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Serão os humanos semelhantes às plantas?

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Serão os humanos semelhantes às plantas?

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As angiospérmicas representam cerca de 90% de todas as plantas terrestres e as restantes dependem direta ou indiretamente delas. São conhecidas pelo desenvolvimento de flores, que constituem a sua estrutura reprodutora.
https://doi.org/10.1038/ncomms16047

Passiflora incarnata

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As gimnospérmicas são consideradas as plantas com semente que não produzem flores e, como tal, têm outras estratégias reprodutivas que dependem de cada grupo. Existem 4 divisões principais: cícades, ginkgo, coníferas e gnetales.
https://doi.org/10.1002/9781119312994.apr0490

Ginkgo biloba

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“The love for all living creatures is the most noble attribute of man.”       

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“The love for all living creatures is the most noble attribute of man.”       

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Charles Darwin

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Qual o papel do sexo das plantas?

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O "abominável mistério". Era assim que Charles Darwin descrevia a origem e o processo evolutivo das plantas com flor. O fenómeno atormentava-o por uma boa razão: parecia ser a exceção à sua já publicada teoria da evolução através da seleção natural - na qual defendia que são os seres vivos com as características mais favoráveis às condições do ambiente aqueles que sobrevivem, transmitindo essas características às gerações seguintes, num processo lento e contínuo ao longo do tempo.

Esta ideia de que a natureza não dá saltos era apenas contrariada pelas plantas com flor: de acordo com o registo fóssil, elas surgiram de forma repentina há cerca de cem milhões de anos, durante o Cretáceo Inferior, e multiplicaram-se a uma velocidade alucinante, sendo atualmente o maior e o mais diverso grupo de plantas. Que uma flor pudesse pôr em causa o trabalho de uma vida era algo que provocava pesadelos ao autor de A Origem das Espécies (1859) e partilhou essa preocupação em cartas trocadas com outros naturalistas.

Um século e meio depois, o fenómeno não está ainda completamente esclarecido. Entender como é que a flor - a estrutura responsável pela reprodução da maioria das plantas - evoluiu tem ocupado os pensamentos de Jessy Silva. Ela tem 24 anos, mas não gosta de facilidades: foi a complexidade deste campo de estudo, onde tantas questões ainda persistem, que a atraiu.

Sabemos menos sobre as plantas do que sobre os animais. Esse desconhecimento abre mais possibilidades de investigar, há mais questões a precisarem de resposta. Foi isso que me apaixonou", explica a investigadora do Laboratório Associado para a Química Verde (LAQV)/REQUIMTE no polo da Faculdade de Ciências da Universidade do Porto (FCUP), onde está a realizar o projeto de doutoramento na área da reprodução sexuada das plantas.

"Gosto de comparar o que estudo a uma história de amor. Tal como nós, nas plantas existe uma parte masculina e uma feminina que têm que se unir para haver a formação de novas plantas. A parte masculina são os grãos de pólen e a feminina são os óvulos no centro das flores. Quando se encontram, há a formação de uma semente que depois germina e leva a uma nova geração de plantas."

Saber mais sobre a reprodução das plantas não é um mero exercício de curiosidade intelectual. É uma necessidade. E uma necessidade cada vez mais urgente porque está relacionada com um dos maiores problemas que enfrentaremos a curto prazo: alimentar uma população em constante crescimento.

"Estima-se que, até 2050, a população humana atinja os dez mil milhões. Para alimentar essa população, teremos de aumentar em cerca de 60% a produtividade agrícola, mas sem aumentar a área cultivável e sem danificar ainda mais o nosso planeta. Portanto, temos de maximizar a produção de outra forma. Uma das soluções é estudar o processo de formação de sementes das espécies das quais nos alimentamos."

No doutoramento de Jessy Silva, financiado por uma bolsa da Fundação "la Caixa", a investigadora está a estudar este processo numa espécie modelo, a Arabidopsis thaliana, uma pequena planta com flor nativa da Europa e Ásia. "Apesar de não apresentar um valor económico direto, a sua utilização para estudos genéticos tem inúmeras vantagens: foi a primeira planta a ter o seu genoma completamente sequenciado, tem um ciclo de vida curto de apenas dois meses, produz um grande número de sementes e é facilmente manipulada a nível génico. Ao estudar esta planta modelo é possível adquirir conhecimento sobre a reprodução que poderá ser transferido para plantas com importância económica."

Jessy está focada nas proteínas arabinogalactânicas - um tipo de glicoproteínas envolvidas na reprodução sexuada das plantas. "Gosto de as comparar a algodão doce, porque elas têm um suporte - que é a proteína - coberto de diferentes açúcares. Sabemos que estes açúcares são muito importantes, contudo falta descobrir como afetam as funções destas glicoproteínas."

A cientista está a estudar um destes açúcares, o ácido glucurónico, que - descobriu-se recentemente - se liga ao cálcio. "O cálcio está envolvido em diversos processos do desenvolvimento, crescimento e reprodução das plantas, e esta ligação poderá estar por trás da função destas glicoproteínas." Ela espera ajudar a esclarecê-lo.

Nascida na Suíça, filha de emigrantes portugueses, Jessy veio para Portugal logo com 4 anos. Com clara vocação para as ciências e matemática desde cedo, foi-lhe fácil optar pela vertente do curso científico-natural no secundário. Tinha facilidade em compreender as matérias, mas a média de 19 valores não foi alcançou sem algum estudo. "O que sempre senti foi que não queria ficar limitada na escolha do curso na universidade devido à média. Achava muito triste quando ouvia os colegas mais velhos a contarem que não tinham conseguido entrar no curso que queriam."

Acabou por se decidir por Biologia, mas, surpreendentemente, muitos professores não lhe aprovaram esta inclinação: pareciam achar um desperdício que uma aluna com média de 19 fosse empregar a nota num curso com uma média de entrada de 15. "Por causa das minhas notas, houve alguma pressão para que seguisse Medicina. Mas em casa isso não aconteceu, os meus pais sempre me disseram que devia fazer o que gostasse." E o que gostava era Biologia.

Sem surpresa, foi a primeira candidata colocada no curso de Biologia da Faculdade de Ciências do Porto. Fez a licenciatura e o mestrado com uma bolsa da Fundação Calouste Gulbenkian destinada a alunos com médias de entrada excecionais no acesso ao ensino superior (Gulbenkian Mais). Mas não estava, nesta altura, inclinada para o estudo das plantas. "Comecei por pensar em Biologia Marinha, depois despertou-me interesse a Biologia Molecular, direcionada para o estudo do cancro. Acho que continuava a sentir uma certa pressão: 'Já que não foste para Medicina, então pelo menos faz investigação em saúde'", diz a rir. Foi o estágio que fez no laboratório de Reprodução Sexuada e Desenvolvimento em Plantas (SPReD lab) liderado pela professora Sílvia Coimbra, na FCUP, ainda durante a licenciatura, que a fez mudar de ideias. "Passei a adorar o estudo das plantas e nunca mais quis sair de lá. Acabei por tirar mestrado em Biologia Funcional e Biotecnologia de Plantas, também na FCUP."

"Até 2050, a população humana deve atingir os dez mil milhões. Teremos de aumentar em cerca de 60% a produtividade agrícola sem aumentar a área cultivável e sem danificar ainda mais o planeta"

Agora acorda às seis da manhã, toma o pequeno-almoço e põe-se a caminho do laboratório. Voltou a viver com os pais, em Vila Nova de Famalicão, depois dos anos numa residência no Porto durante a licenciatura e mestrado, e tem quase uma hora de caminho até à cidade. Gosta de sair cedo para evitar o trânsito que a faz demorar mais. Quando chega ao laboratório, às segundas-feiras de manhã cedo, começa a organizar agenda para os dias seguintes. Esta semana esteve a colocar genes modificados em bactérias e, nos próximos dias, vai colocá-los nas suas plantas, mergulhando as flores numa solução dessas bactérias.

Mas nem só as funções mais científicas a alegram. Aprendeu a gostar de tomar conta das plantas que estuda: semear, regar, estacar e transplantar são pequenos prazeres de jardineira que aprecia.

Imagina-se daqui a dez anos talvez a acabar o pós-doutoramento e, com sorte, a dar os primeiros passos como professora na sua universidade, cativando os alunos com os últimos desenvolvimentos no ramo da biologia das plantas. Mas a expectativa, claro, é acompanhada de receios. "O futuro da investigação não parece brilhante, há cada vez mais menos oportunidades e hipóteses de financiamento. E isso é assustador, mas não tenho medo. Acredito que tudo se vai alinhar para conseguir o que quero. E gosto de pensar que o esforço vai valer a pena."
Este artigo faz parte de uma série sobre investigação científica de ponta e é uma parceria entre o Observador, a Fundação "la Caixa" e o BPI. Jessy Faria da Silva, atualmente a desenvolver investigação no REQUIMTE LAQV - Laboratório Associado para a Química Verde, na Universidade do Porto, foi uma dos 65 selecionados (11 em Portugal) - entre 1078 candidaturas - para financiamento pela fundação sediada em Barcelona, ao abrigo da edição de 2020 do programa de bolsas de doutoramento INPhINIT. A investigadora recebeu 115 mil euros para desenvolver o projeto ao longo de três anos. As candidaturas para a edição de 2021 encerram a 4 de fevereiro ou 25 de fevereiro (de acordo com o local de realização da investigação).

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O que vamos comer no futuro depende da vida sexual das plantas

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O "abominável mistério". Era assim que Charles Darwin descrevia a origem e o processo evolutivo das plantas com flor. O fenómeno atormentava-o por uma boa razão: parecia ser a exceção à sua já publicada teoria da evolução através da seleção natural - na qual defendia que são os seres vivos com as características mais favoráveis às condições do ambiente aqueles que sobrevivem, transmitindo essas características às gerações seguintes, num processo lento e contínuo ao longo do tempo.

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Papel dos polinizadores na produção de abacates

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Papel dos polinizadores na produção de abacates

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Keira Dymond ,

Corresponding Author

Centre for Agri-Environmental Research, School of Agriculture, Policy and Development, University of Reading, Reading, UK
Correspondence
Keira Dymond, Centre for Agri-Environmental Research, School of Agriculture, Policy and Development, University of Reading, Reading, UK.

Email: k.dymond@pgr.reading.ac.uk
Search for more papers by this author

Abstract

Insect pollination increases the yield and quality of many crops and therefore, understanding the role of insect pollinators in crop production is necessary to sustainably increase yields. Avocado Persea americana benefits from insect pollination, however, a better understanding of the role of pollinators and their contribution to the production of this globally important crop is needed. In this study, we carried out a systematic literature review and meta-analysis of studies investigating the pollination ecology of avocado to answer the following questions: (a) Are there any research gaps in terms of geographic location or scientific focus? (b) What is the effect of insect pollinators on avocado pollination and production? (c) Which pollinators are the most abundant and effective and how does this vary across location? (d) How can insect pollination be improved for higher yields? (e) What are the current evidence gaps and what should be the focus of future research? Research from many regions of the globe has been published, however, results showed that there is limited information from key avocado producing countries such as Mexico and the Dominican Republic. In most studies, insects were shown to contribute greatly to pollination, fruit set and yield. Honeybees Apis mellifera were important pollinators in many regions due to their efficiency and high abundance, however, many wild pollinators also visited avocado flowers and were the most frequent visitors in over 50% of studies. This study also highlighted the effectiveness of stingless bees (Meliponini) and blow flies (Calliphoridae) as avocado pollinators although, for the majority of flower visitors, there is a lack of data on pollinator efficiency. For optimal yields, growers should ensure a sufficient abundance of pollinators in their orchards either through increasing honeybee hive density or, for a more sustainable approach, by managing wild pollinators through practices that protect or promote natural habitat.

1 INTRODUCTION

Avocado is one of at least 105 crops that receive yield benefits from animal pollination (Rader et al., ), and together, these crops represent approximately 35% of total agricultural production (Klein et al., ). Insects are the most important animal pollinator and therefore, to sustainably increase food production and feed a growing population, we need to better understand the role of insect pollinators and how they can be managed effectively in important animal-pollinated crops such as avocado.

Insect pollinators are thought to facilitate avocado pollination and thus increase production, and there is evidence of opportunities to improve yield through improved pollination service. For example, under normal pollination conditions, fruit set percentage at the tree level is less than 1% whereas, with the addition of hand pollination, fruit set rates have reached 5% at the branch level (Alcaraz & Hormaza, ; Evans et al., ; Garner & Lovatt, ). Furthermore, like many insect-pollinated crops, avocado yields may be adversely affected by widespread pollinator declines (Biesmeijer et al., ; Potts et al., ).

Optimizing avocado yields is increasingly important as demand for this product is rising with 32.6 million tonnes produced from 1999 to 2008 and 50.4 million tonnes from 2009 to 2018 globally (FAO, ). Today, avocados are not only a nutritious staple but also an important export crop for many countries (USD 6.84 billion globally for 2018) (FAO, ). However, in some avocado growing regions, expansion is having adverse environmental impacts such as, biodiversity loss and water resource depletion (Magrach & Sanz, ) and thus improving sustainable production is crucial.

Avocados have a synchronous, dichogamous flowering pattern. Flowers are hermaphroditic (have both male and female parts) but open as female and male separately at different times and this differs between cultivars. In 'A-type' cultivars, flowers commonly open as functionally female in the morning of the first day and functionally male in the afternoon of the second day, whereas, in 'B-type' cultivars, flowers are commonly female in the afternoon of the first day and male in the morning of the second day (Nirody, ; Stout, ). This process encourages outcrossing, however, avocados are self-fertile and pollination from within the same cultivar or tree (close pollination) can occur during the daily overlap of male and female flowers (Nirody, ; Stout, ). Daily overlapping is a common occurrence, but weather conditions play an important role in flowering synchronization and, under cooler temperatures, the length of time for male and female flowers to overlap can significantly increase (Ish-Am & Eisikowitch, ; Pattemore et al., ). In theory, self-pollination is possible during the male opening, as stigmas can still be receptive (Davenport et al., ), however, successful fertilization during this phase is extremely rare (Sedgley, ; Sedgley & Grant, ).

