Biol Invasions https://doi.org/10.1007/s10530-018-1661-z ORIGINAL PAPER Transformation of detritus by a European native and two invasive alien freshwater decapods Thomas M. Doherty-Bone . Alison M. Dunn . Caroline Liddell . Lee E. Brown Received: 15 August 2017 / Accepted: 4 January 2018 Ó The Author(s) 2018. This article is an open access publication Abstract Invasive alien species have the potential to particulate organic matter (FPOM) and dissolved alter biodiversity and ecosystem processes. In fresh- organic carbon. Nutrients (ammonia and soluble waters, detritus decomposition is a major ecosystem reactive phosphorous) derived from excretion (mea- service but it remains uncertain whether invasive alien sured separately in the absence of biofilms) varied decapods process detritus differently to natives. This among decapod species, being lower for P. leniuscu- study examined leaf litter processing, and cascading lus. However, nutrient concentrations did not vary effects on biofilms, by the European native white among species in the detritivory experiments with clawed crayfish (Austropotamobius pallipes) com- biofilm, implying nutrients were utilised for biofilm pared to two invasive alien decapod species: the production and respiration as no differences in American signal crayfish (Pacifastacus leniusculus) biomass were evident among decapod treatments. and the Chinese mitten crab (Eriocheir sinensis). These results show invasive alien decapods have the Invasive alien decapods were responsible for higher potential to increase the magnitude of detrital pro- leaf litter decomposition than the native. In compar- cessing to FPOM in rivers, but indirect impacts on ison with native crayfish, invasive alien crab and primary producers due to nutrient release are uncertain crayfish showed higher rates of litter consumption, based on this experimental context. increased production of smaller leaf fragments, fine Keywords Austropotamobius pallipes Á Eriocheir sinensis Á Pacifastacus leniusculus Á Shredding Á Electronic supplementary material The online version of this article (https://doi.org/10.1007/s10530-018-1661-z) con- FPOM Á Decomposition rates Á Invasive alien species Á tains supplementary material, which is available to authorized Ecosystem functioning users. T. M. Doherty-Bone Á A. M. Dunn (&) Á C. Liddell School of Biology, University of Leeds, Leeds, West Yorkshire, UK Introduction e-mail: [email protected] T. M. Doherty-Bone Á L. E. Brown Invasive alien species are organisms translocated by School of Geography, University of Leeds, Leeds, human action from their native range to a biogeo- West Yorkshire, UK graphically novel locality, where they become estab- lished and spread (Blackburn et al. 2011). Invasive T. M. Doherty-Bone Á A. M. Dunn Á L. E. Brown water@leeds, University of Leeds, Leeds, alien species can alter community structure and West Yorkshire, UK modify ecosystem processes (Ehrenfeld 2010; Strayer 123 T. M. Doherty-Bone et al. 2012), especially in freshwater ecosystems (Strayer function, this could have profound impacts on whole and Dudgeon 2010; Moorhouse and Macdonald 2015). river basin resource processing rates and wider food One major freshwater ecosystem process is the webs. recycling of leaf litter and its transformation into This study investigated the impact of these native other forms of energy and nutrient throughout the food versus invasive alien freshwater decapod crustaceans web (Cummins et al. 1973; Gessner et al. 2010). on the processing of allochthonous resources (abscised Freshwater decapods, particularly crayfish, are key leaf litter) and the consequences of this on a lower processors of allochthonous riparian resources in their trophic level (biofilm). The study tested the following native ranges, with crabs studied to a lesser extent hypotheses: (Hi) the two invasive alien species would (Schofield et al. 2001; Rosewarne et al. 2013). A consume and breakdown more leaf litter than the recent meta-analysis of the impacts of aquatic invasive native crayfish, owing to their greater consumption species on lower trophic levels and ecosystem and metabolic rates (Rosewarne et al. 2014, 2016); attributes found substantial impacts, including on (Hii) Production of secondary products such as smaller nitrogen and organic matter standing stocks but did not leaf fragments (coarse particulate organic matter explicitly examine detritus decomposition rates (Gal- CPOM), fine particulate organic matter (FPOM) and lardo et al. 2015). dissolved nutrients would be higher in invasive alien Invasive species often differ from taxonomically species treatment due to their increased consumption, analogous natives in physiological and behavioural thus excretion rate; (Hiii) enhanced production of traits (e.g. Dick