A global synthesis of fire effects on pollinators Carbone, Lucas M.; Tavella, Julia; Pausas, Juli G. ...
Global ecology and biogeography,
October 2019, 2019-10-00, 20191001, Volume:
28, Issue:
10
Journal Article
Peer reviewed
Open access
Aim
Understanding fire effects on pollinators is critical in the context of fire regime changes and the global pollination crisis. Through a systematic and quantitative review of the literature, we ...provide the first global assessment of pollinator responses to fire. We hypothesize that pollinators increase after fire and during the early postfire succession stages; however, high fire frequency has the opposite effect, decreasing pollinators.
Location
Terrestrial ecosystems, excluding Antarctica.
Time period
Data collected from 1973 to 2017.
Major taxa studied
Insects (Coleoptera, Diptera, Hymenoptera and Lepidoptera) and a few bird species.
Methods
We first compiled available studies across the globe that assessed fire effects on pollinator communities. Then, by means of hierarchical meta‐analyses, we evaluated how different fire regime parameters (fire frequency, postfire time and fire type) and habitat characteristics affect the abundance and richness of animals that act as pollinators. We also explored to what extent the responses vary among taxa groups and life history traits of pollinators (sociality system, nest location and feeding specialization), and among biomes.
Results
The overall effect size of fire on pollinator abundance and richness across all studies was positive. Fire effect was especially clear and significant in early postfire communities, after wildfires, and for Hymenoptera. Taxonomic resolution influenced fire effects, where only studies at the species/genus and family levels showed significant effects. The main exceptions were recurrent fires that showed a negative effect, and especially wildfire effects on Lepidoptera abundance that showed a significant negative response.
Main conclusions
Pollinators tend to be promoted after a wildfire event. However, short fire intervals may threat pollinators, and especially lepidopterans. Given the current fire regime changes at the global scale, it is imperative to monitor postfire pollinators across many ecosystems, as our results suggest that fire regime is critical in determining the dynamics of pollinator communities.
Selection leading to adaptation to interactions may generate rapid evolutionary feedbacks and drive diversification of species interactions. The challenge is to understand how the many traits of ...interacting species combine to shape local adaptation in ways directly or indirectly resulting in diversification. We used the well‐studied interactions between Lithophragma plants (Saxifragaceae) and Greya moths (Prodoxidae) to evaluate how plants and moths together contributed to local divergence in pollination efficacy. Specifically, we studied L. bolanderi and its two specialized Greya moth pollinators in two contrasting environments in the Sierra Nevada in California. Both moths pollinate L. bolanderi during nectaring, one of them–G. politella–also while ovipositing through the floral corolla into the ovary. First, field surveys of floral visitors and the presence of G. politella eggs and larvae in developing capsules showed that one population was visited only by G. politella and few other pollinators, whereas the other was visited by both Greya species and other pollinators. Second, L. bolanderi in these two natural populations differed in several floral traits putatively important for pollination efficacy. Third, laboratory experiments with greenhouse‐grown plants and field‐collected moths showed that L. bolanderi was more efficiently pollinated by local compared to nonlocal nectaring moths of both species. Pollination efficacy of ovipositing G. politella was also higher for local moths for the L. bolanderi population, which relies more heavily on this species in nature. Finally, time‐lapse photography in the laboratory showed that G. politella from different populations differed in oviposition behavior, suggesting the potential for local adaptation also among Greya populations. Collectively, our results are a rare example of components of local adaptation contributing to divergence in pollination efficacy in a coevolving interaction and, thus, provide insights into how geographic mosaics of coevolution may lead to coevolutionary diversification in species interactions.
Summary
Floral colour mediates plant–pollinator interactions by often signalling floral resources. In this sense, hummingbird‐pollinated flowers are frequently red‐coloured, and there are two ...tentative hypotheses to explain this pattern: 1. hummingbirds are attracted to red due its easier detection and 2. bees are sensorially excluded from red flowers. The second hypothesis is based on bees’ red colour blindness, which lead them to be less frequent and less important than hummingbirds as pollinators of red‐reflecting flowers.
Here, we untangled the role of different flower traits mediating plant–pollinator interactions and empirically tested the above hypotheses. We chose Costus arabicus due to its synchronopatric white‐ and pink‐flowered individuals and its bee and hummingbird pollination system. Although pink flowers are not totally achromatic as pure red ones, they show an achromaticity degree that could drive bee exclusion. Specifically, we tested whether differences on red reflectance work attracting hummingbirds or excluding bees and the consequent implications for the plant's reproduction.
