Functional and energetic consequences of climate change on a predatory whelk

https://doi.org/10.1016/j.ecss.2017.03.007Get rights and content

Abstract

The increasing rise in sea surface temperature caused by human activities currently represents the major threat to biodiversity and natural food webs. In this study we used the Lessepsian mussel Brachidontes pharaonis, one of the most recent invaders of the Mediterranean Sea, as a model to investigate the effect of a novel prey and a chronic increase in temperatures on functional parameters of local consumers, compared to the native mytilid species Mytilaster minimus. In particular we focused on the whelk Stramonita haemastoma, a widespread Mediterranean intertidal predator that actively preys on bivalves, barnacles and limpets, by studying the direct effects of such multiple stressors on feeding and growth rate, projected into a future climate change scenario (RCP8.5) relative to 2046–2065 with higher hypothesized temperatures of 2 °C. Gastropods showed a significantly higher feeding rate (ADFR) on M. minimus at high (6.45 ± 0.43) vs low temperatures (5.15 ± 0.33) compared to B. pharaonis (2.84 ± 0.37 vs 2.48 ± 0.27). Ingestion rate (ADIR), however, recorded higher values for B. pharaonis at high (1.71 ± 0.22) and low (1.49 ± 0.16) temperatures, compared to M. minimus (0.17 ± 0.01 vs 0.14 ± 0.01). Prey significantly influenced growth rate, condition index and the length-weight relationship (LWR) of whelks, while only ADFR seemed to be influenced by higher temperatures. In conclusion the extra amount of energy from the novel prey, together with temperature side effects, successfully influenced growth rates and reproductive events, positively affecting the global fitness of whelks.

Introduction

Biotic interactions of local species are naturally shaped by environmental variability (Vasseur et al., 2007, Post, 2013). Seawater temperature, through the fundamental influence on metabolic machinery (Brown et al., 2004), plays a prominent role in driving functional and life history (LH) traits of most ectotherms, affecting their local persistence over time (sensu Sibly et al., 2012). Increasing temperature, as a consequence of future climate change (CC; IPCC, 2014), will probably determine cascading effects within natural communities, modifying current biodiversity (Gooding et al., 2009, Yamane and Gilman, 2009). Intertidal shores are harsh habitats with regard to temperature; the body temperatures of ectotherms can vary greatly according to daily tidal cycles and seasonal weather conditions (Helmuth, 1998, Helmuth and Denny, 1999). Intertidal organisms are, for this reason, considered to live “on the edge” and thus CC is expected to modify the structure and species composition of those communities. CC may favour the spread of much more thermo-tolerant alien marine species, such as jellyfishes, bivalves and fishes by increasing the likelihood of reinforcing facilitation mechanisms (Southward et al., 1995, Stachowicz et al., 2002, Galil et al., 2015) or through the availability of empty niches in the invaded range (Hierro et al., 2005). Invasive species originated from the Red Sea (also called Lessepsian) and introduced to the Mediterranean Sea through the Suez Canal, are considerably more thermo-tolerant and better able to cope with highly changing thermal conditions than most Mediterranean species (Zerebecki and Sorte, 2011). Thus, when these species interact with local ecological equivalents, they will be advantaged by their major innate ability to survive under harsher conditions (Sarà et al., 2008). Invaders may then be able to replace native species in the local food webs (Simberloff et al., 2013) and consequently, local native consumers may count on a larger selection of prey. Nonetheless, local consumers, for their part, will also have to cope with increasing temperatures due to CC. However, although the effect of temperature is essentially pervasive (Gillooly et al., 2001), there is still little research to investigate the crossed effect between an alien prey and the increasing temperature on feeding behaviour (e.g. prey preference and consumption rate) of a local consumer apart from a single study dealing with the planktonic food webs (Seifert et al., 2014). According to theory (e.g. Arrhenius law; Kooijman, 2010, Sarà et al., 2014), increasing temperature should be particularly effective in enhancing the consumption rates in ectotherms (Sibly et al., 2012, Seifert et al., 2014). As a consequence, it is possible that an altered scheme of consumption dynamics of an abundant local predator has important local implications for the destabilization of the entire community equilibria (Vasseur and McCann, 2005, Seifert et al., 2014). Consumers are widely believed as able to adapt their feeding behaviour, and in particular the quality and quantity of food consumed in order to adjust their energy intake as a response to a varying environment (Tylianakis et al., 2008, Kordas et al., 2011, Kaspari et al., 2012). Ecologists use the term “plasticity” to describe this ability of organisms to modify their feeding behaviour, with compensatory feeding patterns, e.g. increased predation or ingestion rate to compensate for low quality resources or stressful conditions (Duarte et al., 2015). The same kind of plasticity can also be observed when consumers maximize consumption of high quality resources (Jacobsen and Sandjensen, 1994, Falkenberg et al., 2013) at the same time satisfying their energetic requirements and enhancing the individual fitness as suggested by classical ecological theory (Optimal Foraging Theory; Pyke, 1984). Here, we designed an experimental set-up to test if a widespread intertidal carnivorous gastropod, Stramonita haemastoma, when fed with an invasive bivalve, Brachidontes pharaonis (Sarà et al., 2000, Sarà et al., 2003) under constant increased temperature of a few degrees (IPCC, 2014; RCP8.5 scenario relative to 2046–2065), will show any difference in the individual fitness with respect to when it fed with the native ecological equivalent prey, the bivalve Mytilaster minimus. Thus, we investigated whether (i) functional traits, such as those involved in feeding processes (i.e. predation and ingestion) were modified, and (ii) if any repercussions on life history (LH) traits, such as growth and fecundity, were evident. Brachidontes and Mytilaster (and Stramonita) represent a perfect model for this study: the former is one of the first time invaders (Pallary, 1912, Sarà et al., 2000, Sarà et al., 2003), forms dense clusters on lower mid-littoral and subtidal rocks where Stramonita lives and spreads to the Western Basin (Sarà et al., 2013, Porporato et al., 2017). If present, it out-competes M. minimus (Safriel et al., 1980) that usually, in the absence of the alien species, proliferates and represents one of the most frequent items in the Stramonita diet (Safriel et al., 1980). Results from the present experiment comprise an important tool to evaluate the species colonization process and predict future spread, but will also be useful when assessing the potential expansion of Lessepsian species under higher temperatures and salinity conditions in the Mediterranean Sea, as a result of current global warming, where Lessepsian species would have a distinct advantage over native species (Sarà et al., 2008).

