Reproductive Biology of the Tropical-Subtropical Seagrasses of the Southeastern United States

Mark D. Moffler

and

Michael J. Durako

Florida Department of Natural Resources Bureau of Marine Research 100 Eighth Ave., S.E. St. Petersburg, Florida 33701

ABSTRACT

Studiesof reproductivebiology in seagrassesof the southeasternUnited States have addressed descriptive morphologyand anatomy,reproductive physiology, seed occurrence,and germination.Halodale wrightii Aschers.,Halophila engelmannii Aschers., Syringodium filiforme Kutz., and Thalassiatestudiaum Banks ex Konig are dioecious;Halophila decipiens Ostenfeld and Ruppiamaritima L. are monoecious.In Halophila johrtsoaii Eiseman, only fernale flowers are known. With the exception of R, maritima, which has hydroanemophilouspollination, these species have hydrophilous pollination. Recent reproductive-ecology studiessuggest that reproductivepatterns are due to phenoplasticresponses and/or geneticadaptation to physico-chemicalenvironmental conditions. Laboratory and field investigationsindicate that reproductive periodicityis temperaturecontrolled, but proposedmechanisms are disputed.Water temperature appears to influencefloral developmentand maybe importantin determiningsubsequent flower densities and fruit/seed production.Flowering under continuouslight in vitro suggeststhat photoperiodplays a limitedrole in floral induction.Flower expression and anthesis,however, may be influencedby photoperiod.Floral morpho- ontogeneticstudies of T. testudinumfield populationsdemonstrated the presenceof early-stageinflorescences during short- and long-dayphotoperiods, further suggestingday neutrality in this species.High initial reproductiveefforts, annual variation in male sex expression,secondary sex characters,and possible interaction of ramet agewith sex expressionhave also been detected.

INTRODUCTION

TABLE 1. BREEDING SYSTEMSFOR SEAGRASSSPECIES OCCURRING IN S.E. UNITED STATES, Seagrassesexhibit two modesof propagation vegetativeand sexual.The mostcommon method of SPECIES DIOECIOUS MONOECIUS propagationis vegetative,but sexualreproduction allowsgenetic recombination and dispersalof pro- Halodule u rigMi geny. Flowering plants, including the seagrasses, Halophito decipieos Kalophila eogelmanniui + can generallybe placedinto one or more of three +'t major reproductive categories hermaphroditic, Holophito johosonii monoecious,or dioecious.Three to four percent of Ruppia marihma all flowering plants are dioecious;however, nine of the twelve seagrassgenera are dioecious Pettitt et Syringodiwn filiforme al, 1981!.Table 1 showsbreeding systems for the Thaloeeio testuCiouoi seagrassspecies of the southeasternUnited States. 78 FLORIDA MARINE RESEARCH PUBLICATIONS

Seagrasses have apparently descended from The first filamentous-pollen-development terrestrial flowering plants. Although their vegetative studies were conducted by Bornet 864! on organs demonstrate adaptation of form and anatomy, Cyrnodoceae aeguorea Konig C. nod0sa Ucria! the reproductive organs are quite similar to those of Aschers.!. In his studies, he observed anther related land plants Sculthorpe, 1967!, and the elongation and rapid extension of the peduncle basic sequence of seagrass reproductive events is before anthesis. He also documented longitudinal not discernibly different from that of flowering land splitting of stamens containing cottonwood-like plants. Seagrasses, like their terrestrial relatives, pollen. Clavaud 878! observed pollen tubes formed have floral adaptations allowing pollination, regula- from one end of the Zostera marina pollen grain, tion of outbreeding, nurturing of the embryo, and which subsequently forced their way into the stigma. efficient seed dispersal Pettitt et aL, 1981!. He also noted that any water movement dislodged The first studies of seagrass reproductive and dispersed the pollen from the stigmas. biology can be traced back to the 4th century B.C., Prior to the 1960's, studies of seagrass repro- when the father of botany, Theophrastus, observed ductive biology principally concerned basic descrip- that Zostera ocean ca Posidonia oceanica L Delile! tive morphology Addy, 1947; Black, 1913; Bo~ produced fruits similar to oak acorns Ducker et aL, 1916, 1922; Dahlgren, 1939; Dudly, 1893; Graves, 1978!. Subsequent early studies were principally 1908; Murbeck, 1902; Rosenberg, 1901; Rydberg, taxonomic in nature, presenting descriptive mor- 1909; Setchell, 1929; Svedelius, 1904; Taylor, phology of flowers and pollen. Ducker et aL 978! 1957a, b; Tepper, 1882a, b!, and only a few studies presented an excellent historical review of the early concerned reproductive ecology or population biology scientific studies of seagrasspollen. Kausik, 1941; Kausik and Rao, 1942; Pascasio and Santos, 1930!. These works were confined primarily Cavolini 806! conducted the first major to qualitative observations. study on seagrasspollen and developed an ingenious Interest in seagrass biology was renewed after method of directly growing and studying Posidonia Phillips' 960! pioneer treatise on seagrasses in submerged containers. Konig 806! added to Table 2!. Since that time, the number of published Cavolini's observations by noting the filamentous papers concerning seagrass reproduction has in- pollen of Posidonia and Cymodoceae,as well as the creased steadily Table 2!. Work covering the south- dioecious nature of Cyrnodoceae.Gaudichaud 826, eastern United States has also increased consider- cited in Ducker et al., 1978! provided the first ably, with an 86% increase in publications over the evidence that the pollen of Arnphibolis antarctica last 25 years, 70% of these occurring since 1970. was thread-like and was released from the anthers in Seventy-one percent of all seagrass papers have rope-like strands. been published since 1960. Much of the seagrass- Fristche 837! found that the pollen of many reproductive-biology literature published since 1960 submerged plants is mucilaginous and that the has centered on the temperate Amphibolis, Phyl- pollen-surrounding mucous has the property of lospadix, and Zostera species Churchill, 1983; absorbing and swelling in an aqueous medium, a Churchill and Riner, 1978; DeCock, 1978, 1980, feature not observed in aquatic plants with aerial 1981a, b, c; Ducker and Knox, 1976; Ducker et aL, flowers or in land plants. 1977; Ducker et al., 1978; Gagnon et al., 1980;

TABLE 2. PUBLICATIONS CONCERNING SEAGRASS REPRODUCTION.

NUMBER OF PUBLICATIONS TIME PERIOD ALL SP. SP, S.E,U,S,

1860-1959 38 5 1960-1969 10 6 1970-1979 38 12 1980-1985 JULY! 41 14

TOTAL 127

PERCENT SINCE 1960 71% 86% NUMBER 42 79

Harada, 1948, 1949; Harrison, 1979; Jacobs, 1982; Subsequent sections of this paper present a Jacobs and Pierson, 1981; Keddy and Patriquin, suinmary of available information concerning the 1978; Lsmounette, 1977; McConchie et aL, 1982; reproductive biology of the five genera of seagrasses McMillan, 1983b; Nozawa, 1970; Orth and Moore, in the southeast United States. 1983; Pettitt et aL, 1983; Phillips, 1972; Phillips et aL, 1983; Riggs and Fralick, 1975, Robertson and HALODULZ WMGHT1T Mann, 1984; Silberhourn et aL, 1983; Stewart and Rudenberg, 1980; Yamashita, 1973!, and on the tropical Indo-Pacific-Australian species Thalasso- Floral Morphology dendron ciliatum, Cymodocea spp., Syringodium isoett'folium, Thalassia hemprichii, Enhalus acoroides, This species is dioecious, with inconspicuous Halophila spp., and Zostera capensis Brock, 1982; flowers enclosed in a vegetative shoot resembling a Ducker et aL, 1978; Ducker and Knox, 1976; perianth. In the staminate flowers, anthers are borne Harada, 1951; Issac, 1969, Kausik, 1940a, b; Kay, on a 12-23 inm long filament. Anthers are slender, 1971; Kirkman, 1975; Lakshamanan, 1963; Lipkin, 3.5-5 mm long, and white when immature. Mature, 1975, McMillan, 1980a; Pettitt, 1976, 1981; Pettitt pollen-containing anthers are usually green, turning et aL, 1981; Sachet and Fosberg, 1973; Swamy and brown after anther dehiscence Johnson and Lakshinanan, 1962; Verhoeven, 1979!. Principally, Wiliimns, 1982!, However, inature anther color can these studies have concerned descriptive morphology be variable, ranging from cream to red Den Hartog, and cursory physiology. 1970; Phillips et al., 1974!. Pistillate flowers are Seven species of seagrasses occur in the sub- comprised of two ovules; the ovaries are ellipsoid, tropical-tropical coastal waters of the southeastern ovoid, or globose, 1.5-2 mm long with 10-28 mm United States. Four species, Thalassia testudinum long style. The fruit is ovoid or slightly compressed, Banks ex K'bnig, Halophda decipiensOstenfeld, H. 1.5-3 mm long, with a short subterminal or lateral engebnannii Aschers., and H. johnsonnii Eiseman, rostrum It is black, rough textured, and has a hard represent the Hydrocharitaceae family, and three coat McMillan, 1981!. The fruit-seed coat separates species, Halodule wrightii Aschers,, Syringodium into nearly equal halves at germination, ftliforme Kutzing, and Ruppia maritima L., repre- sent the Potomagetonaceae family. Little informa- Reproductive Ecology tion exists concerning reproductive processes in six of the seven species Table 3!. Most research has Published literature includes little information centered on the dominant species, Thalassia testu- concerningthe reproductive dynamicsof H. wrightii dinurn. However, our recent observations Durako field populations. Phillips 960! reported that and Moffler, 1981, 1985a, b, in press; Moffler et aL, sexual reproduction in Diplanthera Halodule! is 1981! suggestthat the basic reproductive dynainics rare, and he never encountered flowering in Tampa of even this species may have been previously mis- Bay. McMillan and Moseley 967! also reported interpreted. This aspect of seagrass biology clearly infrequent sexual reproduction in Halodule in Texas requires further attention, particularly becausede- coastal waters, and suggested that the Texas popu- mand for seed material for restoration and mitigation lation might be tropical clones that reproduce projects is increasing Durako and Moffler, 1984; vegetatively under temperate conditions. In a later PMllips and Lewis, 1982!. paper, however, McMillan 979! suggested that sexual reproduction permits the selection of genetic variants that are adapted to temperate conditions. TABLE 3, PUBLICATIONS ON THE REPRODUCTIVE McMillan 976! observed Halodule patches con- BIOLOGY OF S.E. UNITED STATES SEAGRASS SPECKS. taining both male and female shoots and patches comprisedof all male or all femaleclones. Eleuterius SPECIES NUMBER OF PUBLICATIONS 977! reported that Halodule beds in Mississippi are composed of only male plants, again reflecting Hatodute wrightii 11 Halophila Sp. 8 the clonal nature of Halodule. Eleuterius personal Ruppia maritima 13 communication! has also observed that flowering is Syrinttodium fi liforme 13 more extensive along the edges of beds, but he does Thatassia testudirtum 21 Zostera mari ti ma 32 not yet have quantitative data on these populations. Halodule fruits subsequently develop at the 80 FLORIDA MARINE RESEARCH PUBLICATIONS rhizome level and may remain buried for long mm long, and 1.5 mm wide. The flower produces periods. McMillan 983a! has shown that seeds of approximately thirty seeds, each 0.20 mm long. Halodule can germinate up to 46 months or more Flowering takes place year-round, with the greatest after collection. The long dormancy provides a seed abundance occurring from January to April Den reserve in the sediment, which may be important for Hartog, 1970!. The reproductive dynamics of this recolonization after disturbance McMillan, 1981!. species are not known. McMillan 981! determined that Halodule seeds have also been found in the sediments of Syroigodium and Thalassia beds, providing further evidence that HALOPHIL4 ENGELMANNll Halodule is a pioneer species in seagrass succession, permitting rapid recolonization of denuded areas Floral Morphology Johnson and Williams, 1982; McMillan, 1981; Zieman, 1982!. This plant is dioecious. Each male flower is In the Caribbean, Halodule typically flowers in borne singly, on a pedicel 4-10 mm long. Tepals are April, with maximum male flower production on or broadly elliptic and reflexed when mature. Anthers before 5 April, and peak seed production occurring are 4 mm long and bilocular, producing yellow on 12 April Johnson and Williams, 1982!. pollen grains in fine filaments. The female flower Investigating seagrass reproductive physiology has a minute perianth and a 3-4 mm long ovary with under laboratory-culture conditions, McMillan 976, 3-5 mrn long hypanthium, Each of the three styles is 1982! has observed flowering under continuous 30 mm long. light, which suggests that photoperiod plays a limited role in floral production. He also reported Reproductive Ecology that flowering of Halodule populations in Texas appeared to reflect the influence of temperature. Of the Halophila species, H. engelmannii has The April flower production coincided with increases received the greatest amount of study. However, in temperature and salinity. Halodule flowers at prior to 1970, little was known about H. engelmannit',, temperatures between 22'C and 26'C; 24'C is and the male flowers have only recently been optimal when salinities are between 26%0 and 36%a. described Short and Cambridge, 1984!. The first to McMillan 982! was also able to induce fruitj investigate the reproductive physiology of H. engel- seed development in the laboratory. mannii, MclVlillan 974, 1976! transplanted H. engelmannii into an aquarium containing 37%a artificial seawater in January, with the plants flower- ing two months later, under a 14 h photoperiod. He noted that flowers did not occur under 12, 14, or 16 h photoperiods when plants were transplanted in Three species of Halophda occur in the south- late March. He also observed that staminate and eastern United States; H. decipiens,H, engelmannii, pistillate clones exhibited apparent differences in and H. j ohnsonii. leaf morphology. In a later study, McMillan 976! investigated the effects of salinity, temperature, and photoperiod HALOPHILA DECIPIENS on H. enI,elrnannii and other seagrass species. Flowering of H. engelmannii occurs from late April Floral Morphology through mid-June, with peak abundance of stami- nate and pistillate flowers in May McMillan, Early investigations indicate that this species 1985!. This time frame also corresponds to the is monoecious, with male and female flowers occur- flowering period noted by Short and Cambridge ring in the same spathe Bowman, 1916!. The 984! for Florida populations. tepals are oblong-elliptic to ovate. Male flowers are Flowering of H. engelrnannii is inhibited at low 1-1.5 mm long. Anthers are approximately 1 mm salinities 0-18%.!, and heavy rain causes leaf and long and contain ellipsoid pollen. Each female flower deterioration. flower containsan ovoid ovary that is 1 mm long, a Conflicting views exist concerning the role of hypanthium that is 1-2 rnm long, and three styles, teinperature and photoperiod in the f1owering of H. each 2.5 mrn long. Fruits are broadly ellipsoid, 2.5 engelmannii. Short and Cambridge 984! indicated NUMBER 42 Bl

that temperature did not appear to be unportant, 974! discussedthe developmentof the flowersof because flowers occurred during the same periods in R. maritima var, maritima, Phillips 960! reported 1982 and 1983, even though the temperature was abundant flowering material in Tampa Bay, Boca 24'C-29'C in 1982 and 3'C-5'C warmer in 1983. Ciega Bay, and other areasof Florida. R<4ppiatypi- They concluded photoperiod was the critical factor. cally flowers in the southeast from March through However, McMillan 985! found that the key factor June. was warming temperatures, rather than photoperiod. Early work Bourn, 1935; Setchell, 1924! indi- He concluded that temperatures between 22 C and cated that Ruppia required salinities of less than 27.5'C and a photoperiod with more than 12 h light 28%a to set seed. Phillips 960! reported flowering were needed for consistent production of pistillate and fruiting at 31.4%,. and noted that fruiting flowers, and therefore, temperature was the primary material was collected by Blodgett in the mid- control for the phenological timing of sexual repro- 1800's, in Key West, Florida. We have also duction in H. engelmannii. collected fruiting Ruppia growing in 38%. salinity at Stock Island near Key We~3t, Florida. Ruppia is the only southeastern United States HAL OPHILA JOHNSONII seagrassthat does not have hydrophilouspollination. Pollination can be hydroanemophilous, whereby the hydrophobic pollen grains float on the water surface, Floral Morphology allowing selfing or outc.rossing. In late winter, Ruppia begins profuse wegetative growth, with Very little is known about H. johnsonii repro- festoon-like stems rising frnm the bottom to near duction, and only female flowers have been observed the water surface. The flowers are borne on these Eiseman and McMillan, 1980!. These are sessile festoons near the surface, s ith stigmas occurring and enclosed in a two-leaved spathe. The ovary is 5 right at the air/water inter.face. In portions of mm long with a spade-shapedbase, Tampa I3ay, this festoon-like growth habit may be especially favorable, becausemuch of the plant can Reproductive Ecology be expoe.ed to greater insolation at the surface in these normally turbid waters. H. johnsonii has only been reported from the We have observed. az< apparent increase in coastal lagoon in eastern Florida, from Sebastian Ruppia ija Tampa Bay oveu the past five years, Inlet to Virginia Key. Becauseonly fernale flowers which suggeststhis type of growth habit and seed have been found, Eiseman and McMillan 980! production does indeed have a selective advantage suggest that H. johnsor

