Implications of conserving an ecosystem modifier: Increasing green turtle (Chelonia mydas) densities substantially alters seagrass meadows

Abstract

Ecosystem modifiers have the ability to significantly alter the ecosystem they inhabit sometimes with serious consequences for their own populations. We evaluated the ability of green turtles (Chelonia mydas) to modify seagrass ecosystems by their foraging activity. This study was conducted in a seagrass-dominated lagoon in the Lakshadweep Islands, Indian Ocean, where a stable high-density congregation of green turtles is present. We determined a gradient of turtle density in the lagoon and measured the intensity of turtle herbivory across the gradient. We then measured the impact of increasing grazing on seagrass structural parameters, growth and flowering along this gradient. Our results indicate that turtles substantially change seagrass meadow structure (canopy height, shoot length, width and density), reduce flowering and can potentially even cause changes in the species composition of the meadow. We discuss the implications of these results for seagrass ecosystem function, green turtle movement and human attitudes. When conserving ecosystem modifiers like the green turtle, any management strategy needs to include a detailed knowledge of the roles these species play in the ecosystems they inhabit.

Introduction

One of the most visible footprints of the Anthropocene (sensu Crutzen and Stroemer, 2000) is the dramatic decline of top predators and large herbivores. Reversing the alarming trends in the populations of these species has been the focus of much conservation attention. Emblematic species typically receive higher, and sometimes disproportionate conservation action for a variety of reasons, particularly because it is often easier to generate public policy and funding for their management. Such single-species conservation efforts are often justified with the reasoning that they are umbrella species or ecosystem keystones, and their protection implies an indirect protection of the habitats, processes and services they represent (Roberge and Angelstam, 2004, Simberloff, 1998). It has been suggested that keystone management efficiently combines both single-species conservation and ecosystem management since it presupposes detailed knowledge, monitoring and management of key species interactions and ecosystem processes (Simberloff, 1998, Simberloff, 2004).

The urgency of some conservation problems often permits scant regard for a fuller understanding of the role these species play in the systems they inhabit. Thus, keystone management often becomes a simple numbers game, where population numbers of the species in question is the sole measure of management success (Andelman and Fagan, 2000). When the keystone species being conserved is additionally an ecosystem modifier, increasing their densities could have potentially important implications for ecosystem structure and function (Van Aarde and Jackson, 2007), implications that are often left unexamined. The actions of ecosystem modifying herbivores like elephants, dugongs and sea urchins, allogenic engineers in Jones et al.’s (1994) classification, can modify community structure, change edaphic conditions, increase susceptibility to fire, and even trigger major shifts in ecosystem state (Aragones and Marsh, 2000, Caughley, 1976, Estes and Duggins, 1995, Laws, 1970).

Populations of the green turtle (Chelonia mydas) have declined several orders of magnitude on a global scale during the last few centuries (Jackson, 1997, Knowlton and Jackson, 2008, Thayer et al., 1984) due to direct off take and hunting of all life stages, fatal interactions with fisheries, boat strikes, degradation and loss of feeding and nesting habitats, and ingestion of synthetic material (Campbell and Lagueux, 2005, McCauley and Bjorndal, 1999, Seminoff, 2002). The IUCN Red List classifies the species as Endangered, and several regional and international efforts have focused on reversing its global decline. These efforts include the protection of nesting beaches, banning turtle hunting, installation of Turtle Excluding Devices (TEDs) on fishing gear and the creation of turtle hatcheries, among others (Hays, 2004, Mounsey et al., 1995, Troëng and Rankin, 2005).

The success of these efforts is critically linked to the protection of turtle feeding grounds, primarily seagrass meadows. While substantial research has focussed on understanding the feeding ecology of green turtles (Bjorndal, 1980, Bjorndal, 1985, McDermid et al., 2007, Moran and Bjorndal, 2007, Ogden et al., 1983), considerably less effort has been directed at understanding the impacts of this feeding on the seagrass meadows themselves (see however, Moran and Bjorndal, 2005, Ogden et al., 1980, Zieman et al., 1984). Increased turtle numbers beyond carrying capacity could significantly alter the structure and functioning of these important habitats (Moran and Bjorndal, 2005). It is vital to understand these interactions for a conservation strategy that protects the flagship along with the ecosystem.

Green turtles were among the dominant herbivores of seagrass meadows in the past (Bjorndal and Jackson, 2003, Jackson, 1997), but given their current declines, they rarely attain densities that can modify present meadow functioning. The current paradigm of the functioning of seagrass systems suggests that herbivory plays a relatively minor role, and the major fate of seagrass production is primarily governed by detrital trophic pathways (Duarte and Cebrian, 1996). However, new research is reevaluating the importance of herbivory as a structuring agent of seagrass meadows (Alcoverro and Mariani, 2002, Kirsch et al., 2002, Prado et al., 2007, Rose et al., 1999). Under high herbivore densities, the impact of intense grazing could seriously diminish the long-term sustainability of seagrass beds. Sufficient information already exists to suggest that historically close interactions with grazers have shaped many physical and chemical features of seagrasses as an adaptation to intense levels of sustained herbivory (Valentine and Duffy, 2006, Valentine and Heck Jr., 1999). Indeed, this close co-evolutionary relationship, coupled with evidence of ‘cultivation grazing’ where herbivores actively optimize the food quality of seagrass meadows through selective grazing techniques, indicates that mega herbivores are likely to have played a role in determining many of the life history characteristics of seagrasses (Valentine and Duffy, 2006). However, the impacts of herbivory (by species like sea urchins and dugongs) have also been observed to have detrimental effects on seagrass meadows, and may even result in seagrass meadow decline (Aragones and Marsh, 2000, Eklöf et al., 2008, Rose et al., 1999).

Our study was designed to determine if green turtles have the ability to significantly modify the structure of the seagrass meadows they inhabit. We conducted this study in the shallow coral lagoon of Agatti Island, Lakshadweep, Indian Ocean. Agatti has an exceptionally high density of green turtles that have persisted for several years in the clear and shallow seagrass-dominated lagoon. To determine the impact of green turtles on seagrass meadows we first (i) determined a temporally maintained gradient of turtle density across the lagoon, (ii) measured herbivory pressure (using herbivory assays) across this gradient and (iii) measured the impact of this herbivory pressure on seagrass structure across this gradient. Finally we discuss the implications of seagrass modifications for the management of green turtles as keystone modifiers, and of seagrass ecosystems as a whole.