PHENOLOGY AND DEMOGRAPHY OF FICUS SUPERBA OF SINGAPORE YEO CHOW KHOON NATIONAL UNIVERSITY OF SINGAPORE 2007 PHENOLOGY AND DEMOGRAPHY OF FICUS SUPERBA OF SINGAPORE YEO CHOW KHOON 2007 PHENOLOGY AND DEMOGRAPHY OF FICUS SUPERBA OF SINGAPORE YEO CHOW KHOON (B.SC (HONS.), NUS) A THESIS SUBMITTED FOR THE DEGREE OF MASTER OF SCIENCE DEPARTMENT OF BIOLOGICAL SCIENCES NATIONAL UNIVERSITY OF SINGAPORE 2007 Name: Yeo Chow Khoon Degree: Master of Science Department: Biological Sciences Thesis Title: Phenology and Demography of Ficus superba of Singapore Abstract The reproductive and leaf production phenologies of Ficus superba in Singapore was studied Owing to the small population size, a census of all individuals was possible, allowing estimation of potential pollinator flight distances Syconium production is aseasonal, strongly associated with leaf change Larger trees reproduce and undergo leaf change more frequently One the other hand, leaf change is seasonal Though total crop failure of pollination was rare, unpollinated syconia and parasites were common in any crop Ficus superba demographies of man-modified and natural habitats were different probably because of niche availability, growth spurts, selective felling and natural mortality A logistic regression model, derived from the phenological study, was used with the demographic information to identify probable reproductive individuals Most flights occur between trees below 1.0 km apart, accounting for more than 25% of inferred flights — this probably attributable to the clumping of the coastal and insular species Keywords: Ficus superba, Moraceae, phenology, demography, pollination, Platyscapa corneri i ACKNOWLEDGEMENTS The thesis is made possible by the help and support provided many First and foremost I would like to express my gratitude to my supervisor Associate Professor Hugh Tan Tiang Wah, for his great patience and support Many persons took interest in the topic of my work and freely shared their ideas and advice They included Dr Shawn K.Y Lum, Dr Richard T Corlett, Dr Rhett D Harrison and Dr Yap Von Bing Dr Lum was the first to suggest a project on Ficus, though in another specialization, and started me thinking about the topic Dr Harrison was generous in offering his expertise in identifying pollinators and non-pollinators of Ficus, while stopping over briefly in Singapore, and sharing numerous ideas on my work Dr Corlett also freely shared his big store of insightful ideas, experience and advice with me, though sadly it was toward the end of my candidature and I could not include many of them Dr Yap who has taken an interest in botanizing, was a great help with discussion and interpretation statistics Not to be forgotten are my many friends, acquaintances, and colleagues, many of whom did not merely hang around passively in the background, but provided company, braved field trips, contributed suggestions, acted as sounding boards, spotted my oversights, added their own observations and showed moral support You know who you are and what you did, so without ado and in no order of merit or entertainment value, you are: Ang Kai Yang, Chua Siew Chin, David Tng, Edwin Phua Ek Kian, Giam Xingli, Loh Tze-Lynn, Look Su Lee, Morgany d/o Thangavelu, Neo Chin Ming, Oh Sin Tian, Ong