Microrefugia, Small Scale Ice Age Forest Remnants Author(S): M

Microrefugia, Small Scale Ice Age Forest Remnants Author(s): M. E. Leal Source: Systematics and Geography of Plants, Vol. 71, No. 2, Plant Systematics and Phytogeography for the Understanding of African Biodiversity, (2001), pp. 1073-1077 Published by: National Botanic Garden of Belgium Stable URL: http://www.jstor.org/stable/3668739 Accessed: 22/05/2008 06:59

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http://www.jstor.org Syst. Geogr.PI. 71: 1073-1077(2001)

Microrefugia, small scale ice age forest remnants

M.E. Leal

Laboratoryof PlantTaxonomy, Wageningen University, General Foulkesweg 37, 6700 ED Wageningen,The Netherlands [[email protected]]

Abstract. - In this study the possibility of rainforest outside the postulated refuge areas is explored by assessing the presence of rainforest Caesalpinioideae in Lope forest savannah mosaic in Gabon. In this dry area twenty-six tree species of this subfamily were located. Their physiological ability to cope with drought stress and their impossible migration from the nearest postulated refuge area strongly suggests that these species remained in the Lope area during the last ice age. Extrapola- ting this observation and incorporating all refuge indicator species outside the postulated refuge area, supports the idea that fragmentssmall of forest persisted during the last ice age acting as micro rejugia. Key words: rainforest, Pleistocene forest refuge theory, ice age, Caesalpinioideae, microrefugia, Gabon Resume. - Les micro-refuges, reliques forestieres a petite echelle de l'epoque glaciaire. L'exis- tence possible de la foret ombrophile a l'exte'rieur des aires-refuges pre'sume'es est envisagee dans cette etude par l'examen de la presence des Caesalpinioideae dans la mosaique foret-savane a Lope au Gabon. Dans cette region seche, vingt-six especes d'arbres de cette sous-famille ont ete signalees. Leur capacite physiologique a faire face au stress hydrique et l'impossibilite' qu'elles aient pu migrer a partir de l'aire-refuge presume'e la plus proche suggerent que ces especes ont du subsister dans la region de Lope au cours de la derniere periode glaciaire. L'extrapolation de cette observation et la prise en compte de toutes les especes indicatrices d'un refuge hors de l'aire-refuge presumee conduisent a postuler que de petits fragments de forets ont persiste au cours de la derniere periode glaciaire, constituant des micro-refuges. Traduit par le journal.

Introduction

The Pleistocene ForestRefuge Theorystates thatcurrent centres of biodiversityand endemismin the African rainforestare the locationswhere fragmentsof rainforestpersisted during ice ages, so-called forest refugia.These forestrefugia are placed along the continentaledges of West Africa and western Central Africa, at the foothillswest of the Rift Mountainsand in the centreof the Congo Basin (fig. 1) (Maley 1987, Sosef 1996, Van Rompaey1996, Colyn etal. 1991, Ndjele 1988). Althoughthe strong reduction of rainforestinvolved is met with some hesitation,the loss of the rainforestshould not be taken too lightly, since even western Cameroon,the wettest area in Africa had been affected and became largelydeforested (Maley & Brenac 1998).

E. Robbrecht,J. Degreef & I. Friis (eds.) Plant systematicsand phytogeographyfor the understandingoqf African biodiversity. Proceedingsof the XVIthAETFAT Congress, held in 2000 at the NationalBotanic Garden of Belgium. Subjectto copyright.All rightsreserved. ? 2002 NationalBotanic Gardenof Belgium Permissionfor use mustalways be obtainedfrom the NationalBotanic Garden of Belgium. ISSN 1374-7886 Syst. Geogr. Pl. 71 XVIth AETFAT Congress

Pollen recordsand fossil deposits are very restrictedin the Africanrainforest and the best evidence at presentis affordedby the distributionof plantspecies. Knowingthat during the last ice age species were aggregated into smaller forest pockets, it is not implausiblethat with ameliorationof climatic conadient becameestablished within the expandedrainforest as a resultof differencesin dispersal rate between species. However, opinions remaindivided whethercentres of biodiversityare historicallydetermined or determinedby present-dayecological factors,since manyof these centres are situatedin geomorphologicallyheterogeneous areas, which are associatedwith high levels of niche-differentiation. A way to bypass this impasse is by focussingon rainforestspecies with a restrictedseed dispersal mechanism, eliminatingthe possibilityof a restrictingecological factoror niche. Species of Begonia sect. Loasibegonia and sect. Scutobegoniaare such plants and their presence outside the postulated forest refugia(Sosef 1996) stronglysuggests thatmore forest existed thanis presentlyproposed in the Pleistocene forest refuge theory. This study sets out to test the possibility of rainforestoutside the postulatedrefuge areas during the last ice age, i.e. rainforestspecies survivingin dry areas.

