# The importance of living collections for botanical research: Araceae as a case study

Christian Lacroix, Denis Barabé, Marc Gibernau

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Christian Lacroix, Denis Barabé, Marc Gibernau. The importance of living collections for botanical research: Araceae as a case study. Botany / Botanique, 2025, 103, pp.1-11. 10.1139/cjb-2025-0056. hal-05385053

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The importance of living collections for botanical research:

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Araceae as a case study

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Christian Lacroix¹, Denis Barabé², Marc Gibernau³

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¹ Department of Biology, University of Prince Edward Island, Canada C1A 4P3

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² Institut de recherche en biologie végétale, Jardin botanique de Montréal, Université de

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Montréal, 4101 Rue Sherbrooke est. Montréal, Canada, H1X 2B2

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³ CNRS – University of Corsica - Laboratory Sciences for the Environment (UMR 6134 SPE),

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Natural Resources Project - Vignola - Route des Sanguinaires, 20000 Ajaccio, France

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15 Abstract

Botanical gardens play a crucial role in botanical research by maintaining living collections of plants that serve educational and scientific purposes. This article examines the significance of living collections, using the Araceae family as a case study. Botanical gardens worldwide house diverse collections that contribute to studies in systematics, taxonomy, anatomy, morphology, floral biology, pollination ecology, phytochemistry, and medicine. The Araceae family, with its extensive diversity and distribution, provides an excellent model for comparative studies. Historical and contemporary research has utilized these collections to advance knowledge in specific areas. For instance, molecular systematics has benefited from these collections, as have studies on calcium oxalate crystal production, floral anatomy and development, pollen-ovule ratios, pollen viability, seed size and growth type, thermogenesis, and pollination syndromes. The article highlights the indispensable role of living collections in facilitating research that would be challenging to conduct solely in the field. It underscores the need for continued investment in botanical gardens to preserve their scientific and educational value, and outlines future research opportunities that living collections can offer.

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31 **Introduction**

32 For most people, botanical gardens are inviting places with colourful flowerbeds that
33 showcase a wide variety of plants. For others, botanical gardens are repositories that house
34 historic herbarium collections that contributed to our knowledge of taxonomy. The vision of
35 botanical gardens varies from one individual to another. They are generally perceived as a
36 continuum between educational establishments and recreational spaces. In reality, they are
37 institutions where collections of living plants are maintained for educational and scientific
38 purposes. This more formal perspective provides a framework for analyzing the complementary
39 roles of botanical gardens which include, to various extents, education, research, as well as
40 maintaining collections of living plants and landscaped gardens, depending on the type of garden
41 and its administrative framework (Barabé et al. 2012). According to data compiled by Pautasso
42 and Parmentier (2007), there are approximately 700 botanical gardens and over 1,700 arboreta
43 in 169 countries. Half of these are in 11 temperate countries: Australia, China, France, Germany,
44 India, Italy, Japan, Russia, Switzerland, the UK and the USA. The smallest occupies an area of 0.1
45 ha and the largest 1681 ha.

46 The scientific potential of botanical gardens was recognized since they were first
47 established. For example, throughout the history of botany as a discipline, they have provided
48 exceptionally useful resource material for studies in systematics and taxonomy. Additionally, since
49 the creation of the first botanical gardens in the 16th century, plants that grow there have been a
50 valuable source of material for a broad array of scientific studies beyond systematics and
51 taxonomy. Collections of living plants can be put to profitable use in various fields of plant biology,
52 such as anatomy, morphology, floral biology, pollination ecology, phytochemistry, and medicine.
For example, Hallé and Escoubeyrou (2002), formulated original and ground-breaking hypotheses on plant development, architecture and ecology based on observations made on specimens from Les Cèdres botanical garden in France.

**The Araceae family** - The Araceae family is one of the most diverse and distinct angiosperm families from a systematic point of view. It is the fourth largest monocot family divided into eight subfamilies with 150 genera and about 4,600 species currently described (Boyce and Croat 2018, current Uberlist). Araceae have amazing habit diversity and size differences, ranging from the tiny free-floating aquatic duckweeds (subfamily Lemnoideae) less than 1 cm wide to massive leaves up to 4 m long and 2 m wide in *Alocasia robusta* or giant inflorescences up to 3m high in *Amorphophallus titanum*. Araceae are nearly worldwide in distribution. Although the vast majority occur in tropical regions, several genera grow in temperate areas (North America, Europe, Africa and Asia) and particularly a group of genera have adapted to the Mediterranean climate (Croat 2019).

