ABSTRACT Species phenology - the timing of key life events - is being altered by ongoing climate changes with yet underappreciated consequences for ecosystem stability. While flowering is

generally occurring earlier, we know much less about other key processes such as the time of fruit ripening, largely due to the lack of comprehensive long-term datasets. Here we provide

information on the exact date and site where seeds of 4,462 taxa were collected for the _Index Seminum_ (seed exchange catalogue) of the Botanic Garden of the University of Coimbra, between

1926 and 2013. Seeds were collected from spontaneous and cultivated individuals across Portugal, including both native and introduced taxa. The database consists of 127,747 curated records

OTHERS A DATABASE OF SEED PLANTS ON TAXONOMY, GEOGRAPHY AND ECOLOGY IN THE QINLING-DABA MOUNTAINS AND ADJACENT AREAS Article Open access 04 November 2022 CENOZOIC SEEDS OF VITACEAE REVEAL A

DEEP HISTORY OF EXTINCTION AND DISPERSAL IN THE NEOTROPICS Article 01 July 2024 TRACING THE INTRODUCTION HISTORY OF THE TULIP THAT WENT WILD (_TULIPA SYLVESTRIS_) IN SIXTEENTH-CENTURY EUROPE

Article Open access 13 June 2022 BACKGROUND & SUMMARY There is clear evidence that ongoing climate change is rapidly altering the timing of key recurring life events – species phenology

– including plant flowering, insect emergence, or bird migration1,2,3. Indeed, phenological shifts are one of the first responses of organisms to environmental changes and thus one of the

more sensitive biological indicators of climate changes, largely preceding other more insidious responses such as range shifts or extinctions4,5. The growing realization of the importance of

phenology on ecosystem functioning and stability has triggered a revival of phenological research in recent decades, spearheaded by research on flowering phenology6,7,8. While flowering is

key for pollination and plant reproduction, the production of seeds and fruits is at least as important, for it is only during this short period that plants can colonize new sites or endure

periods of unfavourable environmental conditions through seed dormancy9,10. Indeed, the timeframe available for fruit production is a key driver of global diversity patterns and is central

to understand how these can be affected by climate change11. Furthermore, evidence shows that the drivers of fruit ripening are not necessarily the same as those driving flowering

phenology12,13,14, rendering fruiting phenology research particularly needed14,15. Fruiting phenology has important ecological and conservation implications, as reviewed in Morellato _et

al_.16, including the potential to create mismatches between the availability of ripe fruit and their migratory seed dispersers17,18, modulating the dispersal services available to invasive

alien plant species19,20, or determining regeneration potential after wildfires21,22. All of these have a recognized potential to change the composition of future ecosystems, especially

forests15,18,23. It is thus unfortunate that fruiting season information is generally not available from botanical species descriptions in the same way that flowering is. Fruiting phenology

information can be obtained by several methods. The most straightforward is the establishment of long-term phenological stations where plants are periodically inspected (ideally daily) and

the date of the first ripe fruit on multiple individuals is recorded24. Alternatively, fruiting can also be identified by periodically checking fruit traps25. However, while these methods

originated some of the most comprehensive and accurate datasets on fruiting phenology available to date, they require a very large commitment in terms of continued sampling effort,

particularly challenging under the constraints of short funding cycles, and therefore not practical to characterize entire floras over long temporal series and large spatial scales. The

compilation of metadata from biological collections, chiefly from herbarium specimens, has been a highly valuable solution e.g.8,26. However, this approach also comes with its own intrinsic

biases27,28 and is particularly suited to track flowering phenology due to the taxonomic value of flowers, more commonly present in herbarium specimens than fruits29. Although fruiting

phenology studies are not uncommon, their taxonomic coverage and duration is generally low30. In particular, due to stringent trade-offs between the number of species included and effort

required to monitor them31, it is possible to find some remarkably long-term datasets e.g. a single species followed for 633 years32, and some remarkably comprehensive studies e.g. 1202

species followed for 7 years33. However, to our knowledge, no study to date has managed to follow any sizeable fraction of an entire flora for more than a decade15. While new technological

