Hydrobiologia DOI 10.1007/s10750-014-2165-1
PRIMARY RESEARCH PAPER
Temporal patterns of megalopal settlement in different areas of an East African mangrove forest (Gazi Bay, Kenya) Lapo Ragionieri • Sara Fratini • Stefano Cannicci
Received: 8 July 2014 / Revised: 15 December 2014 / Accepted: 23 December 2014 Ó Springer International Publishing Switzerland 2015
Abstract Most intertidal brachyurans produce planktonic larvae which develop pelagically and, after a certain time in the ocean, migrate towards the habitats that they will eventually settle in. One of the main physical processes affecting larval release and settlement in species inhabiting estuaries and mangroves is the tidal regime. In this study, we investigated whether patterns of settlement of brachyuran larvae at four sites (differing in tidal inundation and crab zonation) of a Kenyan mangrove were affected by the diurnal and lunar cycle of the tide. We collected megalopae at the four sites twice a day throughout two lunar months. Settlement differed at the four sites: at the subtidal site (the main creek within the forest)
megalopae arrived during diurnal and nocturnal neap and spring tides, while at the three sites within the forest settlement occurred only at spring tide periods. Specific differences among these latter sites existed in terms of full versus new moon spring tides and, to a smaller extent, with diurnal period. Our results show that larval settlement in mangrove forests takes place at both landward and seaward belts and is a temporally complex event, driven by tidal cycles, but also in synergy with other factors. Keywords Brachyuran crabs Planktonic larvae Settlement East African mangroves Tide
Introduction Handling editor: K.W. Krauss L. Ragionieri RNA Biology Laboratory, Department of Biology and CESAM, University of Aveiro, Campus Universita´rio de Santiago, 3810-193 Aveiro, Portugal L. Ragionieri S. Fratini (&) S. Cannicci Department of Biology, Universita` degli Studi di Firenze, Via Madonna del Piano 6, Sesto F.no, 50019 Florence, Italy e-mail:
[email protected] S. Cannicci The Swire Institute of Marine Science and The School of Biological Sciences, The University of Hong Kong, Pokfulam, Hong Kong
Like most marine fauna, the majority of marine decapods produce pelagic planktonic larvae, which can potentially disperse from the parental populations (Shanks, 1995; Sponaugle et al., 2002; Queiroga & Blanton, 2005; Di Bacco et al., 2006). After a speciesspecific time in the planktonic phase, dispersing larvae must return to the adult habitats that they will exploit as juveniles and recruit into the adult populations. The target habitat of this return migration (sensu Shanks, 1995) has the same characteristics as the parental habitat and, in brachyurans, selection of this habitat is achieved during the megalopal stage, which is the final larval stage.
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Hydrobiologia
The megalopal stage includes two phases. During the first, mainly planktonic phase, termed the ‘‘noncompetent’’ phase, megalopae do not possess the physiological capacity to metamorphose, while in the subsequent phase, the ‘‘competent’’ phase, larvae adopt specific strategies to reach the appropriate settlement areas (Epifanio, 1988). Settlement of these post-planktonic larvae represents the transition between the pelagic and benthic phases, when individuals become associated with the benthic substratum (Rodrıguez et al., 1993; Hunt & Scheibling, 1997; Forward et al., 2001). This lifestyle transition is extremely significant in intertidal and semi-terrestrial brachyurans, since megalopae settle in habitats characterised by completely different ecological factors and respiratory media than those of the planktonic marine realm. The supply of new settlers to adult habitats is a crucial process for populations of benthic species, largely determining the geographical distribution of natural populations (Mwaluma & Paula, 2004) as well as their structure and dynamics (Underwood & Fairweather, 1989; Flores et al., 2002; Papadopoulos et al., 2002; Anger, 2006). In intertidal habitats, such as rocky shores, estuaries and mangrove forests, settlement of brachyuran megalopae has proved to be a complex event, variable in time and space (Bilton et al., 2002a, b). Physical processes, such as winds and currents, play an important role in settlement by influencing the transport of larvae to adjacent benthic habitats (Shanks, 1995; Paula et al., 2001; Queiroga & Blanton, 2005; Pardo et al., 2010; Pralon et al., 2012). In coastal habitats, tides are also crucial as they influence the movement of water masses in and out from estuaries or mangrove forests. The tidal periodicity and amplitude, with increased tidal currents during spring tides, are also a deterministic factor responsible for the timing of settlement and recruitment of brachyuran larvae in coastal populations (Moser & Macintosh, 2001; Paula et al., 2001; Flores et al., 2002). Spawning and settlement of intertidal crabs, for example, appear to be greater during spring than neap tides and at night rather than during the day, probably to minimise predation risk (Dittel & Epifanio, 1990; Dittel et al., 1991; Tanskersley et al., 1995; Papadopoulos et al., 2002; Paula et al., 2004; Skov et al., 2005; Christy, 2012), although some examples of diurnal settlement events exist (Moser & Macintosh, 2001).
