MARINE ECOLOGY PROGRESS SERIES Vol. 155: 137-145, 1997 Published August 28 Mar Ecol Prog Ser

Between-habitat differences in burrow characteristics and trophic modes in the southwestern Atlantic burrowing Chasmagnathus granulata

Oscar Iribarne*,Alejandro Bortolus, Florencia Botto

Departamento de Biologia (FCEyN),Universidad Nacional de Mar del Plata, Funes 3250 (7600) Mar del Plata, Argentina

ABSTRACT Burrow characteristics, food type, and feeding hab~tsof the SW Atlantlc burrowing crab Chasmagnathus grdnulata were compared between ~ndiv~dualsliving in mud flats and In Spartina- dominated marshes. Burrows were shorter (X- 19.7 cm, SD = 5 8, n = 54) and more dynamlc (entrance displacement: X = 3 2 cm d-l, SD = 1 7, n = 21) in mud flats than In Spartlna-dominated areas (length X= 41 cm, SD = 12, n = 78, no entrance displacement). Sediment turnover rate was much higher in mud flats (X- 5 9 kg m-' d-l) than in Spartlna-dominated areas (X= 2 4 kg m-' d.'). Burrow shape differed between areas, being straight, near-vert~caltunnels in the vegetated area, but oblique (average angle to vertical = 60'. SD = 16", n = 110),and having a funnel-shape entrance and a much large]-diameter in mud flats Stomach contents also differed between habitats. Pleces of plants dominated contents in the vegetated area, while sediment (with polychaetes, diatoms, ostracods, and nematodes) dom~natedin the mud flats, lndicatlng that are mainly deposit feeders In the mud flats and herb~vorousin the Spart~na-dominatedareas. This pattern suggests that the heuristic model relatlng burrow arch~tecture to trophic modes prev~ouslyproposed for fossorial thalassinidean shrimps applies to individuals of a C granulata populat~onThe burrow content showed higher organic content and vegetal parts in the veg- etated area than in the other area. Burrows in the mud flat showed a significantly higher abundance of nematodes and ostracods. Due to their hydrodynalnic characteristics and content, burrows in the mud flats may work as passive traps for sediment and organic matter. Given the extensive intertidal area inhabited by C granulata in SW Atlantic estuanes, and the locatlon of their burrows (between marshes and the open estuary), these burrows may work as traps for detritus, thus reduclng the export rate of organic matter from marshes.

KEYWORDS Spartlna marsh . Chasmagnathus granulata . Burrowing . Herbivory

INTRODUCTION alterniflora; Bertness & Miller 1984, Bertness 1985). Particular attention has been given to the Importance Benthic fauna play an important role in the sedimen- of crabs as habitat modifiers in salt marshes (e.g. Mon- tary process, leading to important changes in marsh tague 1980, Bei-tness 1985). Burrowing crabs may be characteristics (Frey et al. 1978, Bertness 1985) The present in large numbers in these environments (e.g. fauna of mud flats and creeks include inany deposit Boschl 1964, Bertness & Miller 1984), significantly and filter feeders that modify sediment particle size influencing microtopography, sediment chemistry and and chemistry (Levinton 1989).Their burrowing activ- drainage (Bertness 1985). Sediment disturbance result- ities may have considerable effects on soil aeration and ing from the foraglng and burrowing activities of on growth and distribution of the flora (e.g. Spartina decapods may have direct and indirect impacts on other species (e.g.Thrush 1988, DePatra & Levin 1989, Warwick et al. 1990). Species that are sensitive to bur- ial or disturbance may suffer higher mortality due to