Aroids may be terrestrial and caulescent, cormose, tuberous, rhizomatous, rheophytes, appressed-climbing growing as primary or secondary hemiepiphytes, or true epiphytes. Aroids also inhabit a wide variety of habitats, including the forest understory, mid-canopy, stream banks, open marshy areas, or even moderately dry habitats (Croat 2019). Given their great morphological, floral, ecological and system pollination diversity it is a taxonomic group that is more and more used to study evolutionary problems (Croat and Ortiz, 2020).
Many botanical gardens in the world have collections of Araceae that are used in one way or another for research and public education, whether in North America (e.g. Fairchild, Missouri, Montreal), South America (e.g. Rio de Janeiro), Europe (e.g. Berlin, Brussels, Kew, Lyon, Munich, Nancy) or Asia (e.g. Bogor, Sarawak). Among these, there are the great collections whose scientific value is recognized worldwide, both in terms of the number of genera and species and the accuracy of their identification. These include among others the Missouri Botanical Garden, Munich Botanical Garden, Kew Royal Botanical Gardens, and Nancy Botanical Garden. These large collections, built up from specimens collected directly from the wild, are indispensable reference material that have been and can be used to further our scientific knowledge of Araceae.

The famous botanist Adolph Engler (1844 - 1930), for example, did not hesitate to use plant specimens from botanical gardens in his monographs. He wrote in detail about the organization of the Aroid shoot, basing his work almost exclusively on living plants from botanical gardens and herbaria (Engler 1877). The plants used for this study came mainly from the botanical gardens of Vienna, Munich and Berlin. In Das Planzenreich (1905 to 1920), 1,869 species of Araceae are described. References to specimens from botanical gardens are mentioned for 145 species representing 7% of all Aroid species. These publications clearly show how, at the end of the 19th century and the beginning of the 20th century, European and Asian botanical gardens played an important role in research on Araceae. Several years after the publication of Engler's work, a seminal book describing the genera of the Araceae family by Mayo et al (1997) would not have been possible without relying on plants cultivated at Kew Royal Botanic Gardens (England) and Munich Botanic Garden (Germany). In the second half of the 20th century, North American botanical gardens began to play an increasingly important role in Aroid research. Richard Keating
(2003), who made extensive use of the collections of the Munich Botanical Garden and the Missouri Botanical Garden for his book on the anatomy of the Acoraceae and Araceae notes in his acknowledgments: "The existence of living collections of two botanists in particular were vital to conceiving and completing this project. Josef Bogner (Munich) and Thomas Croat (Missouri Botanical Garden, St-Louis) both manage extensive, carefully documented and named living collections which are based on extensive field experience." This is an excellent example that sums up the scientific qualities of a reference collection.

In classical taxonomic studies, living collections often enable us to observe the flowering and sometimes the fruiting of specimens that were not in flower at the time of harvest, thus facilitating the description of new species. Araceae specialist Tom Croat, who manages a collection of over 10,000 specimens at the Missouri Botanical Garden, provides insight on the usefulness of collections for systematic research: "Perhaps the greatest asset is the fact that I can bring back sterile, unknown collections and later study them when they come into flower. Many of these have proven to be new species"; "Pollination in the greenhouse often allows you to study fruits of plants that have never been since in fruit in the wild"; "One of the major ways the collection was essential is that I did breeding studies on *Anthurium* sect. *Pachyneurium* which much to my surprise showed that while the Central American species would cross with one another, as would the South American species, few if any Central American species would cross with South American species. This study would have been impossible without the living collection" (Barabé, personal communication, 2010).

The following examples also illustrate the importance of living collections. *Philodendron scherberichii* was described 10 years later after it flowered from an unidentified specimen of
118 *Philodendron* collected in Colombia in 1995 that was brought into cultivation at the Lyon Botanical Garden (France) (Croat et al. 2007). *Philodendron bicolor* was also described from a wild Peruvian collection once it flowered at the Botanical Garden du Montet (Nancy) in 2001, after 22 years of cultivation (Croat et al. 2012). Similarly, a second Peruvian species, *Philodendron pierrelianum*, was described from a wild source collected in 1980 after its flowering in 2007 in the same garden in Nancy (Croat et al. 2012). In these three cases, the cultivated specimens and their vouchers constitute the holotype of these species.

125 The Aroid collection of the Montreal Botanical Garden (MBG) contains more than 30 genera and 300 species for a total of more than 1,000 specimens. Some species (e.g. *Anthurium jenmannii* and *Philodendron melinonii*) are represented by many specimens that are frequently used in floral exhibits. During the 50's and 60's, the great majority of the aroids were acquired through purchases from plant growers. Some specimens originating from Costa Rica were also sent to the Garden by a plant hunter working there. However, since the 80's, Denis Barabé a botanist who worked at the garden was able to significantly augment the collection with many specimens originating from tropical regions such as the Ivory Coast, the People's Republic of the Congo and Gabon. However, the main core of the collection was collected in French Guiana during field work to study different facets of Aroid biology. This collection was used in conjunction with specimens from the Herbier de Guyane during the preparation of the book *Les Aracées de Guyane Française* (Barabé and Gibernau 2015).

