Wetlands Ecology and Management (2006) 14: 1–9 DOI 10.1007/s11273-004-5075-6
Springer 2006
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A comparison of methods for estimating relative abundance of grapsid crabs C. P. Salgado Kent* and K. A. McGuinness Faculty of Education, Health and Science, Charles Darwin University, Darwin NT 0909, Australia; *Author for correspondence (Present address: Centre for Marine Science and Technology, Curtin University of Technology, Kent St., Bentley, WA 6102, Australia; e-mail:
[email protected]; phone: +61-89266-3104) Received 27 January 2004; accepted in revised form 18 October 2004
Key words: Burrow counts, Estimating crab density, Grapsidae, Mangroves, Pitfall traps, Relative abundance, Sesarmid
Abstract Grapsid crabs are one of the most common, and potentially important, elements of the mangrove fauna but relatively little information is available on patterns in their distribution and abundance. In part, this may be due to difficulties in estimating the abundance of burrowing species. By not having reliable methods of estimating changes in distribution and abundance of crabs, ecological impacts of crabs may be greatly underestimated. We tested several methods for estimating the apparent abundance of eight species of grapsids in a north Australian mangrove forest. These methods included continuous and instantaneous visual counts at two distances, two types of pitfall traps and photography. We also excavated crabs to test the reliability of the best of these methods. Overall, pitfall traps equipped with funnels proved most useful, although these did preferentially capture larger crabs. An exception was the large crab, Neosarmatium meinerti, which was rarely captured and more reliably estimated by burrow counts. Traps proved to be most useful in this study and may be for long term studies of grapsid species, however, the selection of a method should be made after careful evaluation of the questions and relevant information required for any particular study. Finally, these methods may also prove to be useful in other environments such as salt marshes.
Introduction Grapsid crabs (which include the sesarmids) are one of the most abundant groups of fauna inhabiting mangrove forests (Golley et al. 1962; Jones 1984; Smith et al. 1991), and recent research indicates that they play important roles in the ecology of these ecosystems (see review by Lee 1998). They may affect forest structure by attacking mangrove propagules (Smith 1987; McGuinness 1997a), influence nutrient cycling by feeding on litterfall (Robertson 1986) and alter the properties of the
soil by their burrowing activities (Smith et al. 1991). As a consequence, Smith et al. (1991) suggested that sesarmid crabs may ‘occupy a keystone position in the overall ecology of Australian mangrove forests.’ Despite increasing interest in the role of grapsids in mangrove ecosystems, there are still relatively few studies testing for, and attempting to explain, patterns in the distribution and abundance of these animals, although such information is clearly important. In part, this may be due to the difficulties involved in obtaining reliable estimates of
2 the abundance of these cryptic, burrowing animals. Indeed, the effectiveness of the various methods that have been used to estimate grapsid abundance is not well understood (Lee 1998). This situation differs from that of the other main group of crabs in mangroves, the ocypodids, for which recent studies have tested and compared methods. For example, Nobbs and McGuinness (1999) tested the effectiveness of several observational protocols for four Uca species, and Skov and Hartnoll (2001), Skov et al. (2002), and Jordao and Oliveira (2003) compared the suitability of binocular observations, burrow counts and excavations for quantifying the abundance of Uca spp. Some of these methods have been tested in salt marsh habitats as well (Johnson 2003). The results of these studies may, however, not transfer from ocypodids to grapsids because the two kinds of crabs may display different behaviours. For example, Skov et al. (2002) found that visual counts underestimated U. annulipes by 27–37% (varying according to site), but underestimated N. meinerti by as much as 49%. Nobbs and McGuinness (1999) noted that pitfall traps (which are commonly used to sample arthropods, reptiles and mammals; Southwood and Henderson 2000) were unsuitable for estimating the abundance of ocypodids because these crabs rarely fell into traps. Pitfall traps, in contrast, have been used successfully in studies of grapsid crabs (Warren 1987; Frusher et al. 1994). For cryptic animals, such as burrowing crabs, the distinction between apparent and absolute abundance is important. Apparent abundance involves estimates of the relative numbers of individuals and is used to compare the densities of active animals among areas or times (Caughley 1971; Warren 1990). Estimates of apparent abundance may vary through time simply because of changes in the activity of individuals but, in environments such as mangrove forests, obtaining estimates of absolute abundance is often prohibitively destructive as it usually requires excavation. Any study using excavation which incorporates reasonable spatial and temporal replication would almost certainly involve considerable disturbance to the habitat. This disturbance could affect the behaviour of the crabs, and invalidate the results of the study, even if it were not considered unacceptable for other reasons. On the other hand, limited excavation may be done, as in this study, to
test and validate other methods (see Skov and Hartnoll 2000; Skov et al. 2002; Jordao and Oliveira 2003). Thus, the overall objective of this study was to test several methods for estimating abundance of sesarmids. Some of these methods have already been used previously in studies on sesarmids (Warren 1987; Frusher et al. 1994; Micheli et al. 1991; McGuinness 1994, 1997a, b, c; Emmerson 2000) or other crabs (Nobbs 1999; Johnson 2003) but comparisons of their usefulness are limited or rare (Lee 1998). Various considerations (see later), suggest that most underestimate absolute abundance, therefore the study aimed to determine the method with higher values, which did not vary significantly in efficiency among crab species or habitats.