O Inter-Research 1997 Resale of full artlcle not permitted Mar Ecol Prog Ser 155: 137-145, 1997

crab activities (e.g Kneib 1.991, Billick & Case 19941, or tion between trophic mode and burrow architecture. predators may be attracted to areas where infauna are Crabs living in creeks and channels show shallow bur- exposed due to sediment reivorking (e.g Auster & rows with large entrances and surface sediment Crockett 1984). mounds, while crabs living in the S. densiflora marsh The interpretation of autoecological characteristics show deep burrows with small entrances and often from physical structures has been an active area of without surface sediment mounds. Preliminary obser- research during the past few years. Suchanek (1985) vations on stomach contents of crabs living in creeks and Griffis & Suchanek (1991), comparing thalassinid show only mud, while crabs obtained from marsh areas shrimps, identified species-specific burrow architec- show fragments of vascular plants. This suggests thdt ture suggesting that burrow morphology reflects the heuristic models that relate feeding mode, burrowing feeding modes of the organism, and proposed a heuris- activity and burrow architecture (as proposed by tic model relating burrow architecture to trophic Griffis & Suchaneck 1991) also apply for conspecifics modes. Although this classification has been criticized within the same population of C. granulata, which are due to the lack of flexibility to account for intraspecific deposit feeders in mud flats (creeks and channels) and variations (i.e. Nickel1 & Atkinson 1995. Rowden & herbivorous-detritivorous in the marsh area. In this Jones 1995), the important value of this approach was work we evaluate this general hypothesis by investi- to point out the interrelationship between feeding gating if burrow architecture, burrow dynamics, sedi- modes, burrow architecture and effects on sediment ment turnover rate, and feeding modes vary between dynamics. individuals living in open mud flats and those living in The crab Chasmagnathus granulata, one of the most the marsh area dominated by the cordgrass S. densi- abundant macroinvertebrates on salt marshes of the flora. southwestern Atlantic (Boschi 1964, Capitoli et al. 1977, 1978, Botto & Irigoyen 1979, D'Incao et al. 1990, Spivak et al. 1994), is also a burrowing species that METHODS inhabits the intertidal, from the soft bare sediment flats to areas vegetated by the cordgrass Spartina densiflora The study was performed in the Mar Chiquita (Boschi 1964, D'Incao et al. 1988, Spivak et al. 1994). coastal lagoon (Argentina, 37" 32' to 37" 45' S, 57" 19' These crabs excavate and maintain semipermanent to 57" 26' W) from spnng 1995 to autumn 1996. The open burrows (Boschi 1964. Spivak et al. 1994) and, as study site is a body of brackish water (approximately suggested for other burrowing species (e.g. Uca spp.; 46 km2) affected by low amplitude ($1 m) tides (e.g. Teal & Kanwisher 1961), their burrowing activity may Lanfredi et al. 1987, Spivak et al. 1994) and character- oxygenate marsh soil, enhance soil drainage, and mod- ized by mud flats surrounded by a large cordgrass ify sediment meiofaunal abundance. C. granulata bur- Spartina densiflora area (Olivier et al. 1972a, b, Fasano rows can extend up to 1 m into the marsh sediment and et al. 1982). Two sites located 20 m apart were com- density can be as high as 60 crabs m-2 (pers. obs.) pared during this study: (1) tidal mud flats and (2) a Given their high density and the important role of marsh area dominated by cordgrasses. deposit feeding on sediment composition (e g. Rhoads To investigate variations between habitats in burrow 1967), this species is likely to play a key role in marsh shape, castings (made with gypsum plaster of Paris) of production and integrity. Despite these facts, no atten- 20 burrows of average size in each habitat type tion has been directed to understanding the impact of (entrance diameter 4.5 to 6.5 cm in mud flats, and 2.0 to their burrowing and deposit feeding activities on salt 4.0 cm in the marsh area) were made. After a harden- marsh community or sediment dynamics. On the basis ing time of 72 h, casts were hand-excavated from the of stomach content analysis of individuals of unidenti- sediment, washed free of sediment, and allowed to dry fied origin, this species is described as omnivorous- and harden in a heated room. Then, a visual descrip- detritivorous (Botto & lrigoyen 1979, D'Incao et al. tion in terms of entrance and tunnel shape was made. 1990). However analyses of gut contents without For the quantitative comparison of burrows between regard to the behavior and feeding patterns may lead habitats, burrows were sampled following 2 different to a misunderstanding of dietary scope and the spe- designs. A sample of burrow was obtained by ran- cies' potential impact within different habitats (see domly placing ten 1 m2 quadrats in each habitat, Kneib 1995). counting burrow entrances and measuring their diam- In previous studies, it has been observed that bur- eter (major axis and mlnor axis). The null hypothesis of rows of Chasmagnathus granulata vary in size and no difference in the size frequency distribution of max- shape in intertidal mud flats compared with dry mud in imum entrance diameters between habitats was tested the Spartina densiflora marsh (Olivier et al. 1972a, b, using a Kolmogorov-Smirnov test (Zar 1984) To inves- Goya 1988). Our observations also suggest an associa- tigate differences in shape of burrow entrances, the Iribarne et a1 : Crab burrow character~stics 139