137 Collection-based studies make it possible to compare plants gathered from different environments and to make observations that are often difficult to record in nature. These studies can focus on particular specimens, as in the case of studies of floral development, or on a genus
or an entire family of plants, as in comparative anatomy. Although the Aroid collection at the
Montreal Botanical Garden is not as large as other collections maintained in other botanical
gardens, it has been well used to study various aspects of the biology of Aroids.

Field studies and collecting expeditions are the main sources of material necessary to develop the scientific value of herbaria and botanical gardens (Fig. 1). Without collections from the wild, it is very difficult to conduct comprehensive studies on development, pollination and systematics. Conversely Herbaria and Botanical Garden play an important complementary role to studies performed in the field. As it will be shown below, living collections can even support studies by making biological predictions that can later be tested in the field. In this article, the role of living collections is discussed mainly by focusing on the MBG. However, the authors also used the collections of the Missouri Botanical Garden and Nancy Botanical Garden for specific studies.

The aims of this review using the Araceae as focus family are: (1) to highlight the importance of living collections to conduct botanical research; (2) to identify the inroads that have been made in this family in several contexts ranging from developmental to ecological viewpoints; (3) to highlight features that are noteworthy in this particular taxonomic group; and (4) to outline future areas of exploration that will broaden our understanding of this diverse and complex group.

Systematics - The first study of the molecular systematics of the Araceae, based on chloroplast genes (French et al. 1995) was based mainly on the collections of the Botanical Gardens of Munich, Missouri and Fairchild, but also on a collection assembled by French at Rutgers
162 University. A phylogenetic tree of the Araceae, showing for the first time that the Lemnaceae
163 should be included in this family as an early-diverging clade was also drawn up using material
164 obtained largely from the MBG collections (Barabé et al. 2002c), a result that was later confirmed
165 using more ‘powerful’ sequencing methods (Cusimano et al. 2011; Nauheimer et al. 2012;
166 Henriquez et al. 2014; Haigh et al. 2023) or critically discussed (Tippery et al. 2021). This use of
167 living collections has continued to contribute to the further development of molecular
classifications. For example, molecular phylogenies by Cabrera et al. (2008) and Cusimano et al.
168 (2011) are based on the rich collections at Kew Gardens and the Munich Botanical Garden.
169 Chartier et al. (2014) contributed new sequences of many specimens from the Nancy and Lyon
170 Botanical Gardens to produce a new family molecular phylogeny combining nuclear and
171 chloroplast genes. The most recent and complete (e.g. 111 genera) Aroid phylogenomic tree
172 based on the Angiosperm 353 target genes was also produced mainly from the rich collections of
173 different Botanical Gardens (Royal Kew, Missouri, Nancy and Lyon) and the Sarawak Conservatory
174 Institute (Haigh et al. 2023).
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177 Calcium oxalate crystals - The production of extracellular calcium oxalate crystals is an
178 uncommon phenomenon in vascular plants. Many Araceae produce calcium oxalate crystals
179 mixed with pollen during anthesis. To pinpoint the origin of the crystals, observations must be
180 made on fresh material, at the time of flowering. In the MBG collection, we observed that two
types of extracellular calcium oxalate crystals can be mixed with pollen during flowering:
181 prismatic crystals and raphides (Fig. 2). Some genera (e.g. Philodendron and Xanthosoma)
182 produce both types of crystals simultaneously, while others produce only raphides. A survey of
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184 65 species showed that the early-diverged subfamilies of Araceae contain only raphides, whereas
185 more recent subfamilies may contain both raphides and prismatic crystals (Barabé et al. 2004a).
186 This suggests that the nature of extracellular crystals might have a taxonomic significance across
187 the family. However, a survey of a greater number of species will be necessary to test this
188 hypothesis.

189
190 **Floral anatomy** -- Since the early days of botanical gardens, collections have played an important
191 role in the development of plant anatomy as a discipline. The collections of the MBG have been
192 used to study the vascularization of various genera of Araceae, for example *Calla* (Barabé and
193 Labrecque 1983) *Culcasia* (Barabé and Forget 1992), *Spathicarpa* (Barabé et al. 1986),
194 *Symplocarpus* (Barabé 1982), and *Zamioculcas* (Barabé and Forget 1988). These studies
195 contributed to the interpretation of the floral structures in different genera of Araceae. In *Calla*,
196 the study of floral anatomy showed that the unilocular gynoecium is formed by three carpels
197 surrounded by 10 to 12 stamens. It was hypothesized that 6 of the 12 stamens of *Calla* correspond
198 to the 6 tepals of *Orontium* (Barabé and Labrecque 1983).