SYRINGODIUM 2<~lFDRME

Floral Morphology Floral Morphology Tomlinson and Posluszny 978! give a detailed Flowers are perfect, 2-4 in a cluster, termi- account of Syringodium morphology and develop- nating in a slenderpeduncle. The flower is wrapped ment, which we will summarizebriefly. This species in a sheathing leaf base and has two sessile stamens is dioecious, producing inflorescences that are and four capsules.The stigma is peltate; fruits are essentially cymose, with up to 30-50 flowers of oblique druplets. different ages. The male flower terminates in a unit of the sympodium and consists of four pairs of Reproductive Ecology microsporangia inserted directly on the axis and enclosed by a pair of bracts, The surface of the Little work has been done on the reproductive anther is covered with numerous large tannin cells, dynamicsof the monoeciousR. maritima in the except along the narrow longitudinal line of dehis- southeastern United States. Posluszny and P~attler cence. The pollen is filamentous. Each female 82 FLORIDA MARINE RESEARCH PUBLICATIONS

flower consists of a pair of carpels on the common Tomlinson 969!. Flowers are borne an short axis, but has no additional perianth or ridge. Each shoots, in the axil of the foliage leaves. Plants are carpel includes a single bitegenic ovule that is apparently dioecious; thus, short shoots can be pendulous from the apex of the locule. The carpel male or female, although we do not knaw if this continues as a short style that further extends into sexuality is fixed. Female flowers are almost always twa rather short stigmata. solitary; male flowers may be solitary, but more often are in groups of 2-4, most commonly 3. Reproductive Ecology Peduncle and pedicel are longer in male than in female flowers; however, the flawers are similar in Phillips 960! reported that floe ering in size. In both sexes, the floral axis bears a tubular, Synngodium was a rare event, and the importance of two-lipped organ, which may be referred to as the sexual reproduction for this species is probably "spathe." Each male flower has three tepals and a negligible. Tomlinson and Posluszny 978! repozted variable nuznber of anthers inserted at the end of that apparent clones of one sex are quite extensive, the pediceL The number of stamens varies from 8 to suggesting proliferative branching maintains and 13. Each anther has 4 pollen sacs surrounding an extends individual genets. McMillan 980b! sug- elongated connective. Tannin sacs are conspicuous, gested that conditions of late fall-early spring are especially in the connective, Female flowers possess znost likely to induce flowering. Field populations niorphologically inferior ovaries because the tepals typically flower between January and June, and are inserted above them. Each ovary consists of a MclVIillan 980b! speculated that flowering is a lower, swollen, fertile portion, with 3-5 ovules, and a response ta winter teznperature minima, His labora- longer, narrower distal portion or "neck." The neck tory studies indicated temperatures from 22'C to is largely enclosed by the spathe so that only 29'C can induce flowering, but photaperiods of less stigznas and recurved tepals protrude. The surface than 11 h inhibit inflorescence production. Mcmllan of the lower part of the ovary is covered with 980b! further suggested the presence of ecotypic numerouslaw warts that becomemore prominent in variations among Gulf-Caribbean populations. Syrin- the fruit. The ovary is unilocular, ovules are erect, godium populations in Texas have a slightly lower unitegznic, but more or less anatropous. Stigmas are temperature requireznent for anthesis than Caribbean always in pairs, within staminodes. Numbers vary populations. from 12 ta 18, but 14 is most common. Each Little informatian exists concerning quantita- stigma's epidermis is papillose and evidently well tive analysis of sexual reproduction. Johnson and adapted for retaining pollen. Williams 982! found that, for a third of the year, reproductive activity was greater than vegetative Reproductive Ecology meristematic activity in St Croix, Virgin Islands. Reproductive densities were highly variable within The reproductive biology of Thalassia has stands, Peak densities occurred in late April and received, by far, the greatest concentratian of study. seed maturation occurred in early May. The seeds Thalassia flowers throughout the range af its dis- of Synngodium, like those af Halodule, can have a tribution in the southeastern United States, with pronounced dormancy and can germinate as much f1owering znaterial callected from Texas, Mississippi, as three years after collection McMillan, 1983a!. and north, central, and southern Florida Durako Unlike fruit production and dissemination in and Moffler, 1985a; Eleuterius, 1971; Marmelstein Halodule, Synngodium fruits mature on reproductive et aL, 1968; McMillan, 1979; Moff1er et al., 198I; shoots above the sediment and can be widely dis- Phillips et aL, 1981; Rydberg, 1909!. persed McMillan, 1983a!. The ecological role of Phillips 960! was the first to publish infor- seed dorinancy in Syringodium requires further znation on Thalassia sexual reproduction, He found study. flowering on several occasions during his survey of Tampa Bay, and reported that 10% of the plants col- TIIALAS SlA TZS TUDliVUM lected in Boca Ciega Bay during May 1958 were flowering. He also first reported seedlings harvested in Florida at Anclote Key. Orpuzt and Boral 964! Floral Morphology published the first detailed account of the flowers, fruits, and seeds of Thalassia. Tomlinson 969! The following description is summarized from elaborated further on Thalassia flowers with a cam- NUMBER 42 83 prehensivestudy of floral morphologyand anatomy, synchronizereproductive events Durako and Moffler, based on serial sections. Grey and Moffler 978! in press! and affect reproductive densities Durako reportedon spatialpatterns of reproductiveshort- and Moffler, 1985b!. Durako and Moffler in press! shoot distributions with data on frequencies, den- also noted that the highest reproductive densities sities, and ratios of male and female short-shoots, especially for male short-shoots! in Tampa Bay, Thorhaug 979! observed flowers and fruits in a Florida, were preceded by relatively dry years, four-year-oldrestored Thalassia bed. suggesting that, although temperature may be Marmelstein et al. 968! discovered that a instrumental in inflorescence survival and develop- Thalassia population in St, Andrew Bay, north ment, it acts in concert with salinity. They further Florida, flowered, extending the flowering range to suggested that salinity may be important in fruit and the furthest northern limit of distribution in the con- seed production because it affects pollination success; tinental United States. They also conducted the in lower Tampa Bay, mature fruits and viable seeds first investigations of photoperiod influence on are produced only in areas of higher salinity Lewis Thalassia by observing field populations and con- et aL, 1985!. ductinglaboratory studies that includedmanipulation Phillips 960! and Eleuterius personal com- of photoperiod. Salinity was maintainedat 28-32'!" munication! noted that flowering patches of Thalassia and temperatureswere between27'C and 30 C. were unisexual,and that little or no fruit production The photoperiod treatments they chosewere 6, 12, occurred in these patches. Durako and Moffler 18, and 24 h of light per 24-hour cycle. The first 985b! suggested that while this spatial segregation flowering response was at 12 h of light, indicating of the sexes ensures genetically variant progeny, that Thalassia is an intermediate day plant, Unfor- dilution effects may diminish pollination. Spatial tunately, because flower buds may have been patchiness in reproduction may reflect clonal varia- induced prior to the laboratory culture, these tion Cook, 1983!, or the age structure of the studies did not reveal the role of photoperiod in Thalassia beds Durako and Moffler, 1985b!. The floral induction, but rather, only in floral expression. latter possibility is supported by the observation McMillan 976! initiated a series of experi- that female short-shoots have narrower leaves than mental studies investigating flowering and repro- male short-shoots Durako and Moffler, 1985a!, and duction in seagrasses.In his early studies, he also have lower numbers of leaf scars Durako and compared flowering and reproductionin laboratory- Moffler, in press!. Both of these characteristics indi- cultured Thalassia and in Texas field clones. Labor- cate female short-shoots may be younger than male atory-cultured Halophila and Halodule flowered, short-shoots. The predominance of female short- but the Thalassia did not, even though this species shoots at fringes of beds also supports this possi- did flower in the field; all of which suggests that bility. Coupled with the recent report that individual flowering conditions do not affect all seagrasses short-shoots can flower more than once Durako and uniformly.Phillips et al. 981! conductedmore Moffler, in press!, these observations raise new studies on Thalassia reproductive physiology under questions regarding the reproductive ecology of controlled conditions. They proposed that flowering Thalassi a testudi num. in Thalassia is related to temperature progressions following winter minima, Thalassia plants from Texas populations were induced to flower at 23'C or below, with anthesis at 23'C. However, plants LITERATURE CITED from St. Croix, Virgin Islands, and Mexico flowered at 24'C-26'C and flowered less frequently. More- ADDY, C. E. over, plants of diverse origins flowered under con- 1947. Germination of eelgrass seed, J, WildL tinuous light, suggestingthat Thalassia may be day Manage. 11: 279. neutraL This suggestion is reinforced by the occur- BLACK, J. M. rence of early stage inflorescences, on 44% of the 1913. The flowering and fruiting of Pectinella short-shoots collected, coincident with early fruits antarctica Cyrnodocea antarctica! Trans. Moffler et al,, 1981!, and throughoutthe repro- R Soc. S. Aust, 37: 1-5. ductive season Durako and Moffler, in press!. BORNET, E. Although reproductive structures are present 1864. Recherches sur le Phucagrostis major in Thalassia for most of th year, seasonal tempera- Cavol. Ann. Sci. Nat. Bot. Biol. Veg., ture regimes at more northern locations seem to Ser. 5! 1: 5-51. FLORIDAMARINE RESEARCH PUBLICATIONS

BOURN, W. S. 1935, Seawatertolerances of Ruppiamarilima Zosteramarina L. underlaboratory con- L Boyce ThomsonInst. Contrib. 7: 249- ditions. Aquas Bot. 10: 115-123. 255, 1981c. Influenceof temperatureand variation of BOWM Vl, H. H. M. temperature on flowering in Zostera 1916. Adaptabilityof Seagrasses.Science N,S. marina L. under laboratoryconditions. No. 1103. 43: 244-247. Aqua@Bot, 10: 125-131, DEN HARTOG, C. 1922. The distributionand pollination of certain sea grasses. Michigan Acad. ScL Arts 1970. The Seagrassesof the World. North Letters. VoL 2. Holland,Amsterdam, 275 pp. BROCK, M. A. DUCKER, S. C., and R. B. KNOX 1982. Biology of the salinity-tolerantgenus 1976. Submarinepollination in seagrasses. Nature 263: 705-706. Ruppia I . in saline lakes of South Australia II Populationecology and re- DUCKER,S. C.,N. J. FOORD,and R. B. KNOX productive biology. Aquat, Bot. 13: 249- 1977. Biologyof AustralianSeagrasses: the 268. genusAmphibolous C. Agardh Cymodo- CAVOLINI, P. ceaceae!,Aust. J. Bot. 25: 67-95. 1806. On the floweringof Zosteraoceanica Linn. DUCKER,S. C.,J, M. PEITIT, andR B. KNOX Ann. Bot. 2: 77-91.pp. 1-6 trans.by 1978. Biologyof AustralianSeagrasses: Pollen Karl Kbnig!. developmentand submarinepollination CHURCHILL, A. C. in Amphibolisantarctica and Thalasso- 1983. Field studies on seed germinationand dendronciliatum Cymodoceaceae!. Aust, seedling development in Zostera marina J, Bot. 26: 265-285. L Aquat. Bot. 16: 21-29. DUDLEY, W. R. CHURCHILL, A. C,, and M. I. RINER 1893. Thegenus Phyllospadix. Wilder Quarter 1978, Anthesisand seedproduction in Zostera CenturyBook Comstock,Ithaca, New marina L. from Great South Bay, New York York, USA. Aquat. Bot. 4: 83-93. DURAKO,I J., andM. D. MOFFLER CLAVAUD, A. 1981, Variationin Thalassiatestudinum seed- 1878. Sur le veritablemode de fecondationdu linggrowth related to geographicorigin. Zosteramarina. Ann. Soc.Linn. Bordeaux. Pp. 100-117in R. H Stovall, ed. Proc. 2: 109-115. 8th Ann. Conf. Wetlands Restoration COOK, R. E. and Creation.Hillsborough Community 1983. Clonal plant populations.Am. Sci 71; College,Tampa, Florida 244-253. 1984. Qualitativeassessment of five artificial DAHLGREN, K V. O. growthmedia on growthand survivalof 1939. Endos perm und embryolobildingbei Thalassiatestudinum Hydrocharitaceae! Zostera marina. Bot. Notiser. 92: 607- seedlings.Pp. 73-92in F. J Webb,ed. 615. Proc.11th Ann. Conf.Wetlands Restora- DECOCK, A. W. A. M. tion and Creation.Hillsborough Com- 1978. Germinationof the threadlikepollen munity College,Tampa, Florida. grains of the seagrass Zostera marina. 1985a.Observations onthe reproductive ecology Bull. Soc. Bot. Fr. 125: 145-149. of Thalassiatestudi num Hydrochari- taceae!.II. Leafwidth as a secondarysex 1980. Flowering,pollination, and fruit develop- character.Aquat. Bot. 21: 265-275. ment in Zosteramarina L Aquat. Bob 9: 201-220. 1985b.Observations onthe reproductive ecology 198la. Developmentof the floweringshoot of of Thalassiatestudinum Hydrochari- taceae!.III Spatial and temporalvaria- Zosteramarina L. underlaboratory con- tions in reproductivepatterns within a ditions in comparisonto developmentin seagrassbed. Aquat. Bot. 22: 265-276. two different natural habitats in the In Factorsaffecting the reproductive ecology Netherlands. Aquat, Bot. 10: 99-113. Press. of Thalassiatestudinum Hydrochari- 1981b.Influence of lightand dark on flowering in taceae!. Aquat, Bot, NUMBER 42

