MARINE ECOLOGY PROGRESS SERIES Vol. 176: 291-302, 1999 Published January 18 Mar Ecol Prog Ser

REVIEW herbivory: evidence for the continued grazing of marine grasses

John F. Valentine*, K. L. Heck, Jr

101 Bienville Boulevard, Dauphin Island Sea Lab, Dauphin Island, Alabama 36528-0369, USA and Department of Marine Science, University of South Alabama, Mobile, Alabama 36688-0002, USA

ABSTRACT: Unlike the majority of marine , are believed to experience little damage from the feeding activities of marine herbivores. Based on our previous work, plus a review of the lit- erature, we suggest that this paradigm significantly underestimates the importance of seagrass her- bivory in nearshore environments. In this review, we provide evidence from over 100 publications, showing that grazing on seagrasses is widespread in the world's . Overwhelmingly, reports of grazing on seagrasses are based on observations, laboratory measurements, and bioenergetic calcula- tions. To date, few field experiments have been conducted to evaluate the importance of seagrass graz- ing in the nearshore environment. Of these, even fewer have considered the possibility that herbivores may stimulate rates of primary production of the role of belowground nutrient reserves in determining the impacts of grazers on seagrasses. We contend that the currently accepted view that herbivory plays a minor role in the energetics of seagrass habitats needs to be reexamined by measuring seagrass responses to grazer induced tissue losses in controlled field manipulations. Only then will we be able to determine the in~portanceof the seagrass-grazing pathway in marine food webs.

KEY WORDS: Seagrass . Herbivory . Waterfowl . Fishes . Sea urchins . Food webs

INTRODUCTION environments, grazing by coral reef fishes and inver- tebrates can cause shifts in macroalgal community Herbivores often greatly influence the productivity structure from dominance by highly competitive, fast- and abundance of plants in aquatic and marine envi- growing, edible to competitively inferior, slower ronments (e.g. Porter 1973, 1977, Lynch & Shapiro growing, but chemically defended algae (reviewed by 1981, Lewis 1985, Vanni 1987a, Mallin & Paerl 1994). Hay & Steinberg 1992). Similarly, gastropod grazing For example, in freshwater lakes, zooplankton graz- can alter macroalgal community structure in temper- ing can reduce the abundance of small or naked ate rocky intertidal zones by removing competitively phytoplankton , favoring the survival of larger dominant, fast-growing, more palatable species, phytoplankton species with gelatinous sheaths or which are then replaced by competitively inferior, other structures that reduce their vulnerability to slower growing, less palatable species (reviewed by grazing (e.g. Porter 1973, 1977, McCauley & Briand Lubchencho & Gaines 1981, Gaines & Lubchencho 1979, Demott & Kerfoot 1982, Vanni 198713). In marine 1982). In one of the most dramatic examples of herbi- vore impacts on primary producers, graz- ing can convert macroalgal kelp forests to grazer 'Address for correspondence: Marine Environmental Sci- ences Consortium, 101 Bienville Boulevard. Dauphin Island resistant coralline dominated algal pavements in ten?- Sea Lab, Dauphin Island, Alabama 36528-0369. USA. perate and boreal settings (reviewed by Lawrence E-mail: jvalentiQjaguar1 .usouthal.edu 1975).

