A field guide to Kenyan mangroves

Review of Kenyan mangrove flora and fauna with an emphasis on adaptations to this biotope

1.0 Definition and general setting

Mangroves are salt-tolerant trees and shrubs that usually grow in the intertidal zone throughout the tropics and sub-tropics. They are most often located along sheltered shores and can penetrate deep into the estuaries of rivers (Macnae, 1968). Mangroves trees have a very plastic form; the same species can grow as a short stunted bush in unfavorable conditions or as a full sized tree reaching heights of 40 meters, forming dense forests several kilometers thick under favorable conditions (Macnae, 1968).

The word ‘mangrove’ may be applied to the entire community or to any one of the individual trees within that community. This, at first, may seem confusing, but when taken in context it is not. Some authors have used the word ‘mangrove’ for the individual trees and ‘mangal’ for the community, I however prefer ‘mangrove forest’ or ‘forest’ when the term ‘mangrove’ alone may possibly bring confusion.

Mangrove forests can be composed of both true mangroves (including both major and minor components) and mangrove associates. Tomlinson (1986) separates these two groups by defining true mangroves as those species that possess all or most of the following elements:

• Complete fidelity to the mangrove environment;
• Play a major role in the structure of the forest and can form pure stands;
• Morphological specialization that adapts them to their environment (e.g. aerial roots and vivipary);
• Physiological mechanism for salt exclusion and / or
• Taxonomic isolation from terrestrial relatives at least at the generic level.

There is no agreement on the number of true mangroves in the world. Tomlinson (1986) states that the Eastern Hemisphere has 40 true mangrove species and that the Western Hemisphere has eight true species. He later provides a figure of 54 true mangrove species worldwide, neglecting to tell us where the six missing species are. Nonetheless, the Eastern Hemisphere has a much higher biodiversity.

Nine species of true mangroves are represented in Kenya: Avicennia marina (Forsk.) Vierh., Rhizophora mucronata Lam., Ceriops tagal C.B. Rob., Lumnitzera racemosa Van Steenis, Bruguiera gymnorrhiza (see note on spelling) (L.) Lam., Sonneratia alba J.E. Smith, Xylocarpus granatum Koenig, Xylocarpus moluccensis (Lamk.) Roem 1846 and Heritiera littoralis Dryand. (Isaac and Isaac, 1968; nomenclature according to ITIS, 2000 and Tomlinson, 1986).

2.0 Mangrove Flora

2.1 Zonation

Mangrove species often occur in mono-specific or mixed bands or zones that parallel the coastline (Macnae, 1968). The causes of zonation in mangroves has been a well debated issue. Santos et al. (1997) review the theories for observed zonation patterns which include:

• Plant succession: spatial zonation patterns represent the mangrove succession sequence, in time, towards a climax terrestrial community.
• Geomorphic change: assumes the development of zonation patterns, both in time and space, as a dynamic response to continuously changing environmental and physical properties of the mid-littoral zone such as size, configuration, topography and geology.
• Physiological ecology: it is thought that each species has its own optimum environmental condition and would therefore be restricted to certain segments of the environmental gradient.
• Population dynamics: zonation is a response to biotic factors such as interspecific competition and plant reproductive and colonization strategies.

All of these concepts have been justly criticized and new concepts bridge these theories in such a way that the physical gradient controls zonation in physically extreme environments and interspecific competition in less stressful environs (Santos et al., 1997). Furthermore, Johnstone (1983) proposed that the center of every zone is a climax forest under the current conditions.

2.2 Adaptations

Mangroves have developed many adaptations to survive in harsh saline conditions. Moreover, the soils they grow in are often anaerobic, causing many physiological challenges to the plant. The two most obvious adaptations mangroves have evolved are their roots and vivipary.

2.2.1 Roots

Most well developed mangroves posses aerial roots (e.g. stilt or prop roots in Rhizophora spp.; pneumatophores in Avicennia spp.; knee roots in Bruguiera spp. and Ceriops spp.). These roots function to ventilate the buried portion of the root system that lies in the highly anaerobic sediment (Scholander et al., 1962).

