Benthic Animals in Mangrove Swamp: A Revie forest (tree height: ca. 30 m) in southern Thailand. Most species, including polychaetes (Leonnantes ... Benthic Animals in Mangrove Swamp:

REVIEW ARTICLE 183

Global Environmental Research ©2013 AIRIES 17/2013: 183-188 printed in Japan

Benthic Animals in Mangrove Swamp: A Review

Keiji WADA

KYOUSEI Science Center for Life and Nature, Nara Women’s University,

Kitauoyahigashimachi, Nara 630-8506, Japan e-mail: [email protected]

Abstract This paper reviews the current knowledge of macrobenthic animals in mangrove swamps, focusing on

their spatial organization and ecological functions. Spatial patterns are described separately for arboreal ani-mals and animals living on the bottom, in dead wood, and in rivulets. Some sesarmid crabs and snails graze on higher proportions of mangrove litter in various parts of the world. Positive influences of macrobenthic ani-mals on mangrove plants have been identified: sesarmid crabs and fiddler crabs are beneficial to the growth of mangrove trees, and some fouling and boring animals enhance the growth of mangrove prop roots.

Key words: macrobenthic animals, mangrove swamp, positive interaction, spatial organization

1. Introduction

Mangrove swamps contain diverse marine and ter-

restrial fauna. Mangrove-associated animals depend on the environment created by mangrove plants and they, in turn, affect mangrove plants. The faunal composition of mangrove swamps and their spatial organization have been described in various tropical areas (e.g., Berry, 1963; Macnae, 1966; Day, 1974; Sasekumar, 1974; Frith et al., 1976; Shokita et al., 1989). The intimate interrela-tionships between animals and mangrove plants have recently been unraveled (e.g., Perry, 1988; Ellison et al., 1996; Lee, 1998; Cannicci et al., 2008; Kristensen, 2008; Smith et al., 2009; Chen & Ye, 2010). Knowledge about the faunal composition of mangrove swamps and rela-tionships among mangrove plants and associated fauna are important for understanding the ecological structure of mangrove ecosystems.

This paper reviews two aspects of benthic animals that occur in mangrove swamps: faunal composition and their spatial organization, and the ecological roles of benthic animals.

2. Benthic Animals and Spatial Organization

The spatial organization of benthic animals can be

described according to distinct habitat types. Arboreal animals are found on leaves, stems and aerial roots of mangrove trees. Littorinid snails live on leaves or stems in the supratidal to uppermost intertidal zones. Their vertical zonation in Japan and Indonesia has been de-scribed as Littoraria pallescens on leaves in the upper-most zone (Fig. 1), L. scabra on stems in the middle level, and L. intermedia on stems in the lower level (Ohgaki,

1992; Boneka, 1994). The bark of lower stems and aerial roots is inhabited by several gastropod species, such as Nerita spp. and the pulmonates Cassidula mustelina and Melampus coffeus (Berry, 1963; Proffitt & Devin, 2005).

Typical arboreal crabs include the sesarmids Aratus pisonii, Armases elegans, and Parasesarma leptosoma, all of which spend their entire adult life on trees. Aratus pisonii, a Caribbean species, moves up to six meters above the ground to feed on mangrove leaves and buds (Hagen, 1977: Beever III et al., 1979). Parasesarma leptosoma occurs in East African mangrove forests and shows vertical migrations from the lower part of the man-grove aerial root to the canopy of the tree (ca 12-13 m height) to forage on leaves (Vannini & Ruwa, 1994). This species has recently been found to forage on mangrove flowers on Iriomote Island, Japan (Takaso, unpublished). Parasesarma leptosoma also shows conspicuous tree fidelity: crabs that were moved to trees seven meters away returned to the original tree within a few days (Cannicci et al., 1996).

Fig. 1 An arboreal snail, Littoraria pallenscens.

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Mangrove roots, trunks, branches, and leaves bear rich sessile animals, including sponges, hydroids, anemones, polychaetes, bivalves, barnacles and ascidians. The most conspicuous are barnacles (Balanus spp.), which foul trunks, aerial roots, and leaves (Fig. 2). Zonation in sessile animals on red mangrove prop roots was described by Rützler (1995); the mangrove oyster Isognomon alatus occupied the uppermost part, followed by the sponges Haliclona implexiformis and Lissodendoryx isodictyalis, and the lower area was oc-cupied by the sponge Scopalina ruetzleri.

