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The biodiversity of food webs is composed of horizontal (i.e. within trophic levels) and vertical Qinghua Zhao, Paul J. Van 1,2 diversity (i.e. the number of trophic levels). Understanding their joint effect on stability is a key den Brink,* Camille challenge. Theory mostly considers their individual effects and focuses on small perturbations near Carpentier, Yingying X. G. equilibrium in hypothetical food webs. Here, we study the joint effects of horizontal and vertical Wang, Pablo Rodrıguez- 1 5 diversity on the stability of hypothetical (modelled) and empirical food webs. In modelled food Sanchez, Chi Xu, Silke 1 1 webs, horizontal and vertical diversity increased and decreased stability, respectively, with a stron- Vollbrecht, Frits Gillissen, ger positive effect of producer diversity on stability at higher consumer diversity. Experiments Marlies Vollebregt, Shaopeng with an empirical plankton food web, where we manipulated horizontal and vertical diversity and Wang, and Frederik De measured stability from species interactions and from resilience against large perturbations, con- Laender, firmed these predictions. Taken together, our findings highlight the need to conserve horizontal biodiversity at different trophic levels to ensure stability. Keywords Equilibrium, horizontal diversity, large perturbations, small perturbations, stability, vertical diver- sity. Ecology Letters (2019) 22: 1152–1162 higher number of consumer species decrease the per capita INTRODUCTION energy flux in consumer–resource interactions by decreasing Diversity (i.e. species richness) within food webs is important the per capita consumption rate (Crowder et al. 1997; Perna for sustaining ecosystem functions such as biomass produc- et al. 2004; Finke & Denno 2005), hence stabilising the con- tion, energy flow and nutrient uptake (Otto et al. 2007; Roo- sumer–resource links (Rip & Mccann 2011; Gilbert et al. ney & McCann 2012; Soliveres et al. 2016; Barnes et al. 2018; 2014). Producer diversity can increase stability (McCann Wang & Brose 2018). Diversity can be characterised in two 2000) by increasing the potential for niche differentiation dimensions (Duffy et al. 2007; Srivastava & Bell 2009; Wang among consumers (Novotny et al. 2006; Jetz et al. 2009; Poi- & Brose 2018): the number of species within trophic levels sot et al. 2013) or again weaken consumer–resource interac- (i.e. horizontal diversity) and the number of trophic levels (i.e. tions (Berlow 1999; Hillebrand & Cardinale 2004; Edwards vertical diversity). Horizontal and vertical diversity both affect et al. 2010; Moore & de Ruiter 2012). In contrast, vertical the functioning and stability of food webs, via different mech- diversity is expected to decrease stability in simple food chains via increasing recovery times (Pimm & Lawton 1977; anisms (Duffy et al. 2007). Effects of horizontal diversity are driven by competitive interactions, while effects of vertical Morin & Lawler 1995; Post 2002). This negative vertical diversity are mediated by predation. Horizontal and vertical diversity effect has been evoked as an explanation for the lim- diversity may interact with each other (Duffy et al. 2007). For ited number of trophic levels in natural food webs (Pimm & instance, producer coexistence can be indirectly mediated by Lawton 1977; Morin & Lawler 1995; McHugh et al. 2010; consumer diversity (Brose 2008). Sabo et al. 2010). Until now, the effects of horizontal and vertical diversity In natural systems, horizontal and vertical diversity will on food web stability (i.e. via local stability analysis) have vary jointly. For example, the decrease in vertical diversity been mostly treated separately (Pimm & Lawton 1977; Duffy (e.g. the extinction of top predators) could cause cascades that et al. 2007), and mainly using small trophic modules (Pimm lead to species extinction, lowering horizontal diversity & Lawton 1977; McCann et al. 1998; Thebault & Loreau (Crooks & Soule 1999; Borrvall & Ebenman 2006; Srivastava 2005). No information is available on their joint effect in & Bell 2009). In addition, ecosystem succession and degrada- multitrophic food webs. Horizontal diversity of consumers is tion often change both horizontal and vertical diversity (Ferris & Matute 2003; Maharning et al. 2009; Yang et al. 2018). expected to increase stability (McCann et al. 1998), because a 1 4 Aquatic Ecology and Water Quality Management Group, Wageningen Resource Ecology Group, Wageningen University, Droevendaalsesteeg 3a, University, P.O. Box 47, 6700 AA, Wageningen, The Netherlands 6708 PB, Wageningen, The Netherlands 2 5 Wageningen Environmental Research, P.O. Box 47, 6700 AA, Wageningen, School of Life Sciences, Nanjing University, Nanjing 210023, China The Netherlands Institute of Ecology, College of Urban and Environmental Science, and Key Research Unit of Environmental and Evolutionary Biology, Namur Institute Laboratory for Earth Surface Processes of the Ministry of Education, Peking of Complex Systems, and Institute of Life, Earth, and the Environment, University, 100871, Beijing, China University of Namur, Rue de Bruxelles 61, 5000,Namur, Belgium *Correspondence: E-mail: paul.vandenbrink@wur.nl © 2019 The Authors. Ecology Letters published by CNRS and John Wiley & Sons Ltd. This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made. Letter Horizontal and vertical diversity shape stability 1153 Hence, it is critical to understand how horizontal (both pro- diversity (2 or 3 trophic levels). This design reflects the empir- ducer and consumer) and vertical diversity interact and shape ically observed triangularity of food webs (Woodward et al. food web stability. 