Physiological responses of two ecologically important Kenyan mangrove crabs exposed to altered salinity regimes
Introduction
Crabs are the most abundant of the mangrove macro-fauna and are a valuable asset to the mangrove ecosystem. Crabs aerate the sediment by burrowing (Micheli et al., 1991), modify topography and grain size distribution (Warren and Underwood, 1986), reduce pore water salinity by allowing flushing of the sediment via their burrows Ridd, 1996, Stieglitz et al., 2000, trap energy within the mangrove forest Robertson, 1986, Robertson and Daniel, 1989, Lee, 1998, Ashton, 2002, create microhabitat for other fauna Bright and Hogue, 1972, Gillikin et al., 2001, contribute to secondary production (Lee, 1997), and increase the amount of nutrients and decrease the sulfide concentration in the sediment by a plethora of activities (Smith et al., 1991). Due to the critical role burrowing crabs play in the mangrove ecosystem, Smith et al. (1991) considered them keystone species. In Kenya, two burrowing congeners, Neosarmatium meinerti and Neosarmatium smithi, have opposing distributions across the mangrove forest (with N. meinerti inhabiting the high shore and N. smithi the mid- and lower shore), relatively large body sizes, deep (∼1 m) and wide diameter (∼4 to 5 cm) burrows, and occur in high densities Micheli et al., 1991, Gillikin, 2000. Therefore, these two species probably play a very significant role in the function and structure of Kenyan mangrove ecosystems.
Despite their importance, data on mangrove grapsoid ecophysiology remains patchy. Gross et al. (1966) showed that the mangrove crabs N. meinerti and Cardisoma carnifex (Herbst, 1794) are powerful osmoregulators in both concentrated and dilute media (concluded from a 2-day experiment), which would allow them to survive in the landward Avicennia marina (Forssk.) Vierh. zone subjected to periodic extreme salinity fluctuations. Although mangrove crabs usually show a distinct zonation, osmoregulatory ability has not been shown to be linked with the observed zonation patterns (Frusher et al., 1994) However, osmoregulatory ability may not be enough to explain actual salinity tolerances. For example, the temperate estuarine crab Callinectes similis Williams, 1966, has been shown to be a strong osmoregulator, although scope for growth and long-term actual growth experiments show that the energy remaining for somatic growth is slightly reduced in higher salinities and is reduced by more than half in lower salinities Guerin and Stickle, 1997a, Guerin and Stickle, 1997b. Therefore, the long-term extra energy expenditure due to subtle, sublethal, effects of salinity may dictate long term salinity tolerances, especially for animals already living above their optimal salinity.
High evaporation and natural episodic fluxes of freshwater input into estuaries from meteorological events are common and often result in acute salinity fluctuations; whereas anthropogenically induced changes in freshwater input result in chronic, if not indefinite, changes in estuarine salinity regimes (Christensen et al., 1997). Groundwater has been shown to contribute large amounts of water to estuarine water budgets, generally buffering salinity Church, 1996, Moore, 1996. It is especially important in large riverine mangrove forests away from direct river input where water circulation is reduced and evaporation is high. For example, Kitheka (1998) calculated that the backwater residence time was more than 11 days in Mida Creek, Kenya. Anthropogenic changes in groundwater outflow may be leading to changes in mangrove and seagrass distribution, community structure, faunal distribution and species richness Kitheka, 1998, Kitheka et al., 1999, Tack and Polk, 1999, Kamermans et al., 2002. Furthermore, the degree of community change induced by freshwater flow alterations is difficult to predict quantitatively because of the lack of field-based salinity range data available (Christensen et al., 1997).
Although there have been studies of acute osmotic stress tolerances of mangrove crabs Gross et al., 1966, Frusher et al., 1994, Schubart and Diesel, 1998, Anger and Charmantier, 2000, few studies have looked at chronic salinity tolerances. Since both growth and osmoregulation are energy requiring processes, the sublethal effects of chronic salinity stress may include changes in the energy budget of the animal. Physiological rates can be measured across a salinity gradient and converted to energetic equivalents to determine what effect salinity has on components of the energy budget. An energy budget can then be estimated from energetic equivalents of fundamental physiological processes such as food uptake, excretion and oxygen consumption (Withers, 1992).
N. meinerti usually inhabits the landward fringing A. marina zone of the mangal, with large fluctuations in salinity and have been found inhabiting salinities ranging from 1‰ to 65‰ (Gillikin, 2000). N. smithi occupy the lower broad Rhizophora mucronata Lam. zone, which is usually inundated daily and thus has a more stable salinity regime, but which may be as low as 21‰ and as high as 53‰ (Gillikin, 2000). Both species are semi-terrestrial and are well suited for aerial respiration. They were chosen for this study due to their abundance, large size, wide geographical distribution (see Davie, 1994) and fossorial mode of life. Much ecological work has been done on N. meinerti (see references herein), while little has been done on N. smithi. N. smithi is widely distributed throughout the Indo-Pacific, but has been wrongly identified in the south-western Pacific (e.g. Giddens et al., 1986, Robertson and Daniel, 1989, Micheli, 1993) where it is replaced by its sister species N. trispinosum (Davie, 1994).