O Inter-Research 1999 Resale offull article not permitted 292 hlar Ecol Prog St

The seagrass-detritus paradigm 1997). In fact, f~eldpalatability testing using both sea- grasses and marine macroalgde has found that sea- In contrast, marine vascular plants or seagrasses, grasses are of intermediate palatability among several which are common in coastal waters along every conti- species of algae offered to marine herbivores through- nent except Antarctica, are reported to experience out the and Indian (e.g. Hay very low levels of herbivory because their leaves are 1981, 1984a, b, Lewis 1985, hlacIntyre et al. 1987). If thought to be of poor nutritional value, owing to high true, seagrasses are likely to contribute to the diets of C/N ratios (e.g. Bjorndal 1980, Duarte 1990, Lalli & many of marine herbivorous fishes in some significant Parsons 1993, Valiela 1995), and the inability of most way. grazers to digest cellulose (Lawrence More importantly, we and others have shown, from 1975). Current levels of seagrass herbivory are also field observations and short-term experiments, that thought to be low because of the historical overhar- the variegated sea urchin Lytechinus variegatus (La- vesting of larger vertebrate herbivores (e.g. green marck) consumes from 50 to 200% of the aboveground turtles, dugongs, manatees, fishes, and waterfowl; seagrass biomass produced in some areas of the east- Randall 1965, Heinsohn & Birch 1972, Lipkin 1975, ern and Caribbean Sea (Moore et Charman 1979, Bjorndal 1980, Kiorboe 1980, Jacobs et al. 1963, Camp et al. 1973, Greenway 1976, 1995, al. 1983, Thayer et al. 1984, Dayton et al. 1995). As a Zimmerman & Livingston 1976, Bach 1979, Valentine result, the amount of seagrass production entering & Heck 1991, Heck & Valentine 1995). At densities of food webs via grazing is believed to be small, usually 10 ind. m-2, L. vanegatus can reduce turtlegrass habi- less than 10 % of annual net aboveground primary pro- tats to barren unvegetated substrates from fall through duction, with most macrophyte production thought to early spring (Valentine & Heck 1991). If grazing is per- enter food webs through the detrital pathway (e.g. sistent throughout the winter and spring, sea urchins Fenchel 1970, 1977, Kikuchi & Peres 1977, Nienhaus can reduce these vegetated habitats to permanently & Van Ierland 1978, Kikuchi 1980, Thayer et al. 1984, barren unvegetated substrates (Heck & Valentine Nienhaus & Groenendijk 1986, Zieman & Zieman 1995). In summer, turtlegrass persists under severe 1989). Consequently, investigations of the factors con- grazing pressure and regrows to levels that either trolling seagrass growth and biornass have empha- equal or exceed the standing crop of nearby ungrazed sized the primacy of nutrient supply (e.g. Patriquin turtlegrass. The apparent mechanism by which turtle- 1972, Short 1987, Powell et al. 1989, Fourqurean et al. grass overcomes the effects of this grazing is to 1992, Short et al. 1993), light availability, and/or increase the production or recruitment of new shoots in physical factors (e.g. Patriquin 1975, Backman & Bari- the grazed area rather than to increase the production lotti 1976, Dennison & Alberte 1985, Thom & Albright of existing shoots (Valentine et al. 1997). Similarly, the 1990). sea urchins Tripneustes ventricosuscan, and Diadema antillarum did, until recently, consume large quantities of seagrass in some Caribbean settings (e.g. Ogden et COUNTER EVIDENCE al. 1973, Lilly 1975, Vicente & Rivera 1982, Keller 1983, Tertschnig 1984 in Tertschnig 1989). Although it was There are, however, few actual tests of this para- once thought that grazing on seagrasses was predomi- digm, and there is an existing body of evidence which nantly a Caribbean phenomenon (Ogden & Zieman shows that its underlying assumptions need reevalua- 1977, Ogden 1980, Ogden & Ogden 1982), observa- tion. For example, several investigators have provided tions elsewhere show that sea urchins also consume evidence that nitrogen concentrations in seagrasses significant amounts of seagrass in the tropical Pacific are similar to those of algae (e.g. Lowe & Lawrence and Indian Oceans (Bak & Nojima 1980, Kirkman & 1976, Lobe1 & Ogden 1981, reviewed in Thayer et al. Young 1981, Hulings & IClrkman 1982, Verlaque & 1984). There is also substantial evidence that detrital Nedelec 1983, Jafari & Mahasneh 1984, Larkum & seagrass leaves are an even poorer source of nutrition West 1990, Klumpp et a1 1993, Jernakoff et al. 1996). (i.e. have higher C/N ratios) for consumers than are In tropical settings where fishing pressure is low, living leaves (Klumpp & Van der Walk 1984), as sea- herbivorous fish, not sea urchins, are the dominant grass detritus resists decay, requinng long periods of herbivores (e.g Ogden 1976, 1980, Hay 1981, 1984a, conditioning time before detritivores can use it (Harn- Carpenter 1986, but see Jackson 1997). More than 30 son & Mann 1975, Zieman 1975, Fenchel 1977, Thayer species of Caribbean fishes, predominantly parrot- et al. 1977, Rice 1982). fishes and surgeonfishes, have been found with sea- In addition, many herbivorous fishes are 'extreme' grasses in their guts (Randall 1967, McAfee & Morgan generalists that feed on vegetation in proportion to its 1996, Lewis & Wainwright 1985, but see Hay 1984a). abundance (Ogden 1980, Hay & Steinberg 1992, Hay It is likely that even more species draw nutrition from Valentine & Heck: Seagrass herbivory 293

