Carry over effects of nutrient addition on the recovery of an invasive seaweed from the winter die-back

Highlights

• Nutrient addition during both winter and spring promoted earlier regrowth of Caulerpa cylindracea equally.

• Native species did not respond to nutrient addition during winter or spring.

• Impacts of the invader upon the native community were weak, likely as a result of the stressfulness of the environment.

Abstract

Nutrient enrichment of coastal waters can enhance the invasibility and regrowth of non-native species. The invasive alga Caulerpa cylindracea has two distinct phases: a well-studied fast-growing summer phase, and a winter latent phase. To investigate the effects of nutrient enrichment on the regrowth of the seaweed after the winter resting-phase, a manipulative experiment was carried out in intertidal rockpools in the North-western Mediterranean. Nutrients were supplied under different temporal regimes: press (constant release from January to May), winter pulse (January to March) and spring pulse (March to May). Independently from the temporal characteristics of their addition, nutrients accelerated the re-growth of C. cylindracea after the winter die-back, resulting in increased percentage covers at the peak of the growing season. Nutrient addition did not influence the number and length of fronds and the biomass. Native components of the algal community did not respond to nutrient additions. Our results show that nutrient supply can favour the spread of C. cylindracea even when occurring at a time of the year at which the seaweed is not actively growing.

Introduction

The introduction and spread of non-native species is globally acknowledged among the causes of alterations in the biodiversity and functioning of natural ecosystems globally (Mack et al., 2000, Pimentel et al., 2000). The potential for non-native species to establish and spread outside of their native range is often related, among other factors, to the level of disturbance that characterizes recipient systems (Burke and Grime, 1996, Hobbs and Huenneke, 1992) and on the biology of the invasive species (Leung and Mandrak, 2007). Many invaders are opportunistic species that can readily take advantage of enhanced resource availability in the non-native range due to increases in supply or reduced uptake by native species following a disturbance (Davis et al., 2000, Lohrer et al., 2000). Eutrophication of water in coastal environments from anthropogenic activities has increased in the last two decades (DeBruyn and Rasmussen, 2002, McClelland and Valiela, 1998), causing significant alterations to benthic and pelagic ecosystems (Bokn et al., 2003, Burkholder et al., 2007, Hillebrand, 2003, Hughes et al., 1999, Micheli, 1999, Worm et al., 2000). Enhanced nutrient loading can favour the establishment and spread of non-native species by conferring invaders a competitive advantage over native competitors (Incera et al., 2009, Sánchez and Fernández, 2006), and through the degradation of native communities (Atalah and Crowe, 2010, Balata et al., 2010, Stimson et al., 2001, Torres et al., 2004). Nutrient enrichment is generally constant in urban areas (i.e., eutrophic conditions) and, to date, most studies have considered nutrient enrichment as a press disturbance. However, inputs along less developed coastlines are generally linked to river run-off (Bonsdorff et al., 1997, Justić et al., 1995, Turner and Rabalais, 1994) and, hence, characterized by large temporal variation. Thus these environments are more likely to experience pulse rather than press events. Because of the more stochastic nature of nutrient delivery to these systems, we may expect the response of native and non-native species to vary according to the timing of their release. Positive effects in invasive algae may occur when nutrients become available at times of the year at which non-native species are able to uptake and use them more readily than extant native species.

Seaweeds are among the most noxious invaders in coastal environments (Gribben et al., 2013, Maggi et al., 2015, Schaffelke and Hewitt, 2007, Williams and Smith, 2007, Wright and Gribben, 2008). Correlative and experimental studies have shown that nutrient inputs often enhance their establishment and spread (Ceccherelli and Cinelli, 1997, Ceccherelli and Sechi, 2002, Gennaro and Piazzi, 2011, Piriz et al., 2003, Steen and Scrosati, 2004; but see Vaz-Pinto et al., 2014 as an example of less efficient uptake than native counterparts) and many of these opportunistic invasive algae can store nutrients in their tissues to sustain growth in periods when they are in short supply (Fong et al., 2004, Gennaro et al., 2015). Moreover, differences in the storage capacity among species may contribute to shape the structure of macroalgal assemblages. For instance, Fujita and Goldman (1985) found that greater N uptake during periods of high availability, allowed Gracilaria tikvahiae to sustain its growth longer than Ulva lactuca and Enteromorpha spp. in N-free medium. In addition, N uptake in macroalgae is less sensitive to temperature than growth (Duke et al., 1989) and winter uptake rates - a time of low algal growth - can be as high as those occurring during summer months (Pedersen et al., 2004). Thus, the ability to efficiently uptake and store nutrients during pulses of release throughout the year may explain the success of some non-native seaweeds.

The invasive green seaweed, Caulerpa cylindracea, (previously Caulerpa racemosa var. cylindracea) is among the most widespread invasive species in the Mediterranean Sea (Piazzi and Balata, 2009, Renoncourt and Meinesz, 2002). C. cylindracea does appear to be N-limited in its invasive range and the positive effects of nutrient enhancement on its growth (Gennaro and Piazzi, 2011, Gennaro and Piazzi, 2014) are likely the result of its tolerance to hypertrophic conditions and an ability to quickly uptake and store nutrients in its coenocytic thallus (Gennaro et al., 2015). Positive effects of nutrients enhancement have been documented in summer for C. cylindracea, when this seaweed is actively growing (Gennaro and Piazzi, 2011, Gennaro et al., 2015). However, in the Mediterranean Sea, C. cylindracea alternates a fast-growing phase during summer (Ceccherelli et al., 2002, Piazzi and Balata, 2009) with a latent phase during winter, characterized by loss of fronds and ramuli (Ruitton et al., 2005). To the best of our knowledge, no study has assessed how the supply of nutrients outside of the period of active growth influence the competitive ability of C. cylindracea in respect to that of native components of macroalgal assemblages. Similarly, no known study has studied how nutrient input in small long-lasting increases (press) promotes regrowth when compared to a sudden increase in them (pulse).

Here, we experimentally evaluated how nutrient input regimes differing in timing and duration (but not intensity) influenced the dynamics of C. cylindracea in intertidal rockpools.

In particular, we predicted that: (1) if C. cylindracea is able to uptake and store nutrient during the declining phase, nutrient addition in winter (January to March) would reduce its regression and/or promote an earlier recovery during the spring re-growing phase, thus resulting in a greater summer peak abundance if carry over effects are long lasting; (2) if C. cylindracea is able to uptake and store nutrient during the resting phase, nutrient addition during this phase (March to May) would promote an earlier recovery during the spring re-growing phase and enhance summer peak abundance even if carry over effects are short lasting; (3) if C. cylindracea is able to uptake and store nutrient throughout the declining – regrowing phase, a continuous nutrient addition (Press) during that period would reduce the winter regression, promote an earlier recovery during the spring re-growth and enhance summer peak abundance even if carry over effects are short lasting. Finally, we predicted that (4) the ability of C. cylindracea to take advantage of nutrient inputs would be greater than that of native macroalgae, irrespective of the temporal regime.