2.2.2 Vivipary

Vivipary, where the embryo that results from normal sexual reproduction has no dormancy, but grows while still attached to the parent plant (Macnae, 1968), is known in many mangrove families, including both Avicenniaceae and Rhizophoraceae. In Rhizophoraceae, the hypocotyl extends out of the fruit resulting in a propagule (see, for example, Rhizophora mucronata). Although the exact advantages this provides the plant is unknown, it is believed to be important due to the convergent evolution in many families of mangroves (Tomlinson, 1986). One advantage is that while growing on the parent tree, the propagule is exposed to lower ionic concentrations (Zheng et al., 1999). Propagules also float and are able to remain viable for weeks in seawater (Rabinowitz, 1978), thus facilitating dispersal

2.2.3 Salt regulation

A less apparent, but highly important adaptation is how mangroves cope with excess salt. All mangroves, to some degree, exclude salt at their roots and secrete salt through their leaves. Rhizophora, Bruguiera, Lumnitzera and Sonneratia all are highly effective at excluding salts at their roots, but are poor secretors (termed ‘non-secretors’) (Scholander et al., 1962). Avicennia on the other hand, can secrete salts at special salt glands on their leaves at a high rate (op. cit.). It has also been found that as the non-secretors leaves age their salt concentration increases, so that when they are shed the plant is effectively removing excess salts (Zheng et al., 1999). Moreover, one of the biochemical mechanisms by which mangroves counter the high osmolality of salt is an accumulation of osmolytes, including nitrogen compounds (Popp et al., 1985). Additionally, these adaptations have been found to help limit heavy metal bioaccumulation in mangroves (MacFarlane and Burchett, 2000).

It should be noted that mangroves are facultative halophytes; they do not need salt water to grow (Macnae, 1968; pers. obs.). Moreover, although mangroves can tolerate relatively high salinities, the additional energy required to cope with this stress allows less energy to be allocated for plant growth and stunted forms usually result (Takemura et al., 2000). Macnae (1968) and Wells (1982) provide some general upper salinity tolerances based on field observations (see Table 1).

Table 1. Salinity tolerances of selected mangroves.

^a Macnae 1968; ^b Wells 1982

2.3 Physiognomy

Lugo and Snedaker (1974) have devised five classifications of forests based on tidal and hydroperiod characteristics: fringe, riverine, overwash, basin and dwarf. Cintrón et al., (1978) aggregated these into three classifications:

1. riverine: tall floodplain forests, flushed daily by tides;
2. basin: varied forest types, mostly flushed daily by tides, and
3. fringe: zonation present, occasionally affected by strong winds and high current velocities.

As a general rule, riverine forests exhibit the highest level of structural development and lowest amount of physical stress, followed by basin then fringe (Cintrón and Novelli, 1984).

2.4 Geological significance

It has long been thought that mangroves are land builders following the theory of plant succession (Lugo and Snedaker, 1974). Macnae (1968) offers some examples of how mangrove lined shores have extended at rates up to 125 m per annum. Mangroves generally follow the mud flat accretion, but mangroves also enhance the sedimentation rate (Young and Harvey, 1996). In an Australian mangrove, Furukawa et al. (1997) calculated that about 80% of suspended sediments brought into the mangrove were trapped there. Mangroves also facilitate the formation of flocs and their breakdown within the forest by physical and mechanical means (Wolanski, 1995). In addition to sedimentation, this also reduces turbidity in near shore waters protecting coral reef systems.

Although mangroves have been shown to increase sedimentation, it has been postulated that it does not represent land building, but land retaining during sea level rise (Snedaker, 1982; Ellison, 1996). If their sediment budget is not high enough, mangroves will retreat landward with rising sea level and increased wave action (Ellison, 1996). However, as long as there is adequate freshwater input to maintain an optimum low salinity, along with low sulfate, proper nutrient balance and productivity, it has been hypothesized there would be a net accumulation of peat proportional to the rising sea level and mangroves would not retreat. With low freshwater input, high salinities would lower production and high sulfate concentrations would increase anaerobic peat decomposition (Snedaker, 1995). This hypothesis fits well the findings of Tack and Polk (1999), whom demonstrated a positive correlation between groundwater flow and mangrove forest presence.

2.5 Ecological and economic importance

Historically, mangroves have been defined as wastelands and their removal thought beneficial (Lugo and Snedaker, 1974), however more recently their value has been appreciated. Table 2 lists some of the ecological services and products provided by mangrove ecosystems.

Table 2. Natural products and ecological services of mangrove ecosystems

Sources include: Ruitenbeek, 1994; Jin-Eong, 1995; Gilbert and Janssen, 1998; Rönnbäck, 1999.