Section snippets

Materials and methods

Specimens of S. haemastoma were collected alive at low tide during the month of June 2014 from the intertidal shores near San Vito Lo Capo and the natural reserve of Monte Cofano (Castelluzzo, TP) (LAT: 38° 6′23.42″N; LONG: 12°42′17.84″E), where the mussels B. pharaonis and M. minimus were both present, although with different densities. As in surveys conducted along 100-m transects, whelks were relatively abundant in this site with a density of ∼0.56 ind./m2 (Giacoletti et al., 2016), while

Results

Different temperatures were significantly (χ2 = 29.5, df = 140, p < 0.05) maintained through the 135 day experimental period (Fig. 2). Mean temperatures recorded through the whole experimental period were 24.65 ± 1.65 for Tank A and 22.64 ± 1.76 for Tank B.

Discussion

The modification of phenology (Duarte, 2007) and reproductive failure (Helmuth et al., 2014, Montalto et al., 2014, Montalto et al., 2016) are the two most important repercussions of temperature change in a context of CC claimed to have a strong effect on the persistence of local populations over time. Here, we showed that S. haemastoma consumption rates of two different bivalves were affected by increased temperature. This is consistent with what has already been shown by other authors when

Concluding remarks

Our experiments allowed us to investigate how a novel prey may result as optimal in the diet of a predator, and even if through a borderline descriptor (allometric slopes) increased temperature showed a side effect in only a few months of exposure. Such observations should further raise awareness on the possible role of multiple stressors (here alien vs. increasing temperature; Vye et al., 2015) in reinforcing the effect of increasing temperature on life history traits of marine invertebrates.

Acknowledgements

PROJECT INNOVAQUA financed by the PON “Research & competitiveness” 2007–2013″, PON02_000451_3362185/1, and PRIN TETRIS 2010 grant n. 2010PBMAXP_003, both funded by the Italian Minister of Research and University (MIUR) supported this research. The authors declare no competing financial interests.

References (58)

  • A.J. Underwood et al.

    Solving some statistical problems in analyses of experiments on choices of food and on associations with habitats

    J. Exp. Mar. Biol. Ecol.

    (2005)
  • P.G. Verity et al.

    The relative food value of diatoms, dinoflagellates, flagellates, and cyanobacteria for tintinnid ciliates

    Arch. für Protistenkd.

    (1986)
  • M.J. Anderson

    A new method for non-parametric multivariate analysis of variance

    Austr. Ecol.

