Indirect Effects in and on Communities

1. Indirect Effects in and on Communities • Main Categories • Primary Mechanisms • Detection  Experimental Design and Statistical Analysis • Apparent Competition in Nature?

2. Hierarchy of Higher-Order Interactions • 1st-order interactions involving 2 species • direct effects (e.g., competition, predation) • additive • 2nd-order interactions involving 3 species • most reported indirect effects including mutualisms • non-additive • “Higher-order” interactions involving 3 or more species. • rarely documented • non-additive

3. Scenarios of 2nd-Order Indirect Effects:Apparent Competition • One scenario • presence of a non-competing prey species (R1) increases predation pressure by consumer (C) on R2 (i.e. R1 subsidizes predation by C on R2) • Alternate scenario • selective predation of R2 by C suppresses R2 more than R1. • Third scenario - selective predation of R2 by C stimulates R1 by increasing its resource availability • = apparent competition?

4. Apparent Competition vs Apparent Mutualism • Apparent Competition • A species negatively affects another via a shared enemy (i.e. predator). • Interspecific competition is not required. • Apparent Mutualism • A species positively affects another via a shared enemy • mutualism not required. +

5. Scenarios of Higher-Order Indirect Effects:Apparent Mutualism • One scenario • Consumers (C1 and C2) each show selective predation, which enhances prey availability for both by suppressing competition between prey (R1 vs R2). • Alternate scenario • Consumers (C1 and C2) each prey selectively on different non-competing species (R1 or R2). • = potentially apparent mutualism?

6. Density-Dependent Indirect Effects • Indirect effect = “donor” species (C ) affects a “receiver” species (B) via its effect on a “transmitter” species (A). • indirect effects = dashed vectors • direct effects = solid vectors • Magnitude of effect is each species shown by change in size of nodes. • Category of indirect effect  “interaction chain indirect effect” • = a density-dependent change in abundance of the transmitter species (A).

7. Density-Independent Indirect Effects • Category of indirect effect  “Interaction Modification Indirect Effect” • = indirect effect of C on B via modifying some trait of the transmitter species (A). • no net change in abundance of A. • = Non-density dependent, per-capita effect by C on B • i.e. A Trait Mediated Interaction (TMIs)

8. R D T Experimental Detection of Indirect Effects I -5 -4 • Indirect or Non-Additive Model = Donor species modifies the effect of the Transmitter species on a Receiver species. • Here, combined impact of species D + T is greater than the sum of their individual effects on R. • D amplifies the effect of T • e.g., commenalism or mutualism • Analysis of Variance (ANOVA) results • significant interaction (D x T) • ignore significance of direct effects of D and T +

9. R D T Experimental Detection of Indirect Effects II +2 -4 • Here, a non-additive model shows that the combined impact of D and T is less than the sum of their individual effects on R. • D antagonizes the negative effect of T on R • competition or predation? • Analysis of Variance (ANOVA) results • significant interaction (D x T) • ignore significance of direct effects of D and T -

10. R D T -2 -4 Experimental Detection of Direct Effects • Direct or Additive Model = Each species exerts an independent effect on a target species. • Combined impact of species D + T equals the sum of their individual effects on species R. • Analysis of Variance (ANOVA) results • no significant interaction (D x T) • significant direct effect of D • significant direct effect of T

11. How Prevalent is Apparent Competition in Nature? • Hypothesized environmental factors affecting apparent competition • A mathematical model • Field experiments -

12. Where is Apparent Competition Expected to Exist? • Low-diversity ecosystems • strong predator-prey interactions not diluted by complex foodwebs • low prey diversity and densities • = weak density-dependent interspecific competition • High-diversity ecosystems • strong predator-prey interactions owing to high predator densities • specialized prey + abundant resource base • apparent > actual interspecific resource competition

13. Apparent Competition or Apparent Mutualism? • Abrams et al. (1998) model a 3-species (1 predator + 2 non-competing prey) to test for density- dependent indirect effects. • (+) y = apparent competition • (-) y = apparent mutualism • Apparent competition occurs when • predation pressure is strong. • prey are not checked by resource limitation (large ). • Apparent mutualism replaces apparent competition when • predation pressure is weak • prey are strongly resource-limited (small ).

14. Apparent Competition in a Highly Productive Tropical Food Web • Morris et al. (2004) asked “do specialist herbivores interact via a shared enemy (i.e. apparent competition)?” • Experimental removal of two species from a community of specialized leaf-mining insects exposed to shared parasites. • Here, parasitoid wasps attack non-competing herbivorous leaf-mining dipterans (flies) and coleopterans (beetles).

15. Potential for Apparent Competition - Parasitoid Wasps Shared by Leaf-Miner Species • Morris et al. (2004)  84 parasitoid wasp species attack a total of 93 herbivorous insects (linkage size = strength of interaction). • Shared enemies among leaf-mining fly larvae dipterans shown in orange. • Shared enemies among leaf-mining beetles shown in blue.

16. Experimental Removal of Host Plant and Leaf-Miners • Experimental removal of the tree species that hosts both the dipteran (Calcomyza) and beetle (Pentispa). • removal of these two species should stimulate other leaf-mining that share enemy but inhabit other tree species • Removal of these two species reduced parasitism of other leaf-miners species (no effect, odds ratio = 1).

17. Long-Term Biomass Response • Removal of flies had a greater impact on the total abundance of other dipterans than did removal of the beetle from coleopteran biomass. • Confounding effects of experimental manipulation? • host plant only constituted 0.01% of total biomass in experimental plots. • Does apparent competition lead to the eventual extinction of a prey species, or promote co-existence?

18. Cross-Ecosystem Prey Subsidies and Apparent Competition _ _ ?

19. Indirect Positive Effect of Aquatic Prey on Terrestrial Prey Species • Sabo and Power (2002) report that shielding of forest plots (S) from aquatic invertebrates amplifies the predatory effect of lizards on ground-dwelling insects and spiders (Arctosa). • In other words, aquatic insects subsidize lizards’ diets, releasing terrestrial prey from predation pressure. • Given • 1) non-competing prey • 2) positive effect of aquatic prey on terrestrial prey • 3) potentially no effect of terrestrial prey on aquatic species • apparent ........................?

20. Do Shared Predators Have Negative, Positive, or Neutral Effects on Prey Species? _ _ ?

21. Positive Indirect Effect of a Shared Predator • a,c) Webster and Almany (2002) show presence of Cardinal fish stimulated recruitment and final abundance of other prey fish species (e.g., damsel fish) • piscivorous Chocolate Cod fed more heavily on Cardinal fish, releasing other prey species from predation pressure. • b) No direct effect of cardinalfish on mortality of other prey fish, nor did these species affect cardinalfish. • Apparent ....................?

22. Take-Home Messages • Increasing higher-order species interactions = more complex non-additive indirect effects involving several species. • Indirect effects are density-dependent or density-independent. • Indirect effects can vary in magnitude and direction across different communities.