Fiddler crab burrowing aVects growth and production of the white
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Mar Biol DOI 10.1007/s00227-009-1253-7 123 ORIGINAL PAPER Fiddler crab burrowing aV ects growth and production of the white mangrove (Laguncularia racemosa) in a restored Florida coastal marsh Nancy F. Smith · Christie Wilcox · Jeannine M. Lessmann Received: 1 December 2008 / Accepted: 26 June 2009 © Springer-Verlag 2009 Abstract Positive plant–animal interactions are impor- tant in community ecology, but relatively little attention has been paid to their eVect on the production of mangroves, dominant halophytic trees in tropical coastal marshes. Here, the role of Wddler crab (Uca spp.) burrowing on the growth and production of the white mangrove, Laguncularia racemosa (<2 years old), was examined in a restored marsh in Tampa Bay, Florida (27°41.65 N, 82°30.34 W) with manipulative experiments from June 2006 to May 2007. Fiddler crab burrowing signiWcantly increased mangrove height by 27%, trunk diameter by 25%, and leaf production by 15%, compared to mangroves in crab exclusion enclo- sures. Additionally, the exclusion of Wddler crabs signiW- cantly increased interstitial water salinity from 32.4 to 44.2, and decreased the oxidation–reduction potential of the low organic sediments, but did not aVect soil pH or sulWde con- centration. Mangrove height, trunk diameter, and leaf pro- duction along a transect that varied in crab burrow density were positively associated with the number of crab bur- rows. Further, the density of sympatric Spartina alterniXora shoots was positively correlated with crab burrow density along the transect. As in temperate marshes, Wddler crabs can have signiWcant ecological eVects on mangrove communities, serving as ecological engineers by modulat- ing the amount of resources available to marsh plants, and by altering the physical, chemical, and biological state of these soft sediment communities. In restored coastal sys- tems that typically have very poor sediment quality, tech- niques such as soil amendment could be used to facilitate a more natural interaction between crabs and mangroves in ecosystem development. Introduction The role of positive biotic interactions in inXuencing pro- ductivity is increasingly recognized and may be important in species-poor and physically stressed habitats (reviewed by Bertness and Callaway 1994). For example, positive interactions between plants and their associated fauna may be essential to their growth and survival, where one species ameliorates the immediate environment, reducing or buVer- ing eVects of stressful conditions on the other (Bertness and Leonard 1997; Stachowicz 2001). Numerous studies have shown positive relationships in intertidal marsh habitats (e.g. Kraeuter 1976; Montague 1982; Bertness 1985; Bertness and Leonard 1997; Silliman and Newell 2003). These studies, however, focus primarily on temperate salt marshes dominated by Spartina species. Despite the fact that mangroves dominate at least one-quarter of the world’s tropical coastlines (Chapman 1975; Alongi 2002), provide critical nursery habitats for commercially and ecologically important species (Sheridan and Hays 2003; Nagelkerken et al. 2008), and act as shoreline stabilizers (Carlton 1974), comparatively little attention has been paid to the role of biological interactions on mangrove growth and production, although mangroves often occupy physi- cally stressful habitats that can limit their growth and distri- bution (Macnae 1968; Lugo and Snedaker 1974). Further, Communicated by J. P. Grassle. N. F. Smith (&) · C. Wilcox · J. M. Lessmann Galbraith Marine Science Laboratory, Eckerd College, 4200 54th Avenue South, St. Petersburg, FL 33711, USA e-mail: [email protected] Present Address: C. Wilcox Cell and Molecular Biology, University of Hawaii at Manoa, 651 Ilalo Street, Honolulu, HI 96813, USA
Transcript of Fiddler crab burrowing aVects growth and production of the white
227_2009_1253_Article 1..12Mar Biol
DOI 10.1007/s00227-009-1253-7
ORIGINAL PAPER
Fiddler crab burrowing aVects growth and production of the white mangrove (Laguncularia racemosa) in a restored Florida coastal marsh
Nancy F. Smith · Christie Wilcox · Jeannine M. Lessmann
Received: 1 December 2008 / Accepted: 26 June 2009 © Springer-Verlag 2009
Abstract Positive plant–animal interactions are impor- tant in community ecology, but relatively little attention has been paid to their eVect on the production of mangroves, dominant halophytic trees in tropical coastal marshes. Here, the role of Wddler crab (Uca spp.) burrowing on the growth and production of the white mangrove, Laguncularia racemosa (<2 years old), was examined in a restored marsh in Tampa Bay, Florida (27°41.65 N, 82°30.34 W) with manipulative experiments from June 2006 to May 2007. Fiddler crab burrowing signiWcantly increased mangrove height by 27%, trunk diameter by 25%, and leaf production by 15%, compared to mangroves in crab exclusion enclo- sures. Additionally, the exclusion of Wddler crabs signiW- cantly increased interstitial water salinity from 32.4 to 44.2, and decreased the oxidation–reduction potential of the low organic sediments, but did not aVect soil pH or sulWde con- centration. Mangrove height, trunk diameter, and leaf pro- duction along a transect that varied in crab burrow density were positively associated with the number of crab bur- rows. Further, the density of sympatric Spartina alterniXora shoots was positively correlated with crab burrow density along the transect. As in temperate marshes, Wddler crabs can have signiWcant ecological eVects on mangrove communities, serving as ecological engineers by modulat-
ing the amount of resources available to marsh plants, and by altering the physical, chemical, and biological state of these soft sediment communities. In restored coastal sys- tems that typically have very poor sediment quality, tech- niques such as soil amendment could be used to facilitate a more natural interaction between crabs and mangroves in ecosystem development.
Introduction
The role of positive biotic interactions in inXuencing pro- ductivity is increasingly recognized and may be important in species-poor and physically stressed habitats (reviewed by Bertness and Callaway 1994). For example, positive interactions between plants and their associated fauna may be essential to their growth and survival, where one species ameliorates the immediate environment, reducing or buVer- ing eVects of stressful conditions on the other (Bertness and Leonard 1997; Stachowicz 2001). Numerous studies have shown positive relationships in intertidal marsh habitats (e.g. Kraeuter 1976; Montague 1982; Bertness 1985; Bertness and Leonard 1997; Silliman and Newell 2003).
These studies, however, focus primarily on temperate salt marshes dominated by Spartina species. Despite the fact that mangroves dominate at least one-quarter of the world’s tropical coastlines (Chapman 1975; Alongi 2002), provide critical nursery habitats for commercially and ecologically important species (Sheridan and Hays 2003; Nagelkerken et al. 2008), and act as shoreline stabilizers (Carlton 1974), comparatively little attention has been paid to the role of biological interactions on mangrove growth and production, although mangroves often occupy physi- cally stressful habitats that can limit their growth and distri- bution (Macnae 1968; Lugo and Snedaker 1974). Further,
Communicated by J. P. Grassle.
N. F. Smith (&) · C. Wilcox · J. M. Lessmann Galbraith Marine Science Laboratory, Eckerd College, 4200 54th Avenue South, St. Petersburg, FL 33711, USA e-mail: [email protected]
Present Address: C. Wilcox Cell and Molecular Biology, University of Hawaii at Manoa, 651 Ilalo Street, Honolulu, HI 96813, USA
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mangrove restoration has become a common global activity and there is a need to integrate applied research in coastal restoration and management (Michener 1997; Weinstein 2007). Improving our understanding of the factors that determine initial pathways of site development is critical to improving restoration eVorts, and facilitative relationships, such as that between crabs and mangroves, can be addressed in restored systems, not just natural ones.
Tropical mangrove forests occupy a similar ecological niche as temperate Spartina spp. salt marshes (Mendels- sohn and McKee 2000; Bird 2008) and are habitats for Uca species. In central and south Florida (and other parts of the Gulf of Mexico), mangroves, though dominant, are often sympatric at intertidal elevations with S. alterniXora (Patt- erson et al. 1997; Lewis 2006), where the cordgrass plays a signiWcant ecological role as a nurse plant in mangrove primary succession by stabilizing sediments and trapping propagules (Lewis 2006). With predicted climate modera- tion (reduced hard freezes and increases in air temperature of 1.4–5.8°C by 2100) (USGCRP 2002), there is concern that mangroves are expanding beyond their current range at the expense of Spartina spp. marshes (McKee and Rooth 2008; Perry and Mendelssohn 2009). It will be useful to understand the role of plant–faunal interactions in inXuenc- ing mangrove productivity as has been done in the more thoroughly studied Spartina spp. communities.
Most studies have focused on the role of physical factors, particularly nutrients and salinity, on mangrove growth and metabolism (McKee et al. 1988; Day et al. 1996; Feller et al. 2003; Rivera-Monroy et al. 2004) but mangrove-asso- ciated fauna also play a role. For example, Ellison et al. (1996) found that root-fouling sponges increased mangrove root production and served as facultative mutualists. In con- trast, burrowing isopods and encrusting barnacles signiW- cantly reduced prop root growth of the red mangrove, Rhizophora mangle (Perry 1988). Given their high abun- dance and well-known bioturbating activities, Wddler crabs have the potential to inXuence and regulate mangrove pro- duction like their counterparts in temperate marshes (Smith et al. 1991; Cannicci et al. 2008; Kristensen 2008). Recent work by Anson Hines (Smithsonian Environmental Research Center) and Keiji Wada (Nara Women’s Univer- sity) (unpublished data) in a mangrove marsh in Florida (USA) showed that experimental removal of Wddler crabs from enclosed plots that contained established black man- groves (Avicennia germinans) caused a signiWcant decrease in mangrove survivorship after 2 years. Although the mech- anism is unclear, their work showed that Wddler crabs signiWcantly inXuenced tree survivorship, and potentially, the productivity of mangrove habitats.
Fiddler crabs (Uca spp.) are among the most abundant organisms in salt marsh and mangrove habitats, with densi- ties frequently exceeding 50 crabs m¡2 (Bertness and
Miller 1984; McCraith et al. 2003). In Spartina spp. marshes, crab burrowing (up to 15–20 cm deep; Allen and Curran 1974) can signiWcantly alter plant biomass at inter- mediate tidal heights (Montague 1982; Bertness 1985) due to a combination of several belowground changes, such as increased soil nutrients, oxygenation, decomposition and percolation rates; or decreased salinity and sulWdes (Howes et al. 1981; Montague 1982; Bertness 1985; Gribsholt et al. 2003).
