INTRODUCTION

The St Lucia Estuary is a crucial component of the iSimangaliso Wetland Park, which is a UNESCO World Heritage Site. It is the largest estuarine lake system in Africa and covers approximately 80% of the total estuarine area of KwaZulu-Natal, South Africa (Begg 1978). The estuary is characterised by prolonged mouth closure and experiences large-scale periodic fluctuations in physico-chemical characteristics due to stochastic flood and drought events (Begg 1978; Owen & Forbes 1997; Pillay & Perissinotto 2008). The shallow nature of the lake, combined with its large surface area, results in high evaporative loss. The system experiences additional stress from increased human numbers, forestry and agricultural developments in the catchment area around the lake (MacKay et al. 2010; Cyrus et al. 2011). These activities include manipulation of the St Lucia Estuary mouth, freshwater abstractions from surrounding rivers (Fig. 1a) and the increase in sugar cane farming and number of tree plantations in adjacent areas (Whitfield & Taylor 2009), all of which lead to an intensification of drought conditions. As a result, the St Lucia Estuary experiences regional hypersalinity at times, especially in the northern part of the lake where salinities occasionally exceed 200 ppt (Whitfield & Taylor 2009; Cyrus et al. 2011). In drought conditions, however, the Back Channel (Fig. 1b) may provide a connection to the Mfolozi River and the ocean, thereby supplying water to the system, allowing limited biological migrations into St Lucia from the sea, and decreasing the overall salinity of the Narrows and estuary mouth (Whitfield & Taylor 2009). Most of the recent research on the system has been carried out during drought events (Cyrus et al. 2011).

Fig. 1.

Maps of the St Lucia Estuary: (a) expansion of the estuary and mouth region (adapted from Carrasco et al. 2010); (b) highlighting sampling sites and sources of freshwater inflow via tributary rivers.

The instability and ongoing degradation of the estuarine lake both have a significant impact on associated biodiversity (Schlacher & Wooldridge 1996; Mac Kay et al. 2010). Hypersaline conditions lead to movement of stenohaline species out of the area and extinction of less mobile organisms, resulting in changes in community structure and species richness (Schlacher & Wooldridge 1996; Owen & Forbes 1997). The decrease in salinity caused by freshwater run-off from the Mfolozi promotes biodiversity (Whitfield & Taylor 2009). Persistent mouth closure (since June 2002) has resulted in limited juvenile recruitment from the ocean and no tidal exchange, which has led to desiccation of the extensive mangrove swamps that occur in the regions of the mouth and Narrows (Adams et al. unpubl. data).

Brachyurans (true crabs) play an integral role in the functioning and maintenance of the mangrove ecosystem (Day 1981). Herbivorous and detritivorous species are important components of mangroves as they feed on leaf-litter and decaying organic matter present on the forest floor (Dahdouh-Guebas et al. 1997). They facilitate the decomposition process by breaking down organic matter and exposing it to microbes, thus playing an important role in nutrient cycling and energy flow in these ecosystems (Steinke et al. 1993; Cumberlidge et al. 2009). In addition, burrowing species are important for aeration and oxygenation of the dense mangrove mud. The creation of burrows further allows for movement of nutrients and water through the soil, which in turn is beneficial for the growth and development of mangrove seedlings (Steinke et al. 1993). Brachyurans also modify sediment topography and associated microfloral structure (Skov et al. 2002).

The biological survey conducted by Millard and Broekhuysen (1970) in the St Lucia Estuary revealed the presence of twenty-six brachyuran species, all located mainly within the Narrows and estuary basin. However, the same areas are currently dominated by only a few brachyuran species, such as Paratylodiplax blephariskios (Stebbing, 1924), Hymenosoma projectum Dawson & Griffiths, 2012 together with the mangrove crabs Neosarmatium africanum Ragionieri, Fratini & Schubart, 2012 and Chiromantes eulimene (De Man in Weber, 1897) (Owen & Forbes 1997; MacKay et al. 2010). Moreover, the mangroves along the Narrows have been separated from the ocean for virtually the past 10 years (Whitfield & Taylor 2009). Thus, the unstable salinity levels in many parts of the lake are believed to impact on brachyuran diversity negatively (Owen & Forbes 1997). Land use, mostly in the form of agriculture and forestry, is also a major contributor to the decreased diversity within the system, as it leads to deterioration in water quality, reduction in freshwater inflow, and urbanisation of the natural habitat (Darwall et al. 2009). Brachyurans endemic to the north-east region of KwaZulu-Natal are especially vulnerable to environmental degradation, given their restricted distribution range.