Pp. 150155 in J. J, Symoens, S. S. EISEMAN, N. H., and C. MCMILLAN Hooper, and P. Compere, eds. Studies on 1980. A new species of seagrass, Halophila Aquatic Vascular Plants. R. Bot. Soc. j ohnsonii, from the Atlantic coast of Belgium, Brussels. Florida. Aquat, Bot. 9: 15-19. JACOBS, R. P. W. M., and E. S. PIERSON ELEUTERIUS, L. N. 1981. Phenology of reproductive shoots of eel- 1971. Submerged plant distribution in Missis- grass, Zostera marina L at Roscoff sippi Sound and adjacent waters. J. Miss. France!. Aquat. Bot. 10: 45-60. Acad. Sci 17: 9-14. JOHNSON, E. A., and S. L, WILLIAMS 1977. The Seagrasses of Mississippi J. Miss. 1982, Sexual reproduction in seagrasses: Re- Acad. Sci. 22: 57-59. ports for five Caribbean species with FRITSCHE, C. J. details for Halodule wrightii Ashcers. and 1837. Ueber den Pollen. Meim. Sav. Etrang. Syringodium filiforrne Kutz. Carib. J. Sci Aced. St. Petersburg. 3' 649-672, 18: 61-70. GAGNON, P. S., R. L VADAS, D. B. BURDICK, KAUSIK, S. B. and B. P. MAY 1940a. A contribution to the embryology of 1980. Genetic identity of annual and perennial Enhalus acaroides L, fil! Stud, Proc. forms of Zostera marina L. Aquat. Bot 8: Indian Acad. Sci. Ser. B. 11: 83-89. 157-162. 1940b. Vascular anatomy of the pistillate flower GAUDISHAUD, C. of Enhalus acaroides L fil.! Stud. Curr, 1826. In L. de Freycinet Voyage autour du Sci. 9: 182-184. Monde Botnique Paris!. 1941. Structure and development of the staminate flower and the male game- GRAVES, A. H. tophyte of Enhalus acaroides L, fil.! 1908. The morphology of Ruppia rnaritirna. Stud. Proc. Indian Acad. Sci Ser. B. 14: Trans. Connect. Acad. Arts & Sci. 14: 1-15. 59-170. KAUSIK, S. B., and P. K V. RAO GREY, W. F., and M. D, MOFFLER 1942. The male gametophyte of Halophila ovata 1978. Flowering of the seagrass Thalassia testu- Gaudich. Half-yearly J, Mypore Univ. dinurn Hydrocharitaceae! in the Tampa N.S. 3: 41-49, Bay, Florida area. Aquat, Bot 5: 251-259. KAY, Q. O. N. HARADA, E 1971. Floral structure in marine angiosperms 1948. Nuclear type and formation of filament- Cymodocea serrulata and Thalassoden- like pollen in Zostera, Jap. J. Genet. 23: dron ciliatum Cyrnodocea ciliata!. Bot J. 13-14 in Japanese!. Linnean Soc. 64: 423-429. 1949, Multiple sex chromosomes in the genus KEDDY, J,, and D, G. PATRIQUIN Phyllospadix. Jap. J. Genet. 24: 8-9 in 1978. An annual form of eelgrass in Nova Japanese!. Scotia. Aquat. Bot. 5: 163-170. 1951. Karyotype and the development of "chain- KIRKMAN, H. like pollen" of a seagrassHalophila ovata. 1975. Male floral structure in the marine angio- Jap. J. Genet. 26: 226. sperm Cymodocea serrulata R. BR.! HARRISON, P. G. Ascherson and Magnus Zannichelliaceae!. 1979. Reproductive strategies in intertidal Bot J. I inn. Soc. 70; 267-268. populations of two co-occurring sea- KANIG, K grasses. Can. J. Bot, 57: 2635-2638. 1806. Additions to M. Cavolini's treatise on ISAAC, F. M. Zostera oceanica L. Ann. Bot. 2: 91-98. 1969. Floral structure and germination in pl 7. Cymodocea ciliata. Phytomorphology 19: LAKSHMANAN, K K 44-51. 1963. Embryological studies in the Hydrochari- JACOBS, R, P. W. M taceae IL Halophila ovata Gaudich. J. 1982. Reproductive strategies of two seagrass Indian Bot. Soc. 42: 15-18. species Zostera marina and Zostera noltii LAMOUNETTE, R. Hornem.! along the west European coast. 1977. A study of the germination and viability 86 FLORIDA MARINE RESEARCH PUBLICATIONS

of Zostera marina L. seeds. M.S. Thesis. two seagrasses, Halodule wrightii and Adelphi University, Garden City, New Syringodium jiliforme, from the western York. 41 pp. Atlantic, Aquat. Bot. 11. 279-296. LEWIS, R. R., M. J. DURAKO, M D. MOFFLER, 1982. Reproductive physiology of tropical sea- and R C. PHILLIPS grasses. Aquat. Bot. 14: 245-258. 1985. Seagrass meadows of Tampa Bay: A 1983a. Seedgermination in Halodulewrightii and review. Pp. 210-246 in S. F. Treat, J. L Syringodiumfiliforme from Texas and the Simon, R. R. Lewis, and R L. Whitman, U.S. Virgin Islands. Aquat, Bot. 15: 217- eds. Proceedings, Tampa Bay Area 220. Scientific Information Symposium May 1983b. Seed germination of an annual form of 1982!. Florida Sea Grant Publ. 65. Zostera marina from the Sea of Cortez, Burgess Publishing Co., Minneapolis, Mexico. Aquas Bot. 16: 105-110. Minnesota. 1985. Staminate flowers and reproductive phy- LIPKIN, Y. siology of Halophda engelmaneii. Contr. 1975. On the male flower of Halophila stipu- Mar. Sci 28: 151-195. lacea. Israel J. Bot. 24: 198-200. MCMILLAN C., and F. N. MOSELEY MARMELSTEIN, A. D., P. W. MORGAN, 1967. Salinity talerances of five marine sperma- and W. E. PEQUEGNAT tophytes of Redfish Bay, Texas. Ecology. 1968. Photoperiodism and related ecology in 48: 503-506. Thalassia testudinum, Bot. Gaz. 129: 63- MOFFLER, M. D., M. J. DURAKO, 67. and W. F. GREY MCCONCHIE, C, A., S. C. DUCKER, 1981, Observations on the reproductive ecology and R B. KNOX of Thalassia testudinum Hydrochari- 1982. Biology of Australian seagrasses:floral taceae!. Aquat. Bot. 10: 183-187. development and morphology in Amphi- MURBECK, S. bolis Cymodoceaceae!. Aust. J. Bot. 30. 1902. Ueber die Embryologia von Ruppia ros- 251-264. tellata Koch. K Sven. Vetenskapsalzad. MCMILLAN, C. HandL 36!. 1974. Salt tolerance of mangroves and sub- NOZAWA, Y. mergedaquatic plants. Pp. 379-399in R. 1970, Morphological studies of the embryo and J. Re imold and W. H. Queen, eds. seedling of Zostera. M em Kagoshima Ecology of Halophytes. Academic Press, Junshin Junior College. 1: 90-93. New York ORPURT, P.A,, and L. L BORAL 1976. Experimental studies on flowering and 1964. The flowers, fruits and seeds of Thalassia reproduction in seagrasses.Aquat. Bot. testudinum K'dnig. Bull, Mar. Sci. Gulf 2: 87-92. and Carib. 14!: 296-302. 1979. Differentiation in response to chilling ORTH, R. J., and K A. MOORE temperaturesamong populations of three 1983. Seed germination snd seedling growth of marine spermatophytes, Thalassia test- Zostera marina L. eelgrass! in the tudinum, Syringodium fili forme, and ChesapeakeBay. Aquat. Bot. 15: 117-131. Halodule wrightii. Amer. J, Bot. 66: 810- PASCASIO, J. R., and J. K SANTOS 819. 1930. A critical morphological study of Thalassia 1980a. Flowering under controlled conditions by hemprichii Ehrenb.! Aschers, from the Cymodoceaserrulata, Halophila stipulacea, Philippines. BulL Nat. AppL Sci 1: 1-24. Syringodiumisoetifolium, Zostera capensis, PETI'ITT, J. M. and Thalassia hemprichii from Kenya. 1976. Pollen wall and stigma surface in the Aquat. Bot. 8: 323-336. marine angiospermThalassia and Thalas- 1980b. Reproductive physiology in the seagrass sodendron. Micron. 7: 21-32. Syringodium filiforme from the Gulf of 1981. Reproduction in seagrasses: pollen de- Mexico and the Caribbean. Amer. J. Bot, velopment in Thalassia hemprichit, 67: 104-110. Haloptula stipulacea, and Vhalassodendron 1981. Seed reserves and seed germination for ciliatum. Ann. Bot. 48: 609-622. NUMBER 42 87

PETTITT, J. M., S. DUCKER, and B. KNOX RYDBERG, P. A. 1981. Submarinepollination. Scientific American 1909. The flowers and fruit of the turtlegrass. J. 244: 135-143. New York Bot Garden 10: 261-265. PETTITT, J. M., C. A. MCCONCHIE, SACHET, M. H., and F, R, FOSBERG S. C. DUCKER, and R. B. KNOX 1973. Remarks on Halophila Hydrocharitaceae!. 1983. Reproductionin seagrasses:pollination in Taxon. 22: 439-443. Amphibolis antarctica. Proc. R. Soc. Land. SCHULTHORPE, C, D. B, Biol, Sci. 219215!: 119-136. 1967, The biology of Aquatic Vascular Planta. PHILLIPS, R. C. Edward Arnold, London. 610 pp. 1960. Observations on the ecology and distribu- SETCHELL, W. A. tion of the Florida seagrasses. Prof. Pap. 1924. Rupia and its environmental factors. Ser. No, 2. Fla. State Bti Conserv. Mar. Lab., St. Petersburg, Florida. 72 pp. Proc. Nat. Acad. Sci. 10: 286-288. 1972. The ecological life history of Zostera 1929. Morphological and phenological notes on Zostera marina L University of California, marina L. eelgrass! in Puget Sound, Washington. Ph.D. Dissertation. Univer- Berkeley PubL Bot. 14: 389-452. sity of Washington, Seattle, Washington. SHORT, F. G., and M. L, CAMBRIDGE 159 pp. 1984. Male flowers of Halophila engelmannii. PHILLIPS, R. C., and R. R. LEWIS Description and flowering ecology, Aquat. 1983. Influence of environmental gradients on Bot. 18: 413-416. variations in leaf widths and transplant SILBERHOURN, G. M., R. J. ORTH, success in North American seagrasses. and K A. MOORE Mar. Tech. Soc. Jour. 17: 59-68. 1983. Anthesis and seed production in Zostera PHILLIPS, R. C., C. MCMILLAN, marina L. eelgrass! from the Chesapeake H. F. BITTAKER, and R. HEISER Bay. Aquat, Bot 15: 133-144. 1974. Halodule ivrightii in the Gulf of Mexico. STEWART, J. G., and L. RUDENBERG Cont. Mar. Sci 18: 257-261. 1980. Microsporocyte growth and meiosis in PHILLIPS, R C,, C. MCMILLAN, Phyllospadix torreyi, a marine monoco- and K W, BRIDGES tyledon. Amer. J. Bot. 67: 949-954. 1981. Phenology and reproductive physiology of SVEDELIUS, N. Thalassia testudinum from the western 1904. On the life history of Enhalus acaroides. tropical Atlantic. Aquat, Bot. 11: 263- Ann. R Bot. Gard. Peradeniya 2: 267- 277. 297. 1983. Reproductive strategies of eelgrass SWAMY, B. G, L, and K K LAKSHMANAN Zostera marina L! Aquat. Bot. 16: 1-20. 1962. The origin of epicotyl meristem and POSLUSZNY, U., and R. SATTLER cotyledon in Halophila ovata Guadich. 1974. Floral development of Ruppia maritima Ann. Bot 26: 243-249. var. maritime. Can. J. Bot. 52: 1607- TAYLOR, A. R. A. 1612. 1957a. Studies on the development of Zostera RIGGS, S. A., JR., and R. A. FRALICK marina I, The embryo and seecL Can. J. 1975. Zostera marina L,, its growth and distri- Bot 35: 477-499. bution m the Great Bay Estuary, New 1957b. Studies on the development of Zostera Hampshire, USA. Rhodora 77: 456-466. marina 11. Germination and seedling de- ROSENBERG, O. velopment. Can. J. Bot, 35: 681-695. 1901, Ueber die Pollenbilding von Zostera. TEPPER, J. G. O. Meddel. Stockholms Hogskolas Bot. Inst. 1882a. Some observations on the propagation of 4: 3-21. Cymodocea antarctica. Trans. R, Soc. R. ROBERTSON, A. I., and K H. MANN Aust. 4; 14, 1984, Disturbance by ice and life history adap- 1882b. Further observation on the propagation tations of the seagrass Zostera marina. of Cymodocea antarctica. Trans. R. Soc. Mar. BioL Berl! 80: 131-142. S. Aust. 4: 47-49. FLORIDA MARINE RESEARCH PUBLICATIONS

THORHAUG, A. 1979. The flowering and fruitmg of restored Thalassiabeds: a prelimiruuynote. Aquat. Bot. 6: 189-192. TOMLINSON, P. B. 1969. On the morphology and anatomy of turtlegrass, Thatassia testudinam Hydro- charitaceae!. IIL Floral morphology and anatomy. BulL Mar. Sci 19: 286-305. TOMLINSON, P. B., and U. POSLUSZNY 1978. Aspects of floral morphology and develop- ment in the seagrass, Syringodium jili- forrne Cymodoceaceae!. Bot. Gaz. 139. 333-345. VERHOEVEN, J. T. A. 1979. The ecology of Ruppia dominated com- munities in western Europe. L Distribution of Ruppia representatives in relation to their autecology. Aquat. Bot. 6: 197-268. YAMASHITA, T. 1973. Uber die embryo und Wurzelentwicklung bei Zosterajaponica Aschers. et Graeben, J, Fac. Sci. Univ. Tokyo IIL IL 175-193. Seagrass-associated Invertebrate Communities of the Southeastern U.S.A.: A Review

Robert W, Virnstein

Seagrass Ecosystems Analysts 805 East 46th Place Vero Beach, Florida 32963

ABSTRACT

Community structure of invertebrates associated with seagrassesin the southeastern United States is in- tensively studied and well described at a few sites, but generally is not well understood. A high regional diversity exists, due to the overlap of subtropical, tropical Caribbean!, and warm-temperate Carolinean! faunas. Decapod crustaceans, especially the caridean shrimps, numerically dominate the larger trawl- susceptible! fauna. Dominant species of decapods are similar throughout most of the region. Community structure of smaller macrofauna emphasized in this review! is dynamic. Species composition dominant species!and density vary widely over small and large distancesand over short hours to days! and long years! time scales, Dominant higher taxa are peracarid crustaceans especially amphipods!, gastropod molluscs, and polychaete worms. Important controlling physical factors are sediments for the infauna! and habitat complexity for the epi- fauna!. The latter is determined largely by seagrass density, which is best measured in terms of plant surface area. Seagrassesexert their influence primarily by providing physical structure to the habitat. Additional physical structure is provided by drift algae and epiphytes; the latter is especially important for smaller macrofauna and rneiofsunrL Predation, especially by pinfish and pink shrimp, is thought to be the major biological interaction affecting community structure. Evidence for the importance of predation comes from feeding studies, correlations of invertebrate abundance with predator abundance in the field, and predator- exclusionand -inclusion cagingstudies. Competition affects micro-distribution of two shrimp species,but the effects of competition, habitat selectivity, food supply, migrations, behavior, reproduction, and recruitment have received little attention. Two major functions of seagrassmeadows are the provision of food and of refuge; together, these consti- tute the "nursery" function. Epiphytes, not detritus or living seagrasstissue, provide the major sourceof food for the invertebrates, Small invertebrates are important prey for most abundant species of fish snd decapod crustaceans.Some species of decapodsare herbivores,however, and decapodscannot be lumped into a single trophic category, The degree of refuge provided by seagrassesdepends on the relationships between, and characteristics of, habitat, predator, and prey. Future research questions should emphasize processes and their rates, e.g., secondary productivity, energy flow, and predation. Do size aud morphologymatch betweeninvertebrates and plant seagrassesand algae! architecture?What conditions determine relative importance of detritus and epiphytes. What are the similarities and differences between seagrasssystems, on local, regional, and world-wide scales?