Methods The methods for measuring apparent abundance that were compared in this study covered the range used in studies in mangrove forests (as well as other habitats such as salt marshes and salt flats) and included observational (visual counts of animals active on the surface), photographic, pitfall trap captures and burrow counts. The observational experiments were designed to assess the recovery time required for crabs to emerge from their burrows after disturbance, the effect of the type of observation (continuous versus discontinuous) on the numbers of crabs observed, and the effect of the distance of the observer on the numbers of crabs observed. Two kinds of pitfall traps were tested – traps with and without funnels – both of which have been used in previous studies (Warren 1987; Frusher et al. 1994). The photographic method provided an instantaneous count with a view from above the quadrat, whereas observational counts relied on counts taken from a distance with a sidelong view through binoculars. Pitfall trap captures were also compared with burrow counts of Neosarmatium meinerti de Man 1887 burrows because the latter type of estimate has been used in previous research (e.g. Micheli et al. 1991; McGuinness 1994, 1997a; Lee 1998). This method can be used with N. meinerti because the burrows are large, hooded, and thus easily identified (in contrast to other species where burrows are not easily distinguished from one another and from crabs of other families). Although N. meinerti
3 was not anticipated to be the most abundant species in this study, assessing the effectiveness of abundance estimation is important since the species is known to be a major consumer of mangrove litter in Australia and Africa (Micheli et al. 1991; Emmerson and McGwynne 1992; McGuinness 1994; Dahdouh-Guebas et al. 1997; McGuinness 1997a, b, c; Salgado Kent 2004). Finally, the method found to be most useful was then compared with absolute counts to measure its accuracy and efficiency in sampling different species among several habitats. In addition to comparing numbers of crabs sampled by different methods, population characteristics were also compared. Population characteristics included mean carapace width, sex ratio, and the proportion of females that were ovigerous. These measurements were only possible, however, for crabs that were excavated and caught in pitfall traps.
referred to as Episesarma. Neosarmatium meinerti, Clistocoeloma merguiensis, Ilyograpsus paludicola, Sesarmoites borneensis, and Metopograpsus latifrons were all clearly distinguishable and were recorded at species level.
Study site Work was done in northern Australia at Ludmilla Creek, in Darwin Harbour, a site selected because it offered easy access to a range of habitats (see McGuinness 1994, 1997a, c for descriptions of this forest). All experiments were done in the tidal bank, tidal flat and hinterland assemblages of this forest. The tidal bank assemblage was dominated by Rhizophora stylosa mangroves while the tidal flat and hinterland assemblages were dominated by Ceriops tagal. Apparent abundance experiments were carried out over a 3-day period during spring tides: the 26–28 of November 1998, and during the 5 h of low tide in the daytime.
