Advertisement

Evolutionary Ecology

, Volume 27, Issue 2, pp 269–284 | Cite as

Can floral consumption by fish shape traits of seagrass flowers?

  • Brigitta I. van TussenbroekEmail author
  • Manuela Muhlia-Montero
Original Paper

Abstract

Seagrasses are marine flowering plants with hydrophilous pollination. This abiotic pollination by water assumes absence of flower-animal interaction, but animals can interfere in this process through consumption of reproductive structures. We studied predation on male flowers by fish for three dioecious seagrass species (Thalassia testudinum, Syringodium filiforme and Halodule wrightii) in the Mexican Caribbean. Seagrass flowers have a highly reduced or absent corolla and florivores directly consumed the anthers with pollen. The foliar structures (tepals, bracts or sheaths) protecting the male flower buds were removed by hand in situ. The floral buds were followed by videos or taking pictures at regular intervals and most (56–100 %, depending on seagrass species and experimental setting) artificially denuded male flower buds were consumed within 24 h by juvenile fish of various species. Histochemical analysis showed that the pollen and embedding mucilage were rich in polysaccharides and proteins, thus potentially nutritious. The seagrasses had copious production of pollen (between 0.2 and 1.2 × 106 pollen per flower, depending on the species). But T. testudinum and S. filiforme were often pollen limited, and the probability of fruit set was reduced ~50 % when the females were at the distance of 1 and 5–6 m from the males flowers, respectively. Under natural conditions, depredation on pre-anthesis male flowers in the three species was low because flower bud emergence (few hours) and pollen release (1–4 h) were ephemeral processes. In addition, the release of pollen of T. testudinum occurred at dusk when herbivorous fish became inactive. These life-cycle characteristics aid to avoid excessive pollen consumption by fish, however, whether they are anti-predator strategies or mere adaptations for submarine pollination remains to be established.

Keywords

Fish Marine angiosperm Pollen limitation Pollen predation Plant-animal interaction Seagrass 

Notes

Acknowledgments

M. G. Barba Santos for her assistance in the field and laboratory. F. Negrete Soto for his help with filming and identification of the “culprits” J. Márquez-Guzmán and R. Wong at the Laboratorio de Desarrollo de Plantas, Facultad de Ciencias, UNAM, for their support for the histochemical analysis, pollen counts of S. filiforme and H. wrightii and pollen tube analysis for T. testudinum.