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200 **Floral development** -- Similarly to anatomical studies, developmental studies typically require
201 many specimens representing a variety of stages of development. Even though it may not be
202 realistic in many cases, collections can, in certain circumstances, be the only accessible source of
203 plant material available. Additionally, it is possible to harvest inflorescence primordia from certain
204 species without destroying the plant. Our developmental morphology studies of aroid species
205 have benefitted greatly from the availability of materials in botanical garden collections. In a
206 broader context, our work has established the foundation for understanding the mechanisms that
207 lead to the formation of a variety of floral types in aroid species. The nature of the formation of
208 inflorescences in this family allows for non-destructive collection of inflorescences, something
209 that is particularly important when living botanical collections are involved. Additionally, given
210 recent advances in molecular biology, access to collections for phylogenetic studies is feasible,
211 minimizing the amount of plant tissue that needs to be collected.

212 Developmental studies by our group that have made use of aroid species in collections
213 include the following: organogenesis in *Culcasia* and *Cercestis* (Barabé and Bertrand 1996);
214 aspects of floral development in *Philodendron grandifolium* and *Philodendron megalophyllum*
215 (Araceae) (Barabé and Lacroix 2001a); the correlation between development of atypical bisexual
216 flowers and phylogeny in the Aroideae (Araceae) (Barabé et al. 2002c); study of homeosis in the
217 flower of *Philodendron* (Araceae): a qualitative and quantitative approach (Barabé et al. 2002a);
218 development of the flower and inflorescence of *Arum italicum* (Araceae) (Barabé et al. 2003); on
219 the presence of extracellular calcium oxalate crystals on the inflorescences of Araceae (Barabé et
220 al. 2004a); floral development and phylogenetic position of *Schismatoglottis* (Araceae) (Barabé
221 et al. 2004b); development of the flower of *Anthurium jenmanii*: a new element in our
222 understanding of basal Araceae (Barabé and Lacroix 2008a). The studies listed above, in
223 combination with others, have laid down the foundation for a broader understanding of the
224 evolution of the Araceae as well as unique developmental insights that highlight challenge our
225 interpretation of floral morphology.

226 One of the first detailed studies exploring floral development in the genus *Philodendron*
227 that made use of living collections was based specifically on *P. grandifolium* and *P. megalophyllum*
(Barabé and Lacroix 2001a). The basic layout of the inflorescence of this genus consists of pistillate flowers on the lower portion of the inflorescence and staminate flowers on the upper portion. Of particular interest, between the 'male' and 'female' zones of the inflorescence, an area we refer to as intermediate zone consists of sterile male flowers near the upper (fertile/functional) 'male' zone and 'atypical' bisexual flowers near the lower (fertile/functional) 'female' zone. At the level of individual atypical bisexual flowers, staminodes develop facing the male zone and carpels form facing the female zone. This was our first case study of a species within *Philodendron* that we believe to be a case of homeosis where carpels have been replaced with sterile stamen on the SAME whorl of individual flowers. We confirmed this homeotic phenomenon in a variety of other species of *Philodendron*: *P. solimoesense* (Barabé and Lacroix 1999); *P. melinonii* (Barabé and Lacroix 2000); *P. fragrantissimum* (Barabé, et al. 2000); *P. squamiferum* and *P. pedatum* (Barabé et al. 2002a); *P. insigne* (Barabé et al. 2002b); *P. ornatum* (Barabé and Lacroix 2008b); *P. callosum* and *P. billietiae* (Barabé et al. 2008a).

Ontogenetic similarities between atypical bisexual flowers of *Montrichardia* and *Philodendron* supports a taxonomic relationship between these two groups (Barabé and Lacroix 2001b). As in *Philodendron* and *Montrichardia*, atypical bisexual flowers are also visible in *Caladium* during early stages of development but in fewer numbers. 'The undeveloped synandroidal portion and the rudimentary gynoecium belong to the same meristematic unit and can be viewed as a single whorl (Barabé and Lacroix 2002). Interestingly, this ontogenetic similarity is not supported by molecular data. *Montrichardia* seems to be 'basal' to the Aroideae subfamily and doesn't group with the 'Philodendreae' (Haigh et al. 2023 and other molecular phylogenies) which likely represents a convergence.
Another type of bisexual flower in the Aroids, referred to as the *Cercestis* type, consists of a gynoecium surrounded by stamens on a separate whorl. Barabé et al. (2002c) established that "the two developmental patterns of atypical bisexual flowers in Aroideae do not correspond to two separate evolutionary lineages but rather are more or less consistent within clades". The development of female flowers in *Dieffenbachia* has some similarities with atypical bisexual flowers of *Cercestis*. Atypical flowers of *Dieffenbachia* located in the intermediate zone range in morphology from aborted female flowers to rudimentary sterile male flowers with incomplete staminodes (Barabé and Lacroix 2014). Additionally, atypical sterile flowers are present between the male and female zones on the inflorescence of *Schismatoglottis* but they consist only of aberrant male or female flowers unlike atypical bisexual flowers found in *Cercestis* and *Philodendron* (Barabé et al. Gibernau 2004b). In *Anthurium jenmanii*, another pattern of floral development is observed. Tepals and stamens on bisexual flowers are superposed in this species (Barabé and Lacroix 2008a).

