DIVERSITY AND ECOLOGICAL SIGNIFICANCE OF DEEP-BURROWING MACROCRUSTACEANS IN COASTAL TROPICAL WATERS OF THE AMERICAS (DECAPODA: THALASSINIDEA)

Darryl L. Felder

Darryl L. Felder. Ph.D., Louisiana State University. Professor of Biology, University of Louisiana–Lafayette (ULL). Director of ULL–Laboratory for Crustacean Research. Associate Research Scientist, NMNH, Smithsonian Institution, Washington, DC. Address: Department of Biology, University of Louisiana, Lafayette, LA 70504-2451, USA. e-mail: dlf4517@louisiana.edu

Resumen

Los camarones talasínidos, comúnmente conocidos como camarones de lodo o camarones duende, son excavadores de madrigueras que dominan los substratos muebles y los procesos bentónicos en muchos ambientes marino-costeros. Entre los géneros más frecuentes en las zonas intermareales y someras submareales tropicales se cuenta con Lepidophthalmus y Callichirus, los cuales se asocian con estuarios fangosos y playas arenosas de cuarcita, respectivamente, y el menos conocido laomédido Axianassa, que se encuentra asociado con el mangle rojo. Estudios recientes sobre estos géneros excavadores y otros emparentados sugieren que el recambio de sedimento y la facilitación del flujo de nutrientes por la ventilación de la madriguera pueden ser de gran importancia para los autótrofos asociados, y pueden llegar a dominar los procesos bentónicos en algunas comunidades. Las perturbaciones del hábitat, la contaminación y las alteraciones hidrológicas pueden llevar a que poblaciones de estos excavadores obligados sean vulnerables a mortandades masivas, que son particularmente preocupantes en aquellas especies que han alcanzado un status endémico regional. Bajo otras circunstancias, el enriquecimiento orgánico de los substratos del hábitat, particularmente en parcelas de acuicultura, puede inducir crecimientos poblacionales explosivos. Cualquiera de estas dinámicas podría producir impactos negativos sobre la calidad del agua y la productividad, y contribuir a la declinación de las comunidades asociadas de plantas y animales. La conservación de estas comunidades de camarones excavadores requiere una comprensión completa de sus biohistorias, dependencia del hábitat, relaciones simbióticas, y respuestas poblacionales a las perturbaciones ambientales.

Summary

Deep-burrowing thalassinidean shrimp, commonly called mud shrimp or ghost shrimp, dominate soft substrates and benthic processes in many coastal settingAs. Among the more common genera in tropical intertidal to shallow subtidal areas are Lepidophthalmus and Callichirus, associated with muddy estuaries and quartzite sand beaches, respectively, and the less well-known laomediid genus Axianassa, associated with red mangroves. Recent studies of these and varied relatives suggest that sediment turnover by these deep-burrowers and facilitation of nutrient flux by burrow ventilation can be of major significance to associated autotrophs, and may dominate benthic processes in some communities. Habitat perturbations, contamination and hydrological alterations may render populations of these obligate burrowers vulnerable to mass mortalities, of special concern for those species that are regionally endemized. Under yet other circumstances, organic enrichment of habitat substrates, particularly in aquacultural settings, may induce explosive population increases. Either of these dynamics could result in negative impacts on water quality and productivity, and contribute to the decline of associated plant and animal communities. Conservation of these burrowing shrimp communities requires thorough understanding of their life histories, habitat dependencies, symbiotic relationships, and population responses to environmental perturbations.

