Phylogenetic relatedness and competition: a pot experiment with semiarid tree species

ABSTRACT

Background:

Factors determining the coexistence of species have been recognized since Darwin, but empirical studies have brought the relationship between niche similarity and competition into question. Knowing the mechanisms of coexistence makes it possible to predict biological invasions and determine better species combinations for the restoration and recovery of degraded areas. The aim of this study was to test the competition-relatedness hypothesis for semiarid tree species. Thus, an experiment was carried out with a phylogenetic gradient of tree species, planted in pairs. The phylogenetically closest pair consisted of congeneric species of the same clade, the intermediate pair comprised congeneric species of distinct clades, and the more distant pair were species of the same family.

Results:

Our results show that the phylogenetically closest and the more distant pairs corroborated the competition-relatedness hypothesis, but the presence of one species with high competitive ability in the intermediate pair caused an unexpected pattern.

Conclusion:

Niche differences are important for coexistence, but it is necessary to know the competitive ability of each species and the specific associations that are more productive to improve the efficiency of restoration programs and to reveal the degree of aggressiveness in the case of invasive species.

Keywords:
functional traits; facilitation; Cordia oncocalyx; Cordia glazioviana; Mimosa tenuiflora; Mimosa caesalpiniifolia; Libidibia férrea; Poincianella bracteosa

HIGHLIGHTS

Close phylogentically tree species from the semiarid region have functional similarities.

Close phylogenetically related tree species compete more than distant species.

Phylogenetically distant species show facilitative interaction.

Competitive ability must be considered to determine the effects of species interactions.

INTRODUCTION

Over time, ecologists have attributed the maintenance of biological diversity to mechanisms that limit niche overlap ( MacArthur; Levins, 1967; Webb et al.,2002 ; Cavender-Bares et al., 2009 ; Kraft et al., 2015 ). This diversity enables coexistence and reduces the probability of competitive exclusion, ensuring that each species exhibits preferences for specific resources, in such a way that they will be more limited by intraspecific competition than by competition with individuals of other species ( Chesson, 2000).

Based on theories that involve niche similarity and increased competition, one recurrent hypothesis is that closely related species are less likely to coexist due to considerable functional similarity ( Webb et al., 2002 ; Cahill et al., 2007 ; Cavender-Bares et al., 2009 ). This hypothesis, known as the competition-relatedness hypothesis (CRH), assumes that there is conservatism of functional traits along a lineage, making functionally related species more similar than phylogenetically distant species ( Webb et al., 2002 ). Here, functional similarity means similar traits in resource acquisition and use, which leads to niche overlap and competition.

Studies have already been carried out to test the CRH, and divergent results have been found. While some studies corroborate the CRH ( Straus et al., 2006 ; Maherali, Klironomos 2007; Violle et al., 2011 ), others have found that competition was more intense between distant taxa than between closely related taxa ( Cahill et al., 2007 ; Narwani et al., 2013 ; Alexandrou et al., 2015 ; Lyu et al., 2017 ). The results depended on the species group selected: in species with similar competitive ability, coexistence depended only on the niche differences, so that closely related species and those with more similar niches competed more. On the other hand, when the species group selected included one or more species with high competitive ability, coexistence also depended on competitive ability, and the highly competitive species suppressed the others, closely related or not ( Mayfield, Levine 2010; Cahill et al., 2007 ). Superiority in competitive ability is evident in different traits related to rapidity and the efficiency of light and soil resource acquisition, i.e., traits related to high growth rates ( Godoy 2019).

However, evolutionary relatedness may not be the only explanation for species to share functional traits. They are also influenced by abiotic factors, which select for traits that are better adapted to the physiological requirements of the environment ( Lossos 2008; Kraft et al., 2015 ). Thus, phylogenetically distant species that have evolved in the same environment can have similar traits that permit them to persist under those conditions and resource levels (called functional convergence), and closely related species that have evolved in different environments can be functionally divergent ( Webb et al., 2002 ; Kraft et al., 2015 ).