Tan Ching, Sharon Sim, Tan Kai-xin, Tan Chuen Seng, and Teo Lai Lai As the sites censused in the project covered extensive area, it would not be possible without the help of the staff members of numerous organizations They included Mr Tan Kok Yeang of the Sentosa Development Corporation, Mr Derrick Ng Yew Hong and Ms Lee Xiaoyi of Nanyang Technological University, Mr Chia Way Seng, Mr Teo Yen Pai, Ms Low Lay Yong, Mr Tee Choon Peng of Surbana, Mr Ali Ibrahim, Mr Robert Teo, Ms Chew Ping Ting, Ms Lena Chan, Mr Tan Puay Yok, Mr Alan Tan Chye Soon, Mr Ooi Soon Chye, Dr Ian M Turner, Dr Ruth Kiew, Ms Serena Lee, Mr Benjamin Lee, Ms Sunia Teo, Ms Sharon Chan, Mr Haji Samsuri bin Haji, Mr Tay Soon Lian, Mr James Gan and Ms Boo Chih Min of National Parks Board, Ms Connie Chua of SBS Transit Ltd., Mr Lee Heng Hock, Dr Tan Koh Siang and Dr Michael Holmes of Tropical Marine Science Institute, Ms Yeo Seow Nan of Singapore Tourism Board, Mr Rafael Lam, Mr Gary Goh and Mr Malcom Chung Ministry of Defence, Public Relations Branch, Mr Teo Beng Tiam of Outward Bound Singapore, Mr Mocktarhe Alom of Bedok Water Reclamation Plant, Mr Shamsudin bin Mohd Amil of Public Utility Board, Ms Angie Ng and Dr Tan Geok Choo of Nature Society of Singapore ii TABLE OF CONTENTS PAGE ACKNOWLEDGEMENTS i TABLE OF CONTENTS ii SUMMARY v LIST OF TABLES vii LIST OF FIGURES viii AIMS LITERATURE REVIEW 3 2.1 TAXONOMIC STATUS AND DISTRIBUTION OF FICUS SUPERBA 2.2 ECOLOGY, DEMOGRAPHY AND POTENTIAL POLLINATOR FLIGHT DISTANCES OF FICUS SUPERBA 2.3 PHENOLOGY AND THE NUMBER OF INDIVIDUALS OF FICUS SPECIES NEEDED FOR CONSERVATION 2.4 SEASONALITY AND INTRAPLANT SYNCHRONY 10 2.5 POTENTIAL POLLINATOR FLIGHT DISTANCES 13 METHODS AND METHODS 16 3.1 PRELIMINARY SURVEYS 16 3.2 PHENOLOGICAL STUDY 17 3.2.1 Localities 17 3.2.2 Reproductive Phenological Studies 19 3.2.3 Leaf Production and Abscission Phenological Studies 23 3.2.4 Seasonality of Phenologies 24 3.3 COLLECTION OF POLLINATOR AND NON-POLLINATOR WASPS 25 3.4 CROP QUALITY AND POLLINATORS PER SYCONIUIM 26 3.5 DEMOGRAPHIC STUDY 28 3.6 LOGISTIC REGRESSION 29 iii 3.7 POTENTIAL POLLINATOR FLIGHT DISTANCES 30 RESULTS 31 4.1 PHENOLOGY 31 4.1.1 Circular statistic analysis for seasonality 35 4.2 RELATIONSHIP BETWEEN LEAF CHANGE AND INITIATION OF SYCONIUM PRODUCTION 41 4.3 RELATIONSHIP BETWEEN PHASES AND DIAMETERS OF SYCONIA 43 4.4 NUMBER OF WASPS PER SYCONIUM 48 4.5 CROP QUALITY 50 4.6 RELATIONSHIPS BETWEEN PLANT SIZE, PHENOLOGICAL CHARACTERISTICS AND CROP QUALITY 53 4.7 LOGISTIC REGRESSION MODEL 57 4.8 DEMOGRAPHY OF FICUS SUPERBA 58 4.9 POTENTIAL DISPERSAL DISTANCES OF THE POLLINATOR WASP 63 DISCUSSION 65 ASEASONALITY AND INTRA-PLANT SYNCHRONY OF REPRODUCTIVE EVENTS 65 5.1.1 Causes of Reproductive Aseasonility and Intra-Plant Asynchrony 67 5.1.2 Plant Size and Reproductive Phenology 68 5.2 SEASONALITY OF LEAFING, LEAF LOSS AND LEAF CHANGE EVENTS 70 5.3 THE RELATIONSHIP BETWEEN LEAF CHANGE AND REPRODUCTION 72 5.4 PERSISTENCE OF RIPE SYCONIA, THEIR SEASONAL AVAILABILITY AND FRUGIVORE DISPERSAL 73 5.5 COULD CROP SIZE BE ADAPTIVE? 