What is the significance of sporangiophore

This provides the basic elements for the developmental regulatory changes that we propose to explain the diversity and evolution of equisetacean reproductive morphology. This developmental framework also suggests potential tests for the hypotheses advanced here. Apical region of a growing Cruciaetheca patagonica shoot in reproductive mode. Patterns of sporangiophore shown in red at right, on the explanatory tracing of the photograph size and distribution corroborate the proposition that sporangiophores are produced along internodes as the result of expression of a reproductive programme in the intercalary meristem.

The extent of fertile zones of successive internodes increases with the increase in internode length toward the base of the shoot due to bending of the stem — shown in grey — leaf bases mask significant parts of internodes in the basal portion of this shoot.

Furthermore, within internodes, the largest sporangiophores are located apically and sporangiophore size decreases toward the base of the internode. These observations are consistent with a pattern of development wherein an intercalary meristem produces tissues and sporangiophores which are displaced apically as they mature.

A decrease in sporangiophore size basally within individual internodes, conspicuous in Late Permian Phyllotheca verbitskae Verbitskaja and Radczenko, ; Doweld, , provides further support for the hypothesis proposed here. The same pattern is probably present in Early Permian Cruciaetheca genoensis Cuneo and Escapa, but is less conspicuous because this species produces only two whorls of sporangiophores per internode.

Occurrences that may be illustrating the same developmental pattern include specimens reported as Tschernovia sp. Heterochronic change in the expression of a reproductive programme in the intercalary meristem result in different lengths of the internode portions covered in sporangiophores, depending on the duration of expression of the reproductive programme; these are illustrated by several extinct equisetaleans.

At one end of the spectrum 1 , Cruciaetheca genoensis exemplifies a condition in which the reproductive programme, turned on at the beginning of internode development, is expressed for a short fraction of the entire interval of internode growth, following which the internode completes growth in vegetative mode; the result is an internode that bears only two sporangiophore whorls at its apical end.

Extension of the duration of expression of the reproductive programme over a longer portion of the interval of internode growth 2 produces internodes covered in a higher number of sporangiophore whorls 3—5 in Cruciaetheca patagonica and with a shorter sterile portion at the base.

At the other end of the spectrum 3 , Peltotheca furcata exemplifies a condition in which the reproductive program is expressed throughout the entire interval of internode growth, producing internodes covered in sporangiophore whorls from top to base. In some of the cases referenced here, the extent of fertile zones is difficult to assess due to imperfect fossil preservation or poor quality of published illustrations.

For the same reasons, it is unclear whether any equisetaleans provide evidence for variations in the timing of the onset of RM4 with respect to the beginning of intercalary meristematic growth. Such variations would be reflected in fertile regions positioned along the internode at different distances below the node, but evidence from the fossil record is equivocal, i. The diversity of teratological forms encountered in various species of Equisetum has fascinated plant morphologists for many years and inspired hypotheses for the homologies of equisetalean reproductive morphology reviews in Page, ; Naugolnykh, Taken together, the different teratologies demonstrate tremendous variability in reproductive morphology.

This variability spans the whole range between terminal strobili and internodes lined with sporangiophores, including transitional forms that bridge the morphospace between regular sporangiophores and sporangium-bearing leaves e. Page, These reflect a great deal of plasticity in the location of expression of the regulatory programmes responsible for development of the sporangiophore, as a whole, and of individual sporangia, demonstrating that virtually everything is developmentally possible in the reproductive morphology of Equisetum.

This very broad heterotopic and heterochronic potential cautions against indiscriminate use of individual teratologies as evidence in support of specific interpretations, when assessing competing hypotheses on evolutionary change in equisetacean reproductive morphology.

Nevertheless, some Equisetum teratologies show close similarity to reproductive morphologies documented in the fossil record, corroborating our developmental hypothesis.

Cases in which up to four sporangiophore whorls are borne along the top part of Equisetum internodes e. Boureau, ; Naugolnykh, correspond to the Cruciaetheca -type morphology. Tschudy, ; Page, ; Naugolnykh, , like those of Peltotheca. These Equisetum teratologies are important because they provide parallels between the reproductive morphology of extinct equisetaceans for which the anatomy of development has yet to be documented, and a living species in which the development is well understood.