The objective of the present study is to give insight into the possible long-term effects of altered salinity regimes on the bioenergetics of two of the potentially most important Kenyan mangrove crab species.
Section snippets
Laboratory methods
Intermolt adult specimens were collected in Gazi Bay, Kenya (S04°25′ E039°30′) (Fig. 1) in September 1999. Pore-water salinity was ±32‰ in collection areas. Individuals of both species were captured by hand and were transferred to the field laboratory within 3 h, rinsed with seawater, blotted dry, sexed, weighed (to the nearest 0.01 g) and carapace width (CW) measured. Average weight and size of freshly caught N. meinerti was 35.65±11.06 g and 37.6±2.9 mm CW (n=54) and for N. smithi was
Laboratory
A distinct difference was observed in the mortality rates of N. smithi and N. meinerti during acclimation (Fig. 2). N. meinerti survived equally well in all salinity treatments, while N. smithi had 100% mortality at 65‰ after just 5 days at the target salinity. Subjecting this species to 16‰ and 48‰ also resulted in high mortality rates, while those in 32‰ had comparable rates with N. meinerti in all treatments. There was no significant weight change in any of the animals throughout the
Discussion
The results show that N. meinerti is a strong hyper- and hypo-osmoregulator, allowing them to survive in salinities from at least 16–65‰. N. meinerti appeared healthy at the end of the experiment as they aggressively ate during the feeding experiment and had comparable feeding rates to those in the study of Emmerson and McGwynne (1992), in all salinities but 65‰. Although food consumption (FC) of N. meinerti decreased in 65‰, energy expenditure (R+U) did not, driving their energy budget below
Acknowledgements
Financial support was granted by the EC project ‘Anthropogenically induced changes in groundwater outflow and quality, and the functioning of Eastern African nearshore ecosystems’ (contract IC18-CT96-0065) and a Flemish Interuniversity Council (V.L.I.R.) travel scholarship to D.P.G. We are much indebted to Drs. A. Verheyden for both laboratory and field assistance and to Dr. F. Dehairs, Dr. S. Bouillon Dr. C.D. Schubart and anonymous reviewers for useful comments on this manuscript. Staff of
References (58)
- et al.
Ontogeny of osmoregulation and salinity tolerance in a mangrove crab Sesarma curacaoense (Decapoda: Grapsidae)
J. Exp. Mar. Biol. Ecol.
(2000) Mangrove sesarmid crab feeding experiments in Peninsular Malaysia
J. Exp. Mar. Biol. Ecol.
(2002)Nitrogen metabolism
- et al.
Feeding and assimilation of mangrove leaves by the crab Sesarma meinerti de Man in relation to leaf-litter production in Mgazana, a warm-temperate southern African mangrove swamp
J. Exp. Mar. Biol. Ecol.
(1992) - et al.
Salt and water balance in selected crabs of Madagascar
Comp. Biochem. Physiol.
(1966) - et al.
A comparative study of two sympatric species within the genus Callinectes: osmoregulation, long-term acclimation to salinity and the effects of salinity on growth and moulting
J. Exp. Mar. Biol. Ecol.
(1997) Groundwater outflow and its linkages to coastal circulation in a mangrove-fringed creek in Kenya
Estuar. Coast. Shelf Sci.
(1998)- et al.
Hemolymph ammonia, urea and uric acid levels and nitrogenous excretion of Marsupenaeus japonicus at different salinity levels
J. Exp. Mar. Biol. Ecol.
(2003) Impacts of habitat complexity on physiology: purple shore crabs tolerate osmotic stress for shelter
Estuar. Coast. Shelf Sci.
(2001)Feeding ecology of mangrove crabs in North Eastern Australia: mangrove litter consumption by Sesarma messa and Sesarma smithii
J. Exp. Mar. Biol. Ecol.
(1993)
Temperature, salinity and food thresholds in two brackish-water bacterivorous nematode species: assessing niches from food absorption and respiration experiments
J. Exp. Mar. Biol. Ecol.
Improvements in the determination of urea using diacetyl monoxime; methods with and without deproteinisation
Clin. Chim. Acta
Carbon, nitrogen contents and stable carbon isotope abundance in mangrove leaves from an East African coastal lagoon (Kenya)
Aquat. Bot.
Flow through animal burrows in mangrove creeks
Estuar. Coast. Shelf Sci.