Crab species The grapsid crabs found in this study belong to two subfamilies, the Sesarminae and the Grapsinae (Dana 1851). The Sesarminae, in this study, include Sesarma (Perisesarma) darwinensis Campbell 1967, Sesarma (Perisesarma) semperi semperi Bu¨rger 1896, Neosarmatium meinerti de Man 1887 (Figures 2 and 3), Episesarma sp. nov, Sarmatium unindentatus Davie 1992, Sarmatium hegerli Davie 1992 Sarmatium germaini A. Milne Edwards 1869, and Sesarmoides borneensis Tweedie 1950. The Grapsinae include Clistocoeloma merguiensis de Man 1888, Ilyograpsus paludicola Rathbun 1909, and Metopograpsus latifrons White 1847. All of the genera (and many of the species) occur in the Indo-Pacific region, and some have distributions in mangrove habitats around the world. All crabs recorded during sampling were identified by genus, subgenus, or species, according to the level at which the grapsids could be easily distinguished in the field. Sesarma darwinensis and Sesarma semperi were grouped together and simply recorded as Sesarma. Sarmatium unindentatus, Sarmatium hegerli, and Sarmatium germaini were also grouped into their genus, Sarmatium. Episesarma sp. nov, was easily identified, but since the species has not been described nor named, it is
Experiment 1: Recovery times In their tests of observational methods, Nobbs and McGuinness (1999) found that most Uca emerged within about 10 min of the observer taking position and concluded that this was a suitable ‘recovery time’. This experiment was done to determine an appropriate ‘recovery time’ for sesarmids. Three quadrats 0.75 · 0.75 m were marked with translucent, nylon fishing line wrapped around thin wooden skewers inserted into the sediment (Nobbs and McGuinness 1999 found that the use of fishing line did not affect counts of Uca species). The size was selected on the same basis as Nobbs and McGuinness (1999): it was large enough to include a reasonable number of crabs but not so large that all individuals could not be distinguished and followed. In this experiment these quadrats were observed simultaneously and were placed about 6 m apart in an arc around the observer’s viewpoint. The three quadrats were observed continuously for 30 min and the time of appearance and species of all crabs emerging from burrows were recorded. A repeated measures analysis of variance (ANOVA) on percentage of crabs that emerged at
4 the identified suitable recovery time was used for the analysis, with factors including assemblage (fixed, three levels) and day (repeated, fixed, two levels). A repeated measures analysis was used since it was unlikely that days would be independent from each other since the same quadrats locations were used on consecutive days. Data were tested for homogeneity of variances using Cochran’s Test to ensure that the data fit the assumptions of ANOVA (this was conducted wherever ANOVA was used throughout this paper).
Experiment 2: Comparison of continuous and instantaneous counts at two distances This experiment compared ‘continuous’ and ‘instantaneous’ counts made at distances of 1 and 6 m. At 6 m, three quadrats could be observed for 30 min simultaneously, using binoculars, without difficulty or obviously disturbing the crabs: these quadrats were arranged in an arc as in the previous experiment. At 1 m, only one quadrat could be observed and binoculars were not used. Between replicates, the observer changed positions and allowed 30 min to elapse before beginning observations so that crabs once again emerged after being disturbed. During continuous counts, crabs were observed, identified, and counted as they emerged from their burrows. Those crabs that re-entered their burrows and emerged again later were only counted once. Instantaneous counts were based on the number of crabs visible on the surface at the end of the 30 min period. Each treatment was replicated four times and the entire experiment was repeated on three successive days. The same quadrats were observed under both methods, distances and on all three days. Sesarma counts were analysed with a 4-factor repeated-measures ANOVA with assemblage (fixed, three levels), day (repeated, fixed, three levels), distance (repeated, two levels) and method (repeated and fixed, two levels) as factors.
vation at a distance of 1 m), funnelled and unfunnelled pitfall trapping methods, and a photographic method. The observational method was conducted for 15 min rather than 30 min since the shorter time is a more practical period for observations while still allowing time for adequate recovery period (evident from the recovery experiment). Each treatment was replicated four times. The pitfall traps were made of plastic planting pots (185 cm wide · 17 cm deep) with a 1-mm mesh taped tightly around the bottom (to close the drainage holes). Funnels were made by cutting the ends off shorter planting pots (185 cm wide · 9 cm deep) and clipped to the trap using small ‘sprinkler’ clips inserted through small holes (see Figure 1). Three replicate pitfall traps were placed randomly in each assemblage, buried flush with the surface of the sediment and checked one and two days after placement (e.g. traps were deployed for a full 24 h, twice). Crabs were counted and removed each time the traps were checked. The fourth method tested was taking photographs of three replicate 0.25 · 0.25 m quadrats placed randomly in each assemblage using 400 speed ASA film in a 35 mm Pentax automatic camera. This camera was fitted with a zoom lens and attached to a two-legged camera stand, made out of steel rods with a PVC support beam, which held it 1 m above the sediment surface. The camera was fired manually (from 6 m away) using an FM signal to trigger the shutter (once) for each quadrat 30 min after the stand and camera were positioned to allow for crabs to recover from the disturbance. Crabs were counted and identified on the resulting photographs.