ratio between the major axis (maximum diameter) was used to test the null hypothesis of no difference in divided by the minor axls (minimum diameter) was cal- the mean daily burrow displacement (linear distance culated in each area. The null hypothesis of no differ- In cm, between initial and final position) between ence in the distribution of ratios between habitats was zones. evaluated with a Kolmogorov-Smirnov test (Zar 1984). Amount of sediment removed by crabs per day In To investigate the relationship between dlameter of each habitat was also quantified by weighing (wet burrow entrances and burrow volume, 40 burrows weight) the new sediment that appeared each day In from each habitat were sampled, covering hoinoge- the mound around the burrow entrance (precision neously the size range of opening diameters found in ?l g). However ~t is important to note that, although each site, and measuring: (1) major and minor axis tldal energy or wind transport in this area is low, we entrance diameter (precision: ~0.1mm), and (2) bur- may have underestimated the actual values in the row volume (measured filling them with a known vol- open mud flat because measurements of sediment ume of fine-gralned dry sand). The null hypothesis of mounds were obtained after a full tidal cycle. The null no difference between habitats in the relationship hypothesis of no relationship between diameter of the between entrance diameter and burrow volume was burrow entrances and mound wet weight was evalu- evaluated by comparing the slopes of the relationship ated by a correlation analysis (Zar 1984). The null of burrow volunle and burrow diameter (major axis) for hypothesis of no difference between habitats in daily each habitat (Zar 1984). Data were log-transformed to sediment turnover rate per burrow as a function of comply with the assumptions of linearity of a simple entrance diameter was evaluated by comparing the hear regression (Zar 1984). To investigate differences slopes of the relationship between sediment welght in burrow inclination in relation to the marsh or open and maximum diameter of the burrow entrance (Zar mud floor, a 1 m long stlff wire was inserted into the 1984). burrow entrance and its angle measured in relation to Position of burrow mounds in relation to the burrow the vertical plane (marsh-floor or open mud). The null opening of at least 100 randomly selected burrows per hypothesis of no difference in frequencies of a range of site, in 3 parts of the channel with different orientation angles was evaluated with a chi-squared test (Zar (main channel orientation of site A: 90" to 270'; site B: 1984). 20' to 200"; site C: 70" to 250°), were determined dur- Burrow entrances were also characterized in relation ing low tide. Orientation was defined as the bearing of to their shape. When the openings of burrows were a line between the mound and the burrow entrance. funnel-shaped, we measured the maximum diameter The null hypothesis of no preferential direction was of the exterior part of the burrow entrance, the diame- evaluated with a chi-squared test (Zar 1984). Since ter of the shaft and the depth of the funnel (distance preferential orlentation of mound locations in relation between the plane generated by the burrow entrance to burrow entrances were found, the area around the and the plane generated by the end of the funnel burrow was divided in 2 semicircles, one In the beginning of the tunnel). We also measured the total upstream direction and other in the downstream direc- length of each burrow. The null hypotheses of no rela- tion. The null hypothesis of no preferential location of tionship between external maximum diameter and burrow mounds in relation to the upstream or down- diameter of the shaft, external maximum diameter and stream current was evaluated by a binomial test depth of the funnel, and diameter of the shaft and fun- (Conover 1980). nel depth were evaluated by a correlation analysis (Zar Burrow contents were sampled in each slte by using 1984). The null hypothesis of no difference between a 1.5 m long hose to suck approximately 100 m1 of zones in mean burrow length was evaluated by a t,- water and sediment from the deepest part of the bur- test (Zar 1984). Here and in all further cases means row. Forty replicates were obtained from each site, were compared wlth the Welch-approxlmatlon t-test sieved through a 100 pm screen, and the retained (t,)to account for differences in variances (Zar 1984). material was identified with a binocular nlicroscope To study differences between zones in burrow (40x1. Individuals found in each sample were standard- dynamics, and sediment turnover rate, 100 burrows (of ized per unit of volume of sedlment [number of organ- average size) were identified in each area. Entrances ~sms(volume of sediment)-']. The null hypothesis of no of these burrows were measured (maximum diameter), difference between habitats in abundance of each spe- and spatially located (centered) in relation to 4 fixed cies in the burrow content was evaluated with a &-test points positioned 20 cm from the burrow entrance. (Zar 1984). An additional 20 samples were obtained Daily measurements of location of burrow entrance in using the same procedure, dried at 60°C for 4 d, and relation to the fixed points and amount of sediment ash free dry weights (AFDW) determined after com- removed were obtained for a period of 30 d (February bustion at 500°C for 24 h. The percentage difference 2 to March 5) at each site. A t,-test analysis (Zar 1984) between dried weight and AFDW was calculated and Mar Ecol Prog Ser 155: 137-145. 1997