Rationale

Caesalpinioideae with a ballistic seed dispersalmechanism have been chosen as a tool to test this possibility, because they have the unique combinationof being well distributedover the African rainforest and of dispersingvery slowly. Their wide distributioncreates the possibility to extrapolate and to make statementson a wider scale and their slow range expansionmakes them forest refuge indicators. Range expansionis slow because seeds are projectedonly over a few tens of metersper reproductive season (Van der Burgt 1997) and secondarydispersal by animalshas provenunlikely (Hughes et al. 1994, Tutin et al. 1997). The ectomycorrhizalcharacter of manyCaesalpinioideae (Newberry et al. 1988) may also inhibitthe advanceby occasionallong-distance events, since seedlings need to be near the mothertree for ectomycorrhizalinfection. Consequently once they have gone locally extinct due to a rainforestreduction as duringthe last ice age theyremain locally extinctfor some time. These characteristicsmake them indicativefor stableforest areas, or forestrefugia. This study deals with this matter,under the assumptionthat tree species with longevity, like the Caesalpinioideae,have had the same physiologicalrange and limitationsduring the last ice age as they have today. Assuming this it gives the opportunityto study species in present-dayenvironmental conditions, which resemble closely the conditionsduring the last ice age. The majorfactor reducing rainforestsurface during the last ice age was increaseddrought (e.g. Maley 1989). There are Caesal- pinioideae, which are adaptedto dry conditions.So the question here is, are rainforestCaesalpi- nioideaeable to live underdry conditions.

Study site

The Lope forest savannahmosaic in centralGabon (fig. 1) is a dry area, which forms a gap in the rainforestas the result of a climaticanomaly. The meanannual rainfall is 1499 mm (yrs 1984-2000) and the area is dominatedby grassland,which is maintainedby annualfires. Fire, however,does not destroy the existing forest, it only preventsthe establishmentof new forest (personal observation; Kellman & Meave 1997). The presenceof grasslandhas been datedback as far as 10,000 BP (Tutin & White 1998). The whole Lope forest savannah area was inventoried for the presence of Caesalpinioideae.Each species was checkedfor its truerainforest character.

1074 PhvtogeographvPhvto2eo ranhv M.E. Leal,Lea, -Microrefugia, icorfuia smallsal scale icec, age foesforest remnants

Figure 1. The postulatedfJorest refuge areas within the present-day rainforest (modified after Maley 1987).

Results and discussion

Twenty-six species with a ballistic dispersal mechanismwere located (table 1). These species are fairly to well distributedover the rainforestor part of it (Aubreville 1968, Caballe 1987, Wieringa 1999). They are not present in deciduousforests (Letouzey 1968) or in woodlandoutside the rain forest.They are all consideredrainforest tree species. Diversity and abundanceof the Caesalpinioideaevaried over the mosaic, but levels were highest at places where moistureis elevated by local circumstances,excluding marshes and other long-term inundatedareas. Althoughmean annual rainfall is 1499 mm, annualminima have been close to 1200 mm. So these Caesalpinioideaeare rainforesttree species, which in a dry region are restrictedto the moister places where they are physiologicallyable to cope with a considerableamount of drought stress. The droughtstress these species are now experiencingis more then duringthe last ice age when temperatureswere lower and evaporationwas not as strong as today. This proves that these rainforest trees did not necessarilyhave to become locally extinct when deterioratingclimatic conditions reducedthe rainforesthabitat. An estimation of dispersalrate is needed to establish whetheror not these species could have reachedthe outerlimits of theirpresent distribution from one of the refugeareas since the last ice age. Measurementson seed dispersaldistances have been done on the Caesalpinioidtree species Tetraber- linia moreliana Aubrev.(Van der Burgt 1997), which is representativefor this kindof seed dispersal. The maximumseed dispersaldistance was 60 m from a 40 m tall tree;a recordfor a seed ballistically dispersed (Van der Burgt 1997). As a non-pioneertree species, a considerableamount of time will pass before a seed has become reproductiveand disperses the next generation.So range expansion per generation for these Caesalpinioideaeis slow, i.e. a few tens of meters. The time involved for these Caesalpinioideaeto reach their reproductivephase is unknown,but it can be calculatedhow much it should have takenfor them to reach at least the Lope areafrom the nearestpostulated refuge area. The nearest postulatedrefuge area is the Massif du Chaillu, 100 km furthersouth. For the 26 species to have reachedthe Lope forest savannahmosaic they must have covered 100 km in 18,000 years (the time since the heightof the last ice age), i.e. a rangeexpansion of 5.6 m per year.For a non- pioneer tree, like Tetraberliniamnoreliana this would mean that it had to reach reproductiveage in