Experiment 3: Comparison of observational, photographic, and pitfall trap count methods This experiment compared four methods: the most effective observational method (continuous obser-
Figure 1. Configuration of pitfall traps.
5 Counts using all three methods were conducted within 1.5 h (some methods could be conducted simultaneously) for each assemblage, and one day of experimentation across all assemblages was conducted during a 5-h low tide period. The experiments were conducted over three days. Data were analysed with a 2-factor ANOVA with method (fixed, 3 levels), assemblage (fixed, 3 levels), and day (repeated, fixed, three levels) as factors.
Experiment 4: Comparison of N. meinerti burrow counts to trap captures This experiment compared counts of N. meinerti burrows to records from the pitfall traps. Burrows were counted in 0.5 · 0.5 m quadrats and each method was replicated three times in each assemblage. Data were analysed with a 2-factor ANOVA. The factors included method (fixed, two levels-including unfunnelled traps and burrow counts), and assemblage (fixed, three levels).
Experiment 5: Comparison of trap captures with excavation captures This experiment compared the numbers of crabs falling into pitfall traps with those captured from excavated quadrats in order to relate apparent abundance to absolute abundance. The excavated quadrats were 0.5 · 0.5 m. There were four pitfall traps in the tidal bank and tidal flat assemblages but all other treatments could only be replicated three times. Unfortunately N. meinerti burrows are usually deep and very difficult to excavate so results could not be obtained for this species. Data were analysed with a 2-factor ANOVA with method (fixed, 3 levels) and assemblage (fixed, 3 levels) as factors.
Results Experiment 1: Recovery times With the exception of one M. latifrons, all crabs observed in this experiment were Sesarma. The percentage of crabs that emerged peaked after 9 min in the hinterland and after 23 min in the
Figure 2. Mean cumulative percentage of Sesarma spp. emerging from burrows after disturbance over a 30 min observation period (mean ± 1 SE).
tidal flat and tidal creek assemblages (Figure 2). There were no significant differences in the percentage of crabs that emerged at 15 min among assemblages, days or their interaction (all p> 0.05). Based on these results, a recovery time of 15 min was used in other experiments. This was long enough for most crabs to emerge but still allowed time for a reasonable number of replicates during the 4 to 5-h window between high tides.
Experiment 2: Comparison of continuous and instantaneous counts A total of 255 Sesarma spp. and 15 C. merguiensis were observed. The latter occurred only in the tidal flat and tidal bank assemblages, and were only seen at 1 m (9 in continuous counts, 6 in instantaneous). All main effects and interactions, except those including day, were significant (Table 1). Of most importance here was the Assemblage · Distance · Method interaction (Figure 3). Overall, fewer crabs were recorded with instantaneous (mean = 1.17) than with continuous counts (mean = 2.38) but the difference between the methods decreased markedly with distance (Figure 3). Results were very similar in the tidal bank and tidal flat habitats, but the effects of counting method and distance were much smaller (and arguably trivial) in the hinterland where Sesarma was uncommon. Continuous and instantaneous counts were closely correlated (R = 0.90, N = 144, p < 0.001) and so were counts made at 1 and 6 m, although not as strongly (R = 0.61, N = 144, p < 0.001).
6 Table 1. Repeated-measures analysis of variance on observational methods of estimating abundance of Sesarma. Source
df
MS
Assemblage Residual Day Assemblage · Day Residual Method Assemblage · Method Residual Distance Assemblage · Distance Residual Day · Method Assemblage · Day · Method Residual Day · Distance Assemblage · Day · Distance Residual Method · Distance Assemblage · Method · Distance Residual Day · Method · Distance Assemblage · Day · Method · Distance Residual
2 9 2 4 18 1 2 9 1 2 9 2 4 18 2 4 18 1 2 9 2 4 18
78.19*** 3.11 0.9 1.02 2.83 52.56*** 8.4** 0.84 222.51*** 45.42*** 1.91 0.9 0.1 1.26 0.47 0.38 1.76 18.06*** 4.94** 0.41 0.77 0.65 0.67
The MS column gives the Mean Square for the source and its significance (*p < 0.05,**p < 0.01,***p < 0.001).