For this reason, developmental studies of such teratological Equisetum morphologies are needed as critical tests for the hypothesis presented here. Two hypotheses for the homology of the Equisetum strobilus. The traditional hypothesis proposes that the strobilus is a condensed succession of nodes and internodes or a stack of fertile phytomers.

In an alternative hypothesis, the Equisetum strobilus is regarded as a single fertile internode of a terminal phytomer, as interpreted in Paracalamitina striata Naugolnykh, , Paracalamitina striata redrawn from Naugolnykh ; drawing by Megan Bishop. The anatomy and development of the Equisetum strobilus E. A Tip of a developing fertile shoot; the two arrowheads indicate the limit between vegetative phytomers below and the strobilus above.

This limit coincides with a sharp transition between the vegetative phytomers, which exhibit marked alternation of nodes and elongated internodes, and fertile phytomers, in which such an alternation is conspicuously missing. The latter is consistent with the absence of node—internode differentiation in fertile phytomers. Additionally, acropetal maturation of tissues in the strobilus is consistent with development of successive phytomers from an apical meristem and rejects interpretation of the strobilus as a single fertile internode which would grow from a meristem at its base and, thus, exhibit a basipetal maturation pattern.

B Tip of a developing strobilus; the origin of sporangiophores can be traced to vertically adjacent bulges that are visible 8—10 phytomers away from the apical cell. C A sporangiophore primordium is initiated by periclinal divisions of superficial cells throughout the entire thickness of the phytomer, except for the topmost and basalmost layers of the phytomer arrowheads.

This indicates that a sporangiophore whorl develops from the entire thickness of a strobilar phytomer and not just from its upper or lower section i.

D Longitudinal cell patterning in the mature strobilus lacks the node—internode differentiation that is conspicuous in vegetative shoots, another feature consistent with absence of node—internode differentiation in strobilar phytomers.

In our hypothesis, reproductive development in Equisetum involves all three major regulatory modules discussed above plus RM4.

Production of a terminal strobilus is due fundamentally to the combined activity of RM1 transition to reproductive growth turning on RM4 in each phytomer and RM2 apical meristem determinacy. In addition to these two, the anatomy of the strobilus indicates the presence of a third set of developmental controls on the patterning of fertile structures.

This is clearly apparent in the sharp transition marked by a conspicuous difference in anatomy between the strobilus and the vegetative shoot subtending it: whereas the vegetative shoot exhibits an alternation of nodes and elongated internodes, in the strobilus this alternation is conspicuously missing Fig.

Together, these indicate the activity of an additional regulatory module that alters patterning within strobilar phytomers RM3. This module may be responsible for either shutting down internodal elongation or shutting off node—internode differentiation altogether as suggested by the studies of Barratt, and, with that, the specification of an intercalary meristem at the base of the phytomer.

In developing Equisetum strobili, the origin of sporangiophores can be traced to bulges that are visible on the flanks of the strobilus apex approx. The bulges are initiated by periclinal divisions of superficial cells of the phytomer, which add to the volume of tissue beneath this layer Fig.

Importantly, with the conspicuous exception of cells in the topmost and basalmost layers of the phytomer, the superficial cells throughout the entire thickness of the phytomer undergo periclinal divisions to form a sporangiophore Fig. Furthermore, like the developing strobilus, the mature anatomy of the strobilus Fig.

Together, these corroborate the interpretation that, rather than just shutting down internodal elongation, RM3 shuts off node—internode differentiation in the strobilar phytomers. However, the developmental anatomy of the strobilus implies that the question of whether whorls of sporangiophores mark the position of nodes is irrelevant.

If each sporangiophore whorl 1 corresponds to a strobilar phytomer in which there is no node—internode differentiation, and 2 develops from the entire thickness of that phytomer, then expression of the sporangiophore development programme RM4 is independent of node—internode identity.

This is consistent with the potential for production of sporangiophores at various locations for various durations along internodes, proposed in our hypothesis to explain Cruciaetheca and Peltotheca -type reproductive morphologies. Hypothesis for the evolution of reproductive morphology in the Equisetaceae, reflecting evolution of the complexity of reproductive developmental mechanisms by successive addition of non-overlapping developmental modules.