Flower colour morphs of C. arabicus do differ neither in morphology nor in nectar sugar content. Moreover, white and pink flowers can be discriminated by the bees’ and hummingbirds’ colour vision system. Both groups are able to discriminate the red colour variation morph on the flower petals, the white flowers being more easily detected by bees and the pink flowers by hummingbirds. Bees preferentially visited the white flowers, whereas hummingbirds visited both colours at the same rate – both patterns corroborating the second hypothesis.
Pollen loads deposited on stigmas did not differ between flower colour morphs, indicating that bees and hummingbirds play a similar role in the overall pollen deposition. However, bees are more likely to self‐pollinate than hummingbirds. Self‐pollination limits C. arabicus reproduction, and red‐reflecting flowers may be better pollinated by discouraging bee visitation. Therefore, the intraspecific colour variation is driving flowers to show colour‐related different levels of generalization.
Our results support the ‘bee avoidance’ rather than the ‘hummingbird preference’ hypothesis. Sensory exclusion of bees seems to be the pressure for red‐reflecting flowers evolution, driving specialization in hummingbird‐pollinated flowers due to the costs of bee pollination on plant reproduction.
Lay Summary
Summary
Resolving the consequences of pollinator foraging behaviour for plant mating systems is a fundamental challenge in evolutionary ecology. Pollinators may adopt particular foraging tactics: ...complete trapline foraging (repeated movements along a fixed route), sample‐and‐shift trapline foraging (a variable route that incorporates information from previous experiences) and territorial foraging (stochastic movements within a restricted area). Studies that integrate these pollinator foraging tactics with plant mating systems are generally lacking.
We investigate the consequences of particular pollinator foraging tactics for Heliconia tortuosa. We combine parentage and sibship inference analysis with simulation modelling to: estimate mating system parameters; infer the foraging tactic adopted by the pollinators; and quantify the impact of pollinator foraging tactics on mating system parameters.
We found high outcrossing rates, ubiquitous multiple paternity and a pronounced departure from near‐neighbour mating. We also found that plants repeatedly receive pollen from a series of particular donors. We infer that the pollinators primarily adopt complete trapline foraging and occasionally engage in sample‐and‐shift trapline foraging. This enhances multiple paternity without a substantial increase in near‐neighbour mating.
The particular pollinator foraging tactics have divergent consequences for multiple paternity and near‐neighbour mating. Thus, pollinator foraging behaviour is an important driver of the ecology and evolution of plant mating systems.
Phenological overlap between crop flowering and pollinators is a crucial trait for the pollination of more than 75% of the world's crops. However, crop management rarely considers the seasonal aspect ...of plant–pollinator mutualism. Here, we investigate the phenological overlap between crops and pollinators and how it affects pollination and fruit production.
We measured the abundance and richness of native and non‐native pollinators visiting raspberry flowers at two different times during the flowering season (i.e. early and late flowering periods) and examined their effects on crop yield in 16 fields.
The community of pollinators foraging on raspberry flowers was more diverse and dominated by native pollinators during the early flowering period when most native plant species were flowering. Later in the season, when native flower resources declined in the surrounding environment, raspberry flowers were visited mainly by two non‐native bees: managed honeybees and the invasive bumblebee Bombus terrestris.
Pollinator contribution to raspberry yield was twice as high in the early flowering period compared to the late period (61% vs. 31% increase in drupelet set respectively). Flower damage caused by extremely high visitation frequencies by non‐native bees in the late period was six times higher than in the early flowering period (30% vs. 5% of damaged flowers respectively).
Synthesis and applications. Providing sufficient pollen and nectar resources to support wild pollinators over extended periods in agricultural landscapes can contribute to crop pollination and ensure high fruit weight and quality. This can be achieved by restoring natural and semi‐natural areas near crop fields with native, long‐flowering plant species. Growers and crop breeding programmes should consider selecting flowering times that coincide with periods of high diversity or abundance of native pollinators to reduce dependence on managed pollinators.
Resumen
La coincidencia temporal entre los polinizadores y la floración de los cultivos es un rasgo fundamental para la correcta polinización de más de 75% de los cultivos del mundo. Sin embargo, el manejo de los cultivos raramente considera el aspecto temporal del mutualismo planta‐polinizador. Aquí, exploramos el solapamiento fenológico entre un cultivo y sus polinizadores, y cómo este afecta la polinización y producción de frutos.
Para ello, medimos la abundancia y riqueza de polinizadores tanto nativos como no‐nativos que se encontraban visitando las flores del cultivo de frambuesa durante sus dos floraciones (i.e., temprana y tardía) y evaluamos sus efectos en la producción de fruta en 16 campos.
