Local Consumers Are the First Line to Control Biological Invasions: a Case
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This article appeared in a journal published by Elsevier. The attached copy is furnished to the author for internal non-commercial research and education use, including for instruction at the authors institution and sharing with colleagues. Other uses, including reproduction and distribution, or selling or licensing copies, or posting to personal, institutional or third party websites are prohibited. In most cases authors are permitted to post their version of the article (e.g. in Word or Tex form) to their personal website or institutional repository. Authors requiring further information regarding Elsevier’s archiving and manuscript policies are encouraged to visit: http://www.elsevier.com/authorsrights Hydrobiologia DOI 10.1007/s10750-016-2645-6 PRIMARY RESEARCH PAPER Local consumers are the first line to control biological invasions: a case of study with the whelk Stramonita haemastoma (Gastropoda: Muricidae) A. Giacoletti . A. Rinaldi . M. Mercurio . S. Mirto . G. Sara` Received: 30 October 2015 / Revised: 8 January 2016 / Accepted: 9 January 2016 Ó Springer International Publishing Switzerland 2016 Abstract The increasing spread of invasive species higher handling time. Stramonita showed a greater in the Mediterranean Sea determines several alter- preference for Brachidontes, that resulted as the prey ations in local food webs, changing the feeding habits with the higher energetic content, and the second most of native organisms. The whelk Stramonita haemas- profitable after Patella. This suggests that the higher toma is a widespread Mediterranean gastropod that energy gain is behind the change in the predator’s diet, consumes bivalves, barnacles and limpets. Previous with possible effects on its energy budget. studies showed a shift in its diet from the bivalve Mytilaster minimus to the invasive mussel Brachidon- Keywords Invasive species Á Functional response Á tes pharaonis, presumably due to a higher energy gain. Gastropod Á Mussels Á Stramonita haemastoma Á Here we tested whelks’ preference among natives and Brachidontes pharaonis a novel prey, calculating the profitability ratio, and integrating those results with biochemical analysis on prey tissues and the routine metabolism of the whelks. Further, we used the scaled functional response as a Introduction theoretical tool to describe whelk ability to obtain energy from their environment by using four different There are only so many ways in which local commu- prey species: B. pharaonis, Mytilus galloprovincialis, nities can control biological invasions. Autochthonous- M. minimus and Patella caerulea. Whelks evidenced a predators (sensu Schoener, 1986) are usually the first in Type II functional response for all prey, while line to influence the likelihood of invasion (Ricciardi Brachidontes displayed a lower attack rate and a et al., 2013). Invaders—often r-strategists—deploy their pronounced ability to compete for space—by exploiting local resources and promptly addressing Handling editor: Vasilis Valavanis local establishments. The importance of both predators and top-down control in structuring ecological com- & A. Giacoletti Á A. Rinaldi Á M. Mercurio Á G. Sara` ( ) munities has to date been widely discussed by ecolo- Dipartimento di Scienze della Terra e del Mare, University of Palermo - Local UO CoNISMa, Viale delle gists, and the loss of predators may provide an Scienze Ed. 16, 90128 Palermo, Italy important example of how they shape marine environ- e-mail: [email protected] ments (Terborgh, 2010). In particular, the common Indo-Pacific mussel Brachidontes pharaonis (Fischer A. Rinaldi Á S. Mirto IAMC-CNR, via Giovanni da Verrazzano 17, P., 1870), which entered the Mediterranean Sea after 90194 Castellammare del Golfo, Trapani, Italy the opening of the Suez Canal (1869), is slowly 123 Hydrobiologia colonising near all rocky upper subtidal and lower current literature, functional response experiments in intertidal substrates (Safriel & Sasson-Frosting, 1988) the natural field are quite rare. We thus decided to focus in the south-western Basin (Sara` et al., 2013), thereby on laboratory feeding trials at different prey densities. outcompeting the native bivalve Mytilaster minimus Our specific aims were to investigate the prey choice (Poli, 1795) (Safriel & Sasson-Frosting, 1988). In sea process by studying prey profitability and assimilation locations, however, it seems that the initial Brachidon- efficiency, and comparing experimental results to their tes colonisation process is constrained by predators, respective energetic content derived from biochemical such as Muricid gastropods (Rilov et al., 2002), which analyses. We further estimated the routine metabolism are able to regulate