INTRODUCTION

This paper reviews communityrelationships of rather than as just a summaryof southeasternwork invertebrates associated with seagrasses, and is While inclusion of all aspects of research on sea- based on studies done in the southeastern United grassinvertebrates may have been desirable, it was States. These studies were examined in the broader not feasible. I have liberally incorporated my syn- context of the ecology of seagrass communities, thesis of the literature, rather than simply reviewed 90 FLORIDA MAIUNE RESEARCH PUBLICATIONS individual papers. Emphasis and focus are on eco- mm O'Gower and Wacasey, 1967!. Typical sieve logical relationships and functions and their con- mesh sizes have changed from predominantly 1.0 trolling factors. mm to 0.5 mm, within the last decade. A 0.5-mm Because seagrassesare virtually absent between mesh is recommended for sieving quantitative southern North Carolina and northeastern Florida, samples of macrofauna Lewis and Stoner, 1981; the geographic limits of this review go from the Mahadevan and Patton, 1979!. Smaller mesh sizes Mexican border, around the Gulf of Mexico, through are needed to retain some species and the juveniles the Florida Keys, and up the east coast of Florida to of several other species. If smaller or larger mesh just north of Cape Canaveral. However, because the sizes are used, stacking these with a 0.5-min mesh tropical seagrass species Halodute wrightii Aschers. sieve would at least allow a comparison with most reaches its northern limit in North Carolina, and be- other studies. Standardization is sorely needed; at cause several invertebrate species with tropicaVsub- the minimum, densities should be reported on a per- tropical affinities occur there, studies from North square-meter basis. Carolina are included for comparative purposes. I In addition to the diversity of gear used, equal have excluded strict biogeographic analyses of the diversity exists in the auns or foci of individual distributions of individual species. I have also ex- studies, again making comparisons between studies cluded meiofauna reviewed by Bell et al., 1984! difficult. Rarely is a particular type of study, using except where necessary to illustrate a point. particular methods, done in more than one geo- Structure of communities is reviewed first, graphic area exceptions: Heck, 1979; K L. Heck followed by function. Each of these major sections and K A. Wilson, unpublished manuscript; Nelson, includes two aspects: ! description and ! dis- 1980!. Often, only selected taxa are examined see cussion of factors that control structure or function. next section!. An overall summary and recommendations for The g,ographic distribution of marine labs has future research then follow. largely determined the intensity of research efforts in various localities Figure 1!. Such local concen- trations of research effort can be an advantage, allowing comparisons and correlations between SOME SAMPLING PROBLEMS several factors. Two major centers of research on seagrass communities are apparent Harbor Branch Major problems in comparability of data stem Foundation HBF! in Ft. Pierce, Florida, and from the diversity of sampling methods used. Florida State University FSU! in Tallahassee. The Sampling gear ranges from drinking straws to trawls, HBF effort in Indian River lagoon on the east coast and includes cores of several sizes Lewis and of Florida includes, largely through its post-doctoral Stoner, 1981, 1983!, bottom sleds or scrapes Allen program, publications by Virnstein, Young, Gore, et al, 1980; Greening and Livingston, 1982; Leber, Zimmerman, Nelson, Stoner, Santos, Howard, Fry, 1983; Leber and Greening, 1986!, drop traps with Lewis, Leber, and Main. The FSU program in the subsequent removal of animals by seine Gore et al., northeast Gulf, supported primarily by Livingston, 1981! or suction Brook, 1975, 1977; Leber, 1983, includes publications by Heck, Hooks, Stoner, 1985!, and a variety of devicesdesigned primarily to Lewis, Coen, Dugan, Ryan, Greening, Sheridan, sample epifauna Stoner and Lewis, 1985; Stuart, Clements, Schmidt, Leber, and Main. Additional 1975, 1982; Virnstein snd Howard, in press a, areas where several studies have been done include Walesky, 1976!. For collecting macroinvertebrates, Biscayne and Tainpa Bays in Florida and Corpus Leber and Greening 986! recommend a crab Christi Bay, Texas Figure 1!. Near Beaufort, North scrape rather than a trawl, Stoner et al. 983! Carolina, several studies have been done by Nelson, recommend cores rather than a suction sampler, and Thayer, Pet'erson, Summerson, Adams, Godfrey, Lewis and Stoner 981! recommend small cores Watzin, Homziak, Stuart, Fonseca, and Kenworthy. .5-cm diam! rather than larger cores .6-cm and Differences in taxonomy can be a major prob- 10.5-cm diam!. lem, and stem largely from the researchers' various Mesh sizes used for retaining animals range levels of taxonomic expertise and effort. For froin 0.062 mm to 12 mm. Even for sampling exainple, results of studies can vary greatly, de- macrofauna emphasized in this paper!, sieve mesh pending on ! the lowest taxonomic level to which sizes range from 0.42 mm Thomas, 1974! to 1.0 individuals are identified, ! accuracy of identifi- mm see list of studies in Table 1!, or even to 3.0 cations, and ! validity of taxonomic names. NUMBER 42 91

Corpus Chrkti sey

Mexico

Figure 1, Map showingnumber and locationof studiesof seagrass-associatedinvertebrates,

COMhAJNITY STRUCTURE

DOMINANT TAXA Thorhaug and Roessler, 1977; Yokel, 1975a, b! show that decapod crustaceans,including penaeid The dominant taxa collected depends, to a and caridean shrimps and true crabs, as well as gas- large degree, on type of gear used. Larger devices tropods, were generally the moat abundant inverte- such as scrapes, push nets, seines, and trawls pri- brates in south Florida Zieman, 1982!. In the marily collect decapod crustaceans, and in tropical northeast Gulf of Mexico Apalachee Bay!, dominant areas, echinoderms and large gastropods. Sampling speciesin trawl samples Heck, 1973, 1976, 1979; with cores usually results in dominance by poly- Hooks, 1973; Hooks et aL, 1976; Leber and chaetes, peracarid crustaceans e.g., amphipods, Greening, 1986! were the hermit crab Pagurus isopods, and tanaids!, snd gastropods. bonairensis = P. ynaclaughlinae?!, the caridean Zieman 982! reviewed invertebrate studies shrimps Tozeuynacarolinense, Palaernon floridanus, in south Florida seagrass beds and listed large gas- Hippolytepleuracanthus = H. zostericolaof other tropods Strombus gigas, Fasciolaria tuHpa, and studies?!, Thor floridanus = T. dobkim'?!, and Pleuroplocagigantea!, starfish Oreasterreticulata!, PakxeynonetespuIno, the crabs Neopanope texana and sea urchins Lytechinus uart'egatus, Tripneustes and N. packardii, and the penaeid shrimp Peruxeus ventricosus, and juvenile Diadema antil?arum! as the duorarurn. Use of a more eNcient epifaunal crab most conspicuous invertebrat, s. Many of these large scrape in the same area Greening and Livingston, > 5 crn! invertebrates are direct grazers of seagrass 1982; Leber, 1983; Leber and Greening,1986! gave blades Thayer et aL, 1984b! and are missing or similar dominant species.The top nine species in uncommon outside tropical south Florida Biscayne order of numerical abundance! were Hippolyte zos- Bay and Card Sound, Florida Bay, and the Florida tericola, Pagurus bonairensis,Anachis avara gas- Keys!. Also largely limited to these tropical areas tropod!, Tozeumacarolinense, Palaeynon floridan,us, are abundant, interspersed, sessile invertebrates Thor dobkini, and Neopanope texana. In nearby sponges and both hard and soft corals. Apalachicola Bay reviewed in Livingston, 1984c!, Studies using trawls Bader and Roessler, Callinectessapidus blue crab!, Penaeusduoraruyn 1971; Larson and Ramus, 1984; Roessler and Tabb, pink shrimp!, and Palaernonetesv ulgaris grass 1974; Tabb and Manning, 1961; Tabb et al., 1962; shrimp! comprised81% of the invertebratescollected FLORIDA MARINE RESEARCH PUBLICATIONS

by trawl Sheridan and Livingston, 1983!. Penaeus aztecus, Palaernonetes Uugaris, Periclimenes More quantitative than either trawls or scrapes, ]ongicaudatus, Hippolyte pieuracanthus, and Tozeurna drop nets confine animals within a known area for carolinense. The latter three of these species are subsequent collection. Using 10-m drop nets in rare or absent in eelgrass beds in Chesapeake Bay Indian River lagoon, Gore et aL 981! found that Heck and Orth, 1980a!. only 6 of the 38 species collected constituted 97% When cores, instead of trawls, are used to of the total individuals. In order of numerical abun- sample invertebrates, a different suite of species is dance, these were Hippoiyte pieuracanthus, Palae- collected, for two reasons. First, infaunal species are monetes intermedius, Pagarus bonairensis, Penaeus included; second, a smaller mesh size is used to duoraruyn, Periclimenes arnericanus, and Neopanope retain animals, typically 0.5 or 1.0 mm, compared to packardii. Using a similar drop-net method in the 3 to 6 mm mesh of trawls. General patterns of Redfish Bay, Texas, Hoese and Jones 963! listed species dominance can be given; however, listing dominant invertebrates as Palaeynonetes pugio, dominant species from a large number of studies is Penaeus duorarum, CaUinectes sapidus, and Neo- not practical here. panope texana. Dominant taxa listed in studies using cores for Thus, over a large geographic range, caridean sampling over more than a single season Bloom, shrimps especially of the family Hip polytidae! 1983; Brook, 1975, 1977; Huh and Kitting, 1986; usually are dominant. Hermit crabs and penaeid McBee and Brehm, 1982; McLaughlin et aL, 1983; shrimp are also abundant throughout the region Rudolph, unpublished manuscript; Saloman et al., especially when night collections are included!. 1982; Sheridan and Livingston, 1983; Stoner, 1979, Decapod faunas are strikingly similar, perhaps due 1980b; Virnstein et al., 1983; Young et al., 1976; to wide dispersal of their planktonic larvae. Even as Young and Young, 1977, 1978! include polychaetes, far north as North Carolina, Godfrey 969! reported gastropods, and peracarid crustaceans Figure 2!. a similar suite of species dominant in Zostera Dominant polychaetes reported in these and other ynarina L eelgrass! beds: Caliinectes sap@us, strictly polychaete studies Osborne, 1979; Santos

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Figure2, Map showingdensities and higher taxonomic composition of macrofaunafrom quantitative studies of seagrass-associatedinver- tebrates.Width of the bars is proportionalto the log of the density. NUMBER 4z 93

and Simon,1974; Schmidt, personal communication! of larger invertebrates. Even for the smaller rnacro- include Kinbergonuphissimoni, Prionospiohetero- benthos, comparisons are clouded by variation in branchia,Spiochaetopterus costarum oculatus, Tharyx methods, primarily sieve mesh size. For example, a annulosus,Laeonereis culveri, and various speciesof 0.5-mrn mesh sieve retains 537' Lewis and Stoner, capitellids and syllids. Dominant crustaceans re- 1981!, 508% Mahadevan and Patton, 1979!, or ported in the above and other strictly crustacean 72'7e unpublished data from Virnstein et al., 1983! studies Lewis, 1982, 1984; Nelson, 1980; Nelson et more individuals than a 1.0-mm mesh. al., 1982; Stoner, 1983a! include the amphipods In rnacrofaunal studies using a sieve mesh of Cymadusa compta, C. filosa in tropical areas!, 1,0 mm or smaller, the range of densities is very Ampithoe longimana, Elasmopus levis, Melita elon- great from 292 Brook, 1978! to 38,696 individuals gata, Gammarusmucronatus, Lembos unifasciatus, mz Sheridan and Livingston, 1983! see Figure 2 and Grandidierellabonnieroides, the tanaid Hargeria and Table 1!. Seasonal variation can also be tre- rapax, and the isopods Erichsonella attentuata and rnendous. In spite of greatest seagrass biomass Cymodocefaxoni. Dominant gastropodsusually in- during summer, density of amphipods, for example, clude Bittium varium, Cerithium muscarum, C. ranged from summer minima to spring maxima of eberneum,Crepidula spp,, Anachis avara, Astyris 400 m z to 12,000 m z, in Redfish Bay, Texas Huh lunata, Astrea spp., Caecum spp., and Modulus and Kitting, 1985!, and 44 rn to 3,862 m at the modulus.Similar suites of speciesare reported from Link Port site in Indian River lagoon, Florida Beaufort, North Carolina Nelson, 1978, 1979a, Nelson et al., 1982!. Likewise, year-to-year varia- b, 1980; Stuart, 1975, 1982; Sumrnerson,1980; tion can be higher than seasonal variation Livingston, Summerson and Peterson, 1984; Thayer et aL, 1 982; N e1son et al., 1982! . 1984a!. Except for Bit ti um varium, Pri onospio In studies comparing seagrass beds and ad- heterobranchia, and Spiochaetopterus costarum ocu- jacent bare sand areas, higher invertebrate and latus, most of the above species are rare or absent fish! densities and diversities were found in sea- in ChesapeakeBay Marsh, 1973; Orth, 1973, grasses Lewis, 1984; Orth et aL, 1984; Virnstein et 1977!. al, 1983, and references therein!. Animals associated For these small invertebrates "macrobenthos"! with seagrass blades, more so than the infauna, collected with cores primarily polychaetes,gastro- show the largest seagrass-sand differences, e.g., 13 pods, and peracarid crustaceans!,the geographical times more abundant in seagrasses in Florida variation of dominant species is far greater than Virnstein et al,, 1983! and 52 times more abundant that of trawl-collectedanimals. All of the peracarids in seagrasses in North Carolina Summerson and and some of these dommant polychaetesand gas- Peterson, 1984!. In light of the increased habitat, tropods have direct development,producing crawl- food, and refuge provided by seagrasses, such dif- away juveniles with no planktonic stage. This lack of ferences are not surprising. a life-history stage that permits wide dispersal may allow for the establishment and tnaintenance of localized populations. Such localized populations DIVERSITY occur even on a small scale. For example, two sea- grasssites, only 2 km apart in Indian River lagoon, Although total community diversity might in- were sampled over the same time period, in an iden- clude rnicrobes to loggerhead sponges, components tical manner Virnstein et al,, 1983!. The same of the invertebrate fauna are highly diverse in sea- number of sampleswas taken from each site; 3,258 grass beds. In drop-net collections at a seagrass site Modulus modulus and 3,051 CeriNium muscarurn in Indian River lagoon, Gore et aL 981! reported were found at one site, one and none, respectively, 38 species of decapod crustaceans. Using cores to at the other site. sample total macrobenthos, Lewis and Stoner 981, 1983! collected 80 to 101 speciesin Apala- chee Bay, Virnstein et al. 983! collected 166 species in Indian River lagoon, and Hebling un- DENSITY published species list! collected over 600 species off Key Largo. Variation in sampling methods is again a prob- Diversity of certain groups may vary between lem in comparing densities of invertebrates. Because sites. Although sampled intensively for several trawls, selnes, and scrapes are non-quantitative, years, seagrass beds in Indian River lagoon yielded valid comparisons cannot be made between densities only 15 species of amphipods, compared to over 30 94 FLORIDA MARINE RESEARCH PUBLICATIONS