The dichogamous flowering pattern and other aspects of the avocado flower morphology (e.g. heavy and large pollen grains, the release of a low number of pollen grains, the production of nectar, and the small stigma size), indicate a probable important role for insect pollinators in avocado pollination (Dafni, ; Gazit & Degani, ; Sedgley & Griffin, ; Stout, ; Vithanage, ). Additionally, several studies have explored the effect of insect pollinators on avocado pollination. Controlled pollination experiments carried out by Davenport et al. () and Davenport () showed no significant difference in pollination rates between open-pollinated treatments with high honeybee hive density compared with closed pollination treatments with no access to insect pollinators; therefore, it is argued that wind pollination is the dominant pollination mechanism in these systems. However, most other studies have shown that without insect pollinators; pollination (Cabezas & Cuevas, ), fruit set (Can-Alonzo et al., ; Malerbo-Souza et al., ) and yields (Mulwa, Kahuthia-Gathu, et al., ; Petersen, ; Robbertse & Johannsmeier, ) are significantly reduced in comparison with open-pollinated treatments. A better understanding of the role of insect pollinators in avocado production and what factors result in this variation is needed.

Additionally, across the globe, there is growing evidence of the contribution from wild pollinators and natural habitats to pollination services (Dainese et al., 2019; Martin et al., ; Garibaldi et al., , ). It is therefore important to determine which pollinators are pollinating different crops, including avocado, and identify effective ways to improve and protect this ecosystem service. A review of avocado pollination ecology is necessary to inform sustainable management of this important ecosystem services as well as to help target future research.

We build on previous reviews on avocado pollination and reproductive biology by Wysoki et al. (), Gazit and Degani () and Ish-Am () by providing an updated and systematic analysis of published literature on avocado pollination. The aims of this paper were as follow: (a) to consider the geographic variation and research focus of existing research on avocado pollination, (b) assess the effect of insect pollinators on avocado pollination and production, (c) identify which insect pollinators are the most abundant and effective, and how this varies by geographic location, (d) highlight potential ways to improve insect pollination for higher yields, exploring both wild and managed pollinators and (e) identify evidence gaps and direct future research.

2 METHODOLOGY

2.1 Literature review

Literature was sourced through a systematic review using the following search terms; (avocado* OR 'Persea americana*') AND (pollination* OR pollinators*); 'insect pollination*' AND (avocado* OR 'Persea americana*'); 'insect pollination*' AND (avocado* OR 'Persea americana*') AND Management; Honeybees* AND (avocado* OR 'Persea americana*'); 'Pollination services*' AND (avocado* OR 'Persea americana*'); (avocado* OR 'Persea americana*') AND 'improve pollination*'. These terms were used in two scientific databases; web of knowledge and Google scholar. In web of knowledge, all the returned searches were assessed for suitability, whereas in Google scholar, due to the high volume of searches returned, the first 500 most relevant papers were assessed. Google scholar returned a range of sources (e.g. ebooks and grey literature); however, it is possible, that this search methodology missed some wider literature. These searches provided a total of 4,043 papers in which the title and, or abstracts were assessed for suitability. Papers were selected if they had carried out original research which contributed to this review's key aims. This resulted in 35 unique papers and therefore, to increase the sample size and the range of sources, previous avocado pollination reviews were utilized to source additional relevant papers, from which a further five were found. Paper searches took place from April to June 2020. Searches were carried out in English, and if this returned a paper in another language, it was translated online and assessed for suitability. In total, the search methods produced 40 papers that were included in this review (see Table S1).

2.2 Data analysis

2.2.1 The contribution of insect pollinators to pollination and production

A meta-analysis was carried out to assess the difference in avocado pollination between open and closed pollinated treatments for pollination and production metrics including; the percentage of flowers pollinated, fruit set (data collected between one and three months' post-flowering and either per branch, inflorescence or panicle), final fruit count per tree and fruit weight per avocado. The mean, standard deviation ( SD) and sample size ( N) were extracted directly from three papers (seven experiments); however, in many studies, this information was not provided. Therefore, studies were either excluded from the analysis or, if possible, SD and N were calculated. In one study, SD and N were calculated at the replicate level, however, other studies provided only information for different years or different orchards of differing cultivars. In these cases, year and cultivar were considered replicates, and the mean and SD were calculated accordingly (see Table S2). A random effects model was run using this dataset. The results showed high heterogeneity ( I ² = 95%) and therefore, an influence analysis was used to identify outliers and consequently two studies (three experiments) were removed (see Table S3 for final dataset used in meta-analysis). This resulted in reduced, but still high heterogeneity ( I ² = 79%) and therefore, to further investigate this, the data were sub-categorized based on plausible causes for variance including response variable (fruit set, fruit weight, pollination and yield), climate (humid or dry), cultivar (Hass or other) and experimental scale (branch, tree, site and year). To check for interdependency associated with experiments coming from the same studies, a reduced model was run with data that only included one experiment per study (see Table S4). This was used to assess if interdependency was affecting the overall result and to determine whether the full or reduced model should be used to interpret the results. All meta-analyses models were carried out in R version 3.6.1 (R Core Team, ) using the 'meta' package (Balduzzi et al., ).

In addition to the meta-analysis, to allow the inclusion of studies that had not provided all required data ( N, SD, mean), a further qualitative analysis was carried out where the means of open and closed pollination treatments for each variable were summarized graphically. Data were categorized based on the response metric (fruit set per branch, per cent of flowers pollinated and fruit weight), and violin plots were created. Data which had been excluded from the meta-analysis due to extreme outliers (as identified in the influence analysis) were also excluded from these summaries. A vote count was also implemented for controlled pollination experiments. Studies that had reported statistical significance between pollination treatments were categorized into either Open > Closed, Open < Closed or Non-Significant and tallied. If studies had multiple but conflicting results, either from measuring different variables or applying different treatments (e.g. climate or cultivar) then an overall category was assigned based on which result was most prevalent across the different variables and treatments.

2.2.2 Abundance and efficiency of insect pollinators

A qualitative assessment was also carried out to compare the relative abundance of different pollinators between studies and regions. Eighteen studies provided data on pollinator abundances and data were taken either directly from the paper or calculated from data on total observations per species. Species were categorized into broad taxonomic groups (honeybee, stingless bee, wild bees, wasp, ant, blow flies, hover flies, other diptera, coleoptera, lepidopitera, other) for comparison. Studies were then grouped by country and total abundances across all studies per country were used to calculate average country abundance. To explore pollinator efficiency, data were taken either directly from the paper or supplementary sources (see Table S5-S7). Three studies compared pollen deposition per visit, five studies explored the amount of pollen carried by pollinators, and three studies looked at the visitation rate between different groups of pollinations. A mean was calculated from the raw data and represented in box and whisker plots. All graphical summaries were produced in R version 3.6.1 (R Core Team, ), using the package 'ggplot2' (Wickham, ).

3 RESULTS

3.1 Research focus and geographical spread

The majority of the studies identified by the literature search considered the abundance and efficiency of different pollinator species (33%) or the contribution of insect pollinators to pollination and production (30%) (Figure 1a). Most of the studies were carried out in the USA (14%) and Israel (14%), however, these countries count for only 6.6% of global production (data for 1999-2018) (FAO, ). There were less than five studies carried out per country for all remaining countries, and for three out of the top six avocado producing countries, no studies at all were identified by the search (Dominican Republic, Peru and Indonesia) (Figure 1b).

3.2 Contribution of insect pollinators to pollination and production

Overall for the meta-analysis, eight studies (13 data points) were included in the dataset following the removal of outliers. The result showed that over all, there was a significant increase (standardized mean difference [SMD] of 2.46 and 95% CI 0.75-4.16) in pollination, fruit set and yield in open pollination conditions compared to when insect pollinators are excluded, however, heterogeneity was high ( I ² = 79%) and significant (Figure 2). Following subcategorization by response variable, climate, cultivar and experimental scale, the SMD remained higher for open-pollinated treatments compared to closed for all metrics considered, but heterogeneity remained high and significant for all categories indicating that variability between studies was considerable (see Figure S1). The reduced model to account for interdependency (one data point from each study) showed a similar SMD in comparison with the full model (2.7 and 2.46, respectively) and the general trend for the confidence interval was in the same direction, although this was larger in the reduced model given the fewer data points (95% CI of −0.09 to 5.49) (see Figure S2). This suggested that interdependency did not strongly affect the overall results and as such, the full model was used to interpret the results as this provided the greatest statistical power. These trends seen in the meta-analysis were additionally supported by the outputs from the mean summaries. Nearly all key indicators showed higher values in open treatments compared with closed, and the majority of closed treatments showed close to zero pollination (Figure 3b) or fruit set (Figure 3a). There was often considerable variation in the results for the open treatments. Similarly, the findings from the vote count showed that most studies had a significantly higher value for pollination and yield in open treatments (Figure 4). Fruit weight was the only pollination variable where the majority of studies did not show a significant positive or negative effect of insect pollination (Figure 4) and the mean summaries and meta-analysis showed only a very small difference (Figure 3c and Figure S1).

3.3 Abundance and efficiency of insect pollinators

Managed honeybees were the most frequent pollinators overall and were observed in all studies and countries (Figure 5a,b). In 13 out of 18 cases, they showed the greatest relative abundance of any single pollinator species, but this did vary considerably between 10% and 92% depending on the study. Hoverflies (Syrphidae) were also common pollinators with an overall relative abundance of 12% (Figure 6c). Stingless bees generally had high abundance in locations where they were found, but they were only observed in four studies while conversely, wild bees were seen in nine studies but had lower abundances (Figure 6a,b). Nine studies measured some aspect of pollinator efficiency but different metrics and taxa were measured and therefore, cross-study comparisons and broader generalizations cannot be obtained from this data. However, the general trend indicates that honeybees, stingless bees, and blow flies carried and deposited the greatest amount of pollen (Figure 7a,b) and, honeybees are potentially more effective than blow flies due to the higher number of flower visits per minute (Figure 7c).

3.4 Improving insect pollination

Studies on improving insect pollination have generally focused on three areas; optimizing the contribution of honeybees ( n = 4), utilizing other managed species ( n = 4) and ways to improve pollination by wild pollinators ( n = 2) (Table 1). The results showed that increasing honeybee density leads to significantly higher rates of pollination and production. Other managed pollinators assessed were, the New World Carniolan honeybee Apis mellifera carnica Pollman 1879 ( n = 2), the buff-tailed bumblebee Bombus terrestris Linnaeus 1758 ( n = 1), and the western bumblebee Bombus occidentalis Greene 1858 ( n = 1). The results suggested that buff-tailed bumblebees could be effective pollinators, especially in the Etinger variety, as buff-tailed bumblebee treatment plots showed higher rates of pollination and yield in comparison with honeybee treatment plots (Ish-Am et al., ). The western bumblebee was shown to forage in avocado orchards and the results suggest that the introduction of bumblebee hives may increase yields; however, this study did not record bee activity on the crop (McNeil & Pidduck, ). Trials on the New World Carniolan honeybee explored whether this subspecies had a higher preference for avocado pollen and higher visitation rate on avocado flowers in comparison with the Apis mellifera ligustica Spinola 1806, however, the results showed no significant difference in visitation rate between the two subspecies (Afik et al., ; Fetscher et al., ). Two studies looked at wild pollinators and methods to increase their abundance. These studies showed that intensive management practices such as spraying pesticides and the removal of forested areas and weeds lead to a reduction in pollinator diversity (Villamil et al., ) and that spraying pesticides reduces wild pollinator abundance and avocado yield (Castañeda-Vildózola et al., ).

4 DISCUSSION

Our review highlights the new knowledge obtained through research on avocado pollination since the last significant literature reviews were conducted more than 15 years previously. It has built on these reviews by including the analysis of 24 new studies and current topics such as the impacts of land management on wild pollinators. Additionally, we carried out a meta-analysis on the contribution from insect pollinators to pollination and summarized global pollinator abundance and pollination efficiency of key species, thus providing a more nuanced understanding of these issues.

4.1 Research focus and geographical spread

4.2 Contribution of insect pollinators to pollination and production

The results also showed a wide variation in the contribution of insect pollinators. The meta-analysis had high and significant heterogeneity ( I ² = 79%) and, in the mean summaries, the range for open-pollinated treatments was broad and overlapped with closed pollination treatments. A possible explanation for this variation could be that, in some circumstances, pollinators are thought to contribute little to the pollination process (Clark, ; Davenport, ; Davenport et al., ; Ying et al., ). It is hypothesized that self-pollination is possible if stigmas remain receptive in phase 2 and this is thought to be feasible with specific cultivars (Davenport et al., ) and in humid climates (Gazit & Degani, ). Additionally, in a recent study, Davenport () argues that regardless of other external factors, self-pollination makes up a major part of avocado pollination. However, this study only measures pollen tube growth in the style and wider evidence suggests that during phase 2, pollen tubes are unable to reach the ovule and thus successful fertilization is not possible (Sedgley & Grant, ). Davenport () also suggests that wind pollination is more prominent than insect pollination and shows that there is no difference in the per cent of pollinated stigmas between open and closed treatments. This contrasts with our findings and several other studies and thus indicates there are likely some varietal or management factors affecting the role of insect pollinators.

Variation in pollination services and resource availability between locations are probable explanations for the yield disparities in the open-pollinated treatments. Pollinator abundance and, or efficiency, were seldom reported in controlled pollination studies and this is likely to vary significantly due to differences in; managed beehive densities, proximity to natural areas and wild pollinators, and the availability of native avocado pollinators. Variation in resource availability is also likely to be high and this has been shown to impact fruit set. Alcaraz et al. () show that the amount of starch content in the style has a high correlation with the number of flowers that successfully develop into avocado fruits. Additionally, the scale at which pollination is assessed can also affect the level of contribution to pollination (Howlett et al., ; Webber et al., ) and, this may explain the significant variation between studies which had measured insect contribution at different scales (inflorescence, branch, tree).

