Morphology and Development in the Zingiberales
I am an expert on the flower structure and development in the Zingiberales, the order of tropical plants that contains the culinary gingers and bananas. The order contains eight families and over 2,000 species. The families can be divided into two groups: the monophyletic group of ginger families (Costaceae, Zingiberaceae, Marantaceae, Cannaceae), and the basal and paraphyletic banana families (Musaceae, Strelitziaceae, Lowiaceae, Heliconiaceae). My work has concentrated on the evolution of floral structure, and on morphological constraints on flower development (Kirchoff 1983a, b, 1988a, b, 1991; Kirchoff and Kunze 1995; Kirchoff 1997, 1998, 2000, 2003). These are important areas of investigation because modifications of floral structure are associated with the diversification of the ginger families (Kirchoff 1991; Specht 2006). This is in marked contrast to the banana families, in which there is less structural variation and fewer species. Understanding the developmental basis for floral variation in the ginger families may provide insights on types of developmental changes associated with speciation.
Work in Progress
I am currently completing a study of flower and inflorescence development in banana. This work is being carried out in collaboration with Dr. Chelsea Specht (UC Berkeley). The Musaceae play a crucial role in understanding character evolution in the order because they are the sister group to the other families (Kress et al. 2001). The majority of the families have lateral partial florescences of cincinni, and the flower cluster (“hand”) of cultivated bananas (M. acuminata, M. balbisiana) has been described as a cincinnus based on developmental study (Fahn 1953). However, we have been unable to confirm the cincinnal nature of the hand in a wild species of banana (M. velutina). The sequence of flower formation in M. velutina does not conform to that expected in a cincinnus. This difference calls into doubt the primitive form of the inflorescence in the order.
We have completed data collection on flower and inflorescence development in Musa velutina and a manuscript is being prepared for publication. The plates for this paper were designed in collaboration with a graphic artist (Ross Cangelosi) in order to maximize their information content.
Dr. Specht, her students, and I have also completed data collection on flower development in Phenakospermum guyannense (Strelitziaceae), and data collection on flower development in Orchidantha chinensis (Lowiaceae) is almost complete. A major study of floral anatomy in the family Zingiberaceae is also nearing completion.
In addition to these studies of flower and inflorescence development, I am working to define homologous floral developmental stages across the eight families of the Zingiberales. This work is being carried out as an offshoot of my work on morphological characters, which is described below. I will return to a description of my methods for describing homologous stages after introducing my innovative work on character identification.
Describing Morphological Characters
A central theme of my research has been the development of new methods for describing morphological characters. I used data from my work on ovary structure in the family Zingiberaceae to establish and test the procedures (Fig. 1), but the work has implications far beyond this organ system and family. I am interested in the role of complex data in improving characters, in inter-investigator reliability in describing morphological characters, and in the ability of different types of characters to capture meaningful information (Kirchoff et al. 2004, 2007).
The problem of inter-investigator reliability is particularly troubling for morphological character definitions. Given the same data, different investigators have been shown to partition it in different ways (Gift and Stevens 1997; Kirchoff et al. 2007). An empirical study of character descriptions in the botanical literature has come to similar conclusions (Hawkins 2000).
My work addresses the problem of inter-investigator reliability by establishing and validating a new method of character description (Kirchoff et al. 2004, 2007). The method uses direct comparison and sorting of images of homologous parts to produce hierarchical character-cladograms: graphical representations of a single character that serve as hypotheses of taxonomic relationships (Fig. 1). Character-cladograms are information rich representations of homology. They can be easily coded for inclusion in most types of analyses (Kirchoff et al. 2007), and unlike traditional characters, their inter-investigator reliability has been confirmed (Kirchoff et al. 2007).My work on character description began with two papers that outlined the current problems with morphological characters (Kirchoff 2001, 2002). In the first I explored the relationship between a traditional (“atomistic”) character and its context through a review of the botanical work of Wolfgang von Goethe, the founder of the field of morphology (Kirchoff 2002). This paper uses several examples to show how an awareness of context is important for understanding organismal form. I continued this work with an exploration of Agnes Arber’s dynamic concept of the plant and its potential to change how we describe characters (Kirchoff 2001). This paper was part of a symposium I co-organized with Rolf Rutishauser (
) in celebration of the 50th anniversary of the publication of Arber’s book “The Natural Philosophy of Plant Form.” In this paper, I suggest that a pictorial approach to character description will produce better results than the verbal/linguistic approach that is currently in use. This is because pictures allow the inclusion of the context of the character that is being considered. Verbal descriptions remove this context.
