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VOL. 30. NO.4198BMangrove SwampCommunitiesby Klaus Riitzler, and Candy Feller

Mangrove Swampby Klaus Rulzler, and Candy Feller"T he roots gave off clicking sounds, and the odorwas disgusting. We feillhat we were watchingwsomething horrible. No one likes the mangroves.That is how John Steinbeck and Ed Ricketts depictedThe OOslrychielum communily.based on ,In inrerlid,ll ssociillion of red algae.Oysters are localed al mid-lide,md upper-tide levels. while them;mgrove Iree crab andperiwinkle stay above theWiller line. (Il1us/ralionCandy feller)16by

Communitiesthe mangroves in 1941 in the Sea of Cortez. Manypeople agree with them. So why have two dozenscientists from the Smithsonian Institution, primarilyfrom the National Museum of Natural History, andtwice as many colleagues from American andEuropean universities and museums devoted adecade of exploration 10 one square kilometer of-black mud, . Oies and insects in great numbers. "' impenetrable . mangrove roots .; and-, . stalking. quiet murder"?The study slarted in the early 19805, andfocuses on an intertidal mangrove island known asTwin Cays, just inside the Tobacco Reef section ofthe barrier reef of Belize. a tiny Central Americannation on the Caribbean coast (see article page 76).The principal purpose of Ihis research is todocumenllhe biology, geology, ecological balance.economic importance, and aesthetic value of aprominent coastal ecosystem using the example of adiverse and undisturbed swamp community.Properties of Mangrove SwampsMangrove swamp communities dominate theworld's tropical and subtropical coasts, parallelingthe geographical distribuHon of coral reefs.Mangroves on the Atlantic side of the Americancoasts occur between Bermuda and almost to themoulh of the Rio de Ia Plata (Argentina). andthroughout the West Indies. like reefs, mangroveswamps are environments formed by organisms, butunlike mosl coral communities, they thrive in theintertidal zone and endure a wide range of salinities.'"Mangrove- refers 10 an assemblage of plantsfrom five families with common ecological,morphological, and physiological characteristics thatallow them 10 live in tidal swamps. Worldwide, atleast 34 species in nine genera are considered to betrue mangroves. P. B. Tomlinson's recent book,Botany of Mangroves, defines this group of planls byfive features: 1) they are ecologically restricted totidal swamps, 2) the major element of thecommunity frequently forms pure stands, 3) theplants are mOfphologically adapted with aerial rootsand viviparity (producing new plants instead ofseeds), 4) they are physiologically adapted fOf saltexclusion Of salt excretion, and 5) they aretaxonomically isolated from terrestrial relatives, atleast at the generic level. '"Mangrove swamp- Of'"mangal- refers to communities characterized bymangrove plants.Mangrove trees are used fOf water-resistanttimber, charcoal, dyes, and medicines. They resistcoastal erosion during stOfms and possibly promoteland-building processes by trapping sediment andproducing peat. The protective subtidal root syslemof the red mangrove serves as nursery ground formany commercially valuable species of fishes,shrimps, lobsle , crabs, mussels, and oysters. Anassorted fauna of birds, reptiles, and mammals is alsoat home in the mangrove thickets and tidal channels.Human disturbances have made a heavyimpact on many mangroves near populated areas asa result of dredging and filling. overculting. insectcontrol. and garbage and sewage dumping. Theintertidal environment of mangroves is endangeredby pollutants in the water, air, and soil. Accidental oilspills appear to be particularly damaging. Oil and tarsnot only smother algae and invertebrates, but alsodisrupt the oxygen supply to the root system of themangrove trees by coating the respiratory pores ofthe intertidal prop and air roots.A Mangrove Laboratory in BelizeBelize (fOfmerly British Honduras), boasts the longestbarrier reef of the Northem Hemisphere, extending220 kilometers from the Mexican border in the northto the Gulf of Honduras in the south. Behind thisbarrier lies an enormous lagoon system averaging 25kilometers between the mainland and open ocean.Mangroves border most of the coastline, extendupstream from countless river mouths, and fringe orcover most lagoon cays.One of these is Twin Cays (Figure 1I-anisland divided into two by an S-shaped channel.Twin Cays has become our study site andexperimental field laboratory. Although we usuallyspend the nights and conduct laboratory bench workon nearby Carrie Bow Cay-site of the NationalMuseum's coral reef field station for the last 15years-most days and many nights are spent in themangrove channels, lakes, ponds, mud "a,s, andeven the trees. A self-.:ontained weather Slationestablished on one of the mud flats transmits data onwind, sun, rain, temperatures, and tides to a portablecomputer on Carrie Bow Cay.The bibliographies on mangroves show thatduring the last 200 years more than 6,000 papershave been published describing biological andgeological details from almost as many differentswamps over the world. Our ongoing study aims to17