Variation in resource availability might also explain why our results showed only limited differences in fruit weight between open and closed pollination treatments as agronomic factors that influence general tree health (e.g. irrigation), and resource availability are known to have a greater influence on fruit size (Kremer-Köhne & Köhne, ). However, alternatively, this result could be an indication of pollination deficits in avocado orchards. Open-pollinated treatments have a higher fruit set in comparison with closed pollination treatments and yet, fruit weight per avocado is similar across the two treatments. This suggests that sufficient resources are available as the tree is able to produce a good fruit weight regardless of the number of fruit set and thus, could indicate that yield deficits are the result of low pollination and reduced fruit set.

4.3 Abundance and efficiency of insect pollinators

Overall, managed honeybees appear to be contributing most to avocado pollination in many regions due to their general efficiency and high abundance (average overall abundance was >50%). This finding was noted in the majority of studies and has been highlighted in previous reviews (Ish-Am, ; Wysoki et al., ). However, it is well known that honeybees can be sensitive to wind, rain and low temperatures (Bushuru, ; Can-Alonzo et al., ) and often prefer other nectar sources (Ish-Am & Eisikowitch, ). Therefore, under poor weather conditions or where other flowers are in bloom at the same time, their contribution to avocado pollination could be reduced, and diverse pollinator communities including both wild and managed pollinators may provide more consistent pollination (Woodcock et al., ).

Wild pollinators were also shown to play an important role. In 11 of the 18 studies and six of the 11 countries, they were more abundant than managed honeybees and although the contribution to pollination services is unknown for many wild pollinators, there is some evidence that certain wild species are efficient avocado pollinators. Stingless bees were shown to carry a comparably high amount of pollen (around 500 grains) and qualitative comments suggest they can effectively transfer pollen as their body size suits the shape of avocado flowers (Ish-Am et al., ). Blow flies were also shown to be important pollinators as they deposited a high amount of pollen per visit, which may be attributed to the open structure of the avocado flower making it well suited to fly pollination (Vithanage, ). However, in comparison with honeybees, their flower visitation rate was low, thus reducing their potential effectiveness. The overall contribution to pollination from individual wild species is reduced due their low abundances in comparison with honeybees (e.g. the relative abundance was 28% stingless bees, 19%, for blow flies and 46% for honeybees). As such, active management to increase the abundance of certain wild pollinators may be an effective strategy to increase pollination; however, more research is required to quantify the effectiveness of wild pollinators in specific regions.

Previous studies have highlighted other potentially important pollinators. In certain locations, wasps are efficient pollinators (Ish-Am et al., ; Papademetriou, ; Perez-Balam et al., ) and a study by Ish-Am et al. () shows that managed buff-tailed bumblebees can increase pollination. These pollinator groups were not covered in this analysis due to a lack of quantitative efficiency data and thus, this should be a target for future research. In temperate regions, it is also necessary to consider the potential of nocturnal pollinators, particularly from the diptera and lepidoptera order, as lower night temperatures can result in both male and female flowers opening during the night. Pattemore et al. () showed that pollinating insects such as wood gnats, crane flies, scarab beetles, capsid bugs, forest moths and brown lacewings did visit avocado flowers during the night and were carrying avocado pollen. However, no other studies have explored this topic and therefore further investigations in this area are also needed.

4.4 Improving insect pollination

Tools to better manage pollination in avocado are required given the increasing production of avocados globally (FAO, ), the need for more sustainable production systems that make better use of inputs such as insect pollination (Garibaldi et al., ), and that pollination deficits in avocado are already in evidence (Alcaraz & Hormaza, ; Evans et al., ). This study highlighted three key themes to improve pollination: increasing honeybee density, utilising other managed pollinators, and exploring the potential from wild pollinators.

The results from three studies showed that increasing honeybee density led to an increase in visitation rate and an increase in pollination and production (Ish-Am & Eisikowitch, ; Ish-Am & Lahav, ; Peña & Carabalí, ). Similar findings were concluded in a meta-analysis by Rollin and Garibaldi () who showed that, for a range of insect-pollinated crops, production does increase with honeybee density, up to a saturation point. However, for avocado production, we still lack evidence for optimal stocking densities and spatial arrangements of hives, particularly for some of the significant global producers.

4.5 Study limitations

The low number of available studies presented a major limitation. For the meta-analysis, it was necessary to include papers testing a wide range of variables (fruit set, yield, pollination) and as such, the data were very heterogeneous. Furthermore, some of these studies provided limited information on the methods used, and often, N and SD were not provided and therefore had to be calculated from the information available. The restricted data availability also meant that statistical analysis was not feasible for the majority of the research questions and therefore, the strength and scope of the conclusions made is limited. However, despite these challenges, some general findings, research gaps and recommendations have been identified.

5 CONCLUSIONS

5.1 Key findings and research gaps

Dominican Republic and Mexico are responsible for 37% of global avocado production but only 13% of studies originated from these countries and therefore, further research in these countries is required.

In 19 out of 23 studies, insect pollinators contributed significantly to pollination, fruit set and yield.

Managed honeybees were identified as the most important pollinators due to their frequency and efficiency. However, further information is needed to optimize local field beehive placement and density.

The abundance of wild pollinators ranged from 90% to 8% across locations and further research is required to understand their efficiency and contribution to avocado pollination.

Land management practices affected the abundance and diversity of wild pollinators and this can have negative implications for yield.

5.2 Recommendations for growers

In most situations, growers will benefit from an increased density of pollinators.

Increasing honeybee hive density will likely increase production but may not be cost-effective in all contexts.

The utilization of alternative managed pollinators (e.g. stingless bees) or active management of wild pollinators may also be applicable in some circumstances.

ACKNOWLEDGEMENTS

This research was carried out as part of the BBSRC funded Waitrose Collaborative Training Partnership and the PhD was funded by the University of Reading. The authors also wish to thank Greencell and Jonathan Berry for support provided throughout the project.

CONFLICT OF INTEREST

The authors declare that they have no known competing financial interest or personal relationships that could have appeared to influence the work in this paper.

AUTHOR CONTRIBUTIONS

Dymond and Garratt conceived research. Dymond conducted systematic review, analysed data, conducted statistical analyses and wrote the manuscript. Garratt supported statistical analyses. All authors provided feedback on the manuscript, read and approved the manuscript.

Abstract

Insect pollination increases the yield and quality of many crops and therefore, understanding the role of insect pollinators in crop production is necessary to sustainably increase yields. Avocado Persea americana benefits from insect pollination, however, a better understanding of the role of pollinators and their contribution to the production of this globally important crop is needed. In this study, we carried out a systematic literature review and meta-analysis of studies investigating the pollination ecology of avocado to answer the following questions: (a) Are there any research gaps in terms of geographic location or scientific focus? (b) What is the effect of insect pollinators on avocado pollination and production? (c) Which pollinators are the most abundant and effective and how does this vary across location? (d) How can insect pollination be improved for higher yields? (e) What are the current evidence gaps and what should be the focus of future research? Research from many regions of the globe has been published, however, results showed that there is limited information from key avocado producing countries such as Mexico and the Dominican Republic. In most studies, insects were shown to contribute greatly to pollination, fruit set and yield. Honeybees Apis mellifera were important pollinators in many regions due to their efficiency and high abundance, however, many wild pollinators also visited avocado flowers and were the most frequent visitors in over 50% of studies. This study also highlighted the effectiveness of stingless bees (Meliponini) and blow flies (Calliphoridae) as avocado pollinators although, for the majority of flower visitors, there is a lack of data on pollinator efficiency. For optimal yields, growers should ensure a sufficient abundance of pollinators in their orchards either through increasing honeybee hive density or, for a more sustainable approach, by managing wild pollinators through practices that protect or promote natural habitat.

1 INTRODUCTION

Avocado is one of at least 105 crops that receive yield benefits from animal pollination (Rader et al., ), and together, these crops represent approximately 35% of total agricultural production (Klein et al., ). Insects are the most important animal pollinator and therefore, to sustainably increase food production and feed a growing population, we need to better understand the role of insect pollinators and how they can be managed effectively in important animal-pollinated crops such as avocado.

Insect pollinators are thought to facilitate avocado pollination and thus increase production, and there is evidence of opportunities to improve yield through improved pollination service. For example, under normal pollination conditions, fruit set percentage at the tree level is less than 1% whereas, with the addition of hand pollination, fruit set rates have reached 5% at the branch level (Alcaraz & Hormaza, ; Evans et al., ; Garner & Lovatt, ). Furthermore, like many insect-pollinated crops, avocado yields may be adversely affected by widespread pollinator declines (Biesmeijer et al., ; Potts et al., ).

Optimizing avocado yields is increasingly important as demand for this product is rising with 32.6 million tonnes produced from 1999 to 2008 and 50.4 million tonnes from 2009 to 2018 globally (FAO, ). Today, avocados are not only a nutritious staple but also an important export crop for many countries (USD 6.84 billion globally for 2018) (FAO, ). However, in some avocado growing regions, expansion is having adverse environmental impacts such as, biodiversity loss and water resource depletion (Magrach & Sanz, ) and thus improving sustainable production is crucial.

Avocados have a synchronous, dichogamous flowering pattern. Flowers are hermaphroditic (have both male and female parts) but open as female and male separately at different times and this differs between cultivars. In 'A-type' cultivars, flowers commonly open as functionally female in the morning of the first day and functionally male in the afternoon of the second day, whereas, in 'B-type' cultivars, flowers are commonly female in the afternoon of the first day and male in the morning of the second day (Nirody, ; Stout, ). This process encourages outcrossing, however, avocados are self-fertile and pollination from within the same cultivar or tree (close pollination) can occur during the daily overlap of male and female flowers (Nirody, ; Stout, ). Daily overlapping is a common occurrence, but weather conditions play an important role in flowering synchronization and, under cooler temperatures, the length of time for male and female flowers to overlap can significantly increase (Ish-Am & Eisikowitch, ; Pattemore et al., ). In theory, self-pollination is possible during the male opening, as stigmas can still be receptive (Davenport et al., ), however, successful fertilization during this phase is extremely rare (Sedgley, ; Sedgley & Grant, ).

The dichogamous flowering pattern and other aspects of the avocado flower morphology (e.g. heavy and large pollen grains, the release of a low number of pollen grains, the production of nectar, and the small stigma size), indicate a probable important role for insect pollinators in avocado pollination (Dafni, ; Gazit & Degani, ; Sedgley & Griffin, ; Stout, ; Vithanage, ). Additionally, several studies have explored the effect of insect pollinators on avocado pollination. Controlled pollination experiments carried out by Davenport et al. () and Davenport () showed no significant difference in pollination rates between open-pollinated treatments with high honeybee hive density compared with closed pollination treatments with no access to insect pollinators; therefore, it is argued that wind pollination is the dominant pollination mechanism in these systems. However, most other studies have shown that without insect pollinators; pollination (Cabezas & Cuevas, ), fruit set (Can-Alonzo et al., ; Malerbo-Souza et al., ) and yields (Mulwa, Kahuthia-Gathu, et al., ; Petersen, ; Robbertse & Johannsmeier, ) are significantly reduced in comparison with open-pollinated treatments. A better understanding of the role of insect pollinators in avocado production and what factors result in this variation is needed.

Additionally, across the globe, there is growing evidence of the contribution from wild pollinators and natural habitats to pollination services (Dainese et al., 2019; Martin et al., ; Garibaldi et al., , ). It is therefore important to determine which pollinators are pollinating different crops, including avocado, and identify effective ways to improve and protect this ecosystem service. A review of avocado pollination ecology is necessary to inform sustainable management of this important ecosystem services as well as to help target future research.

We build on previous reviews on avocado pollination and reproductive biology by Wysoki et al. (), Gazit and Degani () and Ish-Am () by providing an updated and systematic analysis of published literature on avocado pollination. The aims of this paper were as follow: (a) to consider the geographic variation and research focus of existing research on avocado pollination, (b) assess the effect of insect pollinators on avocado pollination and production, (c) identify which insect pollinators are the most abundant and effective, and how this varies by geographic location, (d) highlight potential ways to improve insect pollination for higher yields, exploring both wild and managed pollinators and (e) identify evidence gaps and direct future research.

2 METHODOLOGY

2.1 Literature review

Literature was sourced through a systematic review using the following search terms; (avocado* OR 'Persea americana*') AND (pollination* OR pollinators*); 'insect pollination*' AND (avocado* OR 'Persea americana*'); 'insect pollination*' AND (avocado* OR 'Persea americana*') AND Management; Honeybees* AND (avocado* OR 'Persea americana*'); 'Pollination services*' AND (avocado* OR 'Persea americana*'); (avocado* OR 'Persea americana*') AND 'improve pollination*'. These terms were used in two scientific databases; web of knowledge and Google scholar. In web of knowledge, all the returned searches were assessed for suitability, whereas in Google scholar, due to the high volume of searches returned, the first 500 most relevant papers were assessed. Google scholar returned a range of sources (e.g. ebooks and grey literature); however, it is possible, that this search methodology missed some wider literature. These searches provided a total of 4,043 papers in which the title and, or abstracts were assessed for suitability. Papers were selected if they had carried out original research which contributed to this review's key aims. This resulted in 35 unique papers and therefore, to increase the sample size and the range of sources, previous avocado pollination reviews were utilized to source additional relevant papers, from which a further five were found. Paper searches took place from April to June 2020. Searches were carried out in English, and if this returned a paper in another language, it was translated online and assessed for suitability. In total, the search methods produced 40 papers that were included in this review (see Table S1).

