Food Web Interactions Determine Energy Transfer Efficiency and Top Consumer Responses to Inputs of Dissolved Organic Carbon
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Hydrobiologia (2018) 805:131–146 DOI 10.1007/s10750-017-3298-9 PRIMARY RESEARCH PAPER Food web interactions determine energy transfer efficiency and top consumer responses to inputs of dissolved organic carbon R. Degerman . R. Lefe´bure . P. Bystro¨m . U. Ba˚mstedt . S. Larsson . A. Andersson Received: 1 July 2016 / Revised: 15 June 2017 / Accepted: 23 June 2017 / Published online: 15 July 2017 Ó The Author(s) 2017. This article is an open access publication Abstract Climate change projections indicate conclude that the added DOC either acted as a subsidy increased precipitation in northern Europe, leading by increasing the production of the top trophic level to increased inflow of allochthonous organic matter to (mesozooplankton), or as a sink causing decreased top aquatic systems. The food web responses are poorly consumer production (planktivorous fish). known, and may differ depending on the trophic structure. We performed an experimental mesocosm Keywords Food web efficiency Á Carbon transfer Á study where effects of labile dissolved organic carbon Allochthonous dissolved organic carbon Á Mesocosm Á (DOC) on two different pelagic food webs were Planktivorous fish investigated, one having zooplankton as highest trophic level and the other with planktivorous fish as top consumer. In both food webs, DOC caused higher bacterial production and lower food web efficiency, Introduction i.e., energy transfer efficiency from the base to the top of the food web. However, the top-level response to Knowledge about pathways and constraints of energy DOC addition differed in the zooplankton and the fish transfer through food webs is fundamental for the systems. The zooplankton production increased due to understanding of ecosystem function (e.g., Dickman efficient channeling of energy via both the bacterial et al., 2008; Wollrab et al., 2012). The complexity of and the phytoplankton pathway, while the fish pro- food web dynamics and structure inherently means duction decreased due to channeling of energy mainly that both changes in basal production and top–down via the longer and less efficient bacterial pathway. We control can create alternative pathways of energy flow up to the highest trophic level, resulting in patterns of energy transfer and productivity commonly deviating Handling editor: Jonne Kotta from expectations based on classical food chain theory (Vadeboncoeur et al., 2004, Hulot et al., 2014). For R. Degerman Á R. Lefe´bure Á P. Bystro¨m Á example, the presence or absence of classic trophic U. Ba˚mstedt Á S. Larsson Á A. Andersson (&) Department of Ecology and Environmental Science, cascades in marine food webs has been suggested to be Umea˚ University, 901 87 Umea˚, Sweden dependent on the size structure of the phytoplankton e-mail: [email protected] community (Stibor et al., 2004). In aquatic systems, phytoplankton (autotrophs) and R. Degerman Á R. Lefe´bure Á U. Ba˚mstedt Á S. Larsson Á A. Andersson bacteria (heterotrophs) are basal producers, acting as Umea˚ Marine Science Centre, 905 71 Ho¨rnefors, Sweden energy source for higher trophic levels, and thus shape 123 132 Hydrobiologia (2018) 805:131–146 the food webs depending on their production and consumers are planktivorous fish, they suppress the composition (Azam et al., 1983; Legendre & Ras- zooplankton abundance which in turn releases phyto- soulzadegan, 1995, Jansson et al., 2007). The balance plankton from grazing pressure (e.g., Carpenter et al., between autotrophs and heterotrophic bacteria is 1985; Shiomoto et al., 1997; Ordo´n˜ez et al., 2010). governed by both bottom–up factors such as nutrient This may also increase bacterial abundance as zoo- availability, and top–down effects, e.g., trophic inter- plankton predation on ciliates decreases, causing actions via top predators (Carpenter et al., 1985; increased ciliate density and hence a higher grazing Hairston & Hairston, 1993, Vanni & Layne, 1997). pressure on HNF, the main predator on bacteria These food webs are complex, as many consumers (Christoffersen et al., 1993; Nishimura et al., 2011). feed on organisms from both the phytoplankton and Effects on food web dynamics and top consumer the bacterial pathway. Both phytoplankton and bacte- production can therefore be dependent on both the ria are osmotrophic organisms competing for inor- access to dissolved organic carbon (DOC) for hetero- ganic nutrients, nevertheless phytoplankton utilize trophic bacteria and the nature and composition of the inorganic forms of carbon while heterotrophic bacteria top consumers in the system. are in many systems dependent on autochthonous Food web efficiency (FWE) is a measure of the organic carbon produced by phytoplankton (Cole overall system efficiency and is defined as the et al., 1988). However, in aquatic systems influenced proportion of basal production that reaches the top by allochthonous dissolved organic carbon (ADOC), consumers (Rand & Stewart, 1998; Berglund et al., bacteria can be decoupled from