The morphological uniqueness of the inflorescence and atypical floral forms in Araceae lend themselves well to molecular studies exploring the origin of, and interaction between floral organ identity genes. Even though they have not been studied using this lens, Aroids may provide further insight into the diversification of organ identity as it pertains to staminodes for example (Appleton and Kramer 2024a,b). Additionally, current molecular comparative studies (differential gene and protein expression patterns) at different scales such as inflorescence architecture and organ identity (Khojayori et al. 2024) could make use of the unique inflorescence and floral patterns in the Araceae to further test how variations in their developmental pathways and their interaction led to novel morphological forms.
272
273 **Pollen-Ovule ratio** - There are several quantitative relationships between floral traits and reproductive systems in plants (Cruden, 2000). For example, self-pollinated plants will have a lower "number of pollen grains/number of ovules per flower" ratio than cross-pollinated plants.
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276 The Araceae family, with its great diversity of flowers and growth patterns, provides an excellent model for studying this question. To determine the nature of the relationships between floral characters, reproductive system and growth habit, we compared different genera of Araceae from the collections of the MBG, the Montreal Biodôme and the Missouri Botanical Garden (Chouteau et al., 2006, 2008). Thanks to living collections, it was possible to compare species living from tropical and temperate regions without having to travel to the field. Of course, such diverse sampling in the wild would only have been possible in the very long term, and at exorbitant cost.
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283 By staying on site, we were able to test various evolutionary hypotheses and show that the quantitative relationships between floral characters vary considerably depending on the taxonomic level and the environment of origin of the plants selected.
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292 In Chouteau et al. (2008) the relationships between floral characters, pollination mechanisms, lifeforms, and habitats were analyzed on 54 species belonging to 32 genera. The authors observed that floral characteristics seem to be correlated with pollinator type, life form, climatic conditions and self-pollination capacity, but not growth form. Life form and climatic region (temperate vs tropical) are factors affecting investment in male and female functions in Aroids. The authors also concluded (p. 39) that "in aroids, the P/O ratio in the breeding systems behaves contrary to that found in other plant groups, suggesting that it may not be linked to the
293 breeding system". This study was complemented by an analysis of types of pollination in relation
294 to specific floral traits (Gibernau et al. 2010, see pollination syndrome section).

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296 **Pollen viability** - - Another area of research in floral biology for which collections are extremely
297 useful is pollen viability. We know that this character is closely linked to the floral cycle (Barabé
298 et al., 2008) and pollination mechanisms. In this respect, collections can be used to supplement
299 data collected in the wild. Longevity represents the period during which the pollen can produce
300 a pollen tube. This corresponds to the viability of the pollen grain (Barabé et al. 2008). By studying
301 French Guiana species in the field, it has been shown that species with a long anthesis (14-40
days), for example *Anaphyllopsis* and *Anthurium*, are linked with a long longevity of the pollen,
302 contrary to species with a short anthesis (2 days), such as *Montrichardia* and *Philodendron*, where
303 there is a short longevity and fast germination (Fig. 3). Given that this hypothesis was based on
304 the study of only six species, we decided to test more taxa. We were able to use the collection of
305 the Montreal Botanical Garden to study pollen viability in other genera such as *Alocasia*,
306 *Anthurium*, *Spathiphyllum*, *Schismatoglottis* and *Xanthosoma*. The results obtained confirm that
307 the pollen of species with bisexual flowers (*Anthurium*, *Spathiphyllum*), which have a longer
308 flowering cycle, has a longer viability than pollen from species with unisexual flowers (*Alocasia*,
309 *Schismatoglottis*, *Xanthosoma*) that have a shorter pollen cycle (S. Montembault, D. Barabé and
310 M. Gibernau, unpublished results). This study clearly demonstrates how living collections
311 complement field studies.
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Relationship between seed size and type of growth -- A general characteristic of epiphytic plants is the small size of their seeds. In all Angiosperms, almost all epiphytic species have seeds smaller than 2 mm in length (Madison 1977; including hemi-epiphytic plants). When comparing the seed size of epiphytic and terrestrial species in *Anthurium*, epiphytic species have seeds ≈ 2 mm long while they measure between 4 and 8 mm long in terrestrial species. This means that the seeds of terrestrial species are nearly 8 to 64 times larger than those of epiphytic species (Madison 1977).

