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Burrowing, root mat density, and the distribution of fiddler crabs in the eastern United States
J. exp. mar. Biol. Ecol., 1979, Vol. 36. pp. 11-21
0 Elsevier/North-Holland
BURROWING,
Biomedical Press
ROOT MAT DENSITY, AND THE DISTRIBUTION
FIDDLER
OF
CRABS IN THE EASTERN UNITED STATES
PAUL RINGOLD Department
qf'Earth and Planetary Sciences, The Johns Hopkins University, Baltimore, Maryland, U.S.A.
Abstract: This paper discusses the distribution
of two species of fiddler crabs across an estuary. The possibility that sediment size, physical factors (or micro-climate), or food limitation could lead to the observed distributions is discussed, and evidence is presented to show that these factors probably play a minor role in controlling the distribution of Uca pugnax (Smith) and Ii. minax (Le Conte) across an estuary. The results show that the best correlate of the dominant species of Uca in a particular habitat is the density of the root mat of that area. A series of experiments showed that variations in the abundance of large U.pugnax at two tide levels in a marsh very closely parallel the ability of II. pugnax to burrow in substrata taken from those same two areas of the marsh. These two areas have significant differences in density of the root mat.
INTRODUCTION
Fiddler crabs are burrowing deposit-feeders. They feed throughout broad areas of their habitat during low tides, and most of the individuals return to burrows at high tide. These burrows may serve as a refuge from physical factors (Powers & Cole, 1976) and potential predators (Crane, 1975, see p. 511). They may also serve as a place to mate (Crane, 1975, see p. 502). Three species of Uca live on the American coast between northern Florida and Massachusetts: U. pugnax (Smith, 1870) U. minax (Le Conte, 1855) and U.pugilator (Bose, 1802). Two of these, U. pugnax and U. minax, generally live in salt marshes. Root mat density varies systematically throughout a salt marsh (Gallagher, 1974; Table III). If species of Uca differ in their ability to burrow through root mats of differing densities, then changes in root mat density could very well affect the abundance and species composition of fiddler crab populations. Other burrowing animals (e.g., some small mammals, some birds, and many marine deposit- and suspension-feeders) may have patterns of distribution and abundance which are controlled by their ability to burrow in various parts of their habitats. This paper examines hypotheses concerning the distribution of U. minax and U. pugnax across an estuary. Previous hypotheses have included micro-climate, sediment size, and food. These hypotheses are reviewed. A new hypothesis is examined, this being that the species differ in their ability to burrow on different substrata. This implies that these differences control access to burrows, and so control the distribution and abundance of fiddler crabs. 11
12
PAUL RINGOLD LOCATION
Bell Creek marsh in North Carolina (37’47’N; 76”41’W) is the area studied and the salinity is typically 20x,. The site is x 60 m from creek bank to forest and Spartina alterniflora (Loisel) predominates in this region. A 5 m strand of Juncus roemarianus (Scheele) grows between the highest edge of the Spartina alternzflora and the forest. Two transects were established parallel to the creek, one w 10 m shoreward of the creek bank, and the other ~25 m further shoreward in the marsh. These transects will be referred to as the low and high transects, respectively, although the actual height difference is only a few centimeters. METHODS Methods had to be devised to measure the quantity of material that could interfere with the ability of the crabs to burrow. Because the area and depth scales that might reflect burrowing difficulty were unknown, root mat density was measured on two scales. ‘Root mat’ includes not only roots, but also rhizomes and some detrital material. The large samples were x 17 cm wide, 17 cm long and 20 cm deep. The samples were excavated, weighed fresh, and sieved on 6.35 mm mesh (0.25 in). The portion retained on the sieve was dried at 70°C and weighed. Because the samples were of somewhat different sizes, all results are standardized as sieved dry weight divided by fresh weight. Sediment cores (2.54 cm in diameter, and x3.0 cm deep) were collected. These small samples were sieved on 0.5 mm mesh, rinsed in distilled water, dried at 70°C and weighed. DETERMINATIONOF FIDDLER CRABDENSITY Wooden or steel enclosures 0.5 m’ and 25 cm high were placed in the marsh, their lower edges flush with the marsh surface. The frames were placed within 3 m of the high or low transects during high tides in the summers of 1976 and 1977. At low tide all the animals 2 1 cm carapace width were removed. This was done by repeated visits to each frame. When no more animals ( 2 1 cm carapace width) were visible on the surface (and after a minimum of five visits to each frame), the area within the enclosure was dug up, and examined for more fiddler crabs; usually few were found. Any frame which would have allowed escape or entry of crabs was not used. The crabs were identified, measured (carapace width), and weighed. BURROWINGEXPERIMENTS Four 0.12 m* samples of substrata from the high transect and two 0.12 m2 samples from the low transect were brought intact to the Duke University Marine Laboratory.
FIDDLER
CRAB
13
DISTRIBUTION
The sides and bottom of each sample were covered with plastic tacked to a wooden frame in order to restrict crabs to the surface of the substratum sample. These ‘substrata’ were kept moist in running sea water and exposed to natural light. No attempt was made to simulate tidal cycles. Ten male and five female U. pugnax, or live male and two female U. minax were the groups of animals placed on the substrata. The lower density for U. minax reflects its lower field density and its larger size (see Table II). The experimental densities for both species are about ten times the natural density found on the high transect. In addition, in order to determine the effect of size on burrowing ability, each species was divided into two size groups based on the median sizes in the 1976 collections (see Table I). All the crabs used in this experiment were taken from the field one to two days before the start of a given experiment. The crabs were sorted into groups as described above and in Table I. The groups were assigned to the substrata in stratified random fashion. I determined the number of combinations of a particular experiment but the specific combination of crab group, and substratum was determined at random. The set of variables examined in this manner were root mat density, species, and size. TABLE I Description of crab groups for burrowing experiments: the dividing line between large and small crabs is the median size of the 1976 data; sizes are in cm carapace width; average size (in parentheses) refers to the overall average size of all males or females used in a given crab group.