Resumo

Os camarões talasínidos, normalmente conhecidos como camarões de lodo ou camarões duendes, são escavadores de madrigueiras que dominam os substratos móveis e os processos bentônicos em muitos ambientes marinhos-costeiros. Entre os gêneros mais freqüentes nas zonas intermareais e someiras submareais tropicais conta-se com Lepidophthalmus e Callichirus, os quais se associam com estuários lamacento e praias arenosas de quarcita, respectivamente, e o menos conhecido laomédido Axianassa, que encontra-se associado com o mangue vermelho. Estudos recentes sobre estes gêneros escavadores e outros aparentados sugerem que a remudança de sedimento e a facilitação do fluxo de nutrientes pela ventilação da madrigueira podem ser de grande importância para os autótrofos associados, e podem chegar a dominar os processos bentônicos em algumas comunidades. As perturbações do hábitat, a contaminação e as alterações hidrológicas podem levar a que populações destes escavadores obrigados sejam vulneráveis a mortandades em massa, que são particularmente preocupantes naquelas espécies que alcançaram um status endêmico regional. Sob outras circunstâncias, o enriquecimento orgânico dos substratos do hábitat, particularmente em parcelas de acuicultura, pode induzir crescimentos populacionais explosivos. Qualquer destas dinâmicas poderia produzir impactos negativos sobre a qualidade da água e da produtividade, e contribuir à declinação das comunidades associadas de plantas e animais. A conservação destas comunidades de camarões escavadores requer uma compreensão completa de suas biohistórias, dependência do hábitat, relações simbióticas, e respostas populacionais às perturbações ambientais.

KEYWORDS / Thalassinideans / Mudshrimp / Bioturbation / Burrowing /

Recibido: 09/04/2001. Aceptado: 10/08/2001

Ecology of thalassinidean shrimp in intertidal and subtidal marine and estuarine habitats has gained growing attention in literature of the last decade. Most recent ecological focus has been accorded to a limited set of genera assignable to several of the eleven families comprising this infraorder (see * in box). In accord with Tudge et al. (2000), the preferred nomenclature does not conform to that proposed by Sakai (1999). Also, as used here, the abbreviation "C." indicates species that remain treated under the genus Callianassa sensu lato, despite recent taxonomic restriction of that genus which excludes these species (see Manning and Felder, 1991).

