High incidence of plant-animal mutualisms in the woody flora of the temperate forest of southern South America : biogeographical origin and present ecological significance

The flora of the temperate forest of southern South America highly depends on animals for pollination and seed dispersal. This resembles more tropical settings and distinguishes it from other temperate floras. This high mutualism-dependency seems paradoxical and potentially “anachronic” in view of this flora’s present interaction with an impoverished fauna. We analyzed the frequency of biotic pollination and seed dispersal across woody genera classified according to growth form and biogeographical affiliation. We found that genera that probably originated in warm or tropical like environments of ancient Gondwana and the Neotropics, two of the main biogeographical sources of this flora, had high incidences of biotic pollination and dispersal. The rich endemic foristic element, mostly related phylogenetically to these two foristic sources, also exhibited a high frequency of mutualism-dependency. Many endemic and Neotropical genera showed distinctive reproductive traits associated with bird pollination, a type of mutualism nearly absent in taxa with other biogeographical affiliations. This suggests that many southern South American plant taxa may have evolved novel mutualistic associations in situ, probably before the onset of present cooler climatic conditions. We propose that, despite the current relictual status of many of these genera and their associated reproductive traits, dependence on mutualists is not necessarily “anachronic” in today’s cool climate and depauperate faunal environment. Our finding that the average southernmost distribution limit is similar both for genera that depend on mutualists for either pollination or dispersal and for those that do not support this view. The steep W-E rainfall gradient created by the rising of the Andes represents a more potent ecological filter than the N-S temperature gradient, sorting out forest plant taxa according to their dependence on hummingbirds for pollination and vertebrates for dispersal. Overall, we believe that plant-animal mutualisms in the temperate forest of southern South America are still well suited interactions, because they rely on animals that are abundant and show a high degree of residency despite being represented by a low number of species. However, present human-induced elevated rates of deforestation, fragmentation and habitat degradation may be particularly threatening for mutualist-dependent plants due to low redundancy in alternative animal partners.Fil: Aizen, Marcelo A.. Universidad Nacional del Comahue - Departamento de Ecología, Bariloche, ArgentinaFil: Ezcurra, Cecilia. Universidad Nacional del Comahue - Departamento de Botánica, Bariloche, Argentin

Approaches to the study of sexual plant reproduction in altered habitats : limitations and perspectives

Las interacciones planta-polinizador son susceptibles a diferentes tipos de perturbaciones de origen antrópico. Aunque se supone que las distintas actividades humanas tienen impactos disruptivos o negativos sobre estas interacciones, el signo y la magnitud de los mismos dependen de una serie de variables ambientales y atributos biológicos cuya modificación puede tener efectos de signo contrario sobre distintos componentes de estos mutualismos. En consecuencia, el impacto de las perturbaciones antrópicas sobre la polinización y éxito reproductivo de las plantas no es fácilmente predecible a priori, dependiendo también de la intensidad, escala espacial y frecuencia del disturbio. El enfoque empleado mayormente en esta clase de estudios es de tipo comparativo y reduccionista. Esto resulta en una falta en la comprensión de los factores mediatos e inmediatos involucrados en la respuesta reproductiva de las plantas a las perturbaciones, y a interpretaciones erróneas, o a lo sumo incompletas, asociadas a repuestas curvilíneas y a una replicación reducida. En este trabajo reviso distintos tipos de limitaciones relacionados a este enfoque y propongo uno alternativo, que si bien es de naturaleza correlativa, permite una comprensión más mecanicista y la puesta a prueba de hipótesis de causalidad. El enfoque propuesto también permite asimilar, en forma más natural, al diseño de muestreo los patrones de perturbación que usualmente se encuentran en el campo, mejor reflejados por gradientes que por clases discretas. Esta aproximación también implica una mayor integración entre las áreas de la ecología reproductiva de plantas y la del paisaje.Plant-pollinator interactions are susceptible to different types of anthropogenic disturbances. Although it is assumed that different human activities can disrupt these interactions, the direction and magnitude of their consequences are mediated by a series of environmental and biological variables that may have opposite effects on different aspects of these mutualisms. Therefore, the impact of human-driven habitat alteration on pollination and plant reproductive success can not be predicted a priori. The sign and magnitude of this impact will also depend on disturbance intensity, spatial scale and frequency. The current approach to study disturbance effects on plant reproduction is mostly comparative and highly reductionist (e.g., seed production is compared between disturbed vs. undisturbed sites). This approach leads to a lack of understanding on the proximal factors involved in the reproductive response of plants to habitat alteration, or even to incomplete or erroneous interpretations when responses are curvilinear or there is a low level of true replication. Here I review and comment on the different types of limitations arising from this comparative approach, and propose an alternative one. The proposed approach is exemplified in a simple conceptual model that can accommodate different aspects of the disturbance itself, including scale considerations, as well as aspects of plants, pollinators, and of the pollination process. This approach, even though of a correlative nature, allows a more mechanistic understanding of the effects of habitat disturbance on plant pollination and reproductive success by testing different proximal variables and causal models using path analysis and structural equation modeling. Also, the proposed approach can incorporate easily the disturbance patterns found in the field, better reflected in gradients than discrete classes. Finally, I advocate a greater integration between the mostly disconnected areas of plant reproductive ecology and landscape ecology