2.2 Data analysis

2.2.1 The contribution of insect pollinators to pollination and production

A meta-analysis was carried out to assess the difference in avocado pollination between open and closed pollinated treatments for pollination and production metrics including; the percentage of flowers pollinated, fruit set (data collected between one and three months' post-flowering and either per branch, inflorescence or panicle), final fruit count per tree and fruit weight per avocado. The mean, standard deviation ( SD) and sample size ( N) were extracted directly from three papers (seven experiments); however, in many studies, this information was not provided. Therefore, studies were either excluded from the analysis or, if possible, SD and N were calculated. In one study, SD and N were calculated at the replicate level, however, other studies provided only information for different years or different orchards of differing cultivars. In these cases, year and cultivar were considered replicates, and the mean and SD were calculated accordingly (see Table S2). A random effects model was run using this dataset. The results showed high heterogeneity ( I ² = 95%) and therefore, an influence analysis was used to identify outliers and consequently two studies (three experiments) were removed (see Table S3 for final dataset used in meta-analysis). This resulted in reduced, but still high heterogeneity ( I ² = 79%) and therefore, to further investigate this, the data were sub-categorized based on plausible causes for variance including response variable (fruit set, fruit weight, pollination and yield), climate (humid or dry), cultivar (Hass or other) and experimental scale (branch, tree, site and year). To check for interdependency associated with experiments coming from the same studies, a reduced model was run with data that only included one experiment per study (see Table S4). This was used to assess if interdependency was affecting the overall result and to determine whether the full or reduced model should be used to interpret the results. All meta-analyses models were carried out in R version 3.6.1 (R Core Team, ) using the 'meta' package (Balduzzi et al., ).

In addition to the meta-analysis, to allow the inclusion of studies that had not provided all required data ( N, SD, mean), a further qualitative analysis was carried out where the means of open and closed pollination treatments for each variable were summarized graphically. Data were categorized based on the response metric (fruit set per branch, per cent of flowers pollinated and fruit weight), and violin plots were created. Data which had been excluded from the meta-analysis due to extreme outliers (as identified in the influence analysis) were also excluded from these summaries. A vote count was also implemented for controlled pollination experiments. Studies that had reported statistical significance between pollination treatments were categorized into either Open > Closed, Open < Closed or Non-Significant and tallied. If studies had multiple but conflicting results, either from measuring different variables or applying different treatments (e.g. climate or cultivar) then an overall category was assigned based on which result was most prevalent across the different variables and treatments.

2.2.2 Abundance and efficiency of insect pollinators

A qualitative assessment was also carried out to compare the relative abundance of different pollinators between studies and regions. Eighteen studies provided data on pollinator abundances and data were taken either directly from the paper or calculated from data on total observations per species. Species were categorized into broad taxonomic groups (honeybee, stingless bee, wild bees, wasp, ant, blow flies, hover flies, other diptera, coleoptera, lepidopitera, other) for comparison. Studies were then grouped by country and total abundances across all studies per country were used to calculate average country abundance. To explore pollinator efficiency, data were taken either directly from the paper or supplementary sources (see Table S5-S7). Three studies compared pollen deposition per visit, five studies explored the amount of pollen carried by pollinators, and three studies looked at the visitation rate between different groups of pollinations. A mean was calculated from the raw data and represented in box and whisker plots. All graphical summaries were produced in R version 3.6.1 (R Core Team, ), using the package 'ggplot2' (Wickham, ).

3 RESULTS

3.1 Research focus and geographical spread

The majority of the studies identified by the literature search considered the abundance and efficiency of different pollinator species (33%) or the contribution of insect pollinators to pollination and production (30%) (Figure 1a). Most of the studies were carried out in the USA (14%) and Israel (14%), however, these countries count for only 6.6% of global production (data for 1999-2018) (FAO, ). There were less than five studies carried out per country for all remaining countries, and for three out of the top six avocado producing countries, no studies at all were identified by the search (Dominican Republic, Peru and Indonesia) (Figure 1b).

3.2 Contribution of insect pollinators to pollination and production

Overall for the meta-analysis, eight studies (13 data points) were included in the dataset following the removal of outliers. The result showed that over all, there was a significant increase (standardized mean difference [SMD] of 2.46 and 95% CI 0.75-4.16) in pollination, fruit set and yield in open pollination conditions compared to when insect pollinators are excluded, however, heterogeneity was high ( I ² = 79%) and significant (Figure 2). Following subcategorization by response variable, climate, cultivar and experimental scale, the SMD remained higher for open-pollinated treatments compared to closed for all metrics considered, but heterogeneity remained high and significant for all categories indicating that variability between studies was considerable (see Figure S1). The reduced model to account for interdependency (one data point from each study) showed a similar SMD in comparison with the full model (2.7 and 2.46, respectively) and the general trend for the confidence interval was in the same direction, although this was larger in the reduced model given the fewer data points (95% CI of −0.09 to 5.49) (see Figure S2). This suggested that interdependency did not strongly affect the overall results and as such, the full model was used to interpret the results as this provided the greatest statistical power. These trends seen in the meta-analysis were additionally supported by the outputs from the mean summaries. Nearly all key indicators showed higher values in open treatments compared with closed, and the majority of closed treatments showed close to zero pollination (Figure 3b) or fruit set (Figure 3a). There was often considerable variation in the results for the open treatments. Similarly, the findings from the vote count showed that most studies had a significantly higher value for pollination and yield in open treatments (Figure 4). Fruit weight was the only pollination variable where the majority of studies did not show a significant positive or negative effect of insect pollination (Figure 4) and the mean summaries and meta-analysis showed only a very small difference (Figure 3c and Figure S1).

3.3 Abundance and efficiency of insect pollinators

Managed honeybees were the most frequent pollinators overall and were observed in all studies and countries (Figure 5a,b). In 13 out of 18 cases, they showed the greatest relative abundance of any single pollinator species, but this did vary considerably between 10% and 92% depending on the study. Hoverflies (Syrphidae) were also common pollinators with an overall relative abundance of 12% (Figure 6c). Stingless bees generally had high abundance in locations where they were found, but they were only observed in four studies while conversely, wild bees were seen in nine studies but had lower abundances (Figure 6a,b). Nine studies measured some aspect of pollinator efficiency but different metrics and taxa were measured and therefore, cross-study comparisons and broader generalizations cannot be obtained from this data. However, the general trend indicates that honeybees, stingless bees, and blow flies carried and deposited the greatest amount of pollen (Figure 7a,b) and, honeybees are potentially more effective than blow flies due to the higher number of flower visits per minute (Figure 7c).

3.4 Improving insect pollination

Studies on improving insect pollination have generally focused on three areas; optimizing the contribution of honeybees ( n = 4), utilizing other managed species ( n = 4) and ways to improve pollination by wild pollinators ( n = 2) (Table 1). The results showed that increasing honeybee density leads to significantly higher rates of pollination and production. Other managed pollinators assessed were, the New World Carniolan honeybee Apis mellifera carnica Pollman 1879 ( n = 2), the buff-tailed bumblebee Bombus terrestris Linnaeus 1758 ( n = 1), and the western bumblebee Bombus occidentalis Greene 1858 ( n = 1). The results suggested that buff-tailed bumblebees could be effective pollinators, especially in the Etinger variety, as buff-tailed bumblebee treatment plots showed higher rates of pollination and yield in comparison with honeybee treatment plots (Ish-Am et al., ). The western bumblebee was shown to forage in avocado orchards and the results suggest that the introduction of bumblebee hives may increase yields; however, this study did not record bee activity on the crop (McNeil & Pidduck, ). Trials on the New World Carniolan honeybee explored whether this subspecies had a higher preference for avocado pollen and higher visitation rate on avocado flowers in comparison with the Apis mellifera ligustica Spinola 1806, however, the results showed no significant difference in visitation rate between the two subspecies (Afik et al., ; Fetscher et al., ). Two studies looked at wild pollinators and methods to increase their abundance. These studies showed that intensive management practices such as spraying pesticides and the removal of forested areas and weeds lead to a reduction in pollinator diversity (Villamil et al., ) and that spraying pesticides reduces wild pollinator abundance and avocado yield (Castañeda-Vildózola et al., ).

4 DISCUSSION

Our review highlights the new knowledge obtained through research on avocado pollination since the last significant literature reviews were conducted more than 15 years previously. It has built on these reviews by including the analysis of 24 new studies and current topics such as the impacts of land management on wild pollinators. Additionally, we carried out a meta-analysis on the contribution from insect pollinators to pollination and summarized global pollinator abundance and pollination efficiency of key species, thus providing a more nuanced understanding of these issues.

4.1 Research focus and geographical spread

4.2 Contribution of insect pollinators to pollination and production

The results also showed a wide variation in the contribution of insect pollinators. The meta-analysis had high and significant heterogeneity ( I ² = 79%) and, in the mean summaries, the range for open-pollinated treatments was broad and overlapped with closed pollination treatments. A possible explanation for this variation could be that, in some circumstances, pollinators are thought to contribute little to the pollination process (Clark, ; Davenport, ; Davenport et al., ; Ying et al., ). It is hypothesized that self-pollination is possible if stigmas remain receptive in phase 2 and this is thought to be feasible with specific cultivars (Davenport et al., ) and in humid climates (Gazit & Degani, ). Additionally, in a recent study, Davenport () argues that regardless of other external factors, self-pollination makes up a major part of avocado pollination. However, this study only measures pollen tube growth in the style and wider evidence suggests that during phase 2, pollen tubes are unable to reach the ovule and thus successful fertilization is not possible (Sedgley & Grant, ). Davenport () also suggests that wind pollination is more prominent than insect pollination and shows that there is no difference in the per cent of pollinated stigmas between open and closed treatments. This contrasts with our findings and several other studies and thus indicates there are likely some varietal or management factors affecting the role of insect pollinators.

Variation in pollination services and resource availability between locations are probable explanations for the yield disparities in the open-pollinated treatments. Pollinator abundance and, or efficiency, were seldom reported in controlled pollination studies and this is likely to vary significantly due to differences in; managed beehive densities, proximity to natural areas and wild pollinators, and the availability of native avocado pollinators. Variation in resource availability is also likely to be high and this has been shown to impact fruit set. Alcaraz et al. () show that the amount of starch content in the style has a high correlation with the number of flowers that successfully develop into avocado fruits. Additionally, the scale at which pollination is assessed can also affect the level of contribution to pollination (Howlett et al., ; Webber et al., ) and, this may explain the significant variation between studies which had measured insect contribution at different scales (inflorescence, branch, tree).

Variation in resource availability might also explain why our results showed only limited differences in fruit weight between open and closed pollination treatments as agronomic factors that influence general tree health (e.g. irrigation), and resource availability are known to have a greater influence on fruit size (Kremer-Köhne & Köhne, ). However, alternatively, this result could be an indication of pollination deficits in avocado orchards. Open-pollinated treatments have a higher fruit set in comparison with closed pollination treatments and yet, fruit weight per avocado is similar across the two treatments. This suggests that sufficient resources are available as the tree is able to produce a good fruit weight regardless of the number of fruit set and thus, could indicate that yield deficits are the result of low pollination and reduced fruit set.

4.3 Abundance and efficiency of insect pollinators

Overall, managed honeybees appear to be contributing most to avocado pollination in many regions due to their general efficiency and high abundance (average overall abundance was >50%). This finding was noted in the majority of studies and has been highlighted in previous reviews (Ish-Am, ; Wysoki et al., ). However, it is well known that honeybees can be sensitive to wind, rain and low temperatures (Bushuru, ; Can-Alonzo et al., ) and often prefer other nectar sources (Ish-Am & Eisikowitch, ). Therefore, under poor weather conditions or where other flowers are in bloom at the same time, their contribution to avocado pollination could be reduced, and diverse pollinator communities including both wild and managed pollinators may provide more consistent pollination (Woodcock et al., ).

Wild pollinators were also shown to play an important role. In 11 of the 18 studies and six of the 11 countries, they were more abundant than managed honeybees and although the contribution to pollination services is unknown for many wild pollinators, there is some evidence that certain wild species are efficient avocado pollinators. Stingless bees were shown to carry a comparably high amount of pollen (around 500 grains) and qualitative comments suggest they can effectively transfer pollen as their body size suits the shape of avocado flowers (Ish-Am et al., ). Blow flies were also shown to be important pollinators as they deposited a high amount of pollen per visit, which may be attributed to the open structure of the avocado flower making it well suited to fly pollination (Vithanage, ). However, in comparison with honeybees, their flower visitation rate was low, thus reducing their potential effectiveness. The overall contribution to pollination from individual wild species is reduced due their low abundances in comparison with honeybees (e.g. the relative abundance was 28% stingless bees, 19%, for blow flies and 46% for honeybees). As such, active management to increase the abundance of certain wild pollinators may be an effective strategy to increase pollination; however, more research is required to quantify the effectiveness of wild pollinators in specific regions.

Previous studies have highlighted other potentially important pollinators. In certain locations, wasps are efficient pollinators (Ish-Am et al., ; Papademetriou, ; Perez-Balam et al., ) and a study by Ish-Am et al. () shows that managed buff-tailed bumblebees can increase pollination. These pollinator groups were not covered in this analysis due to a lack of quantitative efficiency data and thus, this should be a target for future research. In temperate regions, it is also necessary to consider the potential of nocturnal pollinators, particularly from the diptera and lepidoptera order, as lower night temperatures can result in both male and female flowers opening during the night. Pattemore et al. () showed that pollinating insects such as wood gnats, crane flies, scarab beetles, capsid bugs, forest moths and brown lacewings did visit avocado flowers during the night and were carrying avocado pollen. However, no other studies have explored this topic and therefore further investigations in this area are also needed.

4.4 Improving insect pollination

Tools to better manage pollination in avocado are required given the increasing production of avocados globally (FAO, ), the need for more sustainable production systems that make better use of inputs such as insect pollination (Garibaldi et al., ), and that pollination deficits in avocado are already in evidence (Alcaraz & Hormaza, ; Evans et al., ). This study highlighted three key themes to improve pollination: increasing honeybee density, utilising other managed pollinators, and exploring the potential from wild pollinators.

