palaeo- ecological textbooks (Ager 1963; Hecker 1965; Roger 1980; Grant 1981, etc.). In addition, Fagerstrom (1996) provided a judicious account of the strengths and pitfalls of using epifau- nal associations to infer water circulation patterns and feeding mechanisms of the spire-bearing brachiopod hosts. According to Fagerstrom (1990, 1996), one of the essential pre-requisites is to have reliable evidence of a live–live interaction between partners. In other words, the relationship between any guest organism and its host should have developed while both were alive, as opposed to a settlement that took place post mortem. Among the key criteria to be taken into consideration in order to help recognise (or reject) such an interpretation (see also Taylor & Wilson 2003, table 4), one may mention: (i) location and/or distribution of skeletobiont guests on host: it is obvious that in the case of epizoobionts, these should occur only upon the external surface, without surpassing the edge of the valves of the host; encrustation across the commisssure, or over the hinge-line or pedicle opening, or on the internal surface of the shell would give unequivocal proof that such activity happened after death (Chang 1959; Ager 1961; Cooper & Grant 1976; Sparks et al. 1980; Spjeldnæs 1984; Gibson 1992; Fagerstrom 1996). Furthermore, some settlers may consistently occupy pref- erentially one of the valves, or a particular location on either or both of them. (ii) orientation of skeletobiont guest relative to host morpho- logy: significance is attached to conspicuous departures from random orientation (especially with regard to its feeding structures). It is very common for calcareous tube dwellers to be oriented parallel to host ribbing with tube apertures reaching just up to the commissure; conversely, growth towards topographic summits is more likely to reflect post mortem settlement. Like the preceding (and next) criterion, this one may also help clarify whether the host shell was buried in life position, or not (see for instance, Cameron 1969; Gibson 1992; Cuffey et al. 1995). Uncertainty about orientation may arise when a stable life position of the host shell is maintained after death, while still exposed to colonisation on the seabed (unless the hinge or the commissure itself became overgrown, thus revealing post mortem growth) (Chang, 1959; Sparks et al. 1980); (iii) arrangement or clustering of skeletobiont guest: in many instances, it may be possible to establish the order of clustering among individuals belonging to several genera- tions of a single species, or ecological succession among representatives of different taxa. This can be achieved by detailed examination and sequencing of local over- growths, their distance from the umbo at the commence- ment of growth and their overall pattern of average size increase (Ager 1961; Schumann 1967; Sparks et al. 1980; Alvarez & Taylor 1987; Taylor & Wilson 2003); (iv) modification of skeletobiont growth pattern closely match- ing the growth of the host: such as simultaneous growth halts affecting guest and host, or abrupt termination of an epizoobiont at a prominent growth-line of the underlying shell; colonial organisms may even branch preferentially, or extend sideways, along the commissure, thus implying synchronous growth with the host (Ager 1961; Hoare & Steller 1967; Pitrat & Rogers 1978; Alvarez & Taylor 1987; Taylor & Wilson 2003); (v) perturbation of normal growth due to various interferences between skeletobionts and host: common examples include: the host’s commissure may become disrupted, undergoing an abnormal configuration caused by crowded settlement of epizoobionts, the epibionts may develop xenomorphic sculpture as they copy in their own shells incremental growth features of the host (specially rhythmic growth banding), or the secretory regime of the host may be affected, thus building various kinds of bioreactions (tubular, blister-like, etc.) as a response to shell boring or etching (Ager 1961; Biernat 1961; Hoare & Steller 1967; Schumann 1967; Cameron 1969; MacKinnon & Biernat 1970; Rudwick 1970; Chatterton 1975; Cooper 1975, [pl. 4], Rodriguez & Gutschick 1977; Grant 1981; Fagerstrom 1990; Basset et al. 2004, etc.); (vi) host species preference and specificity: this may result from either the skeletobiont larva using a biological cue to selectively settle on a living host, or only those individuals