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During the return migration to the adult habitats, megalopae nevertheless show temporal flexibility in metamorphosis and settlement. Such an ability is intuitively beneficial, since this trait can enhance the probability of locating suitable microhabitats for juvenile and subsequent adult survival (Gebauer et al., 2002). One East African mangrove crab, Chiromantes ortmanni, can, for example, extends its planktonic period by developing into an unusual VI zoea stage before becoming a megalopa (Guerao et al., 2012). Laboratory experiments have shown that the final megalopal competent phase, which occurs after 2–4 days from megalopal metamorphosis (O’Connor & Van, 2006; O’Connor, 2007; Steinberg et al., 2007; Simith et al., 2010), can be triggered by specific chemical and/or physical cues associated with the juvenile and/or adult habitat (Forward et al., 2001; Gebauer et al., 2002; Simith et al., 2013). Physical factors such as the characteristics of the substratum of the parental habitat (Christy, 1989; O’Connor & Judge, 1999; Gebauer et al., 2002; Diele & Simith, 2007) and specific temperatures and salinities (Wolcott & de Vries, 1994; Diele & Simith, 2006) can, therefore, influence settlement. Biological factors such as water soluble chemicals released by conspecific adult crabs (Jensen, 1989; Jensen & Armstrong, 1991; O’Connor & Gregg, 1998; Diele & Simith, 2007; Simith et al., 2010, 2013), inter-specific odours (Gebauer et al., 1998, 2002) and microbial biofilms (Christy, 1989; Diele & Simith, 2007) also feature as stimulants for metamorphosis. In mangrove forests, where brachyurans represent a dominant taxon in terms of biomass and number of species (Cannicci et al., 2008), the choice of the right microhabitat during settlement can be crucial for the survival of the megalopae. Mangrove systems are spatially complex, being characterised by extreme differences in the environmental conditions among the seaward belts which are inundated daily and the landward belts which are only inundated on a monthly basis. As a consequence, Moser & Macintosh (2001) and Paula et al. (2001) reported high levels of megalopae settlement in the seaward belts, which led to the suggestion that megalopae of semi-terrestrial crabs, which colonise the more physically harsh landward belts, also metamorphose in more marine microhabitats and then re-invade, as juveniles, the belts they will occupy as adults. Subsequently, however, Paula et al. (2003) described a stratified
Hydrobiologia
settlement pattern in a mangrove forest of Inhaca Island, Mozambique, reopening the debate on the spatial preferences of megalopae settlement. Paula et al. (2003) suggested that the larvae of mangrove crabs probably develop specific mechanisms to settle in the same area inhabited by con-specific adults, thus supporting laboratory observations on the role of conspecific odours for triggering metamorphosis (Gebauer et al., 1998, 2002; Simith et al., 2013). To contribute to this debate, we deployed a number of megalopal collectors at four sites within the mangrove forest of Gazi Bay, Kenya, with a twofold aim. Firstly, we aimed to test for spatial variation in the settlement pattern of megalopae by sampling at both landward and seaward mangrove belts. At each sampling site, the tree cover as well as the abundance and diversity of the resident crab fauna were recorded to assess possible interrelationships among adult communities and settlement intensity. Secondly, settlement was monitored throughout two lunar months to further investigate an effect of tidal phase and any possible diurnal effects on settlement.