fobocco Ilonge.::.".,."""'*a1. G,.,.j5ot. thCui00f"lCQI'" &owlagoonPolCh Retl,C)g./PD ';",,"0,,,,11Coy.CO". Bow C",G)C",lewC. C'" FiSure ,. ManstOVe ecosystemstudy area. Twin Cays. Belize.The Nation Jl Museum 01Natural History's coral reef fieldstiltioo isIoated on Carrie'Bow Cay, aboul 4 kilomelers5OlI1he.u.l. (FtOm RiJtzlet andMacinlyre, 1981, SmilhsonianContributions 10 lhe MarineSCiences 12)analyze as many components as possible of a singlemangrove swamp and, ultimately, assembk them toa mosaic reflecting structure as well as function ofthis unique ecosystem.Geologic l History of Twin C ysA popular theory holds that mangroves are buildersof land because they trap and hold fine sediments.Early on in our study we discovered thaI this is notnecessarily true. We tried to reclaim nearby CurlewCay, which had been lost to a hurricane (it is nowknown as Curlew Bank), by planting an assortmenl ofyoung red mangroves, but were unsuccessful. So thequestion arose, if islands are not buill by mangroves,how do they get started?To learn more about the Holocene (recenttime-back to 18,000 years before present)stratigraphy under the present island, Ian G.Macintyre of the Smithsonian Department ofPaleobiology, along with Robin G. Lighty and AnneRaymond 01 Texas A&M University, drove pipes8 meters into the sediment down to the Pleistocenelevel (marks the beginning of the Holocene), andretrieved sediment cores that date back 7.000 years:They also collected rock cores below this level.18What they found below the mangroves was acarbonate substrate consisting of a dense limestoneformed mostly by finger corals (Porites) withabundant mollusk fragments. indicating anenvironment of deposition similar to today's calmwaler patch reefs. The sequence of peat, algalproduced sand, and mangrove oysters in thesediment cores indicales that this mangrove wasapparently established on a topographic high formedby a fossil patch reef, and kept pace with the risingsea level. However, there is also evidence thatlheisland repeatedly changed its size and shiftedposition, generally building with lagoon sedimentson the windward coosts, while eroding at theleeward edge, which is characterized by shallowwater bottoms formed by stranded peat deposits.The mangrove community itself can bethought of as being composed of three componenls:the above-water -forest.· the intertidal swamp. and Ahhough lhe HoIcxenecan dale boKlc as much illS 18,000yea .thefe are only 7.000 yea of sedimenl accumulationin lhis particular arN, as sea level did no! flood lhe BelizeIagooo unlillhe upper Holocene.