No. males used (average size, cm) No. females used (average size, cm) Maximum size, cm Minimum size, cm
Uca pugnux small
Uca pugna.x
Uca minax
large
large
10 (1.16) 5 (1.16) 1.25
10 (1.54) 5 (1.49)
5 (2.39) 2 (2.29)
1.25
1.95
1.oo
Initially, each substratum was examined once every hour. Eventually, it was found that a sufficient record could be obtained by observations made once each day. At each observation the total number of burrows, and the position of each burrow was noted. The experiments ran for one week. The crabs were then removed from the substrata, the burrows tilled in, and the next group of crabs were added. PERCENTAGE
CARBON
AND
NITROGEN
Cores 15 mm in diameter and to a maximum depth of 50 mm were taken from open areas of the sediment along both the high and low transects in early September 1976. These cores were dried at 70 C and stored. The sediments were then ground with a mortar and pestle, and ignited in a Model 240 Perkin Elmer Elemental Analyser.
PAUL RINGOLD RESULTS DISTRIBUTIONOF UCA Quantitative sampling results are given in Table II. U. pugnax is found at high density along the low transect, and at lower density along the high transect. The ratio of U. pug~s found low to high is 3.61 (or N, JN,,, = 3.61” see Table VIIB). U. m&ax was foundquantitativelyonly along the high transect, but was observed infrequently, and not quantitatively collected in the low areas of the marsh.
TABLE
I1
Fiddler crab densities from high and low transects: from the 1976 and 1977 0.5 mz samples; data describe only the population characteristics for that of the population; I cm carapace width; the biomass data are g/m*; the median size is carapace width (cm). Transect High
Low
ff. pugnm
U. ~inff~
No./m’ Mean k SD. No. of samples
11.6 f7.2 31
6.0 f 3.5 31
41.7 + 14.5 21
0.0 21
Biomass Mean & S,D. No. of samples
10.63 f 5.53 26
26.59 + 14.78, 30
34.12 f 10.75 19
0.0 21
Median size, cm
1.29
2.15
1.26
-
U. pugnax
ci.
pninax
ROOT MAT
The root mat density data are given in Table III. Both large and small samples show that the high area contains about 30% more material than the low area. These results are comparable with those of Gallagher (1974). The large samples show that the difference between the substrata is significant. The difference between the small samples is not significant. The means of the small samples are relatively as far apart as those of the large samples, however, the coefficient of variation for the small samples is almost three times as high as that of the large samples. This increase in variance probably reflects a fundamental difference in the spatial distribution of root mat material on the two size scales.
15
FIDDLER CRAB DISTRIBUTION TABLEIII
Root mat density: data for the large samples refer to the sieved dry weight divided by the fresh weight of a sample ~0.03 m* and 20 cm deep; data for the small sample refer to the sieved weight in g of a core 2.54 cm in diameter, and s 3.0 cm deep; *, the means of the high and low samples are significantly different (P = 0.95) when tested with a Mann-Whitney U-test. Transect High
Low
High/Low
Large samples Mean + S.D. Coef. of var. No. of samples
0.046 + 0.0045 9.78 7
0.034 * 0.0074 21.76 6
1.35*
Small samples Mean k S.D. Coef. of var. No. of samples
0.255 + 0.105 41.18 18
0.194 f 0.090 46.39 18
1.31
BURROWING
ABILITY
The data in Table IV refer to the total number of burrows dug over a one week period by all the animals on a given substratum. There is a significant effect of root TABLEIV Comparative burrowing ability: total number of burrows dug during each experiment (one week); *, number of burrows dug on high substrata is significantly different (P > 0.95) than the number of burrows dug on low substrata for that crab group when compared by a Mann-Whitney U-test; crab groups are described in Table I. Root mat density High
Low
Small U. pugnax* Mean k S.D No. of expt
1.50 f 1.00 4
4.75 k 0.96 4
Large U. pugnax* Mean f S.D. No. of expt
0.83 * 1.17 6
3.00 + 1.00 3
Large U. minax Mean + S.D. No. of expt
1.43 f 1.40 7
I .67 + 0.58 3
mat density in the numbers of burrows dug by both large and small U. pugnux. The ratio of the number of burrows dug on high to low substrata is nearly the same for both large and small U. pugnux (or B,,,,/B,,,, N B,qsp/B,,sp# 1). There was no root mat effect on the number of burrows dug by U. minux (or B,,,,/B,,,, z 1). There is
16
PAUL RINGOLD
no trend in the data to indicate that it became easier to burrow on the substrata as the later experiments were conducted. PERCENTAGE
CARBON AND NITROGEN
The data in Table V are the percentage of the dry weight of the sample which was detected as either C or N. The high transect has x.507: more carbon and nitrogen TABLE
V
Distribution of carbon, nitrogen, and Uticabiomass: ‘5”carbon and ‘:, nitrogen in samples of surface sediment from the high and low areas of Bell Creek. N.C.; Uuz biomass is the total weight of both species of Uca in g/m’; high/low refers to the ratio of the means in each case; the probability that the high and low means of the carbon and nitrogen data are the same. when tested with a r-test, is given: there are no significant differences in Uccr biomass as a function of tidal height for either 1976. 1977. or 1976 and 1977 combined when tested with a r-test. Transect Low
High % carbon Mean & S.D. No. of samples Tj,nitrogen Mean & S.D. No. of samples Uen biomass, g/m2
High/Low
7.30 * 0.70 63
1.54 (P < O.OOI]
0.87 + 0.07 17
0.59 t_ 0.04 61
1.47 (P < 0.001)
37.22
34.12
1.09 (ns.)
than the low transect. If this be an indication of food availability for fiddler crabs, which are deposit-feeders (Newell, 1964; Adams & Angelovic, 1970; Tenore, 1977) then the high transect contains about 50% more food than the low transect.
