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Green Turtle Herbivory Dominates the Fate of Seagrass Primary Production in the Lakshadweep Islands (Indian Ocean)

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Green Turtle Herbivory Dominates the Fate of Seagrass Primary Production in the Lakshadweep Islands (Indian Ocean) Vol. 485: 235–243, 2013 MARINE ECOLOGY PROGRESS SERIES Published June 27 doi: 10.3354/meps10406 Mar Ecol Prog Ser Green turtle herbivory dominates the fate of seagrass primary production in the Lakshadweep islands (Indian Ocean) Nachiket Kelkar1,*, Rohan Arthur1, Nuria Marba2, Teresa Alcoverro1,3 1Oceans and Coasts Program, Nature Conservation Foundation, IV Cross 3076/5, Gokulam Park, Mysore 570002, India 2Institut Mediterrani d’Estudis AvanÇats (CSIC-UIB), Miquel Marquès 21, 07190 Esporles, Illes Balears, Spain 3Centre d’Estudis Avançats de Blanes (CEAB-CSIC), Accés cala St. Francesc 14, 17300 Blanes, Girona, Spain ABSTRACT: Historical global declines of megaherbivores from marine ecosystems have hitherto contributed to an understanding of seagrass meadow production dominated by detrital path- ways — a paradigm increasingly being questioned by recent re-evaluations of the importance of herbivory. Recoveries in green turtle populations at some locations provide an ideal opportunity to examine effects of high megaherbivore densities on the fate of seagrass production. We conducted direct field measurements of aboveground herbivory and shoot elongation rates in 9 seagrass meadows across 3 atolls in the Lakshadweep Archipelago (India) representing a gradient of green turtle densities. Across all meadows, green turtles consumed an average of 60% of the total leaf growth. As expected, herbivory rates were positively related to turtle density and ranged from being almost absent in meadows with few turtles, to potentially overgrazed meadows (ca. 170% of leaf growth) where turtles were abundant. Turtle herbivory also substantially reduced shoot elongation rates. Simulated grazing through clipping experiments confirmed this trend: growth rates rapidly declined to almost half in clipped plots relative to control plots. At green turtle den- sities similar to historical estimates, herbivory not only dominated the fate of seagrass primary pro- duction but also drastically reduced production rates in grazed meadows. Intensive turtle grazing and associated movement could also modify rates of detrital cycling, leaf export and local carbon burial, with important consequences for the entire seascape. KEY WORDS: Fate of seagrass production · Herbivory pathway · Megaherbivores · Green turtles · Thalassia hemprichii · Cymodocea rotundata · Lakshadweep islands Resale or republication not permitted without written consent of the publisher INTRODUCTION levels of herbivory (Bjorndal & Jackson 2003, Heck & Valentine 2006). The drastic decline of marine megaherbivores from Green turtle Chelonia mydas populations have the world’s oceans over the last few centuries (Jack- recently begun to show surprising recoveries in some son 1997, 2001) has contributed to a general uncer- locations across their range (e.g. Hawaii, Mayotte, tainty of their functional contribution to the trophic Borneo, Lakshadweep; e.g. Balazs 2004, Seminoff dynamics of seagrass meadows. The resurgence of 2004, Broderick et al. 2006, Chaloupka et al. 2008, interest in re-evaluating the role of herbivory in sea- Ballorain et al. 2010, Fourqurean et al. 2010, Lal et al. grass dynamics (Thayer et al. 1984, Cyr & Pace 1993, 2010, Christianen et al. 2012) as a result of active Valentine & Heck 1999, 2001, Alcoverro & Mariani conservation efforts and the decline of large preda- 2004, Valentine & Duffy 2006) raises the question of tors such as sharks (Heithaus et al. 2008). Extant how these systems functioned under historically high high-density populations provide an excellent oppor- *Email: [email protected] © Inter-Research 2013 · www.int-res.com 236 Mar Ecol Prog Ser 485: 235–243, 2013 tunity to reconstruct the ecology of seagrass mead- different inherent evolutionary adaptations to with- ows when megaherbivores were abundant (Valen- stand herbivory pressure (Cronin & Hay 1996, Domn- tine & Heck 1999). In fact, recent studies on these ing 2001, Nakanishi et al. 2009) which could result populations are already throwing light on ecosystem- in habitat-wide compositional shifts under sustained level effects of green turtle herbivory that include herbivory — extreme rates of removal could even modification in seagrass biomass, structure and over- threaten meadow survival (Eklof et al. 2008, Four- grazing of meadows (Lal et al. 2010, Four qurean et qurean et al. 2010). At lower rates of offtake, it is pos- al. 2010, Christianen et al. 2012). However, in the sible that seagrass meadows and their dominant her- absence of direct field measures of herbivory, the bivores exist in a dynamic equilibrium between magnitude of the herbivory pathway