La comunidad de polinizadores visitando las flores del cultivo de frambuesa fue más diverso, y dominado por polinizadores nativos, durante la floración temprana, cuando en el paisaje había mayoría de especies de plantas nativas en flor. Durante la floración tardía de la frambuesa los recursos florales nativos declinaron en el ambiente, y las flores de la frambuesa fueron visitadas mayormente por dos especies no‐nativas de polinizadores: la abeja manejada de la miel y el abejorro invasor Bombus terrestris.
La contribución de los polinizadores en la producción del cultivo fue el doble en la floración temprana en comparación con la floración tardía (61% vs. 31% de aumento en el set de drupas, respectivamente). El daño floral causado por frecuencias de visitas muy altas de abejas no‐nativas fue seis veces mayor en la floración tardía en comparación con la temprana (30% vs. 5% de daño floral, respectivamente).
Síntesis y aplicaciones. Proveer de recursos florales como néctar y polen para promover polinizadores silvestres durante largos períodos en el paisaje agrícola puede contribuir a la polinización de cultivos y así asegurar altos rendimientos. Esto se puede lograr restaurando los hábitats naturales y semi‐naturales que se encuentran próximos a los cultivos con plantas nativas, de larga floración. Adicionalmente, tanto los agricultores como los programas de mejoramiento de cultivos deberían considerar la selección del momento de floración del cultivo para que coincida con los períodos de alta diversidad y abundancia de polinizadores nativos, con el fin de reducir la dependencia de polinizadores manejados.
Providing sufficient pollen and nectar resources to support wild pollinators over extended periods in agricultural landscapes can contribute to crop pollination and ensure high fruit weight and quality. This can be achieved by restoring natural and semi‐natural areas near crop fields with native, long‐flowering plant species. Growers and crop breeding programmes should consider selecting flowering times that coincide with periods of high diversity or abundance of native pollinators to reduce dependence on managed pollinators.
Ecological niches are crucial for species coexistence and diversification, but the niche concept has been underutilized in studying the roles of pollinators in plant evolution and reproduction. ...Pollination niches can be objectively characterized using pollinator traits, abundance, and distributions, as well as network topology. We review evidence that floral traits represent adaptations to pollination niches, where tradeoffs in trait deployment reinforce niche specialization. In turn, specialized pollination niches potentially increase speciation rates, foster species coexistence, and constrain species range limits. By linking studies of adaptation with those on speciation and coexistence, the pollination niche provides an organizing principle for research on plant reproduction, and conceptually unites these studies with fields of biology where the niche perspective is already firmly established.
Pollination is a crucial niche component for plants. The niche concept can apply to both occupied and currently unoccupied niches.Floral traits associated with pollination can be considered to be functional traits that can have similar or even better predictive capacity than functional traits in other areas of ecology.Plant–pollinator network methods provide opportunities for objective recognition of pollination niches, and can form the basis for testing relationships between niches and both floral and pollinator functional traits.The basis of specialization of pollination systems may be tradeoffs that favor adaptation to particular niches.Evidence suggests that, like abiotic niches, pollination contributes to species coexistence within communities, affects the geographic range of plants, and explains the evolution of reproductive isolation as well as differences in diversification rates between lineages.
Premise
Understanding how environmental stress affects the strength of mutualisms is critically important given observed and projected environmental changes. In particular, the frequency and duration ...of drought have been increasing worldwide. We investigated how water availability affects plant traits that mediate a pollination mutualism.
Methods
For butterfly‐pollinated Phlox drummondii, we determined how moisture availability affects flower size, nectar volume, and nectar sugar amount. Furthermore, we explored the role that local adaptation may play in responses to moisture availability by including plants collected from regions that differ in aridity. Finally, we determined whether responses of plant populations to selection may differ under drought by calculating heritability of traits under control and dry conditions.
Results
Flower size was generally smaller in dry plants than in control plants. Early in the treatment period, nectar volume and sugar were higher in dry plants than in control plants for plants from both arid and wetter regions. With prolonged dry treatment, nectar volume and sugar remained higher only in plants from the arid region. Heritability of floral traits was lower for water‐limited plants than for control plants.
Conclusions
Plant investment into pollination mutualisms under environmental stress may depend on the extent to which populations are already locally adapted to such conditions, suggesting that mutualism may remain strong, at least in arid regions. However, decreases in heritability under water‐limitation suggest that responses to selection imposed by pollinators may be low, even if drought‐adapted plants maintain production of rewards to pollinators.