Barabé and Gibernau (2015) calculated the volume of seeds of different species of Araceae from French Guiana using material available at the Herbarium of French Guiana (Barabé and Gibernau 2015). Five groups of species are statistically different from each other in terms of seed volume.

Groups 1, 2 and 3, with large and very large seeds, are terrestrial species with two exceptions: *Heteropsis flexuosa* (group 1) and *Syngonium podophyllum* (group 3). Groups 4 and 5 with small and very small seeds are epiphytic or hemi-epiphytic plants except for *Dieffenbachia paludicola* (group 4). This supports Madison's hypothesis that epiphytic and hemi-epiphytic plants have small seeds. On the other hand, the opposite is not always true: not all epiphytic or hemi-epiphytic species have small seeds, as shown by the presence of large seeds in *Heteropsis flexuosa* (group 1), a hemi-epiphytic plant, and *Anthurium jenmanii* (group 4), an epiphytic plant whose seed volume is close to that of terrestrial species such as *Anthurium sagittatum* and *Dieffenbachia paludicola*. The smallest seeds are found in the genus *Philodendron*, whose flowers have many ovules. Generally speaking, the greater the number of ovules per flower, the smaller the seeds.

In species with a small number of ovules, the seeds tend to be larger, as is the case in *Anaphyllopsis* and *Heteropsis* (group 1), where the fruits contain one and one to four seeds respectively. On the other hand, in the genera *Philodendron* and *Rhodospatha* (group 5), whose
336 flowers contain dozens of ovules, the seeds are the smallest. However, this relationship is not
337 valid for all genera since in *Anthurium*, where the fruits have 2-4 seeds depending on the species,
338 four species were found to belong to group 5 with the smallest seeds. Finally, it is not possible
339 with these data to directly link the mode of growth and the volume of the seeds since terrestrial
340 and hemi-epiphytic plants have seeds ranging from voluminous (*Anaphyllopsis*, *Heteropsis*) to
341 more or less small (*Anthurium sagittatum*, *Monstera obliqua*).

342 Small seeds offer advantages for dispersal and germination. Plants that produce small
343 seeds can produce large numbers of seeds for a similar amount of energy expenditure as plants
344 producing only a few large seeds. Epiphytic plants require a specific environment for seedling
345 development; reproductive success is ensured by saturating the potential growing areas with
346 many small seeds, some of which will find a suitable environment for growth (Madison 1977).
347 Tree bark presents small cracks in which the accumulation of humus provides a suitable
348 germination environment for small seeds (Madison 1977). Thus, the probability of finding a
349 suitable germination site on a tree is greater for small seeds than for large seeds. Small seeds also
350 have a greater surface area to volume ratio than large seeds. Therefore, with a similar
351 permeability rate, they will imbibe water more rapidly than larger seeds. This may be critical for
352 survival in environments where water availability is often intermittent and brief. In epiphytic
353 species that have larger seeds, the seeds are enclosed in mucilage, which may serve to increase
354 the imbibition rate (Madison 1977) or allow germination in the fruit, a phenomenon that is
355 common in Araceae. Finally, the seeds of epiphytic plants do not go dormant; if they fall into a
356 favorable environment, they will germinate immediately. Most epiphytes live in environments
357 where there is sufficient moisture to germinate at any time of the year, so dormancy is not
necessary to survive a dry season (Madison 1977). Testing the relationship between seed size and type of growth represents another example that supports the vast potential of collections to provide data that would otherwise need to be acquired for a wide array of species through field work.

**Thermogenesis** -- In some families of flowering plants (e.g. Annonaceae, Araceae, Cyclanthaceae, Magnoliaceae, ...) and Gymnosperms (Zamiaceae), the temperature of the flower, inflorescence or cone, as the case may be, can rise high above ambient temperature during anthesis in relation to pollination (Seymour 2010). In the tropical species *Philodendron solimoesense*, for example, the temperature can rise to 14°C above ambient. In *Symplocarpus foetidus*, a species native to Québec, which flowers early in spring, there can be a 40° C difference between inflorescence temperature and ambient temperature. Floral thermogenesis was discovered in *Arum italicum* by Lamarck in 1777 (Leick 1915), and Araceae is probably the richest family in terms of thermogenic plants. In his seminal article, Leick (1915) made a review of more than one century of floral thermogenesis studies in Araceae with extensive use of the European collections from tropical genera. Several genera were studied (*Alocasia*, *Anthurium*, *Arum*, *Caladium*, *Colocasia*, *Dracunculus*, *Monstera*, *Philodendron*, *Pothos*, *Sauromatum*, *Schismatoglottis*, *Typhonium*, *Zantedeschia*) and some such as *Anthurium* or *Pothos* were found not to be thermogenic.