The most basic morphology Cruciaetheca type is the result of the expression of a single reproductive regulatory module RM1 , which controls the transition to reproductive growth by promoting the regulatory pathway responsible for sporangiophore development in the intercalary meristem of internodes. The result is a series of fertile phytomers bearing whorls of sporangiophores along internodes, part of a shoot with indeterminate growth. Expression, against this background, of a second regulatory module that induces determinacy in development RM2 , results in a series of fertile phytomers bearing sporangiophores along the internodes that exhibit an apoxogenetic pattern of determinate growth, as seen in the Peltotheca type.

A third regulatory module RM3 is responsible for the repression of node—internode differentiation within phytomers. If expressed in concert with RM1 and RM2, this produces a terminal strobilus of the Equisetum type that is a stack of phytomers, but not a node—internode sequence; each of these phytomers lacks an intercalary meristem and internodal elongation, and produces a single whorl of sporangiophores that develop from the entire thickness of the phytomer.

In Peltotheca , internodes entirely covered in several whorls of sporangiophores form a terminal fertile zone on specialized reproductive shoots Escapa and Cuneo, Like Equisetum, Peltotheca produced fertile shoots with determinate growth.

This is demonstrated by specimens in which all sporangiophores along the internodes are mature — even those on apical internodes that show an apoxogenetic pattern — indicating that the sequence of fertile phytomers occupied a terminal position on the fertile shoot Fig. However, unlike Equisetum but similar to the structure of Cruciaetheca , the fertile phytomers of Peltotheca exhibit node—internode differentiation — as indicated by the presence of leaf scars on the nodes of the fertile zone — and intercalary growth — as demonstrated by the elongated internodes.

Assessment of the rich equisetacean fossil record in light of the distinctive mode of development of Equisetum suggests a model of growth for Equisetaceae that explains the diversity of reproductive morphologies documented in the group. In this model, the equisetacean shoot grows by the combined action of apical and intercalary meristems. The apical meristem lays down a sequence of phytomers along with the radial patterning of shoot tissues , whereas the intercalary meristem at the base of each phytomer increases the length of that phytomer.

Overlain on these patterns of development, expression of one or several reproductive regulatory modules leads to different reproductive morphologies. All these observations and ideas can be integrated into a hypothesis on the evolution of the complexity of reproductive developmental mechanisms in the Equisetaceae by successive addition of non-overlapping developmental modules Fig.

The most basic of these morphologies, seen in the Cruciaetheca type, is the result of the expression of a single reproductive regulatory module, RM1.

This is the minimum requirement for the transition to reproductive growth and promotes the activity of RM4, the regulatory pathway responsible for sporangiophore development, in the intercalary meristem region of internodes. The result is what we hypothesize as the plesiomorphic condition for equisetacean reproductive structures, consisting of series of fertile phytomers bearing whorls of sporangiophores along internodes, that alternate with series of vegetative phytomers along shoots with indeterminate growth.

Heterochronic variations in the expression of RM4 result in different lengths of the internode portions covered in sporangiophores Fig. The second regulatory module RM2 induces determinacy in the development of reproductive structures. The result is a series of fertile phytomers bearing sporangiophores along the internodes that exhibit apically the apoxogenetic morphological pattern characteristic of determinate growth, as seen in the Peltotheca type. The third regulatory module RM3 is responsible for the repression of node—internode differentiation within phytomers.

In combination with the activity of RM1 and RM2, this produces a terminal strobilus which is a stack of phytomers, but not a node—internode sequence — as seen in the Equisetum type. Each of these phytomers lacks an intercalary meristem and internodal elongation, and produces a single whorl of sporangiophores that develop from the entire thickness of the phytomer.

Our hypothesis uses modularity of regulatory programs to explain the different types of reproductive structures produced across the Equisetaceae by the evolution of development.

If this hypothesis is a valid explanation for the range of morphologies reviewed here, then the very existence of these morphologies in tangible organisms points to two basic features of the developmental system of this group of plants. On the one hand, because they can act in concert and yet their concerted expression is not required for the production of each type of reproductive structure, RM1, RM2, and RM3 are uncoupled Fig.

On the other hand, the proposed interactions of regulatory modules required for the production of different morphologies are consistent with hierarchical patterns. At the same time, RM2 and RM3 seem to be independent, e.

Peltotheca vs. Equisetum morphologies. Nevertheless, the range of morphologies observed, as reflections of the realized morphospace of the potential patterns of co-expression of these modules, indicates that RM3 is only expressed downstream of RM2. Irrespective of its implications for the diversity of equisetacean reproductive morphologies, growth of Equisetum shoots from two types of meristems apical and intercalary is a well-established fact.

