Identifying Target Species and Seed Sources for the Restoration of Threatened Trees in Southern Brazil

Identifying target species and seed sources for the restoration of threatened trees in southern Brazil

P. M. HOFFMANN,C.T.BLUM,S.J.E.VELAZCO,D.J.C.GILL and M . B ORGO

Abstract Ecological restoration of trees is often constrained Targets have been set to restore % of degraded land by by limited knowledge of the biology, propagation and man-  (CBD, ) but restoration efforts are often con- agement requirements of individual species. Consequently, strained by lack of knowledge of the biology, propagation restoration initiatives rarely incorporate less well-known and management of tree species or by a lack of sufficient species or those that are difficult to source and grow. We de- seed (Merritt & Dixon, ). A reliable source of high- scribe challenges associated with the restoration of threa- quality seed is critical to the success of restoration projects, tened trees in the Araucaria Forest of southern Brazil, and directly influencing the germination and survival of seed- analyse the effectiveness of methods used to define target lings and the genetic diversity of populations (Zahawi & species, identify seed sources and generate information on Holl, ). the phenology of rare or threatened tree species. A review These challenges are particularly pertinent to the of secondary data identified  rare or threatened taxa as tar- Brazilian Atlantic Rainforest, a biodiversity hotspot gets for seed collection. We then surveyed . km of trails (Myers et al., ) with ., plant species and , in  forest remnants, identifying and mapping , seed- animal species interacting across multiple trophic levels producing trees of  species. Surveys confirmed the scarcity (Mittermeier et al., ; Ribeiro et al., ). Less than of several tree species (including seven species with an abun- % of the forest remains, in isolated remnants, many of dance of ,. individuals per km), and nine species which are highly degraded (Ribeiro et al., ). Attempts showed no signs of fruiting during  years of phenological to restore the biome have evolved from projects focusing monitoring. These findings, together with limited knowl- on a small number of fast-growing species (most of which edge and application of optimal seed collection methods, failed to establish into self-perpetuating forest; Barbosa are significant factors impeding the recovery of these species et al., ) to initiatives adopting a high-diversity planting within their natural habitat. Wider application of the results approach (e.g. planting – tree species; Rodrigues et al., of this case study could support restoration of the Araucaria ). For many tree species, however, a lack of information Forest with seedlings from a wider diversity of species. on their reproductive biology prevents their inclusion in restoration projects (Rodrigues et al., ). Keywords Araucaria Forest, Brazil, conservation, phe- The Araucaria Forest is one of the most threatened eco- nology, propagation, seed collection, subtropical forest res- systems in the Atlantic Rainforest biome. In Paraná state, toration, threatened species where Araucaria Forest was once the dominant vegetation This paper contains supplementary material that can be type, covering ,, ha (Maack, ), ,.% of the orig- found online at http://journals.cambridge.org inal forest remains in advanced successional stages, none of which is considered primary forest (Castella & Britez, ). Such extensive fragmentation means that areas left to regen- erate without human assistance never attain the full range of  Introduction naturally occurring species (Liebsch et al., ). Restoration is the main mechanism available to restore he restoration of damaged but previously complex eco- species richness in the Araucaria Forest, but seed collection Tsystems may be one of the greatest challenges facing and tree planting tend to be focused on a narrow range of tropical forest conservation (Rojas-Briales & Weise, ). species. Partly as a result of low seed collection effort, only  of the  tree species found in Araucaria Forest (Leite & Klein, ) have been cultivated by Paraná state nurseries, P. M. HOFFMANN (Corresponding author), S. J. E. VELAZCO and M. BORGO Sociedade Chauá, 82130-010, Curitiba, Brazil. E-mail [email protected] which are the main producers of seedlings for restoration of this ecosystem (Martins et al., ). It is common practice C. T. BLUM Departamento de Ciências Florestais, Universidade Federal do Paraná, Curitiba, Brazil to produce seedlings of species that are easy to collect,

D. J. C. GILL Fauna & Flora International, Cambridge, UK fast-growing or technically simple to grow, rather than Received  June . Revision requested  August . many native species for which there is a lack of information Accepted  November . on seed collection and germination protocols. Only %of

). Mean annual temperature is –°C and annual pre- cipitation is ,–, mm (IAPAR, ). This subtropical forest is characterized by a dense physiognomy, marked by the dominance of emergent Araucaria angustifolia trees, with a mean height of – m (Scheer & Blum, ).