Macrofauna that live underground in mangrove for-ests show vertical zonation. The dominant animals are crustaceans, mollusks and polychaetes. Shaded areas under the mangrove canopy are inhabited by various decapod crustaceans. The most conspicuous is the mud shrimp Thalassina anomala (Fig. 3), which constructs large mounds and burrows that are 2.5 m deep (Sankolli, 1963). The mounds created by this species harbor many other benthic animals, such as sesarmid crabs. Sesarmid crabs are generally decomposers of mangrove litter and are most common in forested areas. Benthic animals in forested areas are difficult to sample quantitatively be-cause of the underground root systems. However, Wada et al. (1987) investigated the depth distributions of bur-rowing animals to a depth of one meter in a natural man-

grove forest (tree height: ca. 30 m) in southern Thailand. Most species, including polychaetes (Leonnantes sp., Glycera sp. and Dasybranchus sp.) and sesarmid crabs (Chiromanthes haswelli, Sarmatium germaini, Neosarmatium smithi (Fig. 4) and Clistocoeloma merguiense), occurred above 60 cm depth and only two crustaceans, Alpheus euphrosyne (Fig. 5) and Callianasa ranongensis, were found from the shallow layer to the bottom layer (1 m depth).

Nakasone (1977) described the vertical zonation of brachyuran crabs in a mangrove swamp in Okinawa, Japan. The uppermost supratidal area was occupied by land crabs such as Cardisoma carnifex and was termed the cardisomine zone. This was followed by the upper intertidal area under mangrove stands, which was occu-pied by sesarmid crabs (the sesarmine zone). The middle intertidal area of open flats was occupied by fiddler crabs such as Uca perplexa (Fig. 6; the ocypodine zone). This was followed by the lower intertidal area, which was occupied by macrophthalmid crabs such as Macrophthalmus convexus (Fig. 7; the macrophthalmine zone); a mixed zone; and the lowermost subtidal area, where the portunid crab of Scylla spp. occurred (the Scylla zone).

The zonation of mollusks in mangrove forests has a Littorina zone, represented by Littorina scabra and L. melanostoma, on the upper parts of trees; a Nerita zone, represented by Nerita birmanica and N. planospira, on the lower parts of trees and on the mud surface; and a

Fig. 2 Barnacles encrusting a mangrove trunk.

Fig. 3 The mud shrimp Thalassina anomala in a mangrove forest.

Fig. 4 The sesarmid crab Neosarmatium smithi in a mangrove forest.

Fig. 5 The pistol shrimp Alpheus euphrosyne in a mangrove forest.

Benthic Animals in Mangrove Swamp: A Review 185

bivalve zone, represented by Enigmonia rosea and Trapezium sublaevigatum, on the mud surface of the seaward fringe of forested areas (Berry, 1963).

Dead wood (Fig. 8) has characteristic fauna that live on the wood surface, such as gastropods and barnacles, and inside the wood, including boring animals such as the bivalve Teredo and sphaeromatid isopods. Interstices in rotten wood are inhabited by the gastropod Ellobium (Fig. 9), grapsoid crabs, sea anemones, and sipunculids. However, dead wood fauna in mangrove swamps have not yet been studied quantitatively.

Rivulets bear fauna that differ from other habitats in mangrove swamps. They include both a variety of fish larvae and mudskippers. In mangrove swamps in the Ryukyu Islands, rivulet bottoms are inhabited by brachyuran crabs of Scylla and Deiratonotus cristatus (Fig. 10), and shrimps of Palaemon and Penaeus. Benthic animals in mangrove channel areas have not yet been surveyed quantitatively.