then the null hypothesis of no difference between habitats was evaluated with a &-test (Zar 1984) To evaluate ~f feeding modes differed between habi- tats. 100 crabs were sampled at low tide from each habitat, immediately killed and their stomachs pre- served in 5':; formalin. The volume of plants remains and sediment in each stomach was measured by plac- ing the stomach contents, diluted in 5% formalin, into a 5 m1 calibrated flask (0.1 ml), and allowing the con- tent to sink for 4 h. The null hypothesis of no difference between habitats in volume of plant debris or sediment was evaluated with a t,-test (Zar 1984). Comparison between sediment and plants volume was not per- form.ed because, due to their lower specific weight, plants are less closely packed than sediment; thus plant volumes found with our measurement procedure are not the minimum volumes at which they can be held in the stomach.

RESULTS

Casting and excavations showed that burrows in both habitats are simple, with a single shaft or tunnel, + A marsh mud flat I mainly without branches and always reaching the water table. However, burrows differ in shape. Bur- rows located in mud flats are short, with an enlarged funnel-like opening which terminates in a sediment mound. Burrows in the marsh area are straight, long tunnels, usually with an enlarged chamber at the end approximately 2 times the tunnel diameter In the mud flats the minor and major external axes of MAJOR AXIS LENGTH (cm) burrow entrances were usually different but correlated (r2 = 0.85, n = 54, p < 0.05; Fig. 1A). The depth of the Fig. 1. Relationsh~p between major axls length of burrow entrances and (A)minor axis length, (B)funnel depth, (C) tun- funnel was significantly correlated with the diameter nel diameter and (D) tunnel length for burrows sampled in of the burrow entrance (r2 = 0.57, n = 54, p < 0.05; both habitats. The 11ne represents the 1:l relationship. Sample Fig. 1B) and the length of the burrow was also corre- sizes were 54 in the mud flat and 41 ~n the Spartina marsh lated to the major axis of the burrow entrance (r2 = 0.29, n = 54, p < 0.05; Fig. ID). However, there was no significant correlation between burrow length and the 1.09, SD = 0.17, n = 2001 but asymmetric in mud flats entrance major axis in the marsh area (r2 = 0.0002, n = jmean ratio (major axis/rnlnor axis) = 1.38, SD = 0.29, 76, p > 0.05). In the mud area the shaft diameter was n = 200; Fig. 2B]. The difference in the frequency also correlated with the external major axis (r2 = 0.27, distribution of ratios was also statistically significant n = 54, p < 0.05; Fig 1C). Burrows in the Spartina [Kolmogorov-Smirnov: d,,, = 57, (dm,,)o.os, 15, zNl = 12, marsh were significantly longer (X = 41 cm, SD = 12. p < 0.051 The slopes of the relationship between open- n = 78, up to 73 cm) than burrows in the mud flat (X = ing diameters and burrow volume (log-transformed