autochthonous pro- 2007; Lefe´bure et al., 2013). Changes in the relative duction (Karlsson et al., 2002, Stibor et al., 2004). importance of autotrophic and heterotrophic basal Accordingly, in systems with high inputs of ADOC, production, induced either by top–down or bottom–up heterotrophic bacteria tend to contribute substantially drivers, will affect the energy transfer to higher trophic to the total basal production (Pace et al., 2004; levels since bacteria are of poor nutritional quality Berglund et al., 2007, Jansson et al., 2007). Phyto- (i.e., have low C:P ratio, Fagerbakke et al., 1996) and plankton are often directly consumed by primary the heterotrophic-based pathway channels the carbon consumers like mesozooplankton, whereas bacteria through more trophic levels before it reaches top are too small to be readily eaten by such organisms. consumers (Hessen & Andersen, 1990; Sommer et al., Instead, bacteria are consumed by protozoans which in 2002; Brett et al., 2009). As it is estimated that each turn are consumed by mesozooplankton (Hessen & trophic coupling will result in *70% of the Andersen, 1990, Brett et al., 2009). Hence, the energy/carbon loss due to sloppy feeding and meta- heterotrophic-based pathway, i.e., the microbial food bolic losses (e.g., Welch, 1968; Straile, 1997), a web, will have a more complex pattern of energy smaller fraction of the basal production is therefore transfer compared to systems dominated by auto- thought to reach the highest trophic level in food webs trophic production (Sommer et al., 2002; Berglund dominated by heterotrophic production. Accordingly, et al., 2007). it has been shown that FWE in heterotrophic food At the top of the food web, interactions between webs can be up to tenfold lower than in autotrophic predator and prey may also yield strong effects on food webs, due to 1 or 2 extra intermediate trophic levels web function and structure, but the nature and (Berglund et al., 2007). The FWE can also be affected composition of top consumer organisms in the food by other factors, such as the food size preference of the web will exert different top–down impacts on lower inherent mesozooplankton. trophic levels (Hairston & Hairston, 1993, Vanni & The study of the effects of ADOC on pelagic Layne, 1997, Hulot et al., 2014). For instance, in food food webs has gained scientific interest (Pace et al., webs where mesozooplankton function as top preda- 2004; Jansson et al., 2007), largely related to tor, consumption rates on phytoplankton and ciliates climate change predictions of increased run-off of have been shown to be high (Johansson et al., 2004; ADOC to aquatic environments (IPCC, 2007; Calbet & Saiz, 2005; Sommer & Sommer, 2006), HELCOM, 2007). However, most studies have releasing heterotrophic nanoflagellates (HNF) from focused on a limited number of links in the food predation which in turn cause decreased bacterial web to either include only e.g., microbes to abundances (Zo¨llner et al., 2009). In contrast, if top zooplankton (Sterner et al., 1998; Berglund et al., 123 Hydrobiologia (2018) 805:131–146 133 2007; O’Connor et al., 2009) or only phytoplankton Materials and methods or zooplankton to fish (Malzahn et al., 2007; Dickman et al., 2008). With the exception of Experimental design Faithfull et al. (2011, 2012) and Lefe´bure et al. (2013), very few studies have experimentally inves- Four experimental treatments, with three replicates tigated FWE dynamics in systems encompassing each, were used to test differences in food web food webs with both phytoplankton and bacteria at efficiency and productivity in systems with contrasting the base and fish at the top of the food web. structure at the basal trophic level and with food webs Understanding patterns of energy flow in aquatic of differing length (Fig. 1). The basal production systems has proven to be challenging, where even structure was manipulated by adding nitrogen (N) and simplistic food chains can yield highly variable phosphorous (P) to induce a phytoplankton-based food results (Dickman et al., 2008; Heath et al., 2014). web and by adding N, P, and carbon (C) to obtain a Furthermore, there is currently a gap in the bacteria-based food web. A labile carbon source, scientific understanding of how top-down effects glucose, was added to one of the systems to promote can propagate through the food web and impact bacterial growth. Inorganic nutrients were added to the both biomass and production of lower-level auto- other system to promote phytoplankton growth. The trophic and heterotrophic organisms (Hessen & trophic position at the top of the food web was Kaartvedt, 2014). As outlined above, the interplay manipulated by having either a natural zooplankton between top-down predation and bottom-up produc- assemblage as top predator or by the addition of tivity dynamics can profoundly influence food web zooplanktivorous fish, juvenile three-spined stickle- structure and efficiency, and the empirical studies back (Gasterosteus aculeatus). that have investigated these dynamics on natural The experiment was carried out in autumn (Novem- marine food webs are to a large extent lacking.