The results from three studies showed that increasing honeybee density led to an increase in visitation rate and an increase in pollination and production (Ish-Am & Eisikowitch, ; Ish-Am & Lahav, ; Peña & Carabalí, ). Similar findings were concluded in a meta-analysis by Rollin and Garibaldi () who showed that, for a range of insect-pollinated crops, production does increase with honeybee density, up to a saturation point. However, for avocado production, we still lack evidence for optimal stocking densities and spatial arrangements of hives, particularly for some of the significant global producers.

4.5 Study limitations

The low number of available studies presented a major limitation. For the meta-analysis, it was necessary to include papers testing a wide range of variables (fruit set, yield, pollination) and as such, the data were very heterogeneous. Furthermore, some of these studies provided limited information on the methods used, and often, N and SD were not provided and therefore had to be calculated from the information available. The restricted data availability also meant that statistical analysis was not feasible for the majority of the research questions and therefore, the strength and scope of the conclusions made is limited. However, despite these challenges, some general findings, research gaps and recommendations have been identified.

5 CONCLUSIONS

5.1 Key findings and research gaps

Dominican Republic and Mexico are responsible for 37% of global avocado production but only 13% of studies originated from these countries and therefore, further research in these countries is required.

In 19 out of 23 studies, insect pollinators contributed significantly to pollination, fruit set and yield.

Managed honeybees were identified as the most important pollinators due to their frequency and efficiency. However, further information is needed to optimize local field beehive placement and density.

The abundance of wild pollinators ranged from 90% to 8% across locations and further research is required to understand their efficiency and contribution to avocado pollination.

Land management practices affected the abundance and diversity of wild pollinators and this can have negative implications for yield.

5.2 Recommendations for growers

In most situations, growers will benefit from an increased density of pollinators.

Increasing honeybee hive density will likely increase production but may not be cost-effective in all contexts.

The utilization of alternative managed pollinators (e.g. stingless bees) or active management of wild pollinators may also be applicable in some circumstances.

ACKNOWLEDGEMENTS

This research was carried out as part of the BBSRC funded Waitrose Collaborative Training Partnership and the PhD was funded by the University of Reading. The authors also wish to thank Greencell and Jonathan Berry for support provided throughout the project.

CONFLICT OF INTEREST

The authors declare that they have no known competing financial interest or personal relationships that could have appeared to influence the work in this paper.

AUTHOR CONTRIBUTIONS

Dymond and Garratt conceived research. Dymond conducted systematic review, analysed data, conducted statistical analyses and wrote the manuscript. Garratt supported statistical analyses. All authors provided feedback on the manuscript, read and approved the manuscript.

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The role of insect pollinators in avocado production: A global review

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Keira Dymond , Corresponding Author Centre for Agri-Environmental Research, School of Agriculture, Policy and Development, University of Reading, Reading, UK Correspondence Keira Dymond, Centre for Agri-Environmental Research, School of Agriculture, Policy and Development, University of Reading, Reading, UK.

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No ser humano, o resultado da fecundação dá origem ao ovo. Este sofre mitoses sucessivas até originar um embrião que se vai desenvolvendo até ao nascimento. Quando adulto, as células da linhagem sexual sofrem meiose e originam os espermatozoides e os óvulos que, quando se encontram, originam novamente o ovo.

Recordando os ciclos de vida, já apresentados, das angiospérmicas ou das gimnospérmicas, serão os humanos mais ou menos complexos?

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Sexual Reproduction in Plants | Plants | Biology | FuseSchool

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As plantas são os fascinantes seres vivos que fazem parte do Reino Plantae. Uma das principais características que as destacam da maioria dos restantes seres do universo é o facto de realizarem fotossíntese, processo que lhes permite a obtenção do seu próprio alimento. Por este motivo, também são chamadas de autotróficas ou produtores primários, ocupando assim o 1º nível trófico das cadeias alimentares.

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David Attenborough's Kingdom of Plants: Introduction

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Charles Darwin foi um naturalista inglês que, durante o século XIX, ficou famoso em todo o mundo pelo desenvolvimento da Teoria da Evolução e da Seleção Natural. Embora tenha desenvolvido este trabalho em plantas e animais, temos tendência para o associar apenas aos animais, e poucas pessoas reconhecem que ele também foi um botânico proeminente. A verdade é que publicou alguns livros sobre plantas, muitos deles relacionados com a reprodução - a polinização das orquídeas e os efeitos da polinização cruzada e da autopolinização são alguns exemplos de temas abordados.

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Restricted access Articles

Abstract

Charles Darwin studied floral biology for over 40 years and wrote three major books on plant reproduction. These works have provided the conceptual foundation for understanding floral adaptations that promote cross-fertilization and the mechanisms responsible for evolutionary transitions in reproductive systems. Many of Darwin's insights, gained from careful observations and experiments on diverse angiosperm species, remain remarkably durable today and have stimulated much current research on floral function and the evolution of mating systems. Here I review Darwin's seminal contributions to reproductive biology and provide an overview of the current status of research on several of the main topics to which he devoted considerable effort, including the consequences to fitness of cross- versus self-fertilization, the evolution and function of stylar polymorphisms, the adaptive significance of heteranthery, the origins of dioecy and related gender polymorphisms, and the transition from animal pollination to wind pollination. Post-Darwinian perspectives on floral function now recognize the importance of pollen dispersal and male outcrossed siring success in shaping floral adaptation. This has helped to link work on pollination biology and mating systems, two subfields of reproductive biology that remained largely isolated during much of the twentieth century despite Darwin's efforts towards integration.

References

Darwin C.. 1887 The life and letters of Charles Darwin including an autobiographical chapter, vol. 3 (ed. & Darwin F.). London, UK: John Murray. Crossref, Google Scholar

This Issue

Discussion Meeting Issue 'Darwin and the evolution of flowers' edited by Peter R. Crane, Else Marie Friis and William G. Chaloner

Keywords

Subjects

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Darwin's legacy: the forms, function and sexual diversity of flowers

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Restricted access Articles Abstract Charles Darwin studied floral biology for over 40 years and wrote three major books on plant reproduction.

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Inspirado em Cindy Lauper.

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I personally feel a little sorry for plants. When plants want to have sex they can't just go to a bar to meet someone; they are stuck in the ground. So what's an amorous plant to do?

For most of the earth's history plants lived in water. When they wanted to have sex they just released their sperm into the ocean where it would swim around for a while before fertilizing some eggs. Pretty simple. But as the oceans got crowded some plants looked with envy at the land, where there was plenty of room to grow and plenty of sunlight for photosynthesis. So about 470 million years ago (mya) in the Ordovician period, some enterprising young plants decided to head for the hills. These plants were mosses, ferns, club-mosses and horsetails.

What most people don't know about these plants is that they still need water to have sex. For that reason they are actually the botanical equivalent of amphibians. They can live on land but they still need water for reproduction. During wet times of the year, these plants release tiny sperm into the environment that swim through the water on the forest floor to fertilize the eggs of another plant.

For about 80 million years all the plants on land still needed water to complete their life cycles. But it started to get a little crowded in the swamp. Fortunately, there was still a lot of land available where no plants grew. The only problem was, it was too dry. About 390 mya in the mid Devonian some plants looked to the skies for inspiration and noticed something interesting: wind.

A few adventurous species decided to release their sperm into the air all wrapped up in a water-tight, yet aerodynamic little package, kind of like a tiny ping pong ball. This structure is called pollen and the first plants to make pollen were the gymnosperms, better known as conifers or evergreen trees. Gymnosperms are the botanical equivalent of reptiles, which were the first animals to no longer need water for reproduction.

About 125 mya yet another group of plants evolved and they had a distinct advantage over the gymnosperms: they could reproduce a lot faster. Gymnosperm reproduction takes a long time: about 15 months for most species to produce a ripe seed. In contrast, some flowering plants can complete their life cycle in a just a couple of months. The very first flowering plants also used wind for reproduction.

Wind pollination is fine and dandy but it can be fairly wasteful; most of the pollen produced just lands on the dirt and dies. Then about 100 mya an enterprising group of insects saw an untapped market for their services; they would open a plant dating service for all those lonely trees-let's call it "Timber". In exchange for a few grains of pollen, which probably would have died anyway, the insect would move pollen from one flower to another. It was a win-win situation! Eventually, some plants started producing a sweet beverage called nectar to "pay" the insects in order to reduce pollen losses even further. Wasps and beetles were some of the very first insect pollinators.

As with most businesses, sometimes the employees don't get along. Although wasps drink nectar from plants, they also eat meat, mainly in the larval stage. Now, one group of wasps found that they preferred a strictly vegetarian diet. They decided to split from their colleagues at "Timber" and form their own dating service; let's call it "Bumble...bee".

Bees are wasps' vegan cousins and because they rely exclusively on plant nectar and pollen to survive, they are among the most faithful and effective pollinators in the world. In Manitoba over half of all pollinator visits in the prairies and parklands are performed by bees. It is because bees are such good pollinators that scientists have been so worried about declining bee populations. Although we don't always notice pollinators, they fertilize about 87.5% of the worlds' flowering plants (Ollerton et al. 2011) so the loss of our planet's pollinators would truly be a disaster.

If you think your sex life is complicated, you don't have anything on plants. Some plants have separate males and females just like people (e.g. buffalograss ( Buchloe dactyloides), salt grass ( Distichlis stricta), willows ( Salix spp.), Manitoba maples ( Acer negundo), etc.). But some of these plants, like sweet gale ( Myrica gale), can switch their sexual orientation from year to year; female one year, male the next. Most plants are hermaphrodites, producing both sperm AND eggs. Furthermore, plants can reproduce themselves without even having sex. Some plants can self-pollinate, or even skip the pollination process altogether and grow a cloned seed. The pads of prickly pear cactus ( Opuntia spp.) can detach and form completely independent plants-essentially little clones. This would be like you detaching your arm and having it grow into a clone of yourself.

Pollen is everywhere: in the water, in the sky and covering many of the animals. As pollen grains contain sperm and germinate when they land on the stigma of a flower, they are essentially tiny, little male plants. This spring, when you're walking outside and you see pollen falling around you I want you to remember that sometimes it really does rain men!

Reference

Ollerton, J., R. Winfree, and S. Tarrant. "How many flowering plants are pollinated by animals?." Oikos 120.3 (2011): 321-326.

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I personally feel a little sorry for plants. When plants want to have sex they can't just go to a bar to meet someone; they are stuck in the ground. So what's an amorous plant to do? For most of the earth's history plants lived in water.

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How bees help plants have sex - Fernanda S. Valdovinos

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As orquídeas (Orchidaceae) podem ser encontradas em quase todos os continentes nas mais variadas formas, tamanhos e cores. Será que sabemos o porquê disso? Será que tal está relacionado com a sua vida sexual? Vamos descobrir!

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Bees are great pollinators-and so important for crops such as almonds and apples that they're driven in to farms and orchards by the truckload each spring. But when it comes to cotton, butterflies play an unexpected role. A new study suggests that by cross-fertilizing cotton flowers that bees don't visit, other kinds of insects-principally hoverflies and butterflies-add about $120 million per year to the cotton harvest in Texas alone.

"This paper will drive people to look at the importance of butterflies as pollinators," says Karen Oberhauser, a butterfly biologist at the University of Wisconsin, Madison, who was not involved in the research. If the results hold up in other crops, butterflies might be added to a short list of commercially important pollinators including honey bees, bumble bees, hoverflies, and beetles.

Until now, biologists haven't rigorously examined butterfly pollination in agriculture. Butterflies aren't as abundant as bees, and they don't go out of their way to collect pollen. Unlike bees, whose hairy bodies are easily coated in the yellow dust, butterflies have long, delicate legs that seldom brush up against a flower's pollen-producing anthers. When it comes to pollination, the dainty nectar sippers "have been scoffed at," says Sarah Cusser, a landscape ecologist at the University of Vermont who conducted the new study.

Cusser studies how habitat and pollinator diversity contribute to agriculture. For her Ph.D. in landscape ecology at the University of Texas, Austin, she researched these factors in cotton. There was no shortage of field sites along the Gulf Coast. "You can stand on top of your car and see nothing but cotton," she says.

To find out how well cotton was being pollinated, Cusser counted a lot of insects. Three times over 3 years, she slowly traversed 9 hectares of cotton fields, hunched over and looking for pollinators. She often went barefoot, because the mud would have sucked off her shoes. Each time Cusser saw an insect visiting a flower, she tried to capture it with a net and stow it in a vial of ethanol.

Back in the lab, she identified the insects-2444 in all-and the kind of pollen they were carrying. She had expected to find mostly honey bees. But she also frequently encountered a native bee, the long-horned bee, and she came across hundreds of flies and butterflies. All told, she counted 40 bee species, 16 fly species, and 18 butterfly species, including the gray hairstreak ( Strymon melinus) and the little yellow ( Eurema lisa). "I was really surprised by the awesome diversity of insects."

That wasn't her only revelation. Cusser noticed that various pollinators visited the flowers at different times throughout the day. Flies would be out early, perhaps because they tend to nest in the fields. Then, butterflies would arrive; by the time it got really hot, bees were out in force. Timing matters because each cotton flower is receptive to pollen for just a few hours and withers by sunset.

Cusser also discovered that various insects tended to visit different parts of the cotton plant. Bees preferred to forage on inner flowers, closer to the main stem (though it's not known why). Flies and butterflies landed on outer flowers, possibly because they're less nimble fliers. These preferences essentially mean roughly 50% more flowers are visited, thanks to flies and butterflies, than if bees were the only pollinators, Cusser and her advisers report this month in Agriculture, Ecosystems & Environment. "It was extraordinary, the extent of it," Cusser says.