22.8, SD = 56.6, n = 54, up to 33 cm; C, = 13.5, df = 118, volume; Fig. 2C) were significantly different between p i 0.05; Fig. ID). habitats (mud flat: b = 0 01451, SD = 0.0026, n = 39; The size frequency distribution showed that maxi- marsh area: b = 0.0054, SD = 0.00187, n = 39; t, = 17.43, mum diameters of burrow openings in the marsh area df = 76, p < 0.005). Burrow volumes for a given diame- were on average smaller (X= 26.6 mm, SD = 8.9 mm. ter in marsh areas were larger than in mud flats when n = 200) than in the open mud flat (X = 52.8 mm, SD = openings were relatively small, but smaller for larger 17.8 mm, n = 200; Kolmogorov-Smirnov: d,,, = 76, p < burrow openings (Fig. 2C) These differences were not 0.05; Fig 2A). Burrow entrances were mainly circular related to the internal shape of the burrow, instead the in the marsh area [mean ratio (major axis/minor axis) = larger volumes of burrow with larger openings were Iribarne et al.. Crab burrow characteristics 141

lateral movement of burrow openings in mud flats was significantly higher, averaging 3.27 cm d-l (SD = 1.7, n = 100; t,. = 19.2, df = 99, p < 0.05; Fig 3B).There was a significant relationship between amount of sediment removed per day and burrow opening diameter in mud flats (r' = 0.89, n = 35, p < 0.005) and in the marsh area (r' = 0.46, n = 35, p < 0.05). However the amount of sed- MAXIMUMDIAMETER (cm) iment removed as a function of burrow entrance diam- eter was higher in the mud flat area (slope of the rela- tion of sediment weight to burrow entrance diameter: b = 3.7433, SD = 0.3262, n = 33) than in the marsh area 0 (b = 2.3604, SD = 0.4464, n = 34; t, = -14.506, df = 60, 20 - MUD FLAT p < 0.05; Fig. 4). a SPARTINA 0' Location of sediment mounds around the burrow 11.2 1.4 1.6 1.8 22.2 2.4 RATIO: MAJOR AXISIMINOR AXIS entrances in the open mud flat were significantly dif- ferent from a random distribution at all sites (site A: x2= 16 5, p < 0.05, s~teB: x2= 19.7, p 0.05; site C: = 18.18, p < 0.05). Mounds were preferentially located along the axis of the main channel (Fig 5) with no pref- erential location in relation to the upstream or down- stream side at site A (upstream 48% n = 70, binomial 2345678910test: t, = 26, t, = 50, p > 0.05), and preferentially located OPENING DIAMETER (cm) downstream at the other 2 sites (site B: upstream 64 'X,, n = 70, binomial test: t, = 27, t, = 43, p < 0.05; site C: upstream 67'Jtj,n = 80, binomial test: t,= 31, t2 = 49, ,p < 0.051.

E o!L . L- 10 20 30 40 50 60 70 80 90 ANGLE

Fig. 2. Percentage d~str~butionof (A) maximum diameters of burrow entrances, (B)ratlos major axis/minor axis (n = 2001, and (D)burrow angles (in relation to the vertical) rn both habitats. (C) Relat~onshipbetween burrow volume and open- ing diameter. Open bars: data from the Sparlina marsh; shaded bars: clata from the mud flats

mostly due to the enlarged entrance forming a funnel- like depression instead of a small straight entrance. The burrow inclination, in relation to the vertical axis, was greater in open mud flats (X= 60". SD = 16". n = 110), and significantly different from burrows in the marsh area (X = 33", SD = 11°,n = 110; = 930. X? ,,,,>,= 15.5, p < 0.05; Fig 2D) where they were almost perpendicular to the surface. The continuous observations of burrows in open mud flats showed that only a small proportion of burrows (-2OC%,)were closed (Fig. 3A) during the experimental period. Burrows were much more dynamic in chan- 2 8 12 16 20 24 28 32 36 nels, in terms of percentage of active burrows per day DAYS (X= 79.5'%, SD = 7.6':1,, n = loo),than in the marsh area Fig. 3 Burrow activrty In mud flats dunng a period of 30 d (X= 32%, SD = 3'%, n = 100; t, = 58.1, df = 129, p < when they were followed ~ndivrdually[n = 100). (A)Percent- 0.05). There was no noticeable lateral movement in age of burroivs closed each day, [B)mean (ZSD)burrow burrow openings located in the marsh area while mean movement between days Dashed lines represent *l SD 142 Mar Ecol Prog Ser 155: 137-145, 1997