settling on the appropriate host surviving and prospering; many associations appear to be facultative (if not ran- dom), though some others may show weak host prefer- ence, and a few may prove obligate (Thayer 1974; Taylor & Wilson 2003); statistical testing can help corroborate such preferential links among fossils (cf. Kesling et al. 1980; Sparks et al. 1980). Another important aspect to be taken into account concerns the feeding strategy of the zoobiont organism, which may be easier to ascertain in the case of taxa still represented (and sufficiently well studied) in modern seas, and more difficult (or well-nigh impossible) to guess for extinct taxa (especially if closely related descendants are wanting). Spire-bearing bra- chiopods are often found associated with a variety of epizoo- biont body fossils, such as: protozoans (foraminifers), corals (both rugose and tabulate), bryozoans (cyclostomes, ctenos- tomes, trepostomes, cystoporates, etc.), polychaetes (spiror- bids), cornulitid ‘worms’, brachiopods (discinoids, cranioids, spiriferoids), echinoderms (crinoid holdfasts), etc., as well as with several skeletozoan-produced trace fossils, usually attrib- uted to acrothoracican barnacles, spionid polychaetes, clionid sponges or even phoronids. This implies a wide choice of locations as to where feeding occurs or how and what food is taken by the guest. Yet, in this connection, the paramount distinction to be made is between those trophic strategies that would attract guest settlement around inhalant regions of the host (mostly suspension feeders, or passive carnivores or even microphagous organisms that would benefit from intercepting the inhalant current for capturing their own food) and those favouring location near exhalant regions (obviously including those with coprophagous, gametophagous, or larvae-eating habits, even also certain microphagous or suspension feeders specialised in obtaining ‘leftover’ smaller particles or some nutrients – or both – not consumed by the host). In some cases, although a preference for locating along the margin of the host clearly in a way to intercept its feeding currents has been demonstrated, the guest may take advantage of either current, irrespective of its inhalant or exhalant nature, as shown for 350 MIGUEL O. MANCEÑIDO AND RÉMY GOURVENNEC living forams on terebratulides (Zumwalt & DeLaca 1980). This is a plausible behaviour that may have been valid for other ancient zoobionts, too. As perceptively pointed out by Fagerstrom (1990, 1996), this evidence is difficult to use, without the risks of falling into circular reasoning, since the argument may be easily turned inside out, if the interpretation of the feeding mode of the guest is switched from one trophic category to another. This was honestly admitted by Schumann (1967) when stating that his reconstruction of the Mucro- spirifer feeding current system could be diametrically reversed if cornulitids were interpreted as coprophagous, yet this is not the only possibility (as just commented above). It may be recalled incidentally that other present day epizoobionts (bar- nacles) are known to be oriented predominantly facing the exhalant currents of their host (crab), even though not engaged in coprophagy (Taylor & Wilson 2003, fig. 10). Last but not least, one should also consider the kind of interorganismic coaction that was most likely operative, in the light of comprehensive reviews of the relevant terminology available in the literature (e.g. Ager 1963; Lawrence 1971; Fagerstrom 1996; Taylor & Wilson 2003). The varied diets displayed by Recent analogues hinders elucidation of the correct interaction that may have actually taken place in the distant geological past. Here, too, one faces the inherent limitations of attempting a uniformitarian approach with fossils of unknown biological affinities or taxa that have evolved by different rules (Grant 1981; Fagerstrom 1996). For the purpose of this present discussion, it may be convenient to discriminate three broad, combined categories (keeping in mind that ideally, in each category, epibionts present on different hosts or substrates should be distinguished from epibionts with specific guest-host relationship, the latter being of greater value for upholding the model). 