Allertonia 17, 2018, pp. 1–52 Wood Anatomy of Atherospermataceae and Allies: Strategies of Wood Evolution in Basal Angiosperms Sherwin Carlquist1 Santa Barbara Botanic Garden, 1212 Mission Canyon Road, Santa Barbara, CA 93105 ABSTRACT Atherospermataceae and Gomortegaceae, a clade of Laurales, occur in moist, swampy, riverine, and cloud forest habitats. They have apparently departed little in habitat preference from their ancestors, in the cloud forests of Gondwana, whereas Siparunaceae, a clade not far distant from (or sister to) the Atherospermataceae clade have radiated into more diverse habitats in South and Central America. Key features of wood anatomy are related to habitat occupancy shifts rather than to systematics. Narrow thin-walled vessels with scalariform perforation plates denote slow flow rates under low tension. Scalariform perforation plates may sieve out bubbles, as Zimmermann hypothesized, or they may compartmentalize the vessel for increased safety. Longer vessel elements lower flow resistance. All species of Atherospermataceae and Gomortegaceae have perforation plate dimorphism; narrower perforations in latewood plates promote conductive safety, whereas non-resistive plates (in most of a growth ring) permit more flow. There is little deviation among Atherospermataceae in perforation plates and other features; the family has shifted very little away from cool moist forests since the breakup of Gondwana. Wider vessels in the trees of Dryadodaphne differ from the narrow vessels of the relatively small trees of Daphnandra, etc. There is diversification in tracheary elements. Tracheids, the basic type in some species of Atherospermataceae, offer conductive safety, but have been supplanted in other species by septate fiber-tracheids, which combine mechanical strength with photosynthate storage and serve as a cell type substituting for axial parenchyma, which is almost completely absent in the family. Where tracheids and septate fiber-tracheids co-occur, the fiber-tracheids tend to group near vessels, suggesting a mechanism for releasing sugars into vessels. Multiseriate rays consist mostly of procumbent ray cells suggesting radial flow of photosynthates, but lack sheath cells. Upright ray cells in wings of those rays, and throughout uniseriate rays, have scalariform vessel-ray pitting that suggests active transfer of sugar into vessels to maintain water columns. Ray-to-ray cell pits on horizontal and vertical radial walls are sparse by comparison, but tangential walls of ray cells bear numerous pits which are bordered. Oil cells occur idioblastically in upright ray cells of some species, and resin-like deposits were seen idioblastically in rays of all species. Microcrystals of unknown composition occur in several species. Wood of Gomortega differs from that of Atherospermataceae in abundance of axial parenchyma, potentially better than fiber-tracheids because of denser pitting. Siparunaceae are a model of how an angiosperm group departs from mesic habitats like cloud forests into areas where temperature and humidity fluctuate more markedly. In Siparuna, perforations plates are scalariform to simple or with a few thin bars (lowered resistance accommodates peak flow in warm but wet habitats), with conversion of wood background to axial parenchyma plus libriform fibers. This division of labor balances better mechanical support against lower conductive resistance. Vessel grouping in Siparunaceae provides redundancy and pathway maintenance to preserve conduction during peak transpiration. KEY WORDS AND PHRASES: Atherospermataceae, Gomortegaceae, Siparunaceae, ecological wood anatomy, flow in rays, septate fiber-tracheids, perforation plate dimorphism, pitting in rays, tracheids, vessel grouping INTRODUCTION Hemisphere distribution of Gondwanic origin. Recent evidence has shown that Atherosper- One genus, Laurelia Juss., is disjunct between mataceae (seven genera, 15 or more species) Chile and New Zealand. Atherospermataceae form a clade with Gomortegaceae (monotypic) occur in moist forest with such long-term as- in Laurales (Renner, 1999). This clade is of spe- sociates as Nothofagus Blume, Podocarpus cial interest because it represents a Southern L’Hérit. ex Pers., and Weinmannia L. Some of 1e-mail: [email protected] 2 ALLERTONIA Volume 17 these localities, although moist, may experience eny of the family. The wood of Atherospermata- frost to various degrees (Tasmania, southeastern ceae does show a series of variations on a basic Australia, southern Chile). There are fossil re- pattern. Some of those variations are smaller, cords of Atherospermataceae from Antarctica, some greater: atherosperm wood is not uniform, Patagonia, and even South Africa (see Renner but is not diversified in ways that one sees