3. Mangrove Litter Decomposers

Stable isotope analysis suggests that fiddler crabs and

bivalves consume algae, and grapsoid crabs and gastro-pods eat a variety of food items, from algae to mangrove plants (Rodelli et al., 1984). Grapsoid crabs and some gastropod species function as decomposers of mangrove litter. The most well-known are sesarmid crabs, which graze on litter or bury litter in their burrows for later

feeding. These species include Sesarma plicata in China (Chen & Ye, 2008); Perisesarma eumolpe and P. onychophorum in Peninsular Malaysia (Malley, 1978; Ashton, 2002); Sesarma messa, Sesarma erythrodactyla, and Neosarmatium smithi in Australia (Giddins et al., 1986; Robertson, 1986; Camilleri, 1989; Micheli, 1993); and Sesarma guttatum, Sesarma ortmanni, and Neosarmatium meineriti in East Africa (Emmerson & McGwynne, 1992; Dahdouh-Guebas et al., 1999). In Brazil, litter consumption is led by the ocypodoid crab Ucides cordatus (Nordhaus et al., 2006; Nordhaus & Wolff, 2007). It is estimated that this species eats

Fig. 8 Dead wood in a mangrove swamp.

Fig. 9 A pulmonate gastropod, Ellobium sp., in dead wood in a mangrove swamp.

Fig. 10 Deiratonotus cristatus in a rivulet of a mangrove swamp.

Fig. 6 The fiddler crab Uca perplexa near a mangrove forest.

Fig. 7 Macrophthalmus convexus on an open flat around a mangrove forest.

186 K. WADA

approximately 81% of total litter fall from mangroves (Nordhaus et al., 2006). In Australia, the sesarmid crab Sesarma messa can remove 28% of the annual litter fall of Rhizophora stylosa (Robertson, 1986). In southern Africa, Sesarma meinerti is estimated to consume 44% of leaf litter from Avicennia marina (Emmerson & McGwynne, 1992).

Some gastropod species are also responsible for the degradation of mangrove litter. The potamidid snail Terebralia palustris (Fig. 11) is a grazer of mangrove leaf litter in Japan (Nishihira, 1983) and Kenya (Slim et al., 1997; Fratini et al., 2004). Mangrove leaves on the sub-strate surface are grazed on by aggregations of large snails of this species (Nishihira, 1983), but juvenile snails do not graze on leaves (Slim et al., 1997). In African mangroves, it is estimated that 11.2% and 18.6% of litter is processed by macrobenthic animals, including Terebralia palustris, in Ceriops tagal and Rhizophora mucronata vegetation, respectively (Slim et al., 1997). In Florida, USA, the pulmonate gastropod Melampus coffeus consumes 40.5% of the litter from Rhizophora mangle and Avicennia germinans (Proffitt & Devlin, 2005). Recently, cellulase activity has been found in the potamidid snail Terebralia palustris (Niiyama & Toyohara, 2011) as well as some sesarmid crabs (Adachi et al., 2012), which indicates that the ability to digest cellulose using enzymes is responsible for the breakdown of mangrove litter by these animals.

4. Positive Influences of Macrofauna on

Mangroves Fiddler crabs in salt marshes have beneficial effects

on marsh plants (Bertness, 1985); similarly, sesarmid crabs have a positive influence on mangroves. Smith III et al. (1991) was the first to demonstrate such positive effects of burrowing crabs (mainly Sesarma messa and S. temperi) through field manipulation experiments in Rhizophora-dominated forests in Australia. They found that when crabs were removed by pitfall traps over a twelve-month period, there was a significant reduction in cumulative forest growth (measured as the stipule fall rate) and increased soil sulfide and ammonium concen-trations. Similar experiments were conducted in a Florida

mangrove swamp by Wada and Hines (unpublished), in which the removal of fiddler crabs (Uca pugilator and U. rapax) via pit traps caused a significant decrease in mangrove (Avicennia germinans) survivorship after two years. Smith et al. (2009) also examined the effect of fiddler crab presence on the mangrove Laguncularia racemosa in a Florida mangrove swamp. They found that the removal of fiddler crabs over a one-year period caused significant decreases in mangrove growth and leaf production, together with increases in interstitial water salinity and the oxidation-reduction potential of low- organic sediments. Predation on mangrove propagules can cause damage that hinders mangrove regeneration. In Australia, seed predation by grapsoid crabs affects ca. 75% of the seeds on the bottom surface (Smith III, 1987). However, some propagules are found inserted into crab burrows, with some parts grazed (Fig. 12). On Amami- Oshima Island, a similar phenomenon has been observed in burrows of the grapsoid crab Pseudohelice sub-quadrata (Fig. 13). It is likely that by carrying propagules into burrows, these crabs enhance the regen-eration of mangrove plants.