et al. 2014), and in their trophic secondary products in the invasive decapod treatments position (Tran et al. 2015). Species vary in their body would have a positive impact on the biomass of elemental composition, which co-varies with their biofilm, via dissolved nutrients fuelling growth. consumption of resources (Vanni 2002). Invasive alien species thus have the potential to alter nutrient cycling through possessing novel stoichiometric traits Methods (Capps and Flecker 2013), which can be indicated by nutrient composition of excreta. Decapod crustaceans Materials excrete ammonia, soluble reactive phosphorous and other nutrients (Kristiansen and Hessen 1992). The Alder (Alnus glutinosus) leaves collected around the fragmentation of leaf litter potentially also increases University of Leeds campus on senescence were oven organic matter surface area for microbial activity. dried at 50 °C and stored in paper bags prior to Released nutrients are then made available to primary experimentation. Alder was chosen as it is a dominant trophic levels such as heterotrophic microbes and native riparian species in Europe, and is commonly algae (Dyson et al. 2007; Kominoski et al. 2014). used in studies on decomposition rates (Abelho 2001). Many studies on leaf litter processing by invasive Leaves were subsequently combined into pre-weighed alien decapods have looked only at the invasive packs (3.0–3.5 g), placed in a labelled mesh bag, and species without comparing processing by invasives to conditioned (sensu Gessner et al. 1999) in water from a the analogue native (Moore et al. 2012; Twardochleb nearby stream (Meanwood Beck, Leeds: 53.820937N, et al. 2013), which may be because it has already been 1.5604979W) for 2 weeks for microbial communities driven to extinction (e.g. Rudnick and Resh 2005; to colonise. Schuster et al. 2010). In the British Isles and mainland Chinese Mitten Crabs were obtained from the River Europe west of the Alps, the indigenous White Clawed Thames at Chiswick, London (51.488489N, Crayfish, Austropotamobius pallipes still maintains 0.24471175E). American Signal Crayfish were col- viable populations in some areas but is at risk of total lected from Fenay Beck, Huddersfield (53.641660N, extirpation with the advance of two larger invasive 1.7310895W). White Clawed Crayfish were collected decapods: the American Signal Crayfish, Pacifastacus from Clapham Beck, North Yorkshire (54.117165N, leniusculus, which can be followed by invasions of the 2.3921497W), Wyke Beck, West Yorkshire Chinese Mitten Crabs (Eriocheir sinensis) (Rogers (53.827819N, 1.4893696W) and Adel Beck, West and Watson 2010; Almeida et al. 2014). If these Yorkshire (53.855078N, 1.5743397W). All animals invasive decapods differ in their leaf litter shredding were captured by hand, held in the laboratory for a 123 Detrital processing by decapods minimum of 2 weeks prior to experimentation for among species (see Supp. Fig. 1) and added to acclimatization, and fed Crab CuisineÒ pellets ad libi- microcosms following a randomised design. This tum. Animals were starved for 24 h prior to the age class forms a significant proportion of populations experiment start to standardise hunger (Rosewarne of all these species (Doherty-Bone personal observa- et al. 2016). tion) and been shown to shred leaf litter (Bondar et al. To examine biofilm growth, unglazed stone tiles 2005; Rosewarne et al. 2013). All treatments consisted (22 9 22 9 10 mm, with a reactive surface area of of 24 replicates (with equal representation of males 1364 mm2) were incubated outdoors for 3 months and females), with the exception of Chinese Mitten (July–October 2014) in a water tank seeded from a Crabs (13 replicates; 6 males and 7 females; fewer nearby lake (Wothersome Lake, Bramham; individuals were available owing to mortality). The 53.874944N, 1.3913008W) and pond (Kirkstall Val- experiment ran for 14 days. On day 7, 4 l of water was ley Nature Reserve, Leeds; 53.811316N, exchanged through siphoning to ensure welfare of 1.6032428W). The tiles were then brought into a decapods (Kemp et al. 2003). controlled environment room (see below) for 2 weeks After 14 days, measurements were taken of: to acclimatise before use in the experiments. A subset decapod mass, remaining leaf litter mass, mass of of 25 tiles were sampled to measure biofilm biomass at smaller coarse particulate organic matter fragments the start of the experiment. (CPOM, 1–10 mm), mass of fine particulate organic matter (FPOM, 0.7 lm–0.1 mm), nutrient concentra- Experimental design tions (organic and inorganic carbon, ammonia, nitrate, soluble reactive phosphorous). To measure decompo- Microcosms were set up in the laboratory to compare sition rates, CPOM and FPOM production, the con- the effects of native and invasive alien