1075 Syst. Geogr. Pl. 71 XVIth AETFAT Congress

eleven years and grown 40 m tall to be able to projectthe next generation60 m furtheraway. Eleven years is an unlikely short time for a non-pioneertree to have become reproductive.A more realistic time is 30 years and consequentlythis results in a dispersal rate of 2 m per year with a maximum range expansion of 36 km since the height of the last ice age. Consideringthis slow and short range expansion, migration from the nearest postulated forest refuge area is not very plausible. Occasional long-distance seed dispersal events are not considered here as very likely, because secondarydispersal by animalshas not been observed(Hughes et al. 1997, Tutinet al. 1997). Also the need for ectomycoryzalinfection by the mothertree may hamperthe establishmentof seedlings over a long distance. Besides, it is unlikely that 26 species reached the Lope forest savannah mosaic depending on occasional long-distance seed dispersal only.

Table 1. Caesalpinioideaepresent in the Lope forest savannah mosaic.

Aphanocalyx djumaensis (De Wild.) J.Leonard Augouardia letestui Pellegr. Baikiaea insignis Benth. Baikiaea robynsiiGhesq. Berliniaauriculata Benth. Berliniabracteosa Benth. Bikiniagrisae Wieringa Brachystegia mildbraediiHarms Cryptosepalum staudtii Harms Cynometra schlechteri Harms Eurypetalum batesii Baker Gilbertiondendrongrandistipulatum (De Wild.)J.Leonard Guibourtiademeusii (Harms) J.Leonard Hymenostegia klainei Pierre ex Pellegr. Hymenostegia pellegrinii(A.Chev.) J.Leonard Julbemardia brieyi (De Wild.) Troupin Julbemardia pellegrinianaTroupin Julbemardia seretii (De Wild.) Troupin Neochevalierodendron stephanii (A.Chev.) J.Leonard Oddoniodendron micranthum(Harms) Baker Pellegriniodendrondiphyllum (Harms) J.Leonard Scorodophloeus zenkeri Harms Sindoropsis letestui (Pellgr.) J.Leonard Tessmannia anomala (Micheli)Harms Tessmannia dewildemaniana Harms Tetrabeliniabifoliolata (Harms) Hauman

Conclusions

Since migrationfrom the nearestpostulated forest refuge is not very plausibleand since these species have proven to be able to cope with a considerableamount of drought stress, it is much more plausible that they survivedthe last ice age in situ, i.e. the Lope forest savannahmosaic. Also the presence of refuge Begonias in the Lope forest savannahmosaic supports the probabilitythat rainforest persisted during the last ice age. The 26 refuge Caesalpinioideae and the two refuge Begonias are not restricted to the Lop6 forest savannahmosaic, but are fairlyto well distributedover the Africanrain forest and undermuch wetter conditions. Deteriorationof these wet conditionsand reductionof the rainforesthabitat as duringthe

1076 Phytogeography M.E.ME. Leal, Microrefugia, small scale ice age forest remnants last ice age does not necessaryhave to lead to their local extinctionas theirpresence in the Lope area has proven. There are many more refuge Begonias not present in the Lope area, but outside the postulated forest refugia and there are also many more refuge Caesalpinioideaewith a distributionbeyond the distance of 36 km from the nearest postulatedforest refuge areas (e.g. see distributionmaps in Wieringa 1999). All these refugeindicator plants togetherstrongly indicate that outside the postulated large areas of continuousforest, (macro)refugia,small patchesof forestmust have remained,acting as small scale refugeareas or microrefugia.