2005; Turney & Buddle 2016). We deliberately omitted omni- The individual effects of horizontal and vertical diversity on vores (species consuming at multiple trophic levels), because local stability are often examined by analysing the Jacobian omnivores have already been proven to stabilise food webs matrix (hereafter ‘Jacobian’). This approach assumes that sys- by creating weak predator–prey interactions (Neutel et al. tems are near equilibrium and exposed to small perturbations 2002, 2007). Food web connectance (i.e. the number of links (May 2001; Allesina & Tang 2012, 2015). However, ecosys- divided by the square of the number of species) was set to tems are often far away from equilibrium (Allesina & Tang 0.10 (Williams et al. 2002; Dunne et al. 2002a,2002b). The 2015) and face large perturbations (De Laender et al. 2016). links were randomly distributed between adjacent trophic This makes it uncertain whether stability analyses based on levels. the Jacobian provide useful information for real-world pertur- We described community dynamics with generalised Lotka– bations (May 2001). Alternative stability measures have there- Volterra equations (eqn 1) (Emmerson & Yearsley 2004; fore been proposed (Grimm & Wissel 1997; Arnoldi et al. Gibbs et al. 2018; Maynard et al. 2018): 2016; Donohue et al. 2016). Examples include population dN recovery and resistance following severe perturbations (Isbell ¼ N b þ a N ð1Þ i i ij j dt et al. 2015; Baert et al. 2016; Hillebrand et al. 2018) and the coefficient of temporal variation of population dynamics where N and N are the population density of species i and j, i j (McCann 2000; Pennekamp et al. 2018). Recent work indi- respectively; b is the intrinsic per capita growth rate of species cates that these alternative stability measures may correlate i. The b is positive for producers, where it represents the den- poorly (Ives & Carpenter 2007; Montoya et al. 2013; Hille- sity-independent growth rate, while b is negative for con- brand et al. 2018; Radchuk et al. 2019). For example, tempo- sumers and predators, where it represents a death rate. The a ij ral stability is positively associated with diversity, while the is the per capita effect of species j on the growth rate of spe- latter is negatively correlated with resistance (Pennekamp cies i. et al. 2018). The growth rate b for all producers was equal to 1, which In this paper, we combine models and experiments to exam- guaranteed that emergent food web patterns were a direct ine the joint effect of horizontal and vertical diversity on food effect of horizontal/vertical diversity, rather than fitness differ- web stability. We define stability using two kinds of metric: ences among species (Maynard et al. 2018). For consumers either based on the assumption of small near equilibrium per- and predators, we randomly drew b from a uniform distribu- turbations or based on biomass and compositional recovery tion U(0.001, 0) while b for predators was generated from following large perturbations away from equilibrium. To this U(0.0001,0) (Eklof € & Ebenman 2006). We ensured that the end, we first analysed the joint effect of horizontal (the num- b of predators was less negative than the b of consumers, i i ber of producer/consumer species) and vertical diversity (the because species at higher trophic levels often have larger body number of trophic levels) on the Jacobian-based stability of sizes and therefore lower mortality rates (Borrvall et al. 2000). randomly created food webs. Second, we manipulated hori- We ensured that intraspecific competition a (i = j) was stron- ii zontal and vertical diversity in an experiment with a plank- ger for primary producers (1) than for consumers and tonic food web and quantified their joint effect on stability, predators (0.1) (Berg et al. 2011; Kadoya et al. 2018). Inter- measured using empirically established Jacobian matrices. specific competitions a (i 6¼ j) among producers were sampled ij Finally, we quantified the effect of horizontal and vertical from U(0.5, 0) and set symmetrically to avoid cycling or diversity on the stability of the same food web, but now mea- chaos (Eklof € & Ebenman 2006; Maynard et al. 2018). Con- sured as resilience following large perturbations caused by sumers competed indirectly by sharing producers, and direct two types of chemicals. interspecific interactions among consumers were thus set to Overall, our results show for the first time that the positive zero (Eklof & Ebenman 2006). effect of producer diversity on stability