Estuarine, Coastal and Shelf Science 184 (2017) 158e165 Contents lists available at ScienceDirect Estuarine, Coastal and Shelf Science journal homepage: www.elsevier.com/locate/ecss Potential effect of fiddler crabs on organic matter distribution: A combined laboratory and field experimental approach Luís F. Natalio a, b, Juan C.F. Pardo a, b, Glauco B.O. Machado c, Monique D. Fortuna a, * Deborah G. Gallo a, d,Tania^ M. Costa a, b, a Universidade Estadual Paulista (Unesp) - Instituto de Bioci^encias, Campus do Litoral Paulista, Praça Infante Dom Henrique, s/n, Parque Bitaru, 11330-900, Sao~ Vicente, SP, Brazil b Universidade Estadual Paulista (Unesp) - Instituto de Bioci^encias, Programa de Pos-Graduaç ao~ em Ci^encias Biologicas e Zoologia, Campus de Botucatu, R. Prof. Dr. Antonio^ Celso Wagner Zanin, s/n, Distrito de Rubiao~ Junior, 18618-689, Botucatu, SP, Brazil c Universidade de Campinas (Unicamp) - Instituto de Biologia, Programa de Pos-Graduaç ao~ em Ecologia, R. Monteiro Lobato, 255, Cidade Universitaria, 13083-862, Campinas, SP, Brazil d Universidade de Sao~ Paulo (USP) - Instituto Oceanografico, Programa de Pos-Graduaç ao~ em Oceanografia Biologica, Praça do Oceanografico, 191, Cidade Universitaria, 05508-120, Sao~ Paulo, SP, Brazil article info abstract Article history: Bioturbators play a key role in estuarine environments by modifying the availability of soil elements, Received 3 October 2016 which in turn may affect other organisms. Despite the importance of bioturbators, few studies have Accepted 3 November 2016 combined both field and laboratory experiments to explore the effects of bioturbators on estuarine soils. Available online 5 November 2016 Herein, we assessed the bioturbation potential of fiddler crabs Leptuca leptodactyla and Leptuca uru- guayensis in laboratory and field experiments, respectively. We evaluated whether the presence of fiddler Keywords: crabs resulted in vertical transport of sediment, thereby altering organic matter (OM) distribution. Under Bioturbation laboratory conditions, the burrowing activity by L. leptodactyla increased the OM content in sediment Burrows fi Sediment transport surface. In the long-term eld experiment with areas of inclusion and exclusion of L. uruguayensis, we did fl fi Estuaries not observe in uence of this ddler crab in the vertical distribution of OM. Based on our results, we Genus Leptuca suggest that small fiddler crabs, such as the species used in these experiments, are potentially capable of alter their environment by transporting sediment and OM but such effects may be masked by envi- ronmental drivers and spatial heterogeneity under natural conditions. This phenomenon may be related to the small size of these species, which affects how much sediment is transported, along with the way OM interacts with biogeochemical and physical processes. Therefore, the net effect of these burrowing organisms is likely to be the result of a complex interaction with other environmental factors. In this sense, we highlight the importance of performing simultaneous field and laboratory experiments in order to better understanding the role of burrowing animals as bioturbators. © 2016 Elsevier Ltd. All rights reserved. 1. Introduction et al., 1994). Studies have investigated how engineers change the environment and how the intensity of those changes can modify How organisms interact with their environment and how those our understanding of ecosystem functioning (Wang et al., 2010; interactions modify ecosystem functioning is a central theme in Richards et al., 2011; Schaller, 2014). Bioturbators, for example, ecological studies. The important role of ecosystem engineers in have a significant impact on sediment biogeochemistry (Kristensen modifying the local environment has long been recognized (Jones et al., 2012). The bioturbation alters sediment matrices and the distribution of its components (Meysman et al., 2006; Kristensen, 2008; Michaels and Zieman, 2013). Sediment texture, influx of soil particles and interstitial transport of solutes in different eco- * Corresponding author. Universidade Estadual Paulista (Unesp) - Instituto de systems (Meysman et al., 2006) are modified by bioturbation, Biociencias,^ Programa de Pos-Graduaç ao~ em Ciencias^ Biologicas e Zoologia, Campus de Botucatu, R. Prof. Dr. Antonio^ Celso Wagner Zanin, s/n, Distrito de stimulating organic matter (OM) decomposition and reminerali- Rubiao~ Junior, 18618-689, Botucatu, SP, Brazil. zation (Kristensen, 2000; Lohrer et al., 2004; Martinez-Garcia et al., E-mail address: [email protected] (T.M. Costa). http://dx.doi.org/10.1016/j.ecss.2016.11.007 0272-7714/© 2016 Elsevier Ltd. All rights reserved. L.F. Natalio et al. / Estuarine, Coastal and Shelf Science 184 (2017) 158e165 159 2015) and enhancing