Thermogenesis can easily be studied using living collections, as they allow plants with different flowering cycles to be compared *ex situ*. For example, the thermogenesis of *Amorphophallus titanum* has been described in detail using specimens from the Botanical Garden of the University of Bonn (Barthlott et al. 2008). It is also possible to compare in detail the thermogenetic patterns
380 from several species of a same genus; *Monstera*, *Philodendron*, and *Syngonium* species were studied from the collections of MBG (Barabé and Gibernau 2000, Chouteau et al. 2007, 2009).

381 But is the physiology of a tropical plant grown in a greenhouse in Montreal comparable to that of a plant in nature? We compared the thermogenetic cycle of plants growing in their natural environment with those cultivated in greenhouses. For example, specimens of *Philodendron melinonii*, collected in 1987 in French Guiana and grown in MBG greenhouses since that time, show ~10 years later the same thermogenetic cycle as those growing in their natural environment (Gibernau et al. 2000). This indicates that the thermogenetic pattern is an endogenous process that can be analyzed on plants grown outside their natural habitat.

389 Based on plants grown at MBG, we have built a theoretical model across different genera showing a quantitative relationship between the volume of the thermogenic zone of the spadix and the maximum of the temperature difference between the inflorescence and ambient air (Gibernau et al. 2005). We showed that the increase in the temperature difference between the spadix and ambient air appears to be physically constrained and corresponds to the value of a thermal model of heat conduction in an insulated cylinder with an internal heat source. In the model, we applied the average aroid heat metabolic rate for the different species, but it can vary among species as shown by respirometry approaches (Seymour 2010).

397 Floral thermogenesis is a floral trait closely associated with pollination and can be an appropriate indicator of the pollination mechanism. For example, the thermogenetic pattern of the genus *Syngonium* was studied for the first time by using living collection of the MBG and the Biodome of Montreal. In regard to the diverse thermogenic patterns observed in the genus, Chouteau et al. (2007) were able to hypothesize the existence of a particular pollination
mechanism in *Syngonium angustatum*. In fact, this species had a thermogenic sequence characterized by four temperature increases occurring during the day contrary to the crepuscular biphasic thermogenic pattern of *Syngonium schottianum* (section *Cordatum*) similar to what is observed in the genera *Caladium* and *Philodendron* which are both pollinated at night by beetles (Gibernau 2011). Based on these differences, the authors hypothesized the *S. angustatum* is pollinated by an unknown pollinator during daylight (Chouteau et al., 2007). Recently Etl et al. (2022) showed that *Syngonium hastiferum* is pollinated diurnally by *Neella* plant bugs (Miridae; Heteroptera) and wrote (p.7): "Another representative of the genus *Syngonium*, *S. angustatum*, was previously studied in greenhouse by Chouteau et al. (2007). It was found to have a similar thermogenesis pattern as *S. hastiferum*, which led the authors to suggest that *S. angustatum* is possibly pollinated by unknown, diurnal pollinators rather than by the usual nocturnal Cyclocephalini scarab beetles. *S. angustatum* also has echinate pollen grains (Grayum 1990) and, like *S. hastiferum*, is native to Costa Rica (Hammel et al. 2003). Thus, this species may also be pollinated by plant bugs, but its pollination system remains to be investigated and documented in the field". This study of *Syngonium*, made both in greenhouses and in the field, shows the predictive value of observations made on living collections.