Figure 2. Channel (ringed byred mangro\lE'. Sponges andother sessile organisms areauached to prop roolS and 10lhe underwashed peal bank 10the righl; lurtle grass and algaecover lhe mud bollom. A blackmangrove wilh short intertidalair roolS prolruding from thebottom is seen on Ihe lefl.(After RUIZ!er, 1969.Proceedings of a Coastallagoon Symposium, MexicoCity; redrawn by Molly Ryan)High Tid,';.'.'.'.the underw-ater system (Figure 2). In ourdescriptions, we will start from the bottom and work"PoEnvironments Below the TidesThe boUom of the mangrove from the intertidal to3 meters, the greatest depth of the main channel, iscomposed of what most people would call muck. Tous, it displays many varieties, such as carbonate silt,mud, and sand with varying amounts of mucus,organic detritus (products of plant and animaldecay), peat, and silicious skeletons derived fromdiatom algae and sponges. Many fine-grainedlimestone sediments are produced by physical andbiological erosion on the nearby reef and carriedinto the mangrove by water currents. Sands, on theother hand, are primarily produced within thecommunity by digestion or decay of calcareousgreen algae (Halimeda).The most abundant and ecologicallyimportant plant on the submerged mangrovebottoms is the turtle grass (Thalassic1l. It stabilizes themuddy bottom, offers substrate (or egg cases andmany small sessile organisms, and provides food andshelter to animal groups ranging from microbes to2·meter manatees. Jorg A. Ott, a seagrass ecologistfrom the University of Vienna, determined that turtlegrass in the Twin Cay mangrove is more dense, andgrows 3 times faster, than Thalassia in the nearbyopen lagoon, resulting in an almost lO·fold net leafproduction.Red mangrove stilt roots line all channels,creeks, and ponds and, below tide level, supportspectacularly colored clusters of algae, sponges,tunicates (sea squirts), anemones, and manyassociates. They also provide hiding places for manymobile animals, such as crabs, lobsters, sea urchins,and fishes.Algae without the ability to root in mudbottoms abound on the stilt roots. Mark littler. fromthe Smithsonian Department of Botany, and coworkers Diane littler and Philipp Taylor found that,curiously, fleshy algae seem to prefer roots that hadpenetrated the water surface, but had not yetreached the boltom of the channel or lake.Calcifying aigae (such as the sand-producingHalimeda), on the other hand, are common on thesubmerged parts of anchored roots and along thechannel banks. Experiments demonstrated that thehanging roots offer palatable plants protection frombenthic (bottom-living) herbivores such as seaurchins and many fishes, whereas Halimeda has itsown skeletal protection.Certain algae and many sessile invertebrateson the subtidal mangrove roots are protected frompredators by toxic substances stored in their tissuesand produced by their own metabolism. Sponges areparticularly well-known for their antibiotic and19