3.0 Mangrove fauna (excluding brachyurans)

3.1 Vertebrates

Mangroves host, and are vital to many vertebrates including birds, fish, mammals, reptiles and amphibians. Many bird species use the mangroves as roosting and feeding sites during northern winters. 500-800 individuals of the rare Crab plover Dromas ardeola Paykull, 1805, with only 50,000 – 10,000 specimens remaining world-wide, winter in the mangroves of Mida Creek, Kenya alone (Seys et al., 1995). Moreover, some species are highly associated with the mangroves, such as the Mangrove Kingfisher, Halcyon senegaloides Smith, 1834 (Zimmerman et al., 1996). Fish also show unique adaptations to the intertidal ecosystem, such as the Gobidae mudskippers common to mangroves (Macnae, 1968). It has also been postulated that mangroves are nursery grounds for many commercially important fish species and positive correlations have been drawn between fish population abundance and mangroves (see Gilbert and Janssen, 1998 for brief review). Mammals present in the mangroves include monkeys, of which some are almost entirely restricted to the mangroves (Presbytis cristatus (Raffles) and Nasalis larvatus (Wurmb, 1787)), flying foxes (Pteropus spp.), wild pigs (Sus spp.) (Macnae, 1968) and baboons (pers. obs.). Reptiles that inhabit the mangroves include snakes and lizards. An unidentified snake (appox. 1 m in length, 4 cm circumference and turquoise green in color) was seen about 300 m into the mangroves at Mida Creek, Kenya (pers. obs.), showing that reptiles penetrate deep into mangroves. Furthermore, many lizards, probably of the genus Cyptoblepharus, were seen throughout the mangroves in Kenya (pers. obs.). Saltwater crocodiles are not present in Kenyan mangroves, but are in Asian and Australian mangroves (Macnae, 1968). Amphibians are rare in the coastal environment, however there is a frog (Rana cancrivora Gravenhorst) that inhabits the mangroves of South East Asia (Macnae, 1968). This brief listing further substantiates the importance of the mangrove ecosystem towards maintaining global biodiversity.

3.2 Invertebrates

The majority of mangrove fauna is composed of invertebrates. Arachnids and insects abound in the mangroves with the spiders and ants and of course mosquitoes being the most easily noted (pers. obs.). Additionally, fouling communities on mangrove roots are highly diverse. In a mangrove in Venezuela, Sutherland (1980) recorded Porifera, Coelenterata, Bryozoa, Tunicata, Polychaeta, Mollusca and Arthropoda on the roots of R. mangle.

There is a high diversity of mollusks in mangroves, most of which remains poorly studied. One exception includes the mangrove oyster, Saccostrea cucullata (Born, 1778) (e.g. Tack et al., 1992; Tack and Polk, 1995a, 1995b, 1996). As recently as 1986, Littorina scabra (Linnaeus, 1758) in the Indo-Pacific has been subdivided into 17 species (Reid, 1986). However, Plaziat (1984) offers a nice review of mangrove mollusk distribution. Kenyan mangroves host Littoraria spp., Terebralia palustris (Linnaeus 1758), Cerithidea decollata Linnaeus, 1758, Peronia sp., Isognomon ephippium (Linnaeus, 1758), I. isognomon Lightfoot 1786 and S. cucullata (pers. obs., as identified in Richmond, 1997).

It is surprising that T. palustris has not received more attention. They are large snails, up to 190 mm in length (Houbrick, 1991), that can occur in high densities: 130 ind./m² in Indonesia (Soemodihardjo and Kastoro, 1977), 33 ind./m² with an average length of 45 mm in Gazi Bay, Kenya (Slim et al., 1997) and 31 ind./m² with an average length of 98 mm in Dabaso, Mida Creek, Kenya (based on an average of three plots at one site with relatively high density of individuals; pers. obs.). They are mobile substrate for oysters and other biofouling organisms (Houbrick, 1991; pers. obs.). They have been shown to consume up to 3.2 g WW R. stylosa leaf litter /snail/day in Japan (Nishihira, 1983) and are important grazers in Gazi Bay, Kenya (Slim et al., 1997). As they are such effective grazers and prefer areas under the canopy of mangrove trees (Crowe, 1997; Crowe and McMahon, 1997) and muddy substrate to sandy substrate (Rambabu et al., 1987), they may be important competitors with crabs in certain areas within the mangrove.

From an economic viewpoint, shrimp or prawns are the most economically important invertebrate (Rönnbäck, 1999). They are also ecologically important insofar as the mass destruction of mangroves that has occurred in much of Asia due to improper prawn aquaculture practices (Corea et al., 1995; Davie and Sumardja, 1997).

Possibly the most ecologically important and well-studied group of invertebrates in the mangroves are the brachyuran decapod crustaceans, or true crabs.

4.0 Mangrove crabs (Brachyura)

4.1 Taxonomy

Mangrove crab diversity is very high with an estimated 275 species from six families of brachyurans (true crabs) associated with the mangrove ecosystem (Table 3) (cf. Warner, 1977 and Lee, 1998).

