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Synchronized Anthesis and Predation on Pollen in the Marine Angiosperm Thalassia Testudinum (Hydrocharitaceae)

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Synchronized Anthesis and Predation on Pollen in the Marine Angiosperm Thalassia Testudinum (Hydrocharitaceae) Vol. 354: 119–124, 2008 MARINE ECOLOGY PROGRESS SERIES Published February 7 doi: 10.3354/meps07212 Mar Ecol Prog Ser Synchronized anthesis and predation on pollen in the marine angiosperm Thalassia testudinum (Hydrocharitaceae) Brigitta I. van Tussenbroek1,*, J. G. Ricardo Wong2, Judith Márquez-Guzman2 1Unidad Académica Puerto Morelos, Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Apdo. Postal 1152, Cancún, 77500 Quintana Roo, Mexico 2Facultad de Ciencias, Universidad Nacional Autónoma de México Laboratorio del Desarrollo en Plantas, Circuito Exterior, Ciudad Universitaria, Del. Coyoacán, México D.F. 04510, Mexico ABSTRACT: Synchrony in the anthesis of male and female flowers of the hydrophilous dioecious marine angiosperm Thalassia testudinum was studied by following flower buds of 64 staminate and 34 carpellate flowers in situ during night and day to observe the timing of flower opening. Anthesis of female flowers occurred throughout the day, with a slight peak between 15:00 and 17:00 h. The time lapse between initiation of anthesis and full opening of the flowers was ∼2 to 3 h. Anthesis in male flowers was highly synchronized, and all ripe primordia initiated anthesis within 1 h at dusk at ∼18:00 h, and pollen was released within 1 to 2 h. Male flowers in anthesis, or briefly after anthesis, were a targeted food source for herbivorous fish and >30% of the staminate flowers were consumed during our observations. The highly synchronized nocturnal pollen release is unusual for an abiotic pollinator, and we hypothesize that this may be a mechanism to ensure fertilization or, alternatively, may be a reponse to avoid pollen predation by fish. KEY WORDS: Seagrass · Hydrophilous pollination · Synchronization · Fish · Scaridae · Caribbean Sea Resale or republication not permitted without written consent of the publisher INTRODUCTION ble mechanism to maximize probability of fertilization, in addition to excess production of pollen (Ackerman There are 59 species of seagrasses (Green & Short 2006), may be synchronization of the anthesis of male 2003), which complete their entire life-cycle in the and female flowers. In the marine environment, syn- marine environment. All species but one (Enhalus chronous release of gametes is common and is thought acoroides [L.f] Royle) have mechanisms of submersed to result in high fertilization levels. An impressive pollination (hyphydrophily; Ackerman 2006). The evo- example of the latter is the synchronized mass spawn- lution of hydrophily required adaptations in originally ing of the algae in the order Bryopsidales (Clifton 1997). terrestrial floral morphology (Sculthorpe 1985, Kuo & Various species of seagrasses growing in the intertidal McComb 1989). Floral structures of seagrasses gener- zone have synchronized staminate flower anthesis with ally have reduced petals, or lack a perianth altogether. low tides when the pollen masses are transported to the Pollen is either filiform, or consists of spheroidal pollen stigmas of the pistillate flowers on the water surface grains embedded in mucilaginous strands (Pettit 1984). (Cox 1991). However, much less is known about the Hydrophily is an abiotic mechanism of pollen transfer anthesis of subtidal seagrasses. Turtlegrass Thalassia and therefore nondirectional; thus, much pollen never testudinum Banks ex König (Hydrocharitaceae), the comes into contact with a stigma of the same species dominant seagrass species in the Gulf of Mexico and (Barrett et al. 1993). In addition, most seagrasses are Caribbean Sea, rarely grows intertidally and is usually dioecious, and separation of sexes increases variance in found at depths between 0.3 and 5.0 m. It is dioecious, reproductive success (Wilson & Harder 2003). A possi- and male inflorescences tend to be more abundant than *Email: [email protected] © Inter-Research 2008 · www.int-res.com 120 Mar Ecol Prog Ser 354: 119–124, 2008 female flowers (van Tussenbroek et al. 2006). The 12 to 18 stigmas (usually 14). At the base of the pedun- pollen grains of T. testudinum are spherical, ~56 µm cle, well below sediment level, a separate spathe cov- in diameter, and are released (by means of longitudinal ers the inferior ovary. The primordia of both staminate slits in the anthers) in strands of mucilage matrix, which and pistillate flowers are situated below the sediment are slightly negatively buoyant (Cox & Tomlinson until maturity is reached, when they are raised a few 1988). Nocturnal anthesis of male flowers was noted by cm above the level the level of the substrate, in Cox & Tomlinson (1988), but they did not present quan- between the strap-like leaves. titative data. Synchronized opening of flowers at dusk During the reproductive season in May 2004, a site is not uncommon in terrestrial angiosperms, where it with a high incidence of