these plants, as investigators have typically considered areas. We have so far emphasized the importance of the presence of seagrass leaves in the guts of fishes to sea urchin and fish grazlng on seagrasses, but several be incidental intake associated with the capture of ani- species of waterfowl have also been shown to consume mal prey (e.g. Thompson 1959, Carr & Adams 1973, large quantities of seagrass production (both above- Bell et al. 1978). When seagrass leaves are isotopically and belowground) during their seasonal migrations labeled or fishes have been presented with seagrass in through subtropical, temperate and boreal estuaries laboratory studies, it has been found that seagrasses (e.g. Charman 1977, Wilkins 1982, Tubbs & Tubbs leaves can contribute to fish growth (e.g. Conacher et 1983, Baldwin & Loworn 1994, Michot & Chadwick al. 1979, Montgomery & Targett 1992). Using stable 1994, Mitchell et al. 1994). In addition, green turtles isotopes, Fry et al. (1982) found that seagrasses and Chelonia mydas (Linnaeus) and sirenians (manatees benthic algae contributed significantly to the diets of and dugongs), which are still abundant in some areas, many fishes in the seagl-ass beds of St. Croix, USVl. Fry are intense seagrass grazers (Heinsohn & Birch 1972, & Parker (1979) also found that seagrasses and other Spain & Heinsohn 1973, Lipkin 1975, Heinsohn et al. benthic plants contributed significantly to the diets of 1976, Anderson & Birtles 1978, Nietschmann & Nietsch- and fishes in some areas of Texas. mann 1981, Marsh et al. 1982, Ogden et al. 1983, Nishi- In some locations, fish grazing on seagrasses is so waki & Marsh 1985, Lanyon et al. 1989, Nietschinann intense that 'halos' are created and maintained within 1990, Provancha & Hall 1991, de Iongh et al. 1995, seagrass habitats at the base of coral reefs (e.g. Randall Preen 1995). These large herbivores can have even 1965, Ogden & Zieman 1977, Hay 1984a, McAfee & greater impacts on seagrass productivity and abun- Morgan 1996). Not all foraging in and on seagrasses is dance than sea urchins or fishes (Zieman et al. 1984). near the base of coral reefs, however (Ogden & Zieman All of the examples cited above show that seagrass 1977). While many herbivorous fishes seek shelter on herbivory, although probably reduced in a historical coral reefs at night, they commonly forage In nearby context, continues to represent an important and seagrass habitats throughout the day (Randall 1965, underestimated trophic pathway in many areas, and Ogden & Zieman 1977, Zieman et al. 1984, McAfee & not a highly localized anomalous event. Morgan 1996). For example, the Scarus gua- camaia and S. coelestinus have been reported to move up to 500 m inshore from coral reefs to feed (Winn & SEAGRASS-HERBIVORE INTERACTIONS Bardach 1960, Winn et al. 1964).Juvenile and smaller species of parrotfish also feed on seagrasses away from If this view is correct, how do seagrasses persist in the reef (Ogden & Zieman 1977, Handley 1984, MacIn- the face of such grazing pressure? We believe that part tyre 1987, McGlathery 1995, McAfee & Morgan 1996). of the answer lies in the unrecognized potential of Once large enough, many juvenile fish abandon struc- seagrasses to compensate for grazing losses, and the turally simpler seagrass habitats for more structurally belowground location of much seagrass biomass. Dur- complex coral reefs where it has been hypothesized ing the summer months we have shown that turtle- that they find increased protection from large piscivo- grass responds to sea urchln grazing by increasing the rous fishes (Springer & McErlean 1962, Ogden & Zie- production of new shoots, which leads to increased man 1977, Dubin & Baker 1982, Handley 1984, Car- area1 aboveground primary production (Valentine et penter 1986). These observations suggest that the flow al. 1997). Because of the increased production of new of energy from seagrass habitats to coral reefs can be shoots, aboveground biomass in grazed areas does not substantial, but quantitative estimates are constrained change when compared to nearby ungrazed plots dur- by the limited amount of information on coral reef food ing the growing season. We suggest that this increased webs (cf. Polunin 1996). turnover of leaf material allows seagrasses to compen- Investigators have used tethering, stable isotope, gut sate for tissue lost to herbivores and enables seagrass content studies, and reconstructive sampling tech- to persist during intense grazlng (Valentine et al. niques to show that seagrasses are readily consumed 1997). Since new shoots are produced only at by fishes, at times in large quantities, in some areas of apices (Tomlinson & Vargo 1966), we hypothesized the Mediterranean Sea, the Indian and Pacific Oceans that sea urchin grazing should also lead to increased (Kirkman & Reid 1979, Hay 1981, 1984a, b, Klumpp & belowground production (Valentine et al. 1997). Our Nichols 1983~1,b, Lewls 1985, Nlchols et al. 1985, data suggest that focussing solely on seagrass biomass Nojima & Mukai 1990, Cebrian et al. 1996a, b, Pinto & without accounting for the material produced between Punchihewa 1996, Marguillier et al. 1997). In virtually sampling periods can lead to large underestimates every study seagrass leaves were readily consumed by of the amount of seagrass consumed by herbivores herbivores, thereby demonstrating the susceptibility of (cf. Jacobsen & Sand-Jensen 1994, Sand-Jensen et al. seagrasses to herbivores across broad geographic 1994). 294 Mar Ecol Prog Ser 176: 291-302, 1999

Table 1. Summary of selected studies or reports of herbivory in seagrasses. W: waterfowl; U: urchin; G: gastropod; C: ; F: fish; R: reptile; M: mammal

I Grazer Seagrass, location, study type Description of results Source I Branta bemicla bemicla (W), Zostera noltij and Z. marina. Solent. England. Large reductions in seagrass area1 coverage Tubbs & Tubbs Anas penelope (W), Anas Field study, percent cover recorded at 5 attributed to brent geese feeding. (1983) crecca (W) stations. Exclosures used to monitor seagrass change due to grazing.

B. bemicla (W), A. dcuta (W). 2. noltii and 2. marina. Dutch Wadden Sea. An estimated 1426 kg DW of seagrass (-50% of Jacobs et al. (1981) A. penelope (W),A. Field-based bioenergetic study and field ex- all SAV production) consumed, mostly by A. acuta platyrhyncha (W) periment where change in submerged aquatic and A. penelope. vegetation (SAV) shoot density, blomass, and percent cover were monitored.