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species found in Apalachee Bay Lewis and Stoner, major iinpacts on seagrass systems Livingston, 1981, 1983!, and over 50 species in Puerto Rico 1984b!, although Morgan and Kitting 984! found Zimmerman, 1978! and at Islas Los Roques off the no major impact from the passage of a hurricane. coast of Venezuela Stoner and Lewis 1985!. Only 7 Impacts couLd be modified by mixing processes. species of amphipods were collected in two seasons Temperature can also have a strong direct at two sites in Biscayne Bay Virnstein, unpublished impact, perhaps by affecting seasonal recruitment data!, patterns or eliminating predators Gilmore et aL, 1978!. Seasonal variations in temperature and sun- light are presumed to be a major cause of seasonal patterns in seagrass communities, The effects of water currents have been FACTORS CONTROLLING studied very little. Fonseca et aL 982! have shown COMjSKUNITY STRUCTURE that seagrass canopy structure alters the effect of water currents on sediment properties. PHYSICAL FACTORS Sediment properties are especially important for the infauna, yet might have little effect on the Latitude is an important factor influencing epifauna. Osborne 979! found that infaunal poly- diversity of several higher taxonomic groups, chaete distribution depended on sediment proper- Virnstein et aL 984! demonstrated that, with de- ties. Another group of polychaetes was influenced creasing latitude: ! diversity of most taxa increased; by seagrass leaf biomass. Orth 977!, studying ! amphipoddensity showedno pattern; ! sizesof Chesapeake Bay, and Thomas 974!, studying individuals of free-living amphipods decreased; and Indian River lagoon, concluded that physical stability ! free-living amphipods tended to be more numeri- of sediments was important in maintaining a dense cally dominant than infaunal and tubicolous forms. and diverse infaunal community, Bloom 983! and No comprehensive, well-supported hypothesis could Wiederhold 976! suggested that seasonal influx of explain the patterns observed. seagrass detritus increased sediment organic con- tent to which the infauna responded. The role of Bloom's 983! study is the only one to report other physico-chemical sediment properties e.g., a gradient of community structure relative to depth. pH, Eh, dissolved oxygen, and sediment porosity! Jackson 973! found that some species of infaunal has largely been ignored. bival ves in Jamaica were excluded froin Thalassia testudinum Banks ex K5nig beds shallower than Major studies of pollution effects on seagrass 1 m. He concluded that they were excluded by ex- invertebrates are largely limited to the effects of tremes in environmental conditions. bleached kraft mill effluents KNIE! in Apalachee Salinity has a major effect on seagrass- Bay from a paper mill, and thermal effluents in associated communities, but has not been studied Biscayne Bay and Crystal River, Florida, from per se. Young and Young 977! and Young et al. nuclear-powered,electricity-generating plants. The 976! found highest density and diversity of macro- negative effect of KME on various invertebrate benthos in Indian River lagoon at a station farthest groups has been demonstrated by Dugan and from an inlet and with the widest salinity fluctuations. Livingston 982!, Heck 976!, and Hooks et aL This station also had the largest increase in macro- 976!. However, the effect is indirect: changesin faunal density in response to caging designed to ex- water quality affect seagrasses,which subsequently clude predators. Livmgston 984b! concluded that affect associated animals. Effects of thermal effluents salinity and other physical factors determined such may be more direct, with upper lethal limits of overall habitat parameters as plant biomass and several organisms near 32'C-34'C Zieman, 1975; productivity. Except for Ruppia maritima L,, other Zieman and Wood, 1975; Zimmermanet al., 1979!, genera of seagrasses do not occur in low-salinity but, again, a decline in animals could be attributed waters approximately 10-I2'/! . to a decline in seagrass. Some adverse effects of Freshwater input can have a profound impact drilling fluid muds have been demonstrated in sea- on coastal and estuarine seagrass communities, not grassmicrocosms by Morton et aL 986!. Dredging only through its direct effect on salinity Livingston, activities have a direct negative impact on suspen- 1984b!, but also by an overall, indirect effect on sion-feeding animals by clogging filtering mecha- water quality. In soft-bottom communities Boesch nisms! and seagrasses by decreasinglight levels! et al., 1976!, a severe rainfall event can have similarly Godcharles, 1971!. NUMBER 42 97

BIOLOGICALLY-PRODUCED drift algal clumpscan exceed150 individualsg ' PHYSICAL FACTORS dwt Lewis, 1982; Virnstein, unpublished data; Virnstein and Howard, in press b!, indicating the Although seagrasses are living organisms, potential importance of drift algae as a habitat for several aspects of their influence are exerted small invertebrates. In Florida Bay and the Florida through their physical structure. For example, arti- Keys, drift algae primarily Laurencia spp.! provide ficial seagrass is rapidly colonized by suites of the primary habitat for settling of the first benthic animals similar to those found in natural seagrass stage of the Florida spiny lobster' Butler and beds Bell et aL, 1985; Moulton, 1971; Virnstein Herrnkind, 1985; Marx, 1983!. and Curran, 1986!. By increasing habitat complexity, drift algae Habitat "complexity" is widely touted as one provide increasedrefuge from predators K L Heck of the most important factors regulating the structure and K A. Wilson, unpublished manuscript; Leber, of seagrass-associatedcommunities. Heck and 1985; F. G. Lewis, unpublished data; Marx, 1983!. Wetstone 977!, in an often-cited paper concerning The complex branching or convoluted architecture tropical Panamanian!seagrass beds, contend that of many algaemay provide superior refuge for small both abundance and species richness of invertebrates invertebrates whose sizes "match" the small hiding are correlated with habitat complexity, as measured spaces created by certain algal architectures. by macrophyte biomass, regardless of macrophyte In addition to drift algae,attached green algae speciescomposition. Their data, however,are insuf- of the genera Cauterpa,Halimeda, Penicillus, and ficient to support their conclusion. Udotea can be abundant in tropical regions and on Although abundance of amphipods was not the Florida Gulf coast, adding to the overall habitat correlated with seagrass biomass over a wide latitu- camplexity of seagrassbeds, Lewis 982, in press! dinal range Virnstein et al, 1984!, several studies and Stoner 985! report high densities of macro- have shown that within-site invertebrate abundance crustaceans associated with some of these and other is positively correlated with plant biomass Gore et attached algaewithin seagrassbeds. Both attached al, 1981; Heck and Wetstone, 1977; Homziak et al., and drift algal clumps make convenient, easily ma- 1982, Hooks et al., 1976; Lewis, 1982; Lewis and nipulated microhabitat "islands" for experimental Stoner, 1983; Roessler and Zieman, 1970; Stoner, studies e.g., Stoner, 1985; Stoner and Lewis, 1985; 1980b, 1983a; Summerson and Peterson, 1984; Virnstein, unpublished data; Virnstein and Curran, 1986!. In this regard, addition of an understory of Tabb et al,, 1962!. Brook 978!, in contrast, found the calcareous green alga Halimeda opuntia to no such pattern. patches of Thalassia testudinum resulted in rapid However, the picture presented by Heck and increases in abundance and diversity of associated Wetstone 977! and by within-site correlations crustaceans Stoner and Lewis, 1985!. above! is too simplistic; seagrassbiomass is neither Another major biologically-producedstructural the only nor the best measureof habitat complexity. componentis provided by algal epiphytes attached Other plants, such as drift algae and epiphytic algae to seagrass blades. In some estuarine seagrass "epiphytes"!, provide habitat structure in seagrass systems,productivity and biomassof epiphytes inay systems. equal or even surpassthat of seagrasses Heffernan Drift algae unattached, benthic macroalgae! and Gibson, 1983; Jensen and Gibson, 1986; Jones, are common to very abundant in seagrass systems, 1968; Kitting et al., 1984; Morgan and Kitting, and provide significant habitat for invertebrates 1984; Penhale, 1977!. Seagrasseshave lang been Cowper, 1978; Dawes et aL, 1985; Gore et al, assumedto provide the basis of seagrassfood webs, 1981; Greening and Livingston, 1982; Heck, 1977, either directly, through grazers, or indirectly, after 1979; Hoese and Jones, 1963; Hooks et al,, 1976; initial breakdown of the leaves, through the detritus Kulczycki et aL, 1981; Leber, 1985; Lewis, 1982; food web Peters en and Boysen-Jensen, 1911; Virnstein and Carbonara, 1985; Virnstein and Thayer et al., 1975; Thayer et aL, 1984b; Zieman, Howard, in press b; %einstein et al, 1977!. In a 1982!. However, food web analyses using remote grassbedin Indian River lagoon,where the summer- photographic sampling, coupled with microacoustic time maxiinum of above-ground seagrass biomass monitoring and/or high- resolution gut analyses averagedover a 15-ha area of seagrassand bare Kitting, 1984a; Leber, 1983, 1985!, and carbon sand! was 59 g dwt m2, drift algal biomass in isotope analyses Fry, 1984; Fry and Parker, 1979; April, 1982, averaged164 g dwt m 2 Virnstein Fry et al., 1982, 1987; Lobel and Ogden, 1981; and Carbonara, 1985!. Abundance of macrofauna in Morgan, 1980; Morgan and Kitting, 1984; Parker, FLORIDA ~E RESEARCH PUBLICATIONS

1964; Thayer et aL, 1975; Zimmerman et aL, 1979! and three species of seagrassesin the lab randomly suggest that epiphytes are more important than distributed themselves among the plants Stoner, detritus as a food source in most seagrass systems. 1980 a!. Most of the mobile animals that live on seagrass In the field, however, such a direct relation- bladesfeed on epiphytes Howard and Short, 1986; ship does not hold. Abundances of several inver- Kitting, 1984; Leber, 1983; Orth and van Montfrans, tebrate taxa vary greatly among different species of 1984; reviews by van Montfrans et aL, 1982, and van seagrasses at proximate sites, even when abundances Montfi'ans et aL, I 984; Virnstein, Carbonara, and are standardized to individuals per surface area of Clark, unpublished data!. For a review of this con- seagrass blades. On all compared species of sea- troversy about the importance of epiphytes and grasses, similar suites of species occur, but relative detritus, see Fry et al. 987!. abundances differ Lewis, 1984; Virnstein and Epiphytes also increase the structural com- Howard, in press a!. Of the 15 moat abundant plexity of the habitat. For small invertebrates, species, 11 have significant differences in abundance especially the meiofauna those animals passing on three seagrasses, when abundance is calculated through a 0,5-mm mesh sieve and retained on 0.063- as individuals per blade surface area Virnstein and nun mesh!, the epiphytic "fuzz" presents a veritable Howard, in press a!. "forest," providing a tremendous increase in habitat, refuge, and food, compared to an unepiphytized sea- This question of habitat structural complexity grass blade. Bell et aL 984!, M. O. Hall personal is not a simple one, and perhaps the term "com- communication!, and Lewis and Hollingworth 982! plexity" is not appropriate. If, as found on a local report meiofaunal densities on Thalassia testudieum scale in several studies, animal abundance is blades exceeding30,000 individuals m~ of blade directly correlated with plant abundance, then plant surface area On a single, densely epiphytized abundance is simply a measure of the amount of 77iohssia blade, Hall found up to 4,000 amphipods. habitat space and not a measure of "complexity." Amphipod and harpacticoid copepod abundance Some additional measure of the structural com- was significantly correlated with epiphyte abun- plexity of plants is needed; this is referred to here dance on both real and artificial seagrasses and as "architecture" Bell, 1985!, but the term has not epiphytes M. O. Hall, personal communication!, been defined. This strong correlation of animal abundance with Stoner's 980a! lab experiments support the epiphyte abundance might overwhelm relationships idea that plant surface area is the best measure for between animal abundance and seagrass biomass, determining animal abundance. In the presence of and might be responsible for the lack of such a rela- predators, however, this relationship does not hold. tionship on a latitudinal scale Virnstein et aL, Twice as much seagrass does not provide twice the 1984!. Abundances of motile epifauna were signiTi- refuge from predators. Instead, a minimum seagrass cantly greater at a site with sparse seagrasses7 g density is needed to provide any significant refuge dwt m2! with a dense cover of epiphytesthan for associated prey Heck and Orth, 1980b; Heck at a nearby site with higher seagrassbiomass 74 g and Thoman, 1981; Nelson, 1979a; Stoner, 1979, dwt m~! and a sparsecover of visible epiphytes 1982, 1983b!. For some invertebrate species, selec- Virnstein et aL, 1985!. Evidently, epiphytes can tion for high macrophyte structural complexity can provide protection from predators for small inverte- explain distribution and abundance patterns, but for brates. Haiodule wrightii without epiphytes did not other species, predation and refuge from it! is a provide a refuge for mysids from predation by grass major determinant of these associations Leber, shrimp, Palaemonetespugio, but the addition of epi- 1985!. Thus, the role of seagrass abundance varies phytes significantly reduced predation pressure with I! seagrass species, ! seagrass density, ! Morgan, 1980!. abundance of associated algae, ! invertebrate Although plant biomass has generally been species, and ! predation pressure. This complex of used as the measureof the amount of habitat pro- factors acting in concert is a major determinant of vided by macrophytes, plant surface area may be animal distribution and abundance in seagrass more appropriate Lewis, 1982, 1984, in press; meadows, Stoner, 1980a, 1983a; Virnstein and Howard, in Habitat "heterogeneity"is anotherterm fraught press a, b!. Amphipods select microhabitats where with problems of definition and interpretation. As plants provide a greater surface area; amphipods used in the literature, the term can have two dis- that were offered equal surface areas of drift algae tinct, but not mutually exclusive meanings: ! a VUMBER 4s 99