Materials and methods Study area The study was conducted in Gazi Bay (4°220 S; 39°300 E), 50 km south of Mombasa, South coast of Kenya. The bay is connected to the Indian Ocean through a 3,500 m wide opening characterised by the presence of an uneven reef system. The average depth of the bay is 5 m (Kitheka, 1996). Two tidal creeks, formed by the Kidogoweni and the Kinondo rivers, whose banks are dominated by mangrove vegetation, receive a freshwater supply during the wet season, i.e., between April and June. The water circulation in Gazi Bay is controlled by the river discharge, tidal patterns, and onshore winds (Kitheka, 1997). Salinity in the bay and in the Kidogoweni creek is influenced by the freshwater supply, evaporation, and oceanic influx (Kitheka, 1997). Tides are semidiurnal with an average height of 3.2 m, above datum at spring tide, and 1.4 m at neap tide. Tides can reach a maximum height of 4 m during equinoxial spring tides. Tidal currents are 50% stronger during spring than during neap tides (Kitheka, 1996). During tidal flooding, the current follows the
coastal line of the bay directed toward the entrance of the Kidogoweni creek. Offshore winds blow shoreward throughout the year. The forest of Gazi Bay covers a 5-km2 area and shows the typical pattern of tree zonation well known for East African mangrove forests (Macnae & Kalk, 1962; Macnae, 1968; Dahdouh-Guebas et al., 2002). A number of clear belts can be seen from from land to sea including: a landward belt dominated by dense, welldeveloped trees of Avicennia marina with a fine-sandy substrate, flooded once a month at the highest spring tides; an open belt sparsely covered by A. marina and Ceriops tagal shrubs, characterised by a sandy substrate and flooded, on average, twice a month during spring tides (‘Avicennia parkland’, sensu Macnae, 1968); a belt densely inhabited by C. tagal trees, with a sandy substrate; and, finally, the most seaward zone comprised dense stands of Rhizophora mucronata trees with a fine and muddy substrate and flooded twice a day. Sampling area selection Three of the four experimental sites were chosen to represent the above described belts (Fig. 1), with the exception of the Ceriops dominated belt, which is known to host a low diversity and sparse crab fauna (Dahdouh-Guebas et al., 2002). From land to sea, the first site was selected in the landward A. marina dominated belt (Avicennia site, 4°250 17.500 S; 39°300 27.500 E); the second was established within the Avicennia parkland belt (Avicennia parkland, 4°240 59.600 S; 39°300 31.200 E); while the third was set in the R. mucronata dominated belt (Rhizophora site, 4°250 1.400 S; 39°300 32.700 E). A fourth site was finally set in the middle of the main channel of the Kidogoweni creek, two hundred meters up the creek (Channel site, 4°250 11.100 S; 39°300 43.700 E) and was permanently submerged. Assessment of diversity and abundance of adult crab populations Species richness and abundance of crab species at each intertidal site were determined at spring and neap tides along two random transects (100–500 m apart). In each transect, five 2 9 2 m quadrats were randomly established and different sampling techniques were used to assess the abundances of the crabs of the
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Hydrobiologia Fig. 1 Map of Gazi Bay (adapted from DahdouhGuebas et al., 2002) showing the position of the sampling sites (Av Park, Avicennia parkland; Av, Avicennia site; Rhiz, Rhizophora site, and Chan, Channel site)
various families due to their differing behaviour (Skov et al., 2002; Cannicci et al., 2009). For fiddler crabs (genus Uca), represented in Gazi Bay by U. annulipes, U. inversa, U. chlorophthalmus, and U. urvillei, individuals were first counted visually in each quadrat to assess the frequency of the different species present. Secondly, crab burrows were counted in three random 50 9 50 cm sub-quadrats to avoid underestimation of individuals not active during the visual counts. The density of each species was thus obtained from the burrow counting data and calibrated with the species ratio (Skov et al., 2002). The small sesarmids, represented by Chiromantes ortmanni, C. eulimene and Perisesarma guttatum, were counted visually throughout the quadrat. Visual counts were conducted 2 h after the diurnal low tide using binoculars at a distance of 3.5 m from the plot. Observers remained still for 15 min before counting, following a standardised protocol (see Hartnoll et al., 2002; Skov et al., 2002).