B. bemlcla (W). Anas Zostera japonica and Z. marina. Boundary Bird density positively correlated with SAV Baldwin & americana (W),A. platy- Bay, British Columbia. Collections and field distnbutlon. Dabbling ducks and geese consumed Loworn (1994) rhynchos (W).A. acuta (W) based bioenergetlc study. Above- and below- some 362 t of Z. japonjca leaves and ground standing stock were monitored. Water- (-50% of aboveground and 43% of belowground fowl use days were estimated. Some birds were biomass) at the study site. Lesser amounts of collected and esophagus contents recorded. Z. marina consumed.

I Aythya arnencana (W) Halodule wrightil Lower Laguna Madre, TX. Rhizome biomass was 75% lower in grazed areas Mitchell et al. Two years of field collections and 1 experi- than where grazers were excluded. When rhizome (1994) ment at 3 sites were used to assess impacts of biomass was grazed below 0.18 g DM" core-' (at redhead ducks on SAV biomass. '4 of the sites), grass did not recover.

R. bernicla (W).Anas Zostera noltjj and Zostera manna. Dutch Brent geese and widgeon reduced aboveground Madsen (1988) penelope (W).A. crecca (W) Wadden Sea. Field surveys plus an exclosure biomass some 30% faster than In areas where experiment were used to quantify impacts of grazers were excluded. Belowground biomass in wildfowl grazing on seagrass biomass. grazed cages was 48% lower than in ungrazed plots.

Cygnus olor (W),Anas Zostera marina. Lake Grevelingen, SW An est~mated7.5% of Zostera manna product~on N~enhuis& penelope (W),A. platyrhyn- Netherlands. Field-based bioenergetic study consumed by waterfowl and a s~nglespecles of Groenendijk chos (W), A. acuta (W), A. and laboratory experiment. isopod. (1986) creeca (W). Aythya ferina (W), Branta bernida (W), Fulica atra (W),ldotea chelipes (C)

Branta bernicla hrota (W), Zostera sp. Strangford Slough. Northern Grazing led to faster rates of seagrass loss than Portig et aL (1994) Anas penelope (W) Ireland. Field study. The impact of grazers was occuning due to weathering in ungrazed was documented by monitoring changes in areas. Belowground biomass was 48% lower in seagrass biomass at the study area along with grazed plots than measured in ungrazed plots. the use of excluston cages in grassbeds wtth uniform coverage.

Aythya americana (LVl Halodule wrighti~.Chandeleur Sound, LA. Waterfowl grazing was found to reduce above- Michot & Chad- Field monitoring of seagrass biornass to ground and belowground biomass by 90 and 49% wick (1994) document the impact of waterfowl grazing on respectively. seagrass.

Lytechinus variegatus (U) Zhalassia testudinum. Miskito Cays, Sea urchins were estimated to consumed some 0.5 Vadas et al. (1982) Nicaragua. Laboratory measurements, field g DW per urchin d-' of seagrass However, gut collections and observations Feeding contents indicated that 40% of this urchin's diet preferences determined by turning over was detrital turtlegrass. Less than 5% of the diet urchins. Urchin gut contents examined at was Live grasses. l station.

L vanegatus (U),Spansoma testudinum. Kingston Harbour, 5 species of fish found to feed on both hve and detrital Greenway (1975, radians (F). Archosargus Jamaica. Laboratory measurements, field seagrass along wth algae and cruslaceans. Only the 1995) rhomboides (F), Monocanthus sampling, stomach content analysis, and field sea urchin Lytechinus and the bucktooth parrotfish S. setiferus (F), Acanthurus experimentation to estimate herbivory on radians were found to feed predominantly on sea- chjrurigus (F). Sphaerojdes grazers on seagrass. grass.Lytechinus was estimated to consume some spenglen (F).Acan- 49% of the SAVleai tissue producedeachday. A thostrac~onquadricor n~s(F) small fraction of ths production was consumed by fishes. L. variegatus (U) 7halassla testudinum. Offshore grass beds of Camp et al. (1973) west Florida. Field observations and An episodic settlement of sea urchins led to measurements signif~cantreduct~ons of seagrass coverage Crazlng was found to have denuded an estunated 20 ha area of seagrass habitat. L. variegatus (U),Tripneustes Thdassia testudinum. Discovery Bay, KeUer (1983) venMcosus (U] Jamaica. Field experiment tested for Tripneustes grazing had a hlghly significant effect intraspecific and interspecific competition on seagrass biomass in enclosure treatments. between 2 species of urchins. Aboveground Lytechinus had a moderate effect on seagrass biomass within cages was used to document biomass. the effects of urchin manipulations. Valentine & Heck: Seagrassherbivory 295

Table 1 (continued)

Grazer Seagrass,location, study type Descript~onof results Source

L vanegatus(U) Thalassia testudinum. Biscayne Bay,FL. Urchlns ingested decayed leavesat a signif~cantly h4ontague et al. Laboratoy est~mateof sea urchin ingestion hlghcr ratc than whcnfed grccn Icavcs. No cvi- (1991) rates and preferences when fedlive seagrass dence of a sign~f~cantpreference for decaycd and scagrdss detritus. leaves over green ones was found.