INFRAORDER: THALASSINIDEA Latreille, 1831

Superfamily - Thalassinoidea Dana, 1852

Family - Thalassinidae Dana, 1852

Superfamily - Callianassoidea Dana, 1852

* Family - Callianassidae Dana, 1852

Callianassa sensu stricto, Biffarius,

Neotrypaea, Trypaea, Lepidophthalmus,

Callichirus, Sergio, Nihonotrypaea, Glypturus,

Corallianassa, Eucalliax, Neocallichirus,

"C." tyrrhena, "C." candida, "C." filholi,

"C." truncata,"C." kraussi, "C." laurae

Family - Ctenochelidae Manning and Felder, 1991

Family - Callianideidae Kossmann, 1880

* Family - Laomediidae Borradaile, 1903

Axianassa, Jaxea

Family - Thomassiniidae de Saint Laurent, 1979

* Family - Upogebiidae Borradaile, 1903

Upogebia

Superfamily - Axioidea Huxley, 1879

* Family - Axiidae Huxley, 1879

Axius, Axiopsis

* Family - Calocarididae Ortmann, 1891

Calocaris

Family - Micheleidae Sakai, 1992

Family - Strahlaxiidae Poore, 1994

As here evident, genera treated in modern ecological works are for the most part callianassids, a single family that includes a large number of intertidal and shallow subtidal representatives. Recent treatments of thalassinidean reproductive ecology have focused on recruitment, settlement stimuli, reproductive output and environmental constraints on reproduction of callianassids, while those in physiological and behavioral ecology have centered on ventilatory mechanisms, burrow construction and metabolic constraints imposed by hypoxia and reduced nutrients or contaminants in burrow waters for callianassids and members of several other families (Table I). Scant attention among these has been afforded to tropical populations of the Americas except in studies of burrow construction by the laomediid Axianassa australis Rodrigues and Shimizu in Brazil (Dworschak and Rodrigues, 1997) and recruitment and growth of the callianassid Lepidophthalmus sinuensis Lemaitre and Rodrigues on the Caribbean coast of Colombia (Nates and Felder, 1999). Ecological studies at the community and ecosystems level form a larger body of recent work, which calls attention to varied roles of thalassinidean populations in determining assemblage structure and their involvement in biogeochemically modulated processes (Table II). Major contributions in this arena over the last decade have centered on population dynamics, community composition, bioturbation, related geochemical effects, nutrient cycling, and food webs. Among these, works on populations of (at least in part) the callianassids Eucalliax jonesi (Heard) and Neocallichirus rathbunae (Schmitt) in the British Virgin Islands (Murphy and Kremer, 1992), the callianassids Glypturus acanthochirus Stimpson, Neocallichirus grandimana (Gibbes), Corallianassa longiventris (A. Milne Edwards) and axiid Axiopsis serratifrons (A. Milne Edwards) in Belize (Dworschak and Ott, 1993) and the callianassid Lepidophthalmus sinuensis on the Caribbean coast of Colombia (Nates and Felder, 1998) do demonstrate the potential significance of such populations in community and ecosystems level dynamics of the American tropics.

One implication of these studies, be they focused on American tropical or other environments, is that deep burrowing thalassinidean shrimp are repeatedly observed to dominate processes in a number of intertidal and subtidal habitats, where they often form dense aggregations. Aggregation may be favored by larvae adapted for estuarine retention or abbreviated development; in at least some cases, specific sedimentary cues favor dense and gregarious settlement of larvae. Physiology and behavior may be adapted to facilitate burrowing within and exploiting of hypoxic or even anoxic sediments for nutrients, with controlling consequences on populations of associated microbes, macrobenthos, rooted autotrophs, or planktonic autotrophs and heterotrophs of the overlying water column. Through their modulation of physiochemical parameters within porewaters and the overlying water column, the activities of thalassinidean populations may touch upon virtually all aspects of productivity in shallow marine systems. Regardless, the scope of this impact remains largely unmentioned in traditional treatments of coastal marine ecology, and the diversity of thalassinideans and their commensal associates responsible for these impacts remains markedly underestimated.

Aside from compiling major ecological works on thalassinideans from the last decade, the present paper briefly treats in further detail three genera among these animals, all now known to occur widely and often in dense accumulations throughout the American tropics, though species-level systematics in this region remain in part unresolved. Recent and ongoing studies of selected species among these genera, some not previously published, are herein used to further exemplify ecological roles of thalassinideans, especially in the context of environmental issues bearing on populations of the American tropics.

Populations of Lepidophthalmus along Warm-Temperate to Tropical Coastlines

Emphasis on this genus is warranted because of 1) its potentially dominant role in ecosystem processes of tropical estuaries, 2) its previously underestimated diversity and regional endemism in these habitats, and 3) perception of it as potential threat to penaeid shrimp aquaculture operations in the American tropics. Lepidophthalmus populates river mouths and oligohaline estuaries of the Atlantic and Pacific coasts, a distribution facilitated by its osmoregulatory ability in both adult and larval stages (Felder, 1978; Felder et al., 1986; Nates et al., 1997) and its remarkable adaptation to hypoxia in highly organic, sometimes sulfidic, coastal sediments (Felder, 1979; Nates and Felder, 1998; Bourgeois and Felder, 2001). Some species are widely distributed in shallow embayments, provided sediments are clayey or that clay-rich lamina are accessible to the animals for incorporation into burrow walls (Felder and Rodrigues, 1993; Felder and Griffis, 1994). Development appears to be abbreviated in members of this genus, often strongly so, favoring estuarine retention and thus limited dispersal (Nates et al., 1997).