Both competition and abiotic factors select species that will coexist, and drive community structure, generating phylogenetic patterns in the species composition. A community structure comprised of phylogenetically closer species (phylogenetic aggregation) is found when traits are conserved among related species and abiotic conditions are the filtering process by which functionally similar taxa are selected, being more able to survive under the conditions imposed ( Hoiss et al. 2012). In contrast to the phylogenetic aggregation pattern caused by environmental filtering, competition can lead to a community structure with a phylogenetically disperse pattern (phylogenetically distant species). If traits are conserved among related species and competition is filtering the species composition, functionally and phylogenetically distant species will remain in the community ( HilleRisLambers et al 2012). Another factor that drives phylogenetic dispersion is positive interaction. The most common kind of positive interaction among plants is facilitation, where an adult plant, called a nurse plant, increases germination and growth of other species by environmental amelioration. It has been shown that facilitation can occur between highly phylogenetically distant species, creating a pattern of phylogenetic dispersion in the community structure ( Verdú et al. 2012).

To test the CRH hypothesis, it is necessary to induce interaction among species with different degrees of similarity. Competition is investigated by different methods, mainly field and pot experiments. Manipulation is a feature of both approaches, and variation in the density of individuals is a common technique. Frequently, species growing alone (intraspecific treatment) are compared to two (or more) species growing together (interspecific treatment). It has been demonstrated that individuals grow better alone if the other species in the interspecific treatment is a strong competitor, or grow worse alone if the other species in the interspecific treatment has facilitative effects ( Burns, Straus 2012). In experiments which compare intra- and interspecific interactions it is expected that competition will be more intense in the intraspecific interaction, due to greater niche similarity ( Chesson, 2000), but the result strongly depends on the competitive ability of the species involved in the interspecific interaction ( Cahill et al., 2007).

Within this theoretical framework we are interested in understanding the consequences of ecological interactions among species in a phylogenetic gradient, to test the CRH. Our specific aims are to determine: (i) if phylogenetically closely related species are also functionally similar, primarily in traits related to water use; (ii) if there is phylogenetic conservatism among the species; and (iii) if the interaction between phylogenetically closely related species is competition and between distantly related species is facilitation.

MATERIAL AND METHODS

Study conditions and species selection

The experiment was conducted in a greenhouse at the Federal University of Ceara (located in the municipality of Fortaleza, Ceara, Brazil; 3º48’26.60”S 39º21’8.40”W; 1448 mm average rainfall; 26.3ºC average temperature). The species selected for the study are commonly found in vegetation locally known as Caatinga, which can be classified as Seasonally Dry Tropical Forest (SDTF; Pennington et al., 2009 ; Oliveira et al., 2013 ). Caatinga vegetation is predominant in the Northeast region of Brazil where the climate is semiarid and the main characteristic is seasonality in water availability due to drought events that vary in intensity and duration annually ( Sampaio, 1995). Seedlings and seeds of the species were collected from SDTF remnants located at the Vale do Curu Experimental Farm in the municipality of Pentecoste, Ceara, Brazil (3º48’S, 39º21’W; 759 mm; 28.3°C) and from the private nature reserve Não Me Deixes Farm, in the municipality of Quixadá, Ceara, Brazil (4º49’S, 38º58’ W; 765 mm; 27.1°C).

To test the CRH we used a gradient of species phylogenetic relatedness for the interaction experiment. The gradient was: close species pair (close), intermediate pair (intermediate) and distant pair (distant). The close pair consisted of two species of the same genus that belong to the same clade, signifying that they have recently evolved from a common ancestor. The intermediate pair was composed of two species from different clades of the same genus, signifying that their last common ancestor was less recent. Finally, the distant pair included species from different genera but from the same family. The species selected were: close pair, Cordia oncocalyx Allemão and Cordia glazioviana (Taub.) Gottschling & J.S. Mill; intermediate pair, Mimosa tenuiflora (Wild) Poir. and Mimosa caesalpiniifolia Benth; and distant pair, Libidibia ferrea (Mart. ex Tul.) L. P. Queiroz and Cenostigma bracteosum (Tul.) E. Gagnon & G.P. Lewis ( Fig. 1). C. oncocalyx and C. glazioviana belong to the Boraginaceae family, M. tenuiflora and M. caesalpiniifolia belong to the Fabaceae family and Mimosoideae subfamily, L. ferrea and C. bracteosum belong to the Fabaceae family and Caesalpiniodeae subfamily. We selected these species because they fulfilled the following requirements: they comprised a phylogenetic gradient, co-ocurr in Caatinga vegetation, and seeds or seedlings were available.

