Transcribed, by permission, from Tuatara (1984) Vol. 27 (1): 26-48
(The following text should not be treated as an authoritative citation substitute for the original)

Principia Botanica:
Croizat's Contribution to Botany

By Michael heads
E. L. Hellaby Indigenous Grasslands Research Fellow, Botany Department, University of Otago, Dunedin.

INTERPRETATION OF LEAF AND STIPULE

The question of "What is a leaf?" is certainly one of the great problems of botany. As mentioned above, the current state of despair is well exemplified by the comment:

"Although no satisfactory definition of a leaf is thus possible I shall assume that we all know what we shall be talking about (Gregory 1956).

It is clear that the definitional approach, using morphological, especially anatomical, criteria has failed to supply us with efficient concepts involving the true nature of the leaf. If we agree that the assumption "we all know what we shall be talking about" is hopeful but unfounded, we must also agree that it is necessary to do something.

It is Croizat's connection that descriptive anatomical criteria cannot supply an answer to the question "what is a leaf", and are, in fact, an inappropriate basis for evolutionary studies. In support is the comment by Schmid (1972: 442) that it is Croizat who provides:

"the most pertinent and clear statement I have encountered regarding the problem of the validity of vascular conservatism".

Croizat asserts that the most useful analysis of "leaf" would be in terms not of unanalyzed morphological homologies, but rather of morphogenetic processes. With respect to Croizat's attitude towards interpretation of morphogeny vs. technical description of morphology, it is interesting to note Einstein's view that"

"It is really strange that human beings are normally deaf to the strongest arguments while they are always inclined to overestimate measuring accuracies." (from a letter, quoted in Feyerbrand 1978:58).

Croizat's analysis of leaf form and morphogeny (Princ. Caps. 9. 10) includes consideration of many structures which were traditionally regarded (if at all) as unusual, insignificant, and, ultimately, accidental. Arber (1934: 312) has summed up this unproductive attitude well:

"Another dictum of formal morphology is that the power of producing lateral shoots is confined to axes. When a leaf does, in fact, bear a shoot-bud, this shoot is described as 'adventitious', which means, literally, 'accidental'. This is a typical example of the tyranny exercised by words over thought; just because they have themselves labeled these buds 'accidental', botanists feel justified in dismissing them as of no morphological significance."

Just as 'inexplicable", thus "accidental", patterns of dispersal (such as trans-tropical-Pacific) are analyzed in his Panbiogeography, Croizat does not fail to consider the nature of "inexplicable" and "accidental" morphological facts in the Principia Botanica. The morphology of plants with structure problematic in the light of traditional interpretations has often led students, for example Jong and Burrt (1975) working on Gesneriaceae, to reject the "traditional morphological categories" as adequate guides for efficient analysis. In Croizat's work these "difficult" plants are not ignored, on the contrary, as with incongruent area/taxa cladograms in biogeography, they are shown to be in themselves useful guidelines in analysis.

The problem of the modern leaf was eliminated in the past, when "leaf" was proposed to be itself an irreducible category, an elements, and essentially simple structure. The sociological and philosophical reasons for this proposition are complex suffice to say that Croizat begins with no such assumption. Indeed, but means of a thorough analysis of leaf form, Croizat demonstrates that, in fact, the modern angiosperm leaf is an essentially compound body (c.f. his analysis of Wallacean areas of endemism as compound entities). We are all aware of the complexity of leaf organogenesis, attained by a variety of meristems (Jeune 1981) and Croizat's conclusion may initially seem relatively innocuous. Nevertheless, it has important consequences.

Croizat approaches the morphogeny of the modern foliage leaf, stipules, cataphylls, buttress, buds and certain types of thorn (Cactaceae, Euphorbia, Fouquieria) as a general problem As with the leaf/shoot question, rather than simply providing homologies between unanalyzed organs it would seem more productive to inquire about the limits between the organs, thus identifying processes of divergence. Croizat's analysis concludes in fundamental agreement with Tyler (1897) that the "lower foliar organs" (stipule, cataphyll etc.) are neither reduced leaves fro additions subsequent to the development of the modern leaf, but are the "primitive foliar organs". The modern leaf represents a development of, and upon, this primitive leaf. The lateral portions of the primitive leaf, when separated, form the stipules, petiole wings etc, of the modern leaf. The sheathing petiole is a product of the development of lateral and central basal parts of the primitive leaf it is essentially distinct from the true petiole of the modern leaf. The leaf buttress represents the immediate continuation of the primitive leaf into the cortex.

