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Effects of Nitrogen Concentrations in Turtlegrass Thalassia Testudinum on Consumption by the Bucktooth Parrotfish Sparisoma Radians

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Effects of Nitrogen Concentrations in Turtlegrass Thalassia Testudinum on Consumption by the Bucktooth Parrotfish Sparisoma Radians MARINE ECOLOGY PROGRESS SERIES Vol. 286: 239–248, 2005 Published February 2 Mar Ecol Prog Ser Effects of nitrogen concentrations in turtlegrass Thalassia testudinum on consumption by the bucktooth parrotfish Sparisoma radians M. E. Goecker*, K. L. Heck Jr., J. F. Valentine Dauphin Island Sea Lab, University of South Alabama, 101 Bienville Boulevard, Dauphin Island, Alabama 36528, USA ABSTRACT: Terrestrial herbivores often preferentially consume plants that have higher nitrogen concentrations. In these circumstances, low nitrogen concentrations in exposed tissues would be an effective defense against herbivory. In marine environments, the relationship between nitrogen con- centration in plants and herbivore preferences has only recently been explored, and results are inconsistent. We examined preferences of the bucktooth parrotfish Sparisoma radians for the turtle- grass Thalassia testudinum with high or low nitrogen concentrations in both field and laboratory experiments. These species were chosen for study because (1) turtlegrass, the dominant seagrass in the Caribbean, is the primary food resource of the bucktooth parrotfish and (2) S. radians is known to be undeterred by the chemical defenses (i.e. phenolic compounds) and physical defenses (i.e. tough tissues) of T. testudinum. In field choice experiments, we found that S. radians consumed a greater proportion of T. testudinum shoots with high nitrogen concentrations than shoots with low nitrogen concentrations (68 vs 5%). Similarly, in laboratory experiments, S. radians consumed more T. tes- tudinum with high nitrogen than with low nitrogen concentrations (25 vs 5%). To determine whether S. radians used the color or shape of shoots as a basis for its preferences, we repeated laboratory experiments using an agar mixture with powdered T. testudinum leaves of either high or low nitro- gen concentration. S. radians again showed a significant preference for the high nitrogen food source. We, therefore, conclude that mechanisms for choice of high nitrogen food were most likely related to gustation and/or olfaction of chemical cues (i.e. nitrogen or phenols). KEY WORDS: Herbivory · Nitrogen concentration · Seagrass · Parrotfish · Phenolics Resale or republication not permitted without written consent of the publisher INTRODUCTION susceptibility to herbivore attack (Hay 1984, Steneck & Dethier 1994). Chemical deterrents such as phenolic Herbivores consume substantial quantities of pri- acids and condensed tannins are also commonly used mary production in most marine environments (Cyr & by marine macrophytes to reduce their palatability or Pace 1993, Valentine & Heck 1999, Shurin et al. 2002). increase toxicity to herbivores (e.g. Steinberg 1985, As a result, it is widely believed that marine plants Hay et al. 1987, 1994, Hay & Fenical 1988, Steinberg et have evolved both morphological and chemical al. 1991, Arnold et al. 1995, Targett et al. 1995, Hay defenses that reduce their palatability to herbivores 1996). While both morphological and chemical (Hay & Fenical 1988, Hay et al. 1994, Steneck & defenses of marine macrophytes have been studied Dethier 1994). Morphological defenses have been extensively, a third, incompletely studied category of studied extensively (e.g. Littler & Littler 1980, Littler et defenses against herbivory involves the reduction of al. 1983, Duffy & Hay 1990) and include concentrated nutritional quality (often measured by plant nitrogen compounds in cell walls that make tissues tough and concentration) of plant tissues vulnerable to herbivory indigestible, as well as alterations in form that reduce attack. *Email: [email protected] © Inter-Research 2005 · www.int-res.com 240 Mar Ecol Prog Ser 286: 239–248, 2005 Studies of terrestrial plant-animal interactions have tion efficiencies of S. radians (Targett & Targett 1990) shown that some herbivores selectively consume and their alkaline stomachs allow for dissociation of plants with high nitrogen concentration in their tissues protein-tannin complexes (Lobel 1981). (e.g. McNeill & Southwood 1978, Mattson 1980, Sparisoma radians does display strategies for deal- Schroeder 1986, Athey & Connor 1989, Minkenberg & ing with the low nitrogen content of turtlegrass. During Ottenheim 1989). It has, therefore, been suggested daylight hours, these fish feed continuously (Lobel & that some plants may reduce the nitrogen concentra- Ogden 1981, Robblee & Zieman 1984) on turtlegrass, tion of their tissues and thereby cause herbivore pref- which constitutes 88% of their diet (Randall 1968). erences to shift to other plants (Moran & Hamilton S. radians