Experiment 3: Comparison of observational, photographic, and pitfall trap methods Of the 90 crabs observed, 82 were Sesarma. Sesarma was the only genus recorded by all methods. N. meinerti was only observed in the hinterland assemblage and only in pitfall traps
Figure 3. The mean number of Sesarma counted by continuous and instantaneous counts at 1 and 6 m in the hinterland (h’land), tidal flat and tidal bank assemblages (mean ± 1 SE).
(one in a funnelled trap and two in unfunnelled traps). A single I. paludicola was caught in the tidal bank in an unfunnelled trap and two C. merguiensis and two S. borniensis were caught in the tidal flat in funnelled traps. Finally, a single M. latifrons was observed in quadrats in the tidal bank. Sesarma counts depended upon both the assemblage and method used (Method · Assemblage interaction, F = 4.48; df = 6, 24; p < 0.01). More crabs were recorded from funnelled traps in the tidal flat assemblage (mean = 6.00) than in any other situation (all other means £2.70; Figure 4).
Experiment 4: Comparison of N. meinerti burrow counts to trap captures There were more N. meinerti burrows counted (mean = 0. 17) than crabs captured in either unfunnelled or funnelled pitfall traps (means £ 0.11). Crabs and burrows were only recorded from the hinterland, with a total of three burrows counted compared to two crabs caught in unfunnelled traps and one in a funnelled trap.
Experiment 5: Comparison of trap captures with excavation captures Overall, more crabs were caught by excavation (mean = 10.67 m 2) than in pitfall traps (mean = 1.36 per trap) but numbers varied among species and assemblages. As before, most of the crabs
Figure 4. The mean number of Sesarma counted by continuous counts (at 1 m for 15 min), funnelled traps, unfunnelled traps, and photography in the hinterland, tidal flat and tidal bank assemblages (mean ± 1 SE).
7 captured were Sesarma (21 excavated (EX), 10 trapped TR)) with the remainder being C. merguiensis (1 EX, 2 TR), S. borneensis (2 EX), Episesarma (1 TR), I. paludicolor (1 TR), and Sarmatium (1 TR). The numbers of Sesarma captured depended only upon the method used (Method, F = 13.68; df = 1,14; p < 0.01) and not on the assemblage (p for the Assemblage main effect, and the Method · Assemblage interaction > 0.10). More crabs were excavated (mean = 9.3 m 2) than were trapped (mean = 0.91 per trap). The proportion of female Sesarma did not differ among assemblages or between methods (all p > 0.25). Excavated Sesarma, however, had a smaller mean carapace width (mean = 0.69 cm, SE = 0.04) than those captured in traps (mean = 0.91 cm, SE = 0.08; Method, F = 5.29; df = 1,14; p < 0.05; p for the Assemblage main effect, and the Method · Assemblage interaction >0.50).
Discussion Experiment 1 showed that a recovery period of about 15–20 min was adequate for visual counts of species in the three assemblages compared. Nobbs and McGuinness (1999) found that over 90% of fiddler crabs they studied emerged in the first 10 min. These differing results suggest that grapsids may be more cautious than fiddler crabs, although the difference might also be due to temporal changes in behaviour as Nobbs and McGuinness (1999) study was done during the early dry season. Nonetheless, this does highlight the importance of testing methodologies on different groups of species. Visual counts of Sesarma and C. merguiensis were greatest when the crabs were observed continuously at 1 m, rather than instantaneously or at 6 m. The Sesarma seen at 1 m tended to be small adults or juveniles while those seen at 6 m were large adults (pers. obs.). These larger adults appeared to be aware of the observer at the closer distance and often appeared to choose to remain in the safety of their burrows. On the other hand, at 6 m distance, many of the small juveniles were overlooked because of their cryptic colour, and because they remained motionless for considerable periods, possibly to avoid being seen by predators. It is presumably for these reasons that there was
only a moderate correlation between the 1 and 6 m counts. In contrast, there was a good correlation between continuous and instantaneous counts, indicating that the latter method would give acceptable results, if time were limited, a conclusion also reached for Uca by Nobbs and McGuinness (1999). The most effective way to estimate apparent abundance of most grapsids in this study, of the several methods compared, was to use pitfall traps fitted with funnels. This method captured most species of crabs, and also the greatest number, which did not vary significantly in efficiency among assemblages (evident by comparing trap captures to excavation counts). The effectiveness of pitfall traps is likely to be due to the fact that they integrate day and night crab activity (because they sample throughout the 24 h). In the case of N. meinerti pitfall traps were the