Figure 1.
Species phylogenetic (a) and functional (b) dendrogram. Phylogenetic tree was based on Simon et al. (2011).

Experimental design

After germination the young plants were maintained in germination trays for 20 days before being transplanted into 8 L pots containing a substrate composed of native soil and earthworm humus at a ratio of 2:1 (v:v). After this period, plants of similar height were randomly placed in the following treatments: alone (one individual), intraspecific interaction (two individuals of the same species) and interspecific interaction (one individual of both species of either the close, intermediate or distantly related pairs), each with 20 replications. The interspecific treatments were: C. oncocalyx with C. glazioviana, M. tenuiflora with M. caesalpiniifolia and L. ferrea with C. bracteosum. The plants were maintained for 120 days and watered daily to prevent water stress. The plants were positioned equidistant (8.33 cm) to one another and to the edge of the pot. When alone, the seedling was placed in the center of the pot. In each treatment, the 20 replications were separated according to measurement type: (a) continuous non-destructive, five pots to measure maximum photosynthesis rate (A _max), stomatal conductance (gs) and transpiration rate (E) and five pots to measure leaf longevity; (b) continuous destructive, five pots to measure leaf water potential at predawn (ΨPD) and at midday (ΨMD); and (c) non-continuous destructive, five pots to determine leaf morphological traits and total biomass.

Leaf functional traits

To determine the physiological traits we measured the maximum rate of photosynthesis ( A _max ; μmol CO ₂ m ^-2 s ^-1), stomatal conductance ( gs; mol m ^-2 s ^-1) and intrinsic water use efficiency ( A _max/gs ; μmol CO ₂ mol H ₂O ^-1). These traits were measured at 48-hour intervals for 10 days, using a portable infrared gas analyzer (Licor LI-6400XT). One leaf from each individual (five individuals per treatment) was kept in the meter chamber for approximately 120 s with a fixed CO ₂ concentration of 400 ppm and a flow rate of 400 μmol s ^-1. Radiation inside the chamber was fixed at 1500 μmol photons m ² s ^-1 using an artificial light source (LI-6400XT LED). A _max , gs and WUE measurements were taken when the species had its highest photosynthetic activity, which was ascertained before the experiments began. The light response curves were constructed using the automatic light response program of the LI-COR 6400XT system (see Evans & Santiago 2014). Three leaves for each species were maintained in the IRGA chamber for 200 minutes under different light intensities (0, 20, 50, 100, 200, 500, 1000, 1500 and 2000 µmol m ^-2 s ^-1) (Supplementary data S1).

We also measured leaf water potential at predawn (Ψ _PD; MPa; between 00:00 and 4:00 a.m.) and midday (Ψ _MD; MPa; between 12:00 and 13:00 p.m.) using a Scholander pressure chamber (model P3005F01, Soil Moisture Equipment, California, USA). One leaf per individual was measured, totaling five measurements per treatment on each measurement day. The measurements were taken on five occasions; once every 48h for 10 days. To understand the hydraulic strategies, it was necessary to simulate drought conditions and then evaluate the water potential behavior. So irrigation was ceased in the treatments, and the leaf water potential was measured under drought conditions until total leaf loss occurred, a duration of four to six months, depending on the species. Ψ _PD and Ψ _MD were used to evaluate the hydraulic strategies of each species in response to the loss of conductivity under drought conditions ( Martinez-Vilalta et al., 2014 ). This approach consists of creating a linear regression between Ψ _PD and Ψ _MD. In the regression, the slope value (σ) categorizes the species based on the degree of stomatal sensitivity to drought, while the intercept value (Λ) represents the maximum rate of transpiration per unit of transported water. The σ value is analogous to the stomatal opening behavior of plants. If σ = 0 the species is isohydric, adjusting their stomatal opening to maintain midday leaf potential relatively stable as soon the soil dries (constant leaf potential as soil potential declines), if σ = 1 the species is anisohydric and has a less strict stomatal control (the difference between leaf potential and soil potential stays constant). Λ signifies the transpiration flow relative to the plant hydraulic capacity under well-watered conditions (equivalent to the leaf water potential at Ψ s≈0) ( Martinez-Vilalta et al., 2014 ).