Methods

A list of target species for seed collection was identified, including all threatened or rare tree species. Threatened species were defined as those listed in the regional, national or global Red Lists (SEMA, ; MMA, ; IUCN, ), including species categorized as Near Threatened. The threat categories of the various Red Lists were standardized according to IUCN (). Rare species were defined as those not included in official Red Lists but with few herbarium records (INCT, ) and a low frequency of occurrence, identified through surveys of the structure of the FIG. 1 Original distribution of Araucaria Forest in Paraná, Brazil Araucaria Forest (Durigan, ; Pasdiora, ; Barddal (adapted from Olson et al., ). The rectangle on the inset et al., ; Geraldi et al., ; Seger et al., ; indicates the location of the main map in Brazil. Watzlawick et al., ; Kozera et al., ; Cordeiro & Rodrigues, ; Cordeiro, ). the threatened species of the Araucaria Forest have been A list of potential forest remnants was developed based grown by state nurseries (Martins et al., ). In cases on the occurrence of at least one target species. Data on where nurseries produce seedlings of threatened species, the conservation status of these remnants were compiled seeds are usually collected from a small number of trees, re- based on our knowledge and on a technical report of the sta- sulting in low genetic variability and fitness of seedlings tus of the Araucaria Forest (Castella & Britez, ). (Zahawi & Holl, ). The final selection was based on geographical variability Fast-growing species play an important role in the resto- (including various floristic associations within the ration process. By developing a canopy layer and encourag- Araucaria Forest, to maximize genetic variability for each ing the return of seed dispersers and pollinators they can species), forest condition (fragments of medium to ad- accelerate forest succession and the natural recruitment of vanced successional stage, with a minimum size of  a wide range of species (Elliott et al., ). However, in de- ha), and guarantee of protection (remnants located in pro- graded and fragmented landscapes, such as the Araucaria tected areas or under other forms of conservation manage- Forest, restoration with a low diversity of species is unlikely ment, thus maximizing the likelihood of selected mother to create the conditions necessary for dispersal of a wider trees surviving and being available for long-term monitor- range of naturally occurring species (Rodrigues et al., ing and seed collection). ). There is therefore a growing need for government Each selected forest remnant was surveyed intensively by agencies and conservation institutions to broaden the walking along all existing trails to search for mother trees of focus of seed collection and restoration efforts to include target species. Species were initially identified in the field threatened or locally rare species as well as fast-growing spe- and later confirmed by comparison with herbarium species. Here we present a list of target species for conservation cimens. The criteria for selection of mother trees were and restoration, identify sources of seeds (mother trees), es- good health (free of damage, disease and infestation by in- timate their frequency and abundance, and present basic in- sects) and full reproductive maturity (tree size, presence of formation about phenological patterns of threatened and old fruits, seeds or seedlings under the tree). rare species in the Araucaria Forest. We attempted to map the highest number of mother trees in the maximum possible number of remnants. To ob- Study area tain seeds with broad genetic variation, they were collected, when possible, from at least three populations of each spe- The Araucaria Forest once covered the plateau regions in the cies (Nogueira & Medeiros, ), and from at least  trees centre and south of Paraná, at –, m altitude (Fig. ). per population (Vencovsky, ). When this was not poss- The climate is humid subtropical, with cool summers and ible, surveys aimed to identify at least  trees per species in no dry season; frost is common in winter (Peel et al., the whole study area. Closely related individuals of the same

http://journals.cambridge.org Downloaded: 18 Mar 2015 IP address: 205.243.145.122 Restoration of threatened trees 3 species (, m apart) were not selected, following Silva & were found for  of the target species (all with ,. indivi- Higa (), and, where possible, selected mother trees were duals per km). Particularly rare species include A. excelsa, . m apart. Shorter distances between selected indivi- O. sellowii, Scutia buxifolia, Bunchosia pallescens, duals were accepted for rare species found only in a single Maytenus aquifolia, Inga lentiscifolia and Quillaja brasilien- cluster. For each mother tree selected the following data sis, which were observed in ,% of the forest remnants, were recorded: reference number, species, remnant, geo- with ,. individuals per km. graphical coordinates, diameter at breast height, trunk and total height, crown diameter, trunk shape, phenological Preliminary phenological assessment Phenological monitor- phase, and distance and azimuth from a reference parameter ing revealed that some species exhibited fruiting or flower- (e.g. road, trail, fence, forest edge). ing seasons that differed from those reported in the General reproductive phenological patterns were ident- literature and herbarium data. The observed fruiting periods ified for the target species, following a review of literature for O. odorifera and O. porosa differed by a few months to and herbarium collection records (INCT, ). Preliminary those reported, and larger variations between literature and information was verified during  field trips throughout the field observations were observed for Oreopanax fulvus, study area, covering all seasons, each year during March – O. sellowii, Cassia leptophylla, Casearia lasiophylla and March . During each phenological evaluation mother Lafoensia pacari (Supplementary Table S). For some spe- trees were categorized according to the presence or absence cies, including Tetrorchidium rubrivenium, Ocotea nutans of fruits and flowers, and the maturation phase. These data and Zanthoxylum kleinii, we recorded a complete absence were used to develop a seed collection calendar. of reproductive structures throughout the phenological monitoring period.