Considering that the last thorough survey of brachyuran diversity in St Lucia was conducted by Millard and Broekhuysen in 1970, the primary aim of this study was to investigate current brachyuran diversity within the estuarine system, with particular emphasis on the Narrows, estuary basin and estuary mouth. The extent to which the brachyuran community has been altered was determined by comparing the distribution and abundance of three key species and examining records of past and present surveys. An additional aim of this study was to provide an illustrated, annotated checklist of all brachyuran species recorded historically in the area, in order to update the current database of brachyurans known from the system and to provide an identification guide for future research and management purposes.

MATERIAL AND METHODS

RESULTS

In total, thirty brachyuran species were recorded at St Lucia from 1948 to 2012. In 1948/49, twenty species were found in the system (Millard & Broekhuysen 1970). These are listed in Table 1 and include four of the five sesarmid species, two fiddlers and the freshwater crab Potamonautes sidneyi (Rathbun, 1904). Six additional species were collected in 1964/65 (Millard & Broekhuysen 1970) (Table 1). In 2012, seventeen species were found in and immediately around the St Lucia estuarine system (this study), including the mangroves near the Mfolozi inlet. Four of these crabs were previously unrecorded from the system, viz. Ocypode madagascariensis Crosnier, 1965, Ocypode ryderi Kingsley, 1880, Neosarmatium smithi (H. Milne Edwards, 1853) and Potamonautes cf. lividus, which may represent a new species.

As regards sesarmids, the following inhabitants of mangrove forests were recorded from 1948 to 2012: N. africanum, Parasesarma catenatum (Ortmann, 1897) and C. eulimene. Perisesarma guttatum (A. Milne-Edwards, 1869) has been known from the system since 1964 and Neosarmatium inerme (De Man, 1887), which was present in 1948, has not since been seen in the system. Varuna litterata (Fabricius, 1798) was found near Charter's Creek and on the mudbanks of the Mfolozi in 1948, but currently has been located alive only at the mouth. Dead specimens were also collected after a flood event at False Bay in March 2012, along the shore just south of Lister's Point.

Of the total of thirty species recorded in the system, nine are known only from single records. Aside from N. inerme, Acanthonyx quadridentatus (Krauss, 1843) and Acanthonyx scutellatus MacLeay, 1838 were both recorded only in 1948, in the channel connecting the Mfolozi to St Lucia. Ptychognathus onyx Alcock, 1900 was found in the mud, also at the mouth, in 1949. Macrophthalmus (Mareotis) depressus Rüppell, 1830 and Uca (Gelasimus) vocans (Linnaeus, 1758) were both collected at the Mfolozi inlet, while Uca (Tubuca) urvillei (H. Milne Edwards, 1852) was found at Shark Basin in 1964. Uca (Paraleptuca) chlorophthalmus (H. Milne Edwards, 1852) was recorded at the Mpate River mouth in 1949. Metopograpsus thukuhar (Owen, 1839) was collected in the South Lake at Catalina Bay and at Shark Basin in 1948. To complete the illustrated checklist, specimens of Ashtoret lunaris (Forskål, 1775), P. sidneyi, Cardisoma. carnifex (Herbst, 1796), M thukuhar, Portunus pelagicus (Linnaeus, 1758), U. (P) chlorophthalmus and U. (T.) urvillei, none of which currently occur in the system, were obtained from a variety of locations along the KwaZulu-Natal coast.

The range of Hymenosoma projectum (Fig. 2) appears to have contracted since the survey conducted in 1948 (Day et al. 1954; Millard & Broekhuysen 1970), when the species occurred throughout the system. In 2012, it was found only at Fani's Island, Charter's Creek and Catalina Bay, all stations within the South Lake. The distribution of H. projectum probably fluctuates with the state of the lake and this current, more restricted distribution is possibly due to the drought conditions that have prevailed in the region until recently. P. blephariskios was recorded throughout the Narrows and at the estuary mouth in 1948 (Day et al. 1954) (Fig. 2). However, during the 2012 survey, the species was not encountered in the system. It was only found along the banks of the Mfolozi and the Back Channel which leads into St Lucia. The mangrove crab, N. africanum, is the only species which has maintained its original distribution (Fig. 2). It still occurs where it was previously found in 1948, from the estuary mouth up to the Mpate River mouth in the Narrows (Millard & Broekhuysen 1970; Owen & Forbes 1997).

TABLE 1

Brachyuran species (with previously used names and describing author) collected from St Lucia since 1948. * — As recorded by Millard & Broekhuysen (1970).