~udnat

MUD FLAT MARSH HABITAT TYPE BURROW DIAMETER(mm) Fig. 6. Mean volume occupied by sediment (open bars) and macrophytes (crosshatched bars) of individuals collected in Fig. 4. Relationship between sedlment mound weight and the mud flats (n = 40) and the Spartlna marsh (n = 40). Lines burrow diameter for burrows in the Spartina marsh area (U, above the bars represent 1 SD n = 34) and the mud flat (B, n = 33)

and copepods (X = 0.08 ind. mg-l, SD = 0.09) than bur- Burrow contents differed between sites. Burrows in rows in the mud flat (nematodes: X = 9.38 ind. mg-l, the Spartina marsh showed significantly lower densi- SD = 4.52, t, = 8.48, df = 19, p < 0.05; copepods: X = ties of nematodes (X= 0.8 ind. mg-', SD = 0.2, n = 20) 4.32 ind, mg-l, SD = 5.48, t, = 3.45, df = 19, p < 0.05) Ostracods (X= 0.65 ind. mg-l, SD = 0.1.7, n = 20) and turbellarians (X=0.12 ind. mg-', SD = 0.17, n = 20) were only found in the open mud. Pieces of plants (probably Spartina leaf) were found in burrows from the marsh area, but not in burrows from the open mud. The per- centage of AFDW of mud obtained inside burrows in the Spartjna-dominated marsh (X = 6.35%, SD = 2.18, n = 20) was not different from the percentage found in- 0 side burrows in the mud flats (X= 5.25%, SD = 0.81, n = SlTE B 20; t, = 2.15, df = 24, p > 0.05), although their variances 02 - were significantly different (F= 7.24,p c 0.05).The dif- i ference in variability was due to pieces of macrophytes A found in burrows from the marsh samples. 0 l Stomach contents of crabs differ between sites F (Fig. 6). All individuals from the marsh area showed the stomach full of macrophytes (mean volume X = 0 rl p-P I 7 0.148 ml, SD = 0.1518, n = 401, while only 9% of them 0 2 1 SlTE C FT-, showed sediment in their stomach, which always occu- pied a low volume (mean volume X = 0.002 ml, SD = 0.003, n = 40). The opposite pattern was found with stomach content of individuals from the mud area (mean volume of macrophytes X = 0.0018 ml. SD = 0.0048, n = 40, l, = 4.28, df = 39, p c 0.05; mean volume of mud X=0.051 ml, SD = 0.0250, n = 40, t, = 8.1, df = 40, ANGLE pc0 05).

Flg. 5. Onentation of sediment mounds (~nrelation to burrow entrances1 CI~the 3 sites (main channel orlentation of slte A: DISCUSSION -270". n = 70; s~teB: 20"-ZOO0,n = 70; site C: 70'-2-50". n = 80). The x-axis represents the onentation angle where 0" and 360" ISnorth. Arrows indicate mound located exactly (?20°) Individuals of Chasmagnathus granulata from the upstream (A)or downstream (l) from the burrow entrance Spartina-dominated marsh and mud flats differ in Irlbarne et a1 : Crab burrow characteristics 143