increases with con- Finally, the a (i 6¼ j), the per capita effect of consumers (or ij sumer diversity, regardless of vertical diversity. In contrast, predators) species j on the per capita growth rate of producers vertical diversity always decreased stability. This trend (or prey) species i, was sampled from U(0.5, 0) when a con- emerged from all analyses and suggests that conserving diver- sumer (or predator) only consumed one producer (or prey) sity within multiple trophic levels is key to promote food web (Eklof € & Ebenman 2006). Considering that interaction stability. strengths in natural system communities often have skewed distributions with mostly weak and only few strong interac- tions (Borrvall et al. 2000), one strong a was sampled from ij MATERIALS AND METHODS U(0.4, 0) and assigned randomly (Eklof € & Ebenman 2006), Model and simulations if the number of producers (or prey) was larger than one. The weak a was sampled from U(0.1,0) divided by the number ij We conducted a full factorial design with 24 food web config- of prey species minus one (Borrvall et al. 2000; Borrvall & urations: four levels of horizontal diversity at the first trophic Ebenman 2006). Hence, the total effect of a consumer (or level (producer diversity equalled 6, 7, 8 or 9), three levels of predator) on all its producers (or prey), a , always varied ij horizontal diversity at the second trophic level (consumer between 0.5 and 0, but the average per capita effect of a diversity equalled 3, 4 or 5) and two levels of vertical © 2019 The Authors. Ecology Letters published by CNRS and John Wiley & Sons Ltd. 1154 Q. Zhao et al. Letter consumer (or predator) on its producers (or prey) decreased diversity (2 or 3 trophic levels) in a full factorial design with the number of producers (or prey) (McCann et al. 1998; (Table S2). At all combinations, we estimated interactions Borrvall et al. 2000). A rationale for this approach and more (within and between trophic levels) to characterise the Jaco- details can be found in the Supplementary Information S1. bian on day 21 after the start of the experiment. The off-diag- The effect of producers (or prey) on consumers (or predators) onal elements of this matrix are per capita interactions, which is given by a , which is positive: a ¼k a , with k repre- we estimated as the per capita material fluxes between con- ji ji ij senting the efficiency of the resources being converted into sumers (or predators) and producers (or consumers) (de Rui- consumers, which was set at 0.2 (Borrvall & Ebenman 2006; ter et al. 1995; Neutel et al. 2007; Schwarz et al. 2017). The Eklof € & Ebenman 2006). effect of consumers (or predators) on producers (or con- ij Per food web configuration, we created 10 000 food webs, sumers) is given by J ¼ , and the effect of producers (or ji ij yielding 240 000 food webs. For each food web, we calculated consumers) on consumers (or predators) is given by J ¼ e , ij j stability as follows. First, we calculated equilibrium popula- where F is the energy flux from i to j (e.g. from producers to ij tion density (directly solving the equations 0 ¼ b þ a N consumers), e is the assimilation efficiency of j, and M and i ij j j i on eqn 1) and verified if all equilibrium densities were posi- M (g m ) are the biomass of i and j, respectively (Schwarz tive. If this was the case, we retained the particular food web; et al. 2017). The diagonal elements of the Jacobian are otherwise, we discarded it. For each food web configuration, J ¼s , where X is the metabolism of trophic level i, and ii i more than 95% of the generated food webs were feasible with s is a free parameter between 0 and 1 (Schwarz et al. 2017). positive equilibrium densities (Table S1). Next, we used these Because s cannot be determined empirically in complex food equilibria to compute the Jacobian for this food web. Finally, webs, we determined the smallest s leading to all eigenvalues we quantify stability using the recovery time, defined as the of the Jacobian having negative real parts. The value of s rep- negative reciprocal of the real part of the dominant eigen- resents the stability of the community against small perturba- value of the Jacobian, that is (1=realðk )) (Pimm & Law- tions, assessed based on estimated interactions (Schwarz et al. max ton 1977; Emmerson & Yearsley 2004; Moore & de Ruiter 2017). It is therefore conceptually similar to recovery time 2012). A larger recovery time indicates a lower stability. (smaller values indicate more stable food webs) obtained with Finally, we conducted two sensitivity analyses to inspect how the model and is referred to as the degree of self-damping. our results changed with the selected parameter ranges Details on the calculation of F , X and M are provided in the ij i (Figs. S1–S3). Supplementary Information S3. Experiments: general conditions Experiment 2: large perturbations We experimentally tested the effect of horizontal and vertical The objective of this experiment was to examine how horizon- diversity on the stability of a freshwater plankton food web tal and vertical diversity affected the stability against