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Ecology and Evolution of Long-Lived Semelparous Plants

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Ecology and Evolution of Long-Lived Semelparous Plants TREE vol. 6, no. 9, September 1991 Ecologyand Evolution of Long-lived SemelparousPlants One of the more dramatic life histories in the natural world is that characterized 6y a Truman P. Young and Carol K. Augspurger single, massive, fatal reproductive episode (‘semelparity’). A wealth of increasingly sophisticated theoretical models on differ- ential life history evolution have 6een pro- duced over the last two decades. In recent species often occur in habitats related iteroparous species have gears, empirical studies of the ecology of where plants have slow growth similarly long juvenile stages6J’,12. semelpurous plants (and their iteroparous rates, such as deserts’, tropical al- Many iteroparous trees and shrubs relatives) have begun to address many pine2 and subalpines areas, bogs and most large rosette plants have aspects of the biology of these species, and to and epiphytic positions. In the sec- delayed reproduction. The long juv- test the assumptions and predictions of ond are highly branched woody enile period is perhaps more noted theoretical models. Semelparity in Iong- species with strong population- among semelparous species be- lived plants is one of the few natural level reproductive synchrony; these cause it is followed by only a single phenomena that has yielded specific quan- species occur in more mesic reproductive episode. titative tests of mathematical evolutionary habitats. An additional consequence of theory. The massive translocation of re- slow growth rates and the giant ro- sources at the time of reproduction sette growth form is the extended Semelparity is a distinct life is fundamental to the biology of time between the initiation of inflor- history in which a massive repro- semelparous species. Stored re- escence formation at the apical mer- ductive output is directly associ- sources from roots, stems and istem in the central leaf bud and ated with preprogrammed whole- leaves are moved to reproductive final seed maturation, which can be organism death. (The alternative - structures at the time of f10wering3-5. many months to years4,‘,9,‘3. This de- repeated reproduction - is known It appears that in truly semel- lay means that the environmental as iteroparity.) In plants, the syn- parous plants, virtually all avail- conditions under which flowering is drome of death after first repro- able resources are devoted to initiated are likely to be different duction can occur on several levels: reproductions5. This massive and from the conditions into which ( I I death of the reproductive mer- destructive reproductive effort seeds are dispersed, making it diffi- istem or ramet; (2) death of the makes plant death inevitable, but cult for plants effectively to track physiological individual, not in- results in reproductive outputs far year-to-year environmental vari- cluding disconnected ramets; and higher than the output per episode ation. Additionally, long-lived semel- 131 death of the entire genetic indi- of closely related iteroparous parous plants often exhibit little vidual. In this review, we restrict species or subspecies3,6,7 (Table 2). or no seed dormancy5~6,9~‘0J3-‘5, put- ourselves mainly to long-lived This parallels similar patterns in ting them further at the mercy of semelparous plant species that short-lived semelparous plants and environmental variation (but see grow for at least five to ten years, their iteroparous relatives that first Box I). and up to several decades, before flower at a similar age3. This syn- There is little understanding of reproduction and death of the en- drome of whole-organism death the genetics or the physiology of tire individual. The botanical terms associated with high reproductive semelparity in long-lived plants. monocarpy and polycarpy are effort is a special case of the more However, semelparity in long-lived equivalent to the general terms general phenomenon of the cost of plants occurs in at least 20 fam- semelparity and iteroparity, which reproduction in plants and animals. ilies (Table I), and has apparently refer to both plants and animals. Fruit and seed production in evolved many times. The existence Many short-lived plants and ani- semelparous Yucca and Lobelia are of intraspecific variation in this mals are semelparous. Among long- highly variable, and strongly related trait7J6 and interspecific hybrids be- lived organisms semelparity is to resource availability3,8. This is tween iteroparous and semelparous relatively rare, but taxonomically not surprising, given that there is species”.17 suggests that the num- diverse, including both vertebrate no alternative sink for resources. ber of mutations required to evolve (salmon, alewives) and invertebrate On