only method apart from burrow counts that can be used since this species is infrequently observed outside of burrows (pers. obs.) in this region (in contrast to a study in Zanzibar where visual counts were possible since this species was frequently active on the surface; see Skov et al. 2002). Pitfall traps also allow other information, such as sex and carapace width, to be more easily collected. Given its prominent role as a consumer in local forests (McGuinness 1994, 1997a, b, c), it is particularly important to have reliable estimates of N. meinerti abundance. Previous studies have largely relied on counts of burrows to estimate the abundance of this species (e.g. Micheli et al. 1991; McGuinness 1994, 1997a, b, c; Emmerson 2000). The results here seem to support this approach as N. meinerti were rarely captured in pitfall traps in comparison to the number of burrows evident nearby. Pitfall traps have the limitation of being dependent on crab surface activity and catchability (Skov and Hartnoll 2001). Estimates of apparent numbers of N. meinerti crabs appear to be particularly susceptible to this limitation. These crabs spend much of their active time maintaining their burrows, and do not appear to frequently forage far from their burrows (Micheli et al. 1991; Emmerson and McGwynne 1992, pers. obs.). Thus, it appears that N. meinerti may have a lower chance of falling into pitfall traps than do other grapsids, which may travel further from their burrows and spend longer periods foraging on the surface. Thus, pitfall traps may allow information
8 such as sex and carapace width of N. meinerti to be collected, but it appears that burrow counts are likely to provide more reliable estimates of apparent abundance. One potential problem with burrow counts is the possibility of inflated estimates by including abandoned burrows. Micheli et al. (1991), however, estimated N. meinerti burrow turnover rates to be only about three weeks, indicating that this problem may not be severe. Double entrances appeared to occur within a couple of centimetre of each other, and in almost all cases connected to the main burrow at a depth of less than 5 cm. Visually, double entrances were generally easily recognised, and counted as one. Conversely, underestimates could arise from multiple crabs inhabiting one burrow (see Emmerson 2000). Indeed, Skov et al. (2002) found that N. meinerti in their study were underestimated by 19%, which could be for this reason. Comparison of pitfall captures with excavations showed that traps underestimated true abundance of Sesarma in the tidal bank and tidal flat assemblages. A test of differences between apparent and absolute estimates of other species was not possible due to limited sample sizes. Nonetheless, the differences found for Sesarma indicate that there may be a possibility of similar differences to occur with other species. A possible way to increase the accuracy of pitfall trap sampling would be to increase the period in which the traps are deployed. An increase in trap size would likely increase numbers simply due to a larger area being sampled. In addition to the difference in numbers of crabs, there was also a bias towards capturing larger Sesarma. Smith et al. (1991) obtained similar results with S. messa and S. semperi when they deployed traps to decrease the crab abundance in experimental plots. During their study, there was a shift in the population size structure towards smaller sizes. Although there were no differences in the present study in the sex ratio between crabs captured and excavated, the sample size was limited and it would not be wise, on this basis, to assume that male and female crabs did not differ in activity or behaviour. In the case of fiddler crabs, male dominated populations have been frequently recorded (Johnson 2003). In Johnson (2003), experiments showed that fiddler crabs sampled with both pitfall traps and excavations yielded male dominated sex ratios, but females dominated
among juvenile crabs. Also, males tended to occur more on the surface (foraging) while females dominated in burrows. Overall, the results indicate that pitfall traps, equipped with funnels, are likely to provide better estimates of the apparent abundance of most of the grapsid crabs in this study than other nondestructive methods (with the exception of N. meinerti). This method may allow valuable information on the large grapsid, N. meinerti, to be collected, although the behaviour of this species means that population estimates may not be reliable.
Acknowledgements This study was supported by a Large ARC grant (to K.A. McGuinness). We thank other local mangrove researchers for support and assistance. J. Warren provided helpful advice on the design and use of pitfall traps. We offer particular thanks to P. Davie for his valuable assistance in the identification of Northern Territory grapsid crabs.
