Complex food webs of tropical intertidal rocky shores (SE Brazil) – An isotopic perspective

Highlights

• Seventy-one food web nodes were isotopically characterized in a tropical intertidal ecosystem.

• Food web length was 3.3, similar to temperate intertidal ecosystems.

• Two invasive crustaceans were top consumers, Lysmata lipkei and Charybdis hellerii.

• Top consumers depended mostly on the macroalgal and pelagic energy pathways.

• Drastic changes are expected that should favour the detrital energy pathway.

Abstract

Knowledge on food web structure, trophic links and energy pathways is essential for the understanding of complex and highly biodiverse tropical ecosystems. Emerging issues related to global change and species invasions call for an urgent advance on this topic. Isotopic analyses were applied to the tropical intertidal rocky shores of Southeastern Brazil, with the aim of 1) describing the general food web structure, 2) estimating food web length, 3) estimating the trophic level of the secondary consumers, and 4) their dependence on different energy pathways. An exceptionally high number of food web nodes (71) was analysed. The maximum trophic level (TL) was 3.3, similarly to what has been previously reported for temperate rocky intertidal ecosystems. Fish were the dominant top consumers (TL > 2.0), along with an important number of gastropods and crustaceans (both crabs and shrimp). Primary consumers were mostly crabs, gastropods and bivalves. Two invasive crustaceans were found among the top consumers, the Japanese peppermint shrimp, Lysmata lipkei (TL = 3.0), and the Indo-Pacific swimming crab, Charybdis hellerii (TL = 2.3). Among the primary consumers, one invasive bivalve was found, Isognomon bicolor. Mixing models showed that the top consumers depend mostly on the macroalgal and pelagic energy pathways. The food web currently established has low dependence on the benthic pathway. Given the important increase in precipitation predicted for this region and the increment in detritus it incurs, this food web is likely to suffer important alterations in the future.

Introduction

The tropics are home to high biodiversity and complex ecosystems. As the knowledge on global change increases, so does the awareness that tropical ecosystems are likely to be more sensitive than temperate ecosystems to the multiple pressures they will face over the next decades (e.g. Tewksbury et al., 2008, Somero, 2010, Sunday et al., 2011, Watson et al., 2013, Vinagre et al., 2016, Vinagre et al., 2018a, Vinagre et al., 2018b). Yet, compared to their temperate counterparts, the ecological functioning of most tropical coastal habitats is still poorly studied.

Lying at the interface between the terrestrial and the marine realms, the intertidal zone of rocky shores is not only subject to changes in water temperature, but also to oscillations in air temperature, making this a physiologically challenging environment for marine organisms (e.g. Helmuth et al., 2006, Madeira et al., 2012, Vinagre et al., 2016). Tropical intertidal organisms live closer to their thermal limits than their temperate counterparts, being this way more vulnerable to the increase in mean and in extreme temperatures predicted for these areas (Stillman and Somero, 2000, Stillman, 2003, Vinagre et al., 2016, Vinagre et al., 2018a, Vinagre et al., 2018b).

Rocky shores are, nevertheless, among the most productive ecosystems in the world, constituting an important link in the transfer of energy between the marine and terrestrial systems (e.g. Hori and Noda, 2001; Ellis et al., 2007), and providing refuge and nursery grounds to many commercial fish species and crustaceans (e.g. Turra and Leite, 2000, Barreiros et al., 2004, Cunha et al., 2008, Dias et al., 2014, Dias et al., 2016). Knowledge on the food web structure and energy pathways of tropical intertidal food webs is crucial for the understanding of their general functioning and to achieve their sustainable use and the conservation of biodiversity.

The intertidal rocky shorelines of Southeastern Brazil are predicted to be among the coastal areas of the world hardest hit by climate change, with an increase in temperature of up to 6 °C and an increase in rainfall of up to 60% by the year 2100 (PBMC, 2012). Besides a possible impoverishment of trophic interactions involving mobile consumers owing to exceedingly high thermal stress, a severe increase in rainfall will certainly lead to surplus terrestrial matter reaching coastal waters, likely fueling alternative energy pathways through nearshore pelagic and benthic compartments that may potentially disrupt present coastal food webs. Moreover, the rocky reefs in this region have been recently invaded by exotic species that have built very large populations, at times dominating seascapes. This is the case of sun corals Tubastraea spp (da Silva et al., 2014) in the subtidal and of the bicolored purse-oyster Isognomon bicolor in the intertidal zone (López et al., 2014). Other recent introductions included mobile consumers that may alter the structure of food webs through generalist epibenthic feeding (i.e. the peppermint shrimp Lysmata lipkei; Pachelle et al., 2016, Madeira, 0000) or through predation of higher-order prey (i.e. the Indo-Pacific swimming crab, Charybdis hellerii; Mantelatto and Dias, 1999). Corbisier et al. (2006) examined the rocky shore food web at a restricted area in Ubatuba (Flamengo sound), using stable isotopes and focusing on large trophic groups, 18 years before the present study, before the invasive species above have been detected in this ecosystem.

The aim of the present study was to conduct an in-depth analysis of the food web occurring in the tropical intertidal rocky shores of Southeastern Brazil, with the aim of 1) describing the general food web structure, 2) estimating food web length, 3) estimating the trophic level of the secondary consumers, and 4) their dependence on different energy pathways. Important attention was given to the new invading species given that their trophic role and dependence on energy pathways are entirely unknown in Brazilian waters.

Stable isotope analysis of δ¹³C and δ¹⁵N was applied in this investigation, since these two isotopes allow the estimation of the food sources, energy pathways and trophic levels of the organisms that compose the food web (e.g. Kwak and Zedler, 1997, Riera et al., 1999, Corbisier et al., 2006, Vinagre et al., 2015, Duarte et al., 2017). The δ¹³C isotope is typically used to determine the origin and pathways of organic matter in food webs, an issue of crucial importance in the understanding of ecosystem’s functioning, since it informs on the relative dependence of the organisms on the different energy pathways feeding the food web. This is possible when the primary sources (e.g. phytoplankton, macroalgae, detritus) are isotopically distinct, which often occurs in transition ecosystems, such as shallow coastal areas and estuaries (Hobson et al., 2002, Le Loc’h and Hily, 2005). Values of δ¹⁵N increase by 2.5–4.5‰ from prey to predator making it a marker of trophic position (Owens, 1987, Peterson and Fry, 1987, Post, 2002). It can thus be used to understand the food web’s basic topology.