Table 3. Brachyuran families and number of reported species, world-wide, associated with the mangrove ecosystem.

From Warner, 1977; Grapsidae updated from Lee, 1998

There are more than 35 species of brachyurans and 4 anomura (hermit crabs and porcelain crabs) reported to be associated with Kenyan mangroves (Cannicci et al., 1997; Vannini and Cannicci, 1997 ; Vannini et al., 1997). For a listing of Kenyan species, their descriptors and ecological notes, see Table 4.

Table 4. Listing of Kenyan mangrove crabs (incomplete), their descriptors and ecological notes.

^A Verway, 1930; ^B Macnae and Kalk, 1962; ^C Bright and Hogue, 1972; ^D Hartnoll, 1975;

^E Vannini, 1980; ^F Lee, 1988; ^G Vannini and Ruwa, 1994; ^H Vannini et al., 1997; ^I Cannicci et al., 1998;.

^J Cannicci et al., 1999; ^K Pers. Obs.; ^L M. Vannini (pers. comm.); ^MP.J.F. Davie (pers. comm.).

* Does not burrow, but buries itself.

Specific: narrowly adapted to life in the mangroves; Semispecific: usually inhabiting the mangrove, but survives well in other habitats; Transient: usually found in other sites, but may temporarily reside in mangroves due to proximity of habitat to mangrove (adapted from Bright and Hogue, 1972).

Bold font indicates spp. encountered during this study.

† Ecological significance: common implies common in respective habitat

There has been much confusion with the subfamily Sesarminae, which is still unresolved (Vannini et al., 1997). The Selatium genus has been reworked by Serene and Soh (1970), and now includes S. brocki and S. elongatum (Hartnoll, 1975); Davie (1994) reclassified the Neosarmatium genus, reclassifying Sesarma meinerti and Sesarma smithi to N. meinerti and N. smithi. He also noted that N. smithi does not occur in south-western Pacific region (e.g. Australia) and has often been confused with a sister species N. trispinosum sp. nov. Ecological studies referring to N. smithi in Australia by Giddens et al. (1986), Neilson et al. (1986), Neilson and Richards (1989), Robertson and Daniel (1989) and Micheli (1993) are all actually referring to N. trispinosum sp. nov. (Davie, 1994).

4.2 Zonation

Many abiotic and biotic forces may play a role in the zonation of crabs, such as water salinity and availability, temperature, food availability and preference, sediment properties, interspecific competition and predation. The distribution of crabs within the mangrove has also been defined in terms of vegetation type (Macnae and Kalk, 1962; Macnae, 1963, 1967, 1968). Zonation of Kenyan mangrove crab species and the factors influencing their distribution is one of the objectives of this study and will be treated in more detail in Part II of this work.

4.3 Environmental adaptations

Aside from the Portunidae species, all crabs in this study are ‘land crabs’, which are defined as "crabs that show significant behavioral, morphological, physiological, or biochemical adaptation permitting extended activity out of permanent water" (Burggren and McMahon, 1988a). They all have, to some degree, adapted to life in the mangroves.

4.3.1 Behavioral adaptations

Vannini and Chelazi (1985) have defined two modes of behavioral strategies: isophasic and isospatial. Isophasic animals move according to their favorable phase (air or water) while isospatial animals remain in the same area during the unfavorable phase usually taking refuge. Examples of isophasic animals are the Portunidae which usually migrate into the mangrove forest at high tide to forage for food, however both Kenyan Portunidae mentioned have been observed to adapt isospatial strategies as well and remain in the forest, hidden in their burrow, during low tide (pers. obs.). Isospatial species include the burrowers such as C. carnifex and N. smithi and some will even remain in their burrows until conditions become so unfavorable that death results (Vannini, pers. comm.). Other behavioral adaptations include homing abilities to find refuge (Vannini and Cannicci, 1995; Cannicci et al., 1994), nychthemeral activity (Vannini et al., 1995), tidally rhythmic activity (Gifford, 1962; Cannicci et al., 1999) and changes in locomotor performance (Weinstein, 1998). Burrowing in the isospatial species may be one of the most important behavioral adaptations for many reasons.