flowering in the back-reef has been associated with nocturnal pollinators such as area of Puerto Morelos reef lagoon was selected for moths, bats, or beetles (Gribel et al. 1999, Miyake & this study. The depth was 3.8 m and distance from the Yahara 1999), but as far as we know, it has never been studied flowers to the reef was ∼40 m. Based on prior reported before for abiotically pollinated plants (pollen field observations, 3 phases of anthesis of male flowers transfer by wind or water). were established: (1) bud, which consists of a closed During a previous attempt to examine in situ the primordium, the tepals fully covering the stamen sequence of anthesis of a male flower of Thalassia tes- (Fig. 1A); (2) anthesis, at which the tepals are opening tudinum, we filmed a juvenile parrotfish bite the (thus exposing the stamen), and followed by dehis- dehisced stamen, and return twice to consume left- cence of the anthers and pollen release: this phase lasts overs. This observation was surprising, because during for approximately 1 to 2 h (Fig. 1B–D); and (3) post- our at least twice a month field trips for >15 yr during anthesis, which is often the phase referred to as the daylight in the reef lagoon, we had never observed male flower, at which the dehisced stamen is in an parrotfish grazing on dehiscent male or female flowers. almost horizontal position, but with residuals of The purpose of the present study was 2-fold: (1) to mucilage substance with pollen that remain attached determine if anthesis of male and female flowers to the anthers until the following day (Fig. 1E,F). On occurs simultaneously, and whether pollination is syn- the afternoon of May 17, 2004, between 13:00 and chronized with light regimes; and (2) to establish 16:00 h, 40 male buds, situated well above or just whether parrotfish prey upon young stages of male above the substratum, were marked with a galvanized and female flowers. nail and a numbered ribbon. The nails were joined with a thin cord, to allow the divers to locate the indi- vidual flowers during the night. The flowers were MATERIALS AND METHODS monitored at intervals of 2 h, until 06:00 h on May 18. At each observation, the phase of anthesis was re- The study was carried out in Puerto Morelos reef corded for each flower. Three buds remained closed, lagoon, Mexico (20° 51’ N, 86° 55’ W), which is bor- and they were included in the subsequent trial. For a dered on the seaward side by a fringing reef. Terres- second series of observations on male anthesis, 37 new trial influence is virtually absent because of the lack of buds were marked between 06:00 and 08:00 h in the surface rivers, and salinity is 35.7 psu (Ruíz-Rentería et morning of May 18, and they were followed during al. 1998). Monthly mean surface water temperatures daylight hours until the morning of May 19. In contrast vary between ~25°C in the winter and ~31°C in the to those marked previously, these newly marked buds summer (Ruíz-Rentería et al. 1998). A well-developed were not clearly visible, but were situated just at sedi- seagrass community dominated by Thalassia tes- ment level and completely covered by the spathes. The tudinum covers the coarse calcareous sands in this reef observation procedure was as described above, but an lagoon. Flowering frequency of this seagrass varies additional phase of stretched bud was included. This throughout the reef lagoon, generally being low in stretched bud phase describes rapid elongation of the near-coastal and mid-lagoon areas, and higher near pedicel, through which the bud becomes raised 1 to the reef (ca. 20 to 30% of the shoots produce flowers; 2 cm above the substratum, whereas the spathe, which van Tussenbroek 1994). until then covered the primordium, remains at sedi- Nomenclature of the structures of the inflorescences ment level. of Thalassia testudinum follows Tomlinson (1969) and Female flower buds (N = 37) were marked on Orpurt & Boral (1964). Inflorescences grow in the leaf May 24, 2004, and followed until the morning of axils; the male flowers occur in clusters of 1 to 5 (usu- May 26. In analogy with the male flowers, 3 phases ally 3), and consist of a peduncle with a spathe cover- were distinguished: (1) bud, which consists of a closed ing early-stage primordia, 3 tepals and 8 to 13 stamen primordium, the tepals fully covering the stigmas (usually 9 to 12). The female flowers usually occur (Fig. 1H); (2) anthesis, at which time the tepals are singly and consist of a long peduncle, with 3 tepals and opening, exposing the stigmas still in vertical position; van Tussenbroek et al.: Anthesis and predation on Thalassia testudinum pollen 121 and (3) post-anthesis, which showed lively green- Flowers lost during the above-mentioned observa- coloured stigmas, in a more or less horizontal position tions on anthesis were verified to check whether they (Fig. 1I). The transition between Phases 2 and 3 lasted exhibited typical bite marks of fish, showing a neatly longer than that of the male flowers, with an estimated cut pedicel that lacked remains of stamen or tepals duration of 2 to 3 h.
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