These ideas are supported by studies of leaf organogenesis. For example, Cross (1938) has shown that in Viburnum cataphylls are not leaf homologues - cataphyll and leaf ontogeny diverges dramatically at the 80ì stage and leaf growth progresses by means of a distinctive ventral meristem which cataphylls lack. Bruck and Kaplan (1980) have shown that scale-leaves are not homologous with foliage leaves in Muehlenbeckia. In Morus, Cross (1937) found that the stipule development is unlike that of foliage leaves, but like that of cataphylls. Again the difference is fundamental, the foliage leaves being the result of the activity of a ventral meristem totally absent in the cataphylls and stipules. Thus the primitive scaliform leaf, represented by stipules and cataphylls, and the modern foliage leaf represent essentially distinct variants, at a very low level, of a single foliar type the scale of Croizat. In the case of the foliage leaf, this scale or undeveloped phyllomes has inherited a specialized "dab of meristem" which, once activated, leads to leaf organogenesis.

Macdonald (1981) stated recently that "The phylogeny of the stipule remains unresolved", indicating that little, if any, conceptual progress has been made since Sinnott and Bailey (1914) made similar comments sixty seven years earlier. Macdonald also noted that:

"to conclude that the stipules of Comptonia (Myricaceae) are lobes or outgrowths of the leaf base, while true in an empirical sense, contributes little to our understanding of their phylogeny".

However, recent work by Jeune (1981) concludes that, in the light of current knowledge of leaf ontogeny, Croizat's analysis is of special significance in adequately resolving the morphogenetic and phylogenetic nature of the stipule.

Macdonald concluded his perceptive paper by suggesting homology between the stipule and prophyll (he unfortunately overlooked Croizat's analysis of "prophyll", and his identification of it with "stipular sector" in Princ. 718).

Croizat's synthesis of the morphology of the modern foliage begins with verticals or whorls of primitive "leaves" (to be regarded more as phyllomes or primordial). As Howard's (1974: 160) has noted:

"The evolutionary progress from alternative and spirally arranged leaves to opposite or whorled leaves has become established as a dictum inmost botanical publications…without any real evidence."

Howard (1974: 163) concludes that "the primitive leaf was probably borne in whorls or even vertically grouped clusters…"

These verticils, each of n "leaves" became suppressed, recombined and dirempted, or pulled apart, along the shoot into local sectors of 1 foliage leave + 2 stipules (undeveloped leaves). This process of reduction naturally takes place within the limits imposed by laws of symmetry, for example those outline above.

What is the explanation for the development of the single leaf as the keystone of reduction and diremption of the ancestral verticil? The stipule/leaf distinction is not adequately defined by the presence of an axillary bud (e.g. Chaenomeles japonica stipules may have axillary buds), but histologically the distinction cab be made on the basis of the ventral foliar meristem. The crucial question thus becomes "What is the phylogenetic and morphogenetic nature of this important meristem? What is its origin?" The only real answer given it this question is that of Croizat. The meristem is the product of ancient fusion of axes and primitive "leaves" leading to the modern leaf. The meristem itself represents the incorporation into the primitive "leaf" of the primordium of the ancient axis.

Fundamental to Croizat's analysis is the nature of the axillary buds observed in modern plants. Although some plants may have only one bud per axil, in principle there may be a series of axillary primordial lined up between the petiole and the axis. Today these are responsible for shoot making of various kinds (floral and vegetative) including the fusion of epiphyllous inflorescences and leaves. In the history of the leaf, one element of these primordia has been competent in fusing an axis with the ancient "leaf" leading to the meristem which characterizes the "modern" leaf. The relationship between the primitive scaliform "leaf" and the axis which it subtends and later fuses with is essentially hypocladial, in the sense of Kursner (1954). Hypocladial relationships between rameal and foliar organs are well known in many extent plants, for example, see Fig. 2. The axis which has become reduced and incorporated into the primitive scaliform leaf, leading to the development of the modern, hypocladial leaf could naturally be expected to have left some indications as to its nature in other words the hypocladial transfusion may well not have been completed in every instance.