The turgor loss point (π _TLP) was also measured as an indicator of water stress and drought tolerance ( Bartlett et al., 2012 ). To determine π _TLP, pressure-volume curves were constructed using the bench-drying method. Three leaves from three individuals of each species were used to create the curves The leaves were hydrated in water overnight, then weighed, and their water potential was measured. They were then placed on the bench to dry and were weighed, and water potential was measured, every two hours until the water potential became constant. The dry leaf weight was measured and the relative water content was calculated. Pressure-volume curves were constructed for each species from the sequential relative water content and water potential measurements ( Tyree; Hammel, 1972; Bartlett et al., 2012 ). Species with higher π _TLPs avoid excessive water-loss, do not expose their tissues to large negative pressure and have better chances of continuing to function under drought conditions ( Bartlett et al., 2012 ; Martınez-Vilalta et al. 2014 ).

The following leaf traits were also measured: specific leaf area (SLA; leaf area / dry mass, mm ² mg ^-1), relative water content (RWC; fully saturated leaf mass – dry leaf mass / dry leaf mass, g g ^-1), leaf dry mass (LDM, mg) and leaf longevity under drought (LL, days). To make these measurements, five fully expanded mature leaves with no visible injury were collected from each individual. To avoid water loss the leaves were stored in a refrigerated thermal box after collection, as detailed by Pérez-Harguindeguy et al., (2013 ) in their protocol for the measurement of leaf functional traits. In the laboratory, leaf fresh mass was measured with a precision scale (Mark S SSR2 version 2.0), then the leaves were scanned (HP DeskJet GT S822) and their areas were measured using Image J v.1.44 software. To obtain the dry mass, the leaves were dried in an oven (315SE - FANEM) at 60 ºC until their mass became constant. Leaf longevity (measured in days), was evaluated in five pots which were not watered, allowing leaf permanence under drought conditions to be observed.

Phylogenetic signal analysis

To address whether phylogenetically closely related species are also functionally similar we used phylogenetic independent contrasts (PIC), that denote the existence of a phylogenetic signal. This signal can be strong, indicating phylogenetic conservatism, or weak, indicating no phylogenetic conservatism. We analyzed whether a phylogenetic signal was present in each of the traits measured. A phylogenetic signal is the tendency of taxonomically closer species to show more similar traits than expected at random ( Blomberg; Garland, 2002). PIC consist of the difference between two species in the values of a given trait divided by the phylogenetic distance between them ( Felsenstein 1985). Therefore, if two closely related species are very similar, the PIC value is low. To identify whether the PIC value is lower than expected at random, we used randomized positions of the species in the phylogenetic tree and determined a mean PIC, then we compared the observed PIC to the simulated value, considering it significant, i.e., phylogenetic signal present, if the P value is <0.025 ( Münkemüller et al., 2012 ). In addition, to identify whether there was phylogenetic conservatism of the traits, the strength of the phylogenetic signal was quantified using Blomberg’s K ( Blomberg et al., 2003 ). If Blomberg’s K is equal to one (K = 1) this indicates that the traits match Brownian motion expectation, K less than one (K < 1) indicates low phylogenetic signal (the species are more different than expected by chance), and K larger than one (K > 1) indicates a high phylogenetic signal (trait conservatism). To test the significance of K, the values of the traits were then randomized 999 times to generate a null distribution where the p value was calculated.