solutions, such as artificial intelligence and large-scale citizen science initiatives, can facilitate the automated collection of massive contemporaneous data16, they cannot offer solutions

to reconstruct past phenology against which recent shifts can be compared28. Here we explore the historical dataset of a longstanding seed exchange program that has documented fruiting

phenology data for a broad spectrum of species over an extensive temporal series. This dataset was made possible by the renewed interest on the natural sciences and the proliferation of

botanical gardens in the late 18th century, when some gardens established seed and plant exchange programs to expand and preserve their botanical collections and to resolve taxonomical

ambiguities34. To facilitate this exchange, numerous Botanical Gardens published a list of seed species available yearly, known as _Index Seminum_ (Latin for: Seed Catalogue), many

continuing to be issued to this day35. The _Index Seminum_ of the Botanic Garden of the University of Coimbra started in 1868 and was considerably improved in 1926 by expanding and

diversifying taxa and collection range, and standardizing identification, storage and distribution of seeds36. Most importantly, there were also improvements in the gathering and storage of

the information associated to each collected seed, which started to include the name of the species, subspecies, variety or form of the plants, taxonomic authority, as well as the exact

collection date and site. By 1932, the Botanic Garden was regularly exchanging seeds with 359 institutions worldwide, and at its peak, the service offered seeds of 2,758 species, shipping

over 11,000 seed packages to 800 scientific institutions around the globe37,38. METHODS Our dataset includes the records collected since 1926 by the staff of the Botanic Garden of the

University of Coimbra that include the date, location, and species or infraspecific taxa for the seeds collected every year to integrate the seed exchange catalogue. These records were

stored in a wood cabinet (“armário” in Portuguese) and kept in the original handwritten cards, to which every year a new location and date was added when each taxon was newly collected (Fig.

 1). The dataset includes both native and introduced species, as well as spontaneous and cultivated species collected inside the Botanic Garden, but also on dedicated field trips across

continental Portugal, including the Berlengas island (Fig. 2). The initial dataset included 138,191 entries, which were carefully curated and georeferenced, resulting in 127,747 fully

validated records after discarding incomplete, dubious or duplicated records, as well as those referring to reproductive organs other than seeds (i.e. bulbs and fern spores). Finally, a

small proportion of the most recent records (2.7%) were retrieved directly from field notebooks that had not been incorporated into the cards catalogue, and an additional 0.9% were retrieved

from the online catalogue of the Herbarium of the University of Coimbra, where they have been directly entered (https://coicatalogue.uc.pt, accessed on 2023-01-05). The complete dataset

includes collection records for 4,462 plant taxa. The day of collection indicates that at least one individual plant of that taxon was fruiting on a given day, at a given site. Since the

collected seeds were destined to germplasm exchange programs, collectors specifically targeted ripe fruits with viable seeds. This means that seeds that were not fully formed and likely to

be viable (based on the accumulated experience of the collectors/gardeners for each plant species) would not be collected and that site would need to be revisited latter to collect ripe

fruits. TAXONOMIC HARMONIZATION Botanical nomenclature was first manually verified by in-house botanists that uniformized small spelling mistakes and confirmed the taxonomic authorities.

This consolidated list was then harmonized with the Global Names Resolver with function _gnr_resolve()_ in R39, with the package _taxize 0.9.9_40,41, against the Global Biodiversity

Information Facility (GBIF) backbone taxonomy accessed on 2023-03-01. The accepted taxon name and taxonomic rank were extracted at this stage (Table 1). The list of native species for

Portugal was extracted from the World Checklist of Vascular Plants (WCVP42) with function _wcvp_distribution()_ in the R package _rWCVP 1.2.4_43 accessed on 2023-06-28. Species that were

collected in the country but are not considered native were classified as introduced. To facilitate data interoperability, the dataset includes the original name, as well as the harmonized

taxonomy according to both GBIF and the WCVP. GEOREFERENCING PROTOCOL Throughout the 87 years of data collection, the same collection site was often recorded with slightly different wording

by different generations of collectors. The original list of localities, containing 3,753 distinct entries, was initially clustered based on the textual description using OpenRefine and then

manually confirmed and further grouped into 1,485 unique curated localities. This clustering was performed only on toponymical homogenization without any loss of spatial accuracy (i.e., all

unique sites were preserved and not clustered into broader categories). The final list of localities was georeferenced using the point-radius georeferencing method44,45. The latitude and

longitude of each point and the confidence level for each coordinate was obtained using the online tool available on Maps.ie46 and coordinate uncertainty was calculated according to the

