Abstracts
In Brazil, Ficus mexiae is classified as Vulnerable under IUCN criteria, and to date there is only one report on pollinator activity for this species. Is not unusual to find cases where more than one species of wasp simultaneously occurs on and pollinates the same fig. In this study we present evidence that two Pegoscapus wasp species contribute to the pollination of F. mexiae and relationship between pollinators maybe competitive. These results indicate that the F. mexiae population represent an important element in the complex dynamics of maintaining diversity in neotropical Ficus spp.
co-occurrence; pollinators; Pegoscapus ; Ficus mexiae
No Brasil, Ficus mexiae é classificada como uma espécie vulnerável sob os critérios da IUCN, e até agora não há um único relatório sobre a atividade dos polinizadores desta espécie. Não é raro encontrar casos em que mais de uma espécie de vespa, simultaneamente, ocorre e poliniza o mesmo figo. Neste estudo, apresentamos evidências de que duas espécies de vespas Pegoscapus contribuem para a polinização de F. mexiae, possivelmente em uma relação competitiva. Estes resultados indicam que a população F. mexiae representa um elemento importante na dinâmica complexa de manutenção da diversidade de Ficus spp. neotropicais.
coocorrência; polinizadores; Pegoscapus ; Ficus mexiae
1. Introduction
The Atlantic Forest biodiversity hotspot includes a large number of species of fig,
Ficus L. (Moraceae) (Carauta, 1989CARAUTA, JPP., 1989. Ficus (Moraceae) no Brasil: Conservação e
Taxonomia. Albertoa, vol. 2, p. 1-365.) that
play an important role in providing key resources to many species - provisioning edible fruits, and
contributing to the maintenance of faunal diversity (Shanahan et
al., 2001SHANAHAN, M., SO, S., COMPTON, SG. and CORLETT, R., 2001. Fig-eating by vertebrate
frugivores: a global review. Biological Reviews, vol. 76, no. 4, p. 529-572.). Many Ficus species are threatened with extinction, among them
Ficus mexiae Standley that is classified as vulnerable by the International Union
for Conservation of Nature and Natural Resources (IUCN,
2011IUCN, 2011. IUCN Red List of Threatened Species. Version 2011.2. Available from:
www.iucnredlist.org. Access in: 16 nov. 2011.
www.iucnredlist.org...
). This is a rare medium-sized plant measuring up to 10 meters in height, which is
restricted to Minas Gerais and Bahia (Carauta and Diaz,
2002CARAUTA, JPP. and Diaz, BE., 2002. Figueiras do Brasil. Rio de Janeiro: Editora
UFRJ. 212 p.). Little is known about the reproductive aspects of this plant, although there is one
report of two Pegoscapus Cameron (1906) species of fig wasp, simultaneously
occurring in its syconiums (Schiffler, 2002SCHIFFLER, G., 2002. Fig Wasps (Hymenoptera: Agaonidae) associated to Ficus mexiae
Standl (Moraceae) in Lavras, Minas Gerais, Brazil. Neotropical Entomology, vol. 31, no. 4, p.
653-655.).
There are over than 800 known species of Ficus (Moraceae) genus
distributed in the tropical and subtropical regions of the world (Harrison, 2005HARRISON, RD., 2005. Figs and the diversity of tropical rainforests. Bioscience,
vol. 55, p. 1053-1064.), and for a long time it was believed that each species of fig had only one
pollinating species of wasp (Ramirez, 1970RAMIREZ, WB., 1970. Host specificity of figwasps (Agaonidae). Evolution, vol. 24, p.