Continued

TABLE 2

Density codes indicating the maximum density of brachyuran species at each sampling period in St Lucia Estuary. A = abundant (1001–10000 m^-2), C = common (101–1000 m^-2), R = rare (11–100 m^-2) and V = very rare (1–10 m^-2). Figures in brackets denote average abundance over the entire estuary (m^-2), except for P. blephariskios, found at the Back Channel in 2012.

Fig. 2.

Distribution of Hymenosoma projectum (red), Paratylodiplax blephariskios (grey) and Neosarmatium africanum (blue) in 1948 and 2012.

In terms of abundance (Table 2), P. blephariskios was regarded as common to abundant in the Narrows during 1994 (Owen & Forbes 1997). In 2005, it was recorded as rare in this region (Pillay & Perissinotto 2008) and in 2012, its status was rare in the Mfolozi Back Channel. H. projectum has been designated as either rare or very rare in the Narrows and South Lake and its abundance appears to fluctuate erratically. N. africanum has always been very rare at all locations (Pillay & Perissinotto 2008).

DISCUSSION

Only 13 of the originally recorded brachyuran species appear to be in the St Lucia system at present, with 5 additional species having being found. As most of these species occur naturally in mangroves or on the beach berm, they are the least affected by the extreme salinity fluctuations of the system, which at times experiences a reverse salinity gradient. The exceptions were all at the mouth or the Mfolozi inlet. P. blephariskios individuals were seen burrowing in the muddy banks of the Mfolozi near the inlet; Scylla serrata (Forskål, 1775) was found dead at the mouth and alive on the banks of the Mfolozi; and V litterata occurred regularly at the mouth.

Therefore, the distribution range of brachyurans around the estuarine lake has changed compared to earlier surveys (Millard & Broekhuysen 1970). In the late 1940s, H. projectum specimens were netted as far north as the North Lake, while V litter ata was found at False Bay (Fig. 1). In the 1960s, P. pelagicus occurred as far north as Catalina Bay. In 2012, Fani's Island was the northernmost point of collection of live specimens previously recorded in the system and only H. projectum was found here in high abundance, while only dead V litterata were collected at False Bay. However, P. sidneyi was present in a freshwater stream flowing into the lake just north of Lister's Point and P. cf. lividus was netted from ephemeral pans between Dukandlovu and Lister's Point. This species is yet to be conclusively identified and appears to occupy only ephemeral pans, as it has not yet been found in any other habitat. These pans represent a harsh but unique habitat niche for specialised species, as they are often waterless for long periods during the dry season. It has been suggested by Millard and Broekhuysen (1970) that salinity levels affect crab distribution. They reported an “excessively high” salinity of 89 ppt at False Bay. In recent years, salinity has been much higher in this region, even exceeding 200 ppt at times during 2010”2011 (Carrasco & Perissinotto 2012).

Brachyurans play a prominent role in maintaining mangrove forests, as they facilitate a process known as tidal flushing. The construction of burrows allows for oxygenation of the dense mangrove mud (Vopel & Hancock 2005). Tidal fluctuations or, in the case of St Lucia, wind-driven fluctuations in water levels transport nutrients through the mud and burrows, allowing for the removal of ammonium and other forms of nitrogen by the outgoing flow. Even in systems where tidal movement is negligible or completely absent, the feeding and burrowing behaviour of the inhabitant brachyurans is vital to preservation of the mangrove system. In a study conducted by Smith et al. (1991) in Queensland, Australia, mangrove crabs were removed over a 12-month period to determine whether or not burrowing activity influenced nutrient concentrations, soil sulphide concentration, forest productivity and growth. It was determined that burrowing affects soil aeration, which in turn affects reproduction and growth of mangrove forests. Furthermore, feeding and selectivity of feeding allows for recycling of nutrients and shaping of the mangrove community structure, respectively (Lee 1998).

The genus Uca and the family Sesarmidae are the two most important taxa in South African mangroves in terms of abundance (Skov et al. 2002). Uca maintains an important flow of nutrients by feeding on microphytobenthos, making this source of production available to higher trophic levels (Nagelkerken et al. 2008). By feeding largely on benthic micro-organisms, they alter both the sediment topography and composition of the mangrove forest floor (Skov et al. 2002). However, as this genus has an obligate marine phase for its larvae, it is unable to colonise when there is no sea-estuary connection (Papadopoulos et al. 2002). The current loss of Uca from the St Lucia mangroves is detrimental. There is a similar problem in respect of the swimming crab S. serrata. The only two specimens of this species collected from the system during 2012 were both dead. Hill (1975) reported a similar phenomenon: large numbers of dead and dying S. serrata were found following heavy rainfall in Eastern Cape estuaries. This indicates that the species is drastically affected by a sudden change in physico-chemical parameters, despite its euryhaline nature (Forbes & Hay 1988). The negative impact on the St Lucia S. serrata population could be exacerbated by the need for females to move out to sea with their fertilised eggs in order to release their larvae (Hill 1975). The closure of the mouth means that females have difficulty reaching the sea and larvae have limited access to the estuary once they are released.