the other hand, closely related semelparity is not large. (cicadas, squids) animals, and a iteroparous species may keep re- For a physiological explanation of wide variety of plant species in at productive output relatively con- semelparity, a source-sink model least 20 families. stant with increasing resource may be appropriate. In short-lived The ecological and morphological availability, but increase allocation perennial species that were nor- diversity of long-lived semelparous to vegetative structures3. Again, this mally unbranched and semel- plants can be classified into two parallels similar patterns in short- parous, experimental elimination of basic syndromes (Table 1 I. In the lived semelparous plants and their the sink (pollinator exclusion and first are unbranched rosette plants iteroparous relatives3. flower removal in lpomopsis’s) and with terminal inflorescences; these By definition, long-lived semel- supplementation of the source parous plants have extended juv- (high soil nutrient treatments in Truman Young is at the Center for Population Bi- enile stages, from a few years to Picris and Scabiosa19) resulted in ology and Dept of Botany, University of California, several decades. This ‘delayed re- branching and iteroparity. Appli- Davis, CA, USA; Carol Augspurger is at the Dept of production’ in semelparous species cation of fertilizer to normally Plant Biology University of Illinois, 505 S Goodwin has been the subject of consider- semelparous bamboo can also Av., Urbana. IL, USA. able attention4,9,‘0. However, closely result in iteroparity’O. 285 TREE vol. 6, no. 9, September 1991 Table I. Known long-lived semelparous plants Family Unbranched rosette plants with hapaxanthic shoots Alpine Theoretical approaches to the evolution of Lobelia spp. (Africa) Lobeliaceae Trematolobelia spp. Lobeliaceae semelparity Argyroxiphium spp. Compositae Numerous theoretical treatments Espeletia floccosa Compositae of the differential evolution of Puya spp. (South America) Bromeliaceae semelparity and iteroparity have Echium wildprettii Boraginaceae Lupinus alopecuroides Leguminosae been developed over the last two decades. All assume a trade-off Subalpine between present and future re- Frasera speciosa (western US) Gentianaceae Harmsiopanax ingens Araliaceae production, i.e. that semelparity is Phoenicoseris spp. Compositae associated with an increase in Centaurodendron dracenoides Compositae fecundity (Table 2). All of these Arid and semi-arid treatments are mathematically re- Agave spp. Agavaceae lated, but they fall into three basic (Furcraea spp.) Agavaceae types of model. Yucca whipplei ssp. Agavaceae Aeonium spp. Crassulaceae Wilkesia gymnoxiphium Compositae Bet-hedging models One set of models predicts that Bogs Lobelia spp. (Hawaii) Lobeliaceae increasing environmental variability Puya dasylirioides (Central America) Bromeliaceae and unpredictability favor itero- Epiphytic parity over semelparity20,21. This for- Tillandsia spp. Bromeliaceae malizes the intuition that limiting reproduction to a single episode is Other Corypha spp. Palmae particularly risky in an unpredict- Plectocomia spp. Palmae able environment (see Box 1). How- Frasera caroliniensis (Eastern US) Gentianaceae ever, some bet-hedging analyses insufficiently known (unbranched?) rosette plants with hapaxanthic shoots’ produce the opposite prediction**. Aechmanthera spp. Acanthaceae In addition, many semelparous, Boea spp. Gesneriaceae and not iteroparous, plants are Brillentarsia nitens Acanthaceae found in habitats likely to be more Dendroseris spp. Compositae Drachophyllum verticillatum Epacridaceae variable. Annuals and biennials are Ensete spp. Musaceae typically found in habitats that Greenovia spp. Crassulaceae are ephemeral and unpredictable, Heterochaenia spp. Campanulaceae either successionally (disturbed Hymenoxys spp. Compositae Kalanchoe spp. Crassulaceae sites) or edaphically (deserts and Orchis spp. Orchidaceae dunes). Long-lived semelparous Spathelia spp. Rutaceae rosette plants are commonly found Sohnreyia excelsa Rutaceae in drought-prone habitats (Table I), Streptocarpus spp. Gesneriaceae which can be highly variable with Tauschia decipiens Umbelliferae Yunquea tenzii Compositae respect to rainfall and correlated demographic parameters3,6,9,“.17,23. Synchronously flowering branched woody plants The variability of these environ- Bamboo spp. (>17 genera, ,150 species) Gramineae Mimulopsis solmsii Acanthaceae ments is particularly difficult to track Strobilanthes spp. Acanthaceae for plants without seed dormancy Tachigalia spp. Leguminosae and with long inflorescence pre- Cerberiopsis candelabrum Apocynaceae formation times, as are common Parasite on Strobilanthes in long-lived semelparous plants. Campbellia aurantiaca Orobanchaceae aMostly from Refs 5,30 and 44. Reproductive effort model A second theoretical
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