DISCUSSION
The data show a strong parallel between the burrowing ability of Ii. pugnux and its abundance on natural substrata. I suggest, therefore, that burrowing. as modified by the root mat, controls the distribution and abundance of U. pugtzax on root mats of intermediate to high density. U. m&ax shows no evidence to date of the root mat affecting its burrowing ability and so I suggest that its distribution is controlled by other factors which may in turn be correlated-with root mat density. If root mat density (or its correlates) controls the distribution and abundance of Uca, then species distribution or abundance may reflect variations in root mat density. If this hypothesis be true, then a relationship between Uca species and root mat density should be observed in the existing data. In Table VI I have compiled information on root mat ranks, numerically dominant species of Uca, sand
17
FIDDLER CRAB DISTRIBUTION
content, tidal height, and distance from the creek bank for a variety of salt marsh habitats. All the data except for the root mat ranks are from Teal (1958); the root mat ranks follow the observations of Gallagher (1974) and Table III. Within areas of Spartina alterr@ora there are generally greater root mat densities higher in the marsh, and lower densities near the creek bank. Bare creek banks are assigned the lowest rank for root mat density. The remaining problem is how to rank the Distichlis-Salicornia area. Within one plant type and, therefore, one root mat type, the weight of material retained on a specific mesh sieve is probably a good index of burrowing difficulty. The Distichlis-Salicomia root mat is, however, very different from the Spartina root mat, and its rank based on weight of material retained on a sieve may not reflect the true difficulty that animals have in burrowing on this substratum when compared with the Spartina substratum. With this reservation, and the knowledge that medium Spa$ti~a, the next most dense root mat, has almost twice as much material as Distichlis-Sffli&orni~, the root mats are ranked based largely on Gallagher (1974) whose data, like Teal’s, come from Georgia salt marshes on or near Sapelo Island. TAELE
VI
Description of marsh habitats and the distribution of Ucn: the root mat data are modified from Gallagher (1974); rest of data from Teal (1958); all areas containing Ucu are given; in tidal height, lowest area is ranked 1; in root’mat density, least dense root mat is ranked 1.
Area Creek Bank Salicornia-Distichlis marsh Medium Spartina, low marsh Short Spartina, low marsh S~ort,S~artinu, high marsh ~j~a~ marsh
Rank of distance from creek bank
Tidal height. rank
Sand, 0, ,D
1 6 3.5 2 3.5 5
lo-70 8&95 O-10 O-10 4%70 30
Root mat density, rank
Numerically dominant UCG
V. pugilator U. pugilator V. pugnax U. pugnax U. pugnax U. n&ax
Table VI shows that the prediction that species reflect root mat density is upheld. The areas with the lowest root mat densities have Uca pugilator dominant, the intermediate areas have U. pugnax dominant, and the highest density root mat habitat has U. minax dominant. Two of the habitats have a second species - U. pugnax is found with U. pugilator in the Salicornia-Distichlis Marsh, and with Uca minax in the Minax Marsh. No other habitats have a second species. This pattern of distribution supports the view that root mat density is important to the distribution of Uca. Different factors have been shown to regulate populations of a single species through ontogeny (e.g., Hutchinson, 19.59). The importance of burrows in controlling Uca density may vary with the age of the crab. At Bell Creek, early crab stages
PAUL RINGOLD
18
of Ucu are found just inside the lip of burrows dug by larger individuals, or in the flocculent surface layer (pers. obs.; Crane, 1975, see p. 510). They are not necessarily living in burrows that they have dug, and it is, therefore, unlikely that they are regulated by factors related to burrowing or burrowing ability. Larger crabs use and defend burrows for a variety of purposes, and it is more likely that their abundance is controlled by factors that are related to their burrows. One might, therefore, predict that the parallel between burrowing ability and field abundances should be strongest for the largest animals, and weaker for the smaller animals. An examination of the data from the 1976 and 1977 collections shows that this is true. Table VIIB TABLE
VII
A, numbers of burrows dug and numbers of individuals found on substrata. B, ratios of burrows dug and numbers of individuals found on low to high substrata. Bij, number of burrows dug on the ith substratum by the jth crab group; Niti, number of individuals found on the ith substratum of the jth crab group; j or g = Ip for large U. pugnax (1.25 cm carapace width), = sp for small U. pugnax (1.0&l .25 cm), =p for U. pugnux ( < 1.00 cm), and =Im for large CJ. minax ( > 1.95 cm), = sm for small U. minax (1.00-1.95 cm), =m for CJ.minax (< 1.00 cm); i or k = h for high substrata (i.e., high root mat density from the high transect), =I for low substrata (i.e., low root mat density from the low transect). A
Substratum (i)
Crab group 0’)
h h h
1P sP P 1P sP
I I 1 h h h
No. of burrows dug
B,,, 0.83 1.50
5.3 6.3 11.6 21.3 20.4 41.7 4.0 2.0 6.0 0.0 0.0 0.0
3.00 4.75 1.43
1: sm m Im sm m
1 1 1
Density of crab group N!.,
_ 1.67 _
B
Substratum (i)
1 1
1
Crab group 0’)
sP IP Im
Substratum (k)
h h h
Crab group (g)
sP IP Im
Ratio of burrows dug on low to high substrata B,,,IBk,n
3.17 3.60 1.17
Ratio of no. of individuals found on low to high substrata
Nil/INk,g 1976
1977
1.76 3.09 0.00
7.10 3.29 0.00
FIDDLER
CRAB DISTRIBUTION
19