680-91.; Ramirez, 1974RAMIREZ, WB., 1974. Coevolution of Ficus and Agaonidae. Annals of the Missouri
Botanical Garden, vol. 61, p. 770-80.; Wiebes,
1979WIEBES, JT., 1979. Co-evolution of figs and their insect pollinator. Annual Review
of Ecology and Systematics, vol. 10, p. 1-12.). It is true for many species, because the fig wasps show a peculiar morphological
adaptation, with a high level of phenological synchrony and many are indeed extremely specific about
the host (Wiebes, 1979WIEBES, JT., 1979. Co-evolution of figs and their insect pollinator. Annual Review
of Ecology and Systematics, vol. 10, p. 1-12.). On the other hand, several cases are
reported in which multiple wasp species can act as pollinators for a fig tree, and this may occur
from 25 to 50% all fig species (Cook and Rasplus, 2003COOK, JM. and RASPLUS, JY., 2003. Mutualists with attitude: coevolving fig wasps and
figs. Trends in Ecology & Evolution, vol. 18, p. 241-248.; Machado et al., 2005MACHADO, CA., ROBBINS, N., GILBERT, MTP. and HERRE, EA., 2005. A critical review of
host-specificity and its co-evolutionary implications in the fig/fig wasp mutualism. Proceedings
of the National Academy of Sciences. vol. 102 (suppl1), p. 6558-6565.). The simultaneous occurrence of more than one
species of wasp that are Ficus pollinators had already been demonstrated by several
authors (Rasplus, 1996RASPLUS, JY., 1996. The one-to-one specificity of the Ficus-Agaoninae mutualism:
howcasual? In VAN DER MAESEN, LJG., VAN DER BURGT, XM., VAN MEDENBACH DE ROOY, JM. (Ed.). The
Biodiversity of African Plants. Wageningen: Kluwer Academic Publishers. p. 639-649.; Weiblen, 2001WEIBLEN, GD., 2001. Phylogenetic relation- ships of fig wasps pollinating function-
ally dioecious figs based onmitochondrial DNA sequences and morphology. Systematic Biology, vol. 50,
p. 243-67.; Wieblen, 2002WIEBLEN, GD., 2002. How to be a Fig Wasp. Annual Review of Entomology, vol. 47, p.
299-330.; Vaamonde et al., 2002VAAMONDE, LC., DIXON, DJ, COOK, J. and RASPLUS, JY., 2002. Revision of the
Australian species of Pleistodontes (Hymenoptera: Agaonidae) fig-pollinating wasps and their host
plant associations. Zoological Journal of the Linnaean Society, vol. 136, p.
637-683.; Haine et al., 2006HAINE, E., MARTIN, J., and COOK, JM., 2006. Deep mtDNA divergences indicate cryptic
species in fig-pollinating wasps. BMC Evolutionary Biology, vol. 6, no. 83.
doi:10.1186/1471-2148-6-83.
https://doi.org/10.1186/1471-2148-6-83...
),
as well in different continents (Compton et al., 1991COMPTON, SG., HOLTON, KC., RASHBROOK, VK., VAN NOORT, S., VINCENT, L. and WARE, AB.,
1991. Studies of Ceratosolen galili, a non-pollinating Agaonid fig wasp. Biotropica, vol. 23,
p.188-94.; Kerdelhué et al., 1997KERDELHUÉ, C., HOCHBERG, ME. and RASPLUS, J.Y., 1997. Active pollination of
Ficus sur by two sympatric fig wasp species in West Africa. Biotropica, vol. 29, p.
69-75.). However, only one co-occurrence
record is known within the South American, between two Pegoscapus (species not yet
described) species in Ficus mexiae, without knowing which one is actually the
pollinator (Schiffler, 2002SCHIFFLER, G., 2002. Fig Wasps (Hymenoptera: Agaonidae) associated to Ficus mexiae
Standl (Moraceae) in Lavras, Minas Gerais, Brazil. Neotropical Entomology, vol. 31, no. 4, p.
653-655.). Considering that
Pegoscapus sp 1 and Pegoscapus sp 2 possessed pollen in their
mesoternary cavities (pollen pockets), Schiffler (2002)SCHIFFLER, G., 2002. Fig Wasps (Hymenoptera: Agaonidae) associated to Ficus mexiae
Standl (Moraceae) in Lavras, Minas Gerais, Brazil. Neotropical Entomology, vol. 31, no. 4, p.
653-655.
proposed the hypothesis that both species play a role in pollinating Ficus mexiae.
Based on this information, this work presents preliminary results on Ficus mexiae
pollination by Pegoscapus sp 1 and Pegoscapus sp 2 that occurs
simultaneously in the plant's syconium.
2. Material and Methods
We analyzed 57 syconium collected from two native Ficus mexiae individuals, located in the Universidade Federal de Lavras' campus, in the city of Lavras, state of Minas Gerais, Brazil (21°13′43″ S and 44°59′04″ W). Before collection, the syconiums were individually covered by polyester nets (forming little bags) to retain emerging wasps. The bags were placed on the syconiums on May 14, 2001, and remained there during the time of wasp hatching (2 to 3 days). After the hatching, all the material was taken to the laboratory for sorting. Following this the hatching wasps were captured using an entomological aspirator and afterwards packed together with the original syconium, in flasks with a solution of 10% of formaldehyde. We counted the number of individuals for each wasp species present in each syconium and the number of ovaries with seeds. We also recorded measurements of the syconiums' size and weight. To verify if the data presented Gaussian distribution, the Kolmogorov-Smirnov's test (Zar, 1974ZAR, JH., 1974. Bioestatistical analysis. Englewood Clifs: Prentice-Hall. 620 p.) was applied. Spearman correlation was used to test the correlation between the abundance of Pegoscapus species and the syconium's structural data (Zar, 1974ZAR, JH., 1974. Bioestatistical analysis. Englewood Clifs: Prentice-Hall. 620 p.). The difference between the average individual number of Pegoscapus sp 1 and Pegoscapus sp 2 in the syconiums was tested using the Mann-Whitney (U test) (Zar, 1974ZAR, JH., 1974. Bioestatistical analysis. Englewood Clifs: Prentice-Hall. 620 p.).
