Mangrove Leaf Litter Processing by Sesarmid Crabs

107 Cey. J. Sci. (Bio. Sci.) 35 (2):107-114, 2006

MANGROVE LEAF LITTER PROCESSING BY SESARMID CRABS

S. Ravichandran*, T. Kannupandi and K. Kathiresan Centre of Advanced Study in Marine Biology, Annamalai University, Parangipettai – 608 502, India. Accepted: 30 May 2006

ABSTRACT The sesarmid crabs belonging to the Family Grapsidae and Subfamily Sesarminae are mainly herbivorous as proven in the present study by their gut-contents. Gut contents of Sesarma brockii, S. andersoni, and S. plicatum are almost similar containing high amount of vascular plant matter ranging from 58.33 to 72.54% of total diet. However, Metapograpsus maculatus (52.94%) and M. messor (40.27%) consumed a low amount of plant material. Under laboratory conditions, S. brockii preferred to consume 40-day decomposed Avicennia marina leaves. This serves as a good-quality food, helping growth, survival and moulting frequency of the crabs. Thus, the leaf-eating crabs breakdown the mangrove leaf litter to detrital sized particles and they regulate the nutritive pathway in the mangrove environment.

Key words: Sesarmid crabs, Mangrove leaf litter

INTRODUCTION Mangrove crabs especially sesarmids play an were collected from the Pichavaram mangrove important role in the initial processing of litter in forest (11° 27’ N; 79° 47; E) located about 250 km intertidal, riverine and fringing forests (Dahdouh- south of Chennai on the south-east coast of India. Guebas et al., 1997; Ravichandran et al., 2000; Kathiresan and Bingham, 2001). The sesarmid crabs For gut content analysis, 30 individuals of each Chiromanthes bidnes and C. maipoensis together crab species were collected randomly from the entire consume more than 50% of the daily litter mangrove study area. They were brought production in infrequently inundated, landward immediately to the laboratory for analysis. After mangroves at the Mai Po marshes, in Northwestern identification of the crabs, sex, carapace width, Hong Kong (Lee, 1989). The diets of sesarmid crabs weight and the approximate fullness of mainly consist of mangrove leaves and animal proventricules of the crabs were recorded. All the debris (Kwok and Lee, 1995; Dahdouh-Guebas et contents from the stomach and rectum were al., 1997). The sesarmid crabs may select particular removed and stirred with distilled water at 1:2 litter types of the mangrove leaf species available, volumes in a square petri-dish. The samples were leading to variable rates of litter mineralization. then smeared on a microscopic slide and five Studies on processing of mangrove leaf litter by random samples were observed at 100 X and 400 X sesarmid crabs are lacking for the Indian mangroves. magnifications for large and small organisms Hence, the present study has been carried out for the (Poovachiranon and Tantichodok, 1991). The first time to assess the role of Sesarmid crabs in contribution of each food item from the total diet is mangrove litter processing based on gut contents in expressed in terms of percentage of the visual field the crabs. Further, food preference of five different occupied by the different categories recorded. The mangrove crabs with six different mangrove diets categories used in classifying the stomach and rectal with reference to relative growth rate, assimilation contents were plant material, sand, silt, microalgae, efficiency and food conversion efficiency in crabs fungal material, macroalgae, crustacean debris, are also reported here. unidentified debris and filamentous algae. Faecal material in the hindgut region were also analysed and categorized. MATERIALS AND METHODS Leaf preference experiments Gut content analysis Individuals of the grapsid crabs namely Sesarma brockii, S. andersoni, S. plicatum, S. brockii, S. plicatum, S. andersoni, Metopograpsus Metopograpsus messor and M. maculatus crabs maculates and M. messor were collected from the *Corresponding author’s e-mail: [email protected] S. Ravichandran, T. Kannupandi and K. Kathiresan 108