This limited dispersal likely serves in part to maintain remarkable levels of endemism in this genus, most species of which were discovered only within the last decade (Figure 1A, B). Diversity appears to center in the American tropics, with distributions there often restricted to disjunct estuaries. Antitropically distributed warm-temperate forms (Felder and Rodrigues, 1993; Staton et al., 2000), to the north and south of a diverse core of tropical species, suggest a historical model in which members of this genus have been (perhaps repeatedly) compressed into tropical refugia by glaciation (Figure 1C). Given the restriction of this genus to shallow subtidal and intertidal habitats, direct effects of even small temperature changes, including contemporary global warming, could impact distributions.

Figure 1. a: Diversity and distribution of Lepidophthalmus as accepted in 1990. b: Diversity and distribution of Lepidophthalmus as known by late 2000, including four new species (n. sp.) currently in description. c: Proposed model for impact of glacial advance and retreat, as determinant of diversity and modern coastal species in American warm-temperate to tropical waters and as supported by distributions of Lepidophthalmus spp. d: Mean density for burrows of Callichirus islagrande and shoots of the cordgrass Spartina alterniflora, for three 15m transects across newly established cordgrass patches on bay side of Isles Dernieres, Louisiana, May 94. e: Schematic of the cycle of bioturbation or vertical conveyor in callianassids, which potentially entrains vegetation propagules. f: Schematic of typical habitats for Axianassa australis and its symbionts, where associated with mangrove-lined shorelines.

Dense accumulations of burrows, often exceeding several hundred per m², may occur in natural, perturbated or aquaculture pond settings (Felder and Griffis, 1994; Nates and Felder, 1999), sometimes adjacent to intertidal stands of grasses or fringing mangroves. A short maturation cycle, ready access to mates, high fecundity and limited dispersal of larvae all contribute to rapid, sometimes explosive population increases (Felder and Lovett, 1989; Nates and Felder, 1999). Intense bioturbation in these circumstances can rapidly bury associated epibenthic biota, leading to dominance of Lepidophthalmus among the benthic macroinfauna. Burrow depths can exceed 2m, and the cumulative surface areas provided by burrow walls markedly augment zones of redox transition in sedimentary environments.

Ecological studies to date have centered on the warm-temperate species L. louisianensis (Schmitt) from the Gulf of Mexico and the narrowly endemized tropical species L. sinuensis from the Caribbean coast of Colombia. In both species effluent waters can be richly charged with reduced nutrients (Felder and Griffis, 1994; Nates and Felder, 1998), and thus play a major role in nutrient cycling. It is, however, noteworthy that comparable recent samples of effluent waters from burrows of L. bocourti (A. Milne Edwards), L. eiseni Holmes and L. "sp. D" (DLF, in description) in sandy river mouths along the tropical Pacific coast of Nicaragua to date do not exhibit such marked elevations of reduced nutrients, even though redox levels are comparable; this may reflect the generally nutrient-poor state of some tropical estuaries.

Several Lepidophthalmus spp. opportunistically invade hypoxic bottom sediments of coastal shrimp mariculture farms. L. sinuensis, an undescribed species at the time it invaded mariculture ponds near the mouth of the Rio Sinú, Colombia (Lemaitre and Rodrigues, 1991), affords the best-documented case of such an invasion. Highly organic pond sediments, enriched by feeding of the penaeid shrimp under culture, appeared to there provide near optimal habitats for rapid colonization and explosive population increases, with burrow densities at times exceeding 1000/m². Detrimental impacts on penaeid shrimp likely stemmed from combined effects of callianassid bioturbation and burrow ventilation, both of which re-suspended highly reduced nutrients (including ammonia and sulfides). Toxicity and BOD of these materials both potentially contributed to negative effects on growth and survival of cultured penaeids. Diel oxygen lows, depressed by BOD and respiratory demands of the thalassinideans themselves (which often exceeded areal biomass of the penaeid shrimp under culture), reached stressful levels. In addition, extreme bioturbation rates may have contributed to burial of penaeid shrimp artificial feeds distributed onto the pond bottoms (Nates and Felder, 1998; 1999).