3. Results and Discussion
We captured a total of 305 individuals (DP ± 101) of Pegoscapus per syconium, 16% of which were from Pegoscapus sp 1 and 71% Pegoscapus sp 2. The Ficus mexiae syconium presented an average size of 15.3 mm (DP ± 1.3 mm) and weight of 1.6 g (DP ± 0.3 g). As was expected, the heaviest syconiums were also the biggest (rs = 0.83; p < 0.0001) and the thickest (rs = 0.50; p < 0.01). The number of individuals from both Pegoscapus species increased as the syconium increased in size (rs = 0.27; p < 0.05). This correlation may become stronger when also taking account of the number of non-pollinating wasps. With an increase in the syconium size the production of seeds also increases (rs = 0.61; p < 0.001), possibly because it aids the entrance of more pollinator wasps (founders). There was a statistically significant correlation between the number of individual Pegoscapus sp 1 and the size of the syconium (rs = 0.37; p < 0.005), but the same pattern was not true for Pegoscapus sp 2. The number of individuals of Pegoscapus sp 1 was positively correlated with the number of seeds produced (rs = 0.48; p < 0.0002), suggesting that it does provide a pollinator function. However, and contrary to what was expected, the most abundant species (Pegoscapus sp 2) did not correlate with the seed production. Yet, in cases where only Pegoscapus sp 1 occurred (7%) or only Pegoscapus sp 2 (35%) seed production was recorded, and average size of seeds produced from both was similar (U = 14.5; p < 0.05; Figure 1), as was their average abundance (U = 17.5; p < 0.05; Figure 1). There was no difference between the average abundance of Pegoscapus sp 1 and Pegoscapus sp 2 (U = 414.5; p < 0.05), although their pair-wise abundance showed a negative correlation (rs = -0.70; p < 0.0001). This evidence of an antagonistic relation between these two Pegoscapus species suggests that these species may compete for ovaries on Ficus mexiae. However, independently of the interaction between these two wasps it provides evidence that both promote the pollination of Ficus mexiae.
Average abundance of wasps and seeds per syconium, when only one species of Pegoscapus occurs (error bars represent SD).
One species of Ficus may be host for two or more different pollinator or non pollinator wasp species (Wiebes, 1995WIEBES, JT., 1995. The new World Agaoninae (pollinators of figs). Verhandelingen Koninklijke Nederlandse Akademie Wetenschappen Afdeling Natuurkunde. 2nd ed. Wetenschappen. 60 p.), and one pollinator wasp species may have more than one Ficus species as a host (Compton, 1990COMPTON, SG., 1990. A collapse of host specificity in some African fig wasps. Society African Journal Science, vol. 86, no. 1, p. 39-40., Ware and Compton, 1992WARE, AB. and COMPTON, SG., 1992. Breakdown of pollinator specificity in an African Fig Tree, Biotropica, vol. 24, no. 4, p. 544-549.; Rasplus, 1996RASPLUS, JY., 1996. The one-to-one specificity of the Ficus-Agaoninae mutualism: howcasual? In VAN DER MAESEN, LJG., VAN DER BURGT, XM., VAN MEDENBACH DE ROOY, JM. (Ed.). The Biodiversity of African Plants. Wageningen: Kluwer Academic Publishers. p. 639-649.). When the host specificity is broken, the process of introgression between figs could occur giving rise to new species, thereby contributing to the increased diversity of figs (Machado et al., 2005MACHADO, CA., ROBBINS, N., GILBERT, MTP. and HERRE, EA., 2005. A critical review of host-specificity and its co-evolutionary implications in the fig/fig wasp mutualism. Proceedings of the National Academy of Sciences. vol. 102 (suppl1), p. 6558-6565.).
While preliminary, these results indicate that the F. mexiae population besides being maintained by more than one Pegoscapus, and therefore represent an important element in the complex dynamics of maintaining diversity in neotropical Ficus spp.
We thank the assistance of Dr. Tob Gardner, Cambridge University, UK and Dr. Jos Barlow, Lancaster University, UK in the revision of this manuscript.
References
- CARAUTA, JPP. and Diaz, BE., 2002. Figueiras do Brasil. Rio de Janeiro: Editora UFRJ. 212 p.