Long-term global trends in crop yield and production reveal no current pollination shortage but increasing pollinator dependency

Fil: Aizen, Marcelo A. Universidad Nacional del Comahue. Centro Regional Universitario Bariloche. Laboratorio Ecotono; Argentina.Fil: Garibaldi, Lucas Alejandro. Universidad Nacional del Comahue. Centro Regional Universitario Bariloche. Laboratorio Ecotono; Argentina. Universidad de Buenos Aires (UBA). Facultad de Agronomía; Argentina.Fil: Cunningham, Saul A. CSIRO Entomology; Australia.Fil: Klein, Alexandra M. University of California; USA.Fil: Klein, Alexandra M. University of Goettingen; Alemania.Fil: Aizen, Marcelo A. Instituto de Investigaciones en Biodiversidad y Medioambiente (INIBIOMA); Argentina.Fil: Aizen, Marcelo A. Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET); Argentina.Fil: Garibaldi, Lucas Alejandro. Universidad de Buenos Aires (UBA). Facultad de Agronomía; Argentina.There is evidence that pollinators are declining as a result of local and global environmental degradation 1, 2, 3, 4. Because a sizable proportion of the human diet depends directly or indirectly on animal pollination [5], the issue of how decreases in pollinator stocks could affect global crop production is of paramount importance 6, 7, 8. Using the extensive FAO data set [9], we compared 45 year series (1961–2006) in yield, and total production and cultivated area of pollinator-dependent and nondependent crops [5]. We investigated temporal trends separately for the developed and developing world because differences in agricultural intensification, and socioeconomic and environmental conditions might affect yield and pollinators 10, 11, 12, 13. Since 1961, crop yield (Mt/ha) has increased consistently at average annual growth rates of ∼1.5%. Temporal trends were similar between pollinator-dependent and nondependent crops in both the developed and developing world, thus not supporting the view that pollinator shortages are affecting crop yield at the global scale. We further report, however, that agriculture has become more pollinator dependent because of a disproportionate increase in the area cultivated with pollinator-dependent crops. If the trend toward favoring cultivation of pollinator-dependent crops continues, the need for the service provided by declining pollinators will greatly increase in the near future

Seed dispersal by birds in a temperate forest of southern South America: : who disperses to whom?