L. louisianensis is also now known to have invaded shrimp farms in the western Gulf of Mexico (Tamaulipas, Mexico), and an undescribed species, "L. sp. D", along with other taxonomically questionable members of what is sometimes called the "L. bocourti complex", have invaded shrimp farms on the Pacific coast of Colombia, Panamá and Costa Rica. Observed densities and effects to date are not apparently of the scale observed with L. sinuensis, but early control programs may have avoided such impacts. Even in the case of L. sinuensis, moderate densities of this species in shrimp farms, comparable to densities observed in natural rather than aquaculture settings, can be of potential benefit rather than harm to penaeid shrimp production (Nates and Felder, 1998). This perhaps demonstrates direct potential benefits these thalassinidean populations to secondary production, albeit in the somewhat atypical mesocosm of a shrimp farm. Such might be expected with moderate and continuous rates of nutrient re-suspension, bioturbation and oxidation of sediments, as may occur in stable natural populations of these thalassinideans. Such optimal population densities have been achieved in these aquaculture settings, with benefits to penaeid production, but to date only by use of pesticides for population control.

Control has focused primarily on applications of either carbaryl (Sevin®) or the organophosphate trichlorfon (Neguvon®). These are used either to limit the above-discussed direct impacts of thalassinidean invasions or for more general extermination of broader groups of local aquatic species from pond waters, the latter strategy targeted to eradication of putative penaeid shrimp disease vectors. While the use of carbaryl for control of thalassinideans has been studied in open estuarine habitats of the US northwestern Pacific coast (Dumbauld et al., 1997), the efficacy of such practices in distinctly warmer tropical aquaculture settings is largely undocumented, and regulation throughout tropical America appears very limited and poorly enforced. Acute toxic effects of trichlorfon, while believed to be not as persistent as organochlorines, remain poorly known and are reported to become elevated in some marine crustaceans at higher temperatures such as those occurring in tropical estuaries (Brecken-Folse et al., 1994; see also, Extension Toxicology Network, http://pmep.cce.cornell.edu).

As Lepidophthalmus spp. appear to be highly endemized within the tropics, where they may contribute in substantive or even dominant ways to essential benthic processes of the natural estuaries they inhabit, it is urgently important that potential impacts of pesticides and other potential perturbations to their habitats be included in regional conservation and management planning for the coming millineum. This group of thalassinideans may represent but one of many burrowing invertebrate taxocenes in which both diversity and ecological roles have been long undervalued.

Populations of Callichirus in Coastal Louisiana

By contrast to the above taxocene, Callichirus is commonly encountered in intertidal to shallow subtidal beach environments of open shores or embayments, usually where sediments are comprised heavily of siliceous sands in "swash" and subtidal bar zones, and often along quartzite beaches of relatively high wave energy (Felder and Griffis, 1994; Rodrigues and Shimizu, 1997). Larval history is more protracted than in Lepidophthalmus spp. (Strasser and Felder, 1999a; 2000). The genus ranges widely from temperate to tropical shores, but is of special interest along tropical American coastlines because of 1) its frequent dominance of sandy shoreline infaunal assemblages and processes, 2) its vulnerability to tropical storm perturbations of the readily transported substrates it occupies, and 3) its occupation of sites that are commonly coated by oil and other pollutant spills as they wash ashore. Taxonomy of the group is problematic, with newly defined relationships in even well-studied temperate to warm-temperate habitats yet to be reflected in nomenclature, and relationships in tropical waters currently under study by molecular methods (Staton and Felder, 1995; Felder, unpublished). While even recent references (and herein Figure 2) may refer to populations of "Callichirus major" from the American tropics and Gulf of Mexico, that species C. major (Say) sensu stricto is most likely restricted to the Atlantic US coast, Florida and northward along the US Atlantic coast. Others so labelled from the Gulf of Mexico, Caribbean and Brazil must eventually be assigned to separate taxa. Other species that range into the American tropics include populations of C. islagrande (Schmitt) (Figure 3A) in the Gulf of Mexico and varied tropical Pacific populations currently assigned to C. garthi (Retamal) or C. seilacheri (Bott); however, broad applications of these taxonomic assignments are best considered provisional until ongoing molecular studies are completed.