These papers led to experimental research and publications using human subjects to investigate inter-investigator reliability of characters (Kirchoff et al. 2004, 2007). In addition to providing some of the only data on character reliability, this work expanded my expertise into the area of educational research, and familiarized me with aspects of the cognitive psychology literature. This work is relevant not only to morphological character description, but has also allowed me to develop new methods for training young scientists (see below).
Many of the conclusions that I reached on theoretical grounds (Kirchoff 2001, 2002), have been validated by experimental cognitive psychology research on visual processing modes (Gauthier and Tarr 1997; Gauthier et al. 1998; Bukach et al. 2006). This line of research has led me to a large follow-up study to my 2007 paper. In it I compared inter-investigator reliability with conventional characters and character-cladograms. Forty six undergraduate students were involved as subjects, with four additional undergraduates and one technician assisting in the research. All of the data has been collected, but further data analysis is necessary before the research is ready for publication.
Work in Progress
Describing Homologous Stages of Flower Development
The ability to establish homologous developmental stages among a variety of species will open a vast reservoir of data for phylogeny reconstruction, the study of the evolution of development, and will assist in the genetic characterization of development in non-model species. Based on my work with character-cladograms I am working to characterize homologous developmental states in the flowers of the Zingiberales.
Flower development can be thought of as a sequence of developmental events that are conventionally arranged into a temporal sequence of stages. Floral shape varies continuously throughout this sequence. Except in the rare instances where standardized stage definitions have been developed in model species (Bowman 1994), each individual investigator divides the developmental variability he or she sees in a single species into discrete stages with the assumption that these stages will be comparable across species. This procedure works well in cases where the floral organs are formed in discrete, non-overlapping stages; e.g., all of the sepals are formed before any of the petals (Fig. 2). In these cases, it is a relatively simple matter to define developmental stages based on the organ type being formed: stage of sepal formation, stage of petal formation, etc. However, in the Zingiberales floral organs are not formed in discreet stages. For instance, organs at the center of the flower may form before sepal initiation is complete (Fig. 3). This makes it difficult to identify developmental stages based solely on comparison with an idealized label (sepal formation, etc.).
In order to identify homologous stages I am partitioning the developmental variability across the eight families into discrete stages through a series of sorting tasks (Kirchoff et al. 2007). That is, I am creating character-cladograms. The photographs are partitioned into groups (developmental stages) along two dimensions: (1) the temporal variation within a species is partitioned into distinct stages; (2) comparable stages are identified across all study species. Since flower development varies across the order, sometimes considerably (Kirchoff 1983a, 2003), homologous stages are difficult to define. The use of a standardized visual method of homology assessment, coupled with archiving of the images in an online image repository (Morphbank: http://www.morphbank.net/), provides a method of producing standardized, verifiable homology assessments.
Character Description in Lupine Seed Coats
In collaboration with Dr. Ellen Simms (Department of Integrative Biology, UC Berkeley) I am working to identify characters in Lupinus seed coats. Aside from my work on character description (Kirchoff et al. 2004; Kirchoff et al. 2007), there are no published procedures for character discovery. Dr. Simms and I are applying a variation on my character-cladogram methods to describe the seed coats of two California species of Lupinus, L. bicolor and L. nanus. A central tool in this research is the computer program (the “engine”) developed as part of my Image Quiz Project (see next section), and used in Woody Plants of the Southeastern United States: A Field Botany Course on CD (Kirchoff 2008). I have adapted this program to a research context and have used it to train myself and my collaborators in seed coat pattern recognition. The need for this training is clearly established in the cognitive psychology literature on visual expertise (Bukach et al. 2006). Following training, we applied methods adapted from my work on character-cladograms to define characters in the seed coats. So far we have identified 18 characters, most of which have never been described before. This work is supported by an NSF Research Opportunity Award co-written with Dr. Simms.
Paedomorphosis and The Evolution of Secondary Woodiness
The theory of paedomorphosis in the secondary xylem is a description of certain characteristics found in the secondary xylem of plants with shrubby, suffrutescent, pachycaulous, or lianoid growth forms. These characters include a decreasing, or stable, length of vessel elements as the xylem ages; the presence of scalariform perforation plates; scalariform or pseudoscalariform lateral wall pitting; and the absence of rays. Since many species with paedomorphic wood are found on islands, the concept of insular woodiness is closely associated with paedomorphosis and with the occurrence of secondary woodiness, the origin of wood from non-woody ancestors.