nutrient flux throughout the ecosystem (Machado et al., 2013). In this sense, it could be expected that both (Fanjul et al., 2015). Then, the ecological consequences of bio- fiddler crabs have comparable bioturbation effects in mangrove turbation have been extensively investigated in many groups of soils. burrowing invertebrates, such as polychaetes (Giangrande et al., 2001; Volkenborn et al., 2007), bivalves (Kanaya, 2014; Harris 2.2. Laboratory experiment et al., 2015), shrimps (Gagnon et al., 2013), crayfishes (Usio and Townsend, 2004), and crabs (Kristensen, 2008; Pülmanns et al., The bioturbation potential of L. leptodactyla on mangrove soil 2014). was investigated by manipulating its presence in terrariums at Burrows and galleries constructed by some organisms, such as laboratory. This species was chosen as a model of bioturbator burrowing crabs, tend to expose deep soil areas, with higher OM because it is found at high density at Portinho mangrove (LF contents (Michaels and Zieman, 2013), acting on both carbon Natalio, pers. obs.). Our experimental design consisted of three export via CO2 release, increasing decomposition and facilitating treatments, two with crabs and one without them. Both treatments aerobic degradation (Kristensen et al., 2008; Araújo et al., 2012; with crabs were identical except for the position at which sediment Pülmanns et al., 2014; Martinetto et al., 2016), as well as carbon was sampled: inside the burrow or near the burrow. These treat- storage, by increasing retention of nutrients in the environment ments were defined to verify the effect of crab bioturbation on OM (Martinetto et al., 2016). In turn, bioturbator crabs may promote content resulting from the burrowing excavation (inside the changes in the estuarine carbon pathways, which are a relevant burrow) and, consequently, from the excavation pellet deposition issue due to the importance of mangrove soils in stored carbon and (near the burrow). Each treatment had eight replicates (39 cm  22 its relation with climate change (Donato et al., 2011; Murdiyarso cm  24.5 cm terrariums), and in the treatments with crabs, eight et al., 2015). Consequently, these organisms profoundly modify L. leptodactyla adult females were added per terrarium (equivalent soil characteristics by changing biogeochemical processes (Araújo density reported in the field: 94 ind/m2 - LF Natalio, pers. obs.). et al., 2012; Chatterjee, 2014). However, bioturbation effects on In order to run the laboratory experiments, 128 L. leptodactyla the carbon cycle caused by burrowing crabs are usually related to adult females (carapace width larger than 4.1 mm; Cardoso and crab density (Kristensen et al., 2008; Andreetta et al., 2014) and Negreiros-Fransozo, 2004) were collected from Portinho size, with larger species presenting more significant effects (Araújo Mangrove. Only females were used to standardize crab effects, et al., 2012; Pülmanns et al., 2014). since bioturbation behavior (e.g. excavation and feeding) differs Fiddler crabs are burrowing animals broadly distributed in between sexes (Caravello and Cameron, 1987; Weis and Weis, tropical and subtropical estuaries (Crane, 1975). These bioturbators 2004). In the laboratory, crabs were acclimated for 48 h at 25 C are classified as biodiffusers and regenerators, according to sedi- in terrariums with sediment moistened with estuarine water. ment transport they perform in coastal ecosystems (see categories Sediment of high (20.09 ± 1.34% (mean ± SE)) and low in Kristensen et al., 2012). Therefore, they are key organisms in (1 ± 0.11%) OM content was collected from two different sites in mangrove forests (Smith III et al., 1991). Fiddler crabs are often used Portinho mangrove. Ten sediment samples of each site were dried as a model species to test the effects of bioturbation on the distri- in a heater (60 C, 72 h), and then a 10 g portion of dried sediment bution of soil components (e.g. OM, metals; Nielsen et al., 2003; was burned in a muffle (500 C, 4 h) to obtain OM content (%) by Kristensen and Alongi, 2006; Wang et al., 2010). High density and loss on ignition (Heiri et al., 2001). Sediment was boxed and wide distribution in intertidal areas facilitate the use of fiddler transported to the laboratory, where it was carefully sieved in a crabs in laboratory experiments (Wolfrath, 1992; Thomas and 2 mm mesh to remove macrofauna and organic detritus that could Blum, 2010; Fanjul et al., 2015). However, there are few studies overestimate organic content. Afterwards, the boxed sediment was performing both laboratory and long-term field experiments with kept for 48 h at 25 C to remove the excess of surface water. Thus, fiddler crabs. In this study, we investigated the bioturbation po- we avoided the instability of high humidity