in modifying offtake and production, determined by herbivore seagrass production fate remains unclear (see Prado feeding rates, movement patterns, plant growth and et al. 2007). composition, among others. In seagrass ecosystems not dominated by herbi- Green turtle populations in the Lakshadweep vores, physical agents (primarily marine currents) Archipelago (Indian Ocean) have recently under- mainly regulate the fate of primary production by de- gone major increases in shallow seagrass lagoons. At termining the proportion of in situ and ex situ decom- one lagoon (Agatti), high green turtle densities have position pathways (Duarte & Cebrián 1996, Cebrián persisted for over a decade (Lal et al. 2010), and these et al. 1997, 2000, Mateo et al. 2006). However, when numbers are gradually increasing in other lagoons. It herbivores are abundant, they can have important is difficult to speculate on what has triggered these consequences for nutrient cycling and leaf export changes but the increase has coincided with a local (Valentine & Heck 1999, Valentine et al. 2004). Herbi- ban on the hunting of turtles for oil, overfishing of top vores with low mobility tend to increase in situ de- predators such as tiger sharks (Heithaus et al. 2008) composition and carbon burial, as pre-digested plants and immigration of turtles from nearby regions in the are less prone to be exported (Duffy & Hay 1994, Ce- western Indian ocean in response to effective turtle brián et al.1997, 1998, Heck et al. 2008). In contrast, conservation programs (Broderick et al. 2006). These when widely ranging large herbivores (such as green high population densities provide an ideal context to turtles) are common, the bulk of leaf export is driven evaluate the importance of herbivory as a transfer by their movement (Hay et al. 1988). Thus, when the pathway for primary production in seagrass mead- herbivory pathway dominates, it can have profound ows with large feeding aggregations of megaherbi- consequences for the entire sea scape (Lundberg & vores. To estimate the extent of the herbivory path- Moberg 2003, Burkholder et al. 2011). way in these atolls we used direct measurements of In this context, it is critical to evaluate the magni- aboveground herbivory and production rates from tude and importance of herbivory towards the fate of 9 meadows with a range of turtle densities in the seagrass primary production. Direct field measures Lakshadweep archipelago. We hypothesized that of herbivory are only recently becoming available herbivory at these meadows would directly reduce and indicate that earlier indirect measurements may seagrass production. To test this hypothesis, we com- have considerably underestimated the herbivory pared primary production in meadows with different pathway (Prado et al. 2007). For instance, direct levels of herbivory pressure and validated these measurements of fish herbivory have shown that it observations with seagrass clipping experiments can represent 50 to 100% of primary production in that simulated turtle cropping rates observed in these some regions (Kirsch et al. 2002, Prado et al. 2007, meadows. Uns worth et al. 2007) compared with previous indi- rect estimates that concluded that only about 10% of primary production was transferred to herbivores MATERIALS AND METHODS (Cebrián & Duarte 1998, Williams & Heck 2001). Direct field measures have also helped identify clear Study area mechanisms, such as herbivore density, resource availability and feeding preferences, that influence The Lakshadweep Archipelago (Arabian Sea, herbivory rates in seagrass meadows (Vergés et al. Indian Ocean) comprises 12 atolls and submerged 2007, Prado et al. 2008), and how these drivers in - banks, with 36 islands covering a total area of 32 km2. teract will eventually determine the intensity and The islands are low-lying (<5 m above sea level) and persistence of seagrass herbivory (Williams 1988, occur between 8° to 12° N and 71° to 74° E at the Four qurean et al. 2010). Seagrass species may have northern end of the Laccadive-Chagos submarine Kelkar et al.: Green turtle herbivory dominates seagrass production fate 237 ridge. Seagrass meadows occur in shallow lagoons of marking these shoots in situ with a hypodermic nee- the Lakshadweep islands. The study was conducted dle (Short & Coles 2001, Prado et al. 2007). Briefly, over 2 yr (2010 to 2011) in the well-formed seagrass the length of each leaf per shoot was measured, the meadows of 3 different lagoons: Agatti (16.8 km2), number of leaves counted, and the sheath base Kadmat (20.9 km2) and Kavaratti (6.2 km2). Three marked with a needle. Only shoots that did not have seagrass meadows were selected in the Agatti pre-existing grazing marks were selected. After an lagoon, 4 in Kadmat, and 2 in Kavaratti lagoon, rep- interval of 3 to 5 d, total leaf length was again meas- resenting ca. 70% of the seagrass meadows of this ured
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