Burrows have been shown to act as a microclimate which the crab designs for itself and which protects it from predators and temperature and water stress (Herreid and Gifford, 1963; Macnae, 1968; Icely and Jones, 1978; Pinder and Smits, 1988; Takeda et al., 1996a). Burrow depth in semi-terrestrial species usually penetrates to the water table (Verway, 1930; Atkinson and Taylor, 1988). When the tide approaches, many species can plug their burrows with mud and remain in an air pocket safe from predators (e.g. fish and portunidid crabs) (Macnae, 1968; Macintosh, 1988; pers. obs.). However, burrows also pose potential problems of hypoxia (low O₂ concentration) and hypercapnia (high CO₂ concentrations); burrowing crabs are better adapted to an aerial existence than they are to a fossorial mode of life (Atkinson and Taylor, 1988). Flood prevention in burrows is an important survival tactic due to the anaerobic nature of the surrounding sediment and the slow rate of diffusion of oxygen along water-filled burrows (Withers, 1978). Smaller specimens need not plug their burrow as long as it is smaller than ~3 mm due to the air bubble that forms and blocks the flooding water (Maitland and Maitland, 1994). However, burrows are increasingly hypercapnic and hypoxic with increasing depth and decreasing diameter because of restricted ventilation and metabolism of soil microorganisms and other burrow inhabitants (e.g. other crustaceans) (Pinder and Smits, 1988). Crabs subjected to hypoxic conditions experience a buildup of lactate, which can stimulate both a metabolic and behavioral response (De Wachter et al., 1997). Cardisoma guanhumi Latreille, 1825 has two responses to hypercapnia: a short-term apnea in response to rapid changes in external PCO₂ and long-term increase in ventilation during longer-term hypercapnia (op. cit.). Interestingly, it has been shown that brachyuran decapods are able to actively regulate hemolymph flow and distribution during activity, which could supply the increased oxygen demand of the scaphognathite muscles (in Cancer magister (Dana): De Wachter and McMahon, 1996a).

Non-burrowing crabs can either make use of other crabs burrows (e.g. S. ortmanni and S. guttatum) (pers. obs.), natural ‘dens’ or crevices (e.g. E. dentatus) (Cannicci et al., 1998), find refuge under the bark of dead trees (e.g. S. longipes and S. villosum) (pers. obs.), or adapt an aerial strategy where they can climb trees to avoid the incoming tide (e.g. S. leptosoma) (Vannini et al., 1997; Cannicci et al., 1999).

4.3.2 Morphological adaptations

Many examples of morphological adaptations in mangrove crabs exist including adaptive aspects of feeding mechanisms, walking appendages, water uptake appendages and respiratory organs.

The most obvious adaptation to feeding appendages are the chelae of the predatory crabs. Although not a general mangrove adaptation, the portunidids have large powerful chelae used to crush even large T. palustris shells (Houbrick, 1991). Less obvious adaptations in feeding mechanisms occur in the Ocypodidae. Miller (1961) has described the feeding mechanisms of Uca spp. Small portions of sediment are scooped up by the minor cheliped and carried to the mouth parts. Water is pumped from the branchial chamber into the buccal cavity to assist the sorting process. The organic matter is suspended and the heavier material sinks to the lower part of the buccal cavity to be periodically discharged as feeding or pseudofecal pellets. Icely and Jones (1978) have shown that the minor cheliped and second maxilliped differs between the Kenyan Uca species according to the sediment grain size of their habitat.

Walking appendage adaptation is evident in highly arboreal species. Both true arboreal species, the American Aratus pisonii Milne-Edwards, 1837 and the East African S. leptosoma, show morphological adaptations to life in the trees (Hartnoll, 1988a; Vannini et al., 1997). Typical arboreal adaptations include: a flat carapace, relatively long walking leg carpus and propodus and short dactylus (see S. leptosoma) (Vannini et al., 1997).

Many intertidal crabs are capable of taking up soil capillary water via setal tufts located between the walking legs, which is considered an evolutional advantage to intertidal life (Greenaway, 1988). By rapidly pumping the scaphognathite, the crabs are able to build a negative pressure in their branchial chamber and suck water in via the setal tufts (Wolcott, 1976). In fact, Wolcott (1976) found that O. quadrata is capable of obtaining suction pressure as low as 76 mm Hg below ambient.

Crabs originating from the marine environment must adapt their respiratory organs to cope with life in air. Aquatic gills are not suitable for aerial respiration because they collapse when the buoying effect of water is removed (Burggren and McMahon, 1988b). Furthermore, as air has a higher capacity for O₂ than water, less gill surface is required. Generally with increasing terrestrialness, there is a reduction in gill size (Cameron, 1981) and an increase in branchial chamber size (Burggren and McMahon, 1988b). Although these gills can function when exposed to air, they must still remain wet (op. cit.). Takeda et al. (1996b) recorded reduced gills in Ocipodidae occupying upper drier habitats (Uca spp.) compared to those (Macrophthalmus spp.) inhabiting moister environments. It also should be noted that gills play a major role in ion regulation (Pequeux, 1994). In the Kenyan mangroves, C. carnifex shows the most ‘terrestrial’ gills (cf. Alexander and Ewer, 1969, Cameron, 1981, and Takeda et al., 1996b). Although Cardisoma spp. do not need free water for respiration, they do for ion regulation, nitrogen excretion and acid base regulation (Wood and Boutilier, 1985). In fact, being that their burrow water is so hypoxic and hypercapnic, it is unlikely that they use it as a respiratory medium at all (Pinder and Smits, 1993).