measure of the number of kinds of habitat e.g,, patterns Adams, 1976a; Carr and Adains, 1973; Abele,1974!, including number of seagrassspecies, Huh and Kitting, 1985; Livingston, 1982; Stoner, and! thespatial patchiness of a habitat e.g., Holt 1980c! that are related to ontogenetic changes in et al, 1983!.Habitat heterogeneityprimarily affects feeding inorphology Stoner and Livingston, 1984!. speciesdiversity of associatedanimals, not abun- As exemplified in Apalachee Bay, young of the year dance, An increasein both aspectsof habitat 8-15 rnm! are planktivorous, then at 16-60 mm! heterogeneity,especially diversity of habitat types become carnivorous, feeding primarily on amphi- as originallyproposed m the classicpaper by pods, Then pinfish go through two stages of omnivory MacArthur and MacArthur, 1961!, usually is asso- 0-120 mrn!, during which they consume inore ciated with an increase in animal diversity Abele, shrimp and plant material; finally, at > 120 inm! 1974; Heck, 1977;Heck and Orth, 1980b;Stoner, they become herbivorous, feeding on living seagrass, 1985;Stoner and Lewis,1985; Virnstein et aL, especially Syringodium fiHforme KQtzing Stoner, 1984!. Diversity of fauna would presuinablybe 1980c!. Thus, pinfish go through stages of carnivory, related to diversity of seagrassesat a site Mangrove oinnivory, and herbivory, and each stage represents Systems,1985!. a "trophic unit" Stoner, 1980c!. Resident species, such as gobies and pipefish, are often discovered to be numerically dominant when more efficient devices for collecting fish, such as drop nets or throw cages, are used Gilmore, BIOLOGICAL INTERACTIONS 1987!. These fishes also change diet with increasing AND PROCE SSES size, from primarily copepods to amphipods Gilmore, 1987; Huh, 1984; Huh and Kitting, 1985; Kulczycki Biological interactions and processes can have et ai., 1981!. Thus, small invertebrates are impor- a powerful local influence on the structure of sea- tant prey for the dominant fishes in seagrass beds. grass communities. Although physical factors may "run the show" in defining habitat characteristics Decapod crustaceans, also, are important pre- and limits of a community, biological factors largely dators of smaller invertebrates. Nelson 979a, determine the specific structure Livingston, 1984b!. 1981a, b! has shown that several species of decapods Most prevalent in the literature is the suggestion of consume amphipods. Leber 983, 1985! studied predation as a mechanism that regulates community the food habits of 14 species of decapods in grass- structure. Other influential biological factors include beds in Apalachee Bay and found a wide range of competition, habitat selectivity, migrations, and diets, from complete carnivory to complete herbivory. reproductioe'recruitment. Decapods,therefore, could not be consideredcol- lectively as one trophic group. Penaeid and caridean Predation shrimps were generallymuch more carnivorousthan xanthid and majid crabs, but with noted exceptions. Studies of predation are generaHy one of two Living plant material especially epiphytic algae! types feeding studies or caging studies. To date, was far more important than detritus, disputing the no published studies include measures of actual in- paradigm that detritus provides the major trophic tensity or rate of predation, e.g., numbers of prey link eaten m s day i. Because most fishes and decapod crustaceans Several field studies have examined feeding are carnivorous during at least part of their life cycles, predation is a potentially important factor habits of fishes associated with seagrasses Adams, 1976a, b; Brook, 1975, 1977; Carr and Adams, 1973; regulatingprey populations,However, due to lack of information on daily rations and generally poor esti- Clements and Livingston, 1983, 1984; Gilmore, un- mates of fish density, no feeding studies provide an published data; Hoss, 1974; Livingston, 1982, 1984a; Nelson, 1979a, b; Peterson, 1981; Ryan, eetimate of predation mteneiti prey eaten m day i!. Only for an eelgrass community in Australia 1981; Sheridan et al., 1984; Stoner, 1979, 1980c, 1982; Stoner and Livingston, 1984!. Major emphasis has this been done Robertson, 1983!. has been on the pinfish, Lagodori rhornboides, one of Several inferences have been made by corre- the doininant fishes throughout most seagrass beds lating inforination from feeding studies with inver- in the southeast see review by Gilmore, 1987!. The tebrate distribution and abundance patterns, For food habits of pinfish change with age, progressing example, a seasonaldecline in densities of amphi- through a series of distinct ontogenetic feeding pods to a minimum in summer has been attributed 100 FLORIDA MARINE RESEARCH PUBLICATIONS

to a seasonal influx af predatory fishes aud burrowing by infauna Brenchley, 1982!. decapods Huh and Kitting, 1985; Nelson, 1979a, Variations in predation intensity or efficiency b; Nelson et al1982; Sheridan and Livingston, have also been suggested to explain differences in 1983; Stoner, 1980d; Thayer et al., 1975!. An abundance and relative dominance of invertebrate example case; in a Halodule tvrightii bed in species among different seagrass species Lewis, Apalachicola Bay, the four most abundant species of 1984; Nelson, 1979a, b; Stoner, 1983a!. Syringodiurn fish, comprising 84'7~ of the total, were Bairdiella filiforme generally supports the greatest abundance chrysoura, Orthopristis chrysoptera, Lagodon rhom- of epifaunal crustaceans, both per leaf biomass and boides, and Cynoscion nebulosus; the three most per leaf surface area Stoner, 1983a; Virnstein and abundant species of large, epibenthic trawl-sus- Howard, in press a!. Densities of predatory pinfish ceptible! invertebrates, comprising 81% of the are lowest in Syringodium Staner, 1983b!, which total, were Callinectes sapidus, Penaeus duorarum, provides the greatest protection from pinfish preda- and Palaemonetesvulgaris Sheridan and Livingston, tian Staner, 1982!. Thus, the species composition 1983!. These seven species all prey on macrofauna, and biomass af seagrasses can affect the abundance and all were mast abundant during summer, when and foraging efficiency of predators, which subse- macrofaunal density and diversity were lowest. quently affect abundance and diversity of macro- Also, various spatial patterns of seagrass- fauna associated invertebrates have been attributed to Currently, predator-caging studies provide the patterns of predation or predators. In the Indian most direct evidence for the effect and importance River lagoon, densities of amphipods Nelson et al., of predators Peterson, 1979; Virnstein, 1980!. 1982! and total macrofauna Young et al., 1976! Unless specific predators are identified and their were lower near inlets and the southern end of the densities successfully manipulated with proper con- lagoon, and were attributed to greater densities of trols the latter is a difficult task, and not to be fishes and decapod crustaceans there. On a local undertaken lightly!, results will be ambiguous. To scale, low densities of invertebrates in sparse sea- merely set up cages, under the pretext of excluding grass beds have been attributed to greater preda- all and unknown! predators, is folly. tion intensity Heck, 1979; Homziak et al., 1982; Most predator- exclusion experiments designed Lewis, 1984; Lewis and Stoner, 1983; Nelson, to examine the effects of predation on seagrass 1979a, b, 1980; Osborne, 1979; Stoner, 1980b, d, communities have been inconclusive or have pro- 1983a; Stuart, 1975; Summerson and Peterson, duced mixed results Nelson, 1978, 1981a; Orth, 1984!. In both lab Coen et al, 1981; Heck and 1975; Peterson, 1979; Summerson and Peterson, Thoman, 1981; Main, 1983, 1987; Nelson, 1979a; 1984; Virnstein, 1977, 1978; Virnstein et al., 1983; Orth and van Montfrans, 1982; Stoner, 1979, 1982! Young and Young, 1977, 1978; Young et al., 1976!. and field Leber, 1985; Leber and Virnstein, in pre- Generally, response to predator-exclusion cages in paration! experiments, predators find and capture seagrass communities is small, compared to that in prey more efficiently in sparse seagrasses. Dense unvegetated soft-sediment reviewed by Peterson, seagrass beds can provide increased refuge by 1979! and rocky intertidal communities Menge and making prey harder ta see and by impeding move- Lubchenco, 1981!. ment of larger predators. Two of the major problems that have plagued Greater densities of infauna in dense seagrass predator-caging studies in seagrass habitats, other beds have been attributed to protection afforded by than the usual problems see Virnstein, 1978!, are the root and rhizome mat, which makes the sedi- ! invasion and increase of intermediate-level pre- ments less accessible to predators Bloom, 1983; dators and ! establishment of an appropriate Orth, 1977; Peterson, 1979, 1982; Reise, 1978; control We shall see that both of these problems Santos and Simon, 1974; Stoner, 1982; Virnstein, can be solved. 1977, 1978!. This refuge for infauna was examined The failure of supposed "predator-exclusion" experimentally in the lab Blundon and Kennedy, cagesto result in the expected increase in density of 1982; Orth and van Mantfrans, 1982; Peterson, seagrass macrofauna has been blamed on inter- 1982!. Infauna living deep within the sedimentsare mediate-level predators Nelson, 1979b; Peterson, protected by the rhizome mat, but the refuge value 1979; Reise, 1978; Virnstein, 1978; Virnstein et al., for infauna would vary, depending on seagrassroot 1983; Young and Young, 1977, 1978; Young et al., and rhizome morphology.Although a dense rhizome 1976! and led those authors to conclude that mat inhibits diggingby predators, it also may hinder decapod crustaceanswere the culprits. While the NUMBER 42 ioi

mesh cages excluded large predators mostly fish!, measure rates of predation in nature without a cage, small decapods could enter through the cage mesh but it is not without artifacts. Heck and Wilson com- and were then protected from their predators. Such pared risk of predation in vegetated and unvege- increases in decapods most of which were considered tated habitats in Florida, Bermuda, and New Jersey, potential predators! prevented increases, or even and found wide variation between sites, seasons, caused decreases, in macrofaunal densities within and years. For small decapods set out in vegetation these "predator-exclusion" cages. Experimental evi- for 24 hr, the proportion eaten ranged from 16% in dence for this, however, is lacking. New Jersey to 74% in Bermuda. Subsequent to these caging "failures," Leber 985!, Leber and Virnstein in preparation!, and Competition Nelson 981a, b! successfully used field caging techniques to demonstrate that predation by decapod Although competition is often implied as an crustaceans can significantly reduce densities of important factor, few studies clearly demonstrate macrofauna. The shrimps Penaeus duorarum and that it actually occurs in seagrass systems. Compe- Palaemonetes intermedius and the crab Callinectes tition might occur for ! refuge, ! foraging sites, sapidus were shown to have significant negative or ! primary substratum. Coen et aL 981! have impacts on density of same macrofaunal groups. shown that the caridean shrimp Palaemon flori- These successful solutions to caging problems were danus excludes Palaemonetes Uulgaris from pre- accomplished by the use of up to four techniques: ferred vegetated habitat, and conclude that this ! the use of small mesh Nelson 981a, interspecific competition explains the shrimps' non- b! used 1.2-mm mesh and Leber 985! used 4-mm overlapping microgeographical distribution. Kitting mesh; in press! demonstrated intraspecific microhabitat ! controls established within cages this partitioning in the snail Anachis avara serniplicata, allows valid testing of principal treatment effects and related this partitioning to sites of preferred e.g., presence/absence or density of predators!; algal foods on the seagrassblades and ta camouflage partial cages e.g., topless, sideless! may produce from visual predators. Taylor and Virnstein unpub- significant and often interesting! artifacts, but lished data! tested for changes in behavior due to should not be used to test principal treatment intraspecific interactions between individuals of the effects; amphipod Cyrnadusa compta at high density 2 amphipods 46 cm2 of Thalassia testudinuni blade ! use of short time scales to measure re- surface area! and at low density amphipods 46 sponse the above experiments ran for 3 weeks em 2!. SigniTicant changes occurred in the amounts Nelson! and 4 weeks Leber!, instead of months, as of time spent swimming and not moving, but most was typical in earlier studies; subsequent experi- behaviors were not affected at these densities. ments by Leber and Virnstein unpublished! have successfullyused experimentaltime periods as short as 1 day; Habitat selectivity ! initial defaunation of cages Nelson had In an elegant lab study of microhabitat selec- some problems when some of his cages were placed over natural concentrations of predators, trapping tivity, Stoner 980a! showed that three species of them within cages; Leber solved this problem by ini- epifaunal amphipods, when offered three different densities of the same seagrass, selected the greatest tially defaunating cages using light suction, removing a11epifauna while leaving the seagrass undisturbed; biomass. When offered three seagrass species then prey could be allowed to colonize, or prey and rhalassia testudinum, Syringodium flili forme, and Halodule rarightu! with the same biomass, amphipods predators could be introduced in known densities. chose the seagrass with the greatest surface area More evidence of the importance of predation, Halodule!. When offered equal surface areas of the beyond that from feeding and caging studies, is three seagrass species, they were randomly dis- provided by tethering studies. In this technique, tributed. Surface area, rather than seagrass biomass, animals are attached by monofilament line to a wire should be a better indicator of animal abundance. anchor in the sediment This technique has been This selection for high surface area should minimize used in the lab Heck and Thoman, 1981! and in the predation. In the field, however, Stoner 983a! field Heck and Wilson, unpublished manuscript!. It found a lower density of amphipods on Halodule has the advantage of enabling researchers to than on SyrinI odiuurn.He attributed this discrepancy 10Z FLORIDA MARINE RESEARCH PUBLICATIONS

to his findings Stoner, 1982! that pinfish forage 1983!. Thesemigrations and colonizationsall occur more efficiently in Halodule than in 77mtassia or more extensivelyat night. Syring odium. Short time scales hours to days are the Field demonstration of differential abundances moststriking aspect of thesemigrations and coloni- in microhabitats is not sufficient, however, to zations.The questionthat mustbe asked,given this supportthe often-madeimplication that such dif- rapid turnover within and betweenmicrohabitats, ferencesare due to habitat selectivity. Several other is "what processesare intense enough to maintain factors could produce the same distribution pattern. differencesin density amongmicrohabitats."