Because of the critical roles of sulWdes and salinity in mangrove growth (particularly in young plants), as well as their potential alteration by crab burrowing, these variables were assessed in this study. Fiddler crab burrowing pro- motes soil aeration and can thus oxidize hydrogen sulWde, which may inhibit plant growth by aVecting the plant’s energy production, growth, and nitrogen uptake (Howarth and Teal 1979; Bradley and Morris 1990; Koch et al. 1990; Wiessner et al. 2005). Mangroves (McKee 1993; Holmer et al. 1994) and Spartina spp. (Koch and Mendelssohn 1989; Lee 2003) can adapt to sulWde by oxidizing the toxin within their rhizospheres. Limited research has shown high sulWde levels can reduce the growth of mangrove seedlings, likely through stomatal closure and reduced gas exchange (Youssef and Saenger 1998). However, this adaptation has not been well documented for young mangroves (McKee 1993). Crab burrowing can also reduce salinity (Montague 1982) by increasing water Xow through sediments. Salinity has been shown to aVect the productivity and growth of mangroves (McKee 1993; Sylla et al. 1996; Twilley and Chen 1998).
Of the three mangrove species occurring in Florida, Laguncularia racemosa is the Wrst to recruit into newly opened Florida coastal marshes (Chen and Twilley 1998; Berger et al. 2006; Lessmann, personal observation) and may often dominate the marsh plain for the Wrst several years of site development (Lessmann, personal observation). The pres- ent study provided an opportunity to increase our knowl- edge of this understudied species, especially during primary succession in mangrove communities.
We examined the inXuence of Wddler crab burrowing on the growth of white mangroves, L. racemosa (<2 years old), in a restored marsh at Cockroach Bay Aquatic Pre- serve, Hillsborough County, Florida, USA. The hypothesis that Wddler crab burrowing facilitates mangrove growth was tested with (1) manipulative experiments in which Wddler crabs were removed and excluded from interacting with white mangroves in enclosures, and (2) by testing the association between mangrove production and Wddler crab burrow density along an established transect. Concurrently, we measured soil edaphic factors (sulWde concentration, pH, salinity, and redox potential) to determine whether Wddler crab burrowing alters the chemical state of marsh sediments, thereby aVecting growth and production.
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Study site
A newly restored marsh at the Cockroach Bay Aquatic Pre- serve in Florida, USA (27°41.65 N, 82°30.34 W), managed by the Department of Hillsborough Parks and Recreation, provided an opportunity to study the eVect of Wddler crab burrowing on early mangrove growth and production. Con- sisting of approximately 283 hectares, this county preserve was established in 1993 to restore upland and marine habi- tat loss due to agriculture and to mitigate eutrophication by removing anthropogenic nutrients (FDEP 1987; TBEP 1996) through wetland Wltration (Mitsch and Gosselink 1993; Wiessner et al. 2005; Gonzalias et al. 2007). During 2004 and 2005, parts of the preserve were restored by the Southwest Florida Water Management District to its ‘pre- farming’ state. The upper 1-m layer of soil in the farm Welds was removed and tidal creeks installed to establish intertidal elevation and wetland hydrological conditions, followed by the hand-planting of thousands of Spartina alterniXora and S. patens plugs at 2-m spacing within the low marsh, along dredged, engineered tidal channels.
The restored marsh was connected to Tampa Bay in October 2005, allowing for ambient tidal exchange between the marsh and estuary, and the natural recruitment of plants and animals. Immediately after tidal connection, two species of detritivorous Wddler crabs, Uca rapax and Uca pugilator, readily colonized the restored habitat in great abundance, while thousands of seedlings of the white man- grove, L. racemosa (L.) Gaertn f. (Combretaceae), naturally recruited into the restored mudXats and low marsh.
We initiated data collection in our transect survey and exclusion experiment in June 2006, approximately 8 months after the restored marsh at Cockroach Bay Aquatic Preserve was connected to Tampa Bay (October 2005), and thus, we assumed all mangroves within our study area were no more than 8 months old.
Field transect survey
We established a permanent 60-m transect parallel (within 5 m) to a tidal channel at an elevation that was Xooded during MHW, but not during MLW (maximum range of about 1 m), and was equally inXuenced by semidiurnal tides along its length. The transect varied in Wddler crab burrow density allowing us to evaluate the relationship between mangrove production and Wddler crab abundance. Along the transect, production of 20 randomly selected white mangroves (L. racemosa) that naturally recruited to the study area, all similarly sized with unbranched shoots (Wrst order) and sepa- rated by at least 2 m, was monitored beginning in June 2006 every 3–6 weeks for 11 months (11 sample periods). Each
mangrove was marked with non-toxic acrylic paint at the base of the trunk as a standard reference point, and growth was estimated by measuring changes in height (cm) from the paint mark to the apical tip using a meter stick placed perpen- dicular to the ground. Mangrove basal trunk diameter (mm) was estimated at the paint mark using digital calipers. We also counted the number of live attached leaves per man- grove (leaf production) as an additional indicator. Leaf counts did not account for mortality between sampling peri- ods. The above measurements are standard, non-destructive methods of measuring plant production (e.g. Saintilan 1998).
Fiddler crab and S. alterniXora shoot densities for each sample period were estimated by counting the number of crab burrows and plant shoots, respectively, in a 0.25-m2
quadrat placed during sampling with the mangrove in the center. Crab burrow density has been shown to be a signiW- cant predictor of Wddler crab abundance (Warren 1990; Skov and Hartnoll 2001; Skov et al. 2002). Since the burrows of U. pugilator and U. rapax are diYcult to distinguish, and these crabs spent most of the time in their burrows during our measurements, we were not able to distinguish which species of Wddler crab was present in each quadrat.
Means § SE (n = 20) for mangrove height, trunk diame- ter, number of attached leaves, as well as S. alterniXora shoot and crab burrow densities were calculated per sample period and compared among sample periods by a repeated measures analysis of variance (ANOVA). Since marsh plant and crab burrow density are known to be positively correlated (Nomann and Pennings 1998), we tested for the strength of this association with a Pearson’s correlation coeYcient. To determine the relationship between man- grove production and crab burrow density, and between mangrove production and S. alterniXora shoot density, we performed stepwise forward multiple-regression analyses with crab burrow and S. alterniXora shoot density as pre- dictor variables for mangrove height, trunk diameter, and leaf production (number of attached leaves).
Fiddler crab exclusion experiment
To determine the eVect of Wddler crab burrowing on man- grove production, we initiated a crab removal experiment in April 2006. Mangroves were selected by identifying L. racemosa seedlings at least 2 m from their nearest neigh- bors, of similar height, unbranched, and with a minimal amount of surrounding vegetation, all at a parallel elevation to a tidal channel (within 5 m) that was Xooded during MHW, but not during MLW. Fifteen 1-m2 open-topped enclosures made of 4.0-mm Vexar screening and framed by 1.9-cm PVC, were then installed around each of 15 man- grove seedlings. The enclosure walls extended 25 cm below and above the sediment surface to prevent crabs from enter- ing. After installation and within all 15 enclosures (control
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and exclusion) we removed as many Wddler crabs as possi- ble from the surface by hand. All Xora (except the young mangrove in the center of the enclosure) were removed from the enclosures over a 2-week period to reduce any potential confounding eVects of these other plant species (primarily S. alterniXora) on mangrove production. We also removed any marsh plants within the 0.5-m band around each enclosure (1.5 m from the white mangrove).
After 1 month of recovery, enclosures were randomly assigned to one of two groups: control and exclusion. For the control group (n = 7), we covered the top PVC frame with the Vexar mesh to allow the Wddler crabs to climb over the PVC barrier and access the enclosure. The smooth PVC barrier of the other eight enclosures reduced their ability to climb over the enclosure (personal observation). Any Wddler crab sighted in an exclusion enclosure was captured on the sediment surface so that the sediment was not dis- turbed. When juvenile crabs began recruiting (·4.0 mm) in July 2006, a Wberglass layer (0.50 mm diameter window screening) was added to the sides of the exclusion enclo- sures. This layer covered the exterior of the Vexar mesh from the sediment surface to the PVC frame. To avoid dis- turbing the sediment, we removed juvenile crabs with a cordless hand-held Black and Decker vacuum. Prior to the start of the experiment, we veriWed that there were no sig- niWcant diVerences in height, diameter, and leaf abundance between the mangroves in the control and exclusion enclo- sures using a Student t test (see “Results”).
In June 2006, we began our measurements (every 3– 6 weeks) over the next 11 months (11 sampling periods). We counted the number of crab burrows in each enclosure as an estimate of crab density. We estimated mangrove pro- duction for each enclosed mangrove by measuring tree height (cm), trunk diameter (mm), and number of attached leaves using the same methods as in the transect survey.
Means § SE were calculated for each dependent variable per sample period. Our experimental data were then analyzed statistically using a two-way repeated measures ANOVA with date (monthly sampling) and enclosure (control, exclu- sion) as independent variables on the following repeated measures: mangrove height, trunk diameter, number of leaves, and number of crab burrows. We used the PROC GLM (general linear model) procedure in Statistical Analyti- cal Software, version 8.2 (SAS Institute, Cary, NC) for all ANOVA tests since we had an uneven number of replicates in the control (n = 7) and exclusion (n = 8) enclosures. Com- parisons between transect and control enclosure initial and Wnal mean tree heights were made using Student t tests.
Hydroedaphic factors
To assess the eVect of Wddler crab burrowing on marsh sed- iment, several hydroedaphic factors were measured inside
all enclosures, including: pH, salinity, and sulWde concen- tration, similar to methods described in McKee et al. (1988), as well as oxidation–reduction potential (redox) (Eh). No measurements were taken outside the enclosures.
Every sample period, interstitial water samples were col- lected at least 15 cm within the walls for each control (n = 7) and exclusion (n = 8) enclosure using a perforated metal probe wrapped in several layers of cheesecloth to Wlter out sediment and debris. The probe and cheesecloth, attached to clear plastic, Xexible tubing (1-cm diameter), were pressed into the soil to a depth of 15 cm and water was drawn out of the soil using the suction of a 30-ml syringe. A three-way valve between the syringe and tubing allowed any air to be expelled. The Wrst 5 ml of interstitial water was discarded to remove any oxidized water in the tube and any debris and sediment that may have entered as a result of forcing the metal probe into the soil.