trophic mode, sedlment processing rate, burrow archi- generally the water table, always containing water tecture and burrow dynamics. Crabs were herbivorous during the whole tidal cycle. This may be an adapta- when associated wlth the cordgrass S. densiflora, and tion to maintain humidity in the marsh area. Burrows deposit feeders when living in tidal creeks and chan- are shelters from predation and environmental ex- nels. The burrow dynamics and the sediment process- tremes, provide water for physiological needs and are ing rate was much higher in mud flats than in the sites for molting and reproduction. The burrow short- marsh, and similarly to thalassinidean shrimps (Griffis ness in the mud flat area may also be related to feeding & Suchanek 1991, Nickel1 & Atkinson 1995, Rowden & mode. Deposit-feeding may only be productive if done Jones 1995) trophic modes, burrow architecture and in the upper oxygenated layer sediment processing rates are associated. Burrow contents were also significantly different Herbivory and deposit-feeding have significantly between habitats; nematodes and ostracods were sig- different effects on the biological and physico-chemi- nificantly more abundant in mud flats than in the cal environment. Deposit or detritus feeders can marsh areas. This pattern may indicate that burrows decrease the amount of entrained organic matter in the are passive trapping areas. A field and laboratory sediment available to other species (Bird 1982, study of Uca crab burrows showed a similar pattern Suchanek 1985), and control sediment grain size, (DePatra & Levin 1989), which suggests that, as for transport, mixing and deposition (Robertson & Pfeiffer other depressions, meiofauna increases in abundance 1982. Suchanek 1983, Tudhope & Scoffin 1984). Sedi- due to passive accumulation. Burrows in the marsh ment processing, as inferred from sediment mound area are covered by tides only 1 or 2 times a week, size, was much higher in the mud flat than in the marsh while burrows in the mud flats are inundated 1 or 2 area. Based on mound size as an indication of the rate times a day. Thus, if burrows are passive trap areas, of sediment processing (assuming absence of effect of the difference in water circulation may be sufficient to tidal currents; F. Botto pers. obs.), assuming 40 active explain the differences in abundance of meiofauna. burrows m-' d-l, and taking into account the size fre- However, even though meiofauna was higher in the quency distribution of burrows found in each site, we mud flat, mean organic matter of burrow contents was estimate that the amount of sedlment removed per day not significantly different between habitats, although in mud flats is 5.9 kg m-2 d-' and 2.4 kg m-2 d-' in the in the Spartina marsh area AFDW showed larger vari- Spartina-dominated marsh area. Although this is a ability. Larger pieces of plants were occasionally found rough estimation, it shows that crab activity has an in burrows located in the marsh, which may be the important effect in both areas and exemplifies the dif- product of passive transport or have been Introduced ferences in magnitude between these areas. It is also by crabs. Work in progress (Bortolus & Iribarne 1996, Interesting to notice that the amount of sediment pro- 1997) shows that in this area plants located near bur- cessing shown by Cllasmagnathus granulata is higher rows (e.g. Spartina densiflora) suffer much higher than most reports for thalassinidean shrimps [e.g. Cal- losses due to crab herbivory than those located in areas lianassa kraussl, 12.14 kg (wet) m-2 d-' (Branch & without crabs. Prlngle 1987); C. subterranea, 3.5 kg (dry) m-2 yr-' Differences in burrow architecture associated with (Witbaard & Duineveld 1989); C. californiensis 2.7 1 different sediment characteristics may reflect struc- (wet) m-2 d-' (Sw~nbanks& Luternauer 1987); Glyp- tural limitations of the sediment to support particular tel-us armatus, 3.3 kg (wet) m-' yr-' (Vaugelas 1984)], type of burrow shape (Griffis & Suchanek 1991). Bur- which are the marine benthic organisms with the high- row morphology may also be related to sediment type est sediment processing rates. The sediment processed (Frey et al. 1978, Griffis & Chavez 1988). Callianassa in marsh areas appears to be mostly related to burrow pontica excavate burrows with irregular patterns in expansion or repair, since it was relatively low and fine sands, and simple tunnels in coarse sands crabs did not show sediment in their stomach content. (Dworschak 1987). In our study the 2 habitats also have However, the sediment mounds in intertidal areas may different sedimentary composition. While the tidal be indicative of deposit feeding, since it is a large mud flat is characterized by a high percentage of silt amount and crabs show sediment in their stomach con- and clay (52'%) and high penetrability (1.7 kp cm-2), tent. the marsh area is characterized by sand (98%) and Burrows were much deeper in the marsh area than lower penetrability (12 kp cm-'; Spivak et al. 1994). in the mud flat. A similar pattern has been reported for Griffis & Suchanek (1991) suggest that different bur- other intertidal burrowing species (e.g. Upogebia pu- row architecture may also be indicative of different silla, Callianassa californiensis; Dworschak 1987) for feeding behaviors associated with different sediment which burrows reached greater depths in the upper types. In fact, there IS not necessarily cause and effect intertidal than in subtidal areas. In our case individuals in the association between burrow shape and feeding were always intertidal, and the end of the burrow was mode; however, sediment characteristics may restrict Mar Ecol Prog Ser 155: 137-145, 1997