This phenomenon, which goes by the technical term pollination complementarity, isn't unique to cotton. In almond orchards, wild bees and domesticated honey bees visit different parts of the trees. Complementarity could be more common than currently realized, Cusser says. "I find the whole idea fascinating," Oberhauser says. "We just don't give butterflies enough credit for their role."

Granted, bees still do most of the work. In cotton fields, Cusser found they're responsible for about 66% of the pollination. But the work of butterflies and flies still adds up to about $120 million per year of extra cash for cotton farmers in Texas, she estimates. "We kept joking that butterflies aren't quite as useless as everyone thought they were."

Cusser hopes the findings will encourage farmers to conserve or restore habitat that benefits the overlooked pollinators. As a postdoc at the University of Vermont, she plans to study whether habitat restoration benefits cotton farmers by boosting the diversity of pollinators.

"People value butterflies because they're charismatic, and people can see them in their gardens, but now I can point to them as pollinators and know that they can have a significant effect," says Nick Haddad, a butterfly biologist at Michigan State University and co-author. "It really has changed my world."

doi:10.1126/science.abi9757

Erik is a reporter at Science, covering environmental issues.

More from News

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Butterflies provide 'extraordinary' help pollinating cotton fields

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Bees are great pollinators-and so important for crops such as almonds and apples that they're driven in to farms and orchards by the truckload each spring. But when it comes to cotton, butterflies play an unexpected role.

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The sexual deception of orchids - Anne Gaskett

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e animals don't give plants nearly enough credit. "A vegetable" is how we refer to a person who has been reduced to a condition of utter helplessness, having lost most of the essential tools for getting along in life. Yet plants get along in life just fine, thank you, and had done so for millions of years before we came along. True, they lack such abilities as locomotion, the command of tools and fire, the miracles of consciousness and language. But the next time you're tempted to celebrate human consciousness as the pinnacle of evolution, stop for a moment to consider exactly where you got that idea. Human consciousness. Not exactly an objective source.

So let us celebrate some other pinnacles of evolution, the kind that would get a lot more press if natural history were written by plants rather than animals. I'm thinking specifically of one of the largest, most diverse families of flowering plants: the 25,000 species of orchids that, over the past 80 million years, have managed to colonise six continents and almost every conceivable terrestrial habitat, from remote Mediterranean mountaintops to living rooms the world over. The secret of their success? In a word, sex. But not exactly normal sex. Really weird sex, in fact.

Hoping to observe some of this plant sex, the photographer Christian Ziegler and I recently journeyed to one of those remote Mediterranean mountains in search of one of the most ingenious and diabolical of these orchids: the Ophrys, or, as it is sometimes called, the bee orchid. (Some botanists, less politely, call it the prostitute orchid.) I'd been eager to lay eyes on this orchid and meet its hapless pollinator ever since reading about its reproductive strategy, which involves what my field guide called "sexual deception" and "pseudocopulation." What I learned forced me to revise radically my estimation of what a clever plant is capable of doing to a credulous animal.

In the case of this particular Ophrys, that animal is a relative of the bumblebee. The orchid offers the bee no nectar reward or pollen meal; rather, it seduces the male bee with the promise of bee sex, then ensures its pollination by frustrating the desire it has excited. The orchid accomplishes its sexual deception by mimicking the appearance, scent, and even tactile experience of a female bee. The flower, in other words, traffics in something very much like metaphor: this stands for that. Not bad for a vegetable.

Orchid hunting sounds arduous, and in many places it is, but in the mountains of Sardinia Ophrys orchids grow like roadside weeds. Though they're only 8ins or so high, when they bloom in April you can spot them from a moving car. Even close up, the lower lip, or labellum, of these diminutive orchids bears an uncanny resemblance to a female bee as viewed from behind. This pseudobee, which in some Ophrys species comes complete with fake fur and what appear to be folded iridescent wings, looks as though she has her head buried in a green flower formed by the actual flower's sepals. To reinforce the deception, the orchid gives off a scent that, though imperceptible to us, has been shown to closely match the pheromones of the female bee.

It works like this. The male bee alights on the bee-like labellum and attempts to mate, or, in the words of one botanical reference, begins "performing movements which look like an abnormally vigorous and prolonged attempt at copulation". In the midst of these fruitless exertions, the bee jostles the orchid's column (a structure unique to orchids that houses both male and female sexual organs) and two yellow sacs packed with pollen (called the pollinia, another structure unique to orchids) are stuck to his back with a quick-drying glue-like substance. Frustration mounts until eventually it dawns on the bee that he has been had. He abruptly flies off, pollinia firmly attached, in frantic search of more authentic female companionship.

There was something poignant about the solitary bee I spotted, flying around madly with what looked like a chubby pair of yellow oxygen tanks strapped to his back. He'd been deluded by the promise of sex - bee sex - when in fact all that was really on offer was plant sex. Botanists have been known to refer to pollen-carrying bees as "flying penises," but of course most of the world's bees perform that role unwittingly, with food rather than sex on the brain. Not so for the poor, deluded orchid bee.

In fact, the sexual frustration of the bee turns out to be an essential part of the orchid's reproductive strategy, which is to favour mixing one's genes with distant mates. (Preferable, since inbreeding decreases fitness.) When a bee has been discombobulated by sexual frustration, it's much less likely to mate with a flower on the same or nearby plant. Determined not to make the same mistake again, the bee travels some distance and, if things work out for the orchid, ends up pseudocopulating (and leaving his package of pollen) with another orchid. That distant orchid is likely to look and smell ever so slightly different from the first, and some botanists believe these subtle variations from plant to plant are part of the orchid's strategy to prevent bees from learning not to fall for the same flower twice. Think of it: the very imperfection of the orchid's mimicry may itself be part of the perfection of its reproductive strategy.

The pollination strategy of the Ophrys is, like that of so many orchids, ingenious, intricate, wily, and seemingly improbable - so much so that proponents of intelligent design sometimes point to orchids as proof that the hand of higher intelligence must be at work in nature. Though some orchids offer conventional food rewards to the insects and birds that carry their pollen from plant to plant, roughly a third of orchid species figured out long ago - unconsciously, of course -that they can save on the expense of nectar and increase the odds of outcrossing by evolving instead a clever deceit, whether that ruse be visual, aromatic, tactile, or, in the case of the bee orchid, all three at once.

The deception and exploitation of animals has become something of an orchid family speciality. There are orchids in the genus Orchis that lure pollinators with the promise of food by mimicking the appearance of nectar-producing flowers, or, in the case of fly-pollinated Dracula orchids, by producing an array of nasty scents running the scales of putrefaction, from fungus and rotten meat to cat urine. (Believe me, I've sniffed them.) Other orchids, such as the Serapias, promise shelter by deploying floral forms that mimic protective insect burrows or brood rooms. Some of the Oncidiums mimic the appearance of male Centris bees in flight, hoping to incite territorial combat resulting in pollination. And then there are many orchids that hold out the promise of romance.

In one way or another, orchids have evolved reproductive strategies that play on an animal's three most urgent needs: for food, for shelter, for sex. Has the plant world produced any more brilliant students of animals' desire? I doubt it. Orchids are nature's meta-flowers, improvising on what has come before. For orchid deception can only succeed in a world where most things in nature really are what they seem: where flowers really do offer nectar and where they don't dress up as insects.

The orchids' baroque pollination strategies raise challenging questions for the evolutionist, however. Since natural selection seldom rewards unnecessary complication, why haven't orchids stuck with more straightforward pollination strategies based on nectar reward? And how in the world did their sexual practices become so elaborate? As for the hoodwinked pollinators, what, if anything, do they gain from their relationship with these flowers? If the answer is "nothing but frustration", then why wouldn't natural selection eventually weed out insects so foolhardy as to spend their time mating with nature's version of the inflatable love doll? Many of these deceptions are so specific they fool only a single pollinator and, as for the Ophrys, they don't work all that often. So what possible advantages could there be in depending so absolutely on a single pollinator, and one you can't even count on fooling all the time?

Botanists and evolutionary biologists have come up with fascinating answers to all these questions: indeed, the peculiarities of orchid sex offer one of the great case studies of natural selection, as Darwin himself understood. Darwin was fascinated by orchid pollination strategies, and, though he was puzzled by the purpose of Ophrys orchids' uncanny resemblance to bees (pseudocopulation wasn't observed until 1916), he taught us much of what we know about these plants in The Various Contrivances by Which Orchids Are Fertilised by Insects, the volume he published immediately after The Origin of Species. Indeed, some scientists believe that had he published his orchid book first, the theory of natural selection might have encountered considerably less scepticism than it did. Why? Because Darwin painstakingly demonstrated how even the most improbable features of these flowers serve a reproductive function. Many of their structures are so perfectly adapted, both to the plants' requirements and the morphology of their pollinators, that they offered Darwin elegant proofs of his outlandish theory.

More recently, biologists have developed theories to explain why some orchids have evolved away from a simple nectar reward for their pollinators. John Alcock, an evolutionary biologist and author of An Enthusiasm for Orchids, proposes two intriguing explanations. When botanists experimented by adding a nectar reward to a normally nectarless orchid, they found that the pollinators hung around longer, happily visiting other blooms on the same and nearby plants. This does not suit the orchid's interests, however, since inbreeding results in lower-quality seeds. As with the bee orchid, pollinator frustration works to the advantage of the plant, since the insect is apt to leave quickly and travel further. Other studies suggest that a thwarted pollinator will thrust himself more deeply into a flower and thrash about in search of promised food, improving the odds that he'll crash into the pollinia and then leave in a huff.

There may also be benefits to developing a relationship with a single, highly devoted pollinator. Nectar, beloved by so many different animals, attracts all sorts of riffraff that may not deliver your pollen to the right target. But if instead you produce a scent that attracts only the males of one species of bee, then you can ensure that your pollen will end up precisely where you want it: on the stigma of a far-flung orchid of your own kind.

The exactitude of the perfume business may also help explain the astounding biodiversity of the orchid family. A mutation producing even a slight change in an orchid's scent could, strictly by chance, turn out to be the key that unlocks the sexual attentions of a new pollinator, while at the same time completely turning off the original pollinator. This can function much as geographic isolation does in the creation of new species: by preventing new mutant flowers from being pollinated by older ones. The novel orchid can evolve in genetic isolation from its forebears - a prerequisite for creating a new species.

Orchids excel at spinning off new species. In fact, one of the curiosities of the orchid family is the fact that there are so very many species and yet relatively few orchid plants - remarkably little biomass, compared with other important plant families. Yet the orchids' small numbers ensure their survival. If deceptive orchids were more common, their ruses would no longer work, since they depend on the ubiquity of honest flowers.

There is one more characteristic of orchids that helps explain their extraordinary diversity of form as well as the ingenuity of their pollination strategies. Flowers, in general, come in two types: the radial symmetry of the daisy or sunflower, or the bilateral symmetry of the lily or orchid. The second way of structuring a flower is more complex and therefore offers many more possibilities for variation. It also opens up the possibility of mimicking the morphology of your pollinator, since the symmetry of all the higher animals is also bilateral.

To learn all this about orchids is to admire them more but perhaps love them less. And to wonder if we too haven't fallen prey to their deceptive charms. The very name of the orchid comes from the Greek word for testicle, referring not to the plant's flowers but its bulbs, organs that have long been endowed with aphrodisiac properties. But it doesn't take a Freudian to discern a strong sexual subtext in the passion for these flowers, especially among men, who, as any visit to an orchid show will tell you, suffer disproportionately from "orchidelirium" - the Victorians' term for the madness these flowers inspire.

Is it possible that humans can look at an orchid and, like the deluded orchid bees, see an apparition of female anatomy? (Georgia O'Keeffe certainly did.) Could it be that plant sex and animal sex have got their wires crossed in human brains, just as they have in insect brains? Ever since the first human-hybridised orchid bloomed (the earliest in the Western world was recorded in 1856), we humans have become important orchid pollinators, lured into advancing the orchid's interests, assisting it in its quest for world domination. Today, there are some 100,000 registered hybrid orchids, most of them literally inconceivable without us.

Not that any of this was ever in the orchid's plan. In evolution there is no plan, of course, only blind chance. But what are the chances that a flower deemed sexy by a handful of witless insects would also be so deemed by us? Let's face it: we're all orchid dupes now.
This is an edited extract from Michael Pollan's introduction to Deceptive Beauties by Christian Ziegler (University of Chicago Press)

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e animals don't give plants nearly enough credit. "A vegetable" is how we refer to a person who has been reduced to a condition of utter helplessness, having lost most of the essential tools for getting along in life. Yet plants get along in life just fine, thank you, and had done so for millions of years before we came along.

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Chiloglottis valida

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Caladenia excelsa

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Caladenia discoidea

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Paracaleana nigrita

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Caladenia atrovespa

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O termo Orchis, que significa testículos, foi usado pela
primeira vez por Theophrastus, um filósofo grego. Este discípulo de
Artistóteles comparou as raízes de algumas orquídeas mediterrâneas com os testículos humanos e, por isso, desde a Idade Média que propriedades afrodisíacas
são atribuídas a estas plantas.

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As flores são idealizadas para atrair animais devido às suas características morfológicas, ao néctar, aos estigmas e aos tecidos dos estiletes - ricos em água, nutrientes e energia.

O néctar é composto por açúcares primários simples, um meio rico para o crescimento de micróbios.

Alguns patógenos invadem as plantas através do néctar e órgãos sexuais da flor, enquanto o (E)-β-cariofileno promove a resistência da planta.

As características florais permitem que os polinizadores associem o aroma da flor ao respetivo néctar.
Identificamos: cor, odor, forma, design da inflorescência e tipo e qualidade de recompensas florais.

Estes evoluíram como recompensa aos polinizadores pela disseminação adequada de pólen.