Aliquots (»5 ml) of interstitial water were collected and returned to the lab on ice for salinity measurements using a refractometer and for pH using a standardized electrode (Orion model 720A). Additionally, a 5-ml aliquot of inter- stitial water was Wxed in the Weld with antioxidant buVer (1.56 M sodium salicylate, 2.13 M sodium hydroxide, 0.37 M ascorbic acid; 1:1 dilution) and stored on ice until returned to the lab. The Wxed samples were measured within 12 h for total soluble sulWde (H2S, HS¡, S¡2) (mM) using a silver/sulWde electrode. A sulWde standard curve was constructed using a series of Na2S solutions prepared prior to analysis with the same antioxidant buVer.
We measured redox potentials (Eh) at 1- and 10-cm depths using four sets (subsamples) of brightened platinum electrodes within each enclosure, approximately 25 cm from both the mangrove and enclosure wall. Platinum elec- trodes were calibrated in quinhydrone at pH 4 (+218 § 5 mV at 25°C) 1 day prior to measurements. The potential of a calomel reference electrode (+244 mV) was added to each measurement.
Means § SE were calculated for salinity, pH, sulWde con- centration, and redox potential (four subsamples at 1 and 10 cm) between control and exclusion enclosures over the entire 11-month period, with mean comparisons between control and exclusion enclosures made using Student t tests.
Results
Field transect survey
During the Weld transect surveys from June 2006 to May 2007, mangrove height signiWcantly increased (df = 10, F = 56.20, P < 0.0001; Fig. 1a) from its initial height of 34.0 § 2.08 cm. After approximately 5 months (126 days), the increase in mangrove height began to slow, coinciding
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with the fall months of October and November (Fig. 1a), and Wnally reached a mean height nearly double that at the start (65.1 § 3.6 cm). Basal trunk diameter also signiW- cantly increased (approximately 2.75 times) during the study period (df = 10, F = 157.98, P < 0.0001; Fig. 1b), as did leaf production (approximately 3.5 times) (df = 10, F = 24.89, P < 0.0001; Fig. 1c). These latter two parame- ters also slowed after 126 days, but to a lesser extent than the slowing observed in height.
Spartina alterniXora shoot density signiWcantly increased over time (df = 10, F = 8.85, P < 0.0001; Fig. 2a), as did crab burrow density (df = 10, F = 11.30, P < 0.0001; Fig. 2b). Mean S. alterniXora shoot and crab burrow density at the beginning of the study were both only 40% of their values at the end of the study. After 6 months (161 and 191 days), we found a slight decrease in S. alter- niXora shoot density (Fig. 2a), which we attribute to marsh senescence, a pattern frequently observed during cold months (e.g. Baerlocher and Moulton 1999). However, by the end of the study period, S. alterniXora and crab burrow density had nearly tripled (Fig. 2). Both variables were sig- niWcantly correlated with each other (r = 0.43, P < 0.0001).
In individual 0.25 £ 0.25-m quadrats along the 60-m transect, mangrove height was positively associated with the density of crab burrows, which explained 24% of the variance in height, and S. alterniXora shoot density explained only a minor portion (5%) of the total variance in mangrove height (Table 1). The density of crab burrows had the strongest positive eVect on trunk diameter (Table 1) (R2 = 0.29, P < 0.0001). S. alterniXora explained an
Fig. 1 Mean (§SE) a height (cm), b trunk diameter (mm), and c num- ber of leaves of young white mangroves (Laguncularia racemosa) since initiation of study in June 2006 for each sample period (n = 20) over 11 months along an established transect
Fig. 2 Mean density (§SE) of (a) Spartina alterniXora and (b) Wddler crab burrows 0.25 m¡2 for each sample period (n = 20) over 11 months beginning June 2006 along an established transect. Plant and burrow density were signiWcantly correlated (r = 0.43, P < 0.0001)
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additional 5% of the variation in mangrove trunk diameter (Table 1). Leaf production was positively associated with crab burrow density, and weakly with S. alterniXora shoot density (Table 1).
Fiddler crab exclusion experiment
Two weeks after initiating crab removals, we immediately noticed a diVerence in mean burrow density. The exclusion enclosures (7.38 § 5.73 m¡2) had burrow densities 27% lower than the control enclosures (27.57 § 18.8 m¡2). The position of crab burrows constantly changed throughout the experiment, suggesting that burrows were collapsing and Wlling during incoming tides, or that they were being plugged by the crabs. Frequent changes in burrow Wlling and excavation likely resulted from the low amount of organic matter in the marsh sediment, which has been shown to help maintain burrows (Bertness 1985). Ulti- mately, removal and exclusion of Wddler crabs signiWcantly reduced burrow density by 57% in the exclusion enclosure (13.34 § 1.78 m¡2) compared to the control enclosures (30.81 § 2.61 m¡2) over the 11-months study (df = 1, F = 10.73, P < 0.01). Crabs moving and burrowing into the marsh surface were predominately U. pugilator, but we occasionally observed a few U. rapax deposit-feeding on or near the transect and within enclosures. Prior to crab remo- vals, we found no signiWcant diVerence in height (df = 13, t = 1.74, P = 0.10), diameter (df = 13, t = 1.32, P = 0.21) and leaf abundance (df = 13, t = 1.59, P = 0.14) between mangroves in exclusion and control enclosures.
Removal and exclusion of Wddler crabs had a signiWcant eVect on mangrove growth by the second month (evident after 45 days) (Table 2; Fig. 3a). Trees in the control enclo- sures grew on average 27% taller than mangroves in crab exclusion enclosures during the study. Fiddler crabs also had a signiWcant eVect on trunk diameter by the end of the study (Fig. 3b), with mangroves in the control (26.20 § 1.41 mm) growing trunks that were a signiWcant 25% greater than those for mangroves in exclusion enclo- sures (21.03 § 1.95 mm) (Table 2). The production of leaves increased over time and was signiWcantly higher in the control than in the exclusion enclosures throughout the experiment (Table 2; Fig. 3c), Wnally producing 15% more
leaves by the end of the study. Averaged across sampling periods, mangroves in the control enclosures produced 226.8 (§10.71) leaves tree¡1 compared to mangroves in the exclusion enclosures (179.0 § 10.81 leaves tree¡1).
We also found marked diVerences in mangrove produc- tion at the end of the study between trees along the transect and those that grew concurrently in the control enclosures. After 11 months, mangroves in control enclosures grew taller (77.2 § 4.9 cm), wider (26.2 § 1.4 mm) and pro- duced more leaves (318.4 § 21.6) (Fig. 3) than those along the transect (65.1 § 3.6 cm tall, 18.1 § 1.0 mm wide, 145.3 § 14.6 leaves) (Fig. 1). Comparisons of tree heights at the initiation of the experiment revealed that the trees in the control enclosures (47.8 § 4.32 cm) were signiWcantly taller than those along the transect (34.0 § 2.08 cm) (df = 25, t = 3.20, P = 0.004).
Crab burrow densities also diVered between the transect and nearby control enclosures, but showed a diVerent pattern. On average, burrow densities along the transect measured 47.93 § 0.66 m¡2 over the study period, higher than burrow densities within control enclosures (30.81 § 2.61 m¡2). By the end of the study (day 330), crab burrow densities reached 73.2 § 2.09 m¡2 along the tran- sect (Fig. 2b), nearly 50% higher than burrow densities in control enclosures (49.0 § 7.49 m¡2).
Hydroedaphic factors
Fiddler crab activity had a marked eVect on soil interstitial salinity (Fig. 4a), with the mean value in exclusion enclo- sures (44.2 § 0.99) 36% higher than that in the control enclosures (32.4 § 1.04) (df = 131, t = 8.21, P < 0.001).
Table 1 Percentage of variation in mangrove production (partial R2
values from stepwise multiple regression analysis) explained by Wddler crab burrow density and Spartina alterniXora shoot density in the Weld transect survey
* P < 0.001, ** P < 0.0001
Factor Height Trunk diameter Leaf production
Crab burrow density 0.24* 0.29** 0.16**
Marsh plant density 0.05* 0.05* 0.02
Table 2 Results of two-way repeated measures ANOVA on eVects of time (sample periods) and enclosure (control, exclusion) on Laguncu- laria racemosa height (cm), trunk diameter (mm) and leaf production (number leaves/tree) during the exclusion experiment
Field study was conducted at Cockroach Bay Aquatic Preserve, Hills- borough County, Florida, USA
Source of variation df SS F P
Height
Time £ enclosure 10 352.11 1.51 0.143
Diameter
Time £ enclosure 10 111.30 5.86 <0.001
Leaf production
Time £ enclosure 10 8,039.05 0.61 0.803
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In contrast, there was no signiWcant diVerence in the pH of interstitial water between control and exclusion enclosures (df = 132, t = 0.31, P = 0.76; Fig. 4b).
SulWde concentrations (mM) in the control and exclusion enclosures were not signiWcantly diVerent (df = 117, t = 1.13, P = 0.26; Fig. 5a) and concentrations were quite
low compared to natural marsh systems (Carlson et al. 1983; McKee et al. 1988). One sulWde sample taken in June 2006 from an exclusion enclosure had an abnormally high value (0.36 mM) compared to all other samples, and was excluded from the statistical analysis above. When included, there was still no signiWcant diVerence in sulWde between control and exclusion enclosures (df = 118, t = 0.91, P = 0.37).
The redox potential of the marsh substrate diVered between control and exclusion enclosures (Fig. 5b), with redox levels signiWcantly lower in exclusion than control enclosures for both 1-cm (df = 107, t = 2.11, P = 0.04) and 10-cm (df = 107, t = 4.11, P < 0.0001) depths. Within the exclusion enclosures, the redox potential was signiWcantly lower at a depth of 10 cm than at 1 cm (df = 116, t = 3.83, P < 0.001); and similarly, redox was slightly lower, but not signiWcantly so, at 10 cm that at 1 cm for the control enclo- sures (df = 98, t = 1.97, P = 0.05).