Whereas growth by internode elongation is a feature of all vegetative shoots articulated into nodes and internodes Esau, , in most plants internode elongation arises from diffuse cell elongation throughout most of the internode, in the immediate vicinity of the shoot apex, and not from well circumscribed intercalary meristems.

Such intercalary meristematic areas, located at the base of internodes and characterized by prolonged activity, have evolved independently in the sphenopsid clade Equisetales and their close relatives, the Sphenophyllales; Esau, ; Good, ; Schabilion, and in some monocotyledons, particularly grasses Lehmann, ; Prat, These two instances of intercalary growth share a morphological correlate — long internodes — and an anatomical one — rhexigenous protoxylem lacunae.

Termed carinal canals in Equisetum , the rhexigenous lacunae are longitudinal spaces generated by mechanical failure, under excessive tension due to elongation, of the earliest tracheary elements to mature. Whereas internode length is relative and not readily comparable across plants of different sizes and lineages, rhexigenous protoxylem lacunae are comparatively rare among tracheophytes and could serve as a potential anatomical fingerprint for internode elongation from well-circumscribed intercalary meristems.

Because of their mode of formation, the sides of these cavities are lined with the remains of secondary wall thickenings of the torn tracheary elements, which also help in their recognition. In fact, the presence of rhexigenous protoxylem lacunae in several Middle Devonian plants Ibyka and other cladoxylaleans was one of the features that led Skog and Banks to propose that they represented a plexus of taxa at the base of the sphenopsid lineage. While Scheckler has asked for caution in the use of this anatomical feature to recognize sphenopsids deep in the fossil record, the improvements in our knowledge of the Devonian fossil record during the intervening time period could allow for a modern re-evaluation of these views.

In considering the deepest origins of growth from intercalary meristems, it is interesting to note that growth from basally located meristems characterizes the sporophyte axes of mosses and hornworts. Whereas for hornworts it is unclear whether the sporophyte undergoes any organized apical growth, in mosses the sporophyte grows in a first phase from an apical cell.

Following this early phase, intercalary growth leading to elongation of the seta is initiated from sub-apical tissues as the sporophyte apex transitions to a reproductive growth programme, losing meristematic competence and developing into a sporangium Tomescu et al.

In light of these features of bryophyte development, and considering the close relationships between bryophytes and the earliest polysporangiophytes—tracheophytes, Niklas has proposed a combination of growth from apical and intercalary meristems as a hypothetical developmental system for the branched sporophytes of the earliest polysporangiophytes. In his model, elongation in the earliest branched sporophytes arose principally from intercalary meristems located at the base of each of the sporophyte branches, which terminated in sporangia.

A direct implication of the hypothesis presented here is that sporangiophore development is fundamentally independent of node—internode identity: sporangiophores are produced either on phytomers that lack node—internode differentiation in the Equisetum strobilus or in various positions along internodes.

In turn, this is relevant to discussions of sporangiophore homology. These discussions have a rich history and have been complicated by the diversity of morphologies of fertile appendages documented among the Equisetales and the Sphenophyllales, as well as by the lack of resolution in the phylogeny of sphenopsids as a group.

Without attempting to review or even list all the hypotheses that have been proposed, it will suffice to say that discussions of the Equisetum sporangiophore reviewed in some detail by Page, have proposed everything from total or partial foliar homologies to origin as a sui generis structure. If sporangiophore development is independent of node—internode identity, this is inconsistent with leaf homology — leaf development is associated with nodal identity in vegetative phytomers that express node—internode differentiation.

Thus, when considered in the narrow context provided by the canalized organography of extant Equisetum , the sporangiophore appears to represent a sui generis structure, as proposed by Barratt Conversely, when considered within a broader evolutionary context and from the perspective of an upward outlook at plant evolution Bower, ; Stewart, , these observations imply that sporangiophores evolved independently of leaves.

It is possible that the equisetacean sporangiophore represents the expression of a regulatory module that evolved for the production, in basal euphyllophytes trimerophytes , of structures that pre-date the evolution of node—internode differentiation in the sphenopsid clade and the evolution of leaves.