Results Discussion Target species The preliminary list of threatened and rare   tree species included taxa (Supplementary Table S ), of Definition of target species and identification of seed   which were threatened and rare. Of the threatened spe- sources cies,  were listed only in the Paraná state Red List (SEMA, ), one was listed only in the national Red List (MMA, The results indicate that the official list of threatened species ) and  were categorized as globally threatened for Paraná (SEMA, ) needs to be updated, as it does not (IUCN, ). Five species (A. angustifolia, Ocotea cathari- include several rare species that are threatened by habitat nensis, Ocotea odorifera, Ocotea porosa and Trithrinax bra- loss and forest fragmentation. Possible candidates include siliensis) were included in all three Red Lists. Of the  rare Butia eriospatha, Cedrela lilloi, Chionanthus filiformis, species, analysis of secondary data revealed that some taxa Albizia edwallii, Albizia burkartiana, Agarista pulchella, had ,  records in herbarium collections and were gener- Acca sellowiana, Ouratea sellowii, Agonandra excelsa, ally not recorded in phytosociological studies. These include Castella tweedii, Picrasma crenata and Colletia paradoxa. Colletia paradoxa, Maytenus boaria, Maytenus dasyclada, Several tree species were scarce in the study area Agonandra excelsa, Castella tweedii, Picrasma crenata, (Supplementary Table S), which is a common problem in Drimys angustifolia, Ouratea sellowii and Agarista pulchella. seed collection and restoration of rare and threatened species (Jalonen et al., ). Low levels of forest cover, edge ef- Identification of seed sources in the field Twenty-six fects, fragmentation, and the presence of invasive species are Araucaria Forest remnants (Fig. )in municipalities all likely to drive changes in species composition, with rare were identified as priorities for seed collection. Ten and threatened species particularly affected (Phartyal et al., of these are within officially protected areas. A total of ). As demonstrated elsewhere in the Atlantic . km of trails were surveyed (c. . km per remnant). Rainforest, the general absence of fauna from degraded Mother trees of  of the  target species were mapped areas limits seed dispersal and pollination, further biasing (Supplementary Table S). No individuals of the other  species composition in favour of naturally dominant species target species were found in the remnants studied. In total (Silva & Tabarelli, ). , individuals were marked as potential seed sources. The The results also demonstrate the difficulty of obtaining a aim of selecting a minimum of  trees of each species in at broad range of genotypes among seeds collected in the field. least three remnants was achieved only for A. angustifolia, Despite considerable effort, we achieved our aim of locating a Cedrela fissilis, Ilex paraguariensis, O. porosa and minimum of  trees from at least three populations for only Podocarpus lambertii, all of which except P. lambertii were five of the species studied. Way () recommended sam- observed in .% of the surveyed remnants, with an abun- pling  individuals in a population as a benchmark figure dance of . individual per km. In contrast, , individuals to support the production of seedlings for restoration, but