Discussion
As in temperate marshes, Wddler crabs in mangrove com- munities can have a signiWcant eVect on plant production and substrate characteristics. In our restored marsh, Wddler crab burrowing increased Wnal tree height by 27%, Wnal basal trunk diameter by 25%, and Wnal leaf production by 15% over mangroves growing where crabs were removed and excluded. We also observed signiWcant positive associ- ations between mangrove production and crab burrow den- sity along our transect. Crab burrows accounted for 24, 29, and 16% of the variation in mangrove height, trunk diame- ter, and leaf production, respectively. S. alterniXora grow- ing around the white mangroves accounted for only a minor part of the variation (·5%).
We observed that the increase in height of white man- grove began to slow at the onset of the fall season, but basal trunk diameter continued to increase. Meyers and Ewel (1990) showed that L. racemosa has extensive shoot growth in the summer and winter shoot inactivity. This may also reXect that these young plants may allocate energy to developing a wider base to support subsequent increases in height.
In addition, we counted live leaves as a measure of mangrove growth, but did not assess leaf litter (leaves, twigs, bark), which is often used to assess tree productiv- ity. In Florida, litterfall is continuous throughout the year, with minor peaks before the wet season and after periods of high stress. Given the long life of mangrove leaves (Gill and Tomlinson 1977), relatively consistent leaf shedding, and relatively low levels of environmental stress (low sulWde and elevated Eh) at our study site, leaf counts appear to be a good indicator of growth, particularly
Fig. 3 Mean (§SE) a height (cm), b trunk diameter (mm), and c num- ber of leaves tree¡1 in Wddler crab exclusion (Wlled circle) (n = 8) and control (open circle) (n = 7) enclosures since initiation of experiment in June 2006 for each sample period over 11 months
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in conjunction with measures of tree height and girth (Meyers and Ewel 1990).
When comparing production between mangroves along the transect with trees in control enclosures after 11 months, mangroves in control enclosures grew taller, wider, and produced more leaves than mangroves along the transect. We attribute this to diVerences in initial tree size with the mean height of the control mangroves being sig- niWcantly greater than the transect mangroves at the start of the study. It was not our intention to make direct compari- sons between the experiment and transect survey as slightly diVerent criteria were used in setting them up. In particular, mangroves in all of the enclosures were selected for their low proximity to other plants (to minimize soil disturbance by the initial removal of all macrophytes), while the tran- sect mangroves were not.
This signiWcant diVerence in initial and Wnal heights of transect and control enclosure mangroves also suggests that removal of adult S. alterniXora at the initiation of the experiment may have reduced competition with mangrove seedlings for limiting resources such as nutrients and light. López-HoVman et al. (2006) demonstrated that net photo-
synthesis, growth, and survivorship in mangrove seedlings increased with increased light availability (provided by our removal of S. alterniXora) at lower but not higher salinities. Increased light availability to young mangroves could not overcome potential limitations caused by the elevated salin- ities in the exclusion enclosures. Negative eVects of high salinity on seedlings can include reduced stomatal conduc- tance and internal CO2 concentrations, decreased nutrient uptake (particularly nitrogen) (Morris 1980, 1984), or lim- ited water availability, all of which limit productivity.
Moreover, L. racemosa may have shifted biomass alloca- tion to belowground growth (an increase in root to shoot ratio) in the absence of S. alterniXora competition. López- HoVman et al. (2006) have shown increased ratios of mangrove seedling root mass to leaf mass at high salinity (independent of competitor removal). However, S. alterniXora was not removed along the transect and belowground growth was not measured in the experiment or along the transect. Thus, we can not discount that removing all S. alterniXora within 1.5 m of each enclosed mangrove may have inXuenced energy allocation, because mangroves within each enclosure could have experienced reduced resource
Fig. 4 Mean (§SE) a salinity and b pH measured 15 cm below marsh surface for all sample periods over 11 months in Wddler crab exclusion (Wlled circle) (n = 80) and control (open circle) (n = 70) enclosures
Fig. 5 Mean (§SE) a concentration of sulWde (mM) in interstitial wa- ter samples taken 15 cm below marsh surface, and b sediment oxida- tion–reduction (redox) potential (mV) measured 1- and 10-cm below marsh surface in Wddler crab exclusion (Wlled circle) and control (open
circle) enclosures for all sample periods over 11 months. Means with diVerent letters indicate signiWcant diVerence (P < 0.001) in redox between 1- and 10-cm within exclusion enclosures
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competition. Additionally, the removal of S. alterniXora may have reduced crab burrow density in the control enclo- sures since organic debris and belowground tissue of marsh plants is known to support burrows (Bertness 1985).
We also cannot dismiss the possibility that our enclosure experimental design may have contributed to diVerences in tree growth between the control enclosures and transect. For example, enclosure mesh walls may have induced shad- ing, but since the young trees were taller than the enclosure walls (25 cm) and the walls were at some distance from the tree in the center, we consider this unlikely. We also cannot discount that enclosures may have limited the movement of macrofauna other than Wddler crabs. Although the enclo- sures could have aVected tree growth directly, we believe that the initial larger size of enclosure mangroves and the removal of S. alterniXora from the enclosures are likely to have had greater eVects.
Experimental reduction of Wddler crabs in our study (by 43%) markedly reduced interstitial water salinity in control enclosures compared to exclusion enclosures. Reduction in salinity may be due to increased soil drainage as a result of burrowing (Montague 1982; Bertness 1985), with the area of burrow soil exposed to the atmosphere increasing by 12– 59% (Katz 1980; Macintosh 1982). Since mangroves were of similar age and size (<1 m tall, <0.5 m width) and grew in full sun, plant percent cover is unlikely to have impacted soil evaporation rates. Further research is needed to deter- mine whether burrowing can inXuence percolation rates, and thus evaporation rates in marsh sediments (see Stieglitz et al. 2000). Mangroves in the exclusion enclosures, which experienced signiWcantly higher salinity, grew less than mangroves in control enclosures, suggesting that high salin- ity may have a negative eVect on young mangrove growth and production.
On the east coast of central Florida, Lovelock and Feller (2003) found that L. racemosa is less tolerant of highly saline conditions than the sympatric black mangrove, A. germinans, which has higher photosynthetic water-use eYciency where higher soil nitrogen levels are present. However, Cintrón et al. (1978) determined greater salinity tolerance for Gulf of Mexico L. racemosa and A. germinans (salinity 80–90) than for R. mangle (salinity 60–65) and Chen and Twilley (1998) demonstrated a greater salt toler- ance of A. germinans (also dependent upon soil fertility). Relative salt tolerance of mangrove species is highly vari- able and dependent upon the level of other environmental stresses (e.g. low nutrients, increased sulWdes, etc.) (Flow- ers et al. 1977). We did not assess the eVect of increased soil salinity on species other than L. racemosa, as they had not signiWcantly recruited to our site. Although adult L. racemosa has shown tolerance to hypersalinity, we suggest that the signiWcant but modest hypersalinity (44) within our exclusion enclosures (and removal of S. alterniXora) had a
negative eVect on the growth of the very young mangroves, in contrast to those growing in lower salinities (32).
The redox potential of the marsh substrate also diVered between crab exclusion and control enclosures at 1- and 10- cm depths, demonstrating that Wddler crab burrowing can increase soil redox, a feature that has also been observed in temperate salt marshes (Bertness 1985). Our redox levels (Eh) were relatively high compared to the Eh values reported by McKee et al. (1988) for similar depths in man- grove substrates. Their soil redox values demonstrated highly reduced sediment conditions, with Eh ranging from ¡168 to ¡204 mV in unvegetated sites and ¡45 to ¡161 mV in sites with mangrove pneumatophores, well within the range for sulWde production.
Compared to the undisturbed and mature mangrove marsh studied by McKee et al. (1988) in Belize, the sedi- ments at our restored marsh in Cockroach Bay were highly impacted as a result of decades of farming, and more recently, the restoration of farm Welds and nearby shell-min- ing pits into marsh habitat. During restoration, grading and dredging of the upper surface layers left behind very sandy soils with coarse carbonates (mostly in the form of mollusc shells) and very little organic matter. High sand content and low marsh peat most likely reduces water retention and pro- vides less carbon fuel for microbial respiration, resulting in relatively high Eh values. Smart and Barko (1978) found higher redox values for sandy sediments compared to Wne- textured sediments, which is likely to reXect the higher porosity and diVusion of atmospheric oxygen in coarser sed- iments. Given our high redox values, it is not surprising that the sulWde concentrations were quite low compared to those observed in mature marshes (Carlson et al. 1983; McKee et al. 1988). In natural systems, crab burrows and salt marsh plant roots can maintain suYciently high redox levels to prevent accumulation of sulWde to toxic levels in marsh sediment (reviewed by Kristensen 2008). This is further supported by experimental removal of burrowing grapsid crabs of the genus Sesarma in a mangrove marsh in Austra- lia, which caused sulWde and ammonium levels to signiW- cantly increase, resulting in decreased Rhizophora spp. leaf and propagule production (Smith et al. 1991). At our study site, the coarse content of the restored sediment most likely accounts for the low sulWde values, and can not be attributed to crab burrowing, an activity which may be relatively more important in marsh systems with substantial organic matter (e.g. Bertness 1985). The low soil organic content at our Weld site, which normally drives redox functions in healthy natural marshes, is notable. Our data suggest that organic soil amendments should be considered when implementing wetland restoration (Zedler 2000; McDonald 2005).
Restoration of mangrove-dominated wetlands can be followed through the biogeochemistry of the wetland. For example, when sulWdes are high, mangroves will only be
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able to oxidize their rhizospheres to a certain degree, and then they begin to senesce. SpeciWcally, sulWdes bind with enzymes in the electron transport chain and decrease the eYciency of anaerobic metabolism (Koch and Mendels- sohn 1989; Koch et al. 1990). Since energy is used in nutri- ent uptake, sulWdes indirectly aVect the amount of nutrients taken up. Hypoxia causes plants to switch to alcoholic fermentation which decreases productivity (Koch and Mendelssohn 1989; Koch et al. 1990). Since sulWdes accu- mulate in areas of hypoxia and anoxia, they can indicate problems with hydrology. If the water in the wetland does not Xush, sulWdes will accumulate. In this respect, sulWdes can be an indicator of failed or failing restoration (McKee and Faulkner 2000).