References

  1. Ackerman JD (1997a) Submarine pollination in the marine angiosperm Zostera marina (Zosteraceae). I. The influence of floral morphology and fluid flow. Am J Bot 84:1099–1109Google Scholar
  2. Ackerman JD (1997b) Submarine pollination in the marine angiosperm Zostera marina (Zosteraceae). II. Pollen transport in flow fields and capture by stigmas. Am J Bot 84:1110–1119Google Scholar
  3. Ackerman JD (2000) Abiotic pollen and pollination: ecological, functional, and evolutionary perspectives. Plant Syst Evol 222:167–185CrossRefGoogle Scholar
  4. Ackerman JD (2006) Sexual reproduction of seagrasses: pollination in the marine context. In: Larkum AWD, Orth RJ, Duarte CM (eds) Seagrasses: biology, ecology and conservation. Springer, The Netherlands, pp 89–109CrossRefGoogle Scholar
  5. Ashman T-L, Knight TM, Steets JA et al (2004) Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. Ecology 85:2408–2421CrossRefGoogle Scholar
  6. Buckel CA, Blanchette CA, Warner RR, Gaines SD (2012) Where a male is hard to find: consequences of male rarity in the surfgrass Phyllospadix torreyi. Mar Ecol Prog Ser 449:121–132CrossRefGoogle Scholar
  7. Cook CDK (1988) Wind pollination in aquatic angiosperms. Ann Missouri Bot Gard 75:768–777CrossRefGoogle Scholar
  8. Coronado CJ, Candela J, Iglesias-Prieto R et al (2007) On the circulation in the Puerto Morelos fringing reef lagoon. Coral Reefs 26:149–163CrossRefGoogle Scholar
  9. Cox PA, Tomlinson PB (1988) Pollination ecology of seagrass, Thalassia testudinum (Hydrocharitaceae), in St. Croix. Am J Bot 75:958–965CrossRefGoogle Scholar
  10. Cox PA, Elmqvist T, Tomlinson PB (1990) Submarine pollination and reproductive morphology in Syringodium filiforme (Cymodoceaceae). Biotropica 22:259CrossRefGoogle Scholar
  11. De Cock AWAM (1980) Flowering, pollination and fruiting in Zostera marina L. Aquat Bot 9:201–220CrossRefGoogle Scholar
  12. Den Hartog C (1970) Seagrasses of the world. North Holland Publ Co, AmsterdamGoogle Scholar
  13. Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD (2004) Pollination syndromes and floral specialization. Ann Rev Evol Syst 35:375–403CrossRefGoogle Scholar
  14. Friedman J, Barrett SCH (2009) Wind of change: new insights on the ecology and evolution of pollination and mating in wind-pollinated plants. Ann Bot 103:1515–1527PubMedCrossRefGoogle Scholar
  15. Helfman GS (1993) Fish behaviour by day, night and twilight. In: Pitchet TJ (ed) Behaviour of teleost fishes, 2nd edn. Chapman & Hall, England, pp 279–512Google Scholar
  16. Herrera CM (2000) Measuring the effects of pollinators and herbivores: evidence for non-additivity in a perennial herb. Ecology 81:2170–2176CrossRefGoogle Scholar
  17. Kirk WD, Ali M, Breadmore KN (1995) The effects of pollen beetles on the foraging behaviour of honey bees. J Apicult Res 34:15–22Google Scholar
  18. Knight TM, Steets JA, Vamosi JC et al (2005) Pollen limitation of plant reproduction: patterns and processes. Ann Rev Ecol Syst 36:467–497CrossRefGoogle Scholar
  19. Krupnik GA, Weis AE, Campbell DR (1999) The consequences of floral herbivory for pollinator service to Isomeris arborea. Ecology 80:125–134Google Scholar
  20. Kuo J, den Hartog C (2006) Seagrass morphology, anatomy and ultrastructure. In: Larkum AWD, Orth RJ, Duarte CM (eds) Seagrasses: biology, ecology and conservation. Springer, The Netherlands, pp 51–87CrossRefGoogle Scholar
  21. Les DH (1988) Breeding systems, population structure, and evolution of hydrophilous angiosperms. Ann Missouri Bot Gard 75:819–835CrossRefGoogle Scholar
  22. Les DH, Cleland MA, Waycott M (1997) Phylogenetic studies in Alismatidae, II. Evolution of marine angiosperms (seagrasses) and hydrophily. Syst Bot 22:443–463CrossRefGoogle Scholar
  23. López-Curto ML, Márquez-Guzmán J, Murgía-Sánchez G (2005) Técnicas para el estudio del desarrollo en angiospermas, 2nd edn. Science Faculty, UNAM, MexicoGoogle Scholar