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The density of large burrowing sesarmids, represented by Neosarmatium africanum (formerly N. meinerti, Ragionieri et al., 2012) and N. smithi, was assessed by counting the operational burrows, which are known to be occupied by single crabs (Fratini et al., 2000; Emmerson, 2001; Skov et al., 2002; Berti et al., 2008), in a subsample of three 2 9 2 m quadrats in each transect at every site. Sampling of megalopae Megalopal collections were carried out twice a day over 2 months, between 2nd of February and 23th of March 2007. Within this period, four spring tide and three neap tide periods were identified. At each site, three passive artificial collectors were deployed. The collectors consisted of artificial hog hair filter sheets of 1.5 cm 9 40 cm 9 40 cm deployed flat on the substrate with the corners fixed with sticks (Paula et al., 2001). At the channel site, the hog hair filter sheets
Hydrobiologia
were fitted around PVC cylindrical pipes (40 cm long with 10 cm of diameter) attached to a long stick fitted in the middle of the creek (van Montfrans et al. 1990; Paula et al., 2001). The collectors were changed twice a day during the low tide and replaced with clean collectors that had been previously used at the same site for avoiding the risk of mixing possible unknown chemical cues. After their retrieval, the collectors were placed into plastic bags and brought back to the laboratory where they were washed in freshwater to retrieve juveniles and megalopae which were stored in eppendorf vials with 75% ethanol at 4°C. Megalopae were subsequently counted and their carapace length (CL, estimated as the distance between the tip of the rostrum and the posterior margin of the carapace) measured under a stereoscopic microscope. Since it is very difficult to discriminate on the basis of morphological characteristics between megalopae of Ocypodidae and Sesarmidae (i.e. the most common families at our sampling sites), and since the mangrove genera of East African Sesarmidae are on average larger than the Ocypodidae, we measured megalopal size as a rough discrimination tool based on the positive relationship between adult and megalopa size in brachyurans (Hines, 1986). Data analysis To analyse temporal patterns of recorded settlement, a two-way Permutational Analysis of Variance (PERMANOVA, Anderson, 2001) design was utilised, for each experimental site, to test the null hypothesis of no differences in settlement at different lunar and tidal phases and at different light conditions. To analyse settlement trends in the two landward sites, Avicennia site and Avicennia parkland which were never inundated at neap tide, the factors ‘‘lunar phase’’ (full or new moon, fixed and orthogonal) and ‘‘light’’ (day or night, fixed and orthogonal) were included in the analysis. For the Rhizophora and the channel sites, the factors ‘‘tidal phase’’ (spring or neap tide, fixed and orthogonal) and ‘‘light’’ (defined as above) were included. Prior to each analysis, homogeneity of variances was assessed using Levene’s test. Since the test was found significant for all the analyses, data were ln(x ? 1) transformed to obtain homoscedasticity. SNK post hoc tests were utilised for multiple comparisons among significant factors. Linear regression tests were also utilised to investigate possible
relationships between the height of the tide and the number of megalopae collected at each site. Finally, for comparing the mean carapace length of megalopae and the differences in frequency distributions of megalopal size among different sites, a oneway ANOVA and a v2 were performed, respectively. All analyses were performed using PAST and the PERMANOVA ? package for PRIMER (Anderson et al., 2008).