The Kenyan mangrove grapsids have less developed respiratory organs and depend more on free water, however they can respire in air. Cott (1929) noted a "well-developed vascular tuft of considerable size" behind the extremities of the gills in N. meinerti, which he believes to function as a "true lung" (Figure 6), but which was later criticized by Alexander and Ewer (1969). Nonetheless, they still agree that N. meinerti is capable of respiring away from water for extended periods and hypotheses that the moist gills are adequate respiratory surfaces. More recent studies, however, have shown that air-breathing crabs have universally retained gills but have also developed accessory breathing organs, usually lungs formed from the inner linings of the branchiostegites, which are more effective gas exchangers than gills (Farrelly and Greenaway, 1994). Two major patterns of lungs have been identified, with the Ocypodidae having a simple pattern where the afferent system interfingers with an efferent system, and the Gecarcinidae and Grapsidae with a portal system (branching networks) (op. cit.).

Gill structure and function is rather complex and it is beyond the scope of this paper to go into more details (see Vernberg, 1983 and Burggren and McMahon, 1988b for a complete review).

In addition to aerial respiration, mangrove grapsids usually only have access to anoxic mangrove water posing yet another problem. The subfamily Sesarmidae has developed a system of aerating their branhcial water, which probably also aids in ion regulation. When the crabs emerge from water they carry a supply of water in their branchial chambers (Cott, 1929; Alexander and Ewer, 1969; McLaughlin et al., 1996; pers. obs.). As explained by Cott (1929), Verway (1930) and Alexander and Ewer (1969), this water is then driven out of the exhalent openings by the scaphognathites (or ‘gill bailers’; see Figure 6) and over the antero-lateral surfaces of the branchiostegite and pterygostome, where it forms a thin film over the geniculate hairs and finally re-enters the gill chamber via the Milne Edwards openings (a drop of water coming from the exhalent openings can be seen in the first photo of N. meinerti, as well as the geniculate hairs of the antero-lateral surfaces of the branchiostegite and pterygostome). Using this method, crabs can continue to aerate their branchial water for "some hours" (Alexander and Ewer, 1969). Furthermore, it can be hypothesized that if a crab is forced to utilize water with high or low osmolality, it may keep its branchial water for extended periods to reduce osmotic stress.

4.3.3 Physiological adaptations

Mangrove crabs have evolved physiological adaptations to the harsh mangrove environment. They include respiratory compensation for environmental change, osmotic and ionic regulation and water balance.

Many crabs inhabiting the mangrove are subject to considerable temperature variation (Malley, 1977). They must maintain their body temperature within a suitable range, while simultaneously conserving water and regulating salts (Bliss, 1968). Additionally, temperature effects heart rate and regional hemolymph flow (De Wachter and McMahon, 1996b). The easiest method of regulating body temperature is by evaporating water from moist membranes (op. cit.) (tropical crabs do not experience low temperature stress), however this may pose other serious problems, such as desiccation, for species inhabiting the upper littoral zone.

Changes in hemolymph oxygenation resulting from variation in temperature have not been well documented in any land crustacean (Burggren and McMahon, 1988b). Oxygen uptake increases as temperature rises, but little is known of the changes in hemolymph oxygen transport mechanisms that are needed to deliver the extra O₂ to the tissues (op. cit.). In C. carnifex, increases in circulating oxygen levels are associated with decreased O₂ consumption during dehydration (Wood et al., 1986), however the cause of the reduction in metabolism remains unclear (Burggren and McMahon, 1988b). Schlieper (1971) suggests that in higher salinities, CO₂, a stimulant for cellular respiration, would be readily removed from the animal while in low salinities it would accumulate, thus increasing the respiration rate. Also, increased solubility of O₂ at lower salinities may increase respiration. Furthermore, increased metabolic rate may be a result of increased osmotic work, which would make the rate of O₂ consumption dependent on the salinity of the medium the animals are naturally acclimated to (Withers, 1992). Brown and Terwilliger (1999) found that the temperate crab, Cancer magister (collected at a site with salinity varying from 32‰ to 16‰) decreased its O₂ uptake (MO₂) with decreasing salinity (32‰ to 16‰) and increased its MO₂ with increased temperature (10° C to 20° C). On the other hand, Shumway (1983) found that in four tropical species ranging from fully aquatic to semi-terrestrial that between 20‰ and 34‰ MO₂ was unaffected but increased between 0‰ and 13‰.

