Abstract. Indirect interactions occur when the effect of one species on another is mediated by a third species. These interactions occur in most multi-species assemblages and are diverse in their mechanistic pathways. The interest in indirect interactions has increased exponentially over the past three decades, in recognition of their importance in determining plant community dynamics and promoting species coexistence. Here, we review the literature on indirect interactions among plants published since 1990, using a novel synthetic framework that accounts for and classifies intervening species and mechanisms within trophic networks. The objectives of this review are: (1) to identify the geographical regions and ecosystem types where indirect interactions have been examined; (2) to summarize the information on the number of trophic levels examined in studies of indirect interactions; (3) to test whether the frequency of indirect interactions varies across environmental gradients; and (4) to identify the experimental approaches most commonly used in studies of indirect interactions. Studies examining indirect interactions in plants have been conducted primarily in the Northern Hemisphere, with a focus on grasslands and forests. The majority of studies (67%) examined two trophic levels. Indirect facilitation and apparent competition are the interactions that have been most frequently examined, with the latter being reported more frequently in relatively productive environments. Other indirect interactions reported include associational resistance, exploitative competition or facilitation, shared defenses, and trophic cascades. Generally, field experiments tested indirect interactions based on single target species. While the majority of studies on indirect interactions dealt with basic ecology issues, several studies have dealt with such interactions in the context of biological invasions (18%) and rangeland management (12%). This review allowed us identifying a number of research needs, including the study of non-feeding interactions and that for more realistic complex designs, explicitly testing indirect interactions across different trophic levels, in geographical regions that have been under-examined to date, and in stressful ecosystems.
Summary1. Facilitation studies focus primarily on plants often neglecting the extended effects that cascade through ecological networks. Plants interact with other organisms through consumptive effects and a myriad of non-trophic effects such as habitat amelioration or pollination. 2. Shrubs are a dominant benefactor species frequent in plant-facilitation studies but can also have direct and indirect interactions with animals. Herein, we use a systematic review to address the following two objectives: (i) to propose a conceptual framework that explores these interactions including the functional roles of the interacting species, and (ii) to quantitatively summarize the current state of this field examining effects beyond plant-plant interactions. 3. To date, a relatively limited number of studies have examined the importance of coupled benefactor-subordinate plant positive interactions with animals (79 studies in total). From this set of studies, 36 studies documented positive plant interactions generating a total of 53 independent instances of either shrub-plant-animal or shrub-animal-plant interactions. 4. These interaction pathways were evenly split between direct (49%) and indirect (51%) interactions of shrubs with animals. Hypotheses frequently tested included seed trapping, herbivore protection, magnet pollination and facilitation-mediated secondary seed dispersal. The most common functional role of shrubs was protection from herbivory, and the most common animal role associated with plant-facilitation complexes was that of a consumer. 5. None of these studies explored bidirectional plant-animal interactions, used a network approach to describe the interaction sets, nor contrasted interaction strengths. Multitrophic, integrated sets of experiments incorporating plant facilitation into community dynamics are thus critical in advancing management of high-stress ecosystems wherein positive interactions are commonly reported.
The niche is a necessary consideration when estimating habitable area and geographic range of a species. Modellers often examine the fundamental niche and the environmental requirements for plant species, ignoring interactions among species. In deserts, positive plant interactions are important drivers of biodiversity and structure communities through many mechanistic pathways including modifying environmental conditions. Thus, we tested the hypothesis that desert shrubs increase the geographical extent of some annual species because, through modifying the microclimate, they match the niche requirements of beneficiary species. We used the database of the Global Biodiversity Information Facility to construct MaxEnt species distribution models (SDM) with and without reported benefactor species within the Mojave Desert in California. We chose 20 annual species to be modeled including 10 species that had been previously reported in the literature as being facilitated (beneficiary) and 10 that had no record of being facilitated (unreported). Beneficiary annuals co‐occurred significantly more with benefactor shrubs than the unreported annual species. The inclusion of shrubs into SDMs significantly improved model predictability and geographic range for all the beneficiary annual species, but not for the unreported annual species. Thus, positive interactions are species specific and it is possible to determine annual species dependency on benefactor shrubs at the regional scale. The co‐occurrence of benefactor shrubs and annual species can be used as a proxy for facilitation and recent developments in SDM techniques encourage the inclusion of biotic interactions. Species distribution models should include estimates of facilitation because biotic interactions determine the niche of species and can have implications with a changing climate.
ResumenLos ecosistemas costeros de Lomas están constituidos por comunidades vegetales desarrollándose bajo influencia de neblinas invernales. Para explorar este enunciado se determinó la relación entre las condiciones meteorológicas y la dinámica vegetal en las Lomas de Atiquipa, cerros Barrera y Lagunillas (15º46' LS y 74º22' LO, a 800 msnm aprox) entre Febrero 2005 y Febrero 2006. En cada cerro se instalaron 45 parcelas de 0.5 x 0.5 m; evaluándose mensualmente por parcela el número de especies e individuos por especie (plántulas y adultos), cobertura por especie, cobertura de hojarasca y estado fenológico. Además se calcularon los índices de Simpson y Shannon-Wiener. Se registró mensualmente temperatura media, captación de neblina y precipitación natural. Con estos datos se realizaron correlaciones lineales entre los parámetros ambientales (3) y de vegetación (10). Se encontraron varias relaciones significativas (p<0.05); neblina con 5 relaciones significativas: directa con el número total de individuos en Barrera (r=0.79), la emergencia de plántulas en Barrera (r=0.79) y Lagunillas (r=0.77), y con el predominio en Barrera (r=0.65), e inversa con la diversidad de Shannon -Wiener en Barrera (r=-0.76). Existió relación inversa entre temperatura y predominio en la comunidad (Barrera r=-0.61; Lagunillas r=-0.59). La precipitación natural no presentó relaciones significativas, aunque puede sugerirse un efecto acumulativo entre Julio y Agosto que desencadenó emergencia de plántulas en Setiembre. Mayores estudios de estas relaciones son necesarios, especialmente en un escenario de cambio climático que afectaría el régimen de humedad en estos frágiles ecosistemas. Palabras clave: Dinámica vegetal, condiciones meteorológicas, relación clima -vegetación, Lomas costeras, Atiquipa, Sur de Perú, desiertos, zonas áridas Perú Abstract Coastal ecosystems of Lomas are constituted by plant communities developing under winter fog influences. In order to explore this issue we determined the relationship between vegetation dynamics and meteorological conditions at Atiquipa Lomas, Barrera and Lagunillas hills (15º46' LS y 74º22' LW, 800 m.a.s.l. aprox.) from February 2005 to February 2006. Forty-five 0,5 x 0,5 m plots were installed in each hill, with monthly plot evaluations of species number, individuals per species (seedlings and adults), species cover, fallen leaves cover and phenological status. Simpson and Shannon-Wiener indexes were calculated. Natural precipitation, fog collection and medium temperature were also monthly registered. With these data we ran lineal correlations between environment parameters (3) and vegetation (10). Several significant relationships (p<0.05) were found, fog had 5 significant relationships: direct with total individuals in Barrera (r=0.79), with seedling emergence in Barrera (r=0.79) and Lagunillas (r=0.77), and with Simpson's predominance in Barrera (r=0.65), and inverse with Shannon-Wiener's diversity in Barrera (r=-0.76). There was an inverse relationship between temperature and predominance...
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