3.3.1. External attached epizoobionts (commensal or symbi- otic). As mentioned above, one should first check that the relationship between an epizoan and its host has been genu- inely epibiotic, rather than epitaphic (a useful term describing the post-mortem use of a shell merely as a benthic island, see Sparks et al. 1980; Gibson 1992). One of the most remarkable, and oft-quoted, examples of epizoobiosis recorded on Devonian spire-bearers, is encrusting by auloporids (reptant tabulate corals) which are spread along the host commissure, sometimes following a characteristic, candelabra-like, branching pattern (Chang 1959, fig. 1; Ager 1961, fig. 1, pl.1 f.1; 1963, fig. 15.9; Hecker 1965, fig. 5; Pitrat & Rogers 1978, fig. 1; Sparks et al. 1980, pl.1 f.10, pl.3 f.1; Alvarez & Taylor 1987, figs 3.a,d, 6; Brice & Mistiaen 1992, pl.1 figs 1–4; Taylor & Wilson 2003, fig. 15). This unmistakable modular colonial growth pattern has been unanimously inter- preted as resulting from the initial settlement of a single planula that arrived with the inhalant current (reflected in the consistent disposition of the protocorallite), followed by sub- sequent, more or less symmetrical, budding, laterally and forwards, keeping pace with the host’s growth (Pitrat & Rogers 1978, fig. 1; Alvarez & Taylor 1987, figs 3, 6; Brice & Mistiaen 1992, figs 5–6; Fig. 3A–D). The reason for occurrence along exhalant regions need not be a strictly coprophagous diet. For instance, Fagerstrom (1996) has remarked that if fossil corals were zooxantellate (like some distantly related living allies), they could still benefit from nitrogenous wastes or other nutrients contained in the host faeces (whilst not from consumption of the faeces themselves), yet he also warned that if they were not symbiotic with algae, they could have competed for capturing food from inhalant currents. Cornulitids, which often preferred to grow along the grooves of strongly ribbed brachiopods (Schumann 1967; Hurst 1974), occasionally show a weak trend for concentration in the median sector of the host shell (Spjeldnæs 1984; Gourvennec 1989; Brice & Mistiaen 1992), though at other times tend to cluster in lateral sectors (Hoare & Steller 1967; Figure 3 Spinocyrtia clintoni, encrusted in candelabrum fashion by Aulocystis commensalis, from the Devonian Norway Point Fm of Michigan, USA. (A) dorsal and (B) lateral views of the same specimen; (C) (D) anterior zenithal views of two other specimens, in different stages of ontogenetic (host) and astogenetic (guest) development. Hatched arrows inhalant, blank arrows exhalant currents inferred. (C) enlarged by one third, relative to the rest; All adapted from Pitrat & Rogers 1978. FEEDING CURRENT SYSTEMS OF SPIRE-BEARING BRACHIOPODS 351 Sparks et al. 1980) or over both (Morris & Rollins 1971). They are never found with their apertures directed towards the host beak; instead they regularly grow towards the commissure (Schumann 1967; Morris & Rollins 1971; Richards 1974; Watkins 1981; Spjeldnæs 1984; Brice & Mistiaen 1992; Fager- strom 1996). Hence, they were most likely adapted to snatch food from the currents, yet they might perhaps have eaten pieces of the brachiopod mantle as well, according to a few authors (Kesling et al. 1980; Sparks et al. 1980). Schumann (1967) also regarded them as ectoparasites that allegedly utilised incurrent streams of the host (see also Richards 1974; Hurst 1974). Conversely, the occurrence of solitary (reputedly commensal) cornulitids on the dorsal fold of fossil rhynchonel- lides (Richards 1974, pl. 1, figs 1–2) is indicative of an emblematical exhalant location. Cornulitids show a great range of adaptability (Richards 1974) and, as underlined by Fagerstrom (1996), one should remain cautious about their trophic habits, type of interaction and value as a potential indicator of the host’s currents. As evidenced for the foramini- fers randomly distributed along (or near) the commissure of their brachiopod host (Zumwalt & DeLaca 1980; Fagerstrom 1996), the main criterion for settlement here could be the trophic resource availability. Bryozoans may be more likely direct competitors for sus- pended food with their brachiopod hosts (unless developing efficient trophic niche partitioning). Prominent among bryo- zoan associates stand out hederelloid encrusters (Ager 1961; Sparks et al. 1980; Alvarez & Taylor 1987; Brice & Mistiaen 1992; etc.), which sometimes display their tubular zoecia perpendicular to the host commissure (Fagerstrom 1996). Fistuliporoid bryozoans encrusting lateral areas close to the margin