Crabs have developed the means to maintain the preferred solute concentrations of their tissue fluids while inhabiting certain mediums. Several distinct patterns of osmotic and ionic regulation are evident and have been summarized by Greenaway (1988). Species inhabiting the sublittoral usually have body fluids similar in concentration and composition to seawater. They may withstand reduced salinities, but show no ability of regulating the concentration of their extracellular fluids, which remain isosmotic with the medium. Crabs showing this pattern of osmoregulation are termed osmoconformers. Antithetical to this are the osmoregulators, which are capable of regulating the concentration of their hemolymph. In water with solute concentrations of seawater and higher, hyperosmotic regulators have hemolymph isosmotic with the medium, but in dilute media can regulate. In dilute media, lost salts are replaced by absorbing ions from the water by means of ion-transporting enzymes (ATPases) in the gill epithelium and excess water is removed by increasing the rate or urine output, which remains isosmotic with the hemolymph. Hyposmotic regulators have hemolymph concentrations below that of the medium. In dilute media they behave the same as hyperosmotic regulators, but in hyperosmotic seawater there is an outflux of water and influx of ions. To compensate for this, the crab drinks the medium and absorbs its ions and water across the gut. Excess ions are then eliminated across the gills or via the gut.

As has been touched upon in the previous paragraphs, respiration, feeding, excretion and temperature control all contribute to water losses in terrestrial crabs. Usually water loss from respiration is higher in crabs living closer to a water supply, however these crabs easily can replenish this lost water (Edney, 1961; Takeda et al., 1996b), while more terrestrial crabs can respire with access to only "moist" air (Pinder and Smits, 1993). Fecal losses of water have not been quantified, but are assumed low, while urine is the major route of loss of free water in most crabs (Greenaway, 1988). To cope with this, some highly terrestrial crabs store their nitrogenous waste until adequate water is available (Morris and van Aardt, 1998). Water losses due to evaporation can be dealt with by lowering the body temperature by the reflection of heat by concentration of pigments within the melanophores (Bliss, 1968) or by adapting to withstand greater water losses (Greenaway, 1988). The desert crab, Holthuisana transversa, has adapted to be able to tolerate a loss of almost half of its body water (Greenaway and MacMillen, 1978).

4.4 Reproduction

In Uca spp. there is a strong mating ritual with male crabs putting on an elaborate display to attract females into their burrow so that they may copulate behind the plugged entrance (Crane, 1975; Barnes, 1987; Murai et al., 1995). In Uca spp. and other brachyurans, after internal fertilization, eggs develop in the abdomen of the female where they are nourished from the egg yolk (Barnes, 1987). When a female is carrying eggs (or is ‘berried’), the eggs are visible to the human eye and are easily noticed in field conditions. When mature, the eggs are usually released into water where they develop as planktonic larvae. While most crabs use the sea as their nursery, some utilize rice fields, ponds or streams (Adiyodi, 1988; Schuh and Diesel, 1995). However, some crabs need only small pockets of freshwater water that collect in leaf axial (Metopaulias depressus) or shells (S. jarvisi) and exhibit high levels of parental care, including physical protection and maintenance of optimal O₂, pH, and calcium levels (Diesel and Schuh, 1993; Diesel and Horst, 1995; Diesel, 1989, 1992a, 1992b, 1997). However, in most species after the eggs are released, they hatch into zoeal larvae and go through various stages before the final larval stage, the megalops, which metamorphoses to become the juvenile (Adiyodi, 1988).

The number of zoeal stages varies with species, for example: there are two in S. curacaoense (Schuh and Diesel, 1995) four in Carcinus maenas L. (Payen, 1974), five in U. pugilator (Hyman, 1920) and O. quadrata (Diaz and Costlow, 1972), and seven in Callenectes sapidus (Sulkin et al., 1980). Anger (1995) reviewed the life history patterns in grapsids and found terrestrial and freshwater species had a tendency for low fecundity, brood protection, large egg size, unusually high carbon contents and C:N ratios in eggs and early larvae (indicating enhanced lipid content), abbreviated larval development and high larval tolerance of physico-chemical stress, nutritional independence. Of the Kenyan species, information was found on C. carnifex, N. meinerti and S. guttatum larval development with each going through five zoeal stages lasting from 22-25 days and one megalopa stage (Kannupandi et al., 1980, Pereyra Lago, 1989 and Pereyra Lago, 1993, respectively).