L. vanegatus(U) Tlialassia testudinuni. Card Sound,FL. A large populationof sea urch~nsconsumed all ben- Bach (1979) Observations. th~cplants ~na scvcral hectare area of Card Sound.

Trlpneustesgratilla (U), Tlialass~ahemprichil. Bolinao, Phillippines. Preferences testsshowed TI-jpneusteschose live Klumpp et al. Salmacls sphacro~des(U) Field and laboratory measurementsof sea urch~n SAV alternativefood choices Salnldcisconsumed (1993) consumpt~onof seagrass biomass. Food pref- equal quantltlesof all species. Both urchins crcnces for several plant species alsoexamined. efficiently digested and absorbed seagrass (>60°L).Est~mates of total SAV consumption by both sea urchins was 240 to 400 g D\V m -' d ', an average of -17''~~of SAV produced with a range from 3 to 100'';. of SAV production.

Paracentroluslividus (U) Posidonia oceanica.Mediterranean Sea. Field Loss of seagrass biomass was directly proportional Klrkman & Young experimentat~onused to determine grazing to grazing intens~ty. (1981) impacts onseagrass biomass, shoot density. and production.

Astropyga rnagnilicd (U) Zostera marina.Tornioka Bay, Amakusa, A seagrasspatch was reducedfrom -71 to <3 m2 Bak & Nojirna Japan.Eelgrass patch size, density and in 3 mo by grazing. Urch~nstomachs were (1980) biomass used to document the impact of a completely full of seagrass. No other plantswere sea urchin aggregationon seagrass density. observed.The seagrass standingcrop decreased Urchin gut contentswere recorded as well. from 7789 to 375 g DW.

Heliocidar~serythrogramrna Posidonia australis. Botany Bay,A~Strdll

Tripneustes grat~lla(U) Halophila stipulacea. Sinai, Northcrn Red Sea Heavy urchln grazing was recorded on seagrasses L~pkin(19791, and the Jordaniancoast of the Gulf of Aqaba. at depths rdnglng from 5 to 9 m. Gra~ingon sed- Bouchon (1980), Obsenrational. grass was subsequentlyverified by gut content Huljngs & Kirkman analysis. (1982),Jafari & hlahasneh (1984)

Ternnopleur~smlchaelsenil Cockburn Sound, Warnbro Sound, Australia. In Cockburn Sound,seagrasses were grazed by Cambridgeet al. (U! F~eldsampling and saagrass mappingwere locally abundant Temnopleurismchaelsen~~. Most (1986) used to document urchin denudation of a heavy damagcwas localized Where grazlng was seagrass habitat. heavy, plants hadnot recovered 2to 4 yr lalc?r. Urchins Invaded a second slte, reduc~ngrema- nents of one healthy seagrass meadow to bare sand. Jntensc grdnngwas noted In fall of 3 different years.Outbreaks were also rcported from a third site, where sea urchins removedall of the leaves in deeperportions of a seagrass bed.

Tectura deplcla (G) Zostera manna. Monterey Bay,CA. Lab experi- Growth rates, carbon reserves, root prol~fcrat~on, Zmmermanet al. ment. Zoslrra transplantedinto pldstic and net photosynthesis of grazed plants were (1996) pots, at natural dens~ticsot llmprts wrrc main- 50 to 80%:.lower than on ungrazed plants. The tained on 8 plants while 8othrrs werekept carbon allocated to thc roots of un<]razcclpldnls grazer free. Sedgrassgrowth was determined was 800';. higher for unqrazedplants than for wcckly along wlth total lea! length. At thc end grazed plants. L~mpetgrazlng induced carbon of the experiment, plantswere harvested and l~mitationIn eelgrdss growing in an otherwise analyzed for biomass (shoot,rhizome, root), I~ghtreplete env~ronment. rates ol leaf photosynthesis, respiration,and sucrose enzymesu'rrc measured in leaves and shoots. plus protein and sugar contents. Chloro- phyll a was extracted from Leaf segments.

Littorina sitkana [G), Zoslera marina. l7~rnbekLagoon, AK. Eelgrass was found to be incorporated intothe McConnaughey & Marganteshelicjnus (G), Samplingand '-'(::''C analysis. local food chain through herbivoq' by at least 7 McRoy (1979) Lacuna varicgata [G).Tel- species. messus chieragonus(C), MI- crocottus sellaris(F), Bran ta canadensis(M'). Anas CdrO- linel~sis(W), ilnas acuta (W)

(Table continuedoverlrafl Mar Ecol Prog Ser 176: 291-302, 1999

Table l (continued)

Grazer Seagrass, location, study type Descnption of results Source

An~p~thoespp. (C') Syringodlum. F~jiLaboratory ddctcmiinations Init~allyamphipods f~dat the top of the leaf. Mukai & lijima of ~ngestionrates of manatee grass. On6' day later the)' madr nests from frdgments (1995) of grazed rjrdqs Grd7lnq rates ranged from 1 7 to 26.4 mg LVW ind. ' d-'. L's~nga carbon budget approach, the authors est~matcvlthat the amphi- pods graecd of the matrrial produced and further asslm~lated' of it.