feeding-deterrent properties. The sponges, in tum,are used by many smaller organisms, such asanemones, polychaete worms, shrimps, crabs.amphipod crustaceans, gastropod mollusks, andbrittle stars as an effective physical and chemicalestimated 100 million individuals congregated duringthe day in a band of swarms along a l,()()().meterstretch of channel bank.shelter. Collaborating with our Smithsoniancolleagues, Krislian Fauchald, Gordon Hendler (nowAlthough the tidal range in the Caribbean is small, inshallow coast.ll areas it can strongly influence currentflow and distribution of organisms. At Twin Cays, themean tidal range is only 15 centimeters, yet acombination of astronomical, geomorphologic, andmeteorologic factors can cause a range of more thana half meter.Red mangrove (Rhizophora) prop roots, blackmangrove (Avicennia) pneumatophores,. peat banks,and mud flats are the typical substrates of theintertidal zone supporting distinctive communities.Barnacles (Chthama/us), wood boring isopods(Limnoria), oysters (Crasses/rea), and ·mangroveoysters· (lsegnomon, not a true oyster) are the bestknowr indicators of intertidal hard substrates, whilefiddler crabs (Vcal are typical for the mud flats.Green algal mats (Caulerpa, Halimeda) are foundexposed on peat-mud banks during low tide. Themost abundant and characteristic intertidalmangrove community, however, is called thebostrychietum, named after the principalcomponents of an association of red algae(Boslrychia, with Calanella and Calog/ossa).The bostrychietum (see page 16) has aremarkable water-holding capacity, which allows theplants and their associated animals to surviveextended dry periods. We measured water loss ratesin two of the substrate spectes and found evidenceof two different methods of water retention.Bostrychja is a delicate, tufted plant that holds waterprimarily interstitially (between the branches).Catene//a is more fleshy and less elaboratelybranched, and holds water intracellularly (within thecells), in its tissues.loren Coen, Dauphin Island Sea Lab,examined the animal associates of thebostrychietum, particularly in respect to grazing. Hefound that amphipods (Parhyale) becomeconcentrated in the algal mats in high numbersduring receding tides, and that their grazing onBostrychia can match or exceed the algal growth.The mangrove tree crab, AralUs, and other crabsfrom the low-tide level were also found with largequantities of Bosfrychia in their guls.Desiccation and related problems ofincreased temperature and salinity in organismssubjected 10 exposure at low tide becameparticularly apparent during an extreme low tide inJune 1983. A 2().centimeter zone below mean lowtide level became exposed during noon hours undera clear sky.Large communities of low intertidal (rarelyexposed) and subtidal (never exposed) organisms,at the los Angeles County Museum), and BrianKensley, we extracted up to 40 species and 400specimens of endozoans (species living withinanOlher) larger lnan 2.5 millimeters from, as anexample, a l-liler fire sponge (Tedania), a speciestnat causes burning. itching. aocl even severedermatitis in humans.Sponges are among the most common,massive. and colorful invertebrates in the submergedmangrove. To settle and metamorphose. their larvaeneed solid substrate with low exposure tosedimentation, although we observed grownspecimens surviving for months buried in light mudafter they had fallen from their place of originalattachment. Only two kinds of firm substrate areavailable to such settlers, red mangrove stilt roots,and vertical or overhanging banks composed of a feltof peat and mangrove rootlets and flushed by tidalcurrents.In both locations, the competition for space isfierce, not only among sponges, but also betweensponges and other sessile organisms, such as algae,hydroids (the polyp-generation of many medusae),corals, anemones, bryozoans (moss animals), andtunicates (sea squirts). With our colleagues DaleCalder, Royal Ont.lria Museum, Ivan Goodbody,University of the West Indies, and Jan Kohlmeyer,University of North Carolina, we are analyzing thesequence of settlement of species at differentseasons, following their growth and methods andhierarchies of competition.We have found that within days newsubstrates (wood, plastics) are colonized byubiquitous bacteria, fungi, and lower algae. Next toarrive are coralline algal crusts, sponges, hydroids,scyphozoan polyps (the polyp stage of the upsidedown jellyfish Cassiopea), anemones, serpulid andsabellid worms, bryozoans, and ascidians (the Ialtertwo are colonial, encrusting organisms). After 3 to 6months, substrates are fully covered by a spedrumof organisms. This spedrum varies greatly, anddepends on the season in which the experiment wasstarted, the habitat position of the substrate, and theenvironmental endurance of the selliers.Not all subtidal mangrove life is restricted tothe bottoms and roots. Fishes of all size and ageclasses hide or feed in the water column around thered mangrove roots and along the banks. Many ofthese depend on plankton, such as copepods andother small crustaceans (shrimp-like animals), forfood. Members of both groups form characteristicswarms during the day. Smithsonian's Frank Ferrariteamed up with Julie Ambler, Texas A&M University,Ann Bucklin, University of Delaware, and RichardModlin, University of Alabama, to study thesystematics, ecology, and genetics of the swarms andfound population densities much greater thaneXpeded. They counted more than 2,000 copepodsper cubic meter of water in a small bay at night, and20The Intertidal Mangrove Swamp A feature of many mangroves is that some part of the rootsystem is exposed to the atmosphere. In an oxygen-poorsubstrate, o)(ygen is absorbed directly (rom the atmosphere.In the black mangrove, lkese aerial roots, termedpneumalophor"es. occur as direct upward extensions of thesubteffilnean root syslem.