Pichavaram mangroves. Fresh green leaves and Energy budget of S. brockii senescent ones were collected from individual S. brockii crabs collected from the Pichavaram healthy trees of Avicennia marina, Rhizophora mangroves were acclimatized for two days to mucronata and Acanthus ilicifolius. One set of captive feeding of fresh leaves and various stages of leaves was separately placed in nylon mesh bags and decaying leaves. Before the start of experiment, wet submerged for decomposition in water channels of weight, carapace width and sex were recorded for the Pichavaram mangrove forest. The leaves each crab. Ten crabs were kept in each tank. Seventy decomposed for 20,40,60,80 and 100 days along per cent of the tank was filled with muddy sand with freshly collected ones were used for leaf (collected from the mangrove) forming a slope. preference experiments for crabs. After 24 hours, residual leaf material was collected and weighed to calculate the quantity of leaf Sex and carapace width of the crabs were consumed. Feeding was terminated and the crabs recorded before they were placed in experimental purged until faecal production ceased. Water in the tanks. Each tank was filled with 50% sea water up to tank was changed daily. Weight gain, food 1 cm depth to avoid desiccation of the crabs. In consumed, feed conversion ratio and survival of order to recognize leaf identity after crab crabs fed with different mangrove leaves were consumption, the leaves of the six types were cut calculated after 60 days of feeding trial. Differences into different geometric shapes of the same area (4 in treatment means were determined by Duncan’s cm2). Multiple Range test (P<0.05) using SPSS/PC package. The leaf pieces were offered to the crabs and consumption rates of three leaf types were compared after 24 hours. The amount of leaf biomass offered RESULTS for each leaf type was smaller than the expected consumption by the crabs in 24 hours, for The carapace widths of the studied crabs ranged encouraging the crabs to feed on progressively less from 1.3 to 2.6 cm for S. brockii, 2.6 to 3.2 cm for desirable leaf types after exhausting the more S. andersoni, 1.2 to 2.4 cm for S. plicatum, 2.8 -3.4 desirable leaf types. Since the objective of this cm for Metopograpsus maculatus, and from 2.6 to experiment was to define leaf preference, 4.2 for M. messor. The fresh weight varied between consumption by the five crab species of the six leaf 2.02 and 6.20 g for S. brockii, 5.24 and 9.87 g for types was ranked for each crab-trial. Actual S. andersoni, 2.01 and 5.68 g for S. plicatum, 5.63 consumption was measured only for those with very and 23.47 g for M. messor and between 3.01 and similar consumption for different leaf species. 10.56 g for M. maculatus. The mean percentage of food items in relation to total volume found in the proventriculus of five sesarmid crabs is given in Table 1 & Fig. 1.

Table 1. Mean percentage composition of food items found in the proventriculus of grapsid crabs.

Crab species Carapace Weight Food items width (g) range (cm) Plant Sand, Animal Unidenti Filamentous Macro Micro Fungal materials silt & debris -fied algae algae algae material clay debris

Sesarma brockii 1.3-2.5 2.02-6.2 72.54 9.8 1.96 5.08 1.96 3.92 1.96 1.96

S. plicatum 1.2-2.4 2.01-5.68 63.33 6.66 5 16.58 1.66 - 5 1.66

S. andersoni 2.6-3.2 5.24-9.87 58.33 6.66 5 13.33 5 3.33 1.6 3.33

Metapograpsus 2.8-3.4 3.01-10.56 52.94 17.64 4.41 2.94 2.84 1.47 4.41 maculatus 13.23 M. messor 2.6-4.2 5.63-23.47 40.27 6.94 31.94 5.55 2.7 8.33 2.7 1.3