Results Assessment of diversity and abundance of adult crab populations The estimated species richness and abundance per crab species differed greatly at each study site (Fig. 2). At the Avicennia site, only sesarmids were present, in particular Neosarmatium africanum and Chiromantes ortmanni; at the Avicennia parkland site the ocypodids, Uca annulipes and U. inversa dominated, although C. ortmanni was also present. In the Rhizophora site, two species of sesarmid crabs (Perisesarma guttatum and Neosarmatium smithi) and two species of ocypodids (U. urvillei and U. chlorophtalmus) were found. The Channel site was permanently submerged and did not host any intertidal mangrove crab species (hence not included in Fig. 2). Most of the species were thus site specific, with only two species of small sesarmids, Perisesarma guttatum and Chiromantes ortmanni, being present in two sites (the former in the Avicennia parkland and Rhizophora site and the latter in the Avicennia site and Avicennia parkland). Sampling of megalopae Throughout the sampling period, a total of 1,242 individuals, of which 879 were megalopae and 363 juveniles, were collected. The juveniles were excluded from analyses. Different temporal patterns of settlement were recorded at the four sites (Fig. 3). Settlement of megalopae within the two landward belts of the forest of Gazi Bay was significantly associated with lunar phases (Tables 1, 2; Fig. 3), but showing opposite trends. On the new moon, which coincided with the equinoxial spring tide, more settlers were collected at the most landward belt dominated by A. marina, while
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(a) 120 Abundance (specimens m-2)
Fig. 2 Abundance of adult crab populations expressed as mean (±SE) of individuals per square meter, recorded at the three intertidal sampling sites. U. ann. Uca annulipes; U. inv. U. inversa; U. chl. U. chlorophthalmus; U. urv. U. urvillei; P. gut. Perisesarma guttatum; C. eul. Chiromantes eulimene; C. ort. C. ortmanni; N. afr. Neosarmatium africanum, N. smi. N. smithi
Avicennia site
100
Avicennia parkland Rhizophora site
80 60 40 20 0
Abundance (specimens m-2)
(b)
U. ann.
U. inv.
U. chl.
U. urv.
30 25 20 15 10 5 0 P. gut.
the maximum peak of settlers in the Avicennia parkland site was recorded at full moon. At the Avicennia site, more settlement took place during the night at new moon (P \ 0.01, PERMANOVA Post hoc test, Fig. 4). Although there was no significant diel variation in catches of megalopae at the Avicennia parkland, the highest number of settlers was recorded at night during the third spring tide (full moon) of the sampling period, with more than 160 larvae trapped in just one night (Fig. 3). No megalopae were ever caught during neap tide at the Rhizophora site, (Table 2; Figs. 3, 4). In contrast, in the Channel site, megalopae were collected both during spring and neap tides, with the highest number of megalopae collected during the day at spring tide (P \ 0.01, PERMANOVA Post hoc test, Fig. 4). There was a significant relationship between the height reached by the tide and the number of settlers collected at the Avicennia, the Rhizophora and the Channel sites. All linear regressions, however, showed very low R2 values (Table 3). There was a significant difference in average CL among all the four sites (SNK tests following ANOVA
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C. eul.
C. ort.
N. afr.
N. smi.
Test: F = 170.25; df = 3; P \ 0.0001; Channel site, mean CL 1.3 ± 0.01SE mm [ Avicennia parkland 1.18 ± 0. 03 mm [ Avicennia site, 1.1 ± 0.04 mm [ Rhizophora site, 0.98 ± 0.01 mm). Differences among the four sites also emerged in the frequency distribution of length classes (v2 = 1047.8, df = 30, P \ 0.001: Fig. 5a–d). The Channel site was the only site with a clear bimodal frequency distribution, with a few megalopae larger than 2 mm (Fig. 5d); while the frequency distributions of the other three sites were unimodal, each centred on different median values (Fig. 5a–c).