    (2001)
  • J.L. Blois et al.

    Climate change and the past, present, and future of biotic interactions

    Sci.

    (2013)
  • J.H. Brown et al.

    Toward a metabolic theory of ecology

    Ecol

    (2004)
  • Y.W. Chiu et al.

    Morphometric analysis of shell and operculum variations in the viviparid snail, Cipangopaludina chinensis (Mollusca: Gastropoda), in Taiwan

    Zool. Stud. Taip

    (2002)
  • J. Davenport et al.

    A comparison of methods for the assessment of condition in the mussel (Mytilus edulis L.)

    J. Moll. Stud.

    (1987)
  • C. Duarte et al.

    Ocean acidification induces changes in algal palatability and herbivore feeding behavior and performance

    Oecologia

    (2015)
  • L.J. Falkenberg et al.

    Future herbivory: the indirect effects of enriched CO2 may rival its direct effects

    Mar. Ecol. Prog. Ser.

    (2013)
  • B.S. Galil et al.

    ‘Double trouble’: the expansion of the Suez Canal and marine bioinvasions in the Mediterranean Sea

    Biol. Inv

    (2015)
  • D.W. Garton et al.

    Effects of salinity and temperature on the predation rate of Thais haemastoma on Crassostrea virginica spat

    Biol. Bull.

    (1980)
  • A. Giacoletti et al.

    Local consumers are the first line to control biological invasions: a case of study with the whelk Stramonita haemastoma (Gastropoda: Muricidae)

    Hydrobiologia

    (2016)
  • J.F. Gillooly et al.

    Effects of size and temperature on metabolic rate

    Sci.

    (2001)
  • R.A. Gooding et al.

    Elevated water temperature and carbon dioxide concentration increase the growth of a keystone echinoderm

    P. Natl. Acad. Sci. U. S. A.

    (2009)
  • S.J. Gould

    Allometry and size in ontogeny and phylogeny

    Biol. Rev.

    (1966)
  • B.S. Helmuth

    Intertidal mussel microclimates: predicting the body temperature of a sessile invertebrate

    Ecol. Monogr.

    (1998)
  • B.S. Helmuth et al.

    Measuring scales of physical stress in the rocky intertidal

    Am. Zool.

    (1999)
  • B. Helmuth et al.

    Beyond long-term averages: making biological sense of a rapidly changing world

    Clim. Change Resp.

    (2014)
  • J.L. Hierro et al.

    A biogeographical approach to plant invasions: the importance of studying exotics in their introduced and native range

    J. Ecol.

    (2005)
  • Cited by (7)

    • Mission impossible: Reach the carrion in a lithium pollution and marine warming scenario

      2021, Environmental Research
      Citation Excerpt :

      In many marine ectotherms, an increase in temperature causes an increase in energy demand, which is the most common strategy to compensate for this energy demand, increase energy consumption and/or increase metabolism (Détreé et al., 2020; Lannig et al., 2010). According to Arrhenius law (Sarà et al., 2014), temperature rise should be particularly effective in increasing consumption rate in ectotherms as seen in previous studies (e.g., Détreé et al., 2020; Giacoletti et al., 2017). Our data support this statement because the amount ingested by T. neritea was affected by the temperature, the higher the temperature the more the amount ingested by this snail regardless of the Li concentration in the treatment.

    • The entangled multi-level responses of Mytilus galloprovincialis (Lamarck, 1819) to environmental stressors as detected by an integrated approach

      2021, Marine Environmental Research
      Citation Excerpt :

      This generates mainly changes in body temperature during a short time interval (Sokolova, 2004; Banni et al., 2011) and then such organisms develop phylogenetic, physiological and developmental mechanisms leading to short term (acclimation, phenotypic plasticity) or long term (adaptation, selection) responses. Anthropogenic-driven environmental changes are now exacerbated (Stoks et al., 2017) and when multiple stressors co-occur, their interactive influence on metabolic machinery, energy acquisition, immune response and individual performances (Galloway and Depledge, 2001; Giacoletti et al. 2016, 2017) becomes so harsh that it causes functional impairment with repercussions on organisms’ local persistence over time (sensu Sibly et al., 2012). To predict potential effects and to prevent systems reaching tipping points, measuring the chemical or physical status is not sufficient, as such measures provide limited information on the general status of the environment, while the combination of physical, chemical and biological characteristics should be favorable.

    View all citing articles on Scopus
    View full text