large representative of Dutch ditches. These two experiments, each perturbations. Here, we applied functional and compositional lasted for 21 days, were performed in 900-mL glass jars, filled resilience as stability metrics. We manipulated the same exper- with 500 mL WC medium (Guillard & Lorenzen 1972; Fren- imental factors as in experiment 1 and added one additional ken et al. 2018) and contained in a water bath at constant factor: pesticide exposure (absent or present). We performed temperature (19.9 C 0.8 C) and a light regime of this experiment twice, once using the insecticide chlorpyrifos 1 1 12 h : 12 h (light : dark). The light intensity at the surface (1 lgL ) and once using the herbicide linuron (100 lgL ), (measured with a LI-COR LI-250A, LI-COR Biosciences, selectively targeting consumers and producers, respectively 2 1 Lincoln, USA) was 120 lmol m s and was created using (Wijngaarden et al. 1996; Daam et al. 2009). Experimental Ceramalux Philips 430 Watt High Pressure Sodium Non- procedures were identical to the experiment 1. Information on Cycling Lamps. We worked with field-collected organisms (de- chemical administration is provided in Supplementary Infor- tails are in the Supplementary Information S2). The total ini- mation S4. We measured community biomass, community tial biovolume of producers (algae) and consumers composition (using the same methods as for experiment 1 and 3 3 (invertebrate grazers) was always 25 mm and 0.2 mm , on days 6 and 21) and stability. To measure stability, we first respectively, regardless of producer and consumer diversity measured functional resilience (the recovery rate of total bio- (richness). For the systems with three trophic levels, we added mass) as (Isbell et al. 2015; Baert et al. 2016): one individual of predator Chaoborus to each system. The predators used in the experiments had mean individual body B B control;6 stress;6 functional resilience ¼ ð2Þ length 11.21 0.04 mm. In both experiments, we worked B B control;21 stress;21 with four replicates. where B , B , B and B represent the control,6 control,21 stress,6 stress,21 total biomass in the control (no pesticide) and exposure (pesti- Experiment 1: empirical Jacobian matrices cide present) on days 6 and 21. Functional resilience is > 1if The aim of the experiment was to examine how stability, biomass differences between the control and stress treatment based on empirically constructed Jacobian matrices, varied decrease between day 6 and day 21, and < 1 otherwise. Larger with horizontal and vertical diversity. We manipulated hori- values mean faster recovery. zontal diversity, at the first (producers; 1 or 5 species) and sec- Next, we measured compositional resilience (compositional ond trophic level (consumers; 1 or 4 species), and vertical recovery) (Baert et al. 2016; Hillebrand et al. 2018): © 2019 The Authors. Ecology Letters published by CNRS and John Wiley & Sons Ltd. Letter Horizontal and vertical diversity shape stability 1155 here was always three, so we could only analyse the effects of 0 1 BC zfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflffl}|fflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflffl{ horizontal diversity. B C N N i control;21 i stress;21 B i C To the data from experiment 2, we again used linear mixed- P P compositional resilience ¼ B1 C @ N þ N A effects models (species identity was again a random effect) to i control;21 i stress;21 i i test for the effect of producer, consumer and vertical diversity, 0 1 BC and their pairwise interactions on the two measures of recov- zfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflffl}|fflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflfflffl{ ery (eqns 2 and 3). Because these measures depend on how B C N N B i control;6 i stress;6 C 1 P P total biomass changed with time, we also included sampling B C @ A N þ N i control;6 i stress;6 i i time and chemical concentrations into the analysis of total biomass. All models were fitted with the lme4 package in R (Bates et al. 2014). ð3Þ Compositional resilience can be considered an abundance- based change of Bray–Curtis similarity between day 6 (BC ) RESULTS and day 21 (BC ) (Baert et al. 2016; Hillebrand et al. 2018), Model simulations where N is abundance of species i. Positive values reflect that compositions of the control and disturbed communities con- Producer and consumer diversity both promoted stability, that verge between day 6 and day 21, while negative values imply is, decreased recovery time (Fig. 1). The positive effect of pro- compositional divergence. Again, larger values mean faster ducer diversity on stability increased with increasing consumer recovery. diversity, and this trend was not qualitatively changed by ver- tical diversity. Vertical diversity on itself always decreased sta- bility. Stability was highest at high horizontal (producer and Analysis of simulated and empirical data consumer) diversity and low vertical diversity, and lowest at To the simulated data, we applied linear regression to estimate low horizontal diversity and high vertical diversity (Fig. 1a,b), the effect of