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Tree architecture and functioning facing multispecies
environments: We have gone only halfway in fruit-trees
Pierre-Éric Lauri
To cite this version:
Pierre-Éric Lauri. Tree architecture and functioning facing multispecies environments: We have gone
only halfway in fruit-trees. American Journal of Botany, Botanical Society of America, 2021, 108 (1),
pp.3-7. �10.1002/ajb2.1598�. �hal-03108808�
ON THE NATURE OF THINGS: ESSAYS
New Ideas and Directions in BotanyTree architecture and functioning facing multispecies
environments: We have gone only halfway in fruit-trees
Pierre-Éric Lauri1,2
Manuscript received 31 August 2020; revision accepted 24 November 2020.
1 ABSys, Univ Montpellier, CIHEAM-IAMM, CIRAD, INRAE, Institut Agro, Montpellier, France 2Author for correspondence (e-mail: pierre-eric.lauri@inrae.fr)
Citation: Lauri, P.-É. 2021. Tree architecture and functioning facing multispecies environments: We have gone only halfway in fruit-trees. American Journal of Botany 108(1): 3–7. doi:10.1002/ajb2.1598
KEY WORDS agroecology; agroecosystem; agroforestry; biodiversity; biotic and abiotic environment; forest; forest tree; orchard.
Plant architecture analysis aims at deciphering the relative roles of endogenous processes and exogenous above- and belowground factors in the morphological development and functioning of a plant. In their seminal book on tropical trees and forests, Hallé et al. (1978) considered a few simple plants traits such as branch orienta-tion and posiorienta-tion of sexuality and established the main concepts of plant architecture: architectural unit as the basic growth strategy of a plant, architectural model as the growth pattern that determines the consecutive architectural phases, and reiteration as the repeti-tion of a part or the whole of the architectural unit. These concepts were applied on a wide range of biological types, herbs, shrubs, and trees (Bell, 2008) including extinct forms (Chomicki et al., 2017). Hallé and co-workers (1978) were envisaging two complementary and consecutive phases in architectural studies. The first was “to re-move [the tree] from its natural habitat and study it in isolation… Isolated in this way one can study the tree from the point of view of the geneticist and developmental morphologist” (p. VIII). The second phase was to “return to the forest, away from our optimized environment which has been so productive of new information… Now we can ask the question, how, in fact, does it grow in the vigor-ously competitive environment of the forest itself?” (p. IX).
The focus of this essay will be on trees grown commercially for fruit, hereafter referred to as fruit trees, which are characterized by a unique pattern of biomass allocation compared to the trees native in forests, hereafter referred to as forest trees, whether grown for
timber or not, with more carbon allocated to reproductive growth in the former compared to the latter (Lauri et al., 2019). I depart from the fact that, unlike what was developed for forest trees, the imple-mentation of architectural concepts for fruit trees largely remains at the first phase of architectural studies promoted by Hallé et al. (1978). That is, studies are mostly focused on endogenous processes governing tree growth and functioning, and we lack knowledge of the responses of fruit trees in complex systems that include more competitive interactions with neighboring plants. I assert that this lack of knowledge is related to the way the fruit tree is conceptu-alized—as a tree selected by the breeder and manipulated by the farmer to fulfill the objective of fruit production in artificial and simplified agrosystems. With the ongoing trend toward more biodi-versified agrosystems, there is an urgent need to develop studies on how complex environments affect the endogenous processes gov-erning fruit-tree architecture and functioning and eventually fruit production.
FOREST TREE ARCHITECTURE AND FOREST DYNAMICS
The two phases of architectural studies put forward by Hallé et al. (1978) are well documented in forest trees, which can be classified in three dif-ferent classes with distinct sylvigenetic roles: the “tree of the future” con-forms to its architectural model but has a high capacity for reiterating its
ON THE NATURE OF THINGS: ESSAYS Amer ican Jour nal of B otany
4 • Fruit-tree architecture and functioning in multispecies environments—Lauri • Volume 108, January 2021 NEWS & VIEWS
whole architecture and occupies the densely shaded lower forest strata, whereas the “tree of the present”, which is characterized by strong “arbo-rescent” reiteration, often thrives at the top of the forest canopy. Eventually, the frequently damaged “tree of the past” has lost its ability to reiterate and will soon die. Similar tree and forest growth phases were identified in traditional tropical agroforests where “plants with potential production”, “plants in actual production”, and “plants in decaying production” were characterized by their architecture and agronomic potential (Michon et al., 1983). In those agroforests, the need to combine an architectural and a functional view, i.e., the vertical and horizontal structures and the ecological and agronomic roles, of the individual tree is at the core of whole-system management including animal (grazing) and human (plantation density, pruning) actions (Fig. 1; van Noordwijk et al., 2019).