75 5.6 CROP QUALITY AND CAUSES 77 5.1 iv 5.7 LOGISTIC REGRESSION PREDICTIONS AND ORIGINAL ASSIGNMENT OF REPRODUCTIVE STATUS 80 5.8 PATCHY DISTRIBUTION, POLLINATOR FLIGHT DISTANCES AND CONSERVATION 82 5.8.1 Applications to Conservation in Fragmented Habitats 87 DEMOGRAPHIC DIFFERENCES BETWEEN NATURAL AND HUMAN-MODIFIED HABITATS 89 5.9 CONCLUSIONS 91 REFERENCES 93 APPENDIX 100 v SUMMARY Aim To study of the reproductive and leaf production phenologies of Ficus superba (Miq.) Miq population in Singapore, and the demography of exhaustively censused Ficus superba (Miq.) Miq population in Singapore, with relevance to potential pollinator flight Location The main island and offshore islands of the Republic of Singapore Methods Surveys were conducted in various parts of Singapore to census Ficus superba plants For phenological study, 28 plants were observed weekly, from 28 September 2003, to March 2005 The 58 weeks duration of the maximum overlap in observations (weeks beginning 21 October 2003 to 23 November 2004) was used to estimate phenological parameters Syconia from 50 crops were dissected for information on pollination rate, mean number of pollinator per syconium and parasitism rate Statistical tests were performed to elucidate relationships between duration phenological states, size of the plants, habit, size of syconia crop, mean pollinator per syconium and parasitism rate For demographical study, individuals were initially assigned as reproductive or juvenile based on height Following the reproductive phenological study, a logistic regression model was derived to predict probable reproductive individuals Geographical distances between all pairs of assigned and predicted reproductive individuals were used to calculate potential pollinator flight distances Results Initiation of syconia production was aseasonal, but leaf production showed bimodal peaks A strong association existed between leaf change and syconia production Larger plants produced syconia more frequently, consisting of a larger proportion of small crops, tended to have discrete leaf change events Though total failure of pollination was rare, crops with unpollinated syconia, and syconia parasitized by Camarothorax and Apocryptophagus were common Duration of receptive Phase B is positively correlated to the proportion of crop with failed female syconia, while both are negatively correlated with the mean number of pollinator per syconium Crop size is negatively correlated with the mean pollinator per syconium, though was not significantly related to duration of Phase B or proportion of failed female syconia Interestingly, parasitism by Apocryptophagus, but not Camarothorax, increases with proportion of failed syconia, though parasitism by both parasites was positively correlated Of 346 individuals censused, 155 were assigned reproductive Of these, 78 were predicted to be juveniles based on logistic regression, but no juveniles were reclassified Dominance of 0–2 m height class was seen in human-modified habitats, while in natural habitats there were two modal classes (2–4 m and 8–10 m) Potential pollinator flight distances varied little whether assigned or predicted reproductive individuals were used The distances or percentages of flight for the latter are given in brackets: mean of 15.2 km (15.6 km), mode of 1.0 km, with 28.8 % (25.5 %) of potential flights below 1.0 km and 56.2 % (55.4 %) below 16 km vi Main Conclusions Pollinators are usually scarce and