of Silurian Atrypa were considered competitive with the host, thus indirectly revealing the location of inhalant currents of the latter (Spjeldnæs 1984). All brachiopods in general utilise the same suspension- feeding habit (and collecting organ), and there are fine exam- ples of small spiriferides that grew fixed on the ventral median sulcus of a Devonian Paraspirifer. In such cases, it is logical to envisage a water circulation pattern common to both, host and guest (see Sparks et al. 1980, pl. 1, fig. 2, pl. 7, fig. 1; Fig. 4A–B); on the other hand, settlement of inarticulate brachio- pods may be more useful for estimating slope orientation rather than current disposition (Hoare & Steller 1967; Vogel 1975). Likewise, settlement of spirorbids (which lack the ability to change their attachment area, or to increase it appreciably), if preferential, seems to be biased towards vacant spaces on upper surfaces, rather than conditioned by the host’s feeding currents (Hurst 1974; Pitrat & Rogers 1978; Alvarez & Taylor 1987; Brice & Mistiaen 1992 vs. Ager 1963; Gekker 1966). 3.3.2. External shell-boring endozoobionts (parasitic or com- mensal). In the Devonian of Ohio, greater-than-random as- sociation of ‘Clionoides’ borings aligned along a major growth line of the Paraspirifer bownockeri host, are often matched by a similar perforated line on the opposite valve. On that basis, it has been inferred that cessation of a host’s growth was produced immediately after (and as a consequence of) damage by the shell-borer, dismissing that such borings always hap- pened to occur during a quiescent period of growth of the host (Hoare & Steller 1967; Sparks et al. 1980; Kesling et al. 1980). Hence, following a massive endozoobiont larvae settlement that produced a set of borings along the anterior edge of each valve, the host would have curtailed growth and/or feeding while repairing the damage of the infestation, and subse- quently resumed normal growth to secrete a renewed extension of the shell. This would also make sense if the organisms responsible for the borings were acrothoracican barnacles (cf. Rodriguez & Gutschick 1977) rather than ‘clionid sponges’ or polychaetes. Shell borings confidently attributable to activity by genuine acrothoracican barnacles also have been docu- mented in a variety of hosts, sometimes on the fold and sulcus, and often also over the flanks (Rodriguez & Gutschick 1977). Tubular, elongated Trypanites with their apertures clustered at the postero-lateral commissure of Devonian Acrospirifer may be attributable to shell-boring and/or embedment (Fagerstrom 1996, fig. 3) but alternative diets may be possible. Very similar borings often referred to as Vermiforichnus are recorded in several spiriferides and atrypides of various ages and ascribed to the drilling action of spionid polychaetes (Teichert 1945; Jux & Strauch 1965; Cameron 1969). 3.3.3. Internal, tube-dwelling, endosymbionts (parasitic or commensal). Peculiar kinds of exceptionally preserved ichno- fossils are known to occur as open-ended shelly tubes project- ing inwards from the inner surface of the host valves, and these have been variously interpreted as representing a parasitic (Biernat 1961; Ager 1968; Rudwick 1970; Basset et al. 2004), commensal (Chatterton 1975) or endosymbiont (Tapanila 2005) relationship. Regardless of the coaction type eventually accepted in detail, these trace fossils incontrovertibly testify that the intrusive organism became associated with the host while both were alive, and thus stimulated the latter into secreting a tubular structure that extended well into the mantle cavity. The first examples were thoroughly described and aptly named Diorygma atrypophilia by Biernat (1961, pl. 1–4; Fig. 5A–B), who initially attributed them to the activity of putative parasitic annelids drilling into ventral valves of an atrypide from the Middle Devonian of Poland (then identified as Figure 4 Paraspirifer bownockeri, with a small spiriferoid (reportedly ‘Mediospirifer audaculus’) attached on top of its ventral sulcus, from the Devonian Silica Fm of Ohio, USA. (A) anterior zenithal view and (B) close up thereof (enlarged two and a half times). Hatched arrows inhalant, blank arrows exhalant currents inferred, notice how they are reiterated in a self similar fashion at different scales (adapted from Sparks et al. 1980). 