Crab bioturbation has long been suggested to inXuence mangrove production (Smith et al. 1991), since Wddler crabs are conspicuous and abundant in most mangrove for- ests (Salmon 1967; Macnae 1968). Accumulating evidence suggests that Wddler crabs can have signiWcant ecological eVects on salt marsh and mangrove communities. Through their bioturbating activities, Wddler crabs can directly or indirectly modulate the resources available to marsh plants by modifying the biogeochemical state of soft sediments (Gribsholt et al. 2003), subsequently inXuencing their pro- ductivity. For example, active transport of marsh sediment can inXuence the movement of water and oxidants in and out of a patch of marsh or burrow, thus determining the abi- otic conditions of salinity and oxygenation. Because crabs are unevenly distributed and vary in density across a marsh, the movement or Xow of water, oxidants, and other materi- als is likely to vary spatially, resulting in variation in plant production. Kristensen (2008) argued that Wddler crabs are ecosystem engineers in the overall ecology of mangrove marshes (see Jones et al. 1994; Gutiérrez and Jones 2006). Identifying the ways in which mangrove-associated macro- fauna change sediment biogeochemistry is necessary to fully understand how primary production is regulated in mangrove ecosystems.
Acknowledgments We would like to thank Richard Sullivan, man- ager of the Cockroach Bay Aquatic Preserve for access to the restored marsh, and Allie Wilkinson and Courtney Nosach for their generous laboratory and Weld assistance. Comments and discussions with every- one directly involved, and with Randy Runnels and Brandt Henning- sen, were extremely helpful. We would like to thank the associate editor and anonymous reviewers for their valuable comments. This project was funded by a Sigma Xi Grant-in-Aid of Research to C. Wil- cox and by the Natural Sciences Summer Research Program at Eckerd College.
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Abstract
Introduction
DOI 10.1007/s00227-009-1253-7
ORIGINAL PAPER
Fiddler crab burrowing aVects growth and production of the white mangrove (Laguncularia racemosa) in a restored Florida coastal marsh
Nancy F. Smith · Christie Wilcox · Jeannine M. Lessmann
Received: 1 December 2008 / Accepted: 26 June 2009 © Springer-Verlag 2009
Abstract Positive plant–animal interactions are impor- tant in community ecology, but relatively little attention has been paid to their eVect on the production of mangroves, dominant halophytic trees in tropical coastal marshes. Here, the role of Wddler crab (Uca spp.) burrowing on the growth and production of the white mangrove, Laguncularia racemosa (<2 years old), was examined in a restored marsh in Tampa Bay, Florida (27°41.65 N, 82°30.34 W) with manipulative experiments from June 2006 to May 2007. Fiddler crab burrowing signiWcantly increased mangrove height by 27%, trunk diameter by 25%, and leaf production by 15%, compared to mangroves in crab exclusion enclo- sures. Additionally, the exclusion of Wddler crabs signiW- cantly increased interstitial water salinity from 32.4 to 44.2, and decreased the oxidation–reduction potential of the low organic sediments, but did not aVect soil pH or sulWde con- centration. Mangrove height, trunk diameter, and leaf pro- duction along a transect that varied in crab burrow density were positively associated with the number of crab bur- rows. Further, the density of sympatric Spartina alterniXora shoots was positively correlated with crab burrow density along the transect. As in temperate marshes, Wddler crabs can have signiWcant ecological eVects on mangrove communities, serving as ecological engineers by modulat-
ing the amount of resources available to marsh plants, and by altering the physical, chemical, and biological state of these soft sediment communities. In restored coastal sys- tems that typically have very poor sediment quality, tech- niques such as soil amendment could be used to facilitate a more natural interaction between crabs and mangroves in ecosystem development.
Introduction
The role of positive biotic interactions in inXuencing pro- ductivity is increasingly recognized and may be important in species-poor and physically stressed habitats (reviewed by Bertness and Callaway 1994). For example, positive interactions between plants and their associated fauna may be essential to their growth and survival, where one species ameliorates the immediate environment, reducing or buVer- ing eVects of stressful conditions on the other (Bertness and Leonard 1997; Stachowicz 2001). Numerous studies have shown positive relationships in intertidal marsh habitats (e.g. Kraeuter 1976; Montague 1982; Bertness 1985; Bertness and Leonard 1997; Silliman and Newell 2003).
These studies, however, focus primarily on temperate salt marshes dominated by Spartina species. Despite the fact that mangroves dominate at least one-quarter of the world’s tropical coastlines (Chapman 1975; Alongi 2002), provide critical nursery habitats for commercially and ecologically important species (Sheridan and Hays 2003; Nagelkerken et al. 2008), and act as shoreline stabilizers (Carlton 1974), comparatively little attention has been paid to the role of biological interactions on mangrove growth and production, although mangroves often occupy physi- cally stressful habitats that can limit their growth and distri- bution (Macnae 1968; Lugo and Snedaker 1974). Further,
Communicated by J. P. Grassle.
N. F. Smith (&) · C. Wilcox · J. M. Lessmann Galbraith Marine Science Laboratory, Eckerd College, 4200 54th Avenue South, St. Petersburg, FL 33711, USA e-mail: [email protected]
Present Address: C. Wilcox Cell and Molecular Biology, University of Hawaii at Manoa, 651 Ilalo Street, Honolulu, HI 96813, USA
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mangrove restoration has become a common global activity and there is a need to integrate applied research in coastal restoration and management (Michener 1997; Weinstein 2007). Improving our understanding of the factors that determine initial pathways of site development is critical to improving restoration eVorts, and facilitative relationships, such as that between crabs and mangroves, can be addressed in restored systems, not just natural ones.
Tropical mangrove forests occupy a similar ecological niche as temperate Spartina spp. salt marshes (Mendels- sohn and McKee 2000; Bird 2008) and are habitats for Uca species. In central and south Florida (and other parts of the Gulf of Mexico), mangroves, though dominant, are often sympatric at intertidal elevations with S. alterniXora (Patt- erson et al. 1997; Lewis 2006), where the cordgrass plays a signiWcant ecological role as a nurse plant in mangrove primary succession by stabilizing sediments and trapping propagules (Lewis 2006). With predicted climate modera- tion (reduced hard freezes and increases in air temperature of 1.4–5.8°C by 2100) (USGCRP 2002), there is concern that mangroves are expanding beyond their current range at the expense of Spartina spp. marshes (McKee and Rooth 2008; Perry and Mendelssohn 2009). It will be useful to understand the role of plant–faunal interactions in inXuenc- ing mangrove productivity as has been done in the more thoroughly studied Spartina spp. communities.
Most studies have focused on the role of physical factors, particularly nutrients and salinity, on mangrove growth and metabolism (McKee et al. 1988; Day et al. 1996; Feller et al. 2003; Rivera-Monroy et al. 2004) but mangrove-asso- ciated fauna also play a role. For example, Ellison et al. (1996) found that root-fouling sponges increased mangrove root production and served as facultative mutualists. In con- trast, burrowing isopods and encrusting barnacles signiW- cantly reduced prop root growth of the red mangrove, Rhizophora mangle (Perry 1988). Given their high abun- dance and well-known bioturbating activities, Wddler crabs have the potential to inXuence and regulate mangrove pro- duction like their counterparts in temperate marshes (Smith et al. 1991; Cannicci et al. 2008; Kristensen 2008). Recent work by Anson Hines (Smithsonian Environmental Research Center) and Keiji Wada (Nara Women’s Univer- sity) (unpublished data) in a mangrove marsh in Florida (USA) showed that experimental removal of Wddler crabs from enclosed plots that contained established black man- groves (Avicennia germinans) caused a signiWcant decrease in mangrove survivorship after 2 years. Although the mech- anism is unclear, their work showed that Wddler crabs signiWcantly inXuenced tree survivorship, and potentially, the productivity of mangrove habitats.
Fiddler crabs (Uca spp.) are among the most abundant organisms in salt marsh and mangrove habitats, with densi- ties frequently exceeding 50 crabs m¡2 (Bertness and
Miller 1984; McCraith et al. 2003). In Spartina spp. marshes, crab burrowing (up to 15–20 cm deep; Allen and Curran 1974) can signiWcantly alter plant biomass at inter- mediate tidal heights (Montague 1982; Bertness 1985) due to a combination of several belowground changes, such as increased soil nutrients, oxygenation, decomposition and percolation rates; or decreased salinity and sulWdes (Howes et al. 1981; Montague 1982; Bertness 1985; Gribsholt et al. 2003).
Because of the critical roles of sulWdes and salinity in mangrove growth (particularly in young plants), as well as their potential alteration by crab burrowing, these variables were assessed in this study. Fiddler crab burrowing pro- motes soil aeration and can thus oxidize hydrogen sulWde, which may inhibit plant growth by aVecting the plant’s energy production, growth, and nitrogen uptake (Howarth and Teal 1979; Bradley and Morris 1990; Koch et al. 1990; Wiessner et al. 2005). Mangroves (McKee 1993; Holmer et al. 1994) and Spartina spp. (Koch and Mendelssohn 1989; Lee 2003) can adapt to sulWde by oxidizing the toxin within their rhizospheres. Limited research has shown high sulWde levels can reduce the growth of mangrove seedlings, likely through stomatal closure and reduced gas exchange (Youssef and Saenger 1998). However, this adaptation has not been well documented for young mangroves (McKee 1993). Crab burrowing can also reduce salinity (Montague 1982) by increasing water Xow through sediments. Salinity has been shown to aVect the productivity and growth of mangroves (McKee 1993; Sylla et al. 1996; Twilley and Chen 1998).
Of the three mangrove species occurring in Florida, Laguncularia racemosa is the Wrst to recruit into newly opened Florida coastal marshes (Chen and Twilley 1998; Berger et al. 2006; Lessmann, personal observation) and may often dominate the marsh plain for the Wrst several years of site development (Lessmann, personal observation). The pres- ent study provided an opportunity to increase our knowl- edge of this understudied species, especially during primary succession in mangrove communities.