Relative interaction index

The nature (positive or negative) and intensity of the interactions were determined using the relative interaction index RII ( Armas et al., 2004 ). To calculate this index, the dry mass of the individuals was obtained at the end of the experiment (four months). For this, the shoot and root system were dried in an oven at 60 ºC until reaching constant mass (72 hours), checked with a precision scale. The RII index is determined using the formula: RII = ( B _w–B ₀ ) / ( B _w+B ₀ ), where B _w is the final biomass of the species growing in association and B ₀ is the final biomass of the species growing individually. When RII is negative (between 0 and -1), it means that the species are in competition and there is high niche overlap. On the other hand, if the RII value is positive (between 0 and +1), it is interpreted that the species are in facilitation and and niche overlap is minimal. Finally, if the RII value is very close to 0 (between 0 and 0.05) the species are considered to have a neutral interaction and there is niche partitioning.

Data analysis

We verified that our data were normally distributed and homoscedastic and then we applied a t-test (α<0.05) to compare each trait in each pair of species (between species and within groups). An F-test (α<0.05) was used to compare sensitivity to transpiration (σ) and maximum transpiration rate per unit of hydraulic conductivity (Λ) between treatments.

To examine whether there was phylogenetic conservatism of the traits, the phylogenetic signal for continuous traits was quantified using Blomberg’s K (Material and Methods, section 2.4).

Finally, to investigate whether phylogenetically closely related species compete more than distantly related species, a two-factor analysis of variance was performed by comparing the RII values of the phylogenetic relatedness between species (close, intermediate and distant) and interaction (interspecific and intraspecific). The Analysis of variance was preceded by the Shapiro-Wilk test P>0.05 and homoscedasticity test P>0.05, followed by the Tukey post-hoc test, α<0.05.

RESULTS

Functional traits and phylogenetic conservatism

There was a relationship between species functionality and the phylogenetic gradient. The pair of species with greater phylogenetic proximity, C. glazioviana and C. oconcalyx, had four differences and seven similarities in functional traits, differing in only one morphological (LDM), one physiological ( gs _max ) and two hydraulic traits (Λ and π _TLP; Table 1). The species of the genus Mimosa (intermediate pair) differed in four morphological (SLA, SLM, LDM and LLD), one physiological (WUE) and one hydraulic traits (Λ; Table 1), totaling six differences and five similarities. The pair composed of co-family species (distant pair) showed a higher divergence of functional traits compared to the other pairs, differing in eight traits, four morphological (SLA, SLM, SWC, LLD), three physiological ( A _max , gs _max and WUE) and one hydraulic (σ; Table 1), with only three similar traits.

Table 1.
Comparison of morphological, physiological and hydraulic functional traits for each pair of species with different degrees of relatedness: C. glazioviana and C. oconcalyx (closer), M. tenuiflora and M. caesalpiniifolia (intermediate), and L. ferrea and P. bracteosa (more distant).

Trait	Units	C. glazioviana	C. oconcalyx	t	P	M. tenuiflora	M. caesalpinifolia	t	P	L. ferrea	P. bracteosa	t	P
SLA	mm 2 mg -1	18.29(±1.1)	18.86(±0.3)	0.49	0.49	19.53(±0.8)	22.58(±1.0)	2.17	0.03	20.96(±0.3)	19.30(±0.5)	2.48	0.01
RWC	g g -1	1.19(±0.1)	1.58(±0.1)	1.94	0.06	1.69(±0.0)	1.64(±0.1)	0.29	0.77	0.86(±0.0)	1.52 (±0.0)	7.09	0.00
LDM	mg	317.5(±30.0)	498.7(±23.7)	4.73	0.00	293.3(±13.2)	368.7(±25)	2.64	0.01	324.3(±30.2)	325.2(±25.6)	0.02	0.09
LLD	Days	25.280(±0.3)	24.00(±0.6)	1.84	0.07	26.96(±0.7)	20.50(±0.9)	5.28	0.00	12.48(±0.7)	42.32(±1.2)	20.27	0.00
A max	µmol CO 2 m -2 s -1	8.96(±0.3)	8.22(±0.2)	1.73	0.08	12.67(±0.3)	11.78(±0.4)	1.62	0.11	7.94(±0.24)	5.05(±0.3)	6.34	0.00
gs max	mol m -2 s -1	0.29(±0.0)	0.25 (±0.0)	2.73	0.00	0.41(±0.0)	0.45(±0.0)	1.17	0.24	0.27(±0.0)	0.15(±0.0)	8.59	0.00
WUE	µmol CO 2 mol H 2O -1	31.07(± 0.9)	32.66(±1.4)	0.92	0.36	31.02(±1.1)	27.34(±1.3)	2.09	0.04	29.3(±0.7)	33.51(±1.7)	2.21	0.03
σ	MPa	0.70(±0.0)	0.81(±0.0)	1.10*	0.29	0.98(±0.0)	0.73(±0.1)	271*	1.10	0.61(±0.0)	0.84(±0.0)	6.8*	0.01
Λ	MPa	-2.05(±0.1)	-1.49(±0.1)	21.1*	0.00	-1.47(±0.1)	-0.74(±0.0)	129*	0.00	-2.41(±0.1)	-1.76(±0.1)	1.87*	0.46
π TLP	MPa	-2.72(±0.0)	-2.56(±0.0)	5.97	0.00	-2.45(±0.06)	-2.45(±0.03)	2.59	0.97	-2.62(±0.0)	-2.67(±0.0)	0.52	0.59