Monocanthus chinensis (F) Posidonia occdnicd. Quibray Bay. Botany Bay, Gut analysis showed fish ate SAV, along with Conacher et a1 New South Wales. Stomach analysis dnd I~c*ld 5 spp. of algae, crustacrans, and other inverte- (1979) sampling. "C labeled seagrass used to assess brates. Seaqrass and amphipods were most seagrass ass~m~lationby fishes. abundant in fish guts. b.Iicroscopic examlnatlon of Ingested plant matrnill suggested that plants were untouched. (i.e no cell wall damage obsenredl. However, radioactive labrling showed that -22':,. of labclrd SAV was in the liver and gut wdll of the fish, 32 to 33'',-,in thc feces. The remaining ldhel may have been In other tissues. This is siyn~flcant as ~tshows that m~croscopicexamination of the cell walls does not necessarily provide a complelr picture. The actual ";! of SAV production remc~ved was low.

Monacanthus chinensis (F), Posldonia australis. Port Hack~ng,Neiv South Leatherjackets dominated the fish cornrnunlty, Bell et al. (1978) Meuschenia freycineti (F). Wales. Field sampling and stomach contents. averaging 26'',0 oi the number and 34% of the Meuschenia lrach ylepis (F) The entire fish community In a 400 m? area biomass. Seaorasses Ingested were small pieces of P a~lstrdliswas collected twice each in 2 leaf material which were covered with epibionts seasons. Stomachs of all leathejackets were i\/l freycineli cons~stenllyblt off pieces In neat dissected and the contents denti if led.The sem~c~rcularbltes Juveniles of all spcries of fed relative percentages of food items was deter- pnnc~pallyon encrusting l~stedabove mined. Rectal items were identified using with little seagrass being present. Microscopic microscope to determine whlch items were rectal contents from several ind. of each species used as food. found that Posldonla was undigesled.

Monacanthus ciliatus (F) Thalassla teslud~numApalachee Bay. FL These flsh fed on a w~devanety of prey, howt~vcr. Clements & Stephanolep~shispjdus (F) F~eldsampllng and stomach contents of f~lef~shseagrass and ~nvertebralesaccounted for 80", of Livingston (1983) collected over a 9 yr period the stomach contents As f~shgrew, the dietary Importance of sedgrasses and associated cp~fauna lnrreased Approx~mately'2 of the drct of larger f~zhrswas Thalass~aThe pdttern was the same for both specles of f~lef~shc>\The ~nc~denceof SAC' In the d~etsnf Monocanrhus was greatest In late summer and early fall co~ncldrntw~th peak SAV product~v~tyThe ~nc~drnrrof SAV In St.ephdn~le[~dsIncreased brturrn summer and fdll

Hyporharnphus un~fasciatus Ruppla rndridrna and Halodule wrighiii Volume of SAV in gut -501,in large hdlfbcaks. Carr & Adnrns (F) Crystal Hlvrr, FL. Shallow water fish collcrted (1973) w~tha bay In approximately 1 m of water.

Hyporhamphus melanochir Zostera muelleri and Hrterozostera tasrnanica. During the day green eelgrass t~ssuewas In the Robertson & (F) Cirb Point, M'r:stern Port nay, and Duck Point, guts of 93'!!. of thr fish, making up almost 70".( of Klumpp (1983) Corner Inlet, Australia. Field sampling and the total vol~lrne.Insects, drnphrpods, and shnmp stomach contents. larvae made up most of th~rerna~ning food. Amph~podswcrr far more important pry at n~ght. Eelgrass tissue \%,asconsumed by ' I of f~shand was only 18' ., of total volumc at r~~ght.All celgrdss matrrial In the guts wdr macerated by pharyngeal t~.eth.Eelgrass In the fort>gut was undigcstrd, while matcna: 1t1 the hindgut wds colorlrss. bllcroscopic eu.lminatron of the matenal found most plant cells were empty.

Lagodon rhomboldes (F) Zostera manna. Field sarnpllng and laboratory P~nf~shfound to assimililte a substantial portton of btoenergetlc and rad~oact~velabeling study, the orgdnic materlal from cclgrass, but \r.~thless Pinfish (>65mm SLI were fed diets of either efficirncy than . Spcc~tlcgrowth rates of eelgrass or frozen grdss shrimp. Ass~milation p~ntichfed grass shrimp partially substitutctl w~th efficiency for pldnts (either eelgrass or algae) elthpr eelgrass or di!fesl~ble carbohydrates were and shnrnp and labeled seagrass. not significantly tl~ffrrentfrom growth rates when fr-rding solelv on shrimp. P~nfishappeared to increase feed~ngralcs when offerwl low calorie seagrass Valentine & Heck: Seagrass herblvory 297

Table l (continued)

Grazer Seagrass, location, study type Descrlptlon of results Source

Sparrsonla rubr~prnne, Thalassra testudrnum Came Bow Cay, Brllze. Each study found that herb~vorousf~shes readily Hdv 1981, Lews Spdrrsoma chrysoptcrum F~eldtethering study uslng clean freshly col- consumed seagrass leaves but the lntenslty varied (1985) lected plecrs of T. tcstudlnum blades along according to coral reef hab~tatand depth Lew~s with algal species tound that tethered Thalassra was entlrely consumed by 2 parrotf~shSpdr~somarubr~plnne and Spansoma cl~rysoplcrum Lew~salso found that Thalassla was among the preferred sources of food durrng fecdrng tr~als