Discussion The present study, carried out at the mangrove forest of Gazi Bay, was designed to address two relevant issues for the debate on spatial and temporal settlement patterns of intertidal brachyuran crabs. With regards to the spatial patterns, our data support the hypothesis of a strongly stratified pattern of megalopal recruitment in East African mangroves (Paula et al., 2003). Larval
Hydrobiologia
(a) 4,5
(b) Tidal range (m)
4 3,5 3 2,5 2 1,5 1
3
5
7
9
11 13 15 17 19 21 23 25 27 29 31 33 35 37 39 41 43 45 47 49 51 53 55 57 59 61 63 65
Sampling days
N. of megalopae collected
(c) 20 15 10 5 0 1
3
5
7
9
11 13 15 17 19 21 23 25 27 29 31 33 35 37 39 41 43 45 47 49 51 53 55 57 59 61 63 65
Sampling days
N. of megalopae collected
(d) 200 160 120 80 40 0 1
3
5
7
9
11 13 15 17 19 21 23 25 27 29 31 33 35 37 39 41 43 45 47 49 51 53 55 57 59 61 63 65
Sampling days
N. of megalopae collected
(e) 20 16 12 8 4 0 1
3
5
7
9
11
13
15
17
19
21
23
25
27
29
31
33
35
37
39
41
43
45
47
49
51
53
55
57
59
61
63
65
Sampling days
Fig. 3 Differences in tidal range (a) and number of settlers in the collectors deployed at (b) the Avicennia site, c the Avicennia Parkland site, d the Rhizophora site and e the channel site along
the study period. In panel a, data points indicate the tide heights as reported in the Standard Reference Tide Tables for Kilindini (Kenya) at the different days and the line the moving average
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Hydrobiologia Table 1 Two-way PERMANOVAs to investigate variation in settler numbers (ln (x ? 1) transformed) recorded at the Avicennia and Avicennia parkland sites Source
Avicennia site df
Avicennia parkland
MS
F
df
MS
F 24.402**
Moon—m
1
5.159
21.406**
1
28.010
Light—l
1
1.227
5.091*
1
1.984
1.728
m9l
1
1.227
5.091*
1
0.039
0.034
Res
110
0.241
119
1.148
Total
113
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The factors were: Moon (2 levels: full moon, new moon) and Light (2 levels: day, night), orthogonal and fixed (* P \ 0.05; ** P \ 0.01)
Table 2 Two-way PERMANOVAs to investigate variation in settler numbers (ln (x ? 1) transformed) at the Rhizophora and Channel sites Source
Rhizophora site
Channel site
df
df
MS
F
MS
F
Tide—t
1
2.287
15.972**
1
0.51232
Light—l
1
0.162
1.134
1
0.24858
3.9259 1.9049
t9l Res
1 164
0.162 0.143
1.134
1 184
1.4851 0.1305
11.38**
Total
167
187
The factors were tide (2 levels: spring, neap tide) and light (2 levels: day, night), orthogonal and fixed (* P \ 0.05; ** P \ 0.01)
settlement was recorded throughout the sampling period at both the seaward and landward fringes of Gazi Bay forest in line with patterns reported for Mozambique (Paula et al., 2003). This stratified settlement, therefore, may suggest that the zonation of adult populations of crabs may be determined as early as from habitat selection by settling megalopae. Regarding temporal patterns, our results revealed variable and complex patterns of settlement the ecological drivers for which could only partially be identified. Some temporal trends were however recognisable. At the most landward of the sampled sites (the Avicennia site), a significantly higher number of megalopae was collected during the highest of the two monthly spring tides, which occurred during new moon. In contrast, at the Avicennia parkland site, megalopae settled during full moon spring tides. Whilst no megalopae ever recruited at the most seaward site
