TO WHAT EXTENT DO MODE OF REPRODUCTION, LEVELS OF GENOTYPIC DIVERSITY, AND CONNECTIVITY IN Vallisneria americana MICHX. CONFER RESILIENCE TO A CHANGING CLIMATE?

Abstract

The macrophyte Vallisneria americana Michx. (Hydrocharitaceae) is a foundational submersed aquatic vegetation (SAV) species that provides valuable ecosystem services, such as nutrition for waterfowl and shelter for fish. When healthy, V. americana can absorb excess nutrients from the water and stabilize sediments, but many of its meadows, which span freshwater to oligohaline environments in eastern North America, have been declining since European settlers cleared the land. Declines only intensified in the 1950s due to chronic environmental stressors and major storm events. To determine the extent to which remaining populations can adapt through natural selection or acclimate to novel environmental conditions, I combined observational field data, greenhouse experiments, and spatial modeling to quantify V. americana reproduction at local to regional scales, evaluate evidence of local adaptation and acclimation to environmental stress, and assess the extent to which high levels of connectivity in a V. americana-dominated landscape can absorb environmental stress.I quantified reproduction at 15 sites in the Chesapeake Bay and 14 sites in the Hudson River, with sites in each geographic region spanning the portion of the salinity gradient in which V. americana grows (0-12 ppt). Numbers of inflorescences, sex ratios, and distances among male and female inflorescences varied greatly across latitude and along salinity gradients. Hudson V. americana had fewer inflorescences across two sampling seasons than Chesapeake Bay V. americana but delayed phenology, skewed sex ratios, and large distances among males and females relative to the Chesapeake Bay were more pronounced in 2018. In 2018, warmer spring and summer water temperatures in the Chesapeake coincided with our findings of higher flowering, fruiting, and potential for pollination at the three Chesapeake sites that served as means of comparison to the Hudson. By contrast, in 2020 Hudson plants were larger and produced more inflorescences in July than Chesapeake plants produced in June, indicating that the regional difference in phenology may be smaller than our hypothesis of approximately 23 days, although it is difficult to estimate how much smaller. We attribute this result to sites in the Hudson – mainly those in the tidal-fresh zone of the river – being highly responsive to unusually warm 2020 spring water temperatures. But not all sites experienced this warmth. The tidal-saline zone of the Hudson and the non-tidal zone of the Chesapeake had the fewest flowers and fruits of either region, likely due to the synergistic effects of cold temperatures and high salinity and turbidity in the former and fast currents in the latter inhibiting growth and reproduction. Through greenhouse experiments evaluating growth and reproduction of Chesapeake and Hudson V. americana grown in different salinity conditions, we found evidence of one-way local adaptation in plants sourced from brackish waters of both the Chesapeake and Hudson. In the first experiment (parental-generation), brackish-source plants demonstrated phenotypic buffering, a stress-induced version of phenotypic plasticity. When exposed to three salinity treatments (0 ppt, 6 ppt, and 12 ppt) applied after plants had sprouted, brackish-source plants buffered the effects of salt stress via increased vegetative growth in the form of many ramets and turions at the cost of small stature. By contrast, plants sourced from fresh waters of both regions grew tall in fresh water, but photosynthetic leaf material declined from the time of salt application (June) to the end of the experiment (September). The most severe salinity treatment, 18 ppt, was lethal to most individuals regardless of source habitat. Unfortunately, neither phenotypic buffering nor phenotypic plasticity sensu stricto was carried over via transgenerational plasticity (TGP), when turions were exposed to 12 ppt immediately upon planting (offspring generation). This early-development salt exposure proved lethal for some individuals and sublethal (had a negative effect on growth but did not result in mortality) for others, with turions either failing to sprout or growing a single shoot that was minuscule in stature. Parental-generation salt exposure only exacerbated these offspring effects, producing a non-adaptive TGP effect, resulting in even lower chance of sprouting, higher chance of mortality, and smaller stature. Evidence of local adaptation and acclimation to salinity only when exposure begins later in development suggests that populations have potential for resilience to saltwater intrusion (movement of saline water into fresh water) only if salinities do not remain elevated during the time of early plant development (spring/early summer) and across multiple seasons. In the event of prolonged salinity stress, much habitat (~10,000 hectares) that is currently mesohaline (5-12 ppt) but within the range of tolerance for V. americana will become unsuitable. In our spatial model of SAV persistence in the V. americana-dominated Upper Chesapeake Bay, high connectivity and high probability of SAV presence were found not only in the freshwater head of the Bay, but also in mesohaline (5-12 ppt) and oligohaline (0.5-5 ppt) waters near Middle River. Persistence of predominantly freshwater aquatic macrophytes in Middle River suggests that either 1) plants are locally adapted to brackish waters or 2) existing connectivity buffers the stress of low-quality habitat. Excess nitrogen, an anthropogenic environmental stressor that remains at high levels in Baltimore Harbor and other tributaries, was correlated with a decreased probability of SAV presence in the southern portion of our study area. As expected, low nitrogen, low salinity, and high landscape connectivity at the head of the Bay coincided with the highest predicted probabilities of SAV presence, particularly in the core of the one of the largest SAV beds in the entire Chesapeake Bay, the Susquehanna Flats.