Scarus spp (FI. Spal-lsoma Thalassia trstudrnum, Halodule wr~ghtriUS Parrotf~shtotally consumed seagrass patches Randall (1965) spp (F),Acanthurus spp (F) Vlrgln Islands. Flfld expenment, stomach transplanted into a halo zone next to a coral reef content and obscrvat~onThree separate trans- Parrotf~sh(Scarus and Spansorna) all hecm to feed plantat~onsof mlxed plots 7. testudlnum and to some degree on the grass; Scarus guacamala H wrrghtlr were placed into a halo zone next had 95";, of the gut volume f~lled~11th Halodule to a coral recl used to assess the lmpact of her- Acanthurus chrurugrs and A. bahamensrs had 40 blvores on scagrass abundance In addltlon, an and 80% gut volume filled w~thseagrass. art~f~clalreef was bullt In a mlxed turtlegrass and H wngh111 hab~tat

Scarus guacarnla, Thalassra tesludrnum St Crouc, USVl Leaves collected closest to a reef showed b~tes Ogden & Zleman Spar-rsoma radians (F) Sampling Seagrass leavtls collected and f~sh result~ngfrom a populat~onof large parrotf~shes (19771 bltes marks ident~f~eddlong a transect runnlng (Scarus guacama) whereas the statlons 20 and from the base of a coral reef lnto an adjacent 60 m from the reef had bites characteristic of seagrass hab~tat Sparrsoma radians. The statlon 4 m from the reef showed mixed feedlng

Scarus cro~censls(F], Synngod~umfiliforme and Thalassia tes- Each specles of seagrass was heavily grazed but Tnbble (1981) Sparrsoma aorofrenatum (F), ludrnum. San Blas Islands, Panama. F~eld herblvory on these grasses was vanable spat~ally Acanthurus chiurugus (F), tethering study mcasured both feeding A bahlanus (F) selectlv~tyand intens~ty

Scarid and siganld flshes Enhalus, Thalassla hempnchil, Halodule All samples of Thalassla and Cymodocea had blte Ogden & Ogden unrnervrs, C'ymodocea rotundata, Syrrngodrurn marks At one slte approx~mately30 to 40°t3of (1982) isoetlfolium Palau, \Yestern Carolina Islands leaves of all species except Enhalus, had at least 1 F~eld-basedmonltonng. bite taken Enhalus had b~temarks on at least 75",-,of blades.

Tr~chechusrnanalus (M) Syringodum frhforme. Cape Canaveral. FL. Graz~ngled to s~gnlficantreduct~ons in seagrass Provancha & Hall F~eldexperi~nentat~on percent cover, and coverage, biomass and leaf length Manatees (1991) aboveground blomass used to document were hlghly aggregated but thelr d~str~butlonwas herbwore lmpact on seagrass pos~tlvelycorrelated with the Syrrngodium and Halodule denslty

Dugong dugong (M) Halodule uninenlrs Nang Bay, Moluccas. Dugongh were found to remove some 75% of de longh et al. East Indonesia Observat~onand biomass the belowground b~omassIn the upper 4 to 5 cm (1995) monltonng of sediment. Vegetation b~omassr~covered to nearby amb~entlevels In just 4 to 5 rno following grazlng dunng the wet season, no such recovery was noted dunng the dry season.

Dugong dugong (M) Zoslera caprlcorni, Halophlla ovalrs and Dugongs appear to spend most of the~rtlme Preen (1995) Halophrla unrnervrs. Moreton Ray, east grazlng In one area, shoot dens~ty,aboveyround Austral~a.Aerlal dnd boat sun.c>vs,monitoring biomass and belowground b~omasswere reduced along w~thfield cxpenments used to docunient by O5,73 and 3lUt,respecllvely over 3 5 mo dugong grdzlng on seagrass habltats Grazlng Impacts wprp variable, in one drea shoot dens~tywas reduced by 85"- In 12 d, 95"., In 17"0 In another area b~ornasswets reduced by 960A8 (aboveground)and 71'4 bbclowground

Chelonra rnydas (R) Thalassra tesludrnurn. Great Igudna, Bahamas. Turtles grazed grass blades bv b~trngthe lower Blorndal (1980) held-based obs~rvat~onsand bloenerget~c parts of the leaves and alloi;.lng the upper portton study A 3 ha area ol turtlegrass was to float away, creatlng a patch ol closely cropped ~mpoundedalong wlth 12 turtles and changes patches wlth leaves averaging 2.5 cm In length. in seagrass b~oniasswere noted The grazed areas were recropped wh~lradjacent stands of tall blades remalned untouched. There were no sharp boundanes betwcen grdzed and ungrazed areas