**Pollination syndromes** - Araceae are mainly pollinated by insects and this type of interaction may lead to a process of specialization/adaptation of aroid inflorescences (Mayo et al. 1997; Gibernau 2003, 2011, 2016, Diaz et al. 2019). In fact, most of the Araceae seem to have quite a specific or specialized pollination system which can be broadly divided into three types: bee, beetle, and fly (Gibernau 2003, 2011). The first type occurs in the Neotropics within the genera
424 *Anthurium* Schott and *Spathiphyllum* Schott (Schwerdtfeger et al. 2002, Hentrich et al. 2010),
425 which are pollinated by male euglossine bees collecting odoriferous substances in a way very
426 similar to orchids (Diaz et al. 2019, see Etl et al. 2017 for a non-euglossine oil collector) or pollen
427 collecting bees (Hartley and Gibernau, 2019). Note that in the megagenus *Anthurium* (>1,000
428 species) other kinds of pollinators such as *Thrips*, small curculionid beetles, Lepidoptera, gall-
429 midges or hummingbird have been documented (Cuartas-Hernandez and Medel 2015, Hartley et
430 al. 2017, Bleiweiss et al. 2019, Cuartas-Hernandez et al. 2019, Hartley and Gibernau 2019, Etl et
431 al. 2022, Cano et al. 2024). The second type of specialized system is beetle-pollination. This
432 pollination system is widespread within the Araceae and present in several subfamilies involving
433 different genera and families of beetles (review in Gibernau 2003, 2011, 2016). The third type of
434 specialized system is fly-pollination. This interaction is mainly represented by one Asian fly genus,
435 *Colocasiomyia* (Drosophilidae), which pollinates Asian genera belonging to different subfamilies
436 (Fartyal et al. 2013, Shi et al. 2019, Takano et al. 2021). One notable exception is a chloropid fly
437 which is the only obligate pollinator of *Peltandra virginica* in North America (Patt et al. 1995).
438 Generalist pollination systems involving various insects are rare and documented for *Lysichiton
439 camtschatcense* Schott (Tanaka 2004) and *Symplocarpus* species Schott (Uemera et al. 1993,
440 Barriault et al. 2021). In addition to the mutualistic interactions cited above, deceit pollination
441 systems also exist in several genera of Araceae. The inflorescence dupes the pollinators by
442 mimicking its laying sites (faeces, mushrooms, dead animal, etc.). Attracted insects, mainly
443 females, perform pollination but without receiving any reward (Gibernau 2003, Chartier et al.
444 2014).
Through coevolutionary processes, many floral characters became adapted to pollinators resulting in different types of floral morphologies adapted to different categories of pollinators (e.g. pollination syndromes, Fenster et al. 2004). Pollination syndromes can also be studied from collections in order to predict a probable (unknown) pollinator. We investigated this question by measuring about fifteen quantitative floral characters in 68 Araceae species belonging to 41 genera, most of them from the Aroid collections of the Montreal, Kew and Nancy Botanical Gardens (Chouteau et al. 2008, Gibernau et al. 2010). A discriminant analysis of floral characters showed five main types of morpho-functional syndromes associated with pollinators: Coleoptera, Diptera, Hymenoptera, Generalist, and a mixed system with Coleoptera and Diptera (Gibernau et al. 2010, Barabé and Gibernau 2015). Interestingly, deceptive pollination systems were grouped with mutualistic ones based on the type of pollinator. This question was further studied within an evolutionary framework using a phylogenetic approach. By mapping the pollinator type and the nature of the interaction on a phylogenetic tree, Chartier et al. (2014) were able to hypothesize the ancestral aroid-pollinator interaction and showed that these interactions have changed repeatedly during the evolution of the Araceae family, for example several evolutions (e.g. convergence) of beetle-pollination in different aroid groups. Moreover, these pollinators 'changes' were correlated with modifications (e.g. adaptation) of some floral traits, indicating correlated evolution (Chartier et al. 2014).

463

464
465 **Conclusion**

466

467 Our examples, within the context of Araceae show that living collections of Aroids are
468 used extensively for research in different countries; many scientific studies are a direct result of
469 the existence of collections that are also used for educational and aesthetic purposes. The
470 Araceae represents a model for comparative studies for the several reasons: the broad vegetative
471 diversity of the group, the high number of genera with few species, the high amount of floral
diversity (even on the same inflorescence), the rich taxonomical history and delimitation between
472 genera, as well as the existence of very comprehensive collections around the world.
473

474 Our examples show the importance of living collections for anatomical, morpho-
475 physiological and developmental studies. Often these collections make it possible to undertake
476 studies that could not have been conducted otherwise. They are especially useful in cases where
477 observations must be performed during the flowering period. However, there are some
478 constraints on the use of collections, particularly for developmental studies. Such studies often
479 require large quantities of material that cannot always be obtained from collections. For example,
480 in the case of rhizomatous (e.g. *Anchomanes*) or tuberculous plants (*Amorphophallus*,
481 *Dracontium*), few botanical gardens would agree to sacrifice their specimens to provide samples
482 to document all stages of development. Complementary sampling must generally be conducted
483 in the field in such cases. Nonetheless, each botanical garden has its own history and mission.
484 The use of a particular collection should be integrated in the general purpose of a botanical
garden.
485
The maintenance of collections represents a significant financial investment by private or government organizations. Unfortunately, this investment is often insufficiently recognized by grant programs. Yet, collections have more than an educational or ornamental value. They represent a scientific richness for the future. They also represent a reservoir of uncommon morphologies, genetic material, and rare specimens. On the other hand, collection-based research also has a direct impact on the development of living collections and their use for educational and horticultural purposes. For example, research allows for a better identification of specimens, the acquisition of rare and spectacular specimens, and the use of collections in education. Highlighting the value of living plant collections for research certainly constitutes an important aspect of a country's scientific development. In this context, we hope many Aroid researchers will be able to participate actively in the use of living collections of Araceae embellishing our botanical gardens.

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