Int. J. Plant Sci. 164(6):917–932. 2003. ᭧ 2003 by The University of Chicago. All rights reserved. 1058-5893/2003/16406-0010$15.00 BIOGEOGRAPHY OF DISCONTINUOUSLY DISTRIBUTED HYDROPHYTES: A MOLECULAR APPRAISAL OF INTERCONTINENTAL DISJUNCTIONS Donald H. Les,1,* Daniel J. Crawford,†,‡ Rebecca T. Kimball,§ Michael L. Moody,* and Elias Landoltk *Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, Connecticut 06269-3043, U.S.A; †Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence, Kansas 66045, U.S.A; ‡Natural History Museum and Biodiversity Research Center, Lawrence, Kansas 66045, U.S.A.; §University of Florida, Department of Zoology, Gainesville, Florida 32611, U.S.A; and kGeobotanisches Institut ETH, Zu¨richbergstrasse 38, CH-8044, Zu¨rich, Switzerland The extraordinarily wide distributional ranges of aquatic flowering plants have long stimulated phytogeo- graphical discussion. Although aquatic plants occur rarely among the angiosperms, they represent a dispro- portionately large number of taxa with broad distributions including various intercontinental disjunctions that are manifest even at the species level. Throughout the nineteenth and early twentieth centuries, long-range dispersal by waterfowl was the prevailing explanation for widespread aquatic plant distributions. This ex- planation gradually fell into disfavor as biologists raised doubts as to the ability of waterfowl to transport propagules across the extensive transoceanic distances between the continents on which an assortment of aquatic taxa now reside. During the twentieth century, the development of biogeographical displacement theory, i.e., “continental drift,” steadily began to supplant dispersal as the preferred explanation for discontinuous angiosperm distributions. Our study assesses the dispersal/displacement hypotheses from a temporal standpoint using molecular estimates of divergence time for a diverse sample of phylogenetically related aquatic taxa that exhibit discontinuous intercontinental distributions. With few exceptions, we found divergence times that are far too recent to implicate continental drift as a major determinant of discontinuous distributions in aquatic plants. We suggest that long-distance dispersal by birds should continue to be regarded as a viable explanation for widely disjunct aquatic plant distributions, although such dispersal is likely to have involved a combination of overland as well as transoceanic migratory routes. Keywords: biogeography, hydrophyte, aquatic plant, intercontinental disjunction, dispersal. With respect to plants, it has long been known what enormous ranges many fresh- water and even marsh-species have, both over continents and to the most remote oceanic islands. (Charles Darwin [1859], On the Origin of Species) Introduction agules typically resides in the mud of aquatic habitats from which they are easily dislodged and transported by birds (Dar- As early as the mid-nineteenth century, de Candolle (1855) win 1859). observed that the geographical distributions of aquatic plants Schenck (1886) also observed that similar aquatic plant spe- generally are quite widespread, especially for a group com- cies occurred frequently in disparate geographical areas that prising relatively so few species. De Candolle explained this in contrast showed quite distinctive terrestrial floras. Although phenomenon by suggesting that different occurrences of a spe- he credited this pattern to aquatic habitats having greater uni- cies in remote geographical areas might represent incidences formity in different geographical localities than terrestrial hab- of multiple origins. He also attributed aquatic plants with hav- itats, he also believed that widespread aquatic plant distri- ing poor dispersal mechanisms that precluded their transport butions must be a consequence of bird dispersal (Schenck by most animals. Darwin (1859) was impressed that a few 1886). Ho¨ ch (1893) similarly attributed extensive aquatic aquatic members of otherwise large terrestrial plant genera had plant distributions to bird dispersal, reasoning that their pe- acquired far wider distributional ranges; however, unlike de rennial habit was ideally suited for this dispersal method and Candolle, he ascribed this result to their “favourable means that the reduced flowers of many aquatic species indicated a of dispersal.” Specifically, Darwin related the extensive distri- butions of water plants almost exclusively to dispersal by water relatively long existence, thus enhancing opportunities for far- birds. He demonstrated that a large number of viable prop- reaching dispersal. Twentieth-century aquatic plant specialists such as Arber (1920), Sculthorpe (1967), and Hutchinson (1975) all impli- 1 E-mail [email protected]. cated