Migrations Reproductionand recruitment Migrationsaffect community structure by acting in combination with the three factors above pre- dation,competition, and habitatselectivity. Intense If greater reproduction and recruitment occur local migration of a species, Le., from one habitat in grassbedsthan in unvegetated areas, then higher non-selectively to another nearby habitat, would densities could be mamtained in grassbeds. The tend to producerandom or evendistribution of that same pattern could result, however, from random settling and subsequentdifferential survivaLNo species. studyhas addressedthe questionof "fitness,"i.e., Many species do make extensive, abundant, whether reproductive output is greater in seagrass and frequent migrations. Using a vital stain to tag beds. animals in situ without disturbing them, Howard 985! was able to measure turnover rates = pro- More invertebrate larvae settle in pots of sedi- portion of unstained animals migrating into a ment with either real or artificial seagrassthan in markedplot!. Within a 0,6-m2 plot, ! 50% of the pots with no seagrass Fitzhardinge, 1983!. Bloom individuals of a caridean shrimp were replaced 983! attributed the seasonalpatterns of abundance within 3 hr. Turnover rate of gastropodswas lower, of two dominant species both polychaetes! to but some speciesapproached 50% turnover within 6 seasonalpatterns of reproduction.He concluded hr. Using clumps of artificial seagrass as a sub- that this seasonality is in response to seasonal stratum for coloniz ation, Virnstein and Curran patternsof detritusinput. Althoughseveral authors 986! found that colonizationwas extremely rapid imply that seasonalpatterns of invertebrateabun- with abundance and diversity of motile epifauna dance are due to patterns of reproduction and primarily amphip ods and gastropods!reaching recruitment, I find little basis for this conjecture.In equilibrium levels within a week Such rapid coloni- the southeast U.S., many groups e.g., the amphi- zation occurred even as far as 15 m away from any pods!often reproduce throughout the year Stoner, vegetation.Other studiesalso show rapid coloni- 1980d!, and survival may be more important than zation of various substrata by a diverse fauna initial recruitment for predator-susceptiblespecies. Nelson 979b! found that the density of amphi- Conversely, for species less affected by predators, pods colonizingmesh traps peaked after 7 days, He recruitment may be the major factor determining attributed subsequent decline in amphipod density patterns of abundance. to predation by rapidly colonizing Palaernonetes vulgaris.Density and speciesrichness of crustaceans colonizing clumps of algae reach asymptotic levels within 4 days in tropical seagrass beds Stoner, 1985; Stoner and Lewis, 1985!, COMMUNITY FUNCTION A large number of benthic harpacticoid cope- pods and other meiofaunalorganisms periodically By communityfunction, I mean communityre- enter the water column reviewed by Bell et aL, lationships and responsesto physical and biological 1984!. Amphipods and copepods rapidly colonize factors, and I include descriptions of these inter- within days! both real and artificial seagrass, actions and important processes.Far less is known especially when epiphytes are present M. O. Hall, about the function of seagrass-associatedinverte- personal communication!. Tube caps of the poly- brate communities than about their structure. chaete Diopatra cuprea are extensively colonized Nursery and trophic relationships are two of the by meiofauna within a tidal cycle Bell and Devlin, major functionsfor which information is available. NUMBER 42 I 03

NURSERY 1980b; Orth et al., 1984!. The refuge value of sea- grasses increases as density increases, but in a step Seagrass communities function as nursery function rather than in a linear relationship. Below areas by providing refuge and food. For seagrass some level of seagrass density, predation is the beds to demonstrate true "nursery" functio~, juve- same as on bare sediment. Above that level, prey niles within beds must show ! faster growth, due are well hidden, and/or predators' foraging is im- to increased availability of food, and/or ! greater peded. Actively-foraging stalking! predators may be survival, due to increased refuge from predators. less efficient in dense seagrass beds, hut ambush sit-and-wait! predators may be equally or more Food and growth efficient because they are better hidden from their more abundant prey. Prey characteristics affecting Several studies see above and review by Fry susceptibility to predation include ! size, ! et aL, 1987! have demonstrated the importance of cryptic coloration, morphology, and behavior, ! epiphytes as a food source for seagrass macroinver- microhabitat choice, and ! avoidance behavior. tebrates. Epiphytic algae are virtually absent in Using the caridean shrimps Tozeuma carolinense unvegetated soft-sediment habitats. By deflecting and Hippo yte zostericola = H. pleuracaethus?! as and baffling water currents Fonseca et al., 1982!, prey, Main 985! demonstrated that natural prey seagrasses increase deposition of suspended detri- selection by pinfish and pipefish is a consequence of tus. Total organic content of live and dead detrital! prey accessibility, not predator preference. Prey plant material is greater in seagrass beds, but dif- accessibility is primarily a function of visibility, as ferences in organic content of sediments can be sur- determined by prey size and motion, Tozeurrra's prisingly small Almasi, 1983; Peterson et al., 1984; microhabitat choice and behavioral predator- Sumrnerson and Peterson, 1984!. Seagrass beds avoidance response significantly reduce its acces- obviously offer a far greater supply of food for sibility to predatory fish Main, 1983, 1986!. grazers, especially for grazers of epiphytic algae By providing both abundant food and refuge, Leber, 1985! and larger herbivores that graze seagrass beds provide the essential characteristics directly on living seagrasses Thayer et al., 1984b!. of a nursery area, This nursery function is one of the Because seagrass beds support such dense most important functions of seagrassmeadows. populations of grazers, they likewise offer an abundant supply of food for primary predators of these grazing macrofauna. Most decapod crustaceans Leber, 1985! and fishes reviewed in Gilmore, TROPHIC RELATIONSHIPS 1986, and Livingston, 1982! depend either wholly or in part on these macrofauna for fooL Thus, seagrass To attempt to describe, here, all trophic rela- beds clearly supply this food component of the tionships of invertebrateswould be impractical, but nursery function. Only one study, however, has I will review major patterns. Many aspects are demonstrated that animals' growth is faster in a sea- coveredin sections above and will not be repeated grass bed than in adjacent bare-sand areas: a study in detail here. A study of trophic relationships by Peterson et al. 984! of the filter-feeding bivalve should ideally answer questions of who eats what Mercenaria rnercenaria. and how much. The best examples of this are from Australian seagrassmeadows Robertson, 1983!. An Refuge from predators excellentreview of larger herbivoresin seagrass systemsis provided by Thayer et al. 984b!. They This second aspect of the nursery function is acknowledgethat only a few speciesgraze directly much better documented than differential growth. on living seagrassesand only a small portion of the That seagrasses provide refuge from predators is energy and nutrients in seagrasses is channeled now well established see above: "FACTORS CON- through these herbivores,which, however,can have TROLLING COMMUNITY STRUCTURE" !. a profound effect on the seagrassplants and on Lab and field experiments show that the other grazersand fauna. Descriptionsof trophic amount of refuge provided by seagrasses depends relationships are based primarily on evidencefrom on characteristics of habitat, predator, and prey. gut contents, food labeling, and caging studies, These characteristics will be briefly summarized Gut-content studies have clearly shown that here for reviews, see: above; Heck and Orth, small seagrass-associated invertebrates are fed on I04 FLORIDA MARINE RESEARCH PUBLICATIONS

by mast of the abundant fishes Adams, 1976a, The secondsource of informationon trophic b; Brook, 1975, 1977; Carr and Adams, 1973; relationships, food labeling, uses radioactive iso- Clements and Livingston, 1983, 1984; Gilmare, un- topes as tags in the lab, and stable isotopes as published data; Livingston, 1982, 1984b; Nelson, natural tags in the field. Moat studies point to the 1979a, b; Peterson, 1981; Ryan, 1981; Sheridan et importance of epiphytes as a food source for inver- aL, 1984; Stoner, 1979, 1980c, 1982; Staner and tebrates Fiy, 1984; Fry and Parker, 1979; Fry et Livingston, 1984! and decapod crustaceans Leber, aL, 1982; Morgan, 1980; Morgan and Kitting, 1984; 1983!. In general, epifaunal, free-living, non-cryptic, Parker, 1964; Thayer et al., 1975; Zimmerman et competitively-inferior species with no predator- aL, 1979!. Also, see review by Fry et aL 987!. avoidance behavior are preyed upon more heavily Evidence from caging studies, the third source than in faunal, tubicolous, cryptic, competitively- of information on trophic relationships, is indirect: if superior species with predator-avoidance behavior species A responds to the exclusion caging of Coen et aL, 1981; Heck and Orth, 1980b; Huh and species B, predation is not the only process that can Kitting, 1985; Main, 1985, 1987, Nelson, 1979a, b, explain this response. Absence of disturbance or 1981a; Orth et al., 1984; Stoner, 1979, 1980b, c, d, competition, response to the cage, and response to 1983a!. Amphipods, in particular, and hippolytid changed currents or sediments are some af the other shrimp are preyed upon heavily by larger predators. factors that could explain such a response Virnstein, Both are abundant see above! and feed primarily 1978!. Caging studies have shown that epifauna on epiphytic algae reviewed in Kitting, 1984; Kitting respond more than infauna, but results vary con- et aL, 1984; van Montfrans et al., 1982; Zimmerman siderably between studies Orth, 1977; Peterson, et aL, 1979!. When epiphytic algae are not available, 1979; Virnstein et aL, 1983; Young and Young, most amphipods can feed directly an living seagrass 1977, 1978!. In more carefully controlled caging blades, experiments see above and Leber, 1983, 1985; Many feeding studies suffer from problems of Leber and Virnstein, in preparation!, abundances of methodology. The two major problems are tiine of predators and prey can be precisely controlled, and collection and level of taxonomic identification. For actual rates af predation can be measured. an example of the first, suppose that a night-feeding In perhaps the only studies of energy flow, predator is collected during mid-day a common Stuart 975! and Thayer et aL 975! analyzed the occurrence!. If the half-day-old gut contents of this summertime energetics of epifauna in a Zostera predator are examined, they might be called marina bed near Beaufort, North Carolina, In their "debris" or "partially digested organic matt r," mathematical model of energy flow, invertebrate This non-descript material might be lumped in the macrofauna were estiinated to consume 75% of net category "detritus," This would lead ta overestima- primary production. tion of the importance of detritus as a food source. A picture of some of the most important food Obviously, for a correct representation of diet, webs can be put together from all the various organisms must be collected during or immediately studies. The predominant pathway of energy flow after their specific feeding periods. Thus, feeding through these seagrass ecosystems seems to be the studies need ta be conducted over a 24-hr period, at following sequence Figure 3!: least in initial stages. Level of taxonomic identification of gut con- ! Epiphytic algae are important primary pro- tents is the other major problem in feeding studies. ducers with high turnover rates. For example, Nelson 979a! and Staner 979, 1980d! have shown that certain species of amphipods are preyed on mare heavily than others, and not ! Epiphytes are preferentiallygrazed by most necessarily in proportion ta their relative abundance. species of small invertebrates associated with sea- Main 985, 1987! found that relative intensity of grassblades. predation on two caridean shrimp species varies widely and is nat determined by differences in size ! Small invertebrates are preyed on by dec- or abundance but by differences in behavior. These apod crustaceans or by small fishes, bath resident conclusions are supported by results of competition adults and juvenile seasonals. experiments Coen et al., 1981!. Thus, identifymg prey to ~secies is impottant, and proper timing of ! Decapods and small fishes are preyed on collections can make this task possible. by larger fishes. NUMBER 42 105

Figure 3. A proposed major food web for seagrass beds, based on organisms dominant in Indian River lagoon, Florida. Depicted: I! the grazingepifaunal amphipod Cymadasacompta about to be preyed upon by II! Paiaemonrtesmtermedias, which is about to be preyed upon by III! Bairdiella chrysoara front Virnstein et a11983!, In other seagrass systems, other genera may occur in these trophic positions.

SUMMARY

This summary addresses six questions. The show a macrofaunal density of I0,000 individuals first three parallel the organization of this review, m2 and a diversity of l00 species; both values, and the last three concern comparisons outside the however, could vary up or down by a factor of 3 or southeastern United States. more. Many species, especially decapod crustaceans, are widely dispersed with similar dominant species in most areas, Dominant species of smaller macro- fauna can vary widely from site to site, season to WHAT ARE THE CHARACTERISTICS season, and year to year. While same combination of OF SOUTHEASTERN COMMUNITIES? crustaceans, gastropods, and polychaetes dominates in all areas, the structure of communities even at Seagrass-associated invertebrate communities nearby sites can vary widely. Community structure of the southeastern United States are diverse, both is not homogeneous in space or time, but is quite within and between sites. A typical study might dynamic, 106 FLORIDA MARINE RESEARCH PUBLICATIONS

WHAT ARE THE MAJOR temperate Carolinean faunas. Several tropical species CONTROLLING FACTORS? also occur in North Carolina, but are rare or absent in Chesapeake Bay. Some of these disjunct distri- Physical factors largely control the physical butions of seagrass invertebrates are directly related structure of the individual seagrass site. Within the to the absence of seagrassesin South Carolina and seagrass bed, major controlling factors that have Georgia. been implicated and tested for are ! predation, ! habitat complexity, measured as seagrass biomass or better! surface area, and !, for infauna, sedi- WHAT ASPECTS ARE SIMILAR ments. The amount of refuge from predation that TO OTHER REGIONS? seagrassesprovide depends on an interplay of habi- tat, predator, and prey characteristics. Other poten- Worldwide, seagrasscommunities share several tially important factors that have been given little common properties: consideration are ! competition, ! habitat selec- ! They constitute habitat by providing abun- tivity, ! migrations, and ! epiphytes. dant food and refuge from predators. ! Predation and seagrass density are impli- WHAT ARE THE MAJOR FUNCTIONS? cated as important factors controlling the distribution and abundance of invertebrates. The major function of seagrass plants is pro- ! The density and diversity of invertebrates vision of physical structure, which may be more is greater in seagrass beds than in nearby bare important than their contribution of primary pro- sediments. duction. For infauna, this structure provides sedi- ! Composition of higher taxonomic groups is ment stability and protection from digging predators. similar in most systems; dominant epifauna are For the epifauna, this structure provides ! in- peracarid crustaceans or gastropod molluscs, and creased living space, ! substratum for attachment dominant infauna are usually polychaetes. and growth of epiphytes, which serve as the major basis of the food web, ! protection from epi- benthic and demersal predators, and ! a direct, but minor, source of food. By providing food and refuge, WHAT HAVE STUDIES seagrass meadows provide a favorable habitat for IN THE SOUTHEAST SHOWN THAT HAS many species. NOT BEEN LEARNED ELSEWHERE?

WHAT IS UNIQUE Monitoring and experiments have demon- ABOUT SOUTHEASTERN COMMUNITIES? strated the importance of both very long decades! and very short hours! time scales for several pro- A subtropical-tropical influence exists through- cesses. For example, epifaunal colonizations are out the region. South Florida and the Florida Keys measured in time scales of hours to days. Related to are most tropical in nature, having I! sediments of this is the importance of diel studies. calcium carbonate, ! interspersed calcified green Observational studies, including the use of algae, corals, and sponges, and ! several species of sound, have been used to determine feeding pre- large ! 5 cm! herbivores that graze living sea- ferences, habitat selectivity, and the effects of grasses. behavior and habitat complexity on predator/prey Seagrasses throughout the southeast are of relationships, The importance of epiphytes as a tropical origin. Thalassia testudinurn, Syriegodium major source of food and refuge has been clearly fili forme, and Halodule urrightii are found virtually demonstrated. Higher trophic relationships, in- throughout this region and the Caribbean, Halodule cluding diets of fishes and decapod crustaceans, but has a disjunct distribution in North Carolina, where not feeding rates, have been described at a few it overlaps with Zostera marina eelgrass!, which is localities. Certain species, especially I agodon not found south of North Carolina rhornboides and Penaeus duorarurn have been identi- The regional diversity of invertebrates in the fied as important predators of macrofauna, having a southeast is very high because of the overlap of significant impact on invertebrate distribution and subtropical-tropical Caribbean faunas with warm- abundance. NUMBER 42