  24. Malo JE, Leinarana-Alcocer J, Parra-Table V (2001) Population fragmentation, florivory, and the effects of flower morphology alterations on the pollination success of Myrmecophila tibicinis (Orchidae). Biotropica 33:529–534Google Scholar
  25. McCall AC, Irwin RE (2006) Florivory: the intersection of pollination and herbivory. Rev Syn Ecol Lett 9:1351–1365CrossRefGoogle Scholar
  26. McConchie CA, Knox RB (1989) Pollination and reproductive biology of seagrasses. In: Larkum AWD, McComb AJ, Shepherd SA (eds) Biology of seagrasses. A treatise on the biology of seagrasses with special reference to the Australian region. Elsevier, Amsterdam, pp 74–111Google Scholar
  27. Orth RJ, Harwell MC, Inglis GJ (2006) Ecology of seagrass seeds and seagrass dispersal processes. In: Larkum AWD, Orth RJ, Duarte CM (eds) Seagrasses: biology, ecology and conservation. Springer, The Netherlands, pp 111–133CrossRefGoogle Scholar
  28. Pettitt JM (1980) Reproduction in seagrasses: nature of the pollen and receptive surface of the stigma in Hydrocharitaceae. Ann Bot 45:257–271Google Scholar
  29. Pettitt LM (1984) Aspects of flowering and pollination in marine angiosperms. Oceanogr Mar Biol Ann Rev 22:315–342Google Scholar
  30. Ramirez N (2004) Pollen specialization and time of pollination on a tropical Venezuelan plain: variations in time and space. Bot J Linn Soc 145:1–16CrossRefGoogle Scholar
  31. Reusch TBH (2003) Floral neighbourhoods in the sea: how floral density, opportunity for outcrossing and population fragmentation affect seed set in Zostera marina. J Ecol 91:610–615CrossRefGoogle Scholar
  32. Rodríguez-Martínez RE, Ruíz-Rentería F, Van Tussenbroek BI et al (2010) State and environmental tendencies of the Puerto Morelos CARICOMP site, Mexico. Rev Biol Tropical 58:23–43Google Scholar
  33. Roulston TH, Cane JH (2000) Pollen nutritional content and digestibility for animals. Plant Syst Evol 222:187–209CrossRefGoogle Scholar
  34. Sculthorpe CD (1985) The biology of aquatic vascular plants. Koeltz Scientific Books, West Germany (reprint)Google Scholar
  35. Shelton AO (2008) Skewed sex ratios, pollen limitation, and reproductive failure in the dioecious seagrass Phyllospadix. Ecology 89:3020–3029CrossRefGoogle Scholar
  36. Tanaka N, Uehara K, Murata J (2004) Correlation between pollen morphology and pollination mechanisms in the Hydrocharitaceae. J Plant Res 117:265–276PubMedCrossRefGoogle Scholar
  37. Tomlinson PB (1982) Anatomy of the monocotyledons VII Helobiae (Alismatidae). Clarendon Press, Great BritainGoogle Scholar
  38. Valentine JF, Heck KL Jr (1999) Review: seagrass herbivory: evidence for the continued grazing of marine grasses. Mar Ecol Progr Ser 176:291–302CrossRefGoogle Scholar
  39. Van Tussenbroek BI, Wong JGR, Márquez-Guzmán J (2008) Synchronized anthesis and predation on pollen in the marine angiosperm Thalassia testudinum (Hydrocharitaceae). Mar Ecol Progr Ser 354:119–124CrossRefGoogle Scholar
  40. Van Tussenbroek BI, Marquéz Guzmán J, Wong R (2009) Phenology of marine angiosperms [seagrasses]: reproductive synchrony in the sea. In: Pandalai SG (ed) Functional approach to sexual plant reproduction, research signpost, pp 17–46Google Scholar
  41. Van Tussenbroek BI, Muhlia-Montero M, Wong R et al (2010) Pollen limitation in a dioecious seagrass: evidence from a field experiment. Mar Ecol Prog Ser 419:283–288CrossRefGoogle Scholar
  42. Verduin JJ, Backhaus JO (2000) Dynamics of plant-flow interactions for the seagrass Amphibolis antarctica: field observations and model simulations. Estuar Coast Shel Sci 50:185–204CrossRefGoogle Scholar
  43. Williams SL (1995) Surfgrass (Phyllospadix torreyi) reproduction: reproductive phenology, resource allocation, and male rarity. Ecology 76:1953–1970CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Brigitta I. van Tussenbroek
    • 1
    Email author
  • Manuela Muhlia-Montero
    • 1
  1. 1.Unidad Académica de Sistemas Arrecifales/Puerto Morelos, Instituto de Ciencias del Mar y LimnologíaUniversidad Nacional Autónoma de MéxicoCancún, Quintana RooMexico

Personalised recommendations