producer, consumer and vertical diversity, and indicating that high horizontal diversity can compensate the their pairwise interactions, on the recovery time. To interpret stability loss caused by vertical diversity. These results were potential effects on recovery time, we also tested for diversity robust to changing all parameters simultaneously from their effects on average interaction strengths, defined as the square reference value by 20% and +20% (Fig. S1). Outside of this root of the average of all the off-diagonal elements in the range, the model results were sensitive to the conversion effi- interaction matrix J (i 6¼ j) with total species T, that is, ij ciency k (Fig. S2), where larger k destabilised the food webs ! rffiffiffiffiffiffiffiffiffiffiffiffi J and switched the diversity–stability relationship, as expected ij i6¼j (May 2001; Moore & de Ruiter 2012), again TTðÞ 1 (Rip & Mccann 2011; Barbier & Loreau 2019). When fixing the conversion efficiency k to its reference value, the model using linear regression. results were robust to changes of up to 60% and + 60% of To the data from experiment 1, we applied linear mixed all parameters except k (Fig. S3). models to test for the effect of producer, consumer and verti- cal diversity, and their pairwise interactions, on the degree of self-damping, as calculated from the estimated interactions. Experiment 1: empirical Jacobian matrices We used species identity as a random effect to exclude the Producer, consumer and vertical diversity all affected food web potential confounding effect of species identity. stability. In line with the model predictions, both producer and To understand possible effects of diversity on the degree of consumer diversity increased food web stability (i.e. decreasing self-damping, we examined diversity effects on three variables the degree of self-damping) and the impact of producer diver- underlying the degree of self-damping: consumer biomass, the sity on stability increased with increasing consumer diversity. energy flux into consumers and interaction strengths. We did Also in line with the model results, vertical diversity on itself so by first applied the mixed model to test for the effect of decreased stability (Fig. 2a,b). Stability was highest at high hor- producer, consumer and vertical diversity, and their pairwise izontal (both producer and consumer) diversity and low vertical interactions (again with species identity as a random effect) diversity, and was lowest at low horizontal diversity (producer on these three variables. Next, we constructed linear regres- and consumer) and high vertical diversity (Fig. 2a,b). sion models to examine the relationship between (1) consumer The effects of horizontal and vertical diversity on stability biomass and energy flux into consumers, (2) energy flux into were associated with effects on consumer biomass, energy consumers and the absolute value of interaction strength of fluxes and interaction strengths between trophic levels. Con- consumers to producers and finally (3) the absolute value of sumer biomass increased with producer and consumer diver- interaction strength of consumers to producers and degree of sity but decreased with vertical diversity (Fig. 2c,d). Diversity self-damping (minimum s). Again, we used mixed models with did not affect predator biomass (Table S3). species identity as a random effect and included interactions Interactions of producer, consumer and vertical diversity between horizontal and vertical diversity. We adopted the affected the energy flux into consumers (Fig. 2e,f). At high same approach for predator biomass, energy flux into preda- vertical diversity (i.e. 3), horizontal diversity of either produc- tor and absolute value of interaction strength of predator to ers or consumers increased the energy flux into consumers consumer. However, note that by definition, vertical diversity (Fig. 2f). This higher energy flux was associated with higher © 2019 The Authors. Ecology Letters published by CNRS and John Wiley & Sons Ltd. 1156 Q. Zhao et al. Letter Figure 1 Model simulations illustrating the interactive effects of horizontal (producer and consumer) and vertical diversity on recovery time (a lower recovery time indicates a greater stability) consumer biomass (Fig. 3a). Under low vertical diversity (i.e. composition, respectively. Total biomass showed signs of 2), however, horizontal diversity decreased the energy flux recovery after exposure to the herbicide and insecticide, but (Fig. 2e), while increasing consumer biomass (Fig. 3a). We horizontal diversity increased the biomass recovery rate while found no effect of diversity on the energy flux into predators vertical diversity decreased it. This result can be understood (Table S3). from the smaller effect the pesticides had on the horizontally The interaction strength of consumers to producers was more diverse communities (Fig. S4a–d and Fig. S5a–d). influenced by interactions of producer, consumer and vertical Indeed, this smaller effect translates to the numerator and diversity. Horizontal diversity decreased the interaction especially denominator