Mangrove leaf litter processing by sesarmid crabs 109

Proportion of material in the gut The crabs exhibited greater variability in the Leaf tissue was found to have originated from the amount of food in foregut. The foregut content mangrove species present in the vicinity of the crabs consisted of vascular plant matter ranging from collected.The leaf fragments were mostly of two 40.27 to 72.54% of total (Fig. 1). Sesarma brockii, types and they could be identified as Avicennia and S. andersoni and S. plicatum showed almost Rhizophora species on the basis of stomatal features. similar diets and they consumed high amount of The inorganic particles in the gut contents were vascular plant matter (58.33–72.54%). However, p r edo m inantly clay. Animal debris and algae M. maculatus (52.94%) and M. messor (40.27%) contributed little to the gut contents and were consumed a low amount of plant materials. The arbitrarily lumped together. Unidentified material second most important category was sediments, included bacterial colonies and some fruiting bodies. sand, silt and clay particles, constituting the gut content that ranged from 6.66 to 17.64%. Maximum Comparison of fore and hindgut contents of amount of sediment (17.64%) was collected from S. brockii the gut of M. maculatus. Other gut contents were The principal difference between the foregut detected in lesser quantity and they included and hindgut contents is given in Table 2. The unidentified debris (5.08–16.58%), filamentous degraded leaf particles occupied 41.8% of foregut algae (1.66–5.0%), leaf associated fungal hyphae content and 71.2% of hindgut (rectal region). The (1.3–4.41%), micro algae (1.6–5.0) and macro-algae fresh leaf materials decreased from 30.08% in the (2.84 – 8.33%). foregut to 13.9% in the hindgut. The degraded leaf particles were smaller in size than fresh leaf Nature of gut contents materials. The proventricules of S. brockii, S. plicatum, S. andersoni, M. maculatus and M. messor were Faecal pellets observed in the hindgut were normally found to be full. The dominant materials mostly of degraded leaf containing fine particles. present were fresh and degraded leaf tissues. Tissues Further, leaf material ingested by S. brockii was of pneumatophores and bark were not observed. completely digested into fine particles and released back into the environment. The difference in the food items of S. brockii in the foregut and hindgut is statistically notsignificant (P>0.05).

Comparison of gut contents in S. brockii derived from field and laboratory The proventricules of S. brockii were almost full and only three individuals among 30 were found with empty stomachs. The contents of the field and laboratory reared S. brockii were almost the same. However, filamentous algae, microalgae, macroalgae and fungal materials were completely absent in the proventricules of laboratory-reared animals as they were offered only with mangrove leaves. The field specimens showed 72.84% the degraded vascular plant materials and the laboratory-reared animals 89.13% and the difference was statistically significant (P>0.05).

Leaf preference There was a strong tendency for most of the crab species to consume decomposed leaves of

Figure 1. Plant material in the gut of five A. marina. Tables 3 & 4 show the leaf preference dominant mangrove crabs. by S. brockii, S. plicatum., S. andersonii,.

S. Ravichandran, T. Kannupandi and K. Kathiresan 110

M. maculatus and M. messor. The same pattern Growth Rate was found in all the cases, with a very high The results of 60-day growth trials of crabs, preference for decomposed leaves of A. marina and S. brockii, are presented in the Table 5. Decomposed very low preference for fresh leaves of A. ilicifolius. leaves of A. marina showed a significant effect on The experiment showed that about 2 g of leaf weight gain ranging between 0.66 and 1.90 g. The material were enough to feed a crab daily. All the highest weight gain was noticed in crabs fed with experimental animals preferred decomposed leaves decomposed A. marina, whereas lowest weight gain of A. marina and R. mucronata, more than other leaf was in crabs fed with fresh A. ilicifolius leaves. types. M. maculatus did not consume fresh green leaves of A. ilicifolius during the experimental Feed Conversion Ratio (FCR) ranged between 0.98 and 6.81. The lowest FCR was noticed in crabs period. fed with decomposed A. marina and the highest

FCR in crabs fed with fresh A. ilicifolius leaves. In general, the experimental crabs strongly Duncan’s Multiple Range test clearly showed that preferred decomposed A. marina leaves followed by the quality of A. marina decomposed leaf was better R. mucronata leaves. Most of the crabs moved than A. ilicifolius fresh leaf as was also evident from away from fresh A. ilicifolius leaves, and preferred the survival rate (Table 5). ANOVA revealed that decomposed leaves. the weight gain of the crabs with different food

types were significantly different (P < 0.05).

Table 2. Foregut and hindgut content of Sesarma brockii .

S. No. Food items Foregut Hindgut 1. Degraded leaf particles 41.8 ± 0.08 71.2 ± 0.08 2. Vasuclar plant materials 30.8 ± 0.08 13.9 ± 9.42 3. Sand, silt & clay 11.6 ± 0.24 6.4 ± 0.32 4. Crustacean debris 3.4 ± 0.32 2.9 ± 0.03 5. Unidentified debris 6.9 ± 0.07 1.2 ± 0.09 6. Filamentous algae 1.1 ± 0.08 0.0 7. Macro algae 2.3 ± 0.24 2.5 ± 0.08 8. Micro algae 1.0 ± 0.47 0.0 9. Fungal material 1.1 ± 0.08 1.2 ± 0.12 Values denote % mean content, n = 30 Mean ± standard deviation.

