Recovery of a cultivation grazer: A mechanism for compensatory growth of Thalassia testudinum in a Caribbean seagrass meadow grazed by green turtles

Abstract

Recovery of green turtles (Chelonia mydas), mega‐herbivores that consume seagrasses, is resulting in dramatic ecosystem‐wide changes as meadows are returned to a natural grazed state. The green turtle grazing strategy, with long‐term cultivation of meadows and high foraging site fidelity, is distinct from other terrestrial and aquatic mega‐herbivores and may affect seagrass compensatory growth responses. Identifying the mechanisms of compensatory growth responses to grazing is essential to understand the functioning of plant systems under natural grazing regimes. In a naturally grazed Caribbean seagrass ecosystem, we identify a mechanism for compensatory growth responses to grazing by evaluating relationships between Thalassia testudinum morphology and growth, grazing intensity, and canopy light dynamics in grazed and ungrazed areas. The morphological characteristics that explain variability in T. testudinum growth differed between grazed and ungrazed areas. In grazed areas, T. testudinum leaf linear growth, leaf area growth, and productivity:biomass (P:B) significantly increased as above‐ground biomass decreased; P:B also increased with shoot density. Mass growth in grazed areas exhibited an increasing trend with shoot density and was maintained above a threshold of 2.5 g dry mass m−2 above‐ground biomass. In ungrazed areas, trends for mass growth and P:B with above‐ground biomass and shoot density were opposite to those in grazed areas. In grazed areas, shoot density significantly increased with grazing intensity while above‐ground biomass decreased and leaf area index (LAI) was not affected. Light availability at canopy height was greater in grazed areas than in ungrazed areas, and canopy light attenuation increased with shoot density in grazed areas. Synthesis. Grazing removes above‐ground biomass, which increases light availability and stimulates leaf growth and turnover (i.e. compensatory growth). Shoot density increases with grazing intensity, maintaining LAI and canopy light harvesting potential. This maximizes the potential for leaf photosynthetic activity and provides the plant with the capacity to sustain mass growth and support a compensatory growth response to grazing. This study presents novel insight for assessing the underlying mechanisms of plant compensatory growth responses to cultivation grazing and proposes potential thresholds that may be used to evaluate the sustainability of in situ grazing pressure by a recovering mega‐herbivore.

Simulated green turtle grazing alters effects of environmental drivers on seagrass growth dynamics across seasons

“…It is likely such a tradeoff exists along a continuum, and our results suggest the possibility of an inflection point at which, following a cessation of grazing, seagrass would switch from prioritizing increasing biomass to prioritizing increasing photosynthetic surface area (i.e., leaf area index) as it re-grows. Though we are not able to evaluate the presence of such an inflection point from our current experiment, we hypothesize that this point would occur when seagrass shoots reach a sufficient height, size, or density to begin self-shading, as would be predicted under the leaf "self-thinning rule" (Westoby 1984;Enríquez et al 2019;Gulick et al 2021). Future research within grazing patches following green turtle abandonment will be particularly beneficial for increasing our understanding of how seagrass growth is driven by interactions between biotic and abiotic factors.…”

“…Grazed seagrass is unlikely to be similarly affected by self-shading, however. In the Greater Caribbean, green turtles create grazing areas in which blades are cropped (Bjorndal 1980), which results in both higher light availability and lower within-canopy light attenuation compared to adjacent ungrazed areas (Gulick et al 2021). A difference in self-shading, induced by the change in blade morphometry, could explain why leaf area index was affected by temperature in the reference treatment, but not in the clipped treatments.…”

“…Few studies have investigated effects of interactions between grazing and abiotic factors on seagrass growth and how responses may differ from those in ungrazed seagrass (Nguyen et al 2021); however, these interactions are likely to be important. For example, the importance of irradiance in driving production decreases following green turtle grazing (Gulick et al 2020), while at the same time the change in irradiance created by canopy removal provides a mechanism for the compensatory growth response in T. testudinum following grazing (Gulick et al 2021). In regions such as the Greater Caribbean, significant spatial overlap exists between areas where green turtles graze and where environmental conditions are conducive to high rates of seagrass growth (e.g., high temperatures and insolation, optimal salinity).…”

Intraspecific spatial segregation on a green turtle foraging ground in the Florida Keys, USA

“…Foraging green turtles exert pressure on seagrass densities and health over time-both positively through grazing (Gulick et al 2020(Gulick et al , 2021 and negatively by consuming large patches of seagrass (Heithaus et al 2014;Gangal et al 2021). Since the discovery of the large densities of green turtles in the Lakshadweep archipelago of India (Tripathy et al Gangal et al (2021) found that green turtle densities reached numbers above what seagrass beds on the foraging grounds can support.…”

An underwater Serengeti: Seagrass‐mediated effects on intake and cultivation grazing behavior of a marine megaherbivore

“…To evaluate the effects of T. testudinum morphology and leaf nitrogen content on green turtle grazing behavior, we first conducted rapid preliminary transect surveys (Figure 1b) across established grazed areas to determine if natural gradients in T. testudinum morphology existed. We focused our surveys of grazed areas in only shallow meadows (3–4 m), because water depth has a substantial effect on T. testudinum morphology in grazed areas (Gulick, Johnson, et al, 2021). The surveys indicated considerable variation in T. testudinum morphology across grazed areas, which informed the placement of camera arrays for sampling grazing behavior along natural gradients of seagrass morphological characteristics.…”