This would be the regulatory module responsible for the development of lateral determinate fertile branches on the otherwise undifferentiated axes of trimerophytes.

These ideas are not inconsistent with the view of the sporangiophore as originating by sequential modification of fertile lateral branches in early tracheophytes whose sporophytes consisted of undifferentiated branching axes, a perspective taken in one of the most frequently conjured applications of the telome theory Zimmermann, ; Stewart, , Sitting at the tip of one of the deepest branches of vascular plant phylogeny the sphenopsids , Equisetum has a highly distinctive morphology.

Virtually every aspect of its morphology, be it vegetative or reproductive, has generated discussions and hypotheses, many of which have relied heavily upon data from the fossil record. Here we have proposed a hypothesis that addresses one of these aspects: the morphology of fertile zones and strobili. Furthermore, we have focused only on a sub-set of sphenopsid reproductive morphologies for which the distinctive aspects of Equisetum development are directly relevant; these structures consist of successions of sporangiophore whorls and characterize members of the Equisetaceae.

The sphenopsids have produced at least two other major types of fertile structures usually strobili not discussed here. One of these, characteristic of many Calamitaceae, consists of regularly alternating fertile sporangiophore whorls and vegetative bract whorls Good, , whereas the other, characteristic of the Sphenophyllales Riggs and Rothwell, , features sporangium-bearing units with foliar morphology. Hypotheses of homology for all these different types of reproductive structures will be discussed in a forthcoming paper I.

Escapa et al. Nevertheless, it is worth pointing out that while calamitacean and sphenophyllalean reproductive structures are usually regarded as consisting of strobili determinate growth , notes buried in the older literature Hoskins and Cross, and new fossils from the Early Permian of Argentina N.

Cuneo et al. Data S1: a survey of the genetic underpinnings of meristem functioning and the transition to reproductive growth: implications for the capacity of the intercalary meristem to execute reproductive developmental programmes.

Data S2: evaluation of the terminal fertile phytomer hypothesis for the origin of the Equisetum strobilus. We thank Dennis K.

Richard Bateman, an anonymous reviewer, and the handling editor, Silvia Pressel, are thanked for comments and suggestions that improved the manuscript. Acropetal maturation : pattern of tissue maturation along a structure or organ, in which the basal region is the earliest to mature and tissue maturation progresses toward the tip distal region of the structure or organ.

Antonym: basipetal. Acroscopic : refers to position along an axial plant organ relative to a reference location; specifically, positioning closer to the apex, as compared with the reference location. Antonym: basiscopic. Apoxogenetic development n. The opposite pattern is termed epidogenesis. Archaeocalamitales adj. Archaeocalamitales grew in the paleotropics primarily during the Mississippian and Pennsylvanian Periods, and have frequently been hypothesized to have given rise to the Calamitaceae.

Basipetal maturation : pattern of tissue maturation along a structure or organ, in which the apical region is the earliest to mature and tissue maturation progresses toward the base proximal region of the structure or organ.

Antonym: acropetal. Basiscopic : refers to position along an axial plant organ relative to a reference location; specifically, positioning closer to the base, as compared with the reference location. Antonym: acroscopic. Calamitaceae adj. Calamitales grew in the paleotropics primarily during the Pennsylvanian and Permian Periods, and have been hypothesized by some to have given rise to the Equisetaceae by a reduction in plant size, loss of woody tissues and loss of bract whorls within the cones.

Derivative of an apical cell apical cell derivative : cell produced directly by the division of an apical cell. Determinate growth n. Antonym: indeterminate growth. Ectopic expression of a gene : expression of a gene in a location or at a point in developmental time where it is not normally expressed in the regular developmental pattern of an organism.

Equisetaceae adj. The Equisetaceae include living species of Equisetum , as well extinct species of Equisetum and similar plants that extend back through time to the Triassic Period. Equisetales adj. Equisetales are characterized by whorled, usually single-veined leaves that may be basally fused forming a sheath, and fertile regions consisting of one or more whorls of sporangium-bearing appendages that may alternate with foliar appendages leaves or bracts.

Euphyllophytes : informal name for Sub-division Euphyllophytina Kenrick and Crane, , a clade that is the sister group of lycophytes Sub-division Lycophytina. Eupyllophytes include a basal grade of extinct plants with simple organography consisting of undifferentiated branching axes referred to here as trimerophytes , several other extinct lineages, as well as all living non-lycophyte tracheophytes.