Table 3. Leaf preference of mangrove crabs fed with various stages of decomposed A. marina leaves

Days of Amount of leaf consumed by crab species (g/crab) decomposition Sesarma S. plicatum S. andersoni Metapograpsus M. messor brockii maculatus

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4. R S. Ravichandran, T. Kannupandi and K. Kathiresan 112

DISCUSSION with both fresh and 100-day decomposed leaves of A. marina, R. mucronata and A. ilicifolius. This Litter processing preference for A. marina leaves over others, may be The analysis of gut contents in S. brockii, attributed to the physical and chemical characteristics S. plicatum, S. andersoni, M. messor and of the leaves (Lee, 1989; Poovachiranon et al., 1986). M. maculatus indicates that most of the sesarmid The toughness of the leaves is also important in crabs are primarily herbivores. The proventricules and determining the leaf quality. Avicennia leaves in rectum contain very high percentage of mangrove leaf general, are thin when compared to Rhizophora. The material. Both fresh and degraded leaf particles are feed quality of A. marina leaves has also been present in the gut contents of laboratory-reared crabs. attributed to low level of soluble tannin and high However, the field collected crabs have more of protein content of the leaves (Ravichandran and degraded leaf particles. Shell fragments of molluscs, Kannupandi, 2004). crustaceans and fragments of nematodes occur in small quantities in the gut. The sesarmid crabs Sesarmid crabs prefer the decaying mangrove occasionally consume brachyuran crabs and their leave for their most farvourable nutritive status. moults, gastropods, juvenile bivalves, oligochaetes, Senescent mangrove leaves generally have high nematodes, ants, mosquito larvae and spiders (Leh initial C:N ratios up to 100 which decrease in and Sasekumar, 1985). However, these food items are decomposing leaves. The food materials which have at a low percentage in the present study, while plant C:N ratios lower than 17 are considered nutritious to materials are abundant ranging from 40.27 to 72.5% in marine invertebrates (Russel-Hunter, 1970). The the gut contents of the mangrove crabs. feeding activities of crabs speed up the rate of decomposition of leaf litter and may facilitate the Small - sized detrital particles occur more in the release of nutrients to mangal system (Lee, 1997). hindgut than in the foregut region. The proventricule is a site of particle reduction, where much of the Crab species differ in their assimilation materials are reduced. This is in agreement with that of efficiency, depending on the growth strategies of the the previous report that particles in the hindugut are of crabs (Hartnoll, 1983). In the present experiment, a smaller in size than those in the proventriculus of the higher assimilation efficiency has been noted in sesarmid crab, Chiromanthes oncychophorum (Malley, S. brockii offered with decomposed A. marina 1978). mangrove litter. In South African mangrove swamp also, S. meinerti had very high assimilation All the crab species observed in the natural efficiency when fed with 6-month decomposed mangrove habitats display mud-picking behaviour A. marina leaves (Emmerson and McGwynne, which may be the predominant mode of ingestion. The 1992). sediment is passed by the chelae to the mouthparts. The size of litter consumed is considerably larger than Kwok and Lee (1995) have recorded longest that seen in the proventricules. The food items which survival of crabs when fed with decomposed leaves. appear to be picked up by the chelae and ingested by Contrary to this, Micheli (l993a) has found no the crabs, are fragmented into different sizes difference in survival among the crabs fed with depending on the type of grasping and tearing using different amounts of Ceriops tagal litter, but higher chelipeds. frequency of both ovigerious females and moults with continued supply of the mangrove litter than Leaf preference and growth with a restricted supply. Another study by the same In Pichavaram mangroves, the grapsid crabs are author has also reported no difference in survival dominant, leading mostly herbivorous mode of life when the crabs are fed with litters of different utilizing plant materials as a food source. Although species, but contrasting levels of moulting frequency plant materials are available more than animal food, (Micheli, 1993b). In the present study, however, the they are nutritionally inferior in having low nitrogen decaying leaves of A. marina and R. mucronata are content, which is an important limiting nutrient for the not only good quality food for growth and survival herbivores. of mangrove crabs but also, A. marina leaves enhance moulting frequently. In the Pichavaram According to the present findings, crabs strongly mangrove forests, sesarmid crabs descend from their prefer decomposed A. marina leaves when supplied burrows above the high tide mark to feed on

Mangrove leaf litter processing by sesarmid crabs 113

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