gives the ratios of low to high abundance of U. pugnax by year and size. The ratio for the large individuals is remarkably constant and similar to the ratio observed in the burrowing experiments. The ratio for the small individuals is variable from one year to the next, and is not similar to that observed in the burrowing experiments. This is not to say that burrowing ability is not important to the small adults (1.61.25 cm carapace width). It is likely that they have recently entered the stage in their life history where burrows are becoming more important, but their distribution is not yet at equilibrium with factors related to burrowing ability. Other factors have been suggested as controlling Uca distribution in the northwestern Atlantic and elsewhere; sediment, food, and micro-climate will be discussed here. The effects of sediment size on fiddler crab distribution have been discussed by Miller (1961) for U. pugilator, U. minax, and U. pugnax. He found that the mouth parts of Uca could be correlated with the sediment type on which he thought the crabs were typically found; he thought U. minax was adapted for feeding on the finest sediments, U. pugilator for feeding on the coarsest (sand) sediments, and that U. pugnax shows an intermediate adaptation. The percentage of sand along with the species observed to be dominant for a variety of habitats are given in Table VI. There are several violations of the expected relationship between sediment and the expected species. In the short Spartina high marsh, which ranks high in sand content, U. pugnax is found and U. pugilator, the species expected on the basis of mouthpart adaptations, is not found at all. In the two habitats with the lowest sand content, the medium Spartina low marsh, and the short Spartina low marsh, U. pugnax is dominant and U. minax, the expected species, is not found. Sediment size probably acts in a somewhat different way than does root mat density. U. minax is not observed on very sandy substrata probably because of mouthpart adaptations. U. pugilator is not found on very muddy sediments again probably because of mouthpart adaptations. Such adaptations may, therefore, only prevent a species from occupying extremes of sediment type, but play little role in regulating distribution within those sediment extremes. The possibility that the observed distributions are related to food should also be considered. Since availability of food varies with position in the marsh, then different areas of the marsh would be expected to support different biomasses of fiddler crabs. While C, N, and ATP are all more abundant in high marsh sediments (Table V; Christian, Bancroft & Wiebe, 1975) the biomass of fiddler crabs does not reflect the magnitude of this change. If food were responsible for the observed distributions. then U. minax caged in the low marsh. where it is not typically found, would not be expected to survive. Teal (1958) shows that it survives as well or better than U. pugnax in the lower areas of the marsh. This also demonstrates that U. minax is not excluded from the low parts of the marsh by micro-climate. In addition, if food limitations were important, marked effects due to starvation would be expected. Barnwell (1966, pers. comm.) starved U. pugnax and U. minax for up to seven weeks in connection
20
PAULRINGOLD
with studies on endogenous rhythms. Activity decreases rapidly at first, and then less so. U. minux tended to survive longer than U. pugnax in these experiments. This may be due to greater food reserves in U. minax or a greater capacity to tolerate the experimental conditions and again suggests that U. minax is not restricted to the higher parts of the marsh by natural conditions of food and micro-climate. None of these three results is a critical test of the hypothesis that food controls Uca distribution, but together they suggest that it is unlikely. This paper is a step towards explaining the distribution of U. pugnax, U. minax, and U. pugilator. Information on the distribution of U. pugnax on intermediate to dense root mats has been obtained. The question of the maintenance of the borders between U. pugnax and its two sympatric congeners remains. It is likely that the interaction between U. minax and U. pugnax is based on some form of interference competition (Case & Gilpin, 1974).
ACKNOWLEDGEMENTS
I gratefully acknowledge the assistance of the many people who have helped in all stages of this work. Bill Seiple and Terry West helped with much of the field work, Dr J. D. Costlow and members of the staff and students of the Duke University Marine Laboratory provided facilities and hospitality during the course of the work at Beaufort. Dr J. Taft allowed me to use a CHN analyser, and special thanks must go to my advisor, Dr S. A. Woodin. Parts of this work were supported by a Culpepper Foundation Fellowship, by NSF grant GA-4261 1, and NSF grant OCE76-01666 A01 ; both NSF grants were awarded to Dr Woodin.
REFERENCES ADAMS, S. M. & J. W. ANGELOVIC,1970. Assimilation of detritus and its associated bacteria by three species of estuarine animals. Chesapeake Sci., Vol. 11, pp. 249-254. BARNWELL,F. H., 1966. Daily and tidal patterns of activity in individual fiddler crabs (genus Uca) from the Woods Hole region. Biol. Bull. mar. biol. Lab., Woods Hole, Vol. 130, pp. I-17. CASE,T. J. & M. E. GILPIN, 1974. Interference competition and niche theory. Proc. mtn. Acad. Sci. U.S.A., Vol. 71, pp. 3073-3077. CHRISTIAN,R. R., K. BANCROFT. & W. J. WIEBE, 1975. Distribution of microbial adenosine triphosphate in salt marsh sediments at Sapelo Island, Georgia. Soil Sci., Vol. 119, pp. 89-97. CRANE, J., 1975. Fiddler crabs of’ the world (Ocypodidae: genus Uca). Princeton University Press. Princeton, N.J., 736 pp. GALLAGHER.J. L., 1974. Sampling macroorganic profiles in salt marsh plant root zones. Proc. Soil Sci. Sot. Am., Vol. 38, pp. 154-155. HUTCHINSON,G. E., 1959. Homage to Santa Rosalia, or why are there so many kinds of animals? Am. Nat., Vol. 93, pp. 323-349. MILLER, D. C., 1961. The feeding mechanisms of fiddler crabs with ecological feeding considerations of feeding adaptations. Zoologica, N. Y., Vol. 46, pp. 89-100. NEWELL,R., 1964. The rBle of detritus in the nutrition of two marine deposit feeders, the prosobranch, Hydrobio ulvae, and the bivalve, Macoma bnlthica. Proc. zool. Sot.. Land., Vol. 144, pp. 25-45.
FIDDLER CRAB DISTRIBUTION
21
POWERS,L. W. & J. F. COLE, 1976. Temperature variation in fiddler crab microhabitats. J. rxp. mar. Biol. Ecol., Vol. 21, pp. 141-157. TEAL,J. M., 1958. Distribution of fiddler crabs in Georgia salt marshes. Ecology, Vol. 39, pp. 185-193. TENORE, K. R., 1977. Utilization of aged detritus derived from different sources by the polychaete Cupitella capitata. Mar. Biol., Vol. 44, pp. 51-56.