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Mal entrou na puberdade e ela só quer, só pensa, em namorar. Uns argumentam que ainda é jovem, um botão em flor, mas isso nunca foi um grande problema para ela, que vem se preparando para desabrochar desde que era um brotinho. Apesar de ter criado raízes junto aos pais, sente que é hora de formar sua própria família e gerar seus rebentos. Para conceber as sementes dessa transformação silenciosa, a moça se insinua aos 4 ventos, ludibria os varões e cria sugestivas armadilhas. Se preciso, ela se vestirá de forma sensual e se cobrirá com perfumes, tudo para deixar sua herança na terra - e, com sorte, gerar bons frutos para as próximas gerações.

Sob a ótica de uma flor, um jardim é uma grande orgia. Cactos e ipês fazem. Trepadeiras, claro, fazem. A mais prosaica violeta e a rosa caríssima fazem. De fato, assim que provaram o gostinho da coisa pela primeira vez, cerca de 145 milhões de anos atrás, 415 milhões de anos depois de a primeira alga verde chegar à terra firme, as plantas logo perceberam que o sexo poderia trazer benefícios interessantes. Vamos a eles.
Por que é que as plantas (e você) precisam de sexo
À primeira vista, o sexo parece pouco importante para as plantas. Isso porque a maior parte delas é hermafrodita: um mesmo indivíduo tem tanto um ovário, sua porção feminina, quanto grãos de pólen, pequenas estruturas que encerram os gametas masculinos. A reprodução sexuada, que leva o pólen até o ovário, não deveria, portanto, demandar grandes esforços. Mas não é isso que acontece na realidade. Uma flor só se entrega ao solitário prazer da autofecundação quando sua sobrevivência está sob ameaça, como vamos ver mais adiante.

É que um vegetal auto-fecundado cria descendentes geneticamente idênticos à mãe. Mal negócio. A reprodução sexuada junta e embaralha genes de dois indivíduos. O filho nasce com um código genético só dele (é precisamente o seu caso, leitor ou leitora - você é só um embaralhamento aleatório dos genes dos seus pais). A vantagem aí é que códigos genéticos novos produzem anticorpos inéditos na natureza.

É uma bela vantagem do ponto de vista da espécie. Se um vírus mortal infectar todos os indivíduos de uma espécie, alguns vão sobreviver, já que provavelmente terão nascido com anticorpos que, por sorte, conseguem defende-los do ataque. Se todos tivessem os mesmos genes, um único ataque viral poderia exterminar a espécie inteira. É por isso que você faz sexo. Não houvesse essa pressão evolutiva, não existiriam pênis, vagina, tesão, orgasmo. Nada.

Mas voltemos a falar de flores. Como não podem sair do lugar, as flores recorrem a aves, insetos e pequenos mamíferos - seus polinizadores - para misturar seu material genético ao de outras. Essa sacada garantiu às plantas floríferas uma diversidade enorme, se comparadas aos vegetais sem flor, como musgos, pinheiros e samambaias.

Se a planta sente que pode morrer, ela faz sexo consigo mesma, e produz um clone. Se o clima estiver bom, ela busca parceiros.

Ainda assim, isso não quer dizer que uma flor jamais vai se autofecundar. Há casos em que isso se torna necessário. Em condições normais, a violeta-africana produz flores no alto de hastes longas, boas para atrair a atenção de insetos e reproduzir-se embaralhando seus genes com os de outra flor, distante. Mas, se notar que as condições estão ruins - o clima ficou frio ou quente demais, por exemplo -, a mesma violeta pode gerar flores de haste curta, que ficam escondidas pelas folhas e se autofecundam ainda em botão.

Nesse caso, o alerta que vai determinar qual tipo de sexo elas vão praticaré dado por estruturas celulares especializadas, que registram alterações na intensidade da luz solar ou na quantidade de horas de escuro."Uma planta é capaz de perceber mudanças mínimas na oferta de nutrientes ou mesmo detectar que os dias estão ficando maiscurtos e, portanto, o inverno está chegando", diz o biólogo Thales Kronenberger, especialista em biologia molecular e parasitologia.
Dissimulação
As orquídeas são peritas em dissimulação. A Cymbidium serratum, nativa da China, tem cor e sabor absolutamente inexpressivos - a menos que você seja um camundongo da espécie Rattus fulvescens, que a acha deliciosa e se alimenta das pétalas da flor. Em troca, ele arrasta seus grãos de pólen de um lado para o outro. O que parece um ato kamikaze de amor é, na verdade, uma sofisticada estratégia de reprodução, que garante à flor trocar material genético com uma planta situada a quilômetros de distância.

Para a alegria de botânicos e jardineiros, há estratégias sexuais muito menos sacrificantes para a planta - ainda que frustrem o polinizador na maior parte das vezes. O gênero Bulbophyllum, por exemplo, oferece às moscas-varejeiras um banquete delicioso em troca de favores sexuais. Pelo menos à primeira vista. Suas flores têm um aspecto bizarro e cheiram a carniça, iludindo as moscas de que encontrarão ali matéria orgânica em decomposição. Atraídos pelo cheiro, os insetos pousam na flor só para notar que sofreram um embuste. Enquanto passeiam pelas pétalas da orquídea, eles acabam esbarrando nos grãos de pólen, que se aderem às suas patas - e estarão prontos para ganhar os céus em busca de outro Bulbophyllum.

As orquídeas do gênero Coryanthes (acima) vão ainda mais longe. Uma de suas pétalas foi modificada para ficar lisa e côncava como um copo de vidro e fazer as abelhas que pousam nela escorregar. Além disso, a flor tem glândulas que secretam água e óleos para dentro do copo, formando uma piscina na qual os insetos acabam caindo. Com as asas encharcadas e sem poder escalar a flor internamente, as abelhas são obrigadas a fugir da morte pela única parte secae acessível da planta - exatamente o canal que leva aos grãos de pólen.

Algumas plantas são monogâmicas: evoluíram para atrair apenas um ou dois polinizadores específicos. A orquídea-mariposa, por exemplo, produz um estreito tubinho com néctar ao fundo, só alcançado pela língua de algumas espécies de mariposas. Aqui:

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Outras flores se fazem de difícil, têm um alvo muito bem determinado - mesmo um inseto de comportamento semelhante ao do polinizador ideal não poderia se passar por tal. É o caso de uma orquídea australiana que atrai apenas um tipo específico de vespa - primeiro porque ela se parece com a fêmea da vespa e segundo porque ela libera o exato feromônio de reprodução do inseto.

O truque evolutivo que garante a reprodução das orquídeas Coryanthes.

1) As pétalas são oleosas. Quando uma abelha (em azul no desenho aqui em cima) pousa ali, acaba escorregando para dentro da flor, onde geralmente há água que restou da última chuva.

2) Uma vez presa na piscina, a abelha se desespera e tenta escalar as paredes de volta. Mas o óleo não deixa, e ela segue escorregando.

3) Única rota de fuga possível é um canal estreito na borda. A abelha quebra a antera, a capa de proteção do pólen, e fica com alguns grudados em seu corpo.

4) Quando o mesmo inseto pousa numa segunda orquídea, leva involuntariamente os grãos de pólen. Então ele escorrega de novo e repete os passos 2 e 3 all over again. O pólen, então, acaba grudado justamente no canal que leva ao ovário. Pronto. Para todos os efeitos, a orquídea se reproduziu usando a abelha como pênis.
Necrofilia
Mas a maior estratégia sexual do mundo das flores não é a de uma orquídea: é a da Amorphophallus titanum - a planta-cadáver (da imagem ali embaixo).Nenhuma planta é tão criativa como ela. Oriunda da ilha de Sumatra, ela coleciona superlativos: tem a maior flor do mundo, com 3 m de altura por 1,20 m de diâmetro, tem um tubérculo subterrâneo da grossura da perna de um humano adulto, pesando mais de 77 kg, e consegue emitir quase tanto calor quanto um ser humano. Seu feito mais peculiar, no entanto, está em suas estratégias de reprodução. Depois de 5 anos na seca, sem se reproduzir, a planta-cadáver produz uma gigantesca e solitária flor, que emana um cheiro de peixe podre - daí o apelido.

As moléculas que criam o odor são aquecidas por uma estrutura especializada, o espádice, e atingem um raio de 800 m de distância. Tamanho fedor atrai hordas de moscas, besouros, baratas e abelhas que penetram pelas dobras da planta, ainda fechada, e ficam zanzando no meio de suas estruturas reprodutoras. À noite, a inflorescência se abre, mas dura apenas dois dias (para alívio dos povos indonésios), revelando em sua curta vida uma das maiores sacadas reprodutivas dos vegetais: ela amadurece em tempos diferentes as duas partes de seu aparelho reprodutivo.

Nas primeiras 24 horas, apenas a porção feminina da planta está ativa, recebendo dos insetos o pólen trazido de outra planta-cadáver. A porção masculina só é ativada no segundo dia, quando os insetos começam a debandar, carregando consigo os gametas masculinos que serão levados para outro espécime. O gasto de energia é tão grande que a Amorphophallus titanum precisa de outros 3 anos na seca para armazenar energia suficiente para florir mais uma vez.
Pra que tanto stress?
Todas essas estratégias de polinização levantam uma dúvida. Não seria muito mais fácil a planta simplesmente liberar seus grãos de pólen no ambiente? Deixá-los livres para vento, água ou qualquer animal fazer a polinização? A resposta é não. "Se a planta deixar seu pólen em um lugar de fácil acesso, qualquer coisa que esbarre nela levaria embora a única chance que a flor tem de se reproduzir", diz a botânica da USP Ludmila Pansarin.

Para que apenas o polinizador certo encontre os grãos de pólen protegidos pelas pétalas é que a planta cria tantas modificações de cor, cheiro, forma e textura. "Isso garante que somente um animal com tamanho e comportamento adequados será capaz de levá-los até outra flor", diz Ludmila. Se o polinizador for uma mariposa ou morcego, por exemplo, a melhor estratégia é florir à noite e oferecer um cheiro doce e persistente.

E eis aqui a informação mais corta-clima desta reportagem: flores vermelhas são dessa cor exclusivamente para atrair pássaros e borboletas, que enxergam melhor esses tons de cores, enquanto as azuis e amarelas focam as abelhas, que vêm apenas espectros ultravioletas. Nenhuma flor foi feita para a nossa apreciação. A natureza já foi mais romântica.

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Mal entrou na puberdade e ela só quer, só pensa, em namorar. Uns argumentam que ainda é jovem, um botão em flor, mas isso nunca foi um grande problema para ela, que vem se preparando para desabrochar desde que era um brotinho.

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Rare Ghost Orchid Has Multiple Pollinators | Short Film Showcase

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Também conhecida com Pepino de São Gregório  (em inglês "Squirting Cucumber"), quando madura, explode e expele todas as suas sementes envolvidas por um líquido mucilaginoso. As sementes conseguem atingir até 6.1 metros de distância da planta!

Ecballium elaterium

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"Plant Love: The Scandalous Truth About the Sex Life of Plants"

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"Plant Love: The Scandalous Truth About the Sex Life of Plants"

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Neste livro de Michael Allaby   podemos ficar a conhecer as técnicas sexuais que mais de 200 plantas utilizam, a forma como dependem dos polinizadores e também como as orquídeas enganam os insetos. Segundo o autor, até os jardineiros podem ficar surpreendidos.

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Esta espécie utiliza, tal como outras, insetos polinizadores para se reproduzir. Mas, estando inserida na categoria de "Plantas Kinky", não fica por aqui! Ela "venda" os insetos (principalmente abelhas) no seu interior fazendo com que estes fiquem confusos e andem às voltas, acabando por ficar cobertos com o seu pólen antes de conseguirem escapar para a planta feminina. Aí, após a fertilização, a abelha morre.

Arisaema triphyllum

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Este podcast dedica-se à divulgação de conhecimentos acerca das plantas, desde as mais pequenas lentilhas até à maior sequoia, e pretende ainda transmitir o amor pelas plantas e a ideia de que é preciso prestar-lhes mais atenção.

Sugerimos os episódios:
- 268, "How Small Flies Made a lot of Orchids";
- 309, "Plants, Pollinators, Nature and Society";
- 311, "How Oaks Get Around"

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This episode is all about the fascinating world of oak seed dispersal. Many of us have undoubtedly enjoyed watching frenzied squirrels and jays hurriedly collecting and stashing acorns. But such observations are only the tip of the extremely complex iceberg of oak seed dispersal.

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Alec Bristow faz um relato das suas descobertas no que diz respeito à vida sexual das plantas.

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Os indivíduos masculinos deste género de plantas (aquáticas) elevam o nível de romance ao produzirem um "colar de pérolas" feito de pólen envolvido numa mucilagem. Este colar é levado até aos indivíduos femininos pela corrente, fertilizando assim as suas flores.

Zostera marina

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"Mal" é uma publicação trimestral erótica e o tema desta edição, "Plant sex" é uma oportunidade inesperada de sabermos mais sobre as plantas. Neste jornal, elas são apresentadas como um modelo para uma sexualidade verdadeiramente aberta e fluída, uma vez que podem ser consideradas poliamorosas. Segundo Emanuele Coccia, as plantas são inspiradoras porque “não vivem apenas no mundo; elas transformam-no constantemente”.

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If you don't know about the wonderful world of rude plants, you're in for a ride. Not only do plants have rude names ( Rubus cockburnianus and Clitoria ternatea , to name a couple) and look like rude things (click to see 5 rude looking plants!), there are also plants that do rude things...

I'm talking about reproduction! Just as humans and other animals reproduce, plants reproduce too. So without further ado, here are five fantastically rude sex quirks of plants.

Pearl necklace

Male Eelgrass produces pollen in a slimy band that floats away and snags around female flowers in order to fertilise them. Eelgrass plant beds are completely submerged, and they rely completely on water for pollination.

Shoot your load

The Squirting Cucumber does just that - squirt! When ripe, it actually explodes, shooting its seeds in a stream of mucilaginous liquid up to 20ft away from the plant.