We examined the inXuence of Wddler crab burrowing on the growth of white mangroves, L. racemosa (<2 years old), in a restored marsh at Cockroach Bay Aquatic Pre- serve, Hillsborough County, Florida, USA. The hypothesis that Wddler crab burrowing facilitates mangrove growth was tested with (1) manipulative experiments in which Wddler crabs were removed and excluded from interacting with white mangroves in enclosures, and (2) by testing the association between mangrove production and Wddler crab burrow density along an established transect. Concurrently, we measured soil edaphic factors (sulWde concentration, pH, salinity, and redox potential) to determine whether Wddler crab burrowing alters the chemical state of marsh sediments, thereby aVecting growth and production.
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Study site
A newly restored marsh at the Cockroach Bay Aquatic Pre- serve in Florida, USA (27°41.65 N, 82°30.34 W), managed by the Department of Hillsborough Parks and Recreation, provided an opportunity to study the eVect of Wddler crab burrowing on early mangrove growth and production. Con- sisting of approximately 283 hectares, this county preserve was established in 1993 to restore upland and marine habi- tat loss due to agriculture and to mitigate eutrophication by removing anthropogenic nutrients (FDEP 1987; TBEP 1996) through wetland Wltration (Mitsch and Gosselink 1993; Wiessner et al. 2005; Gonzalias et al. 2007). During 2004 and 2005, parts of the preserve were restored by the Southwest Florida Water Management District to its ‘pre- farming’ state. The upper 1-m layer of soil in the farm Welds was removed and tidal creeks installed to establish intertidal elevation and wetland hydrological conditions, followed by the hand-planting of thousands of Spartina alterniXora and S. patens plugs at 2-m spacing within the low marsh, along dredged, engineered tidal channels.
The restored marsh was connected to Tampa Bay in October 2005, allowing for ambient tidal exchange between the marsh and estuary, and the natural recruitment of plants and animals. Immediately after tidal connection, two species of detritivorous Wddler crabs, Uca rapax and Uca pugilator, readily colonized the restored habitat in great abundance, while thousands of seedlings of the white man- grove, L. racemosa (L.) Gaertn f. (Combretaceae), naturally recruited into the restored mudXats and low marsh.
We initiated data collection in our transect survey and exclusion experiment in June 2006, approximately 8 months after the restored marsh at Cockroach Bay Aquatic Preserve was connected to Tampa Bay (October 2005), and thus, we assumed all mangroves within our study area were no more than 8 months old.
Field transect survey
We established a permanent 60-m transect parallel (within 5 m) to a tidal channel at an elevation that was Xooded during MHW, but not during MLW (maximum range of about 1 m), and was equally inXuenced by semidiurnal tides along its length. The transect varied in Wddler crab burrow density allowing us to evaluate the relationship between mangrove production and Wddler crab abundance. Along the transect, production of 20 randomly selected white mangroves (L. racemosa) that naturally recruited to the study area, all similarly sized with unbranched shoots (Wrst order) and sepa- rated by at least 2 m, was monitored beginning in June 2006 every 3–6 weeks for 11 months (11 sample periods). Each
mangrove was marked with non-toxic acrylic paint at the base of the trunk as a standard reference point, and growth was estimated by measuring changes in height (cm) from the paint mark to the apical tip using a meter stick placed perpen- dicular to the ground. Mangrove basal trunk diameter (mm) was estimated at the paint mark using digital calipers. We also counted the number of live attached leaves per man- grove (leaf production) as an additional indicator. Leaf counts did not account for mortality between sampling peri- ods. The above measurements are standard, non-destructive methods of measuring plant production (e.g. Saintilan 1998).
Fiddler crab and S. alterniXora shoot densities for each sample period were estimated by counting the number of crab burrows and plant shoots, respectively, in a 0.25-m2
quadrat placed during sampling with the mangrove in the center. Crab burrow density has been shown to be a signiW- cant predictor of Wddler crab abundance (Warren 1990; Skov and Hartnoll 2001; Skov et al. 2002). Since the burrows of U. pugilator and U. rapax are diYcult to distinguish, and these crabs spent most of the time in their burrows during our measurements, we were not able to distinguish which species of Wddler crab was present in each quadrat.
Means § SE (n = 20) for mangrove height, trunk diame- ter, number of attached leaves, as well as S. alterniXora shoot and crab burrow densities were calculated per sample period and compared among sample periods by a repeated measures analysis of variance (ANOVA). Since marsh plant and crab burrow density are known to be positively correlated (Nomann and Pennings 1998), we tested for the strength of this association with a Pearson’s correlation coeYcient. To determine the relationship between man- grove production and crab burrow density, and between mangrove production and S. alterniXora shoot density, we performed stepwise forward multiple-regression analyses with crab burrow and S. alterniXora shoot density as pre- dictor variables for mangrove height, trunk diameter, and leaf production (number of attached leaves).
Fiddler crab exclusion experiment
To determine the eVect of Wddler crab burrowing on man- grove production, we initiated a crab removal experiment in April 2006. Mangroves were selected by identifying L. racemosa seedlings at least 2 m from their nearest neigh- bors, of similar height, unbranched, and with a minimal amount of surrounding vegetation, all at a parallel elevation to a tidal channel (within 5 m) that was Xooded during MHW, but not during MLW. Fifteen 1-m2 open-topped enclosures made of 4.0-mm Vexar screening and framed by 1.9-cm PVC, were then installed around each of 15 man- grove seedlings. The enclosure walls extended 25 cm below and above the sediment surface to prevent crabs from enter- ing. After installation and within all 15 enclosures (control
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and exclusion) we removed as many Wddler crabs as possi- ble from the surface by hand. All Xora (except the young mangrove in the center of the enclosure) were removed from the enclosures over a 2-week period to reduce any potential confounding eVects of these other plant species (primarily S. alterniXora) on mangrove production. We also removed any marsh plants within the 0.5-m band around each enclosure (1.5 m from the white mangrove).
After 1 month of recovery, enclosures were randomly assigned to one of two groups: control and exclusion. For the control group (n = 7), we covered the top PVC frame with the Vexar mesh to allow the Wddler crabs to climb over the PVC barrier and access the enclosure. The smooth PVC barrier of the other eight enclosures reduced their ability to climb over the enclosure (personal observation). Any Wddler crab sighted in an exclusion enclosure was captured on the sediment surface so that the sediment was not dis- turbed. When juvenile crabs began recruiting (·4.0 mm) in July 2006, a Wberglass layer (0.50 mm diameter window screening) was added to the sides of the exclusion enclo- sures. This layer covered the exterior of the Vexar mesh from the sediment surface to the PVC frame. To avoid dis- turbing the sediment, we removed juvenile crabs with a cordless hand-held Black and Decker vacuum. Prior to the start of the experiment, we veriWed that there were no sig- niWcant diVerences in height, diameter, and leaf abundance between the mangroves in the control and exclusion enclo- sures using a Student t test (see “Results”).
In June 2006, we began our measurements (every 3– 6 weeks) over the next 11 months (11 sampling periods). We counted the number of crab burrows in each enclosure as an estimate of crab density. We estimated mangrove pro- duction for each enclosed mangrove by measuring tree height (cm), trunk diameter (mm), and number of attached leaves using the same methods as in the transect survey.
Means § SE were calculated for each dependent variable per sample period. Our experimental data were then analyzed statistically using a two-way repeated measures ANOVA with date (monthly sampling) and enclosure (control, exclu- sion) as independent variables on the following repeated measures: mangrove height, trunk diameter, number of leaves, and number of crab burrows. We used the PROC GLM (general linear model) procedure in Statistical Analyti- cal Software, version 8.2 (SAS Institute, Cary, NC) for all ANOVA tests since we had an uneven number of replicates in the control (n = 7) and exclusion (n = 8) enclosures. Com- parisons between transect and control enclosure initial and Wnal mean tree heights were made using Student t tests.
Hydroedaphic factors
To assess the eVect of Wddler crab burrowing on marsh sed- iment, several hydroedaphic factors were measured inside
all enclosures, including: pH, salinity, and sulWde concen- tration, similar to methods described in McKee et al. (1988), as well as oxidation–reduction potential (redox) (Eh). No measurements were taken outside the enclosures.
Every sample period, interstitial water samples were col- lected at least 15 cm within the walls for each control (n = 7) and exclusion (n = 8) enclosure using a perforated metal probe wrapped in several layers of cheesecloth to Wlter out sediment and debris. The probe and cheesecloth, attached to clear plastic, Xexible tubing (1-cm diameter), were pressed into the soil to a depth of 15 cm and water was drawn out of the soil using the suction of a 30-ml syringe. A three-way valve between the syringe and tubing allowed any air to be expelled. The Wrst 5 ml of interstitial water was discarded to remove any oxidized water in the tube and any debris and sediment that may have entered as a result of forcing the metal probe into the soil.
Aliquots (»5 ml) of interstitial water were collected and returned to the lab on ice for salinity measurements using a refractometer and for pH using a standardized electrode (Orion model 720A). Additionally, a 5-ml aliquot of inter- stitial water was Wxed in the Weld with antioxidant buVer (1.56 M sodium salicylate, 2.13 M sodium hydroxide, 0.37 M ascorbic acid; 1:1 dilution) and stored on ice until returned to the lab. The Wxed samples were measured within 12 h for total soluble sulWde (H2S, HS¡, S¡2) (mM) using a silver/sulWde electrode. A sulWde standard curve was constructed using a series of Na2S solutions prepared prior to analysis with the same antioxidant buVer.
We measured redox potentials (Eh) at 1- and 10-cm depths using four sets (subsamples) of brightened platinum electrodes within each enclosure, approximately 25 cm from both the mangrove and enclosure wall. Platinum elec- trodes were calibrated in quinhydrone at pH 4 (+218 § 5 mV at 25°C) 1 day prior to measurements. The potential of a calomel reference electrode (+244 mV) was added to each measurement.
Means § SE were calculated for salinity, pH, sulWde con- centration, and redox potential (four subsamples at 1 and 10 cm) between control and exclusion enclosures over the entire 11-month period, with mean comparisons between control and exclusion enclosures made using Student t tests.