0 Elsevier/North-Holland
BURROWING,
Biomedical Press
ROOT MAT DENSITY, AND THE DISTRIBUTION
FIDDLER
OF
CRABS IN THE EASTERN UNITED STATES
PAUL RINGOLD Department
qf'Earth and Planetary Sciences, The Johns Hopkins University, Baltimore, Maryland, U.S.A.
Abstract: This paper discusses the distribution
of two species of fiddler crabs across an estuary. The possibility that sediment size, physical factors (or micro-climate), or food limitation could lead to the observed distributions is discussed, and evidence is presented to show that these factors probably play a minor role in controlling the distribution of Uca pugnax (Smith) and Ii. minax (Le Conte) across an estuary. The results show that the best correlate of the dominant species of Uca in a particular habitat is the density of the root mat of that area. A series of experiments showed that variations in the abundance of large U.pugnax at two tide levels in a marsh very closely parallel the ability of II. pugnax to burrow in substrata taken from those same two areas of the marsh. These two areas have significant differences in density of the root mat.
INTRODUCTION
Fiddler crabs are burrowing deposit-feeders. They feed throughout broad areas of their habitat during low tides, and most of the individuals return to burrows at high tide. These burrows may serve as a refuge from physical factors (Powers & Cole, 1976) and potential predators (Crane, 1975, see p. 511). They may also serve as a place to mate (Crane, 1975, see p. 502). Three species of Uca live on the American coast between northern Florida and Massachusetts: U. pugnax (Smith, 1870) U. minax (Le Conte, 1855) and U.pugilator (Bose, 1802). Two of these, U. pugnax and U. minax, generally live in salt marshes. Root mat density varies systematically throughout a salt marsh (Gallagher, 1974; Table III). If species of Uca differ in their ability to burrow through root mats of differing densities, then changes in root mat density could very well affect the abundance and species composition of fiddler crab populations. Other burrowing animals (e.g., some small mammals, some birds, and many marine deposit- and suspension-feeders) may have patterns of distribution and abundance which are controlled by their ability to burrow in various parts of their habitats. This paper examines hypotheses concerning the distribution of U. minax and U. pugnax across an estuary. Previous hypotheses have included micro-climate, sediment size, and food. These hypotheses are reviewed. A new hypothesis is examined, this being that the species differ in their ability to burrow on different substrata. This implies that these differences control access to burrows, and so control the distribution and abundance of fiddler crabs. 11
12
PAUL RINGOLD LOCATION
Bell Creek marsh in North Carolina (37’47’N; 76”41’W) is the area studied and the salinity is typically 20x,. The site is x 60 m from creek bank to forest and Spartina alterniflora (Loisel) predominates in this region. A 5 m strand of Juncus roemarianus (Scheele) grows between the highest edge of the Spartina alternzflora and the forest. Two transects were established parallel to the creek, one w 10 m shoreward of the creek bank, and the other ~25 m further shoreward in the marsh. These transects will be referred to as the low and high transects, respectively, although the actual height difference is only a few centimeters. METHODS Methods had to be devised to measure the quantity of material that could interfere with the ability of the crabs to burrow. Because the area and depth scales that might reflect burrowing difficulty were unknown, root mat density was measured on two scales. ‘Root mat’ includes not only roots, but also rhizomes and some detrital material. The large samples were x 17 cm wide, 17 cm long and 20 cm deep. The samples were excavated, weighed fresh, and sieved on 6.35 mm mesh (0.25 in). The portion retained on the sieve was dried at 70°C and weighed. Because the samples were of somewhat different sizes, all results are standardized as sieved dry weight divided by fresh weight. Sediment cores (2.54 cm in diameter, and x3.0 cm deep) were collected. These small samples were sieved on 0.5 mm mesh, rinsed in distilled water, dried at 70°C and weighed. DETERMINATIONOF FIDDLER CRABDENSITY Wooden or steel enclosures 0.5 m’ and 25 cm high were placed in the marsh, their lower edges flush with the marsh surface. The frames were placed within 3 m of the high or low transects during high tides in the summers of 1976 and 1977. At low tide all the animals 2 1 cm carapace width were removed. This was done by repeated visits to each frame. When no more animals ( 2 1 cm carapace width) were visible on the surface (and after a minimum of five visits to each frame), the area within the enclosure was dug up, and examined for more fiddler crabs; usually few were found. Any frame which would have allowed escape or entry of crabs was not used. The crabs were identified, measured (carapace width), and weighed. BURROWINGEXPERIMENTS Four 0.12 m* samples of substrata from the high transect and two 0.12 m2 samples from the low transect were brought intact to the Duke University Marine Laboratory.
FIDDLER
CRAB
13
DISTRIBUTION
The sides and bottom of each sample were covered with plastic tacked to a wooden frame in order to restrict crabs to the surface of the substratum sample. These ‘substrata’ were kept moist in running sea water and exposed to natural light. No attempt was made to simulate tidal cycles. Ten male and five female U. pugnax, or live male and two female U. minax were the groups of animals placed on the substrata. The lower density for U. minax reflects its lower field density and its larger size (see Table II). The experimental densities for both species are about ten times the natural density found on the high transect. In addition, in order to determine the effect of size on burrowing ability, each species was divided into two size groups based on the median sizes in the 1976 collections (see Table I). All the crabs used in this experiment were taken from the field one to two days before the start of a given experiment. The crabs were sorted into groups as described above and in Table I. The groups were assigned to the substrata in stratified random fashion. I determined the number of combinations of a particular experiment but the specific combination of crab group, and substratum was determined at random. The set of variables examined in this manner were root mat density, species, and size. TABLE I Description of crab groups for burrowing experiments: the dividing line between large and small crabs is the median size of the 1976 data; sizes are in cm carapace width; average size (in parentheses) refers to the overall average size of all males or females used in a given crab group.