• The functional traits analyzed were: Specific leaf area (SLA), specific leaf mass (SLM), saturated water content (SWC), leaf dry mass (LDM), leaf longevity under drought (LLD), maximum photosynthetic rate (A _max), stomatal conductance (gs), intrinsic water use efficiency (WUE), relative sensitivity of transpiration (σ), maximum transpiration rate per unit of hydraulic conductivity (Λ), turgor loss point (πTLP). *Values marked with asterisk were tested through comparisons between lines using F test.

Although the species with a higher degree of relatedness also had greater similarity between functional traits ( Table 1), this relationship was not confirmed by the phylogenetic signal ( Table 2). In the comparison among the 11 functional traits for the six species, there was no presence of phylogenetic signal for any of them ( P>0.025; Table 2). This result indicates that there is no phylogenetic conservatism in the functional traits analyzed, suggesting that they are less similar than expected in a random phylogeny ( Table 2).

Table 2.
Phylogenetic signal in 11 functional traits among three pairs of species with different degrees of relatedness: C. glazioviana and C. oconcalyx, M. tenuiflora and M. caesalpiniifolia, and L. ferrea and P. bracteosa.

Trait	Unit	Range	Z	K	P
SLA	mm 2 mg -1	18.293 - 22.580	-0.229	0.707	0.304
SLM	mg -1 mm 2	0.043 - 0.053	-0.062	0.667	0.518
SWC	g g -1	0.868 - 1.761	-0.002	0.646	0.423
LDM	mg g -1	293.250 - 498.733	-0.586	0.759	0.398
LL	Days	12.48 - 42.32	2.068	0.422	0.985
A max	µmol CO 2 m -2 s -1	5.050 - 12.669	-1.229	1.004	0.152
gs max	mol m -2 s -1	0.159 - 0.458	-1.250	1.015	0.161
WUE	µmol CO 2 mol H 2O -1	27.344 - 33.511	0.569	0.560	0.694
σ	MPa	0.61 - 0.98	1.284	0.487	0.869
Λ	MPa	-0.74 - -2.41	-0.501	0.744	0.339
π TLP	MPa	-2.030 - -2.720	-0.869	0.813	0.224

• Range – Interval of variation in the values of functional traits, Z – phylogenetic independent contrast, K – intensity of phylogenetic signal and P – significance of the test (α<0.025).

Nature of interactions

In the intraspecific treatment, the species of the genus Cordia showed a neutral interaction, with indices of 0.01 and 0.02 for C. glazioviana and C. oconcalyx, ( Table 1).