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during neap tide in this study, the Rhizophora site, they were recorded at every spring tide. Finally, no significant difference in megalopae was recorded between tides in the Channel site, as larvae were collected during both spring and neap tides. The relationship between the number of collected megalopae at each tide and tidal height was significant but weak at all sites, with the exception of the Avicennia parkland site where the largest settlement event was recorded during the lowest of the two spring tides. Over a lunar month, tides show a cyclicity in tidal amplitude of new moon and full moon spring tide, recently defined as ‘‘Syzygy Tide Inequality Cycle’’ (STIC: Schmidt et al., 2012), with a periodicity of 13.6 months. During the study period in Gazi Bay the highest of the two monthly spring tides occurred at new moon, with a range of differences between the two tidal amplitudes, at datum, of 20–30 cm. Skov et al. (2005) reported a synchronisation of mangrove crab spawning with the STIC in Kenya and Tanzania, with strong correlations between the highest of the spring tides and larval release, especially in species inhabiting the landward belts of the mangroves. If we consider that the majority of crab species present in the mangrove of Gazi Bay have a mean Planktonic Larval Duration (PLD) of 4 weeks (Pereyra Lago, 1987, 1989, 1993), we would predict settlement in the landward belts at new moon, i.e. 4 weeks after the spawning events recorded by Skov et al. (2005). Even if the pattern of settlement at the most landward site was in agreement with these cues, the largest settlement event took place in the Avicennia parkland during full moon, the lowest of the two sampled spring tides in the lunar month. These findings seem to support the idea that reproductive synchronisation to STIC is only one of the key drivers shaping temporal patterns of settlement. Apart from tidal influence, settlers were consistently higher at night than during the day in the Avicennia site, while no significant difference between day and night was present in the other sampling sites. A preference for nocturnal recruitment by the larvae of mangrove crabs has been reported in other studies (Dittel & Epifanio, 1990; Paula et al., 2001; Papadopoulos et al., 2002). The choice of the nocturnal settlement is common among many brachyuran species and is linked to the avoidance of visual predators, such as juvenile fish, which are abundant in mangrove creeks and estuaries (Branda˜o et al., 2011). Diurnal
Hydrobiologia Fig. 4 Mean numbers (±SE) of megalopae settling at day and night and at full and new moons at Avicennia and Avicennia parkland sites (a); and at day and night as well as at spring, full and new moon, and neap tides at the Rhizophora and at the channel sites (b)
(a) 25
Avicennia site Avicennia parkland
Mean number of megalopae
20
15
10
5
0 Day
Night
Day
Full mo o n
Night New mo o n
(b) 1.4
Channel site Rhizophora site
Mean number of megalopae
1.2 1.0 0.8 0.6 0.4 0.2 0.0 Day
Night
Neap tide
Table 3 Linear regression tests between the height of the tide and settler numbers for each sampling event, performed for each site F
R2
Belt
df
MS
Avicennia site
1
12.798
8.632*
0.193
Avicennia parkland
1
57.147
0.554
0.193
Rhizophora site
1
5.097
15.766**
0.226
Channel site
1
1.415
4.908*
0.074
* P \ 0.05; ** P \ 0.01
preferences for settlement have, however, also been reported (Moser & Macintosh, 2001) who suggested that synchronisation of settlement with day spring tides in Uca vocans is a consequence of the high
Day Full moon
Night
Day
Night
New moon
turbidity of the creek waters, which aids avoidance of visual predators. In the present study we recorded significant differences in mean carapace length of megalopae at the four sites as well as different size class frequencies at the two landward and the Rhizophora site. Since megalopal size is known to be positively correlated with adult size (Hines, 1986), these differences could be interpreted as indicators of the arrival of different species at the four study sites. We did not, however, record a settlement of larger megalopae in the Avicennia site where the largest crab species, i.e. N. africanum, was dominant. We are thus not able to support a stratified settlement by the megalopae based on the selection of a site occupied by con-specific adults, as shown by Simith & Diele (2008) and proposed by Paula et al. (2003).