Georeferencing Calculator47,48. The administrative levels below country (stateProvince and municipality) were obtained from the Google Geocoding API49 by submitting the latitude and

longitude coordinates to the Reverse Geocoding Service. The estimated altitude for each pair of coordinates (minimumElevationInMeters) was obtained using the Google Elevation API. DATA

RECORDS The dataset is available at GBIF50 as a species occurrences map, and can also be downloaded from figshare51 as a single text file with information on 127,747 records arranged along

33 columns (total file size 89MB). Table headings follow the Darwin Core guidelines52. TECHNICAL VALIDATION The work largely benefited from the experience of Arménio Matos, Agostinho

Salgado, and António Coutinho who actively participated in field sampling campaigns since 1972 and were thus familiarized with the collection protocols, species, and collection sites. The

accumulated knowledge of the Herbarium of the University of Coimbra (COI) staff, namely Filipe Covelo, Joaquim Santos, and Fátima Sales, was also invaluable in curating the dataset, as many

seeds were collected from the same populations (and often collected simultaneously from the same individuals) from where herbarium specimens were also collected. FINAL QUALITY CHECK

Intermediate quality checks were routinely performed during data entry, taxonomic harmonization and georeferencing to detect and correct errors. Lastly, when the dataset was completed, we

performed a new and standardized quality check to evaluate the accuracy of the data. For this, we randomly selected 1,000 records using a random number generator and carefully rechecked all

the information against the original cards. We found data transcription errors on 7 records that resulted in errors on the collection day (n = 3 records), month (n = 3 records), and taxa (n 

= 1 record), corresponding to an overall error rate of 0.7%. USAGE NOTES The names provided in the fields “ScientificName” have already been harmonized according to the GBIF Backbone

Taxonomy (see _Taxonomic harmonization_ above). Therefore, for future taxonomical clarifications, users should use the “verbetimIdentification” field which corresponds to the original

taxonomic treatment with only minor in-house manual corrections. To facilitate data interoperability, species names according to the WCVP is also provided in the subfield

“scientificName_WCVP” in “dynamicProperties . CODE AVAILABILITY The following code can be used to import the dataset into R and to produce basic descriptive plots at the general and specific

levels (Fig. 3). Since some taxonomic authorities (i.e. the name of the taxon author) include apostrophes, such as _Tetragonia crystallina_ L’Hér., to import data correctly, it might be

necessary to specify that these are not quotes (with, quote = "\"",). data < - read.csv("~path/data.csv", quote = "\"", sep = ";")

#Number of unique species collected per year (Fig. 3a) barplot (rowSums(table(data$year, data$scientificName) >0)) # Number of records on the entire dataset per month (Fig. 3b) barplot

(table(data$month)) # Number of records per month for a single species (Fig. 3c) with(subset(data, scientificName == "Drosophyllum lusitanicum (L.)

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https://dwc.tdwg.org/terms/. (2021). Download references ACKNOWLEDGEMENTS The digitalization and curation of this dataset was funded by the Portuguese Foundation for Science and Technology

(FCT) through project LIFE AFTER FIRE 10.54499/PTDC/BIA-ECO/1983/2020, and grants 10.54499/UIDB/04004/2020, 10.54499/LA/P/0092/2020, 10.54499/CEECIND/00135/2017,

10.54499/CEECINST/00152/2018/CP1570/CT0014, 10.54499/2019.144414.BD and 10.54499/2020.07175.BD. AUTHOR INFORMATION AUTHORS AND AFFILIATIONS * Centre for Functional Ecology, Associate