My M.S. student Max Dulin analyzed the secondary vascular systems of three plants that had been reported to be secondarily woody, and reviewed the related concepts of paedomorphosis, insular woodiness, and secondary woodiness (Dulin and Kirchoff 2010). A careful literature review demonstrated that although paedomorphosis is often associated with secondary woodiness, there is no necessary association between these phenomena. Plotting the possession of paedomorphic wood on a phylogeny of the Ericaceae (Kron et al. 2002) clearly demonstrated this point. The possession of secondary woodiness is best determined by phylogenetic analysis.
If paedomorphic wood is not a consequence of secondary woodiness, what is its function? The xylem structure of the three species Max investigated was found to be consistent with the hypothesis that paedomorphic wood is a response to relaxed selection for mechanical strength (Carlquist 2001). There is an inverse relationship between the mechanical strength of the stem and the degree of paedomorphosis. Given this relationship, the degree of paedomorphosis may be a better indicator of a plant’s mechanical requirements then of its evolutionary history.
Max and I also reviewed the use of the terms herbaceous and woody in the context of new data on stem structure in “herbs” (Schweingruber and Landolt 2005-2008). The vast majority of these “herbaceous” plants possess secondary growth, much of which can easily be called wood. This finding lead us to suggest that the terminology used to describe growth habit should be distinct from that used to indicate the possession of secondary xylem.
A version of Max’s thesis has recently been published in Botanical Review (Dulin and Kirchoff 2010). The manuscript was accepted without revision.
New Pedagogies: Research and Educational Tools
One result of my work on character description has been the development of computer-based techniques for the rapid training of visual experts. These techniques, which are being developed under the auspices of my Image Quiz Project, will find application in any field that relies on visual data. An outline of the project has recently been published (Kirchoff 2007). Based on this work I have developed tools for use in research (character discovery in Lupine seeds) and teaching (Kirchoff 2007), and am in the process of creating new types of visual keys (Kirchoff et al. 2008). The first major publication resulting from this work is a peer-reviewed, active learning CD published by Missouri Botanical Garden Press (Kirchoff 2008). Woody Plants of the Southeastern United States: A Field Botany Course on CD (WPSEUS) took 2½ years to develop and involved collaborations with other systematists, programmers and photographers from five universities and the private sector. One spin-off from this project has been a publication outlining photographic standards for digital plant images (Baskauf and Kirchoff 2008).
I have also worked with programmers to design and develop a second program, Script Editor¸ that allows the creation of customized study routines (scripts) for use with WPSEUS. It is now possible to create custom study routines, distribute them through Blackboard®, receive response files from users, and easily calculate performance grades. Script Editor makes WPSEUS a very effective teaching tool. My colleague, Meg Horton, and I tested its effectiveness in my Plant Systematics (Bio. 354) class and found that it led to an 18.5% increase in exam scores over traditional study methods (p = 0.000). We are in the process of preparing this research for publication.
Control of Invasive Species
Undergraduate students in my lab have tested an organic method for invasive species control. The method originated in the organic farming movement of the early 20th century, but had never been experimentally tested. The method consists of applying a special preparation of burnt seeds to the soil over a period of four years (Steiner 1924/1993). Although anecdotal reports of the method’s efficacy on small farms have existed for many years, there were no controlled tests of its effectiveness. To carry out this research, we developed an experimental system in which we grew five generations of plants in controlled environment chambers in a little over one year. This allowed us to test five applications of the preparation in a short period of time. The use of untreated controls allowed us to make statistical comparisons between treated and untreated soils under the same conditions. Unfortunately, the results did not suggest that this was a viable approach to the control of invasive species. A paper is being prepared for submission.
The Image Quiz Project
Image Quiz Project is focused on developing computer-based tools to improve visual learning. The first fruit of the project was published in spring 2008 by Missouri Botanical Garden Press: Woody Plants of the Southeaster United States: A Field Botany Course on the Computer (WPSEUS). A summary of the project was published in the Proceedings of 2007 UNC Teaching and Learning with Technology Conference, and can be accessed here.