Figure 2. Mean sand elevations and population densities for two species of Callichirus (as estimated from burrow counts) for three transects across Isles Dernieres, Louisiana, from September 91 (prior to Hurricane Andrew in August 92) and three occasions following the storm. In September 91 no burrows were present across center (higher elevations) of the island. For February 95, counts are shown only for the zone that was heterogeneously populated by patches of the cordgrass Spartina alterniflora.

While studies in the northern Gulf of Mexico are focused on warm-temperate populations of Callichirus, they exemplify ecological dynamics and environmental threats as also applicable to many tropical American populations. The potential for mass mortality and population redistribution was demonstrated strikingly along barrier islands of coastal Louisiana following landfall of Hurricane Andrew in August 92 (Figure 2). Long-established populations of C. islagrande along beaches facing the Gulf of Mexico were eradicated by wave-erosion and transport of the sands they formerly occupied. However, in storm wash-over fans, a fraction of this population apparently survived the initial relocation and re-burrowed, as evidenced by the rapid appearance of a few mature adults in highest elevations of the newly deposited fan where no populations of Callichirus spp. were observed before, and the temporary augmentation of bayward populations of both C. islagrande and "C. major" that were covered by the new wash-over fan (Figure 2).

It is noteworthy that the dynamics described above occurred while populations were being monitored in coastal Louisiana to establish baseline population censuses (through 1994), in the event that future oil spills should impact population densities. While oil spills clearly impact this species (Thebeau et al., 1981; Amos et al., 1983), it is clear that catastrophic changes in population structure also occur in response to natural perturbations like storms. The confounding of natural storm and spill effects has previously clouded interpretations in studies along beaches of Texas (Thebeau et al., 1981). However, where these impacts occur independently, the means and timecourse of population recovery could differ markedly. Recovery of the Gulf beach population at Isles Dernieres was well underway as beach sands naturally accumulated during 18 months following the storm (Figure 2), and (while not monitored in February 95) populations there had reached a mean density of 31/m² by May 95 (of no significant difference from pre-storm densities). From size classes in samples, it was evident that re-population of the Gulf beach between September 92 and February 94 occurred almost exclusively by way of newly settled recruits (decapodids), most of which accumulated between May and September 93. Cues to settlement of this species have recently been the subject of several studies (Strasser and Felder, 1998; 1999b; 2001), and contact with the sand was found to play a highly significant role in stimulus of metamorphosis and burrowing. It would thus be of great interest for such studies to also be conducted with sands variously contaminated with oil and oil degradation products, to determine the magnitude and duration of possible impacts on recruitment.

The Isles Dernieres study produced some provocative observations of proximal events as the bayward beaches of the storm wash-over fan were slowly reworked through 1994 and early 1995 (Figure 2). Where dense populations of C. islagrande (79/m²) had existed in a sloped beach prior to the storm, overlayment by sand and isolation from routine tidal inundation contributed to a marked decline by February 1994. Transect means in this region ranged from 12-13/m² throughout most of 1994, but were very heterogeneous with most of this mean number accounted for by denser populations (up to 63/m²) in depressions that were more frequently flooded by at least by the more extreme high tides. By early summer of 1994, new growth of cordgrass shoots (Spartina alterniflora Loisel.) began to appear throughout these depressions, and transects were established to monitor densities of both the plant shoots and burrow numbers, which were highly correlated (p <0.001) (Figures 1d, 3b-c). Examination of small shoots suggested that all were sprouted from sand-entrained propagule fragments rather than seed, and it is hypothesized that entrainment was facilitated by the bioturbating activity of C. islagrande (Figure 1e), which may also have contributed to plant nutrition. Viable seed was uncommon in the immediate area, and had not been observed previously in sparse stands of S. alterniflora that had occupied limited areas of this shoreline prior to the storm. However, by October 94, these stands of S. alterniflora were densely vegetated and heavily endowed with maturing seed (Figure 3d), remarkably more so than in conspecific stands of cordgrass on the opposite (landward) side of the bay.