such as occupants of seagrass meadows (includingthe turtle grass itself), and mangrove mud banks andstilt roots, were killed during the long exposure fodesiccation. Estimates indicate that more species ofalgae and invertebrates, and much more livingmatter (biomass), were destroyed during those daysof June than during two hurricanes combined (Fifi,1974; Greta, 1978).Collaborating eco-physiologist Joan Ferraris,Mt. Desert Island Biological Laboratory, is examininga number of organisms (sponges, sipunculan worms,shrimps, crabs) that are exposed to strong salinitytemperature stress in their natural environment.Results so far show a fine correlation betweenexperimental tolerances in the animals and range ofvariability of stress factors in their natural habitat. Inthe case of sponges, regulatory mechanismscontrolling water-ion balances are still unknown, butin the absence of organs, they must take place insideindividual cells.Unfortunately, the intertidal swamp is notonly an exciting biological study zone, but also agallery of pollutants. Even in this remote locationevery imaginable piece of floating debris discardedby man can be found, washed in by currents amongthe mangrove roots and deposited by the recedingtides.Mangrove forest Above the TideUnlike the adjacent marine systems, the above-waterflora and fauna of the mangrove-covered islandsappear less complex and diverse. From the water, anunbroken, monotonous barrier of red mangrovetrees confronts, and frequently intimidates, thecasual explorer.The species composition of the above-waterplant community around Twin Cays is relativelysimple. Three halophytic· tree species, knowncollectively as mangroves, dominate the naturalvegetation on most of the islands: Red mangrove(Rhizophora), black mangrove (Avicennia), and whitemangrove (Laguncu/ar;a). On cays with slightly higherground, additional woody and herbaceous (softstemmed) halophytes are associated with themangrove, such as buttonwood (Conocarpus),saltwort (Batis), and sea purslane (Sesuvium).In general, mangrove forests have welldefined horizontal zonation. On these mangroveislands, the seaward and channel margins typicallyare fringed by dense, 4- to 1D-meter-tall stands ofred mangrove. Behind this fringe, the red mangroveis usually more open and shorter, with black andwhite mangroves intermixed. The zonation is easilyrecognized: dull gray-green spires of blackmangrove, and flattened, yellow-green crowns ofwhite mangrove stand slightly above and behind thedark green dome of the fringing red mangrove.The interiors of some of the larger islands offBelize, like Twin Cays, have several extensive,unvegetated mud flats and shallow ponds. A plant growing in salty soil or sail waler, lermed ahalophyte, has unique physiological characteristics thatenable ilto oblain fresh water, excrete salt, and reducefresh water loss.Numerous stumps throughout the mud flats areevidence that the trees that once grew there fellvictim to some environmental stress. The redmangrove trees growing around the margins of themud flats and in the ponds are severely stunted andwidely spaced. Over the years, these natural bonsaihave been distorted and pruned by theirenvironment intO fantastic forms, seldom more than1.5 meters tall.The above-water fauna on the cays isconsidered by most investigators to be introducedfrom the Belizean mainland. Even on the largestmangrove islands, most of the oland· is intertidal;therefore, the only environments available toterrestrial animals are arboreal. The fauna is limitedto birds, lizards, snakes, snails, and arthropods, suchas land crabs, spiders, and insects. These animalsprobably reached the cays from the mainland byflying, or rafting on or in pieces of wood and otherfloating debris.A few land bird species have establishedpermanent breeding populations on the mangroveislands. Warblers, vireos, hummingbirds, cuckoos,grackles, and white-crowned pigeons are among thepermanent residents. Several of the islands alsoprovide nesting sites for ospreys. These birdsfrequently build their nests atop tall snags of blackmangrove.At Twin Cays, the green-back heron is themost commonly observed wading bird. It breeds onthe island, and builds its twig nest in the redmangrove fringe along the channels. II is frequentlyseen diving for small fish in the shallow, interiorponds. The most conspicuous birds of the area arethe brown pelican and frigatebird, which flyoverhead or perch in mangrove trees.Insects are, by far, the most diverse andabundant group of above-water animals inhabitingthe Belizean mangrove cays. Ants, in 28 or sospecies, are clearly the most abundant. Termites,because of their huge nests and extensive coveredwalkways, are the most conspicuous. Some majorgroups of insects, such as bees, are poorlyrepresented in mangrove (auna. As is other tropicalecosystems, a large percentage of the insect speciesthat we have found associated with mangroves areundescribed.ConclusionsThe red mangrove fringe, the specialized vegetation,the physical environment, and the associated faunaand flora form a complex and diverse islandcommunity above water as well as below. We havelearned that mangroves produce fine sediments andorganic detritus. and stabilize them by modifying thewave and current regime of the open lagoon. Theinventory of species has yet to be completed, butalready we have shown that most phyla arerepresented by species of which 10 to 25 percent,and in some cryptic (having a hidden or concealedlifestyle) microscopic-sized groups, up to 60 percent,are undescribed. The mangrove swamp is rich inrecycled nutrients and high in production rates, butits occupants are severely stressed by factors such as21

