STUDIES OF THE CYANOGENESIS POLYMORPHISM IN TURNERA (ILMIFOLU L. (TURNERACEAE)AND ITS INTERACTION WITH THE BUTTERFLY EUPTOIETA HEGESU CRAMER (NYMPHALIDAE) ON JAMAlCA PHILLIP JOSEPH SCHAPPERT A thesis submitted to the Faculty of Graduate Studies in partial fuifiient of the requirements for the degree of Doctor of Philosophy Graduate Program in Biology York Univeisity North York, Ontario, Canada June 1997 National Library Bibliothèque nationale I*I of Canada du Canada Acquisitions and Acquisitions et Bibliographie Services services bibliographiques 395 Wellington Street 395, rue Wellington OttawaON KIAON4 ûttawaON KIAON4 Canada Canada Your* VYohsnifërsncs Our Nomriliéma The author has granted a non- L'auteur a accordé une licence non exclusive licence allowing the exclusive permettant à la National Librq of Canada to Bibliothèque nationale du Canada de reproduce, loan, distnbute or sefl reproduire, prêter, distribuer ou copies of this thesis in microform, vendre des copies de cette thèse sous paper or electronic formats. la forme de microfiche/film, de reproduction sur papier ou sur format électronique. The author retains ownership of the L'auteur conserve la propriété du copyright in this thesis. Neither the droit d'auteur qui protège cette thèse. thesis nor substantial extracts fkom it Ni la thèse ni des extraits substantiels may be printed or othefwise de celle-ci ne doivent être imprimés reproduced without the author's ou autrement reproduits sans son permission. autorisation. STUDIES OF THE CYANOGENESIS POLYMORPEISM IN TURNERA ULMIFOLIA L. (TURNERACEAE) AMI ITS INTERACTION WITH W BUTTErCFLY EUPTOIETA EIEGESIA CRAMER (NPMPBALIDAE) ON JAMAICA by Phillip Joseph Schappert a dissertation subrnitted 10 the Faculty or Graduate Studies of York University in partial fulfillment of the requirements for the degree of Permission has been granted to the LIBRARY OF YORK UNlVERSlW to lend or seIl copies of this dissertation, to the NATIONAL LISRARY OF CANADA to microfilm this dissertation and to lend or sel1 copies of the film, and to UNIVERSITY MICROFILMS to publish an abstract of this dissertation. The author reserves other publication righls. and neilher the dissertation nor extensive extracts from it may be printed or otherwise reproduced without the author's wrilten permission. Abstract An investigation of the chemical mediation of tritrophic interactions among a plant, its herbivores and their predatoa was undertaken. Extensive phenotypic variation for cyanogenesis among populations of Tuntera uZrnfoZia on Jamaica has a strong genetic bais, is quantitative in nature, and results fiom dserences in the quantity of cyanogenic giycosides. Seedlings have significantly higher levels of cyanogenesis than mature plants in some populations. Tissue damage to plants varies among populations and appears to be associated with plant cyanogenesis, however, darnage levels are low and do not always correlate with cyanogenesis. Evidence for a tmdeoff between cyanogenesis and the proportion of plants flowering in populations, and between fiower number among populations, was found. Potential selective agents that might account for the spatial distribution of cyanogenesis on the island include a relatively srnall suite of specialist herbivores that are undeterred by cyanogenesis and responsible for most leaf damage. This investigation provides the first detailed study of the ecological genetics of cyanogenesis in natural populations of a tropical plant, and its interactions with generdist and specialist herbivores. Turneru ulmifolia is the primary hostplant of Euptoieta hegesia on Jarnaica Butterfly population size is not limited by the availability of hostplants and larvae are disaibuted non-randomly arnongst hosts. Butterfiies are short-lived, residents of discrete hostplant populations, and experience high mortality levels. Females are damaged more fiequently, sustain more damage and more fiequent symmetrical hindwing darnage attributable :O iv ground-based predators than do males. In experiments, females do not show preference for hostplants on the basis of their cyanogenesis Ievel, however plants with larvae were, on average, less cyanogenic than plants without larvae in nature. Larvae may prefer more cyauogenic tissues, and subsbntial genetic variation for preference exists among larvae, however, hostplant cyanogenesis ha no effect on the growth or developrnent of the larvae. Larvae are capable of sequestering cyanogenic glycosides fiom their hostplants and may dso synthesize these compounds. Significantiy higher levels of cyanogenic glycosides in larvae which have fed on highly cyanogenic plants protects them from terresaial-based predators such as Anolis sagrei. This thesis would not have been possible were it not for my supe~sorycommittee (whom I met while taking field courses during my undergraduate -dies), the U. of T. "brat pack", now at York University: Dr. kel Shore, who has been my fkiend and mentor, source of fünding, had a greenhouse full of caterpillar food, introduced me to spicy Jamaican food and is a fine fiddier to boot; Dr. Laurence Packer, who recognizes the value of natural history in biology, inwduced me to even spicier Indian food and was aiways supportive; and Dr. Marla Sokolowski, whose fiies tormented me continually @ow else wouid 1 know that a single crushed Leaf of cyanogenic T. uhifolia will kill flies in under 10 minutes?). I've benefited fiom the support of a number of lab-mates over the years: Svenja Belaoussoff, who broke in our supewisor and taught me how not to make coEee; Andreas Athanasiou, who began as an egg and lawa counter and ended up doing graduate work in molecula. biology (1 take Ml credit for this); and the various honors students and helpers that have been through the Plant Evolution Lab: Gus Lagos, Oron Anter, Mark DeBoer, Ashley Byun, Steve Little, Karina McQueen, Angela Baker, Ashkan Golshani, Rob Demiglio, Jennifer Lewin and Laurence Giraudi. My thanks aiso to al1 of those people who have made field work in Jamaica possible and enjoyable: Dr. Jeremy Woodley, Dr. Michael Haley and the staff at Discovery Bay Marine Lab., Dr. Eric Garraway, a fellow "butterfiy-man", Susan Mitchell, Pat Schappert, Robert and Ann Sutton, and the many fine folk of Jarnaica who kept me on my toes (and thus dive) on the highways and byways throughout the island. My appreciation also to ail of the correspondents whom I've bothered over the years: Tom Turner, Guy Hallman, Helene Engler, Marcio Cardosa, Catherine Duckett, Adolf Nahrstedt, David Raubenheimer, Keith Brown, Art Shapiro, and anyone who 1 have unthinkingly forgotten. Finally, my entire academic career would never have been possible without the fmancial, logistical, intellecnial and exnotional support of my loving wife, Pat. She deserves this degree as much as, possibly more than, 1 do... "1 promise that you'll always get to live in a warm country.'' 1 lovingly dedicate this thesis to my late mother, Pauline Francis Schappert, who, upon hearing that 1 was giving up a 40K per year job to return to school at the age of 30, said "You're going to do what!?!". vii Table of Contents Preface ............................................................................... 1 Chapter 1: Cyanogenesis in Tmera ulmifolia L. (Tumeraceae). 1. Phenotypic distribution and genetic variation for cyanogenesis on Jamaica ................... 3 1 Chapter 2: Cyanogenesis, herbivory and plant defense in Turneru ulmifolia on Jamaica ............................................................ 72 Chapter 3: Ecology, population biology and moaality of Euproietu hegesia Cramer (Nymphalidae) on Jamaica ............................................. 121 Chapter 4: Effects of cyanogenesis in Turnera ulmifolia on Euptoieta hegesia, a specialist herbivore. .................................................. 180 Appendix A: Cyanogenesis in Turnera ulmijolia L. (Turneraceae). II. Developmentai expression, heritability and con of cyanogenesis. ...............,242 Appendix B: Cyanogenesis in Turnera ulmiflia L. (Tumeraceae). m.Selective impact of specialist herbivores on cyanogenesis and reproductive sucess. ....... -266 Conclusions ........................................................................ 29 1 List of Tables Table 1. Hostplant Relations in the Heliconiinae. ..................................... 14 Table 1.1. Mean cyanogenesis levels for selfed and reciprocal cross progeny. ......... 45 Table 1.2. Population name, nurnber, location, elevation and mean yearly precipitation for 39 populations of T. ulmifoolia on Jamaica ....................... 46 Table 1.3. Two-way ANOVA comparing mean cyanogenesis levels of adult plants versus seedlings for 12 populations. ....................................... 53 Table 1.4. Effect of exogenous glycoside addition on cyanogenesis for three populations showing low levels of cyanogenesis. ................................. 55 Table 1S. ANOVA for differences in mean cyanogenesis of adult plants for three populations following addition of exogenous glycoside. ..................... 56 Table 1.6. Correlations arnong mean cyanogenesis levels and means of four abiotic factors for 39 populations of T. ulmifolia on Jamaica ..................... 57 Table 2.1. Population identification, swey sample sizes, population locations, elevation, mean annual precipitation and cyanogenesis levels of T. ulmifolia populations surveyed. ............................................................ 86 Table 2.2. Cyanogenesis contrast between T. ulntifolia plants on which E. hegesia