FROM CONVENTIONAL AGROSYSTEMS TO FRUIT-TREE AGROECOSYSTEMS
When ecological and agronomic aspects are considered together, a main lever on which new agricultural systems are envisioned is the
use of cultivated (i.e., productive) and asso-ciated (i.e., unintentional and/or nonpro-ductive) plant diversity, combining various plant types (annuals, shrubs or trees) with sought-after functional traits (e.g., ni-trogen-fixing plants, plants attractive to predators or repulsive to plant enemies). Therefore, conservation and restoration of biodiversity is a main pillar of sustainable agricultural development encompassing good management of land-use and food systems. These considerations, inspired by the biodiversity–ecosystem function (BEF) that was developed in the field of commu-nity ecology, led to the promotion of biodi-versity-based farming systems (Duru et al., 2015). Designing such agroecosystems im-plies better integration of agroecological concepts that rely on the functioning of the whole agroecosystem and especially on the use of ecological processes involved in pest and disease regulation and in mineral recycling. Although mostly developed on annual-based agroecosystems, agroecolog-ical approaches are now promoted in fruit-tree-based systems (Simon et al., 2017).
ARCHITECTURE AND FUNCTIONING OF THE FRUIT TREE
Most of the knowledge of architecture and functioning of the fruit tree was developed with the aim of analyzing genetic diversity of tree shape and fruit production (Lauri and Laurens, 2005) and de-ciphering genetic mechanisms underlying architectural (Hollender and Dardick, 2015) and functional (e.g., hydraulics; Lauri et al., 2011) traits. These studies contributed to the development of func-tional structural plant models (FSPM) aimed at integrating relation-ships between plant architecture and physiological functions that ultimately underlie growth and development (Boudon et al., 2020). From an applied point of view, such studies are also at the origin of novel architectural-based fruit-tree management proposals in or-chards (Lauri, 2019). However, while a few studies examined whole-fruit-tree physiology, e.g., light-use efficiency and net primary production of shaded coffee plants in agroforestry (Charbonnier et al., 2017), the relationship between architecture and functioning of fruit trees has rarely been examined in multispecies systems (Fig. 2A). When such work is done, it is most often restricted to young FIGURE 1. Traditional multilayered cocoa-agroforestry system in Cameroon including from top to
bottom, trees grown as shade trees for wood and medicinal products (top layer with large reiterative branches), for fruit (avocado or cola nuts; top-medium layer) that are overtopping oil palm trees, and citrus and cocoa trees (medium layer). The medium layer typically comprises the three categories of productive plants identified by Michon et al. (1983). Image credit: P. É. Lauri.
FIGURE 2. Studies on architecture and functioning of the fruit tree. Apple (Malus domestica Borkh.) is taken as example. (A) Frequency of studies on
architecture and functioning (A&F) in five Web of Science (WOS) categories (Plant Sciences, Horticulture, Agronomy, Forestry, Ecology) from 1900 to 2020, without interactions with the environment (“apple A&F”), and considering interactions with abiotic (“apple A&F X abiotic”), biotic (“apple A&F X biotic”) and both abiotic and biotic (“apple A&F X abiotic X biotic”) environment. The query includes all document types in the WOS database. WOS key words in queries: for “apple A&F”: “plant architecture OR *physiology OR development OR growth OR flowering"; for “abiotic”: “temperature OR light OR humidity OR VPD OR water OR wind OR abiotic”; for “biotic”: “plant assemblage OR multispecies OR plurispecies OR ecosystem* OR agrosyst* OR agroecosystem* OR agroforest* OR intercrop* OR alley crop* OR biotic”. (B) Research on apple architecture and functioning is highly dependent of the agrosystem in which apple is cultivated. From bottom to top: Endogenous processes governing vegetative and reproductive growth are well studied in conventional monocropping (a single species and often a single cultivar) agrosystems; effects of the abiotic environment are mostly investigated in experiments on young trees with simple architecture, with a focus on a single environmental variable. There are still few studies on biodiversified agroecosystems that combine various fruit-tree species and/or cultivars with associated plants from various biological types.