A GallerySlinging sea anemone(Bunodeopsis) on lurtleM80Slon Bay, Twin Cays. Inlhe foregroond are propfOOU of red mangn:wesN8 n. obyG.Mme tRhilophora). (f tx"fl.o byK. RiJuSer)Black mangrove (Avkennia) pneomarophores.(Photo by M. Parrish)Sponges, ascidi;lns, and anemone on a submerged roor.(Photo by K. RutzlerJClapper rail. (fhala by S. Canupp)

of Mangrove LifeYoung upside-downSeahorse (Hippocampus).(PhOlo by G. Mil/ediellyfish (Cassiopea) onmud boflom.(PhOlO by K. ROlzler)Mangrove oyslers (Isogoomon). (Pholo by K.St,lftish (Oreasler). (PIJo(o by K. RilulerJRisrzlerJDrih goods deposited by 1M fidei under black mangrooves.(Pho(o by M.Parrish'

continued from p.osr 21salinity and temperature fluctuations, desiccationpotential, abundance of fine sediments, and shortageof firm substrates. Space, from the sea bottom to thetree tops, is distinctly partitioned by the animals thatexploit this specialized plant community. Theseintertidal islands, because of their isolation from theBelizean mainland, provide us with ideal locations tostudy pure mangrove communities in the Caribbean.Klaus ROIlier is Curalor of Lower Invertebrales and ProgramDireclor of Caribbean Coral Reef Ecosyslems (CCRE),National Museum of Nalural History, Smithsonian Institulion,Washinglon, D.C. Candy Feller is a freelance sdenlificiIIustralor, presently based in MeAlesler, Oklahoma.24AdtnowledgmentThe study described in this article is supported by grantsfrom the hxon (orpmaHon, the Smithsonian SCholarlyStudies Program, and the Smithsonian Women'sCommillee.SeIKt R fetenCftlugo, A. E. and S. C. Sr edaker. 1974. Tke e :oIogy of m,mgroves.AIInw! R 01 Ecology and Systematics 5: 39-64.Mal;nae, W. 1%8. A general account oflhe fauna and flora of""'ngrove swamps and forests in the Indo-West·PaciflC Regioo.AdvancE'l in Marine Biology 6: 73-270.Odum, W. E. C. C. Mcivor. and T. J. Smith. ilL 1981. The EcoIotNoirhe Mangroves 01 SO JIIl Florida:'" Community Profile. FWS/08S·81/24,144 pp. Reprimed Seprem r 1985. Washington, D.C.:U.5. Fish and Wildlife Service, OffICe of Biological Services.Tomlinson, P. B. 1986. Tile 80Iany 01 Mangroves. 413 pp.Cambridge. England: Cambridge University Press.

true mangroves. P. B. Tomlinson'srecent book, Botany ofMangroves, defines this groupof planls by five features: 1) they are ecologically restricted to tidal swamps, 2) the major element ofthe community frequently forms pure stands, 3) the plants are mOfphologically adapted with aer

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