Facultative Annual Life Cycles in Seagrasses

Abstract

Plant species usually have either annual or perennial life cycles, but facultative annual species have annual or perennial populations depending on their environment. In terrestrial angiosperms, facultative annual species are rare, with wild rice being one of the few examples. Our review shows that in marine angiosperms (seagrasses) facultative annual species are more common: six (of 63) seagrass species are facultative annual. It concerns Zostera marina, Z. japonica, Halophila decipiens, H. beccarii, Ruppia maritima, and R. spiralis. The annual populations generally produce five times more seeds than their conspecific perennial populations. Facultative annual seagrass species occur worldwide. Populations of seagrasses are commonly perennial, but the facultative annual species had annual populations when exposed to desiccation, anoxia-related factors, shading, or heat stress. A system-wide 'experiment' (closure of two out of three connected estuaries for large-scale coastal protection works) showed that the initial annual Z. marina population could shift to a perennial life cycle within 5 years, depending on environmental circumstances. We discuss potential mechanisms and implications for plant culture. Further exploration of flexible life histories in plant species, and seagrasses in particular, may aid in answering questions about trade-offs between vegetative and sexual reproduction, and preprogrammed senescence.

Keywords: Halophila; Oryza; Ruppia; Zostera; life history; perennial; sexual reproduction.

Figure 1

Map of locations of annual Zostera marina populations (arrows) and the total distribution of Z. marina (green coastlines). Numbers indicate three types of environments. 1: Environments with yearly recurrent heat stress. 2: Subtidal or permanently submersed environments experiencing anoxia-related stress or shading stress. 3: Mid-intertidal environments with twice-daily exposure to air. More explanation in Section 4 and Supplementary Information S3.

Figure 2

Annual seed production in the six facultative annual seagrass species. A = Annual (open symbols), P = Perennial (grey symbols). If a range was presented, both minimal and maximal values are indicated. Please note that the perennial populations of all species can also have zero seed production, which is quite common for seagrasses. Literature sources and data are in Supplementary Information S2.

Figure 3

Overview of reported habitat characteristics of annual and perennial Zostera marina populations and alleged drivers for transitions between life histories (arrows). The numbers refer to types of reported habitats listed in Box 1. Number 1 is the most typical growth strategy and environment for Z. marina. Thin arrows depict relative differences between environments of annual populations versus nearest perennial populations (correlative). Thick arrows refer to a system-scale inundation “experiment”; see Section 5. The term “anoxia” refers to a situation of more nutrient loading and/or muddier or more organic sediments and/or more anoxic sediment, often accompanied by higher turbidity and lower salinity due to freshwater origin of the nutrient or organic matter loads. These factors usually covariate in eutrophic situations [26].

Figure 4

Dutch waterworks resulting in an unintended system-scale “experiment” in the southwest Netherlands. Prior to coastal defense works, three arms of the Meuse-Rhine estuary harbored annual, mid-intertidal Zostera marina [48]. During the 1960s and 1970s, two of the branches were closed, forming a brackish lake (V = Veere) and a saline lake (G = Grevelingen), whereas the third arm (O = Oosterschelde) remained tidal, though cut off from river water. The freshwater input varied between the lakes; as a result, the brackish Lake Veere had a low salinity, high nutrient loading, macroalgal blooms, high turbidity, and periods of anoxia, whereas the saline Lake Grevelingen had a higher salinity, lower nutrient loading, higher water clarity, and lower algal growth [39]. In the Oosterschelde and the eutrophic brackish lake Veere, Z. marina plants remained annual, but in the oligotrophic saline lake Grevelingen, the plants became perennial within 5 years (comparing [48] with [36,41]). All populations went (near) extinct during the last 3 decades.