in response, the plants lengthen the period of receptivity of the syconia It is suspected that Apocryptophagus exploits unpollinated syconia Further study is required to confirm this Differences in the demography of natural versus human modified habitats could be owing to factors of niche availability, selective removal or mortality or growth spurt The preponderance of short distance flights is surprising, as pollinators of Ficus have been reported to transverse great distances 99 Weiblen, G.D (2002) How to be a fig wasp Annual Reviews in Entomology 47, 299– 330 Weiblen, G.D & Bush, G.L (2002) Speciation in fig pollinators and parasites Molecular Ecology 11(8), 1573–1578 West, S.A., Herre, E.A., Compton, S.G., Godfray, H.C.J & Cook, J.M (1997) A comparative study of virginity in fig wasps Animal Behaviour 54, 437–450 Whitmore, T.C & Sayer, J.A 1992 Deforestation and species extinction in tropical moist forests Tropical Deforestation and Species Extinction (ed by Whitmore, T.C & Sayer, J.A.), pp 1–14 Chapman & Hall Wiebes J.T (1994) The Indo-Australian Agaoninae (pollinators of figs) Verhandelingen der Koninklijke Nederlandse akademie van wetenschappen Afdeling natuurkunde Tweede Reeks, Deel 92 North-Holland, Amsterdam Wiebes, J.T (1979) Co-evolution of figs and their insect pollinators Annual Reviews in Ecology and Systematics 10, 1–12 Wiebes, J.T (1982) Fig wasps (Hymenoptera) Biogeography and Ecology of New Guinea 2(4), (ed by J.L.Gressitt), pp 735–755 Dr W Junk Publishers, The Hague-Boston-London Windsor, D.M., Morrison, D.W., Estribi, M.A & de Leon, B (1989) Phenology of fruit and leaf production by ‘strangler’ figs on Barro Colorado Island, Panama Experientia 45, 647–653 Zavodna, M., Arens, P., van Dijk, P.J., Partomihardjo, T., Vosman, B & van Damme, J.M.M (2005) Pollinating fig wasps: Genetic consequences of island recolonization Journal of Evolutionary Biology 18, 1234–1243 100 APPENDIX Table A Mean diameters of Phase B syconia of different events in descending order with non-significance ranges calculated using a conservative LSD (least square difference) Tree (event) FS-SJI-A026(2) FS-SJI-A026(5) FS-PSA-A010(1) FS-SJI-A019(3) FS-SJI-A029(2) FS-SJI-A026(3) FS-PSA-A010(2) FS-BED-A001(7) FS-SJI-A016(2) FS-PSA-A011(2) FS-BED-A001(6) FS-BED-A001(8) FS-SJI-A016(3) FS-PSA-A001(3) FS-SJI-A026(4) FS-SJI-A019(4) FS-BED-A003(1) FS-SBG-A001(7) FS-SJI-A019(5) FS-SBG-A001(4) FS-SBG-A001(5) FS-SJI-A017(2) FS-SBG-A001(6) FS-SJI-A020(3) FS-NTU-A001(4) FS-PSA-A010(3) FS-SBG-A001(3) FS-PSA-A013(3) FS-SJI-A016(4) FS-BED-A002(2) FS-BED-A002(3) FS-PSA-A013(2) FS-PSA-A001(4) FS-PSA-A009(3) FS-SJI-A029(4) FS-NTU-A001(5) FS-PSA-A001(5) FS-PSA-A008(4) FS-PSA-A008(3) Mean (cm) 1.952778 1.91875 1.875 1.85 1.8375 1.815909 1.814706 1.797753 1.796774 1.775 1.757292 1.754286 1.74375 1.675 1.67 1.648387 1.646667 1.613483 1.572727 1.562179 1.553049 1.55 1.527972 1.525 1.522581 1.515517 1.503788 1.5 1.496154 1.475 1.461111 1.454545 1.425 1.376667 1.366667 1.358889 1.35 1.335714 1.275 Std Dev 0.196643 0.168899 0.114261 0.212132 0.172723 0.128532 0.115603 0.146728 0.200805 0.05 0.202482 0.126304 0.238204 0.136814 0.125167 0.153016 0.167403 0.135211 0.071985 0.141922 0.116361 0.1 0.139494 0.086603 0.085478 0.115034 0.078599 0.08165 0.193069 0.155456 