Ecology, 0(0), 2019, e02874 © 2019 by the Ecological Society of America Intraguild predation enables coexistence of competing phytoplankton in a well-mixed water column 1,2,3,4 1 1 HOLLY V. M OELLER, MICHAEL G. NEUBERT, AND MATTHEW D. JOHNSON 1Biology Department, Woods Hole Oceanographic Institution, Woods Hole, Massachusetts 02543 USA 2Biodiversity Research Centre, University of British Columbia, Vancouver, British Columbia V6T 1Z4 Canada Citation: Moeller, H. V., M. G. Neubert, and M. D. Johnson. 2019. Intraguild predation enables coexis- tence of competing phytoplankton in a well-mixed water column. Ecology 00(00):e02874. 10.1002/ecy.2874 Abstract. Resource competition theory predicts that when two species compete for a single, finite resource, the better competitor should exclude the other. However, in some cases, weaker competitors can persist through intraguild predation, that is, by eating their stronger competitor. Mixotrophs, species that meet their carbon demand by combining photosynthesis and phago- trophic heterotrophy, may function as intraguild predators when they consume the phototrophs with which they compete for light. Thus, theory predicts that mixotrophy may allow for coexis- tence of two species on a single limiting resource. We tested this prediction by developing a new mathematical model for a unicellular mixotroph and phytoplankter that compete for light, and comparing the model’s predictions with a laboratory experimental system. We find that, like other intraguild predators, mixotrophs can persist when an ecosystem is sufficiently productive (i.e., the supply of the limiting resource, light, is relatively high), or when species interactions are strong (i.e., attack rates and conversion efficiencies are high). Both our mathematical and labora- tory models show that, depending upon the environment and species traits, a variety of equilib- rium outcomes, ranging from competitive exclusion to coexistence, are possible. Key words: community ecology; competition; Micromonas commoda; mixotrophy; model-data comparison; Ochromonas. example, Hutchinson’s description of the “Paradox of INTRODUCTION the Plankton” notes the surprising diversity of phyto- Competition among species for limited resources plays plankton communities despite the fact that their member a fundamental role in structuring ecological communi- species appear to occupy the same resource niche delim- ties. All else equal, when two species are limited by the ited by the availability of light and abiotic resources same available resource, the species that can persist at (Hutchinson 1961). In part, some of this surprisingly the lowest level of the resource when grown in isolation high diversity can be explained by a subtler understand- will competitively displace the weaker competitor ing of resource partitioning among taxa (e.g., use of dif- (Tilman 1977, 1990). This Rà theory (where Rà is the ferent forms of nitrogen in phytoplankton; Moore et al. resource-availability threshold required for a species to 2002) and by non-equilibrium dynamics (as was Hutchin- persist) predicts that the composition of an ecological son’s original point; see Hutchinson 1941, 1961). community can be understood by identifying the Trophic interactions can also enhance community resources that limit each member species. The same the- diversity above resource-based expectations. In addition ory holds for light limitation in planktonic communities: to keystone predators, which exert top-down control on à “ Huisman and Weissing (1994) derived Iout, the critical community composition by feeding on competitively light intensity” to which phytoplankton monocultures superior community members (Paine 1969), intraguild draw down available light in a well-mixed water column. predators, species that eat their competitors, may also à In their analysis, the phytoplankter with the lowest Iout increase community diversity (Polis et al. 1989, Polis competitively excludes all other species. and Holt 1992). Specifically, an intraguild predator that However, the observed diversity of some communities is otherwise a weaker competitor may persist in a com- exceeds predictions grounded in resource theory. For munity by consuming its competitors (Holt and Polis 1997), a mechanism that has been empirically demon- Manuscript received 20 August 2018; revised 9 July 2019; strated in several cases (Diehl and Feissel 2001, Borer accepted 15 July 2019. Corresponding Editor: Jef Huisman. et al. 2003, Price and Morin 2004, Wilken et al. 2013). 