Dickinson (1978) in a timely and thorough review of the phenomenon of epiphylly has urged the study of the laws of growth which have determined the development of epiphyllous inflorescences. He has also noted the possibility of epiphylly having been of "fundamental importance…to the origins of the angiosperm leaf itself" and suggests that this concept provides significant avenues for future research. The idea of the inherent sexuality of angiosperm leaves can be traced back to at least C. de Candolle (1890) but its phylogenetic and morphogenetic meaning is first explained by Croizat, in terms of the hypocladial nature and history of the modern angiosperm leaf. Epiphylly is, of course, a worry for traditional morphology which regards the leaf as an irreducible category - the consequent problem lies in explaining how and why an inflorescence managed to "get up" into a leaf. However, with Croizat's analysis of the leaf as essentially complex, the "problem" of epiphylly vanishes, it simply means that the axis involved with the primitive scaliform foliage was, intact, or potentially, floriferous. Thus the hypoclaidal relationship between (potentially) floriferous axes and the primitive scaliform foliate is an important law of growth for the modern angiosperm leaf. In a study of epiphylly in Helwingia japonica Dickinson and Sattler (1975) state:

"The main conclusion is that such conditions (epiphylly) suggests that "laws of growth"…probably are as important, or more so, than lows of natural selection in determining plant form."

The same authors (1974: 8) in a study of the epiphyllous inflorescence of the saxifagaceaous Phyllonoma intergerrima state that:

"our observations cannot be incorporated into the rigidly formulated classical theory of the shoot without distortion of the observations themselves, or of our understanding of them." They also note that (1974: 9) "The value of atypical situations like epiphylly is that they point out aspects of the real morphogenetic potential of plants in nature, corresponding to these "Laws of Growth", that we often overlook."

This potential may lie at no great depth, for example Stebbins (1965) describes the single "gene" controlling the production of epiphyllous inflorescences in pants of Hordeum trifurcatum (see Princ. 1533).

A question of crucial significance for an understanding of the leaf is posted by the nature of glands. Most recent work concentrates on their present day ecological significance and tens to ignore their morphogeny. But as Schnell (1970: 433) has said, regarding etra-floral glands:

"Leur signification…parait a rechercher dans la morphologie et dans la phylogénie de la feuille plutôt que dans une utilité pour lat plante…"¹ [¹ "An understanding of their significance would seem to require research into the morphology and phylogeny of the leaf, rather than into any usefulness for the plant."]

Since Schwend's important 1907 paper, botanists have interpreted the morphology of plant glands as a result of the reduction of the hemming-in of pre-existent structures (e.g. Schnell 1969: 153-154 for discussion).

Glands, often secretory, are well known from the vegetative parts of many plants, as well as from the flowers. Particularly common are glands found at, or near, the petiole-lamina junction. Persistent meristems fo various kinds have also been reported from this locality (e.g. Jong 1973 on Streptocarpus). Glandular teeth are well known on stipules (e.g. the rubiaceous Coprosma) and leaves (e.g. Chloranthaceae). The interpretation supported by Schnell (1969) with respect to domatia found in the axils of foliar venation (again Coprosma provides striking examples). He suggests that they indicate (une croissance avortée". With respect to early theories on the origin of ant domatia by means of natural selection, Philipson (1964) cites Bailey (e.g. 1922, 1923) favourably, to the effect that:

"insects are not concerned with the origin of development of these structures".

Thus there are many different structures present in the morphology of the modern foliage which represent remnants of hemmed-in growth, and which must all be accounted for in any synthesis of leaf morphogeny. Howard (1974), in an important contribution, discusses aspects of nodal and petiolar form and concludes that these provide further support for Croizat's concept of the leaf and its essentially compound nature.