in et al., 2000). Thus, Atherospermataceae can some other families of considerable age (e.g., be said to have become geographically more Dilleniaceae). A rather detailed description of restricted as parts of the Gondwana fragments wood of the family as a whole can be devised, became colder, but expansion into the uplands and is offered below. The main concern of this of some subtropical locations (New Caledonia, essay, however, is the causation of differences New Guinea) has also occurred. Can Atheros- in wood anatomy among the taxa. Are climatic permataceae have reached some of their present differences matched with divergences in wood localities by long distance dispersal? Renner et anatomy in an arboreal group with mesic re- al. (2000) entertained this possibility, although quirements? What anatomical range is to be ex- Schodde (1969) thought otherwise. Atheros- pected within a plesiomorphy-rich (“primitive”) permataceae have bristly achenes that do travel group of woods? Do primitive wood features by wind well within continental areas, and may limit the ecological diversification of a clade, have permitted some travel between separating or do radiations of some clades forestall the continental fragments. The habitats of the spe- radiation of others? How do clades with meso- cies, in riverine, marshy or gully habitats, are morphic woods “escape” (in terms of change in disjunct like those of Salix, which also has hairy anatomical features) into apomorphies suited to (comose) seeds. The achenes of Atherosper- climates with greater ranges of temperature, soil mataceae, however, may not be able to survive moisture, and humidity? Can some accommoda- long aerial transport or immersion in seawater tions to seasonality be achieved by ontogenetic (Schodde, 1969). changes (e.g., growth rings)? Origin of Atherospermataceae as a family The summary of Metcalfe (1987) for wood may date from as little as 85 MYA (fossil evi- anatomy of Monimiaceae includes Atherosper- dence from Poole and Francis, 1999) to as much mataceae and Siparunaceae. It is based largely as 140 MYA (fossil pollen, which is distinc- on the work of Garratt (1934), Patel (1973), tively disulcate: Erdtman, 1952). Interestingly, Meylan and Butterfield (1978), and Foreman if one hypothesizes no dispersal across oceanic (1984). The work of Stern (1955) and Stern and distances, one must assign a minimal age of Greene (1958) are sources for data on wood of 220–244 MYA (Renner et al., 2000)—an exces- Gomortegaceae. The present account attempts sively ancient period of time, judging by floristic to add new information in the following ways: evidence. Fringing archipelagos and stepping- 1. All of the genera of Atherospermataceae stone islands (e.g., portions of the continent and Gomortegaceae have dimorphic (or Zealandia, now mostly underwater) are omitted sometimes possibly polymorphic) perforation as possibilities in that scenario. The occurrences plates. The adaptive significance of perfora- of such ancient genera as Lactoris Philippi and tion plates with axially wide perforations in Drimys J. R. Forst. & G. Forst. on the Juan Fer- most of a growth ring as compared to axi- nandez Islands shows us that some “primitive” ally narrow perforation plates in latewood is groups have crossed seawater to oceanic islands documented and related to wood ecology and of intermediate distance from continental sites physiology. of origin. The present study does not propose to com- 2. The occurrence of axial elements of the pare wood anatomy to systematics in detail, woods—septate fiber-tracheids, tracheids, because wood is only one element in the phylog- and axial parenchyma strands, is studied here 2018 CARLQUIST: WOOD ANATOMY OF ATHEROSPERMATACEAE 3 because the relative proportions of these el- tomical features are related to entrance by ements in woods of Atherospermataceae, some monimioid genera—as well as by other Gomortegaceae, and Siparunaceae prove to clades of angiosperms—into more stressful differ among the species studied. The evolu- habitats than those occupied by the constantly tionary significance of shifts at genus and spe- cool and moist habitats that characterize most cies levels is examined. Atherospermataceae and Gomortegaceae. 3. In angiosperm woods at large, vessels are mostly solitary in woods of mesic places. If MATERIALS AND METHODS tracheids are the imperforate tracheary ele- The contents of Atherospermataceae at pre- ment type, vessels do not group appreciably, sent appear to be: Atherosperma Lab. (one spe- even if a species occurs in a xeric habitat cies, Tasmania to Queensland); Daphnandra (Carlquist, 1984). Atherospermataceae are a Benth. (six species, New South Wales); Dory- group that represents degrees of this phenom- phora Endl. (two species,