352 MIGUEL O. MANCEÑIDO AND RÉMY GOURVENNEC Atrypa zonata Schnur). This host atrypide was subsequently assigned to Desquamatia subzonata Biernat, and the intruder was reinterpreted as a phoronid, stressing at the same time that it was not a shell-borer, but a suspension feeder that settled at the larval stage on the inner epithelium of the ventral valve mantle, while the brachiopod was still immature and alive (MacKinnon & Biernat 1970). These authors further deduced that the soft tissues were pierced by the larva settling in direct contact with the calcitic shell wall (when the host lophophore was still a simple trocholophe). Thereafter, the outer epi- thelium started secreting a layer of secondary fibres around the intruder, which thus became progressively embedded in a double-channelled, tubular outgrowth of the ventral valve projecting internally. Accompanying the transformation through schizolophe to spirolophe, the endobiont gradually diverged from the midline while keeping pace and reorienting the feeding (and excretory) tubes anteriorly to always intercept the inhalant current of the host, deriving nourishment and oxygenation therein (Fig. 5C; cf. Rudwick 1970, fig. 94). MacKinnon & Biernat (1970) preferred to leave the question of a parasitic or commensal relationship unanswered, because it was impossible to judge whether the presence of Diorygma was detrimental or neutral to the wellbeing of Desquamatia, yet they noticed that when the intruders outlived the host this resulted in formation of flared tube apertures, whereas con- stricted ones would be suggestive of the reverse situation. From the Silurian of Gotland, Spjeldnæs (1984) reported (but did not illustrate) several specimens of Atrypa ‘stunted because of internal damage resembling Diorygma atrypophilia’. Very similar examples were later detected by Chatterton (1975, figs 1–2; Fig. 5D–F) from the Early Devonian of Australia (New South Wales and Victoria). They were found in dorsal valves of spiriferides (two species of Spinella and one of Howellella), and were referred to a new genus and species, namely Burrinjuckia spiriferidophilia, of uncertain systematic position (Polychaeta, Tunicata, Coelenterata, Arthropoda were mentioned as candidate phyla, but not Phoronida). The small, isolated, tube-like structures were built by a process equivalent to that of Diorygma, the only consistent minor differences being their exclusive occurrence inside dorsal valves, as single (rather than symmetrical) projections devel- oped along the sagittal plane not far from the anterior margin. Each projection ended in a single (not paired) large hole though, yet according to the figures given by Chatterton (1975, figs 1.9, 1.11), some tubes seemed to be medially divided, mimicking Diorygma. Although silicified, a calcareous original composition was invoked, since they were preserved in exactly the same fashion as the bulk of the host’s shell. The open, distal ends of the tubes were usually directed subventrally or slightly towards the front relative to the host orientation, while their proximal ends may have been open to the exterior, closed, or constricted by irregular shell growth. A few, abortive specimens appear to have been later closed on the interior and covered over by secondary shell of the host. While the possi- bility that the sedentary filter-feeding organism may have bored through the shell of the brachiopod host was not completely dismissed, it was regarded more likely that it arrived as a larva at the host valve that was facing upcurrent. Initially it would have settled at the line of commissure, causing a temporary halt in radial growth, and then became ensheathed in a tube that rose from the floor into the mantle cavity, thereafter maintaining a consistent disposition between the proximal ends of the spires. This was taken as indicative of a commensal relationship, benefiting from an advantageous location whereby food and oxygen were obtained from the inhalant current of the host (thus supporting the Williams– Ager model, see Fig. 5E–F). 