Un gran número de plantas depende de animales mutualistas para la dispersión de sus semillas, tarea principalmente realizada por aves que ingieren los frutos y defecan o regurgitan las semillas en forma intacta. El Bosque Templado de Sudamérica Austral (BTSA) se diferencia de otros biomas boscosos templados por poseer una gran proporción de plantas leñosas (~60% de los géneros) que producen frutos carnosos. Estudiamos las interacciones entre plantas y aves dispersoras en un bosque mésico dominado por Nothofagus dombeyi en la Reserva Municipal de Llao-Llao, Argentina (41° 00’S; 71°30´O), cerca del extremo oriental del BTSA. Las aves fueron capturadas utilizando ocho redes de niebla, y muestreadas por avistaje y sonido en cinco estaciones de conteo durante dos estaciones de fructificación. La dieta de las aves capturadas fue estimada mediante el lavado del tracto digestivo. Se estimó la disponibilidad de frutos carnosos en el área de estudio y se realizaron registros de la fenología de fructificación de las especies de plantas leñosas. Se capturaron un total de 296 individuos de 12 especies de aves. Restos de frutos carnosos y semillas fueron encontrados en sólo dos especies, una migrante, Elaenia albiceps, y otra residente, Turdus falcklandii. Estos frutos pertenecieron a ocho de las nueve especies de plantas leñosas productoras de frutos carnosos presentes en el bosque. Adicionalmente, las dos especies de aves fueron comunes en el área de estudio durante la estación de fructificación, representando el 52% y 9% de todas las capturas y el 35% y 4% en las estaciones de conteo, respectivamente. Resultados de un estudio similar en Chiloé, Chile, concuerdan en señalar la importancia de E. albiceps y T. falcklandii como especies claves en la dispersión de frutos del BTSA.Many plants depend on animals for seed dispersal, a task carried out mainly by birds that ingest fruits and defecate or regurgitate seeds undamaged. Unlike other temperate forest biomes, the Temperate Forest of Southern South America (TFSA) is characterized by a large proportion of woody plants (~ 60% of genera) producing fleshy fruits. We studied the interactions between plants and bird dispersers in a mesic forest dominated by Nothofagus dombeyi at the Llao-Llao Forest Reserve, Argentina (41°00’S; 71° 30´W), close to the eastern boundary of the TFSA. We sampled birds using eight mist-nets and five sight/sound census stations during two consecutive fruiting seasons (1999 - 2000). We also recorded the phenology and fruit availability of six tree and shrub species. Gut content analysis was used to determine which fruits were consumed by the dispersers. Through the two sampling methods, we surveyed a total of 23 bird species occurring in the study area. We captured a total of 296 birds belonging to 12 species. We found evidence of fleshy fruit consumption only in two species, Elaenia albiceps and Turdus falcklandii, that consumed fruits and defecated seeds of eight from the nine fleshy-fruited plant species locally present. These two bird species were common in the forest during the fruiting season accounting for 52% and 9% of all mist-net captures and 35% and 4% of all sight/sound censuses, respectively. Other birds consumed fruit or seeds (without dispersing them), insects, and/or small vertebrates. Phenological records indicated that most plant species bear ripe fruit during January and February. The most important fleshy-fruited plants in the area were Aristotelia maqui and Tristerix corymbosus; the latter dispersed by a marsupial. Results presented here, together with a similar study carried out in Chiloé, stress the importance of E. albiceps and T. falcklandii as key mutualists throughout the TFSA

Soybean expansion and agriculture diversity in Argentina

Se ha propuesto que el incremento en el cultivo de soja (Glycine max) que ha ocurrido en la Argentina durante las últimas dos décadas está asociado a un empobrecimiento de la diversidad de la agricultura. En este trabajo evaluamos esta hipótesis a través de estimar los cambios en la superficie cultivada, en la identidad y magnitud de la dominancia en términos de la proporción del área sembrada con el cultivo principal, y en la diversidad de cultivos a lo largo del período 1961-2006. La superficie total cultivada de nuestro país se ha incrementado aproximadamente 45% desde 1990 hasta 2006, en coincidencia con la gran expansión del cultivo de soja, que ha reemplazado al trigo (Triticum spp.) como cultivo dominante. En 2006, la soja representó alrededor de 50% de la superficie cultivada en la Argentina. Ningún otro cultivo alcanzó en las últimas cinco décadas semejante dominancia. Distintos estimadores indican que, asociado a este incremento de la dominancia de la soja, la diversidad de cultivos del campo argentino ha decrecido >20% durante el período 1990-2006. Además de la expansión de la frontera agrícola y de la pérdida de biodiversidad por destrucción de ecosistemas naturales, nuestros resultados ponen en evidencia una tendencia hacia la homogeneización del paisaje agrícola. De continuarse un aumento en la dominancia del cultivo de soja es probable que se profundicen los múltiples costos ambientales, sociales y económicos asociados a una menor diversidad de cultivos en nuestro país.The environmental and socio-economic consequences of the great expansion of soybean (Glycine max) cultivation in Argentina during the last two decades are strongly debated in our society. Soybean and its derivatives constitute presently most important Argentina's export and cash source. Here, we tested whether soybean´s expansion has caused a detectable decrease in crop diversity. We specifically assessed changes in total cultivated area, identity and degree of dominance of the most important crop (i.e., the one accounting for the largest proportion of the total cultivated area), and crop diversity over the period 1961-2006. Argentina's total cultivated area increased by about 45% from 1990 to 2006 and it was associated with a replacement of wheat by soybean as the dominant crop. In 2006 soybean accounted for ~50% of the total cultivated area in our country, the largest dominance reached by any crop during the last five decades. Different diversity indicators, including Shannon-Wiener´s H´, Pielou´s J and Hurlbert´s PIE indexes agreed that crop diversity has decreased >20% during the period of soybean dominance. In addition to the direct loss of biodiversity caused by deforestation for agriculture expansion, our results evidence a trend towards homogenization of Argentina's agriculture landscape with likely consequences for remnant biodiversity, degradation of different ecosystem services, and a more vulnerable production structure