I have also developed an educational card game (Poison Ivy) based on the same principles embodied in WPSEUS. A limited edition of this game has been produced, and is being distributed to teachings for comment.
Work in progress includes the development of teaching system for Neuropathology, in collaboration with Dr. Hannes Vogel (Stanford University).
A company, Metis LLC, has been formed to produce and market new versions of the software.
Pollen Structure and Essential Oil Secretion
My long term collaboration with Dr. Jing-Ping Liao’s lab at the South China Botanical Garden, Chinese Academy of Sciences, became more active when I was appointed as a Visiting Scientist at the Garden for the years 2007 and 2008. I visited the Garden at their expense during summer 2007, and have been in touch with collaborators in Dr. Liao’s lab on a weekly basis since that time. Our main areas of research have been in pollen development (Liu et al. 2007), secretory trichome development (Huang et al. 2008. 2010), calcium function in pollen development (Chen et al. 2008), and on pollen structure in the Magnoliaceae. (Xu and Kirchoff 2008) and Rubiaceae (Kuang et al. 2008). Two additional papers on calcium function in secretory trichome development are in preparation (Huang et al. in prep-a, b).
A doctoral student (Ms. Kuang) from Dr. Liao’s lab has received funding from the Chinese Academy of Sciences to work in my lab during fall 2008, and has recently arrived. We are continuing our study of pollen morphology in the Rubiaceae.
Collaborators on the Image Quiz project include Steve Baskauf (Vanderbilt), Alexander Krings (NC State), and Ben Purcell, John Cox, and Zubin Chadran (Programers). The software has been tested in a classroom setting in collaboration with Meg Horton (UNCG). Additional testing is being pursued with Carrie DeJacko (Queens University).
Visual Keys: Dr. Dave Remington (Biology), and Dr. Fereidoon Sadri (Computer Science) all at UNCG
Seed coat patterns in California Lupines: Dr. Ellen Simms, Department of integrative Biology, UC Berkeley
Floral development in the Zingiberales: Dr. Chelsea Specht, Department of Plant and Microbial Biology, UC Berkeley
Pollen morphology, trichome structure, floral anatomy (and other projects): Dr. Jing-Ping Liao, Chinese Academy of Sciences, Guangzhou, China
Baskauf, S. J., and B. K. Kirchoff. 2008. Digital plant images as specimens: Toward standards for photographing living plants. Vulpia 7:16-30.
Bowman, J. 1994. Arabidopsis: An atlas of morphology and development. Springer-Verlag, New York.
Bukach, C. M., I. Gauthier, and M. Tarr. 2006. Beyond faces and modularity: The power of an expertise framework. TRENDS in Cognitive Sciences 10:159-166.
Chen, S.-H., B. K. Kirchoff, and J.-P. Liao. 2008. Calcium distribution and function during anther development of Torenia fournieri L. Annales Botanici Fennici 45.
Fahn, A. 1953. The origin of the banana inflorescence. Kew Bulletin 3:299-306.
Gauthier, I., and M. J. Tarr. 1997. Becoming a ''greeble'' expert: Exploring mechanisms for face recognition. Vision Research 37:1673-1682.
Gauthier, I., P. Williams, M. J. Tarr, and J. Tanaka. 1998. Training "greeble" experts: a framework for studying expert object recognition processes. Vision Research 38:2401-2428.
Gift, N., and P. F. Stevens. 1997. Vagaries in the delimitation of character states in quantitative variation - An experimental study. Systematic Biology 46:112-125.
Hawkins, J. A. 2000. A survey of primary homology assessment: Different botanists perceive and define characters in different ways. In: R. P. Scotland, R. T., ed. Homology and systematics, Systematics Association Special Volume 58 Taylor and Francis, New York. pp.22-53.
Horridge, J. 2006. Tomato: truss development - t75.3c Part of a flower truss showing an axillary meristem with one primordium. University of Warrick. Warrick, UK. (http://www2.warwick.ac.uk/fac/sci/whri/research/protectedcrops/researchsummary/jhorridge/tomtruss/) Accessed: June 06, 2010.
Huang, S.-S., B. K. Kirchoff, and J.-P. Liao. 2008. The Capitate and Peltate Glandular Trichomes of Lavandula pinnata L. (Lamiaceae): Histochemistry, Ultrastructure and Secretion. Journal of the Torrey Botanical Society 135:155-167.