4.5 Feeding

Primary production and standing stock in a mangrove ecosystem is dominated by mangrove angiosperm tissue, algae and bacteria (Macnae, 1968, Macintosh, 1984; Alongi et al., 1993). This provides leaf litter and sediment organics as the primary food source for grazers. As already stated Uca spp. are deposit feeders, but to some extent so are the sesarmids. However, the primary food source for grapsids is believed to be leaf litter (e.g. Robertson and Daniel, 1989; Robertson, 1991), supplemented with algae and animal matter (Leh and Sasekumar, 1985; Cannicci et al., 1999; Dahdouh-Guebas et al., 1999). The Xanthids and Portundids are primarily carnivorous but may supplement their diet with leaves and algae (Dahdouh-Guebas et al., 1999; Cannicci et al., 1998). Only one Kenyan mangrove crab is known to eat fresh leaves off of the tree: S. leptosoma (Vannini and Ruwa, 1994). In addition, some species have been shown to become cannibalistic in the laboratory (Kneib et al., 1999).

Several problems arise with species consuming leaf material. Russell-Hunter (1970) proposed a theoretical minimum C:N requirement of 17 for food items to maintain animal tissues. The C:N ratios of mangrove leaves typically are in the range of » 25 to 80 according to the species (Robertson, 1988; Rao et al., 1994). In addition, many mangrove leaves contain high levels of tannins, a herbivore deterrent (Neilson et al., 1986; Wolcott and O’Connor, 1992). This may seem a serious problem, however, recent studies have shown that tannins decrease and heterotrophic nitrogen fixation occurs during leaf-litter decomposition, decreasing the C:N ratio (Robertson, 1988; Pelegrí and Twilley, 1998). Assimilation efficiencies (the percentage of food taken up) for sesarmids fed a leaf-litter diets are highly variable ranging from near zero (Giddens et al., 1986) to 82% (Emmerson and McGwynne, 1992). The deposit feeding Uca spp. have been shown to have assimilation efficiencies as high as 99% when fed bacteria (Dye and Lasiak, 1987). Even though some studies show high assimilation efficiencies for sesarmids, they should be interpreted with caution due to the difficulty in obtaining accurate measurements with some of the methods used (see Part III of this work for further explanation). Moreover, preliminary results from a current study indicate that some sesarmid crabs assimilate only about 50% plant material and 50% animal material from their overall food intake (Bouillon et al., 2002). Although crabs may or may not actually assimilate much energy from leaves, it has been well documented that they do remove, and consume, a large percentage of the leaf-litter, which seriously alters the flow of energy within a mangrove forest (Robertson, 1986; Lee, 1998).

4.6 Ecological significance

Mangrove crabs have been shown to be ecologically significant in many ways. As stated above, they keep much of the energy within the forest by burying and consuming leaf-litter. Furthermore, their feces may form the basis of a coprophagous food chain contributing to mangrove secondary production (Lee, 1997). As mentioned in Robertson et al. (1992), crab larvae are the major source of food for juvenile fish inhabiting the adjacent waterways; indicating that crabs also help nearshore fisheries. Crabs themselves are food for threatened species such as the crab plover (Seys et al., 1995; Zimmerman et al., 1996). Their burrows alter the topography and sediment grain size of the mangrove (Warren and Underwood, 1986) and help aerate the sediment (Ridd, 1996). Smith et al. (1991) found that removing crabs from an area caused significant increases in sulfides and ammonium concentrations, which in turn affects the productivity and reproductive output of the vegetation. Their findings support the hypothesis that mangrove crabs are a keystone species.

5.0 Conclusion

The importance of both mangrove flora and fauna (especially crabs) has been well documented. Brachyuran mangrove crabs are highly diverse and show a plethora of adaptations to this ecosystem, rendering them important for global biodiversity as well as interesting scientific subjects. They are most probably keystone species as their removal alters ecosystem structure and function (Smith et al., 1991). Continual scientific research on this subject will advance our understanding of their importance to the ecosystem and physiological and behavioral adaptations in general.

REFERENCES

This text appeared in:

Gillikin, D.P., 2000. Factors controlling the distribution of Kenyan brachyuran mangrove crabs: Salinity tolerance and ecophysiology of two Kenyan Neosarmatium species. M.Sc. Thesis, Free University of Brussels, Brussels, Belgium.

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