birds as prominent dispersal agents of aquatic plants. Manuscript received November 2002; revised manuscript received July 2003. Arber (1920) suggested that birds were capable of transporting 917 918 INTERNATIONAL JOURNAL OF PLANT SCIENCES aquatic plant propagules for several hundreds of kilometers garded as relatively basal angiosperm clades (Judd et al. 2002), but avoided discussing distributions of greater magnitude. this hypothesis is clearly of interest with respect to aquatic Sculthorpe (1967, p. 332) accepted animal dispersal, mainly plant geography. Following similar reasoning, Koch (1931) by birds, as the explanation for broad distributions of aquatic proposed as a “general rule” that the more ancient a species, plants within geographical regions but also concluded that it the more “disjunct” would be its modern distribution. This was “unlikely to be effective in long-range dispersal between idea is also similar to Cain’s (1944) “theory of generic cycles,” continents.” However, Hutchinson (1975, p. 262) believed that whereby discontinuous distributions arise as old taxa show seed dispersal by migratory birds was “the only reasonable decline in different parts of their range. Because it seems rea- explanation of such very long transoceanic migration.” sonable that continental drift is more likely to have influenced Although bird dispersal over extreme distances was typically the geography of older lineages than those of relatively recent associated with plants having large, fleshy fruits (uncommon origin, it is not difficult to envision that the geographical dis- in aquatics) (Campbell 1926), long-distance dispersal by mi- tributions of at least some aquatic groups could reflect patterns gratory water birds prevailed well into the twentieth century imposed by continental drift. as the preferred explanation for the widespread distributions The previous discussion raises an important question. Did of aquatic plants (Ridley 1930; Camp 1947). Some geogra- the many continentally disjunct occurrences of aquatic plants phers suggested the possibility of former physical connections arise as an outcome of long-distance dispersal, or rather, are or land bridges between continents, a hypothesis perhaps less they relicts of continental drift? One way to evaluate this ques- germane to hydrophyte distributions and one severely dis- tion is by considering relative divergence times. If the specific credited by the mid-1960s (Good 1964). Interest also focused time of divergence is known for any two disjunct entities, then increasingly on “displacement theory” as an innovative ex- it should at least be possible to determine whether continental planation for long-distance angiosperm dispersal (Good 1927, drift could have been involved in their disjunction. If conti- 1964). Amid much controversy, Wegener (1912) hypothesized nental drift created a disjunction, then the divergence time of that some continents were once contiguous landmasses that taxa now occupying different isolated continental areas should subsequently separated, a concept now known as “continental approximate (or precede) the time when the continental masses drift.” He provided fossil and geological evidence to theorize were separated physically beyond their effective dispersal dis- that all modern continents had once been joined as a single tance. In contrast, relatively recent divergence times would landmass and that many organismal disjunctions occurred as indicate that a disjunction probably occurred as the result of formerly contiguous continental areas drifted slowly apart. recent long-distance dispersal or possibly through introduc- Although Wegener’s hypothesis provided a novel explana- tion. Thus, a comparison of divergence times for continentally tion for widely disjunct plant populations such as those dis- disjunct aquatic plant species should provide some insight into tributed across transoceanic barriers, his mechanistic expla- the question of mechanisms involved in establishing their cur- nations were weak and his ideas were criticized severely. Yet, rent distributional patterns. Koch (1931) endorsed continental drift as a more reasonable Here we provide a phytogeographical perspective for alternative to the then-prevailing concept of land bridges to closely related, intercontinentally disjunct aquatic plant taxa explain the continentally disjunct distributions of certain (species and genera) that is based on their temporal rela- plants and animals. Good (1951) summarized a number of tionships. Specifically, we use molecular data to estimate di- phytogeographical observations that he believed could be ex- vergence times for closely related, intercontinentally disjunct plained only by land bridges or by continental displacement.