Marine meso-herbivore consumption scales faster with temperature than seaweed primary production

https://doi.org/10.1016/j.jembe.2016.01.009Get rights and content

Highlights

  • Temperature shapes marine plant-herbivore interaction.

  • Meso-herbivore consumption varies with temperature.

  • Grazer consumption and algal photosynthesis scale differently with temperature.

Abstract

Respiration of ectotherms is predicted to increase faster with rising environmental temperature than photosynthesis of primary producers because of the differential temperature dependent kinetics of the key enzymes involved. Accordingly, if biological processes at higher levels of complexity are constrained by underlying metabolic functions, food consumption by heterotrophs should increase more rapidly with rising temperature than photo-autoptrophic primary production. We compared rates of photosynthesis and growth of the benthic seaweed Fucus vesiculosus with respiration and consumption of the isopod Idotea baltica to achieve a mechanistic understanding why warming strengthens marine plant–herbivore interactions. In laboratory experiments thallus pieces of the seaweed and individuals of the grazer were exposed to constant temperatures at a range from 10 to 20 °C. Photosynthesis of F. vesiculosus did not vary with temperature indicating efficient thermal acclimation whereas growth of the algae clearly increased with temperature. Respiration and food consumption of I. baltica also increased with temperature. Grazer consumption scaled about 2.5 times faster with temperature than seaweed production. The resulting mismatch between algal production and herbivore consumption may result in a net loss of algal tissue at elevated temperatures. Our study provides an explanation for faster decomposition of seaweeds at elevated temperatures despite the positive effects of high temperatures on algal growth.

Introduction

Metabolic rates of organisms are strongly controlled by temperature because the underlying biochemical reactions are governed by the fundamental laws of thermodynamics. Depending on the reactions and enzymes involved metabolic processes display specific responses to changes in temperature. In a physiologically relevant temperature range respiration has been predicted to increase faster with rising temperature than photosynthesis because of the specific temperature-dependency of the kinetics of ATP synthesis in the respiratory complex and Rubisco carboxylation (Allen et al., 2005). The general validity of this prediction is supported by a global analysis of rates of respiration and photosynthesis of diverse organisms from a wide range of ecosystems including marshes, grasslands, forests and shrublands and oceanic plankton (Allen et al., 2005). Accordingly, temperature controls metabolic functions of entire ecosystems, such as the potential of the oceans for capturing CO2, through its effects on the metabolic rates of the constituent individuals (López-Urrutia et al., 2006).

In addition to the direct metabolic effects temperature can indirectly shape the structure and functioning of ecosystems by altering the outcome of species interactions (Kordas et al., 2001). Metabolic theory of ecology predicts that processes at more complex levels of biological organization are constrained by the rates of underlying metabolic processes and their thermal responses (Brown et al., 2004). Therefore, heterotrophic processes, such as food uptake by consumers, should scale faster with temperature than primary production by photo-autotrophs. Accordingly, plant–herbivore interactions provide ideal systems to develop testable hypotheses concerning ecosystem effects of global warming because they allow for directly contrasting herbivore consumption and plant primary production.

Previous studies in the marine environment revealed significant effects of temperature on plant–herbivore interactions but did not confirm a direct temperature effect on herbivore consumption (e.g. Thompson et al., 2004, Morelissen and Harley, 2007). There is strong evidence that floating seaweeds in the North Sea and in the SE Pacific decompose more rapidly in warm waters, presumably because the algae are unable to compensate for enhanced herbivore grazing at elevated temperatures (Vandendriessche et al., 2007, Rothäusler et al., 2009). The authors report on net-changes in algal biomass. However, they do not explicitly compare rates of algal primary production and herbivore feeding in order to mechanistically explain the loss in algal biomass at higher temperatures despite enhanced seaweed growth. Warming was found to increase the per capita interaction strength (i.e. the effect of a consumer on its prey) between the herbivorous amphipod Ampithoe longimana and the seaweed Sargassum filipendula, which was indicated by a reduced biomass of the seaweed in the presence of the grazer at elevated non-lethal temperature (O'Connor, 2009). Higher temperature had a positive effect on algal growth. However, the consumption rate of the grazer was independent of temperature and thus, did not explain the enhanced net-loss of algal biomass at higher temperatures.