Fertile zone : sequence of successive fertile phytomers along a shoot. Fertile zones usually alternate with vegetative sterile zones along shoots. Indeterminate growth : growth pattern in which growth continues indefinitely throughout the life span of the organism.

Antonym: determinate growth. Intercalary meristem : the meristematic region at the base of each internode, found in some plant groups, such as the sphenopsids and grasses Poaceae. Merophyte : a group of clonally related cells resulting from sequential cell divisions that originate in a single derivative of the apical cell of a meristem.

Periclinal division : orientation of the plane of cell division parallel with the outer surface of an organ. Phytomer : modular unit of the shoot consisting of one node with the attached leaf and the subtending internode. Polysporangiophytes : the clade of plants that share the branched sporophyte as a synapomorphy Super-division Polysporangiomorpha of Kenrick and Crane, Primordial ring : set of sectorially contiguous merophytes that form a phytomer Golub and Wetmore, a.

Synonym: segment ring. Promeristem : classic anatomy term for the stem cell niche of an apical meristem. Divisions of promeristem cells produce derivatives which go on to differentiate into primary meristems procambium, ground meristem, protoderm ; select cells of procambial lineage residual procambium , sometimes in combination with select cells in the ground meristem lineage i.

Regulatory module : system of developmental regulators transcription factors, etc. Rhexigenous protoxylem lacuna : elongated, irregularly tubular cavity that occupies the position of a protoxylem strand and is generated by the failure of protoxylem tracheary elements due to tensional stress; it can be recognized by its position and by the presence of secondary wall thickening remnants annular, helical attached to the walls of the lacuna. Sectorially contiguous merophytes : merophytes that are adjacent to each other laterally, i.

Segment ring : set of sectorially contiguous merophytes that form a phytomer Reess, Synonym: primordial ring. Sphenophyllales adj. Sphenophyllales were small shrubs or vines that had worldwide distribution, primarily from the Mississippian through the Triassic Periods. Sphenopsida adj. The Sphenopsida extend from the Late Devonian through the recent and include the Archaeocalamitales, Sphenophyllales and Equisetales, along with several other extinct lineages; of these, only about 15 species of the genus Equisetum are alive today.

Sporangiophore : sporangium-bearing appendage of the sphenopsids. The homology of sporangiophores in different sphenopsid lineages is disputed. Strobilus pl. Taxis : mode or geometry of arrangement, e. Telome theory : system of hypotheses proposed by Zimmermann to explain the evolution of complex plant sporophyte body plans and organs from plants with simple body plans i. At the core of the telome theory are the telome truss, a basic branching unit of the archetypal early land plant body plan, and a set of hypothetical basic processes of morphological evolution; under the telome theory, combinations of several of these processes in different sequences and proportions were hypothesized to have generated different plant body plans and organs.

See Stewart for a comprehensive summary. Teratological form n. Trimerophytes : basal grade of the euphyllophytes from which sphenopsids and other major clades of living euphyllophytes are derived. Includes extinct plants with simple organography consisting of undifferentiated branching axes bearing sporangia at the tips of branches in specialized fertile regions.

Sphenopsids, seed plants, several groups of ferns and the psilopsids i. Psilotum and Tmesipteris all are derived from trimerophyte-grade euphyllophytes. Upward outlook in morphological evolution : a perspective on evolution that emphasizes explanations of complex structures of derived groups as modifications of simpler structures of more basal less derived groups.

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The origin and early diversification of land plants. Washington : Smithsonian Institution Press. Provided by the Springer Nature SharedIt content-sharing initiative. Nature By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Advanced search. Skip to main content Thank you for visiting nature. Abstract AN attempt was made some time ago 1 to relate spiral growth in sporangiophores of Phycomyces to the physical properties of the wall, and the successful semi-quantitative test of the relation proposed against the data of Castle 2 , as well as the more recent extension to the case of spiral grain in conifers 3 , makes it reasonable to assume that, oversimplified though the relation undoubtedly is, it does express spiral growth in terms of the appropriate parameters.

Access through your institution. Buy or subscribe. Rent or Buy article Get time limited or full article access on ReadCube. References 1 Preston, R. Article Google Scholar 3 Preston, R. Author information Affiliations University of Leeds R.

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