our results demonstrate the technical and logistical con- Future research and conservation straints of achieving this for extremely rare species. The num-  ber of target species of which no individuals were found in the We have identified sources of mother trees for rare or Araucaria Forest indicates the need for research on the distri- threatened species and recorded information on their phe- bution, ecology and conservation of these threatened species. nology, providing a basis for further seed collection efforts. Ex situ conservation, through seed collection and storage, However, there remain gaps in the information needed to is an important conservation strategy, but the existence of support seed collection and seedling production of rare species with recalcitrant seeds (e.g. P. lambertii and A. angu- and threatened tree species for restoration. Firstly, there is stifolia; Royal Botanic Gardens Kew, ) demonstrates the a need for extensive surveys to identify mother trees  importance of ensuring the protection of mother trees in for- among the rare or threatened tree species not recorded est remnants. Given the difficulties in storing seeds of recal- in our surveys. Secondly, there is a need for further research citrant species in ex situ seed banks (Phartyal et al., ), the on seed collection and seedling production protocols for the trees mapped are natural seed banks for restoration. Using species we recorded, and to share these with the nurseries and improving information on the distribution of mother and restoration projects currently operating within the trees is esssential for future restoration projects in Paraná. Araucaria Forest landscape. There are good reasons for nurseries and restoration projects to adopt these protocols and incorporate rare and Preliminary phenological assessment threatened species into their operations. Restoration of per- manent forest in other areas of Brazilian Atlantic Rainforest Limited information and research on the phenology of seed has been proven to be more efficient when using a high di- development in wild species is a major constraint for resto- versity of tree species (.; Barbosa et al., ), and the ration initiatives (Broadhurst et al., ). Furthermore, cost per seedling produced does not vary significantly phenology and seed production vary significantly between among species (Rodrigues et al., ). If restoration practi- individual trees of certain species, depending on climatic tioners could gain access to better information and repro- variation from year to year, and genetic and environmental ductive material from a wide range of species they would variation (Way, ). be more likely to adopt these species in planting projects In the Araucaria Forest some species exhibited unexpec- on a larger scale (Jalonen et al., ). ted phenological patterns (and there are several species for In addition to enhancing the restoration of rare and which little is known of their reproductive biology). threatened species in the Araucaria Forest there is a growing Tetrorchidium rubrivenium, for example, occurs in the need to ensure the immediate protection of mother trees be- Araucaria Forest but is more common in forests with war- fore they disappear from the remaining forest fragments. mer climates (INCT, ), which explains the difficulty in Mother trees are essential for the survival of these species observing flowering or fruiting in this colder climate. The within the Araucaria Forest in the short term and are the low fruit production observed for O. nutans and Z. kleinii major source of seed and genetic diversity for long-term re- (both endemic to the Araucaria Forest) may be explained covery of the forest. by the fact that they are dioecious (Melo & Zickel, ; Future research and conservation need to focus on the Brotto et al., ); the individuals selected might have factors that affect seed storage and the germination of indi- been male and therefore unable to produce fruits. vidual seedlings. At a global level these issues are already Ocotea odorifera is expected to fruit in alternate years being addressed by ex situ conservation projects such as (Inoue et al., ), and premature falling of fruits and the the Millennium Seed Bank Partnership at Royal Botanic long period of maturation (Lorenzi, ) make it difficult to Gardens, Kew, UK. For many of the species found in the collect seeds from this species. Araucaria Forest, however, their seed behaviour has yet to Understanding these details is necessary to ensure collec- be studied extensively. For species threatened with extinc- tion trips are timed appropriately to avoid wasted effort. tion, effective seed storage may be an essential ex situ con- Timing of seed collection is particularly difficult for species servation measure. that exhibit seasonal fluctuations in phenology and for those Despite the many challenges associated with collection of with low levels of fruit production or that produce a high seeds from rare and threatened species, our data represent a proportion of non-viable seeds, either as a result of pre- significant first step towards improving the genetic diversity dation or difficulties in maturation. According to Way and species richness of the seedlings produced in the () the frequency of empty and damaged seeds varies Araucaria Forest. The methods described here may be of rel- among species, populations and seasons. This emphasizes evance to ecological restoration programmes elsewhere the need for improved information on the reproductive bi- where the challenges of including rare and threatened tree ology of threatened species in the Araucaria Forest as a pre- species in seed collections, seedling production and planting cursor to improved seed collection for restoration efforts. operations are likely to be similar.

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Acknowledgements Genetic Resources—Thematic Study (eds M. Bozzano, R. Jalonen, E. Thomas, D. Boshier, L. Gallo, S. Cavers et al.), pp. –.FAO We thank Jeniffer Grabias, Marcelo Bosco Pinto, Natalia and Bioversity International, Rome, Italy.  Alejandra Bedrij, Tatiane Andressa Silva and Elivelton KOZERA, C., DITTRICH, V.A.O. & SILVA, S.M. ( ) Fitossociologia do componente arbóreo de um fragmento de Floresta Ombrófila Gurski for assistance during the study. We also thank the Mista Montana, Curitiba, PR, BR. Floresta, , –. Instituto Ambiental do Paraná and Instituto Chico LEITE,P.&KLEIN, R.M. () Vegetação. In Geografia do Brasil: Mendes de Conservação de Biodiversidade for their sup- região Sul. v. , pp. –. Instituto Brasileiro de Geografia e port, and the Fundação Grupo Boticário de Proteção à Estatística, Rio de Janeiro, Brazil. 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