In terms of abundance, the brachyurans belonging to the family Sesarmidae are dominant in St Lucia, currently occurring at all mangrove sites around the estuarine lake. Sesarmids feed predominantly on leaf litter in the mangroves (Dahdouh-Guebas et al. 1997) and have been found to remove up to 67% of all leaf litter produced in a day (Olafsson et al. 2002). N. africanum is the largest and most common mangrove sesarmid (Skov et al. 2002) in South Africa. Individuals are mainly herbivorous, with mangrove leaf litter forming approximately 75% of the diet of this species (Steinke et al. 1993). Individuals compete for fallen leaves and drag them back to their burrows where they are left to senesce for the removal of unpalatable tannins. They are then consumed. In this way, mangrove production is retained within the ecosystem, while detritus is broken down, leading to a faster rate of decomposition and facilitating the biogeochemical cycle within the mangrove ecosystem (Steinke et al. 1993; Dahdouh-Guebas et al. 1997). Additionally, the floor remains relatively free from leaf litter and this is especially important in areas lacking tidal influence. N. africanum usually inhabits the landward side of mangrove forests and can survive in fairly dry areas (Dahdouh-Guebas et al. 1997), largely due to its semi-terrestrial, air-breathing habits (Lee 1998). This could be the main reason for their success and dominance around the St Lucia Estuary and lake system (Fig. 2).

In all surveys, the mouth and the Mfolozi inlet have appeared to exhibit the highest diversity in terms of brachyuran species. A Mfolozi-St Lucia link can be considered a particularly valuable feature of the system. Because of its fairly stable physico-chemical properties, the Mfolozi could serve as a refuge when hypersalinity prevails in the St Lucia estuarine lake. This possibility is evident when the diversity of the Mfolozi mangroves is compared to those fringing St Lucia. In 2012, the mangroves around St Lucia were mostly inhabited by only one brachyuran species, with the exception of the boardwalk mangroves and the Bridge, which had two and three inhabitant species, respectively. On the other hand, six species were found at the Mfolozi mangroves, including Uca annulipes (H. Milne Edwards, 1837). The Mfolozi is also currently the only habitat of P. blephariskios in the entire system (Fig. 2). A species endemic to the southeast coast of Africa (Owen 2003), it occurs abundantly in muddy substrata where it plays an important role as a deposit- and filter-feeder (De Villiers et al. 1999). Until recently, the Mhlathuze and St Lucia estuaries both supported the largest populations of P. blephariskios and in 1997, its average density in St Lucia was calculated at 1500 ind.m ^-2(Owen & Forbes 1997). Owen and Forbes (2002) stated that the species is euryhaline and able to survive in the St Lucia Narrows at a maximum salinity of 55 ppt. This salinity tolerance was, however, affected by food availability and temperature and a marked decline in abundance was observed at a salinity of 38 ppt, whereas torpor was induced at 50 ppt. Moreover, the primary method of dispersal for the species is tidal and the lack of tidal fluctuation in the Narrows and the estuary in general means that P. blephariskios has a limited means of dispersal (Owen & Forbes 2002). As the system experiences highly fluctuating salinity levels, it is unlikely that P. blephariskios would be able to survive the current conditions. Owen et al. (2010) have suggested that during periods of crisis, the Mfolozi-Msunduzi system may provide a refuge to organisms that normally occur in the St Lucia estuarine lake. Indeed, P. blephariskios is found at the Back Channel and, should favourable conditions be restored, dispersal and recolonisation from this “refuge population” could occur via a newly restored Mfolozi- St Lucia link (Owen et al. 2010). This is an important consideration and supports the recently implemented reconnection of the St Lucia Estuary to the Mfolozi.

TABLE 3

Distribution of brachyuran species sampled from 1948 to 2012, where: BM - boardwalk mangroves, BP - black pipe, BR - bridge, CB - Catalina Bay, CC - Charter’s Creek, EM - estuary mouth, FB - False Bay, FI - Fani’s Island, HB - Honeymoon Bend, MI - Mfolozi inlet, MR - Mpate River mouth, MT - Makakatana, NA - Narrows and NL - North Lake.