4. Conclusions 1. All present day spirolophes known thus far are hydrostati- cally supported and functionally inhalant, yet the incurrent stream may be located either laterally (in most cases, as in Figure 5 (A)–(C) Desquamatia subzonata, infested by Diorygma atrypophilia, from Devonian shales of the Holy Cross Mts., Poland: (A) ventral valve interior; (B) cross section of shell; (C) stylised oblique longitudinal section of shell. (D)–(F) Spinella buchanensis, infested by Burrinjuckia spiriferidophilia, from Devonian limestones of Victoria, Australia: (D) dorsal valve interior; (E) stylised dorsal interior; (F) cut-away lateral view of shell. Hatched arrows inhalant, blank arrows exhalant currents inferred, divergent dashes denote conjectural feeding organ of guest, not to same scale. (A)–(B) from Biernat 1961; (C) adapted from Rudwick 1970; (D)–(F) from Chatterton 1975. FEEDING CURRENT SYSTEMS OF SPIRE-BEARING BRACHIOPODS 353 linguloids, cranioids and rhynchonellides), or else antero- medially (as in discinoids). This dual but unified pattern may also be true for extinct taxa whose spirolophes were supported by spiralia. 2. According to the plankton net paradigm for seston- collecting, food-laden water should flow through each helical-conoidal spiralium from the cone base towards its apex, aided (or not) by ciliary pumping action. This sug- gests that the locations of the main incurrent and excurrent streams would differ according to the spire-bearing order considered. Thus, in atrypides, with their centrally or dorsally tapering spiralia, the water probably entered by the sides and exited through the median deflection (see Fig. 6A), whereas in the rest (athyridides, spiriferides and spirif- erinides), with apices of spiralia always tapering away from the sagittal plane (sometimes ventrolaterally, or even pos- teriorly) the intake would be more likely channelled inwards through the dorsal median deflection with the outflows exiting on each flank (see Fig. 6B–C). In addition, an inhalant area greater than the exhalant one may be achieved by allometric increase of width and height of the median fold/sulcus, which is often matched in the shell interior by a comparable separation of the two conical spiralia while enlarging their basal diameters in a bell-like fashion. Overall this would result in a progressive ontogenetic lengthening of the median (inhalant) sector of the commissure at the expense of the lateral (exhalant) sectors on either side. 3. A medially inhalant flow pattern is basically consistent with empirical results obtained from flume experiments with gaping shells oriented across unidirectional ambient flow, oriented with their antero-dorsal margin facing upcurrent (Fig. 2B). 4. The improved flow model envisaged is broadly compatible with overall distribution patterns of a variety of epizoobi- onts, which have settled and grown while the brachiopod host was alive (even if uncertainties as to feeding habits of extinct guest organisms may obscure their detailed ecologi- cal relationship) (Figs 3–4). 5. The improved flow model envisaged is also consistent with the known location and orientation of internal tubular secretions developed by the brachiopod as a reaction to infestation by certain small intruder organisms (parasitic, commensal or endosymbiotic), such as Diorygma or Burr- injuckia, which almost surely opened into the inhalant chamber of the host, near the wide basal zone of its spirolophe (Fig. 5). 6. The solution supported herein, does not strictly conform in every detail with the Rudwick–Vogel nor with the Williams–Ager model, although it may be looked upon as an upgraded modification of the latter, combining strengths of both while trying to overcome any shortcomings (com- pare Fig. 1B–C with Fig. 6B–C, and Fig. 1F with Fig. 6A). Therefore, the outlined proposal for current systems of extinct spire-bearing brachiopods has been favoured in this reappraisal by virtue of its wider explanatory power and agreement with a concurrent variety of confirmatory lines of evidence. 5. Acknowledgements We are indebted to the late Sir Alwyn Williams, for being a source of encouragement and advice with his unmatched wisdom and insight. We are also grateful to the organisers for the kind invitation to submit a contribution to this Memorial Volume. MOM, as a member of the research infrastructure of CONICET acknowledges grants in support of his research. Preliminary ideas contained in this paper were advanced at the 5th International Brachiopod Congress (Copenhagen, 2005) and a local symposium on palaeoecology of the Argentine Palaeontological Association (Santa Rosa, 2003). Dr S. E. Damborenea (La Plata) is thanked for helpful comments on the draft and for assistance with processing of illustrations. Drs D. I. 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