Evolutionary ecology of rare geophytes: Dormancy and mycorrhizae in Cypripedium species

Orchids begin life consuming carbon provided by their mycorrhizal fungi. It is thought that when they become photosynthetic adults, orchids lose their need for fungal carbon. However, lady's slipper orchids (genus Cypripedium ) can spend years without sprouting and photosynthesizing, suggesting a potential lifelong need for mycorrhizal carbon. This condition, called 'adult dormancy', suggests parallels to nonphotosynthetic plants, which acquire all of their carbon from mycorrhizal fungi. Here, I explored the links between adult dormancy and potential mycotrophy in genus Cypripedium by: (1) documenting dormancy across multiple Cypripedium species; (2) exploring the life history context of sprouting; (3) attempting to induce dormancy experimentally; (4) identifying the primary fungi mycorrhizal with genus Cypripedium; and (5) exploring mycorrhizal specialization in this group. In a ten-year census of populations of C. candidum, C. parviflorum, and C. x andrewsii sympatric in a wet meadow in Lake Co., Illinois, USA, I documented parallel trends in adult dormancy among all populations. Dormancy durations up to six years were observed, and dormancy occurred at a cost to annual survival of ten to twenty percent. Reproductive trade-offs were most easily observed in smaller adults of all species. In an experimental study of defoliation and shading on populations of C. calceolus and Cephalanthera longifolia in Estonia, adult dormancy was not induced, but treated plants experienced decreases in sprout quality suggesting scramble competition among ramets. PCR amplification and sequencing of key genomic loci from mycorrhizally colonized orchid tissue revealed that Cypripedium species as a whole form mycorrhizal associations primarily with members of the fungal family Tulasnellaceae, although some also associate with family Sebacinaceae. Cypripedium species associating with both fungal families associated with a narrower phylogenetic breadth of tulasnelloid fungi than those associating with only tulasnelloid fungi, as were Cypripedium populations associating with fewer families relative to populations with more families. Regional variation in mycorrhizal association suggested a geographic mosaic of coevolving mycorrhizal associations. Cypripedium species may be specialized on fungi that best provide carbon during their early years or during dormancy. Conversely, they may be specialized on fungi that best provide nitrogen or phosphorus.