An exception to Darwin's syndrome: floral position, protogyny, and insect visitation in Besseya bullii (Scrophulariaceae)

Abstract

Darwin pointed out that plants with vertical inflorescences are likely to be outcrossed if the inflorescence is acropetalous (flowers from the bottom up), the flowers are protandrous (pollen is dispersed before stigmas are receptive), and pollinators move upward on the inflorescence. This syndrome is common in species pollinated by bees and flies, and very few exceptions are known. We investigated flowering phenology and pollinator behavior in Besseya bullii (Scrophulariaceae) and found that it did not fit Darwin's syndrome. The vertical inflorescence was acropetalous but the flowers were distinctly protogynous, so flowers with newly receptive stigmas appeared on the inflorescence above those with dehiscing anthers. A number of small insects visited B. bullii; bees in the family Halictidae (Augochlorella striata and Dialictus spp.) were most common. When insects moved between gender phases within inflorescences, they moved up more often than down (61% versus 39% of observations, respectively) but this difference was only marginally significant. Most visits were to male-phase flowers only, and this preference was more pronounced for pollen-foraging insects than for nectar-foraging insects. B. bullii was self-compatible, so its flowering characteristics potentially could result in considerable self-pollination. However, an average of 38% of the lowermost flowers opened before any pollen was available on the same inflorescence; these "solo females" had a high probability of outcrossing (though fruit set was relatively low in the bottom portion of the inflorescence). Upper flowers may also be outcrossed because downward insect movement was not uncommon. Therefore protogyny in B. bullii may not necessarily lead to more selfing than would protandry.

Apical pattern of fruit production in the racemes of Ceratonia siliqua (Leguminosae: Caesalpinioideae): role of pollinators

“…This acropetal pattern contrasts strongly with that found in a large number of species (including many Leguminosae), in which fruit production is higher at the base of the inflorescence (Bawa and Webb, 1984;Lee, 1988;Berry and Calvo, 1991;Ehrlén, 1992;Obeso, 1993a, b;Diggle, 1995). Studies on protogynous hermaphrodite species are scarce and show either a visiting pattern opposite to that of the former or the absence of a definite pattern (Wilson, 1978;McKone et al, 1995). In a raceme of Ceratonia siliqua, the flowers open from the base to the apex, but at a certain moment, practically all are receptive at the same time, making it possible for the nonbasal flowers to be pollinated first.…”

Sex‐specific floral attraction traits in a sequentially hermaphroditic species

“…Species with temporal separation of sex roles in which male function precedes female function (i.e., protandrous) are most commonly acropetalous (flowers closest to the base of the stem develop first, Figure 1), resulting in female-phase flowers occurring below male-phase flowers on the stem (the opposite arrangement is very rare) (McKone, Ostertag, Rauscher, Heiser, & Russell, 1995).…”

“…Species with temporal separation of sex roles in which male function precedes female function (i.e., protandrous) are most commonly acropetalous (flowers closest to the base of the stem develop first, Figure ), resulting in female‐phase flowers occurring below male‐phase flowers on the stem (the opposite arrangement is very rare) (McKone, Ostertag, Rauscher, Heiser, & Russell, ). This floral positioning may reduce geitonogamous self‐fertilization if bee pollinators typically forage upward from the base of the stem to the apex, thereby encountering female‐phase flowers prior to male‐phase flowers, which they often do (Harder et al, ) (Figure ).…”

Biologia reprodutiva de Jacquinia armillaris (Primulaceae): uma espécie endêmica das restingas Brasileiras

“…A protoginia seria comum em cantarofilia pois evitaria a autopolinização causada pelo limitado deslocamento dos besouros e pelo tempo de residência dos besouros nas câmaras. Porém a evolução e ocorrência de protandria em espécies cantarófilas tem sido relacionada a casos específicos, relacionados à disposição e tempo das flores de diferentes sexos nas inflorescências e ao comportamento dos visitantes (Routley & Husband 2003), sendo comum a ocorrência desse tipo de dicogamia em flores que recebem pequenos insetos polinívoros que demoram um maior tempo na inflorescência e em espécies que apresentam somente flores femininas por um longo período, quando o pólen já foi praticamente removido das anteras (McKone et al 1995). Esse seria o caso de J. armillaris, que são: visitadas por besouros tipicamente polinívoros (Tenhet & Howe 1939;Kirk-Spriggs 1996); apresentam flores dispostas em pequenas inflorescências; demoram mais de um dia para apresentar as peças florais femininas e ficam expostas por um longo período.…”

“…Esse seria o caso de J. armillaris, que são: visitadas por besouros tipicamente polinívoros (Tenhet & Howe 1939;Kirk-Spriggs 1996); apresentam flores dispostas em pequenas inflorescências; demoram mais de um dia para apresentar as peças florais femininas e ficam expostas por um longo período. Essas características garantem que as visitas durante a fase feminina ocorram após a retirada de grande parte do recurso pólen, o que pode aumentar as taxas de cruzamento, porém em valores inferiores à obtida em espécies protogínicas (McKone et al 1995).…”