of eqn 2 being smaller at higher hori- strength, whereas vertical diversity increased it (Fig. 2g,h). zontal diversity, making their ratio (i.e. functional resilience) The interaction strength was lowest at high horizontal and inevitably larger. The opposite occurred for vertical diversity, low vertical diversity, but highest at low horizontal and high which increased biomass differences (Fig. S4e,f and Fig. S5e,f) vertical diversity (Fig. 2g,h), where the interaction strength and therefore decreased the recovery rate. was positively correlated with the energy flux into consumers On average, the composition of the exposed and control (Fig. 3b). No significant diversity effects were detected on the communities was more similar on day 21 than on day 6, indi- interaction strength of predators to consumers (Table S3). cating compositional recovery. Horizontal and vertical diver- Finally, the interaction strength of consumers to producers sity had also opposite effects on compositional recovery. was positively correlated with the degree of self-damping Because producer abundance accounted for more than 97% (Fig. 3c), indicating that strong interactions decreased food of the whole community, the effects of horizontal and vertical web stability. diversity on compositional recovery can be understood by focusing on the producer community. The herbicide directly decreased the abundance of sensitive Experiment 2: large perturbations producers (Desmodesmus pannonicum, Chlorella vulgaris and In line with the results obtained with the Jacobian method for Selenastrum capricornutum, Fig. S6a) on day 6, but did not simulated and empirical food web data, producer and con- change consumer composition (Fig. S6c,d). A greater pro- sumer diversity both increased stability (i.e. functional resili- ducer diversity caused an insurance effect as tolerant produc- ence) against severe perturbations and the positive effect of ers (e.g. Scenedesmus obliquus in Fig. S6a) became dominant, producer diversity was stronger when consumer diversity was which caused compositional differences between the control high (Fig. 4a–d). Again, vertical diversity decreased stability and the herbicide-treated systems. This difference translates to (Fig. 4a–d). Therefore, functional resilience was highest at the last term of eqn 3 (BC ) being smaller at higher producer high horizontal diversity and low vertical diversity, and it was diversity (no composition changes on day 21), making the dif- lowest when horizontal diversity was low and vertical diversity ference between BC and BC (i.e. compositional resilience) 21 6 was high (Fig. 4a–d). We found qualitatively identical results inevitably greater. We also found that the magnitude of this for stability measured by the compositional resilience insurance effect was increased by consumer diversity, but (Fig. 5a–d), even though the interactive effect of producer and decreased by vertical diversity, which respectively increased consumer diversity was weaker for the case of herbicide expo- and decreased compositional recovery (Fig. S6a–d). sure. The insecticide directly decreased the abundance of sensitive The effects of horizontal and vertical diversity on the func- consumers (i.e. Daphnia pulex and Moina macrocopa in tional and compositional resilience were associated with Fig. S7a), and tolerant species (e.g. Daphnia lumholtzi in effects on total biomass (sum across all trophic levels) and Fig. S7a) became dominant. The dominance of tolerant © 2019 The Authors. Ecology Letters published by CNRS and John Wiley & Sons Ltd. Letter Horizontal and vertical diversity shape stability 1157 Figure 2 The interactive effects of horizontal (producer and consumer) and vertical diversity on stability (the degree of self-damping) (a, b), on consumer biomass (c, d), on energy flux from producers to consumers (e, f) and on the absolute value of interaction strength of consumers to producers (g, h). Plotted are sample mean 1 SD. Detailed statistical results are listed in Table S4. © 2019 The Authors. Ecology Letters published by CNRS and John Wiley & Sons Ltd. 1158 Q. Zhao et al. Letter 2 2 1 Figure 3 Relationships between consumer biomass (g m ) and energy flux from producers to consumers (g c m h ) (a), between the energy flux from 2 1 producers to consumers (g c m h ) and the absolute value of interaction strength of consumers to producers (b), and between the absolute value of interaction strength of consumers to producers and the degree of self-damping (c) species had indirect, top-down, effects on its preferred algae horizontally diverse at various trophic levels, but contain rela- (Scendesmus acutus, C. vulgaris and S. capricornutum), which tively few trophic levels will be more stable. These conclusions increased the abundance of non-preferred algae (D. pannon- are broadly supported. First, both model simulations and two icum), compensating the loss of the preferred algae (Fig. S7c). independent experiments with natural food webs yield consis- Again, this represents an insurance effect, but this time driven tent results. Second, we applied both Jacobian-based stability