Results
Field transect survey
During the Weld transect surveys from June 2006 to May 2007, mangrove height signiWcantly increased (df = 10, F = 56.20, P < 0.0001; Fig. 1a) from its initial height of 34.0 § 2.08 cm. After approximately 5 months (126 days), the increase in mangrove height began to slow, coinciding
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with the fall months of October and November (Fig. 1a), and Wnally reached a mean height nearly double that at the start (65.1 § 3.6 cm). Basal trunk diameter also signiW- cantly increased (approximately 2.75 times) during the study period (df = 10, F = 157.98, P < 0.0001; Fig. 1b), as did leaf production (approximately 3.5 times) (df = 10, F = 24.89, P < 0.0001; Fig. 1c). These latter two parame- ters also slowed after 126 days, but to a lesser extent than the slowing observed in height.
Spartina alterniXora shoot density signiWcantly increased over time (df = 10, F = 8.85, P < 0.0001; Fig. 2a), as did crab burrow density (df = 10, F = 11.30, P < 0.0001; Fig. 2b). Mean S. alterniXora shoot and crab burrow density at the beginning of the study were both only 40% of their values at the end of the study. After 6 months (161 and 191 days), we found a slight decrease in S. alter- niXora shoot density (Fig. 2a), which we attribute to marsh senescence, a pattern frequently observed during cold months (e.g. Baerlocher and Moulton 1999). However, by the end of the study period, S. alterniXora and crab burrow density had nearly tripled (Fig. 2). Both variables were sig- niWcantly correlated with each other (r = 0.43, P < 0.0001).
In individual 0.25 £ 0.25-m quadrats along the 60-m transect, mangrove height was positively associated with the density of crab burrows, which explained 24% of the variance in height, and S. alterniXora shoot density explained only a minor portion (5%) of the total variance in mangrove height (Table 1). The density of crab burrows had the strongest positive eVect on trunk diameter (Table 1) (R2 = 0.29, P < 0.0001). S. alterniXora explained an
Fig. 1 Mean (§SE) a height (cm), b trunk diameter (mm), and c num- ber of leaves of young white mangroves (Laguncularia racemosa) since initiation of study in June 2006 for each sample period (n = 20) over 11 months along an established transect
Fig. 2 Mean density (§SE) of (a) Spartina alterniXora and (b) Wddler crab burrows 0.25 m¡2 for each sample period (n = 20) over 11 months beginning June 2006 along an established transect. Plant and burrow density were signiWcantly correlated (r = 0.43, P < 0.0001)
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additional 5% of the variation in mangrove trunk diameter (Table 1). Leaf production was positively associated with crab burrow density, and weakly with S. alterniXora shoot density (Table 1).
Fiddler crab exclusion experiment
Two weeks after initiating crab removals, we immediately noticed a diVerence in mean burrow density. The exclusion enclosures (7.38 § 5.73 m¡2) had burrow densities 27% lower than the control enclosures (27.57 § 18.8 m¡2). The position of crab burrows constantly changed throughout the experiment, suggesting that burrows were collapsing and Wlling during incoming tides, or that they were being plugged by the crabs. Frequent changes in burrow Wlling and excavation likely resulted from the low amount of organic matter in the marsh sediment, which has been shown to help maintain burrows (Bertness 1985). Ulti- mately, removal and exclusion of Wddler crabs signiWcantly reduced burrow density by 57% in the exclusion enclosure (13.34 § 1.78 m¡2) compared to the control enclosures (30.81 § 2.61 m¡2) over the 11-months study (df = 1, F = 10.73, P < 0.01). Crabs moving and burrowing into the marsh surface were predominately U. pugilator, but we occasionally observed a few U. rapax deposit-feeding on or near the transect and within enclosures. Prior to crab remo- vals, we found no signiWcant diVerence in height (df = 13, t = 1.74, P = 0.10), diameter (df = 13, t = 1.32, P = 0.21) and leaf abundance (df = 13, t = 1.59, P = 0.14) between mangroves in exclusion and control enclosures.
Removal and exclusion of Wddler crabs had a signiWcant eVect on mangrove growth by the second month (evident after 45 days) (Table 2; Fig. 3a). Trees in the control enclo- sures grew on average 27% taller than mangroves in crab exclusion enclosures during the study. Fiddler crabs also had a signiWcant eVect on trunk diameter by the end of the study (Fig. 3b), with mangroves in the control (26.20 § 1.41 mm) growing trunks that were a signiWcant 25% greater than those for mangroves in exclusion enclo- sures (21.03 § 1.95 mm) (Table 2). The production of leaves increased over time and was signiWcantly higher in the control than in the exclusion enclosures throughout the experiment (Table 2; Fig. 3c), Wnally producing 15% more
leaves by the end of the study. Averaged across sampling periods, mangroves in the control enclosures produced 226.8 (§10.71) leaves tree¡1 compared to mangroves in the exclusion enclosures (179.0 § 10.81 leaves tree¡1).
We also found marked diVerences in mangrove produc- tion at the end of the study between trees along the transect and those that grew concurrently in the control enclosures. After 11 months, mangroves in control enclosures grew taller (77.2 § 4.9 cm), wider (26.2 § 1.4 mm) and pro- duced more leaves (318.4 § 21.6) (Fig. 3) than those along the transect (65.1 § 3.6 cm tall, 18.1 § 1.0 mm wide, 145.3 § 14.6 leaves) (Fig. 1). Comparisons of tree heights at the initiation of the experiment revealed that the trees in the control enclosures (47.8 § 4.32 cm) were signiWcantly taller than those along the transect (34.0 § 2.08 cm) (df = 25, t = 3.20, P = 0.004).
Crab burrow densities also diVered between the transect and nearby control enclosures, but showed a diVerent pattern. On average, burrow densities along the transect measured 47.93 § 0.66 m¡2 over the study period, higher than burrow densities within control enclosures (30.81 § 2.61 m¡2). By the end of the study (day 330), crab burrow densities reached 73.2 § 2.09 m¡2 along the tran- sect (Fig. 2b), nearly 50% higher than burrow densities in control enclosures (49.0 § 7.49 m¡2).
Hydroedaphic factors
Fiddler crab activity had a marked eVect on soil interstitial salinity (Fig. 4a), with the mean value in exclusion enclo- sures (44.2 § 0.99) 36% higher than that in the control enclosures (32.4 § 1.04) (df = 131, t = 8.21, P < 0.001).
Table 1 Percentage of variation in mangrove production (partial R2
values from stepwise multiple regression analysis) explained by Wddler crab burrow density and Spartina alterniXora shoot density in the Weld transect survey
* P < 0.001, ** P < 0.0001
Factor Height Trunk diameter Leaf production
Crab burrow density 0.24* 0.29** 0.16**
Marsh plant density 0.05* 0.05* 0.02
Table 2 Results of two-way repeated measures ANOVA on eVects of time (sample periods) and enclosure (control, exclusion) on Laguncu- laria racemosa height (cm), trunk diameter (mm) and leaf production (number leaves/tree) during the exclusion experiment
Field study was conducted at Cockroach Bay Aquatic Preserve, Hills- borough County, Florida, USA
Source of variation df SS F P
Height
Time £ enclosure 10 352.11 1.51 0.143
Diameter
Time £ enclosure 10 111.30 5.86 <0.001
Leaf production
Time £ enclosure 10 8,039.05 0.61 0.803
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In contrast, there was no signiWcant diVerence in the pH of interstitial water between control and exclusion enclosures (df = 132, t = 0.31, P = 0.76; Fig. 4b).
SulWde concentrations (mM) in the control and exclusion enclosures were not signiWcantly diVerent (df = 117, t = 1.13, P = 0.26; Fig. 5a) and concentrations were quite
low compared to natural marsh systems (Carlson et al. 1983; McKee et al. 1988). One sulWde sample taken in June 2006 from an exclusion enclosure had an abnormally high value (0.36 mM) compared to all other samples, and was excluded from the statistical analysis above. When included, there was still no signiWcant diVerence in sulWde between control and exclusion enclosures (df = 118, t = 0.91, P = 0.37).
The redox potential of the marsh substrate diVered between control and exclusion enclosures (Fig. 5b), with redox levels signiWcantly lower in exclusion than control enclosures for both 1-cm (df = 107, t = 2.11, P = 0.04) and 10-cm (df = 107, t = 4.11, P < 0.0001) depths. Within the exclusion enclosures, the redox potential was signiWcantly lower at a depth of 10 cm than at 1 cm (df = 116, t = 3.83, P < 0.001); and similarly, redox was slightly lower, but not signiWcantly so, at 10 cm that at 1 cm for the control enclo- sures (df = 98, t = 1.97, P = 0.05).
Discussion
As in temperate marshes, Wddler crabs in mangrove com- munities can have a signiWcant eVect on plant production and substrate characteristics. In our restored marsh, Wddler crab burrowing increased Wnal tree height by 27%, Wnal basal trunk diameter by 25%, and Wnal leaf production by 15% over mangroves growing where crabs were removed and excluded. We also observed signiWcant positive associ- ations between mangrove production and crab burrow den- sity along our transect. Crab burrows accounted for 24, 29, and 16% of the variation in mangrove height, trunk diame- ter, and leaf production, respectively. S. alterniXora grow- ing around the white mangroves accounted for only a minor part of the variation (·5%).
We observed that the increase in height of white man- grove began to slow at the onset of the fall season, but basal trunk diameter continued to increase. Meyers and Ewel (1990) showed that L. racemosa has extensive shoot growth in the summer and winter shoot inactivity. This may also reXect that these young plants may allocate energy to developing a wider base to support subsequent increases in height.
In addition, we counted live leaves as a measure of mangrove growth, but did not assess leaf litter (leaves, twigs, bark), which is often used to assess tree productiv- ity. In Florida, litterfall is continuous throughout the year, with minor peaks before the wet season and after periods of high stress. Given the long life of mangrove leaves (Gill and Tomlinson 1977), relatively consistent leaf shedding, and relatively low levels of environmental stress (low sulWde and elevated Eh) at our study site, leaf counts appear to be a good indicator of growth, particularly
Fig. 3 Mean (§SE) a height (cm), b trunk diameter (mm), and c num- ber of leaves tree¡1 in Wddler crab exclusion (Wlled circle) (n = 8) and control (open circle) (n = 7) enclosures since initiation of experiment in June 2006 for each sample period over 11 months
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in conjunction with measures of tree height and girth (Meyers and Ewel 1990).