0.208833 0.061051 0.129422 0.206905 0.152753 0.113462 0.070711 0.089974 0.037796 n 18 28 16 22 17 89 31 96 140 40 10 31 15 89 11 78 82 143 31 29 66 13 11 15 45 LSD 0.05 Non-sig ranges a ab ab abc abc abc abc abc abc abcd bcd bcd bcd cd cde cde cde cde cdef cdef cdef cdefg cdefg cdefg cdefg cdefg cdefg cdefg defg defg efg efg efg efg efg fg fg fg g 0.227495 cm 101 Table B Mean diameters of Phase Bw syconia of different events in descending order with non-significance ranges calculated using a conservative LSD (least square difference) Tree (event) FS-BED-A001(6) FS-SJI-A026(2) FS-SJI-A026(5) FS-SJI-A016(1) FS-SJI-A015(2) FS-SJI-A016(4) FS-BED-A003(1) FS-SJI-A016(3) FS-PSA-A011(2) FS-BED-A001(8) FS-BED-A002(3) FS-PSA-A011(1) FS-SBG-A001(7) FS-PSA-A006(1) FS-PSA-A010(4) FS-SJI-A017(2) FS-BED-A002(2) FS-SBG-A001(6) FS-SBG-A001(3) FS-SJI-A029(4) FS-BED-A003(2) FS-PSA-A001(5) FS-PSA-A008(4) Mean (cm) 2.016 1.95 1.94 1.913636 1.87 1.86 1.819231 1.783333 1.75 1.738462 1.73 1.69 1.68 1.65 1.64 1.58 1.5525 1.521429 1.511111 1.48 1.46 1.414706 1.375 Std Dev 0.199332 0.195789 0.147479 0.138005 0.125499 0.163554 0.087888 0.125831 0.040825 0.160815 0.095991 0.155724 0.057009 0.102598 0.119373 0.171756 0.19566 0.11127 0.069722 0.115109 0.124212 0.119589 0.041833 n 25 11 5 13 26 15 5 20 5 20 15 17 LSD50 Non-sig ranges A Ab Ab Ab Abc Abc Abc Abcd Bcd Bcd Bcd Bcde Bcde Bcde Bcdef Cdef Def Def Def Def Ef F F 0.227967 cm 102 Table C Mean diameter of Phase Bc syconia of different events in descending order with non-significance ranges calculated using a conservative LSD (least square difference) Tree FS-SJI-A016(2) FS-BED-A001(6) FS-SJI-A026(3) FS-SJI-A029(2) fallen FS-PSA-A010(1) FS-BED-A001(7) FS-BED-A001(8) FS-SJI-A019(3) FS-PSA-A010(2) FS-BED-A001(8) fallen FS-SBG-A001(7) fallen FS-SBG-A001(7) FS-SJI-A019(4) FS-PSA-A001(3) FS-PSA-A009(3) FS-SBG-A001(4) FS-NTU-A001(4) fallen FS-SBG-A001(6) FS-SBG-A001(6) fallen FS-NTU-A001(4) FS-SBG-A001(5) FS-SBG-A001(3) FS-NTU-A001(5) fallen FS-NTU-A001(5) Mean (cm) 2.038 2.027273 1.94 1.927273 1.892857 1.881481 1.8625 1.85 1.82 1.734375 1.712162 1.675 1.663636 1.657143 1.626563 1.61125 1.606154 1.605556 1.57 1.558594 1.55 1.474242 1.443548 Std Dev 0.170953 0.123215 0.070711 0.181659 0.108082 0.189997 0.169359 0.047871 0.238298 0.167 0.107577 0.102338 0.171945 0.100216 0.130475 0.093312 0.08585 0.102129 0.090568 0.075829 0.134976 0.15411 0.128769 0.104676 n 25 11 11 14 27 15 10 16 37 24 22 32 40 65 18 64 33 31 LSD 0.05 Non-sig ranges a a ab ab ab ab ab abc bc bc cd cd cd cd cd d d d d de de de e e 0.179829 cm Table D Smith-Satterthwaite test of significant difference in means between the smallest Bw and four smallest values of B Refer to Tables D and E Smallest Bw vs 4th smallest B 3rd smallest B 2nd smallest B The smallest B t' 0.636715 1.03236 2.236068 4.611488 Degree of freedom 4.41898 8.740928 7.941176 10.2518 Significance α>0 (ns) α>0 (ns) α40 fs 7.800 0.800 1.200 2.833 1.333 0.667 FS-SJI-A019 20 20 fs 8.667 0.857 1.714 2.833 1.600 0.833 FS-SJI-A023 36 29 fs 14.500 0.750 1.000 2.000 0.667 1.000 FS-SJI-A029 23 22 fs 11.250 0.800 1.250 3.333 2.000 1.750 FS-SJI-A026 19 22 fs 10.750 1.200 1.600 3.000 1.000 1.600 FS-SJI-A020 18 - 20 ep 18.500 0.333 0.667 - - - - - - - 11.612 0.952 1.434 2.879 1.222 