Acknowledgements. - I am gratefulto the Ministryof the Eaux et Foretsfor permissionto work in the Lope Reserve, and the research station CIRMF/WCS and research staff for logistics, accommodation and discussions. I thank K. Abernethy, B. van Gemerden, M. Sosef and one anonymousreviewer for theircomments and suggestions.Financial support for the work was provided by the NetherlandsFoundation of the Advancementof TropicalResearch (WOTRO).

References

Aubreville A. (1968) Legumineuses-Caesalpinioid6es.Flore du Gabon15. Paris,Mus. Nat. d'Hist.Nat. Caballe G. (1978) Essaisur la g6ographieforestiere du Gabon.Adansonia, sdr.2 17:425-440. Colyn M., Gautier-Hion A. & Verheven W. (1991) A re-appraisalof palaeoenvironmenthistory in CentralAfi-ica: evidence for a majorfluvial refuge in the ZaireBasin. J. Biogeogr.18: 403-407. Kellman M. & Meave J. (1997) Fire in the tropicalgallery forest of Belize. J. Biogeogr.24: 23-34. Letouzey R. (1968) Etudephytog6ographique du Cameroun.Lechevalier, Paris. Maley J. (1987) Fragmentationde la foret densehumide africaine et extensiondes biotopesmontagnards au quaternairerecent: nouvelles donneespolliniques et chronologiques.Implications paleoclimatiques et biogeographiques.Palaeoecology of Africa 18: 307-334. Maley J. (1989) Late Quaternarychanges in the Africanrainforest. In M. Leinen& M. Sarnthein(eds.) Palaeoclimatologyand Palaeometeorology;modern and past patterns of globaltransport: 585-616. London,Kluwer Academic Publishers. Maley J. & Brenac P. (1998) Vegetationdynamics, palaeoenvironments and climaticchanges in the forest of west Cameroon duringthe last 28,000 yearsBP. Rev. Palaeobot.Palynol. 99: 157-187. Ndjele M. (1988) Principalesdistributions obtenues par l'analyse factorielle des elements phytogeographiquespresumes end6miquesdans la flore du ZaYre.1985 AETFATproceedings-contributed papers. Monogr. Syst. Bot. 25: 631-638. Sosef M.S.M. (1996) Refuge Begoniasand Africanrain forest refuges:general aspects and recentprogress In L.J.G. van der Maesen, X.M. van der Burgt& J.M. van Medenbachde Rooy (eds.) The biodiversityof AfricanPlants: 602-611. Dordrecht, KluwerAcademic Publishers. Tutin C.E.G. & White L.J.T. (1998) Primates,phenology and frugivory:present, past and futurepatterns in the Lope Reserve, Gabon. In D.M. Newberry,H.H.T. Prins & N. Brown(eds.) Dynamicsof populationsand communitiesin the tropics:135-146. Brit.Ecol. Soc. Symposium37. Oxford,Blackwell Scientific. Tutin C.E.G., Ham R.M., White L.J.T. & Harrison M.J.S. (1997) The primatecommunity of the Lope Reservein central Gabon:diets, responsesto fruitscarcity and effects on biomass.Amer. J. Primatol.42: 1-24. Van der Burgt X.M. (1997) Explosive seed dispersal of the rainforesttree Tetraberliniamoreliana (Leguminosae- Caesalpinioideae)in Gabon.J. Trop.Ecol. 13: 145-151. Van Rompaey R.S.A.R. (1996) Rainforestrefugiain Liberia. In L.J.G. van der Maesen, X.M. van der Burgt & J.M. van Medenbachde Rooy (eds.) The biodiversityof AfricanPlants: 624-628. Dordrecht,Kluwer Academic Publishers. Wieringa JJ. (1999) Monopetalanthusexit. A systematicstudy of Aphanocalyx,Bikinia, Icuria, Michelsonia and Tetraberlinia (Leguminosae,Caesalpinioideae). Wageningen, PhD thesis, Wageningen Agric. Univ. Papers.

Manuscriptreceived November 2000; acceptedin revisedversion March 2001.

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