the population dynamics of their of S. haemastoma by measuring the oxygen consump- prey (Safriel et al., 1980). In the Mediterranean Sea, the tion rate. At the same time, we derived the functional whelk Stramonita haemastoma (Linnaeus, 1767; Gas- response of S. haemastoma over B. pharaonis,com- tropoda: Muricidae) is a widely distributed intertidal paring it with some of their most common indigenous top consumer that adopts opportunistic strategies to prey, the model species used many times in companion consume a large number of species (Basedow, 1994). studies: mussels Mytilus galloprovincialis (Lamark, Before dense beds of the invading mussel B. pharaonis 1819) (Sara` et al., 2011; Montalto et al., 2014)andM. were established along the Israeli Mediterranean coast, minimus (Sara` & De Pirro, 2011), and the limpet indigenous barnacles, small native mussels, Vermeti- Patella caerulea (Linnaeus, 1758) (Prusina et al., 2014) dae gastropods and limpets were the main potential in order to analyse predator–prey trophic interactions in food items for S. haemastoma (Rilov et al., 2001). greater detail. We examined whether (i) whelks exhib- Previous laboratory experiments have shown that B. ited a Type II or Type III functional response; (ii) pharaonis was the food item preferred by S. haemas- functional responses differed between natives and a toma over the indigenous mussels and barnacles (Rilov, novel prey and (iii) the new prey determines changes in 1999), and that in sites where it was abundant (densities the whelk’s ecology by altering functional response [25 % of the available prey), it constituted the whelks’ parameters such as the attack rate (a) and prey handling main food, except when energetic limitations ‘‘forced’’ time (h), affecting the duration and the cost of the the predator to prey on the more abundant, but predatory event, with a probable different energy intake presumably less profitable prey (Rilov et al., 2002). from the new prey. Trophic interactions are generally well described by functional response models quantifying consumer per capita consumption rate depending on local prey Materials and methods abundance (Holling, 1959). Several authors have measured the number of prey eaten by single predators Sampling and experimental design in small ‘‘arenas’’ (Hassel, 1978; Lang et al., 2012; Toscano et al., 2014), in order to eliminate the Specimens of S. haemastoma were collected alive at possibility of seeing anything other than prey depen- low tide during February 2014 from the intertidal dence (Abrams & Ginzburg, 2000). Using the func- shores near San Vito Lo Capo and the natural reserve tional response can explain and predict the impact of of Monte Cofano (Castelluzzo, Trapani). Whelks were predators on prey populations (Juliano, 2001;Dick brought back to the laboratory and placed in a 60-l et al., 2013). In particular, Twardochleb et al. (2012) aquarium at room temperature (18–20°C) and seawa- showed that the functional response might predict, ter salinity (37–38%) and they were allowed to along with simple population growth models, whether a acclimate for 1 week to reduce stress generated by predator will provide biotic resistance against non- manipulation and transport (Garton & Stickle, 1980). native preys at different prey densities. This prediction Specimens were then gradually transferred from room is made by determining the functional response shape temperature, at daily increase of *1to24°C, the and parameters (a, h). Predator functional responses optimal experimental temperature to elicit maximum interact with prey birth rate and abundance, and the feeding rates in the lab (Rilov, 1999; Brown & Stickle, magnitude of this interaction is reflected in the shape of 2002). Having reached this experimental temperature, the curve (Type II or III) and the intensity of the attack whelks were constantly acclimated there for 10 days, rate (a) (Twardochleb et al., 2012). According to the with no feeding (Garton & Stickle, 1980) prior to the 123 Hydrobiologia start of the experiment. We thereby standardised the Profitability of prey hunger level (Garton & Stickle, 1980). Aquaria used in the present study comprised n = 10-1l independent We also compared the biomass of the different prey by plastic compartments (15 9 8 cm base, 10 cm calculating their individual dry weights (oven 95°C for height), each containing a single whelk. We decided 24 h) and the ash content of their flesh (muffle furnace to use individual arenas so that feeding would not be at 450°C for 4 h) to estimate the organic matter as affected by scents from surrounding treatments, as Ash-Free Dry Weight (AFDW) to the nearest 0.001 g. gastropods use chemosensory cues to find food (Smith, Then, to assess the profitability of different prey, we 1983). Each aquarium was aerated, and kept under divided per capita