When comparing production between mangroves along the transect with trees in control enclosures after 11 months, mangroves in control enclosures grew taller, wider, and produced more leaves than mangroves along the transect. We attribute this to diVerences in initial tree size with the mean height of the control mangroves being sig- niWcantly greater than the transect mangroves at the start of the study. It was not our intention to make direct compari- sons between the experiment and transect survey as slightly diVerent criteria were used in setting them up. In particular, mangroves in all of the enclosures were selected for their low proximity to other plants (to minimize soil disturbance by the initial removal of all macrophytes), while the tran- sect mangroves were not.
This signiWcant diVerence in initial and Wnal heights of transect and control enclosure mangroves also suggests that removal of adult S. alterniXora at the initiation of the experiment may have reduced competition with mangrove seedlings for limiting resources such as nutrients and light. López-HoVman et al. (2006) demonstrated that net photo-
synthesis, growth, and survivorship in mangrove seedlings increased with increased light availability (provided by our removal of S. alterniXora) at lower but not higher salinities. Increased light availability to young mangroves could not overcome potential limitations caused by the elevated salin- ities in the exclusion enclosures. Negative eVects of high salinity on seedlings can include reduced stomatal conduc- tance and internal CO2 concentrations, decreased nutrient uptake (particularly nitrogen) (Morris 1980, 1984), or lim- ited water availability, all of which limit productivity.
Moreover, L. racemosa may have shifted biomass alloca- tion to belowground growth (an increase in root to shoot ratio) in the absence of S. alterniXora competition. López- HoVman et al. (2006) have shown increased ratios of mangrove seedling root mass to leaf mass at high salinity (independent of competitor removal). However, S. alterniXora was not removed along the transect and belowground growth was not measured in the experiment or along the transect. Thus, we can not discount that removing all S. alterniXora within 1.5 m of each enclosed mangrove may have inXuenced energy allocation, because mangroves within each enclosure could have experienced reduced resource
Fig. 4 Mean (§SE) a salinity and b pH measured 15 cm below marsh surface for all sample periods over 11 months in Wddler crab exclusion (Wlled circle) (n = 80) and control (open circle) (n = 70) enclosures
Fig. 5 Mean (§SE) a concentration of sulWde (mM) in interstitial wa- ter samples taken 15 cm below marsh surface, and b sediment oxida- tion–reduction (redox) potential (mV) measured 1- and 10-cm below marsh surface in Wddler crab exclusion (Wlled circle) and control (open
circle) enclosures for all sample periods over 11 months. Means with diVerent letters indicate signiWcant diVerence (P < 0.001) in redox between 1- and 10-cm within exclusion enclosures
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competition. Additionally, the removal of S. alterniXora may have reduced crab burrow density in the control enclo- sures since organic debris and belowground tissue of marsh plants is known to support burrows (Bertness 1985).
We also cannot dismiss the possibility that our enclosure experimental design may have contributed to diVerences in tree growth between the control enclosures and transect. For example, enclosure mesh walls may have induced shad- ing, but since the young trees were taller than the enclosure walls (25 cm) and the walls were at some distance from the tree in the center, we consider this unlikely. We also cannot discount that enclosures may have limited the movement of macrofauna other than Wddler crabs. Although the enclo- sures could have aVected tree growth directly, we believe that the initial larger size of enclosure mangroves and the removal of S. alterniXora from the enclosures are likely to have had greater eVects.
Experimental reduction of Wddler crabs in our study (by 43%) markedly reduced interstitial water salinity in control enclosures compared to exclusion enclosures. Reduction in salinity may be due to increased soil drainage as a result of burrowing (Montague 1982; Bertness 1985), with the area of burrow soil exposed to the atmosphere increasing by 12– 59% (Katz 1980; Macintosh 1982). Since mangroves were of similar age and size (<1 m tall, <0.5 m width) and grew in full sun, plant percent cover is unlikely to have impacted soil evaporation rates. Further research is needed to deter- mine whether burrowing can inXuence percolation rates, and thus evaporation rates in marsh sediments (see Stieglitz et al. 2000). Mangroves in the exclusion enclosures, which experienced signiWcantly higher salinity, grew less than mangroves in control enclosures, suggesting that high salin- ity may have a negative eVect on young mangrove growth and production.
On the east coast of central Florida, Lovelock and Feller (2003) found that L. racemosa is less tolerant of highly saline conditions than the sympatric black mangrove, A. germinans, which has higher photosynthetic water-use eYciency where higher soil nitrogen levels are present. However, Cintrón et al. (1978) determined greater salinity tolerance for Gulf of Mexico L. racemosa and A. germinans (salinity 80–90) than for R. mangle (salinity 60–65) and Chen and Twilley (1998) demonstrated a greater salt toler- ance of A. germinans (also dependent upon soil fertility). Relative salt tolerance of mangrove species is highly vari- able and dependent upon the level of other environmental stresses (e.g. low nutrients, increased sulWdes, etc.) (Flow- ers et al. 1977). We did not assess the eVect of increased soil salinity on species other than L. racemosa, as they had not signiWcantly recruited to our site. Although adult L. racemosa has shown tolerance to hypersalinity, we suggest that the signiWcant but modest hypersalinity (44) within our exclusion enclosures (and removal of S. alterniXora) had a
negative eVect on the growth of the very young mangroves, in contrast to those growing in lower salinities (32).
The redox potential of the marsh substrate also diVered between crab exclusion and control enclosures at 1- and 10- cm depths, demonstrating that Wddler crab burrowing can increase soil redox, a feature that has also been observed in temperate salt marshes (Bertness 1985). Our redox levels (Eh) were relatively high compared to the Eh values reported by McKee et al. (1988) for similar depths in man- grove substrates. Their soil redox values demonstrated highly reduced sediment conditions, with Eh ranging from ¡168 to ¡204 mV in unvegetated sites and ¡45 to ¡161 mV in sites with mangrove pneumatophores, well within the range for sulWde production.
Compared to the undisturbed and mature mangrove marsh studied by McKee et al. (1988) in Belize, the sedi- ments at our restored marsh in Cockroach Bay were highly impacted as a result of decades of farming, and more recently, the restoration of farm Welds and nearby shell-min- ing pits into marsh habitat. During restoration, grading and dredging of the upper surface layers left behind very sandy soils with coarse carbonates (mostly in the form of mollusc shells) and very little organic matter. High sand content and low marsh peat most likely reduces water retention and pro- vides less carbon fuel for microbial respiration, resulting in relatively high Eh values. Smart and Barko (1978) found higher redox values for sandy sediments compared to Wne- textured sediments, which is likely to reXect the higher porosity and diVusion of atmospheric oxygen in coarser sed- iments. Given our high redox values, it is not surprising that the sulWde concentrations were quite low compared to those observed in mature marshes (Carlson et al. 1983; McKee et al. 1988). In natural systems, crab burrows and salt marsh plant roots can maintain suYciently high redox levels to prevent accumulation of sulWde to toxic levels in marsh sediment (reviewed by Kristensen 2008). This is further supported by experimental removal of burrowing grapsid crabs of the genus Sesarma in a mangrove marsh in Austra- lia, which caused sulWde and ammonium levels to signiW- cantly increase, resulting in decreased Rhizophora spp. leaf and propagule production (Smith et al. 1991). At our study site, the coarse content of the restored sediment most likely accounts for the low sulWde values, and can not be attributed to crab burrowing, an activity which may be relatively more important in marsh systems with substantial organic matter (e.g. Bertness 1985). The low soil organic content at our Weld site, which normally drives redox functions in healthy natural marshes, is notable. Our data suggest that organic soil amendments should be considered when implementing wetland restoration (Zedler 2000; McDonald 2005).
Restoration of mangrove-dominated wetlands can be followed through the biogeochemistry of the wetland. For example, when sulWdes are high, mangroves will only be
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able to oxidize their rhizospheres to a certain degree, and then they begin to senesce. SpeciWcally, sulWdes bind with enzymes in the electron transport chain and decrease the eYciency of anaerobic metabolism (Koch and Mendels- sohn 1989; Koch et al. 1990). Since energy is used in nutri- ent uptake, sulWdes indirectly aVect the amount of nutrients taken up. Hypoxia causes plants to switch to alcoholic fermentation which decreases productivity (Koch and Mendelssohn 1989; Koch et al. 1990). Since sulWdes accu- mulate in areas of hypoxia and anoxia, they can indicate problems with hydrology. If the water in the wetland does not Xush, sulWdes will accumulate. In this respect, sulWdes can be an indicator of failed or failing restoration (McKee and Faulkner 2000).
Crab bioturbation has long been suggested to inXuence mangrove production (Smith et al. 1991), since Wddler crabs are conspicuous and abundant in most mangrove for- ests (Salmon 1967; Macnae 1968). Accumulating evidence suggests that Wddler crabs can have signiWcant ecological eVects on salt marsh and mangrove communities. Through their bioturbating activities, Wddler crabs can directly or indirectly modulate the resources available to marsh plants by modifying the biogeochemical state of soft sediments (Gribsholt et al. 2003), subsequently inXuencing their pro- ductivity. For example, active transport of marsh sediment can inXuence the movement of water and oxidants in and out of a patch of marsh or burrow, thus determining the abi- otic conditions of salinity and oxygenation. Because crabs are unevenly distributed and vary in density across a marsh, the movement or Xow of water, oxidants, and other materi- als is likely to vary spatially, resulting in variation in plant production. Kristensen (2008) argued that Wddler crabs are ecosystem engineers in the overall ecology of mangrove marshes (see Jones et al. 1994; Gutiérrez and Jones 2006). Identifying the ways in which mangrove-associated macro- fauna change sediment biogeochemistry is necessary to fully understand how primary production is regulated in mangrove ecosystems.
Acknowledgments We would like to thank Richard Sullivan, man- ager of the Cockroach Bay Aquatic Preserve for access to the restored marsh, and Allie Wilkinson and Courtney Nosach for their generous laboratory and Weld assistance. Comments and discussions with every- one directly involved, and with Randy Runnels and Brandt Henning- sen, were extremely helpful. We would like to thank the associate editor and anonymous reviewers for their valuable comments. This project was funded by a Sigma Xi Grant-in-Aid of Research to C. Wil- cox and by the Natural Sciences Summer Research Program at Eckerd College.
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Abstract
Introduction