Leaf-burying crabs: their influence on energy flow and export from mixed mangrove forests (Rhizophora spp.) in northeastern Australia
J. Exp. Mar. Biol. Ecol.
Decomposition of mangrove leaf litter in tropical Australia
J. Exp. Mar. Biol. Ecol.
Keystone species and mangrove forest dynamics: the influence of burrowing by crabs on soil nutrient status and forest productivity
Estuar. Coast. Shelf Sci.
Primary producers sustaining macro-invertebrate communities in intertidal mangrove forests
Oecologia
A synopsis of the burrowing land crabs of the world and list of their symbionts and burrow associates
Contr. Sci. Nat. Hist.
Leaf choice by crustaceans in a mangrove forest in Queensland
Mar. Biol.
A gap dynamic model of mangrove forest development along gradients of soil salinity and nutrient resources
J. Ecol.
An index to assess the sensitivity of Gulf of Mexico species to changes in estuarine salinity regimes
Gulf Res. Rep.
An underground route for the water cycle
Nature
Assimilation of organic matter by zooplankton
Limnol. Oceanogr.
Salt allocation during leaf development and leaf fall in mangroves
Trees-Struct. Funct.
Energy flow measurement
Revision of Neosarmatium Serène and Soh (Crustacea: Brachyura: Sesarminae) with descriptions of two new species
Mem. Queensl. Mus.
Manometric Methods as Applied to the Measurement of Cell Respiration and other Processes
Energy equivalents of oxygen consumption in animal energetics
Oecologia
Cited by (20)
Effects of hypo-osmotic shock on osmoregulatory responses and expression levels of selected ion transport-related genes in the sesarmid crab Episesarma mederi (H. Milne Edwards, 1853)
2024, Comparative Biochemistry and Physiology -Part A : Molecular and Integrative PhysiologyEffects of domestic effluent discharges on mangrove crab physiology: Integrated energetic, osmoregulatory and redox balances of a key engineer species
2018, Aquatic ToxicologyCitation Excerpt :N. meinerti is among the largest and most dominant mangrove crab species in the area, and is most frequently found in the upper part of the mangrove forest (from the Ceriops tagal up to the Avicenia marina). The spider crab is one of the dominant mangrove crab species and plays a key role in structuring this area of the mangrove system (Fusi et al., 2015; Gillikin et al., 2004). It has a bimodal breathing capacity and is exposed to drastic salinity variations, ranging from hypersaline conditions (at low tide and during the dry season) to high levels of fresh water originating from run-off streams during the rainy season.
Ecophysiological adaptations to variable salinity environments in the crab Hemigrapsus crenulatus from the Southeastern Pacific coast: Sodium regulation, respiration and excretion
2017, Comparative Biochemistry and Physiology -Part A : Molecular and Integrative PhysiologyCitation Excerpt :Therefore, we suggest that early benthic stages (i.e. megalopa and juvenile) of H. crenulatus rely more on behavioural strategies to avoid low salinities, but as they grow, the enhancement of the osmoregulatory capacity would allow them to rely more on physiological strategies to colonize areas of low salinity. This size-salinity dependent distribution has been previously suggested to be the result of different size-dependent tolerances to salinity change, originating from the development of osmoregulatory structures and the activity of some key transporters (Na+/K+-ATPase) (Charmantier et al., 2002; Gillikin et al., 2004; Taylor and Seneviratna, 2005; Cieluch et al., 2007), as a mechanism to avoid cannibalism from bigger con-specifics (Iribarne et al., 1997; Luppi et al., 2002; Bas et al., 2005), or a combination of both (Charmantier, 1998; Posey et al., 2005; Anger et al., 2008; Pardo et al., 2011). The crucial role that NKA plays in acclimation to different salinities has been widely suggested in crustacean species.
Behavioural effects of hypersaline exposure on the lobster Homarus gammarus (L) and the crab Cancer pagurus (L)
2014, Journal of Experimental Marine Biology and EcologyCitation Excerpt :In their natural environments, temperate crustaceans that are generally fully marine in nature rarely, if ever, experience hypersalinity hence the lack of attention to this subject. The principal focus of studies that have been made on high salinities relates to the effect of desalination plant discharges in hot climates (Meerganz von Medeazza, 2005; Raventos et al., 2006; Smith et al., 2007) or species that live in saltpan and saline lakes that have high evaporation rates (Clegg and Gajardo, 2009; Nunes et al., 2006) or mangrove swamps (Anger and Charmantier, 2000; Gillikin et al., 2004). Because hypersaline conditions are relatively scarce in temperate regions there is correspondingly less information on the effects of hypersalinity on temperate species.
Organic carbon dynamics in mangrove ecosystems: A review
2008, Aquatic BotanyTidal impacts on riparian salinities near estuaries
2006, Journal of Hydrology
- 1
Current address: Environmental Consulting and Assistance NV, Lange Nieuwstraat 143, B-2000, Antwerp, Belgium.