3 Present address: Department of Ecology, Evolution & Marine Biology, University of California, Santa Barbara, Santa Intraguild predation is widespread in biological systems, Barbara, California 93106 USA. from protists Diehl and Feissel 2001, Morin 1999) to 4 E-mail: [email protected] insects (Wissinger and McGrady 1993, Borer et al. 2003) Article e02874; page 1 Article e02874; page 2 HOLLY V. MOELLER ET AL. Ecology, Vol. xx, No. xx to mammals (Fedriani et al. 2000), and most attention productivity (i.e., the availability of sunlight). We then has been focused on taxa that compete for a living prey compared our theoretical results with experiments using item as opposed to a common, abiotic resource (Arim and two widely distributed marine planktonic taxa. Our Marquet 2004). In contrast, in planktonic communities, analysis highlights the generality of intraguild predation mixotrophy is a common form of intraguild predation by as a mechanism for coexistence and enhanced diversity which predators and their prey compete for an abiotic among organisms that share a resource niche. resource (Thingstad et al. 1996, Wilken et al. 2014b). Mix- otrophic species, which combine photosynthesis with pha- The model gotrophic heterotrophy, come in two forms: (1) Algae that ingest prey are termed constitutive mixotrophs because To study the effects of intraguild predation on the they maintain and regulate their own permanently incor- coexistence dynamics of two competing phytoplankton porated plastids. (2) Protozoa that host symbiotic algae or species, we modified the classic model of Huisman and steal their plastids are known as non-constitutive mixo- Weissing (1994) for phytoplankton living in a well-mixed trophs because, in the absence of prey, they lack photosyn- water column (i.e., each cell experiences, on average, the thetic machinery (Flynn and Hansen 2013, Mitra et al. same amount of light). At a given depth z, the biomass- 2016). Constitutive mixotrophs (referred to as “mixo- specific growth rate gi of a phytoplankter of species i is trophs” hereafter) function as intraguild predators when determined by the difference between its photosynthetic their prey are the phytoplankton with which they compete rate, which is a function of its inherent maximum rate of for light and inorganic nutrients. Mixotrophs are thought carbon uptake via photosynthesis pi and local light avail- to gain a competitive advantage over phytoplankton ability IðzÞ, and its respiration rate ‘i. Thus because they can continue to obtain limiting nutrients, in addition to organic carbon, by grazing (Rothhaupt 1996b, IðzÞ giðzÞ¼pi À ‘i (1) Mitra et al. 2016). Their ability to supplement their ener- hi þ IðzÞ getic and carbon needs through photosynthesis also gives them a competitive advantage over pure heterotrophs where hi is the light level at which half the maximum when prey are scarce (Rothhaupt 1996a,Titteletal.2003). photosynthetic rate is achieved. (All variables and To date, most studies of mixotroph persistence have parameters are listed in Table 1). focused on competition for nutrients. A number of theo- Following Huisman and Weissing (1994), we assumed retical studies have modeled mixotroph persistence in that available light declines with depth following the communities that also contain autotrophs (e.g., phyto- Lambert-Beer law and that each species has a per-cell plankton) and heterotrophs (e.g., bacteria; Crane and light absorptivity ki. Because the water column is well- Grover 2010, Cropp and Norbury 2015, Thingstad et al. mixed, the cell density wi for each species does not 1996), leading to the prediction that mixotrophs should depend on depth. As a result of absorption, the light ð Þ become dominant in ecosystems in which nutrients are intensity I z decreases with depth from the incident limiting (Mitra et al. 2016). This prediction is consistent level Iin at the surface according to with the observation that mixotrophs are particularly ð Þ¼ ½ð þ Þ : abundant in open ocean oligotrophic gyres (Hartmann I z Iin exp k1w1 k2w2 z (2) et al. 2012) and in coastal ecosystems where a single Integrating over the total depth of the water column, nutrient, such as phosphorus, is scarce (Burkholder the rate of change in each of the two species’ total bio- et al. 2008). However, Rothhaupt (1996a) showed that mass W and W is given by the persistence of mixotrophs alongside strictly hetero- 1 2 trophic competitors depended upon the availability of dW p W light and food as joint-limiting resources. 1 ¼ 1 1 dt k W þ k W Here, we instead focus on competition between mixo- 11 2 2 þ (3) trophs and their intraguild prey for sunlight. In keeping h1 Iin À ‘ ln þ ½ðÞþ 1W1 with intraguild predation theory, mixotrophs should h1 Iin exp k1W1 k2W2 gain a competitive advantage when light is the sole limit- ing resource because, by consuming their phytoplankton dW2 ¼ p2W2 dt k W þ k W competitors, they reduce competition for light. In this 11 2 2 (4) paper, we report on our test of this prediction