The boring isopod Sphaeroma peruvianum and the encrusting barnacle Balanus spp., which are closely associated with prop roots of the mangrove Rhizophora mangle, cause 50% and 30% reductions in the root growth rate, respectively (Perry, 1988). However, these effects are indirectly mediated by predation by the snails Thais kiosquiformis and Morula lugubris and the hermit

Fig. 11 The potamidid snail Terebralia palustris grazing on mangrove leaves.

Fig. 12 A propagule inserted into a crab burrow.

Fig. 13 The grapsoid crab Pseudohelice subquadrata, which is common in mangrove swamps in southern Japan.

Benthic Animals in Mangrove Swamp: A Review 187

crab Clibanarius panamensis (Perry, 1988). On the other hand, the boring isopod can be beneficial to mangroves. Damage to prop roots by this boring animal causes branching, so that the number of roots that actually reach the soil surface increases, helping to stabilize the man-grove tree (Simberloff et al., 1978).

Mangrove roots host a range of epibionts, such as macroalgae, barnacles, mollusks, sponges, tunicates, serpulid annelid worms, hydroids, and bryozoans. En-crustations of these organisms can reduce root growth. For example, encrustation by the barnacle Balanus can decrease root production by 52% by blocking lenticels and reducing gas exchange and respiration (Perry, 1988). In contrast, epibionts can benefit mangrove roots in some cases. Ellison and Farnsworth (1990, 1992) found that epifaunal sponges and ascidians reduced damage to the roots of Rhizophora mangle by wood-boring isopods. Foraging by some ocypodoid crabs on prop roots (Fig. 14) can be beneficial for mangroves because the activity removes algae and mud covering the root surfaces (Wada & Wowor, 1989).

Symbiotic nutrient exchange occurs between man-grove roots (Rhizophora mangle) and fouling sponges (Tedania ignis and Haliclona implexiformis) (Ellison et al., 1996). A transplant experiment that moved sponges to bare roots found significant increases in root growth. Furthermore, the transplanted sponges grew 1.4 to 10 times faster than control sponges that were attached to PVC pipes in the same habitat. That study also provided evidence that mangrove roots obtain inorganic nitrogen from sponges and that sponges obtain carbon from mangrove roots.

5. Concluding Remarks

Due to the diversified environmental conditions cre-

ated by mangrove plants, the diversity and spatial organization of macrobenthos are yet to be fully de-scribed. For example, few quantitative studies have de-scribed the zonation of macrobenthos because it is diffi-cult to dig into substrates containing mangrove root sys-tems. The spatial organization of organisms living in unique habitats, such as dead wood and rivulets, has not

yet been studied. The faunal diversity and spatial organization of such habitats represent significant gaps in our understanding of the structure of mangrove eco-systems.

Macrobenthos are important functional components in mangrove swamps through their feeding or burrowing activities. Litter grazing by grapsoid crabs and snails can enhance nutrient processing and contribute to ecosystem function. Burrowing activities by crabs can also be beneficial for mangrove plants. Such positive interac-tions demonstrate the importance of these animals for maintaining mangrove ecosystems. This knowledge is of prime importance for the conservation and restoration of mangrove ecosystems, which are being degraded and lost worldwide. Acknowledgements

I am grateful to two anonymous reviewers for their

valuable comments for improving the manuscript.

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Keiji WADA Keiji WADA is Director of the KYOUSEI Science Center for Life and Nature at Nara Women’s University. He is interested in biodiversity of coastal environments including mangrove swamps, with a focus on behavior, ecology and taxonomy of intertidal crabs. His main published books are Threatened Animals of

Japanese Tidal Flats: Red Data Book of Seashore Benthos (Tokai University Press), Ecology of Marine Benthos (Tokai University Press), Natural History of Tidal Flats (Kyoto University Press), and Guide to Seashore Animals of Japan, with Color Pictures and Keys, Vol. II (Hoikusha Publishing).

(Received 26 November 2012, Accepted 19 June 2013)