the type of burrow that can be constructed and conse- ies. Howevel-, given the extensive intertidal areas quently the type of food to be used. inhabited by Chasrnagnathus granulata in SW Atlantic The differences in architecture between burrows estuaries, the effect of their burrows as modifiers of constructed in mud flats and the marsh area may also nearbed fluxes should not be underestimated. Indeed be related to dissimilarities in the associated food con- all evidence suggests that these extensive burrow beds tent of the substratum and feeding type. Sediments in that are distributed between marshes and the open the mud flats have much higher organ~ccontent (Spi- estuary may also be considered a large macrodetritus vak et al. 1994).If crabs are deposit feeders, they may retention area, reducing the amount of organic matter be d(,pleting the food content of the sediment, and exported from marshes. individuals in the mud flats may be forced to construct burrows, or expand their burrows, to support their Acknowledgejnents. This prolect was supported by the Uni- energetic requirements. Several lines of evidence sug- vcrsidad Nacional de Mar del Plata, Fundacion Antorchas gest that burrows in intertidal mud flats increase the (#13016/1-00012) and International Foundation for Sciences ability to trap organic matter. The burrow entrances (No. A/2501-l). F.B. was supported by a CONICET (Argen- are different between sites, being funnel-shaped in the tina] Scholarship. We are grateful to the anonymous review- ers for many valuable suggestions. mud flat area and stralght tunnels in Spartina marshes. The funnel shape entrance has been suggested to function as a sediment trap in thalassinidean shrimps LITERATURE CITED (Suchanek 1983, Poore & Suchanek 1988, W~tbaard& Duineveld 1989, Vaugelas 1990, Nickel1 & Atkinson ~usterPJ, Crockett LR (1984) Foraging tactics of several 1995) by enhancing capture of bedload particles that specles for infaunal prey. J Shellfish Res 4: 139-143 slip down the sides of the funnel. The increase in the Bertness MD (1985) Fiddler crab regulation of Sparlina size of the surface openings may also be related to alternlflora production on a New England salt marsh. opportunistic trapping of surface-deposited detritus Ecology 66: 1042-1055 that increases the food content of the sediment. A lab- Bertness MD. 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Oblique tunnels allow access to the sedi- College Park ment surface for the movement of sediment or Bortolus A, Iribarne 0 (1996) Efectos del cangrejo cdvador macroorganic materials in or out of the burrow and Chas~nagnalhusgran~llata sobre suelos y comunldades vegetales de marismas. IT1 Encontro de espec~dlistastlrn would thus also suggest a deposit-feeding or omnivo- Brachyura, Rio Grande. Brasil. p 1 IAbstract) rous-scavenging trophic mode (Nickel1 & Atkinson Bortolus A, Iribarne 0 (1997) Interacciones entre el cangrejo 1995). The flume study performed by DePatra & Levin cavador Chasmagnath~isgranulata y un espart~llarbonae- (1989)also suggested that angled burrows should cap- rense. In: XVlIl Reunion de la Asoc~ac~on..Irrjentlna de ture a higher abundance of passively transported Ecologia, Buenos A~res,Argent~na. p 19 (Abstrdct) Bosch~EE (1964) Los Crustaceos Decapodos Brachyura del meiofauna than upright burrows. Thus, all of this evl- litoral Bonaerense (R. Argentina). 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This article was submitted to the editor Manuscript received: April 7. 1997 Revjsed version accepted: June 25, 1997