1 Modality Research progression Effects of the environment Bio c Poorly developed
Apple-tree - based agroforestry system (Image credit: P.É. Lauri)
Abio c Par ally
developed
Effect of water stress Effect of lack of winter chilling (Image credit: P.É. Lauri) (Image credit: J.D. Schmitz) Endogenous
processes Vegeta ve growth Well developed
Gene cs of tree architecture and func oning on progenies or cul vars in intensive agrosystems (Image credit: P.É. Lauri)
Reproduc ve
growth Well developed
A
apple A&F 64%
apple A&F X abio c 33% apple A&F X bio c
1% apple A&F X abio c X bio c2%
ON THE NATURE OF THINGS: ESSAYS Amer ican Jour nal of B otany
6 • Fruit-tree architecture and functioning in multispecies environments—Lauri • Volume 108, January 2021 NEWS & VIEWS
unproductive trees or, when the work is done over several years, restricted to one environmental factor (Fig. 2B).
This poor knowledge of how fruit trees behave in multispecies en-vironments is likely related to the way fruit trees are currently grown in the paradigm of intensive agriculture. In this scheme, the agrosys-tem is reduced to the agronomic plant itself and the soil as physical support. It involves well-known principles: monocropping, standard-ized tree-shape management, and the use of fertilizers, water, and pesticides (Fig. 3). These principles were put forward during the 19th century but have been considerably extended since the Second World War to increase food production through the combination of high investment in agricultural research, especially crop genetic improve-ment, infrastructure, policies, and market development (Lauri and Simon, 2019). Intensive agriculture is considered as nonsustainable with well-identified adverse effects: exhaustion of natural resources, pollution, desertification, and global warming (Brundtland, 1987).
RESEARCH AGENDA TO SUPPORT FRUIT-TREE-BASED AGROECOSYSTEMS
Two main research routes should help reconcile fruit-tree culture and agroecology, diversified system design and genetics of plant architec-ture. At the system scale, the conventional way to design an orchard is to fit various pieces together considering the fruit tree itself (culti-var and rootstock if any), planting density, tree arrangement, support system, and tree and branch management over consecutive years. In this context, architectural analysis mainly contributes to improving tree and branch management methods, aimed at controlling the reg-ularity and quality of fruit production (Lauri, 2019). In a diversified system, these principles are only partly relevant. Here, not only the choice of the fruit-tree species and the cultivar, but also the compo-sition and spatial arrangement of fruit trees and associated plants are key elements to provide the expected services in the long term. However, further diversifying the system by integrating other trees for timber, firewood, or medicinal use, as done in multistrata tropical agroforestry systems for example (Saj et al., 2017), challenges the way
fruit-tree-based systems can be designed in the temperate zone without compro-mising fruit production. Ongoing research shows that the longevity of fruit trees in-volves considering the consecutive stages of fruit-tree growth, from the nonbearing to the bearing stages, with specific tree and branch management strategies that directly entail agronomic performances (Simon et al., 2017).
From the genetic point of view, Litrico and Violle (2015), working on annuals, propose to develop knowledge of pro-cesses underlying the coexistence of species or genotypes in the system (“ideo-mixes”) to provide breeders with traits that permit creation of productive and sustain-able multispecies or multigenotype mix-tures. In fruit-tree-based agroecosystems, the knowledge and control of biotic inter-actions with neighbors, valorizing niche partitioning, for example, belowground (Hafner et al., 2020) and aboveground (Jagoret et al., 2017), is essential. Moving beyond investigation of the endogenous controls of productivity of fruit trees in conventional agrosystems, we now need to get a deeper view on how and to what extent changes in the biotic environment that affect carbon metab-olism and allocation are directly related to fruit tree architecture. As stressed for forest trees (Hartmann et al., 2020), we need more insights on the respective role of source vs. sink limitation and on prioritization among sinks including C storage. Those approaches are especially relevant to fruit trees in multispecies agroecosystems where shade is a main driver of plant growth and functioning with strong effects on resource partitioning among the various tree com-ponents, such as branch length and distribution, and relationships between vegetative growth and flowering. Such work has the poten-tial to better predict fruit production (e.g., apple; Pitchers et al., 2021) or the dynamics of disease (e.g., coffee; Motisi et al., 2019).
ACKNOWLEDGMENTS
I thank Pamela Diggle for encouraging me to write this essay and a reviewer for helpful suggestions on a previous version of this paper. I am indebted to Pr Francis Hallé for making me discover the invari-ant rules governing plinvari-ant architecture and to Jean-Marie Lespinasse for his insights into the genetic diversity of fruit-tree species and the science of tree and branch management.
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