No. males used (average size, cm) No. females used (average size, cm) Maximum size, cm Minimum size, cm
Uca pugnux small
Uca pugna.x
Uca minax
large
large
10 (1.16) 5 (1.16) 1.25
10 (1.54) 5 (1.49)
5 (2.39) 2 (2.29)
1.25
1.95
1.oo
Initially, each substratum was examined once every hour. Eventually, it was found that a sufficient record could be obtained by observations made once each day. At each observation the total number of burrows, and the position of each burrow was noted. The experiments ran for one week. The crabs were then removed from the substrata, the burrows tilled in, and the next group of crabs were added. PERCENTAGE
CARBON
AND
NITROGEN
Cores 15 mm in diameter and to a maximum depth of 50 mm were taken from open areas of the sediment along both the high and low transects in early September 1976. These cores were dried at 70 C and stored. The sediments were then ground with a mortar and pestle, and ignited in a Model 240 Perkin Elmer Elemental Analyser.
PAUL RINGOLD RESULTS DISTRIBUTIONOF UCA Quantitative sampling results are given in Table II. U. pugnax is found at high density along the low transect, and at lower density along the high transect. The ratio of U. pug~s found low to high is 3.61 (or N, JN,,, = 3.61” see Table VIIB). U. m&ax was foundquantitativelyonly along the high transect, but was observed infrequently, and not quantitatively collected in the low areas of the marsh.
TABLE
I1
Fiddler crab densities from high and low transects: from the 1976 and 1977 0.5 mz samples; data describe only the population characteristics for that of the population; I cm carapace width; the biomass data are g/m*; the median size is carapace width (cm). Transect High
Low
ff. pugnm
U. ~inff~
No./m’ Mean k SD. No. of samples
11.6 f7.2 31
6.0 f 3.5 31
41.7 + 14.5 21
0.0 21
Biomass Mean & S,D. No. of samples
10.63 f 5.53 26
26.59 + 14.78, 30
34.12 f 10.75 19
0.0 21
Median size, cm
1.29
2.15
1.26
-
U. pugnax
ci.
pninax
ROOT MAT
The root mat density data are given in Table III. Both large and small samples show that the high area contains about 30% more material than the low area. These results are comparable with those of Gallagher (1974). The large samples show that the difference between the substrata is significant. The difference between the small samples is not significant. The means of the small samples are relatively as far apart as those of the large samples, however, the coefficient of variation for the small samples is almost three times as high as that of the large samples. This increase in variance probably reflects a fundamental difference in the spatial distribution of root mat material on the two size scales.
15
FIDDLER CRAB DISTRIBUTION TABLEIII
Root mat density: data for the large samples refer to the sieved dry weight divided by the fresh weight of a sample ~0.03 m* and 20 cm deep; data for the small sample refer to the sieved weight in g of a core 2.54 cm in diameter, and s 3.0 cm deep; *, the means of the high and low samples are significantly different (P = 0.95) when tested with a Mann-Whitney U-test. Transect High
Low
High/Low
Large samples Mean + S.D. Coef. of var. No. of samples
0.046 + 0.0045 9.78 7
0.034 * 0.0074 21.76 6
1.35*
Small samples Mean k S.D. Coef. of var. No. of samples
0.255 + 0.105 41.18 18
0.194 f 0.090 46.39 18
1.31
BURROWING
ABILITY
The data in Table IV refer to the total number of burrows dug over a one week period by all the animals on a given substratum. There is a significant effect of root TABLEIV Comparative burrowing ability: total number of burrows dug during each experiment (one week); *, number of burrows dug on high substrata is significantly different (P > 0.95) than the number of burrows dug on low substrata for that crab group when compared by a Mann-Whitney U-test; crab groups are described in Table I. Root mat density High
Low
Small U. pugnax* Mean k S.D No. of expt
1.50 f 1.00 4
4.75 k 0.96 4
Large U. pugnax* Mean f S.D. No. of expt
0.83 * 1.17 6
3.00 + 1.00 3
Large U. minax Mean + S.D. No. of expt
1.43 f 1.40 7
I .67 + 0.58 3
mat density in the numbers of burrows dug by both large and small U. pugnux. The ratio of the number of burrows dug on high to low substrata is nearly the same for both large and small U. pugnux (or B,,,,/B,,,, N B,qsp/B,,sp# 1). There was no root mat effect on the number of burrows dug by U. minux (or B,,,,/B,,,, z 1). There is
16
PAUL RINGOLD
no trend in the data to indicate that it became easier to burrow on the substrata as the later experiments were conducted. PERCENTAGE
CARBON AND NITROGEN
The data in Table V are the percentage of the dry weight of the sample which was detected as either C or N. The high transect has x.507: more carbon and nitrogen TABLE
V
Distribution of carbon, nitrogen, and Uticabiomass: ‘5”carbon and ‘:, nitrogen in samples of surface sediment from the high and low areas of Bell Creek. N.C.; Uuz biomass is the total weight of both species of Uca in g/m’; high/low refers to the ratio of the means in each case; the probability that the high and low means of the carbon and nitrogen data are the same. when tested with a r-test, is given: there are no significant differences in Uccr biomass as a function of tidal height for either 1976. 1977. or 1976 and 1977 combined when tested with a r-test. Transect Low
High % carbon Mean & S.D. No. of samples Tj,nitrogen Mean & S.D. No. of samples Uen biomass, g/m2
High/Low
7.30 * 0.70 63
1.54 (P < O.OOI]
0.87 + 0.07 17
0.59 t_ 0.04 61
1.47 (P < 0.001)
37.22
34.12
1.09 (ns.)
than the low transect. If this be an indication of food availability for fiddler crabs, which are deposit-feeders (Newell, 1964; Adams & Angelovic, 1970; Tenore, 1977) then the high transect contains about 50% more food than the low transect.