1.523 Total Tree No of ReproMean Duration of ductive Events Phase E (wk) (inc partial) No of Reproductive Events (only No Repro-ductive No of Samll complete ones) Events Starting Events No of Abscision No of Failed Events Samll Events No of Failed Big Events Freq of ReproDuration of Obser-vation ductive Events (wk) Starting (wk-1) FS-PSA-A008 3.000 4 0 0 60 0.067 FS-PSA-A011 2.000 2 0 0 60 0.033 FS-PSA-A006 2.000 1 0 0 60 0.017 FS-PSA-A009 1.500 3 0 60 0.050 FS-PSA-A010 4.000 4 0 0 60 0.067 FS-PSA-A001 5.000 5 1 0 60 0.083 FS-PSA-A013 5.500 3 0 0 60 0.050 FS-SBG-A001 7.750 8 0 75 0.107 FS-NTU-A001 9.667 5 65 0.077 FS-BED-A002 3.000 3 1 63 0.048 FS-BED-A003 3.333 4 0 65 0.062 FS-BED-A001 3.167 8 0 65 0.123 FS-SJI-A017 2.667 4 0 67 0.060 FS-SJI-A016 6.000 4 0 67 0.060 FS-SJI-A015 1.500 7 0 67 0.090 FS-SJI-A019 3.000 7 67 0.104 FS-SJI-A023 4.667 6 67 0.090 FS-SJI-A029 3.500 5 0 0 67 0.075 FS-SJI-A026 3.800 5 0 67 0.075 FS-SJI-A020 - 3 3 0 67 0.045 4.100 91 86 90 22 58 1.552 Total [...]... keystone species of the genus, it would strengthen the case for protecting small fragments The main aims of this study were thus: a To inventory and study the demography of the entire population of Ficus superba in Singapore 2 b To study the reproductive and leaf production phenologies of Ficus superba in Singapore c To estimate the potential pollinator flight distances of Ficus superba in Singapore 3... parts of the Northern Territory and Queensland) This changed when Berg and Corner (2005) redefined Ficus superba to exclude var japonica Miq and var heneana (Miq.) Corner The former is now Ficus subpisocarpa Gagnep., and the latter a separate Australian species, Ficus heneana Miq This severely restricted the range of Ficus superba to Thailand and southwards through to Java and the Lesser Sunda Islands,... Java and the Lesser Sunda Islands, Borneo (Anambas and Natuna Islands), Celebes and Moluccas (Ceram) Only at the extremes of their distributions at Ceram, Indochina and Thailand do Ficus superba and Ficus subpisocarpa coexist This circumscription is supported by distinct pollinator species for Ficus subpisocarpa (Platyscapa ishiiana Grandi) and Ficus superba (Platyscapa corneri Wiebes) (Wiebes 1994)... ECOLOGY, DEMOGRAPHY AND POTENTIAL POLLINATOR FLIGHT DISTANCES OF FICUS SUPERBA Ficus superba is a deciduous species mostly found in coastal and monsoon forests, often on rocks and at the sea front (Berg and Corner 2005) In Singapore, it is a nationally endangered plant (Turner et al., 1994), found as hemiepiphyte inhabiting beach vegetation (from Ng et al 2005) From the census done, plants of Ficus superba. .. In terms of numbers of individuals left, Ficus faulkneriana of Kenya and Tanzania (CR .. .PHENOLOGY AND DEMOGRAPHY OF FICUS SUPERBA OF SINGAPORE YEO CHOW KHOON 2007 PHENOLOGY AND DEMOGRAPHY OF FICUS SUPERBA OF SINGAPORE YEO CHOW KHOON (B.SC (HONS.),... TAXONOMIC STATUS AND DISTRIBUTION OF FICUS SUPERBA 2.2 ECOLOGY, DEMOGRAPHY AND POTENTIAL POLLINATOR FLIGHT DISTANCES OF FICUS SUPERBA 2.3 PHENOLOGY AND THE NUMBER OF INDIVIDUALS OF FICUS SPECIES... and Demography of Ficus superba of Singapore Abstract The reproductive and leaf production phenologies of Ficus superba in Singapore was studied Owing to the small population size, a census of