by consumer diversity. This mechanism caused composition to assessments that assume small perturbations and population be more different between control and insecticide-exposed sys- equilibrium, but also alternative stability measures following tems on day 6 (no composition discrepancy on day 21), which large perturbations. again translated to the last term of eqn 3 (BC ) being smaller The results from the simulations and empirical food webs at higher consumer diversity, making the difference between (Experiment 1) indicate that, under the assumption of small BC and BC (i.e. compositional resilience) inevitably greater. perturbations and population at equilibrium, horizontal and 21 6 This insurance effect was again increased by producer diver- vertical diversity affect food web stability by changing (aver- sity, but decreased by vertical diversity, which increase and age) interaction strength. The individual and joint effects of decrease compositional recovery, respectively (Fig. S7a–d). producer and consumer diversity as well as the effect of verti- cal diversity, as found through modelling, can be understood from changing average interaction strengths (Fig. S8). The DISCUSSION results from experiment 1 can be explained by biomass Our model and empirical results show for the first time that changes and energy flows between trophic levels, which finally horizontal diversity and vertical diversity jointly affect stabil- change interaction strengths between trophic levels. We show ity. Specifically, the effect of producer diversity was stronger that the well-known positive (and negative) effects of horizon- when consumer diversity was higher, regardless of vertical tal (and vertical) diversity on consumer biomass (Duffy 2002; diversity. Vertical diversity consistently decreased stability. Cardinale et al. 2003) underpin these proposed effects. The Taken together, these results suggest that food webs that are positive interactive effects of producer and consumer diversity © 2019 The Authors. Ecology Letters published by CNRS and John Wiley & Sons Ltd. Letter Horizontal and vertical diversity shape stability 1159 Figure 4 The interactive effects of horizontal (producer and consumer) and vertical diversity on the functional resilience after herbicide (a, b) and insecticide (c, d) exposure. Plotted are sample mean 1 SD. Detailed statistical results are listed in Table S5. on consumer biomass reflect a greater niche differentiation consumer biomass had a higher proportion of large individu- among producers and consumers, optimising consumer bio- als, which have slower metabolic rates, and thus generate mass (Cardinale et al. 2006; Tilman et al. 2014; Barnes et al. lower energy fluxes, than small organisms. 2018). The negative effect of vertical diversity on biomass High energy flux between trophic levels can increase interac- reflects predation on consumers. It should be noted that, in tion strength (McCann 2000; Rip & Mccann 2011; Schwarz this study, we only added a single predator individual. Given et al. 2017; Kadoya et al. 2018), which in turn decreases food that natural systems are controlled by predator populations web stability (McCann 2000; Rip & Mccann 2011; Ushio (Cardinale et al. 2003; Snyder et al. 2008; Griffin et al. 2013), et al. 2018). We found that the large energy flux into con- biomass depression by vertical diversity can be higher than sumers indeed increased the interaction strength between con- reported here. sumers and producers, which led to lower stability. More Increasing the biomass of a focal trophic group generally specifically, producer and consumer diversity positively inter- increases the energy flux into this group (Otto et al. 2007; acted to decrease interaction strength, which increased food Ehnes et al. 2011; Barnes et al. 2014). At high vertical diver- web stability. Vertical diversity increased the interaction sity (i.e. 3), we found a positive interactive effect of producer strength and decreased stability. and consumer diversity on consumer biomass, which was Taken together, interactive effects of producer and con- indeed positively associated with energy fluxes into consumers. sumer diversity can change consumer biomass and the energy However, the positive association between biomass and energy flux into consumers, leading to weak interactions and flux can be overruled by other factors such as body size struc- increased stability. Vertical diversity, in contrast, makes for ture (Barnes et al. 2014, 2018). Under low vertical diversity strong links which will decrease stability. (i.e. 2), we detected that high consumer biomass was nega- Pesticide effects on community biomass were a direct result tively correlated with the energy fluxes to consumers. We of effects on community composition and were buffered by found some support that individual body mass distributions horizontal diversity. This buffering effect has been shown could explain this result (Fig. S9). The treatments with high before for competitive systems (Gonzalez & Loreau 2009; © 2019 The Authors. Ecology Letters published by CNRS and John Wiley & Sons Ltd. 1160 