Generally, there is only weak evidence for an influence of temperature on the consumption rates of small benthic marine herbivores (meso-herbivores). Accordingly, other factors such as body size and food availability have been suggested to be more important determinants of feeding activity in marine herbivores (Hillebrand et al., 2009, Saiz and Calbet, 2011). Yee and Murray (2004) showed that consumption rates of medium-sized gastropods of the genus Tegula from California vary with temperature. However, this result disagrees with the temperature-independent feeding rates of herbivorous amphipods (O'Connor, 2009, Poore et al., 2013) and isopods (Gutow et al., 2014). Strong and Daborn (1980a) found seasonal variations in the feeding rates of the isopod Idotea baltica from Nova Scotia (Canada) but did not separate the effects of temperature, body size and potential seasonal variations in seaweed palatability.

We studied the thermal responses of the benthic seaweed Fucus vesiculosus and its consumer, the marine isopod I. baltica, in order to investigate mechanisms that influence the outcome of a marine plant–herbivore interaction at different temperatures. Both species are common components of coastal marine and brackish ecosystems of the NE Atlantic region. F. vesiculosus forms extensive inter- to subtidal canopies on rocky shores and provides food and shelter for a great variety of associated organisms (Wikström and Kautsky, 2007). I. baltica is the dominant consumer of F. vesiculosus in the Baltic (Engkvist et al., 2000). On floating seaweeds in the North Sea I. baltica reaches exceptionally high densities and contributes substantially to the decomposition of algal rafts (Gutow et al., 2015). We studied the influence of temperature on metabolism and related somatic processes of the two species. Based on the predictions of the metabolic theory of ecology we tested the hypotheses that (i) respiration of I. baltica increases faster with temperature than photosynthesis of F. vesiculosus and (ii) food consumption of the grazer increases faster with temperature than primary production of the seaweed. Laboratory experiments were performed at a temperature range from 10 to 20 °C, which corresponds to natural ambient temperatures in the southern coastal North Sea including incidental maximum values (Wiltshire and Manly, 2004).

Section snippets

Seaweed photosynthesis and growth

F. vesiculosus was collected in January 2013 at low tide from a rocky intertidal groin in the German Wadden Sea (North Sea) near List harbor at the island of Sylt (55°01.02′ N, 008°26.43′ E). One apical piece of about 2 cm length was cut off with a scissor from each randomly selected algal thallus. The pieces were kept humid in a cooler overnight for transport to the laboratories of the Alfred Wegener Institute in Bremerhaven. Upon arrival the distal tips of 1 cm length were cut off the algal

Seaweed photosynthesis and growth

The average (± SEM) photosynthesis of F. vesiculosus remained fairly constant over the temperature range from 10 to 18 °C with only minor variations between 13 °C (31.8 ± 3.8 μmol O2 · g 1 · h 1) and 10 °C (33.6 ± 3.6 μmol O2 · g 1 · h 1; Fig. 1A). At the highest temperature of 20 °C the photosynthesis was slightly elevated. However, the difference to the photosynthesis at all other temperatures was statistically not significant (F4,29 = 0.47; p = 0.75). The overall mean rate of oxygen evolution was 34.3 ± 2.1 μmol O2 · g

Discussion

Temperature profoundly influences biological processes at all levels of organization from the kinetics of enzymes to complex ecosystem processes. Species typically have specific temperature tolerance ranges in which metabolic and somatic processes scale predictably with temperature. We confirmed the temperature sensitivity of growth of F. vesiculosus as well as respiration and food consumption of the meso-herbivore I. baltica. Apart from the photosynthesis of F. vesiculosus, which was

Acknowledgments

The authors appreciate the helpful comments of two anonymous reviewers. This work was carried out within the framework of the PACES II program of the Helmholtz Association. [SW]

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