Continued

The North Lake and False Bay are the least diverse areas, inhabited by the lowest number of species found in the various regions. In 1948, there were two species present at each of these two locations (Day et al. 1954; Millard & Broekhuysen 1970) (Table 3), while in 2012, only V. litterata, was found (dead) in False Bay and had probably been washed downstream from a nearby river. The reverse salinity gradient that persists in the system best explains the lack of brachyurans in the northern reaches of the estuarine lake, as even the most euryhaline species would be unable to tolerate the salinity levels currently prevailing in these areas (Carrasco & Perissinotto 2012). H. projectum was once recorded as Hymenosoma orbiculare Desmarest, 1823 until recent genetic studies proposed splitting of the South African H. orbiculare population into five distinct species (Edkins et al. 2007; Teske et al. 2009). These have subsequently been described by Dawson and Griffiths (2012). The species once occurred throughout False Bay and the North Lake (Fig. 2). It is endemic to the east coast of southern Africa, and is known from as far south as Port St Johns (Branch et al. 2010; Teske et al. 2009).

Lawrie and Stretch (2011) proposed three possible scenarios for the future state of the St Lucia estuarine system. In scenario 1, the St Lucia Estuary is separated from the Mfolozi and an open mouth is artificially maintained. Scenario 2 provides for separation from the Mfolozi with no mouth manipulation (closed), while in scenario 3, the St Lucia Estuary and the Mfolozi have a combined inlet with no further manipulation. In the recent past, Scenario 2 has prevailed, although the mouth has now been linked to the Mfolozi (Scenario 3). Scenario 2 is largely associated with high salinity levels and low water levels for prolonged periods, leading to the predominant closure of the mouth. Salinity would be expected to fluctuate between extremely high and extremely low levels. This would negatively affect the diversity and distribution of brachyurans, as large salinity fluctuations and lack of ocean influence in the estuarine lake and surrounding mangroves create conditions that are unfavourable for them. This is problematic when an affected species depends largely on the St Lucia Estuary and is endemic to the region, as is the case with P. blephariskios. Additionally, scenario 2 would prevent recruitment of new species and juveniles from the ocean, leading to a temporary loss of species such as S. serrata and those belonging to the genus Uca. However, species capable of surviving these conditions, such as N. africanum and C. eulimene, would dominate in the system and possibly spread due to lack of competition. When the mouth does open briefly, as it did in March 2007, diversity would probably increase, although unsustainably so because of reversion to the closed mouth state soon afterwards. Mac Kay et al. (2010) reported an increase in the diversity of brachyurans following the overtopping/breaching event of March 2007, which could possibly indicate that larval recruitment had taken place. However, whereas four species were recorded after the storm, only one was found six months later.

In scenario 1, medium to high water levels would persist, although hypersalinity would be experienced about 30% of the time. This would allow for a much higher diversity and abundance of species, as well as faster recovery after hypersaline events, due to greater stability in salinity. Scenario 3 would have the least extreme conditions, with no anthropogenic intervention subsequent to the linking of the Mfolozi and St Lucia systems. The chances of hypersalinity occurring and desiccation taking place are the lowest in this scenario, while abundance and diversity would be highest (Lawrie & Stretch 2011). Boltt (1974) reported rapid re-colonisation of the system by benthic fauna following a period of high salinity. As there are refuge populations of some species around the Mfolozi River, this could be a future possibility and the presence of U. (T.) urvillei has already been noted near the mouth, in March 2013 (R.H. Taylor pers. obs.) (Table 3). The open mouth in scenarios 1 and 3 would allow for the recruitment of juveniles and possibly new species, although the threat of alien invasion would also increase. A good example of a non-indigenous species is the crab Carcinus maenas (Linnaeus, 1758) which, however, has yet to successfully invade the east coast of South Africa, having been found to prefer sheltered bays as opposed to the high-energy coastline of KwaZulu-Natal (Hampton & Griffiths 2007).

There is no well-defined arrangement for the identification of brachyurans within the system and this is partly due to the recent discoveries of pseudocryptic (identifiable through careful morphological analysis, but easily misidentified) and cryptic (morphologically similar but genetically different) species (Sarno et al. 2005), particularly amongst the sesarmids and within the genera Uca and Hymenosoma (Edkins et al. 2007; Teske et al. 2009, Ragionieri et al. 2012). The aim of the illustrated and annotated checklist in the Appendix is to provide interested parties with an updated and definitive means of identification. This will hopefully reduce identification error and facilitate both research and management.