Q. Zhao et al. Letter Figure 5 The interactive effects of horizontal (producer and consumer) and vertical diversity on the compositional resilience after herbicide (a, b) and insecticide (c, d) exposure. Plotted are sample mean 1 SD. Detailed statistical results are listed in Table S5. Isbell et al. 2015; Baert et al. 2016). Our findings suggest that communities (Bairey et al. 2016; Grilli et al. 2017; Mayfield & this effect also holds for food webs. Importantly, we found Stouffer 2017; Letten & Stouffer 2019). We expect that adding that – in our system where producers were the largest commu- high-order interactions will reinforce the positive effect of hor- nity – this effect occurs both when the pesticide directly izontal diversity we found here, but weaken the negative effect affects producers and when it affects producers indirectly by of vertical diversity on stability. Finally, our results cannot be depressing consumers. extrapolated to food webs that include omnivores. Previous We are cognizant of our study’s limitations. First, in our studies indeed showed that complex food webs with omni- experiments, we only considered two levels per horizontal and vores potentially hold many stabilising weak links (Neutel vertical diversity treatment. Previous studies have shown that et al. 2002, 2007), making the destabilising effect of vertical food webs with higher horizontal (producer or consumer) diversity we report here possibly weaker. Recent studies diversity have larger niche differentiation and lower consump- demonstrated that the presence of omnivores can alter the tion rate (Duffy et al. 2007; Edwards et al. 2010). We there- relationship between vertical diversity and primary productiv- fore expect the positive effect of producer diversity on ity in complex food webs (Wang et al. 2019). stability to be stronger than reported here. Second, natural Our results show that different aspects of biodiversity may systems often vary not only in species richness but also in affect stability in different ways, through effects on biomass, how species biomasses are distributed. Our results may there- energy fluxes and eventually interaction strengths. How our fore change when considering alternative diversity indices (e.g. results scale up to more complex food webs is an outstanding Shannon’s index in Kato et al. 2018). However, a combina- question, but our findings suggest that the benefits of horizon- tion of Shannon’s index and species richness may provide a tal diversity can in theory overcompensate the negative effects deeper insight into future work. Third, our model assumed of vertical diversity. Our results show that conserving horizon- pairwise interactions and neglected potential higher-order tal diversity across trophic levels (multiple horizontal biodiver- interactions, that is pairwise interactions being modulated by sity) can offer a solution to maintain both functioning and a third species, which have been found to stabilise stability of natural ecosystems with high vertical diversity. © 2019 The Authors. Ecology Letters published by CNRS and John Wiley & Sons Ltd. Letter Horizontal and vertical diversity shape stability 1161 Cardinale, B.J., Srivastava, D.S., Duffy, J.E., Wright, J.P., Downing, ACKNOWLEDGEMENTS A.L., Sankaran, M., et al. (2006). Effects of biodiversity on the functioning of trophic groups and ecosystems. Nature, 443, 989–992. We acknowledge feedback and advice from the editor, Tim Crooks, K.R. & Soule, M.E. (1999). Mesopredator release and avifaunal Coulson and three anonymous referees. We thank Carlos extinctions in a fragmented system. Nature, 400, 563–566. Melian and Jurg € W. Spaak for valuable suggestions and com- Crowder, L.B., Squires, D.D. & Rice, J.A. (1997). Nonadditive effects of ments. QHZ is supported by the China Scholarship Council terrestrial and aquatic predators on juvenile estuarine fish. Ecology, 78, (No. 201606190229). 1796–1804. Daam, M.A., Van den Brink, P.J. & Nogueira, A.J.A. (2009). Comparison of fate and ecological effects of the herbicide linuron in AUTHORSHIP freshwater model ecosystems between tropical and temperate regions. Ecotoxicol. Environ. Saf., 72, 424–433. QHZ, FDL, CC, PRS, CX, YXGW and SPW conceived and Donohue, I., Hillebrand, H., Montoya, J.M., Petchey, O.L., Pimm, S.L., developed the models; PJVDB and QHZ designed the experi- Fowler, M.S., et al. (2016). Navigating the complexity of ecological ments; SV, FG and MV assisted the experiments; QHZ and stability. Ecol. Lett., 19, 1172–1185. YXGW analysed all data; QHZ and FDL drafted the manu- Duffy, J.E. (2002). Biodiversity and ecosystem function: the consumer connection. Oikos, 99, 201–219. script; and all authors contributed substantially to revisions. Duffy, J.E., Cardinale, B.J., France, K.E., McIntyre, P.B., Thebault, E. & Loreau, M. (2007). The functional role of biodiversity in ecosystems: DATA ACCESSIBILITY STATEMENT Incorporating trophic complexity. Ecol. Lett., 10, 522–538. 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Ecology Letters – Pubmed Central
Published: May 16, 2019
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