Huang, S-S., J-P Liao, and B. K. Kirchoff. 2010. Calcium distribution and function in the glandular trichomes of Lavandula pinnata L. Journal of the Torrey Botanical Society 137:1-15
Kirchoff, B. K. 1983a. Floral organogenesis in five genera of the Marantaceae and in Canna (Cannaceae). American Journal of Botany 70:508-523.
Kirchoff, B. K. 1983b. Allometric growth of the flowers in five genera of the Marantaceae and in Canna (Cannaceae). Botanical Gazette 144:110-118.
Kirchoff, B. K. 1988. Inflorescence and flower development in Costus scaber (Costaceae). Canadian Journal of Botany 66:339-345.
Kirchoff, B. K. 1991. Homeosis in the flowers of the Zingiberales. American Journal of Botany 78:833-837.
Kirchoff, B. K. 1997. Inflorescence and flower development in the Hedychieae (Zingiberaceae): Hedychium. Canadian Journal of Botany 75:581-594.
Kirchoff, B. K. 1998. Inflorescence and flower development in the Hedychieae (Zingiberaceae): Scaphochlamys kunstleri (Baker) Holttum. International Journal of Plant Sciences 159:261-274.
Kirchoff, B. K. 2000. Hofmeister's rule and primordium shape: Constraints on organ position in Hedychium coronarium (Zingiberaceae). In: K. L. Wilson, and D. A. Morrison, eds., Monocots: Systematics and Evolution, CSIRO Publishing, Collingwood, Australia. pp.75-83.
Kirchoff, B. K. 2001. Character description in phylogenetic analysis: Insights from Agnes Arber's concept of the plant. Annals of Botany 88:1203-1214.
Kirchoff, B. K. 2002. Aspects of a Goethean Science: Complexity and Holism in Science and Art. In: H. Rowland, ed. Goethe, Chaos, and Complexity, Editions Rodopi, Amsterdam. pp.79-89, 189-194.
Kirchoff, B. K. 2003. Shape matters: Hofmeister's rule, primordium shape, and flower orientation. International Journal of Plant Sciences 164:505-517.
Kirchoff, B. K. 2007. Image Quiz: Using principles of cognitive psychology to teach visual expertise In: Proceedings, UNC Teaching and Learning with Technology Conference. UNC TLT Collaborative, Raleigh, NC: 1-7.
Kirchoff, B. K. 2008. Woody Plants of the Southeastern United States: A Field Course on CD. Missouri Botanical Garden Press, St. Louis, MO.
Kirchoff, B. K., and H. Kunze. 1995. Inflorescence and floral development in Orchidantha maxillarioides (Lowiaceae). International Journal of Plant Sciences 156:159-171.
Kirchoff, B. K., D. L. Remington, Lixin Fu, F. Sadri. 2008. A New Type of Image-Based Key. Proceedings of the International Conference on BioMedical Engineering and Informatics, 2008. BMEI2008. 1: 825-829. DOI 10.1109/BMEI.2008.301
Kirchoff, B. K., S. J. Richter, and D. L. Remington. 2007. Characters as groups: A new approach to morphological characters in phylogenetic analysis. Taxon 56:497-492.
Kirchoff, B. K., S. J. Richter, D. L. Remington, and E. Wisniewski. 2004. Complex data produce better characters. Systematic Biology 53:1-17.
Kress, J. W., L. M. Prince, W. J. Hahn, and E. A. Zimmer. 2001. Unraveling the evolutionary radiations of the families of the Zingiberales using morphological and molecular evidence. Systematic Biology 50:926-944.
Kuang, Y.-F., B. K. Kirchoff, Y.-J. Tang, Y.-H. Liang, and J.-P. Liao. 2008. Palynological characters and their systematic significance in Naucleeae (Cinchonoideae, Rubiaceae). Review of Palaeobotany and Palynology 151:123-135.
Liu, H. F., B. K. Kirchoff, G. J. Wu, and J. P. Liao. 2007. Microsporogenesis and male gametogenesis in Jatropha curcas L. (Euphorbiaceae). Journal of the Torrey Botanical Society 134:335-343.
Specht, C. D. 2006. Systematics and evolution of the tropical monocot family Costaceae (Zingiberales): A multiple dataset approach. Systematic Botany 31:89-106.
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Xu, F.-X., and B. K. Kirchoff. 2008. Pollen morphology and ultrastructure of selected species of Magnoliaceae. Review of Palaeobotany and Palynology 150:140-153.