Dladema anlrllarum (U), Thalassra testudlnum. St. Crolx, USVl F~eld Turtle grazlng had a signillcant negatlve unpact Zleman et al Clielonla mydas (R) experiments whrrc changes In seagrass growth on seagrass product~on.Urchins were ineffective (1984) and blomass were recorded along a grazing In controll~ngthe abundance of seagrass. How- grad~ent ever, urchln grazlng drd Increase the rate at which seagrass biornass turned over xv~thinenclosures. 298 Mar Ecol Prog Ser 176: 291-302, 1999

Unlike many species marine macroalgae and phyto- pact of such compensatory responses to herbivory in plankton which are wholly exposed to marine grazers seagrass systems. And while it has been recognized and often totally consumed by them (cf. Hay & Stein- that we need to develop a better understanding of the berg 1992 but see Steneck 1988 and Steneck & Dethier role of sediment porewater nutrient concentrations and 1994), the stored reserves and sites of nutrient uptake rhizome carbohydrate stores in determining seagrass for many seagrasses are located in a belowground production (cf. Zieman et al. 1984, Valentine et al. 'refuge' which is not accessible to most grazers. This 1997), there have been no sustained experiments that belowground refuge represents a stabilizing influence have simultaneously considered the roles of each of that allows seagrasses to persist where herbivory is these factors, how they could be influenced by her- intense and can, depending on the season, allow sea- bivory, or what impact they may have on the transfer of grasses to recover rapidly to levels that equal or exceed energy to nearshore food webs. those in nearby ungrazed plots. What is unclear is what In summary, while grazing on seagrasses is undoubt- factors control seagrass responses to grazing, how long edly reduced in a historical context, herbivores still seagrasses can sustain higher levels of production have significant effects on aboveground seagrass bio- post-grazing, and how they affect rates of energy flow mass in many areas (see Table 1 for a list of publica- through nearshore food webs. tions documenting grazing on seagrasses). Most im- portantly, previous studies of seagrass herbivory have not measured seagrass leaf turnover rates, which are FOOD WEB IMPORTANCE OF essential to accurately estimate the amount of seagrass SEAGRASS HERBIVORY production actually consumed by herbivores (cf. Zie- man et al. 1984, Sand-Jensen et al. 1994, Valentine et We know of only a few attempts to estimate the al. 1997). To date, there have been precious few field amount of seagrass production directly entering near- experiments which have simultaneously considered shore food webs (Greenway 1976, 1995, Nienhaus & the multiple controlling factors that determine just how Groenendijk 1986, Klumpp et al. 1993). From these much energy actually flows from seagrasses to herbi- studies it has been estimated that somewhere between vores in nearshore food webs. We contend that the -3 and 100% of seagrass net primary production en- currently accepted hypothesis that herbivory plays a ters food webs via the grazing pathway. All have relied small role in the energetics of seagrass habitats and on short-term laboratory measurements and anecd.ota1 nearby coastal ecosystems needs to be reexamined field observations to identify the levels of seagrass pro- using controlled field manipulations. Such studies will duction entering local food webs. While laboratory- provide estimates of the amount of seagrass production based efforts provide us with testable hypotheses, directly entering nearshore food webs, and they will relying solely on such approaches allows only a rough improve our understanding of the factors that control estimate of the amount of material being consumed spatial and temporal variability of seagrass herbivory. directly at a particular site. Accurately determining the density and the time spent grazing in a location, which would be required for such an approach, is likely to be Acknoruledgements. We thank Drs R. Aronson and B.Steneck limited to the amount of time a diver can spend under- and MS Michele Eilers for their constructive criticisms of this manuscript. This work was supported by the Biological water and involves an intensive effort. Moreover, in Oceanography Program of the National Science Foundation the case of vertebrate grazers, estimates may be low as (Grant No. OCE-910221?), the National Science Foundation fishes may avoid areas while divers are present. Such (Alabama) Experimental Program to Stimulate Competitive estimates must also be conducted seasonally as many Research (R11-8996152), and the National Undersea Re- of the vertebrate grazers exhibit seasonal migrations. search Center fUNCW #9537). MESC contribution No. 291. In addition, laboratory approaches do not include the possibility that rates of plant regrowth following graz- LITERATURE CITED ing can exceed those of ungrazed areas, which could lead to large underestimates of the amount of material Anderson PK, Birtles A (1978) Behavior and ecology of the grazed by these herbivores. This has been recognized Dugong dugong (): observations in Shoalwater and Cleveland Bays, Queensland. Aust Wild1 Res 5:ll-23 to be significant in many ecosystems (Lehman & Scavia Bach SD (1979) Standing crop, growth, and production of cal- 1982, Cargill & Jeffries 1984, Bianchi 1988, Williams & careous Siphonales (Chlorophyta) in a south Florida Carpenter 1988, Littler et al. 1995, McNaughton et al. lagoon. Bull Mar Sci 29:191-201 1996), and more recently also shown to be substantial Backman TW, Banlotti DC (1976) Irradance reduction. effects on standmg crop of the eelgrass Zostera marina in a in seagrass ecosystems (Valentine & Heck 1991, Sand- coastal lagoon. 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Editorial responsibility: Kennefh Tenore (Contributing Editor), Submitted: November 10, 1997; Accepted: August 11, 1998 Solomons, Maryland, USA Proofs received from author(s): December 14, 1998