Figure 3. a: Mature male of Callichirus islagrande from northern Gulf of Mexico. b: One of several newly established patches of the cordgrass Spartina alterniflora, sculptured by dense burrows of C. islagrande, along the bayward side of Isles Dernieres, Louisiana, in May 94. c: Close-up of flooded burrows of C. islagrande, adjacent to shoots of S. alterniflora, near middle of area featured in b, in May 94. d: Mature, seed-bearing patch of cordgrass S alterniflora, side view of area featured in b, in October 94. e: Mature male of Axianassa australis from mud flats near red mangroves in Indian River Lagoon, southeastern Florida, USA. f: Polyester resin casting of burrow from A. australis, with associated Phacoides pectinatus, same locality as in e. g: Partially recovered casting of burrow from A. australis, including some of the lucinid bivalves (P. pectinatus) that adhered to the casting at varied positions, same locality as in e. h: Close-up of live lucinid bivalves P. pectinatus recovered in contact with burrows of A. australis, same locality as in e.

While cordgrass reproduction in coastal Louisiana is generally reported to occur by way of propagules, and the limited local seed production is usually of low viability, a small sample of this seed exceeded 70% germination in the laboratory. It thus compels further study of the possible role that an associated thalassinid like C. islagrande might play both in the entrainment of propagules and in plant nourishment. The latter could be facilitated by nutrient-loaded burrow effluent waters and fecal pellet production, both of which are well documented (Felder and Griffis, 1994). However, controlled experimentation must be undertaken to confirm this possible relationship.

Populations of Axianassa australis Associated with Tropical Red Mangroves

Axianassa, at least as presently constituted, is a broadly distributed genus ranging onto continental shelves of primarily tropical waters, though present focus is restricted to shallow subtidal and intertidal forms. Formerly thought to be rare, only nine specimens from American waters were known when the genus was last revised taxonomically (Kensley and Heard, 1990). However, the animals appear to be not so rare as they are difficult to collect. Discussion of one species, A. australis (Figure 3e), is included here primarily because this species is now known to be 1) a common and widespread burrower among coastal mangroves and adjacent mud flats, 2) the architect of remarkable burrows sheltering a newly discovered assemblage of poorly known symbionts, and 3) yet another thalassinidean group apparently adapted to strongly reduced, sulfidic environments.

The distribution of laomediid A. australis in the western Atlantic is, in contrast to those of the callianassids discussed above, very broad. It herewith can be confirmed to range from Brazil (the type locality) to Florida, with the distribution including extreme south Texas and the southwestern Gulf of Mexico. Its range in the western Atlantic very nearly matches that of the red mangrove (Rhizpora mangle L.) with which it is commonly, though not exclusively, associated (Figure 1f). Duration of larval development, also currently under study, is protracted, involving a comparatively large number of planktonic stages which would favor wide dispersal.

Among the several remarkable attributes of these animals are their burrows, which appear to occur from near the low tide mark throughout intertidal mudflats that include decomposing roots or other interred vegetation, and well into dense stands of living red mangroves (Figure 1f). Among living prop roots, the animals appear to reside well below the densest concentration of living rootlets in strongly hypoxic and sulfidic muds, sometimes in or near "voids" of hypoxic waters which can sometimes be detected as coring tools break through the dense rootlet mat. Extractions from such areas on the Caribbean coast of Colombia, lower Atlantic coast of Florida, and extreme south Texas have produced a previously undescribed assemblage of associated macrocrustaceans including yet other laomediids, alpheoid shrimp, and brachyuran crabs that are apparently new to science. Males and females of A. australis are usually captured together as one pair per burrow, and are almost invariably accompanied by at least one male and female pair of symbiotic alpheoid shrimp (see also Dworschak and Coelho, 1999).