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Hydrobiologia
(a)
Avicennia site
Number of individuals
40 30 20 10 0
1.2 1.3 1.4 1.5 1.6 1.7
2
2.5
3
3.5
4
4.5
Size frequency class Avicennia parkland
(b) Number of individuals
500 400 300 200 100 0 1.2 1.3 1.4 1.5 1.6 1.7
2
2.5
3
3.5
4
4.5
Size frequency class Rhizophora site
(c) Number of individuals
40 30 20 10 0 1.2 1.3 1.4 1.5 1.6 1.7
2
2.5
3
3.5
4
4.5
Size frequency class
(d)
Channel site
Number of individuals
40 30 20 10 0 1.2 1.3 1.4 1.5 1.6 1.7
2
2.5
3
3.5
4
4.5
Size frequency class
Fig. 5 Size class frequency distribution of megalopae, expressed as Carapace Length (CL), collected at the Avicennia site (a), Avicennia parkland site (b); Rhizophora site (c) and Channel site (d)
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The variability in carapace length of settling megalopae at the Channel site was also greater than at the three intertidal sites and the frequency class size distribution showed a clear break between the two groups of settlers. Megalopae belonging to the most common size classes trapped at all other sites were most common, but larvae belonging to larger size classes (not present at the other three sites) were also present, suggesting the presence of large subtidal species which do not settle in the mangrove, such as portunids and xanthids. There are two possible explanations for the size class distribution recorded at the Channel site: firstly larvae transported by the tide into areas unsuitable for adult life are transported back to the main channel by the ebb tide; and secondly few species typically settling in coastal areas other than mangroves are transported by tidal currents within the main creek. The ‘‘re-invasion’’ of pelagic larvae from open oceanic waters to coastal habitats may be controlled by several factors (beside tides) such as seaward breezes, currents and active swimming behaviour of the larvae, whilst, once the larvae have reached the mangrove creek, they may await in the main channel to be transported to specific areas within the mangroves guided by other physical factors, such as periodic tidal inflow (Bilton et al., 2002a, b). Secondly, larvae which did not find settling cues can delay metamorphosis even for a period double their post-larval stage or until death, being transported back to the main channel of the creeks by the ebb tide (Gebauer et al., 2002; Simith & Diele, 2008). Such behaviour, evolved to favour settlement in the most suitable habitat for the species, may be a source of variability in settlement and may favour the colonisation of novel areas (O’Connor & Van, 2006; Simith et al., 2010). In conclusion, larval settlement in Gazi Bay occurs across the whole forest following a complex temporal pattern partly driven by tides in synergy with a series of abiotic and biotic factors which were not clearly isolated during this study. All these factors are responsible for the temporal variability of settlement over a monthly (spring and neap tides) and diurnal scale (night/daylight). Some species of crabs have megalopae that settle in habitats different from the adults and successively migrate, as juveniles, to the habitat they will exploit as adults (Hartnoll & Clark, 2006). Our results on East African mangrove crab
Hydrobiologia
megalopae support the hypothesis that timing of settlement may be driven by several physical factors apart from tides (such as wind driven surface currents, turbulence, darkness) and underlie how challenging it can be to forecast settlement of brachyuran crabs in such dynamic habitats like mangroves. Acknowledgments This study was funded by the EU 6FP PUMPSEA Project, contract No. INCO-CT2004-510863, by the SP3-People (Marie Curie) IRSES Project CREC (No. 247514) and by MIUR funds (Cannicci ex-60%). We thank Benedetta Finocchi, Riccardo Simoni, Marco Fusi, Filippo Cimo`, Fabrizio Bartolini and Elisha M’rabu Jenoh for their help during the field work and the essential help of the research team of the Gazi Research Station of the Kenya Marine and Fisheries Research Institute, superbly led by Dr. James G. Kairo. We are also grateful to Francesca Porri and Gray Williams for their precious comments to the manuscript and to the two anonymous Reviewers for their useful suggestions.
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