Laboratory TERRA, Department of Life Sciences, University of Coimbra, Calçada Martim de Freitas, 3000-456, Coimbra, Portugal Ruben Heleno, José M. Costa, Filipe Covelo, Joaquim Santos, Pedro

Lopes, António C. Gouveia, M. Teresa Girão da Cruz, João Farminhão, Marta Horta, Guilherme Barreto, Ana V. Marques, Leonardo Craveiro, Patrícia Pinto, Matilde Santos, Bárbara Nunes, 

Margarida Barreiro, André Dias, Gabriel Rodrigues, Leonor Esteves, Marina Wanderley, Inês Santos, José Pedro Artiaga, João Veríssimo, Inês Vilhena, Lucas Moniz, Arthur Leão, Marta Couras, 

Sara B. Mendes, Mauro Nereu, Ana Margarida Dias da Silva, Fátima Sales, M. Teresa Gonçalves, António Coutinho, Helena Freitas, Elizabete Marchante & Sérgio Timóteo * Botanic Garden of

the University of Coimbra, University of Coimbra, Calçada Martim de Freitas, 3000-456, Coimbra, Portugal Agostinho Salgado, M. Teresa Girão da Cruz & João Farminhão * IATV - Instituto do

Ambiente, Tecnologia e Vida, Rua Sílvio Lima, Pólo II, 3030-790, Coimbra, Portugal João Farminhão * Escola Superior Agrária, Instituto Politécnico de Coimbra. Bencanta, 3045-601, Coimbra,

Portugal Mauro Nereu & Joaquim S. Silva * Centro de História da Sociedade e da Cultura, University of Coimbra, 3000-370, Coimbra, Portugal Ana Margarida Dias da Silva * MARE - Marine and

Environmental Sciences Centre/ARNET – Aquatic Research Network, Department of Life Sciences, University of Coimbra, Calçada Martim de Freitas, 3004-517, Coimbra, Portugal Jaime Ramos

Authors * Ruben Heleno View author publications You can also search for this author inPubMed Google Scholar * José M. Costa View author publications You can also search for this author

inPubMed Google Scholar * Filipe Covelo View author publications You can also search for this author inPubMed Google Scholar * Joaquim Santos View author publications You can also search for

this author inPubMed Google Scholar * Pedro Lopes View author publications You can also search for this author inPubMed Google Scholar * António C. Gouveia View author publications You can

also search for this author inPubMed Google Scholar * Arménio Matos View author publications You can also search for this author inPubMed Google Scholar * Agostinho Salgado View author

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Farminhão View author publications You can also search for this author inPubMed Google Scholar * Marta Horta View author publications You can also search for this author inPubMed Google

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Teresa Gonçalves View author publications You can also search for this author inPubMed Google Scholar * António Coutinho View author publications You can also search for this author inPubMed

 Google Scholar * Helena Freitas View author publications You can also search for this author inPubMed Google Scholar * Joaquim S. Silva View author publications You can also search for this

author inPubMed Google Scholar * Jaime Ramos View author publications You can also search for this author inPubMed Google Scholar * Elizabete Marchante View author publications You can also

search for this author inPubMed Google Scholar * Sérgio Timóteo View author publications You can also search for this author inPubMed Google Scholar CONTRIBUTIONS R.H., S.T., J.M.C., P.L.,

J.S., A.C.G. and F.C. designed the study and coordinated data acquisition, processing, and writing. A.M., A.S. and A.C. participated in the field sampling campaigns between 1972 and 2013.

All authors actively contributed to collect, insert, interpret, or curate the data, and approved the final manuscript. CORRESPONDING AUTHOR Correspondence to Ruben Heleno. ETHICS

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permissions ABOUT THIS ARTICLE CITE THIS ARTICLE Heleno, R., Costa, J.M., Covelo, F. _et al._ O armário: Fruiting phenology data for 4,462 plant taxa in Portugal (1926–2013). _Sci Data_ 11,

669 (2024). https://doi.org/10.1038/s41597-024-03520-9 Download citation * Received: 18 January 2024 * Accepted: 13 June 2024 * Published: 22 June 2024 * DOI:

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