DISCUSSION
The data show a strong parallel between the burrowing ability of Ii. pugnux and its abundance on natural substrata. I suggest, therefore, that burrowing. as modified by the root mat, controls the distribution and abundance of U. pugtzax on root mats of intermediate to high density. U. m&ax shows no evidence to date of the root mat affecting its burrowing ability and so I suggest that its distribution is controlled by other factors which may in turn be correlated-with root mat density. If root mat density (or its correlates) controls the distribution and abundance of Uca, then species distribution or abundance may reflect variations in root mat density. If this hypothesis be true, then a relationship between Uca species and root mat density should be observed in the existing data. In Table VI I have compiled information on root mat ranks, numerically dominant species of Uca, sand
17
FIDDLER CRAB DISTRIBUTION
content, tidal height, and distance from the creek bank for a variety of salt marsh habitats. All the data except for the root mat ranks are from Teal (1958); the root mat ranks follow the observations of Gallagher (1974) and Table III. Within areas of Spartina alterr@ora there are generally greater root mat densities higher in the marsh, and lower densities near the creek bank. Bare creek banks are assigned the lowest rank for root mat density. The remaining problem is how to rank the Distichlis-Salicornia area. Within one plant type and, therefore, one root mat type, the weight of material retained on a specific mesh sieve is probably a good index of burrowing difficulty. The Distichlis-Salicomia root mat is, however, very different from the Spartina root mat, and its rank based on weight of material retained on a sieve may not reflect the true difficulty that animals have in burrowing on this substratum when compared with the Spartina substratum. With this reservation, and the knowledge that medium Spa$ti~a, the next most dense root mat, has almost twice as much material as Distichlis-Sffli&orni~, the root mats are ranked based largely on Gallagher (1974) whose data, like Teal’s, come from Georgia salt marshes on or near Sapelo Island. TAELE
VI
Description of marsh habitats and the distribution of Ucn: the root mat data are modified from Gallagher (1974); rest of data from Teal (1958); all areas containing Ucu are given; in tidal height, lowest area is ranked 1; in root’mat density, least dense root mat is ranked 1.
Area Creek Bank Salicornia-Distichlis marsh Medium Spartina, low marsh Short Spartina, low marsh S~ort,S~artinu, high marsh ~j~a~ marsh
Rank of distance from creek bank
Tidal height. rank
Sand, 0, ,D
1 6 3.5 2 3.5 5
lo-70 8&95 O-10 O-10 4%70 30
Root mat density, rank
Numerically dominant UCG
V. pugilator U. pugilator V. pugnax U. pugnax U. pugnax U. n&ax
Table VI shows that the prediction that species reflect root mat density is upheld. The areas with the lowest root mat densities have Uca pugilator dominant, the intermediate areas have U. pugnax dominant, and the highest density root mat habitat has U. minax dominant. Two of the habitats have a second species - U. pugnax is found with U. pugilator in the Salicornia-Distichlis Marsh, and with Uca minax in the Minax Marsh. No other habitats have a second species. This pattern of distribution supports the view that root mat density is important to the distribution of Uca. Different factors have been shown to regulate populations of a single species through ontogeny (e.g., Hutchinson, 19.59). The importance of burrows in controlling Uca density may vary with the age of the crab. At Bell Creek, early crab stages
PAUL RINGOLD
18
of Ucu are found just inside the lip of burrows dug by larger individuals, or in the flocculent surface layer (pers. obs.; Crane, 1975, see p. 510). They are not necessarily living in burrows that they have dug, and it is, therefore, unlikely that they are regulated by factors related to burrowing or burrowing ability. Larger crabs use and defend burrows for a variety of purposes, and it is more likely that their abundance is controlled by factors that are related to their burrows. One might, therefore, predict that the parallel between burrowing ability and field abundances should be strongest for the largest animals, and weaker for the smaller animals. An examination of the data from the 1976 and 1977 collections shows that this is true. Table VIIB TABLE
VII
A, numbers of burrows dug and numbers of individuals found on substrata. B, ratios of burrows dug and numbers of individuals found on low to high substrata. Bij, number of burrows dug on the ith substratum by the jth crab group; Niti, number of individuals found on the ith substratum of the jth crab group; j or g = Ip for large U. pugnax (1.25 cm carapace width), = sp for small U. pugnax (1.0&l .25 cm), =p for U. pugnux ( < 1.00 cm), and =Im for large CJ. minax ( > 1.95 cm), = sm for small U. minax (1.00-1.95 cm), =m for CJ.minax (< 1.00 cm); i or k = h for high substrata (i.e., high root mat density from the high transect), =I for low substrata (i.e., low root mat density from the low transect). A
Substratum (i)
Crab group 0’)
h h h
1P sP P 1P sP
I I 1 h h h
No. of burrows dug
B,,, 0.83 1.50
5.3 6.3 11.6 21.3 20.4 41.7 4.0 2.0 6.0 0.0 0.0 0.0
3.00 4.75 1.43
1: sm m Im sm m
1 1 1
Density of crab group N!.,
_ 1.67 _
B
Substratum (i)
1 1
1
Crab group 0’)
sP IP Im
Substratum (k)
h h h
Crab group (g)
sP IP Im
Ratio of burrows dug on low to high substrata B,,,IBk,n
3.17 3.60 1.17
Ratio of no. of individuals found on low to high substrata
Nil/INk,g 1976
1977
1.76 3.09 0.00
7.10 3.29 0.00
FIDDLER
CRAB DISTRIBUTION
19