Risks to pollinators and pollination from invasive alien species

Invasive alien species modify pollinator biodiversity and the services they provide that underpin ecosystem function and human well-being. Building on the Intergovernmental Science-Policy Platform for Biodiversity and Ecosystem Services (IPBES) global assessment of pollinators and pollination, we synthesize current understanding of invasive alien impacts on pollinators and pollination. Invasive alien species create risks and opportunities for pollinator nutrition, re-organize species interactions to affect native pollination and community stability, and spread and select for virulent diseases. Risks are complex but substantial, and depend greatly on the ecological function and evolutionary history of both the invader and the recipient ecosystem. We highlight evolutionary implications for pollination from invasive alien species, and identify future research directions, key messages and options for decision-making

A common framework for identifying linkage rules across different types of interactions

Species interactions, ranging from antagonisms to mutualisms, form the architecture of biodiversity and determine ecosystem functioning. Understanding the rules responsible for who interacts with whom, as well as the functional consequences of these interspecific interactions, is central to predict community dynamics and stability. Species traits sensu lato may affect different ecological processes by determining species interactions through a two-step process. First, ecological and life-history traits govern species distributions and abundance, and hence determine species co-occurrence and the potential for species to interact. Secondly, morphological or physiological traits between co-occurring potential interaction partners should match for the realization of an interaction. Here, we review recent advances on predicting interactions from species co-occurrence and develop a probabilistic model for inferring trait matching. The models proposed here integrate both neutral and trait-matching constraints, while using only information about known interactions, thereby overcoming problems originating from undersampling of rare interactions (i.e. missing links). They can easily accommodate qualitative or quantitative data and can incorporate trait variation within species, such as values that vary along developmental stages or environmental gradients. We use three case studies to show that the proposed models can detect strong trait matching (e.g. predator‿prey system), relaxed trait matching (e.g. herbivore‿plant system) and barrier trait matching (e.g. plant‿pollinator systems). Only by elucidating which species traits are important in each process (i.e. in determining interaction establishment and frequency), we can advance in explaining how species interact and the consequences of these interactions for ecosystem functioning. A lay summary is available for this articlePeer Reviewe

Pollinator dependence of Argentinean agriculture: current status and temporal analysis.

Fil: Chacoff, Natacha P. Instituto Argentino de Investigaciones de las Zonas Áridas (IADIZA)-CONICET; Argentina.Fil: Morales, Carolina L. Universidad Nacional del Comahue. INIBIOMA-CONICET. Laboratorio Ecotono; Argentina.Fil: Garibaldi, Lucas Alejandro. Universidad Nacional del Comahue. INIBIOMA-CONICET. Laboratorio Ecotono; Argentina.Fil: Ashworth, Lorena. Universidad Nacional de Córdoba. Instituto Multidisciplinario de Biología Vegetal (IMBIV)-CONICET; Argentina.Fil: Aizen, Marcelo A. Universidad Nacional del Comahue. INIBIOMA-CONICET. Laboratorio Ecotono; Argentina.Fil: Garibaldi, Lucas Alejandro. Universidad de Buenos Aires (UBA). Facultad de Agronomía; Argentina.A sizable proportion of agricultural production depends directly or indirectly on animal pollination but estimation of the size of this dependence is missing for most countries, even for some of the most important food producers. Here, we evaluate the current status and temporal trends (1961-2007) in pollinator dependency of Argentinean agriculture. We classified crops in categories according to their pollinator dependence, and estimated their harvested area, production, economic and nutritional values. We also estimated the expected production deficit in the absence of pollinators, the extra area needed to cope with this deficit, and trends in honeybee stocks. From a total of 68 crops, animal pollination increased directly production in 37 and indirectly in 13. More than half of the harvested area and total agricultural production corresponded to pollinator dependent crops, a trend highly influenced by the inclusion of soybean as a modestly dependent crop. Highly pollinator-dependent crops produced 2-4 times more income per hectare than any other crop, and modestly dependent crops bear on average the highest protein and fat content. During the study period the production deficit increased three-fold, reaching 12% in 2007, whereas the area needed to compensate for these deficiencies attained 24%. Regarding pollination services, indicators are mixed; whereas Argentinean honey-bee stock triplicates from 1961 to 2007, native forest area, a source of pollinator diversity, shrank to more than half since 1940’s. Experiments testing the degree of pollinator dependency on the quality and quantity of crop production for soybean varieties cultivated in Argentina are urgently needed. Our estimations depict an agriculture that is becoming more dependent on pollinators, but native forests and other native terrestrial habitats, which host most of the country’s pollinator diversity, are decreasing at an alarming rate