- CARAUTA, JPP., 1989. Ficus (Moraceae) no Brasil: Conservação e Taxonomia. Albertoa, vol. 2, p. 1-365.
- COMPTON, SG., 1990. A collapse of host specificity in some African fig wasps. Society African Journal Science, vol. 86, no. 1, p. 39-40.
- COMPTON, SG., HOLTON, KC., RASHBROOK, VK., VAN NOORT, S., VINCENT, L. and WARE, AB., 1991. Studies of Ceratosolen galili, a non-pollinating Agaonid fig wasp. Biotropica, vol. 23, p.188-94.
- COOK, JM. and RASPLUS, JY., 2003. Mutualists with attitude: coevolving fig wasps and figs. Trends in Ecology & Evolution, vol. 18, p. 241-248.
- HAINE, E., MARTIN, J., and COOK, JM., 2006. Deep mtDNA divergences indicate cryptic species in fig-pollinating wasps. BMC Evolutionary Biology, vol. 6, no. 83. doi:10.1186/1471-2148-6-83.
» https://doi.org/10.1186/1471-2148-6-83 - HARRISON, RD., 2005. Figs and the diversity of tropical rainforests. Bioscience, vol. 55, p. 1053-1064.
- IUCN, 2011. IUCN Red List of Threatened Species. Version 2011.2. Available from: www.iucnredlist.org. Access in: 16 nov. 2011.
» www.iucnredlist.org - KERDELHUÉ, C., HOCHBERG, ME. and RASPLUS, J.Y., 1997. Active pollination of Ficus sur by two sympatric fig wasp species in West Africa. Biotropica, vol. 29, p. 69-75.
- MACHADO, CA., ROBBINS, N., GILBERT, MTP. and HERRE, EA., 2005. A critical review of host-specificity and its co-evolutionary implications in the fig/fig wasp mutualism. Proceedings of the National Academy of Sciences. vol. 102 (suppl1), p. 6558-6565.
- RAMIREZ, WB., 1970. Host specificity of figwasps (Agaonidae). Evolution, vol. 24, p. 680-91.
- RAMIREZ, WB., 1974. Coevolution of Ficus and Agaonidae. Annals of the Missouri Botanical Garden, vol. 61, p. 770-80.
- RASPLUS, JY., 1996. The one-to-one specificity of the Ficus-Agaoninae mutualism: howcasual? In VAN DER MAESEN, LJG., VAN DER BURGT, XM., VAN MEDENBACH DE ROOY, JM. (Ed.). The Biodiversity of African Plants. Wageningen: Kluwer Academic Publishers. p. 639-649.
- SCHIFFLER, G., 2002. Fig Wasps (Hymenoptera: Agaonidae) associated to Ficus mexiae Standl (Moraceae) in Lavras, Minas Gerais, Brazil. Neotropical Entomology, vol. 31, no. 4, p. 653-655.
- SHANAHAN, M., SO, S., COMPTON, SG. and CORLETT, R., 2001. Fig-eating by vertebrate frugivores: a global review. Biological Reviews, vol. 76, no. 4, p. 529-572.
- VAAMONDE, LC., DIXON, DJ, COOK, J. and RASPLUS, JY., 2002. Revision of the Australian species of Pleistodontes (Hymenoptera: Agaonidae) fig-pollinating wasps and their host plant associations. Zoological Journal of the Linnaean Society, vol. 136, p. 637-683.
- WARE, AB. and COMPTON, SG., 1992. Breakdown of pollinator specificity in an African Fig Tree, Biotropica, vol. 24, no. 4, p. 544-549.
- WEIBLEN, GD., 2001. Phylogenetic relation- ships of fig wasps pollinating function- ally dioecious figs based onmitochondrial DNA sequences and morphology. Systematic Biology, vol. 50, p. 243-67.
- WIEBES, JT., 1979. Co-evolution of figs and their insect pollinator. Annual Review of Ecology and Systematics, vol. 10, p. 1-12.
- WIEBES, JT., 1995. The new World Agaoninae (pollinators of figs). Verhandelingen Koninklijke Nederlandse Akademie Wetenschappen Afdeling Natuurkunde. 2nd ed. Wetenschappen. 60 p.
- WIEBLEN, GD., 2002. How to be a Fig Wasp. Annual Review of Entomology, vol. 47, p. 299-330.
- ZAR, JH., 1974. Bioestatistical analysis. Englewood Clifs: Prentice-Hall. 620 p.
Publication Dates
-
Publication in this collection
Aug 2013
History
-
Received
3 Jan 2012 -
Accepted
24 Aug 2012