gives the ratios of low to high abundance of U. pugnax by year and size. The ratio for the large individuals is remarkably constant and similar to the ratio observed in the burrowing experiments. The ratio for the small individuals is variable from one year to the next, and is not similar to that observed in the burrowing experiments. This is not to say that burrowing ability is not important to the small adults (1.61.25 cm carapace width). It is likely that they have recently entered the stage in their life history where burrows are becoming more important, but their distribution is not yet at equilibrium with factors related to burrowing ability. Other factors have been suggested as controlling Uca distribution in the northwestern Atlantic and elsewhere; sediment, food, and micro-climate will be discussed here. The effects of sediment size on fiddler crab distribution have been discussed by Miller (1961) for U. pugilator, U. minax, and U. pugnax. He found that the mouth parts of Uca could be correlated with the sediment type on which he thought the crabs were typically found; he thought U. minax was adapted for feeding on the finest sediments, U. pugilator for feeding on the coarsest (sand) sediments, and that U. pugnax shows an intermediate adaptation. The percentage of sand along with the species observed to be dominant for a variety of habitats are given in Table VI. There are several violations of the expected relationship between sediment and the expected species. In the short Spartina high marsh, which ranks high in sand content, U. pugnax is found and U. pugilator, the species expected on the basis of mouthpart adaptations, is not found at all. In the two habitats with the lowest sand content, the medium Spartina low marsh, and the short Spartina low marsh, U. pugnax is dominant and U. minax, the expected species, is not found. Sediment size probably acts in a somewhat different way than does root mat density. U. minax is not observed on very sandy substrata probably because of mouthpart adaptations. U. pugilator is not found on very muddy sediments again probably because of mouthpart adaptations. Such adaptations may, therefore, only prevent a species from occupying extremes of sediment type, but play little role in regulating distribution within those sediment extremes. The possibility that the observed distributions are related to food should also be considered. Since availability of food varies with position in the marsh, then different areas of the marsh would be expected to support different biomasses of fiddler crabs. While C, N, and ATP are all more abundant in high marsh sediments (Table V; Christian, Bancroft & Wiebe, 1975) the biomass of fiddler crabs does not reflect the magnitude of this change. If food were responsible for the observed distributions. then U. minax caged in the low marsh. where it is not typically found, would not be expected to survive. Teal (1958) shows that it survives as well or better than U. pugnax in the lower areas of the marsh. This also demonstrates that U. minax is not excluded from the low parts of the marsh by micro-climate. In addition, if food limitations were important, marked effects due to starvation would be expected. Barnwell (1966, pers. comm.) starved U. pugnax and U. minax for up to seven weeks in connection
20
PAULRINGOLD
with studies on endogenous rhythms. Activity decreases rapidly at first, and then less so. U. minux tended to survive longer than U. pugnax in these experiments. This may be due to greater food reserves in U. minax or a greater capacity to tolerate the experimental conditions and again suggests that U. minax is not restricted to the higher parts of the marsh by natural conditions of food and micro-climate. None of these three results is a critical test of the hypothesis that food controls Uca distribution, but together they suggest that it is unlikely. This paper is a step towards explaining the distribution of U. pugnax, U. minax, and U. pugilator. Information on the distribution of U. pugnax on intermediate to dense root mats has been obtained. The question of the maintenance of the borders between U. pugnax and its two sympatric congeners remains. It is likely that the interaction between U. minax and U. pugnax is based on some form of interference competition (Case & Gilpin, 1974).
ACKNOWLEDGEMENTS
I gratefully acknowledge the assistance of the many people who have helped in all stages of this work. Bill Seiple and Terry West helped with much of the field work, Dr J. D. Costlow and members of the staff and students of the Duke University Marine Laboratory provided facilities and hospitality during the course of the work at Beaufort. Dr J. Taft allowed me to use a CHN analyser, and special thanks must go to my advisor, Dr S. A. Woodin. Parts of this work were supported by a Culpepper Foundation Fellowship, by NSF grant GA-4261 1, and NSF grant OCE76-01666 A01 ; both NSF grants were awarded to Dr Woodin.
REFERENCES ADAMS, S. M. & J. W. ANGELOVIC,1970. Assimilation of detritus and its associated bacteria by three species of estuarine animals. Chesapeake Sci., Vol. 11, pp. 249-254. BARNWELL,F. H., 1966. Daily and tidal patterns of activity in individual fiddler crabs (genus Uca) from the Woods Hole region. Biol. Bull. mar. biol. Lab., Woods Hole, Vol. 130, pp. I-17. CASE,T. J. & M. E. GILPIN, 1974. Interference competition and niche theory. Proc. mtn. Acad. Sci. U.S.A., Vol. 71, pp. 3073-3077. CHRISTIAN,R. R., K. BANCROFT. & W. J. WIEBE, 1975. Distribution of microbial adenosine triphosphate in salt marsh sediments at Sapelo Island, Georgia. Soil Sci., Vol. 119, pp. 89-97. CRANE, J., 1975. Fiddler crabs of’ the world (Ocypodidae: genus Uca). Princeton University Press. Princeton, N.J., 736 pp. GALLAGHER.J. L., 1974. Sampling macroorganic profiles in salt marsh plant root zones. Proc. Soil Sci. Sot. Am., Vol. 38, pp. 154-155. HUTCHINSON,G. E., 1959. Homage to Santa Rosalia, or why are there so many kinds of animals? Am. Nat., Vol. 93, pp. 323-349. MILLER, D. C., 1961. The feeding mechanisms of fiddler crabs with ecological feeding considerations of feeding adaptations. Zoologica, N. Y., Vol. 46, pp. 89-100. NEWELL,R., 1964. The rBle of detritus in the nutrition of two marine deposit feeders, the prosobranch, Hydrobio ulvae, and the bivalve, Macoma bnlthica. Proc. zool. Sot.. Land., Vol. 144, pp. 25-45.
FIDDLER CRAB DISTRIBUTION
21
POWERS,L. W. & J. F. COLE, 1976. Temperature variation in fiddler crab microhabitats. J. rxp. mar. Biol. Ecol., Vol. 21, pp. 141-157. TEAL,J. M., 1958. Distribution of fiddler crabs in Georgia salt marshes. Ecology, Vol. 39, pp. 185-193. TENORE, K. R., 1977. Utilization of aged detritus derived from different sources by the polychaete Cupitella capitata. Mar. Biol., Vol. 44, pp. 51-56.