References Caughley G. 1971. Analysis of Vertebrate Populations. John Wiley and Sons, London. Dahdouh-Guebas F., Verneirt M., Tack J.F., Van Speybroeck D. and Koedam N. 1997. Food preferences in Neosarmatium meinerti de Man (Decapoda: Sesarminae) and its possible effect on the regeneration of mangroves. Hydrobiologia 347: 83–89. Emmerson W.D. 2000. Aspects of the population dynamics of Neosarmatium meinerti at Mgazana, a warm temperate mangrove swamp in the East Cape, South Africa, investigated using an indirect method. Hydrobiologia 449: 221–229. Emmerson W.D. and McGwynne L.E. 1992. 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. 157: 41–53. Frusher S.D., Giddins R.L. and Smith T.J.III. 1994. Distribution and abundance of grapsid crabs (Grapsidae) in a mangrove estuary: effects of sediment characteristics, salinity tolerances, and osmoregulatory ability. Estuaries 17(3): 647–654. Golley F., Odum H.T. and Wilson R.F. 1962. The structure and metabolism of a Puerto Rican red mangrove forest in May. Ecology 43: 9–19. Johnson P. 2003. Biased sex ratios in fiddler crabs (Brachyura, Ocypodidae): a review and evaluation of the influence of
9 sampling method, size class, and sex-specific mortality. Crustaceana 76: 559–580. Jones D.A. 1984. Crabs of the mangal ecosystem. In: Por F.D. and Dor I. (eds), Hydrobiology of the Mangal. Dr. W. Junk Publisher, The Hague, Netherlands. Jordao J. and Oliveira R. 2003. Comparison of non-invasive methods for quantifying population density of the fiddler crab Uca tangeri. J. Mar. Biol. Assoc. UK 83(5): 981–982. Lee S.Y. 1998. Ecological role of grapsid crabs in mangrove ecosystems: a review. Mar. Freshwater Res. 49: 335–343. McGuinness K.A. 1994. The climbing behaviour of Cerithidea anticipata (Mollusca: Gastropoda): the role of physical versus biological factors. Aust. J. Ecol. 19: 283–289. McGuinness K.A. 1997a. Dispersal, establishment and survival of Ceriops tagal propagules in a north Australian mangrove forest. Oecologia 109: 80–87. McGuinness K.A. 1997b. Tests for artefacts in some method used to study herbivory and predation in mangrove forests. Mar. Ecol. Prog. Ser. 153: 37–44. McGuinness K.A. 1997c. Seed predation in a north Australian mangrove forest: a test of the dominance–predation model. J. Trop. Ecol. 13: 293–302. Micheli F., Gherardi F. and Vannini M. 1991. Feeding and burrowing ecology of two East African mangrove crabs. Mar. Biol. 111: 247–254. Nobbs M. 1999. The behavioural ecology of Fiddler crabs (Genus: Uca) that live in the mangrove forests of Darwin Harbour. Ph.D. Thesis, Northern Territory University, Australia. Nobbs M. and McGuinness K.A. 1999. Developing methods for quantifying the apparent abundance of fiddler crabs
(Ocypodidae: Uca in mangrove habitats. Aust. J. Ecol. 24: 43–49. Roberston A.I. 1986. Leaf-burying crabs: their influence on energy flow and export from mixed mangrove forests (Rhizophora spp. in northeastern Australia. J. Exp. Mar. Biol. Ecol. 102: 237–248. Salgado Kent C.P. 2004. The significance of plant–animal interactions: how crabs affect structure and function. Ph.D. Thesis, Charles Darwin University, Australia. Skov M.W. and Hartnoll R.H. 2001. Comparative suitability of binocular observation, burrow counting and excavation for the quantification of the mangrove fiddler crab Uca annulipes (H. Milne Edwards). Hydrobiologia 449: 201–212. Skov M., Vannini M., Shunula P.J., Hartnoll R.G. and Cannicci S. 2002. Quantifying the density of mangrove crabs: Ocypodidae and Grapsidae. Mar. Biol. 141(4): 725–732. Smith T.J.III. 1987. Seed predation in relation to tree dominance in distribution in mangrove forests. Ecology 68: 266–273. Smith T.J.III, Boto K.G., Frusher S.D. and Giddins R.L. 1991. Keystone species and mangrove forest dynamics: the influence of burrowing by crabs on soil nutrient status and forest productivity. Estuar. Coast. Shelf Sci. 33: 419–432. Southwood T.R.E. and Henderson P.A. 2000. Ecological Methods. Blackwell Science Ltd. Warren J.H. 1987. Behavioural ecology of crabs in temperate mangrove swamps. Ph.D. Thesis, University of Sydney, Australia. Warren J.H. 1990. The use of open burrows to estimate abundances of intertidal estuarine crabs. Aust. J. Ecol. 15: 277–280.