While aggregated in preferred habitats, burrow densities of A. australis do not appear to be high, seldom exceeding 4-5/m², but large amounts of detritus-laden sediment and water issue from them during tidal exposure. Where possible to retrieve burrow castings, it is clear that the burrows are often >1m in depth, expansive, and among the most uniquely sculptured of those known for thalassinideans (Figure 3f). First cast in Brazil (Dworschak and Rodrigues, 1997), the spiral elements appear to be unique to the group and remain of questionable function; among possibilities would seem optimization of the burrow wall surface area for microbial linings or porewater exchange, concentrated mining of selected sediments in the course of deposit feeding, deterring movement through burrows by predatory fishes, and ramping of the burrow to facilitate locomotion. A previous explanation invoked entrainment of thalassinideans in turbulent sediment flows as "doomed pioneers" to account for such spiral castings in the fossil record (Grimm and Föllmi, 1994); while castings of living forms would now cast doubt on that interpretation, is noteworthy that the paleoecological settings for these fossil finds were interpreted as oxygen-depleted and richly organic, much is observed in the modern setting.

Newly noted is the association of these burrows with large numbers of lucinid bivalves, particularly along mangrove-dominated mud banks of the Indian River Lagoon system in eastern Florida and on some degrading seagrass flats of extreme south Texas. In Florida, specimens of what appears to be the bivalve Phacoides pectinatus Gmelin commonly adhere to the burrow cast or partially occlude penetration of the resin fully into the burrow lumen (Figures 3g, h). As burrow casts are excavated, it is also evident that yet other individuals of this clam are closely associated with the burrow lumen, touching it or accessing it across a small gap (Table II). Up to 37 living specimens of these bivalves have been to date retrieved from a single burrow. Living examples have been taken from sediment depths near 1m, even though they lack typical incurrent siphons. However, Phacoides and related lucinids have gills richly invested with symbiotic, sulfide-metabolizing, chemoautotrophic bacteria, and appear to be highly adapted in exploiting sulfidic substrates as an energy source. Thus, the burrow they share may serve to provide them access to rich stores of sulfide, including resources at otherwise inaccessible depths. As to what benefits this relationship might bring to Axianassa, to its alpheoid shrimp symbionts (Dworschak and Coelho, 1999), or to other yet-to-be-described burrow associates, little can be offered at present. Other symbioses between thalassinids and bivalves have been reported (see for example, Kato and Itani, 2000), but these do not appear related to exploitation of sulfides.

Even in tropical marine settings as common as coastal marine mangroves, we have only begun to appreciate the diversity of infaunal assemblages such as here described. It is an even larger and perhaps more urgent task to understand their function and significance. Doing so before we lose this opportunity to environmental degradation and global change is an urgent challenge for the 21st Century.

ACKNOWLEDGEMENTS

The above research benefited from assistance of L. Bilodeau, R. Bourgeois, E. Garcia, R. Griffis, L. LeBlanc, R. Lemaitre, R. Manning, L. McGraw, E. Mouton, S. Nates, J. Neigel, R. Robles, C. Schubart, J. Staton, K. Strasser and T. Zimmerman. Financial support was provided by Grant No. DE-FG02-97ER12220 from the US Department of Energy and by cooperative agreement 00CRAG0009 from the US Department of Interior (USGS/US-AID program). Thanks are also extended to J. Conde and the entire Comisión Organizadora del Simposio "Ecología Tropical para el Siglo XXI" (IVIC) for their invitation to participate in the symposium and contribute this paper. This is contribution number 79 from the UL Lafayette Laboratory for Crustacean Research and number 529 from the Smithsonian Marine Station - Fort Pierce.

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