will increase evacuation rates with low 1980). This strategy is thought to be an effective nutritional foods (Targett & Targett 1990) and they defense against grazing because nitrogen is essential have specialized digestive systems where pharyngeal for herbivore growth and reproduction as well as the mills grind plant cell walls to release nutrients (Lobel & central role nitrogen plays in cell structure and genetic Ogden 1981, Randall 1968). coding (Mattson 1980). With morphological and chemical defenses of turtle- However, herbivores have strategies to deal with grass being ineffective against the bucktooth parrot- plants that have low nitrogen concentrations. Herbi- fish, and with known feeding behaviors associated vores can simply increase the amount that they con- with low nutrient food resources, we were able set up sume (compensatory feeding) or use specialized diges- a model situation for testing if nitrogen concentrations tive systems to cope with a nutritionally deficient food in plants specifically play a role in herbivore choice. To resource (Mattson 1980, Lincoln et al. 1982, Slansky date, few experiments have been designed to test this 1993). However, increasing the length of time spent and where preferential consumption of higher nitro- feeding could in turn increase herbivore exposure to gen plants has been documented, mechanisms and attack by predators. A simpler and more effective cues that would allow herbivores to make such a strategy for maximizing herbivore foraging efficiency choice remain unclear (Stephens & Krebs 1986, Day et would be to identify and preferentially consume al. 1998). Understanding what cues the consumer plants, or parts of plants, that have the highest nitrogen receives from prey, whether through ingestion or contents (Mattson 1980). through external stimuli, will also help in understand- In most western Atlantic tropical and subtropical ing plant defense mechanisms. seagrass meadows, the turtlegrass Thalassia tes- Two primary questions were addressed: (1) does tudinum is the dominant seagrass (Weinstein & Heck Sparisoma radians preferentially choose Thalassia tes- 1979). Morphologically, the flat, strap-like leaves of tudinum containing higher nitrogen concentrations turtlegrass (Zieman & Zieman 1989) are thought to be and if so, (2) do visual or other cues underlie this relatively tough. Turtlegrass also contains a mixture of choice? chemical deterrents within its leaves, including con- densed tannins (proanthocyanidins) (McMillan 1984), 6 different phenolic acids (Zapata & McMillan 1979), MATERIALS AND METHODS sulphated phenols and flavones (McMillan et al. 1980), and lignin. These compounds are thought to make Field based feeding preference experiments. Study turtlegrass leaves unpalatable and toxic to some herbi- sites: Experiments were conducted in 3 seagrass vores, and can also make proteins and carbohydrates meadows within the Florida Keys National Marine unavailable to herbivores (Thayer et al. 1984). In addi- Sanctuary (Fig. 1). The New Found Harbor (NFH) tion, relative to other marine primary producers, T. tes- (24° 36.925’ N, 81° 23.642’ W) site is an inshore reef- tudinum leaves are thought to be poor in nutritional associated seagrass bed approximately 3 m in depth. quality, with nitrogen concentrations that can be ≤1% NFH is a Sanctuary Preservation Area (SPA), in which (Thayer et al. 1984). no harvesting of marine life is allowed. This site is Within Thalassia testudinum meadows, the herbi- located just south of Little Palm Island (LP) and vorous bucktooth parrotfish Sparisoma radians, the the meadow is dominated by Thalassia testudinum. smallest species within its genus (average adult length The second site, Looe Key (LK) (24° 32.830’ N, 80 mm, TL, total length) (Randall 1968), is widespread 81° 23.642’ W), is also a SPA and is located 11.3 km off- and abundant (Lobel & Ogden 1981, Robblee & Zie- shore of Big Pine Key. This seagrass bed is behind a man 1984). The toughness of turtlegrass does not seem well-developed reef and is also approximately 3 m in to deter the strong jaws of the bucktooth parrotfish, as depth. It is dominated by T. testudinum, although evidenced by crescent shaped bite marks on many Syringodium filiforme is also present. The last site turtlegrass leaves. Potential chemical deterrents of was located just off the beach of LP (24° 37.258’ N, T. testudinum are ineffective in reducing the assimila- 81° 24.324’ W), bordering Big Pine Key boat channel. Goecker et al.: Effect of nitrogen concentrations in seagrasses on consumption by parrotfish 241 Fig. 1. Study site locations in Florida Keys, USA This site is not reef-associated, is dominated by T. tes- Statistical analyses: Treatment effects at each site tudinum and is shallow (1 to 2 m) with some areas were analyzed separately using t-tests, where days exposed during low tide. Sparisoma radians were were replicates. Sites were treated separately
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