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Year:2017
Resistanceoftropicalseedlingstodroughtismediatedbyneighbourhood
diversity
O’Brien,MichaelJ;Reynolds,Glen;Ong,Robert;Hector,Andy
DOI:https://doi.org/10.1038/s41559-017-0326-0
PostedattheZurichOpenRepositoryandArchive,UniversityofZurich
ZORAURL:https://doi.org/10.5167/uzh-140576
JournalArticle
AcceptedVersion
Originallypublishedat:
O’Brien,MichaelJ;Reynolds,Glen;Ong,Robert;Hector,Andy(2017).Resistanceoftropicalseedlings
todroughtismediatedbyneighbourhooddiversity.NatureEcologyandEvolution,1(11):1643-1648.
DOI:https://doi.org/10.1038/s41559-017-0326-0
Resistance of tropical seedlings to drought is mediated by neighbourhood diversity 1
Michael J. O’Brien
1,2,3
, Glen Reynolds
2
, Robert Ong
4
and Andy Hector
5
2
1
Estación Experimental de Zonas Áridas, Consejo Superior de Investigaciones Científicas, 3
Carretera de Sacramento s/n, E-04120 La Cañada, Almería, Spain 4
2
Southeast Asia Rainforest Research Partnership, Danum Valley Field Centre, PO Box 5
60282, 91112 Lahad Datu, Sabah, Malaysia 6
3
URPP Global Change and Biodiversity, University of Zurich, Winterthurerstr. 190, 8057 7
Zurich, Switzerland 8
4
Forest Research Centre, Sepilok, 90715 Sandakan, Sabah, Malaysia 9
5
Department of Plant Sciences, University of Oxford, OX1 3RB UK 10
*Correspondence author e-mail: mikey.j.obrien@gmail.com 11
Title: 82 characters 12
Abstract: 201 13
Main: 1999 14
Refs: 40 15
Figures: 4 16
Occasional periods of drought are typical of most tropical forests, but climate 17
change is increasing drought frequency and intensity in many areas across the globe 18
threatening the structure and functioning of these ecosystems. However, the effects of 19
intermittent drought on tropical tree communities remain poorly understood and the 20
potential impacts of intensified drought under future climatic conditions are even less 21
well known. The response of forests to altered precipitation will be determined by the 22
tolerances of different species to reduced water availability and the interactions among 23
plants that alleviate or exacerbate the effects of drought. Here we report the response 24
of experimental monocultures and mixtures of tropical trees to simulated drought that 25
reveal a fundamental shift in the nature of interactions among species. Weaker 26
competition for water in diverse communities allowed seedlings to maintain growth 27
under drought while more intense competition among conspecifics inhibited growth 28
under the same conditions. These results show that reduced competition for water 29
among species in mixtures mediates community resistance to drought. The delayed 30
onset of competition for water among species in more diverse neighbourhoods during 31
drought has potential implications for the coexistence of species in tropical forests and 32
the resilience of these systems to climate change. 33
Many types of tropical forests are characterized by constant temperature and 34
humidity, typically experiencing regular rainfall evenly distributed throughout the year. 35
However, rain forests often experience infrequent droughts, during El Niño Southern 36
Oscillation (ENSO) years for example, although the effect of these events on forest structure 37
and functioning is poorly understood
1,2
. On the one hand, drought could increase the success 38
of some species putting them at an advantage, increasing dominance and potentially 39
decreasing diversity
3
. Alternatively, drought could promote diversity by enhancing density-40
dependent mechanisms that favour uncommon species
4
. For example, drought may increase 41
intraspecific competition for light, water and associated soil resources or predispose trees to 42
pathogen infection or insect attack
5–7
, both density-dependent mechanisms that can influence 43
community diversity
8–10
. 44
Although light is usually considered the most important resource gradient driving 45
species distributions in tropical forests
7
, climate change is projected to increase the severity 46
and frequency of drought for substantial areas of tropical forest
1,11
thereby increasing the 47
importance of water limitation as a driver of species distributions
12
. These changes pose a 48
potential risk to these hyper-diverse ecosystems due to negative effects on reproduction
13
, 49
recruitment
13
, growth
3,14
and survival
3,15
. Species diversity may provide an insurance effect 50
against these alterations and provide stability under drought conditions
16,17
because species 51
vary in their resistance and resilience to severe climatic disturbances
3,18
. Although, if 52
conditions go beyond the physiological limits of even the tolerant species, then large-scale 53
mortality will occur regardless
19
. However, there is limited empirical evidence regarding the 54
direction and magnitude of the interactions between drought and tree diversity as research has 55
largely focused on shifts of species distributions and functional composition
12,15,20
. 56
Here we test how drought affects interactions among tropical tree seedlings in 57
monocultures and mixtures of different species. We used rainfall-exclusion shelters to reduce 58
soil water availability while altering tree seedling diversity by manipulating neighbourhood 59
richness around focal individuals (Fig. 1). Ecological theory predicts that competition for 60
limited resources is more intense when species and individuals are more similar and closely 61
related
21,22
. Therefore, neighbourhood diversity consisted of three treatments in which a focal 62
individual was surrounded by 3 individuals of the same, or 3 different, species as follows: 1) 63
a focal seedling surrounded by seedlings of 3 different species than those used as the focal 64
species (mixtures), 2) monocultures of a focal seedling surrounded by 3 seedlings originating 65
from a different mature tree of the same species (non-sibling) and 3) monocultures of a focal 66
seedling surrounded by 3 seedlings originating from the same mature tree as the focal 67
seedling (sibling). The third neighbourhood represents the dense aggregated seedling 68
communities that form under mature trees after mast seed production, a common 69
reproductive strategy in these ever-wet tropical forests
23
. We used the rainfall-exclusion 70
shelters for two intervals lasting 3 and 6 months over a two-year period in order to simulate 71
drought intensity similar to supra-annual droughts in Malaysian Borneo
24
(Fig. 2). We 72
monitored focal seedling growth and mortality and quantified the magnitude of drought 73
response in leaf physiology while assessing nutrient concentrations to test if drought 74
increased competition for water and nutrients. 75
Results 76
We found an interaction between the drought and diversity treatments in which the 77
strength of competition was related to seedling neighbourhood diversity under drought but 78
not ever-wet conditions (Fig. 3a). Specifically, in the monocultures (i.e. sibling and non-79
sibling treatments) relative growth rate (RGR) was significantly lower in the drought than in 80
the ever-wet treatments, but seedlings in mixtures had RGRs that were statistically 81
indistinguishable under drought and ever-wet conditions (Fig. 3b; Supplementary Table 1). 82
These results are consistent with reduced competition for water in species mixtures relative to 83
monocultures. Furthermore, average RGR over all species under drought was higher in 84
mixtures than in monocultures (reduction in RGR due to non-sibling competition = -0.06 cm 85
cm
-1
yr
-1
, -0.1 to -0.02 and reduction in RGR due to sibling competition = -0.04 cm cm
-1
yr
-1
, 86
-0.07 to 0.003). These results indicate that overall mixtures and monocultures are 87
significantly different under drought (see significant contrast × rainfall term in 88
Supplementary Table 1), but the sibling treatment is only marginally different from the 89
mixture (see neighbor × rainfall term in Supplementary Table 1). Although mortality was not 90