Blindfolded sex

Jack in the Pulpit uses insects to reproduce - and it blindfolds in the process! Bees fly inside the flower of the plant and get disoriented because it's so dark. As they're whizzing about, they get covered in pollen before escaping through a hole and flying to a female flower, which then becomes fertilised. Unfortunately, there's no way of escaping the female flower, so the bee sadly dies.

Gender fluidity

The incredible Dungowan Bush Tomato plant is the first plant to be classed as gender fluid! Having confused scientists since the 70s, DNA has since confirmed that each of its bright purple flowers have both male and female parts, and has no stable sexual expression.

Solo performer

The Blue Violet flowers in both the spring and the autumn. However, during the second flowering in the year, the buds don't open - they remain in the soil, and the male and female parts fertilise themselves. This is a clever back-up plan in case the first flowers do not get pollinated.
Do you know any other plant sex quirks? Leave a comment below!

Michael has been involved with gardening and plants since he was just five years old. He is a self-professed Plant Geek, and was listed in the Sunday Times top 20 most influential people in the gardening world, thanks to his plant hunter role at Thompson & Morgan.

Michael was responsible for new plant introductions such as the Egg and Chips plant and the FuchsiaBerry and keeps busy travelling the world in search of new plants as well as lecturing worldwide, including stints in Japan. He is very active on social media - so why not give him a follow at @mr_plantgeek or Facebook. You can also listen to The Plant Based Podcast with Michael and co-host Ellen-Mary on iTunes, Spotify and Google.

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5 Plant Sex Quirks | Rude Botany! | Mr Plant Geek

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If you don't know about the wonderful world of rude plants, you're in for a ride. Not only do plants have rude names ( Rubus cockburnianus and Clitoria ternatea , to name a couple) and look like rude things (click to see 5 rude looking plants!), there are also plants that do rude things...

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Orchids: The Masters Of Lying, Cheating & Stealing

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O "mistério abominável" das angiospérmicas

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O "mistério abominável" das angiospérmicas

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"O rápido desenvolvimento, tanto quanto podemos julgar de todas as plantas superiores nos tempos geológicos recentes, é um mistério abominável." - disse Darwin em relação às angiospérmicas.
Esta frase remete-nos para o facto de estas plantas terem aparecido repentinamente na Terra no período Cretáceo sem que nada mais antigo se pareça com elas. Se comparadas com outros grandes grupos como os mamíferos, não há registo de uma evolução gradual, questão que surpreendeu Darwin e que continua a ser objeto de estudo para outros investigadores até hoje.

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The sex lives of plants can seem truly bizarre.

"There are some crazy techniques that plants have evolved with over thousands of years" to help them with their sex life, said Jennifer Blake-Mahmud, a doctoral student at Rutgers University who has studied tree sex.

Here are a few examples:

The violet

New Jersey's state flower produces flowers in spring like other species to attract insects that will spread pollen to other violets.

"They're charming," Blake-Mahmud said. But in the fall the violet has a second act to its sex life that is largely hidden from humans. It flowers again, but the buds don't open - they remain in the dirt, and the male and female parts fertilize themselves.

"They have the best of both worlds," Blake-Mahmud said. "The fall blooming is a bet-hedging strategy. This second wave of buds doesn't take as much energy to produce since they are not attracting insects, so they are not as pretty, and there's no need to make nectar or have an attractive smell."

Skunk cabbage

It grows in wet areas of New Jersey forests and is one of the first plants to bloom, well before taller trees leaf out and create shade.

To succeed in such an inhospitable climate, the skunk cabbage has the ability to engage in thermogenesis - it can increase its own heat, to melt the snow around it.

It also produces a fetid odor, which people often compare to the smell of rotting flesh, that attracts the few bees and other insects that have ventured out so early in the season.

Eel grass

This grows in the bays and along the Jersey Shore and relies on the water to spread its pollen.

"But to ensure it doesn't get washed out to sea, the pollen is threaded in a slimy band that looks like a necklace and gets snagged around the female flowers," said Lena Struwe, director of the Chrysler Herbarium at Rutgers.

Bulb plants

These plants grow a sugary appendage on seeds that serves as a food supply for ants. The ants will pick it up and try to bring the food with them, in the process spreading seeds of the bulb plant, said Bruce Crawford, director of Rutgers Gardens in central New Jersey.
More: It's getting hot in here: Ervolino: I think that I shall never see myself on a ladder trimming a tree Some weirdly wild tree sex is about to go down in your backyard Climate change causing trees to bloom weeks earlier, researchers say
Jack-in-the-pulpit

This woodland perennial has a flap on top, which makes the inside of the flower darker.

"Small bees will go inside and get disoriented because it's so dark, and as they're flying around they'll get pollen all over themselves," Crawford said.

But a hole at the base of the flower provides them an escape route, so they can fly off to a female flower, stumble around in that, and brush the pollen onto the pistil. Alas, there is no hole at the bottom of the female flower, so the insect, after helping pollinate the plant, dies inside.

"It's actually gruesome," Crawford said.

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Plants have adapted strange techniques to help with sex

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The sex lives of plants can seem truly bizarre. "There are some crazy techniques that plants have evolved with over thousands of years" to help them with their sex life, said Jennifer Blake-Mahmud, a doctoral student at Rutgers University who has studied tree sex.

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No caso dos sapos, e ao contrário do que acontece com os mamíferos, a fertilização é externa. Durante o acasalamento, a fêmea liberta os ovos (na água ou nas plantas, consoante a espécie) para que o macho os fertilize. Estes irão eclodir cerca de 1 semana depois em forma de girinos, uma pequena criatura semelhante a um peixe. A metamorfose continua por mais algum tempo, até que às 16 semanas o animal se torna um sapo adulto.

E agora? Será a reprodução das plantas mais complexa que a dos sapos?

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Como se reproduzem?

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The Plants & The Bees: Plant Reproduction - CrashCourse Biology #38

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O gametófito masculino, também referido como grão de pólen, desenvolve-se nas anteras e encontra-se compreendido entre duas células espermáticas dentro de uma célula vegetativa. Já o gametófito feminino, referido também como o saco embrionário, desenvolve-se dentro do óvulo que, por sua vez, está dentro do ovário do carpelo. A reprodução inicia-se quando o gametófito masculino é transferido da antera para o estigma, forma um tubo de pólen que cresce através dos tecidos internos do carpelo e deposita as duas células espermáticas no gametófito feminino; umas dessas células fertiliza o ovo e a outra funde-se com a célula central. Depois, segue-se a fertilização que dá origem ao embrião, inicia-se a geração esporófita, e a célula central origina o endosperma cuja função é fornecer nutrientes ao embrião que se está a desenvolver.
https://doi.org/10.1146/annurev.genet.36.040102.131941

Para compreenderes melhor, espreita a imagem seguinte!

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Alexandra Bastos
Tenho 22 anos e vivo em Oliveira de Azeméis desde pequena. Tirei licenciatura em Biologia na Universidade de Aveiro. Frequento agora o Mestrado em Biologia Aplicada.

Bruna Silva
Tenho 22 anos, sou natural de Ovar. Sou licenciada em Biologia e Geologia pela Universidade de Aveiro, e neste momento encontro-me a frequentar o Mestrado em Biologia Aplicada, também na UA.

Rafaela Beleza
Sou natural de Águeda, tenho 22 anos e sempre fui fascinada pela ciência. Sou licenciada em Biologia e Geologia pela Universidade de Aveiro e atualmente frequento na mesma instituição o Mestrado em Microbiologia.

Sara Reis
Tenho 22 anos e sou natural de Setúbal. Licenciei-me em Biologia e Geologia, pela Universidade de Aveiro, e atualmente encontro-me a frequentar o Mestrado em Ecotoxicologia, pela mesma instituição.

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A reprodução assexuada é uma estratégia reprodutiva que não requer pólen, não envolve os gastos de energia usados para a produção de gâmetas e em que não existe fertilização. Por causa disto, a planta filha é por norma geneticamente idêntica à planta mãe. Existem dois grandes tipos de reprodução assexuada:

1. Propagação vegetativa

2. Apomixia

https://courses.lumenlearning.com/boundless-biology/chapter/asexual-reproduction/

As angiospérmicas utilizam ambas as estratégias, mas principalmente a apomixia. Este tipo de reprodução consiste na produção de sementes a partir do óvulo não fecundado e as espécies poliploides das famílias Gramineae, Rosaceae e Asteraceae são alguns exemplos de plantas que possuem esta estratégia reprodutiva.
https://link.springer.com/chapter/10.1007/978-94-011-1524-7_16

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As gimnospérmicas utilizam como estratégia de reprodução assexuada a propagação vegetativa. Este tipo de reprodução acontece a partir de partes de uma planta mãe, como folhas, caules ou raízes. Uma das grandes vantagens da propagação vegetativa é o facto de as plantas não terem que passar pela fase imatura inicial pós germinação, atingindo um estado adulto mais rapidamente.
https://www.sciencelearn.org.nz/resources/1662-vegetative-plant-propagation

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No polipódio (feto), a planta adulta constitui o esporófito. Em certas alturas do ano, as folhas do feto possuem umas pontuações granulosas, os esporângios, que contêm as células-mãe dos esporos. Estas, por meiose, originam esporos haploides que, ao caírem na terra, germinam e originam o gametófito (vida livre). Nesta estrutura diferenciam-se os gametângios que originam, por sua vez, anterozoides e oosferas. A fecundação (dependente de água) origina um ovo que inicia a geração esporófita e a partir do qual surge a planta adulta. E assim ocorre a reprodução sexuada.

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Na maioria das espécies, a mudança de sexo ocorre apenas uma única vez, tanto de fêmea para macho – protoginia – como de macho para fêmea – protandria. Podem ainda ser hermafroditas, como no caso do Hibisco.

A mudança de sexo é uma estratégia sexual que maximiza o sucesso reprodutivo.
https://doi.org/10.1111/jeb.12333

Hibiscus sp.

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As hormonas vegetais – Fito-hormonas – atuam diretamente no desenvolvimento da planta e estão envolvidas em processos como reprodução, floração, frutificação, entre outros.

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Plants have complex sex lives, just like humans. And just like us, their sex lives involve a lot of communication and testing for mutual compatibility. Since today is Fascination of Plants Day, we take a look at the raunchy world of plant sex.

The mechanics of plant sex

Besides being pretty, flowers contain the plant's reproductive organs: the male gametes are produced in the stamens, and female gametes are found in the carpel, topped by a style. To produce pollen, a 'mother cell' goes through a round of meiosis, followed by a round of mitosis. That means that each pollen cell contains two sperm cells and a vegetative cell.

As for the females, seven cells are found in the ovule: an egg cell, two synergid cells involved in signalling, a large central cell that nourishes the developing embryo, and three antipodal cells that eventually disintegrate.

The magic happens once the pollen grain lands on the style. That's also when cell-cell communication starts.

LURE-ing them in

The sperm cells are carried to the ovule through the pollen tube. The pollen tube develops from the vegetative cell; guidance of the pollen tube to the ovule relies on the secretion of protein signals.

A group of cysteine-rich peptides, called LUREs, are the most well-known signalling proteins, known to attract compatible pollen tubes. With the help of these (and other) signals, the pollen tube eventually penetrates the ovule, with one sperm cell fertilizing the egg cell, and the second fertilizing the central cell.

While the mechanics of plant sex have been known for a long time, the proteins involved in male-female communication have remained a mystery until quite recently. Two recent studies, published in the Journal of Proteome Research and Genome Biology, have undressed flowering plant ovules and pollen tubes, respectively, to take a peek at the courting process in flowering plants.

Ovules before brovules

To study the proteins secreted by the ovule, a team of researchers from Université de Montréal played matchmaker with a few potato plants, then dissected the carpels to get to the ovules. The ovules also secrete a sugar-filled fluid that creates an optimal microenvironment for pollen tube growth, but the proteins found in this fluid had never been characterized.

They found 305 unique proteins in the ovary secretome, the bulk of which are involved in metabolic, cell growth, and stimulus response processes.

A comparative proteomic analysis found that 128 of these proteins are involved in pollen-ovule interactions. The majority of these are also not found at the mRNA level.

Almost one-third of the ovule-secreted proteins don't contain the traditional signal peptides, showing the importance of the unconventional protein secretion pathway in plant reproduction. Liu et al. suggest that the sugary fluid secreted by ovules helps to regulate the expression of these unconventionally secreted proteins.

Pistil-whipped

As the pollen tube develops, it also secretes a number of proteins. Hafidh and colleagues (from the Czech Academy of Sciences) recently published the first pollen tube secretome in Genome Biology. The authors identified 801 proteins secreted by the pollen tube after it penetrates through the female reproductive tissues. More than half of these proteins are secreted unconventionally, and the authors show this process at work for the first time.

It's still unknown why the pollen tube would secrete its own proteins, but the authors suggest that the secretome could be involved in perceiving guidance signals released by the ovule.

In both of these articles, a large portion of proteins secreted during plant sex are subject to post-transcriptional and post-translational modifications, showing that the widely-applied gene expression studies only show a very limited picture.

However, until very recently, technical limitations kept researchers from being able to fully study the ovule and pollen tube secretomes in a way that closely mimics what's really happening. The development of a semi- in vivo approach is paving the way for our understanding of the communication involved in flowering plant reproduction.

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Plant Parenthood: new insights into the sex lives of flowering plants - On Biology

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Plants have complex sex lives, just like humans. And just like us, their sex lives involve a lot of communication and testing for mutual compatibility. Since today is Fascination of Plants Day, we take a look at the raunchy world of plant sex.

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A reprodução é uma das principais fases do ciclo de vida e a floração, no caso das angiospérmicas, providencia a transição do estado vegetativo para reprodutivo.

As hormonas, como as giberelinas, jasmonato, ácido abcísico, etileno e auxinas, promovem a floração por regulação epigenética e tem efeitos importantes na compactação de cromatina na metilação do DNA e nas modificações em histonas.