Nectar robbing – harvesting nectar illegitimately – can have a variety of outcomes for plant sexual reproduction and for the pollinator community. Nectar robbers can damage flowers while robbing ...nectar, which could affect the behavior of subsequent flower visitors and, consequently, plant reproduction. However, only nectar manipulation by nectar robbers has so far received attention. We found a short‐tongued bee, Hoplonomia sp. (Halictidae), mutilating the conspicuous lower petal of the zygomorphic flowers of Leucas aspera (Lamiaceae) while robbing nectar. We hypothesized that the mutilation of the conspicuous lower petal deters legitimate pollinators on L. aspera flowers, which, in turn, might affect plant reproduction. We first assessed the proportion of naturally‐robbed flowers in plant populations for three years to confirm that it was not a purely local phenomenon due to a few individual bees. We then studied diversity, community and visitation characteristics of pollinators, nectar dynamics and fruit set in unrobbed and robbed open flowers in naturally‐robbed populations. The proportion of robbed flowers varied significantly across sites and years. Robbing did not affect nectar dynamics in flowers, but it did alter flower morphology, so much so that it reduced pollinator visitation and altered the pollinator community on robbed flowers. However, the maternal function of plant reproduction was not affected by nectar robbing. This study for the first time shows that a nectar robber can have an ecologically significant impact on floral morphology.
The selection of plant provenance for ecological restoration is an intensively debated topic. Throughout this debate, arguments mostly focus on plant performance, but little attention is paid to the ...effects of provenance on other members of the restored ecosystem. On the other hand, in restoration projects that focus specifically on supporting interacting biota, for example, wildflower strips among fields to support pollinators, the provenance choice is often not considered, partly because the effect of provenance on pollinators is unknown. In this pioneering case study, we tested whether pollinators differentiate between experimental plant communities of different provenances.
We established experimental plant communities with the same species composition but with plants originating from three different provenances. We then recorded plant phenology and observed pollinators and flower visitors interacting with these experimental communities and related the pollinator visitation to the provenance identity.
The provenances of the experimental plant communities had a strong and significant effect on the diversity and abundance of flower–pollinator interactions, with one provenance interacting two times as often as the other two provenances. The effect was driven by the differences in flowering phenology among provenances.
Synthesis and applications. Plant provenances substantially differ in their interactions with local pollinators. Therefore, the selection of plant provenance should be considered when planning restoration projects for the support of pollinators.
Die richtige Auswahl der Herkunft von Pflanzen für die ökologische Renaturierung ist ein intensiv diskutiertes Thema. In dieser Debatte liegt der Fokus in erster Linie auf der Performance der Pflanzen. Weit weniger Aufmerksamkeit erhält die Auswirkung der Herkunft auf andere Mitglieder des wiederhergestellten Ökosystems. In Renaturierungsprojekten, wiederum, die sich speziell auf die Unterstützung interagierender Biota konzentrieren, z.B. Blühstreifen zwischen Feldern zur Unterstützung von Bestäubern, wird die Wahl der Herkunft der Pflanzen häufig nicht berücksichtigt. Dies ist teilweise darauf zurückzuführen, dass die Wirkung der Herkunft auf Bestäuber unbekannt ist. In dieser wegbereitenden Fallstudie testeten wir, ob Bestäuber zwischen experimentellen Pflanzengemeinschaften verschiedener Provenienzen unterscheiden.
Wir etablierten experimentelle Pflanzengemeinschaften mit der gleichen Artenzusammensetzung, aber mit Pflanzen aus drei verschiedenen Herkünften. Anschließend erfassten wir die Phänologie der Pflanzen, beobachteten Bestäuber und Blütenbesucher, die mit diesen experimentellen Gemeinschaften interagierten, und setzten den Besuch der Bestäuber mit der Herkunft der Pflanzen in Beziehung.
Die Herkünfte der experimentellen Pflanzengemeinschaften hatten einen starken und signifikanten Einfluss auf die Vielfalt und Häufigkeit von Blüten‐Bestäuber‐Interaktionen, wobei eine Herkunft doppelt so häufig besucht wurde wie die anderen beiden. Dieser Effekt wurde durch die Unterschiede in der Blühphänologie zwischen den Herkünften hervorgerufen.
Synthese und Anwendungen. Pflanzenherkünfte unterscheiden sich erheblich in ihren Interaktionen mit lokalen Bestäubern. Daher sollte bei der Planung von Renaturierungsprojekten zur Unterstützung von Bestäubern die Auswahl des Herkunftsortes der Pflanzen berücksichtigt werden.
Plant provenances substantially differ in their interactions with local pollinators. Therefore, the selection of plant provenance should be considered when planning restoration projects for the support of pollinators.
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