FUTURE RESEARCH should be a valuable tooL ! What are the roles of habitat complexity WHAT ARE THE MAJOR INFORMATION GAPS? and habitat heterogeneity? First, a clear definition of terms is needed. A major complication is that both ! The basic autecology of most species is factorsdepend on scale.For example,the complexity poorly known, e.g., behavior, feeding, life position, and heterogeneityof a single seagrassblade with and preferred microhabitat, epiphytes at the tip and none at the base are not ! The role of plant "architecture" and its perceived similarly by a 100-pm copepod and a match with prey morphology has not been tested. meter-long barracuda. Are the relative size scalesof animals and their pre- ! What are the roles of habitat selectivity ferred plant substrata correlated? Some information and competition?Do animals select a habitat pri- exists for seagrasses,but not for drift algaeor epi- marily for refuge value or food availability? Such phytes, both of which may provide significant determinationswill require behavioralstudies. physicalstructure in someseagrass systems. ! How important is diel variability? For most ! "Epiphytes" are poorly characterized.These species,the magnitudeand causeof this variability attached algae are taxonomically and morphologi- are unknown. cally diverse and harbor abundant microbes, meio- ! What causesso manyanimals to migrate fauna, and detritus. from seagrassbeds, which provide refuge and food? ! The importanceof habitat selectivity, com- Are they avoiding other animals, or are they petition, recruitment, and small-scale migrations has searching for something received only minor attention, ! What are the major processesand their ! Below-ground plant-animal relationships rates? The relative importance of some processes, are virtually unstudied, even though the inajority of e.g.,predation and colonization,is best measuredby seagrassbiomass is below ground. coinparing rates. ! Secondaryproductivity and growth rates ! Whichis moreimportant as a foodsource, have been studied only for commerciallyimportant epiphytes or detritus? Or, under what conditions is species. one or the other more importanP. Site-to-site varia- ! Energy flow through a coinmunity or sea- tion can be considerable. Just as detritus is eaten in grass system has been ineasured at only one site. severalways, so also might epiphytes be consumed Overall, we have only a limited picture of what a in several ways, Le., "epiphytes" in the broad sense seagrass community does and how it does it. of the term, including a diverse assemblageof com- ponentsbesides algae. WHAT SHOULD BE THE DIRECTION 8! Finally, what are the patterns betweensea- OF FUTURE RESEARCH? grass communities? Large-scale similarities between seagrass systems should be exainined, both on a The following is my list of nominations for the regional and worldwide scale. What properties are major questions and topics for future research. common to all seagrass systems? What determines Although such a list could be immenselylong, the differences between systems?Let us hope these following lines of researchare expectedto bring the questions will receive increased attention in the greatest return toward an understanding of seagrass- future. associated communities. ! What is the role of plant "architecture"? Habitat selectivity might be used as a tool to ACKNOWLEDGEMENTS measure invertebrate perception of various plant architectures,both on a microhabitat scale e,g,, tip Critical assistance in assembling the manu- of blade versus base of blade! and on a "nano- scriptwas provided by M. A. Capone,K D. Cairns, habitat" scale e.g., blade surfaceunder epiphyte and P. S. Mikkelsen,with typing by Carol Meo. The canopyversus that betweenbranches of an epiphytic job was also made easier by previous reviews in a alga!, Becauseof their broad morphologicaldiversi- symposiumorganized by R J. Orth and K L. Heck, ties, macroalgae drift and attached! and epiphytes Jr. [Estuaries4A!, 1984I, by massiveregional should be included in such studies. Artificial sub- reviewsby Thayer et aL 984b! and Zieman982!, strata that can be systematically varied in structure and by an extensivebibliography assembled by I OII FLORIDA MARINE RESEARCH PUBLICATIONS

Mahadevan et aL 984!. Thanks to many people BELL, S. S., and D. J. DEVLIN who generously sent me a plethora of reprints, 1983. Short-term macrafaunal recolonization of theses, reports, and unpublished data. Thanks to R. sediment and epibenthic habitats in C. Phillips and M. D, Moffler far organizing this Tampa Bay, Florida. Bull. Mar. Sci. 33: symposium, R. A, Mattson for a helpful review, and 102-108. to M. J. Durako and V. L. Smith of the Florida BELL, S, S,, K WALTERS, and J. C, KERN Department of Natural Resources Bureau of Marine 1984. Meiofauna from seagrass habitats: a re- Research for thorough editing. This constitutes con- view and prospectus for future research, tributian no. 557 of the Harbor Branch Oceano- Estuaries 7: 331-338. graphic Institution, Inc., and S.E.A. contribution BLOOM, S. A. no, 2, 1983. Seasonalityand structure of a macroben- thic seagrasscommunity on the Florida gulf coast.Int. Revue Ges.Hydrabiol 68: 539-564. LITERATURE CITED BLUNDON, J. A., and V. S. KENNEDY 1982. Refuges for infaunal bivalves from blue ABELE, L G. crab, Callinectes sapidus Rathbun!, pre- 1974. Species diversity of decapod crustaceans dation in Chesapeake Bay. J. Exp. Mar. in marine habitats. Ecology 55: 156-161. Biol. Ecol, 65: 67-81. ADAMS, S. M. BOESCH, D. F., R. J. DIAZ, 1976s. Feeding ecology of eelgrass fish com- and R, W. VIRNSTEIN munities. Trans. Am. Fish. Sac. 105: 514- 1976. Effects of Tropical Storm Agnes on soft- 519. bottom macrobenthic communities of the 1976b, The ecology of eelgrass, Zostera marina James and York estuaries and the lower L.!, fish cominunities. II. Functional Chesapeake Bay. Chesapeake Sci. 17: analysis. J. Exp. Mar. Biol. EcoL 22: 293- 246-259. 31 1. BRENCHLY, G, A. ALLEN, D. M., J. H. HUDSON, 1982. Mechanisms of spatial competition in and T. J. COSTELLO marine soft-bottom communities. J, Exp. 1980. Postlarval shrimp Penaeus! in the Florida Mar. Biol. Ecol 60: 17-33. Keys: species, size, and seasonal abun- BROOK, L M. dance, BulL Mar. Sci. 30: 21-33. 1975. Some aspects of the trophic relationships ALMASI, M. N. among higher consuiners in a seagrass 1983. Holocene sediments and evolution af the community Thalassia testudinum Indian River Atlantic coast of Florida!. Konig! in Card Sound, Florida Ph.D. Ph.D. Dissertation. University of Miami, Dissertation. University of Miami, Coral Coral Gables, Florida. 238 pp. Gables, Florida 133 pp. BADER, R. G., and M A. ROESSLER 1977. Trophic relationships in a seagrass com- 1971. An ecological study of south Biscayne munity Thalassia testudinum! in Card Bay and Card Sound. Prog. Rept. U.S. Sound, Florida. Fish diets in relation to Atomic Energy Commission, ML 7008a. macrobenthic and cryptic faunal abun- 81 pp. dance. Trans. Am. Fish. Soc. 106: 219- BELL, J. D,, A. S. STEFFE, and M. WESTOBY 229. 1985. Artificial seagrass: how useful is it for 1978. Comparative macrofaunal abundance in field experiments on fish and macroin- turtle grass Thalassia testudinum!, in vertebrates, J. Exp. Mar. Biol. Ecol 90: south Florida characterized by high blade 171-177. density. Bull. Mar. Scl 28: 212-217. BELL, S, S. BUTLER, M, J., IV, and W. F. HERRNKIND 1985. Habitat complexity of polychaete tube- 1985. Habitat selection and predation in juvenile caps: Influence of architecture on dy- spiny lobsters: the importanceof the red namics of a meiobenthic assemblage. J. alga Iaurencia. BulL EcoL Soc. Am. 66: Mar. Res. 43: 647-671. 149. abstract!. NUMBER 42 109

CARR, W. E. S., and C, A. ADAMS R R. Lewis, eds. Proceedings of the 1973. Food habits of juvenile marine fishes Symposiumon Subtropical-Tropical Sea- occupying seagiass beds in the estuarine grasses of the Southeastern United zone near Crystal River, Florida. Trans. States. Fla Mar. Res. Publ No. 42. Fla, Am. Fish, Soc, 102: 511-540. Dept.. Nat. Resour. Bur. Mar. Res. St. CLEMENTS, W. H., and R. J. LIVINGSTON Petersburg, Florida, 209 pp. 1983. Overlap and pollution-inducedvariability FRY, B., and P. L. PARKER in the feeding habits of filefish Pisces: 1979. Animal diet in Texas seagrass meadows: Monacanthidae! from Apalachee Bay, C evidence for the importance of ben- Florida. Copeia 2: 331-338. thic plants. Estuarine Coastal Mar. Sci 1984. Prey selectivity of the fringed filefish 8: 499-509. Monacanthus cilia us Pisces: Monacanthi- GILMORE, R. G. dae!; role of prey accessibility.Mar. Ecol. 1987. Subtropical-tropicalseagrsss coinmunities Prog. Ser, 16: 291-295. of the southeastern United States: fishes COEN, L. D., K L. HECK, JR,, and L. G. ABELE and fish communities. Pp. 117-138 in M. 1981, Experiments on competition and preda- J. Durako, R. C. Phillips, and R. R. tion amongshrimps of seagrassmeadows. Lewis, eds. Proceedings of the Symposium Ecology 62: 1484-1493, on Subtropical-TropicalSeagrasses of the Southeastern United States. Fla. Mar. COWPER, S. W. Res, Publ, No. 42. Fla Dept. Nat. 1978, The drift algae community of seagrass beds in Redfish Bay, Texas. Contrib. Resour. Bur. Mar. Res. St. Petersburg, Florida. 209 pp. Mar. Sci. 21: 125-132. GILMORE, R. G,, L. H. BULLOCK, DAWES, C. J., M, O. HALL, and R. K. RIECHERT and F. H. BERRY 1985. Seasonal biomass and energy content in 1978. Hypothermalmortality in marinefishes of seagrasscommunities on the west coast south-central Florida, January, 1977. of Florida. J. Coastal Res. 1: 255-262. Northeast Gulf Sci. 2; 77-79, DUGAN, P. J., and R. J. LIVINGSTON GODCHARLES, M. F. 1982. Long-term variation of macroinvertebrate 1971. A study of the effects of a commercialhy- assemblagesin Apalachee Bay, Florida. draulic clam dredge on benthic communi- Estuarine Coastal Shelf Sci. 14: 391-403. ties in estuarine areas. Technical Series FITZHARDINGE, R, No. 64. Fla. Dept. Nat. Resour.Bur. Mar. 1983. Comparisonsof the invertebrate faunas Res. St. Petersburg, Florida 51 pp. colonizingsoft sedimentsm two different GODFREY, M. M. habitats. Bull. Mar. Scl 33: 745-752. 1969. Seasonal changes in the macrofauna of an FONSECA,M. S., J. J. FISHER, J. C. ZIEMAN, eelgrass Zostera marina! community near and G. W. THAYER Beaufort, North Carolina. Ph.D. Thesis. 1982. Influence of the seagrass, Zostera marina Duke University, Durham, North Carolina L, on current flow. Estuarine Coastal 232 pp. Shelf Sci. 15: 351-364, GORE,R. H., E. E. GALLAHER,L. E. SCOTTO, FRY, B. and K A. WILSON 1984. C/ C ratios and the trophic importance 1981. Studies on decapod crustacea from the of algae in Florida Syringodiurnfiliforme Indian River region of Florida. XI. Com- seagrassmeadows. Mar. Biol 79: 11-19. munity composition, structure, biomass, FRY, B., R. LUTES, M. NORTHAM, and species-areal relationships of sea- P. L PARKER, and J. OGDEN grass and drift algae-associatedmacro- 1982. A i~C/iZC comparison of food webs in crustaceans. Estuarine Coastal Shelf Sci. Caribbean seagrassmeadows and coral 12: 485-508. reefs. Aquat. Bot. 14: 389-398. GREENING, H. S., and R. J. LIVINGSTON FRY, B., S. A. MACKO, and J. C. ZIEMAN 1982, Diel variation in the structure of seagrass- 1987. Reviewof stable isotope investigationsof associated epibenthic inacroinvertebrate food webs in seagrass meadows. Pp. 189- communities. Mar. Ecol Prog. Ser. 7: 209 in M. J. Durako, R. C. Phillips, and 147-156. 110 FLORIDA MARINE RESEARCH PUBLICATIONS

HECK, K. L, JR. HOMZIAK, J., M, S. FONSECA, 1973. Effect of pulp mill effluents on species and W. J. KENWORTHY assemblages of epibenthic invertebrates 1982. Macrobenthic community structure in a in Apalachee Bay, Florida. M.S. Thesis. transplanted eelgrass Zostera marina! Florida State University, Tallahassee, meadow. Mar. EcoL Prog. Ser. 9: 211- Florida 100 pp. 221. 1976. Community structure and the effects of HOOKS, T. A. pollution in seagrassmeadows and adja- 1973, An analysis and comparison of the ben- cent habitats. Mar. BioL 35: 345-357. thic invertebrate communities in the 1977. Comparative species richness, composi- Fenhalloway and Econfina estuaries of tion, and abundance of invertebrates in Apalachee Bay, Florida. M.S. Thesis. Caribbeanseagrass Thalassia testudinum! Florida State University, Tallahassee, meadows Panama!. Mar. BioL 41: 335- Florida, 122 pp. 348. HOOKS, T. A., K L. HECK, 1979, Some determinants of the composition and R. J. LIVINGSTON and abundance of motile macroinverte- 1976. An inshore marine invertebrate com- brate species in tropical and temperate munity: structure and habitat associa- turtlegrass Thaiassia testudinum! tions in the northeastern Gulf of Mexico. meadows. J. Biogeogr. 6: 183-200. BulL Mar. Sci 26: 99-109. HOSS, D. E. HECK, K L., JR, and R J. ORTH 1974. Energy requirement of a population of 1980a Structural componentsof eelgrass Zos&ra pinfish I again rhornboides Linnaeus!. marina! meadows in the lower Chesapeake Ecology 55: 848-855. Bay - decapod crustacea. Estuaries 3: HOWARD, R. K 289-295. 1985, Measurements of short-term turnover of 1980b. Seagrass habitats: the roles of habitat epifauna within seagrass beds, using an in complexity, competition and predation in situ staining method, Mar. EcoL Prog, structuring associated fish and motile Ser. 22: 163-168. macroinvertebrate assemblages. Pp. 449- HOWARD, R. K, and F. T. SHORT 464 in V, S. Kennedy, ed. Estuarine Per- 1986. Seagrass growth and survivorship under spectives. Academic Press, New York. the mfiuence of epiphyte grazers. Aquat, HECK, K L., JR., and T, A. THOMAN Bot. 24: 287-302. 1981. Experiments on predator-prey interactions HUH, S. H. in vegetated aquatic habitats. J. Exp. 1984. Seasonal variations in populations of Mar. Biol. EcoL 53: 125-134. small fishes concentrated in shoalgrass HECK, K L., JR., and G, S. WETSTONE and turtlegrass meadows. J. Oceanol. 1977. Habitat complexity and invertebrate Soc. Korea 19: 44-55. species richness and abundance in tropi- HUH, S., and C. L. KITTING cal seagrass meadows. J. Biogeogr. 4: 1985. Trophic relationships among concentrated 135-142. populations of small fishes in seagrass meadows. J. Exp. Mar. BioL Ecol. 92: HEFFERNAN, J. J., and R. A, GIBSON 29-44. 1983. A comparison of primary production rates JACKSON, J. B. C. in Indian River, Florida, seagrasssystems. 1973. The ecology of molluscs of Thalassia Fla. Sci 46: 295-306. communities, Jamaica, West Indies. I. HOESE, H. D., and R. S. JONES Distribution, environmental physiology, 1963. Seasonality of larger animals in a Texas and ecology of common shallow- water turtle grass community. PubL Inst, Mar. species. BulL Mar. Sci 23: 313-350, Sci., Texas. 9: 37-47, JENSEN, P. R., and R. A. GIBSON HOLT, S. A., C. L. KITING, and C. R. ARNOLD 1986. Primary production in three subtropical 1983. Distribution of young red drums among seagrass communities: A comparison of different seagrass meadows. Trans. Am. four autotrophic components. Fla. Sci Fish. Soc. 112: 267-271. 49: 129-141, NUMBER 42

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