Respectively ( Figure 2A). In the interspecific interaction, there were differences between RII, demonstrating negative interaction in C. glazioviana (RII = -0.10) and positive interaction in C. oconcalyx (RII = 0.12; Figure 2A). In the pair of species of the genus Mimosa, M. caesalpiniifolia demonstrated positive intraspecific interaction (RII = 0.09), and negative interspecific interaction with M. tenuiflora (RII = -0.19; Figure 2B). Unlike M. caesalpiniifolia, M. tenuiflora demonstrated negative intraspecific interaction (RII = -0.14) and positive interspecific interaction (RII = 0.06, Figure 2B). The intraspecific interactions for the co-family species ( L. ferrea and P. bracteosa) demonstrated a negative interaction for L. ferrea (RII = -0.06) and neutral for P. bracteosa (RII = 0.04; Fig. 2C). In contrast, L. ferrea had a positive interspecific interaction (RII = 0.16) and P. bracteosa showed a neutral interaction (RII = 0.00; Figure 2C).

Figure 2.
Relative interaction index (RII) and the respective confidence interval at 95% in intraspecific and interspecific interactions and in a phylogenetic relatedness gradient with closer, intermediate and distantly related pairs of species. The closely related pair is composed of Cordia oncocalix and C. glazioviana (Boraginaceae), the distantly related pair by Libidibia ferrea and Cenostigma bracteosa (Caesalpiniodea-Fabaceae), and the intermediate pair by Mimosa tenuiflora and M. caesalpiniifolia (Mimosoideae – Fabaceae). RII was calculated with the values of total biomass. Means (± S.D.) with different uppercase letters indicate significant differences between interactions within species, while lowercase letters represent the comparison between species within interactions.

When we consider the RII value grouping the species into the relatedness pairs (close, intermediate and distant) it was found that the interspecific interaction within the distant pair was positive, different to the intermediate pair that showed the most negative interaction (P = 0.022, Fig. 3). Besides this difference, the distant pair had a positive interspecific interaction but a negative intraspecific interaction (P = 0.012).

Figure 3.
Relative interaction index (RII) and the respective confidence interval at 95% in intraspecific and interspecific interactions and in a phylogenetic relatedness gradient with close, intermediate and distantly related pairs of species. The closely related pair is composed of Cordia oncocalix and C. glazioviana (Boraginaceae), the distantly related pair by Libidibia ferrea and Cenostigma bracteosa (Caesalpiniodea-Fabaceae) and intermediate pair by Mimosa tenuiflora and M. caesalpiniifolia (Mimosoideae – Fabaceae). The horizontal black line represents the absolute neutral interaction and the dashed grey line represents the limits of the neutral interaction. Positive values indicate facilitation and negative values indicate competition. Means (± S.D.) with different lower-case letters indicate significant differences in phylogenetic relatedness within interspecific interaction, and upper-case letters indicate significant differences in interaction within distant pairs (Tukey test P < 0.05).

DISCUSSION

The competition-relatedness hypothesis (CRH) predicts that close phylogenetically related species are more functionally similar and, by having similar niches, compete more than more distantly related species ( Darwin, 1859). If phylogenetic proximity is equivalent to niche proximity, species need to preserve the functional traits of their ancestors as they evolve ( Mayfield & Levine, 2010). However, studies that seek a phylogenetic signal in functional traits do not find phylogenetic conservation of the ecological functions investigated (see Lossos, 2008). The lack of conservation of functionality in the evolution of species is one of the main reasons that a positive relationship between increased competition and increased phylogenetic proximity is not frequently observed (e. g. Cahill et al., 2007 ; Fritschie et al., 2014 ; Alexandrou et al., 2015 ). Our results demonstrate that the six species studied did not show a phylogenetic signal of functional traits, particularly those of water use strategies ( A _max , gs _max and WUE). However, we provide evidence that there is greater functional similarity in the more closely phylogenetically related pair of species and that such similarity decreases with the increase in phylogenetic distance. The greater the phylogenetic distance, the more significant differences were found in the measurements of morphological, physiological and hydraulic variables of the species growing alone.

Although the competition-relatedness hypothesis (CRH) is currently of great interest, few studies support it ( Alexandrou et al., 2015 ). In a meta-analysis, Venail et al. (2014 ) surveyed 20 experimental studies and, of these, only six provided support for the CRH. In addition to this, to accept the CRH it is also necessary to accept that there is greater competition between more functionally similar species ( MacArthur & Levins, 1967), which is not always found ( Mayfield & Levine, 2010). It is necessary to consider that traits that confer competitive ability of a species could appear in the evolutionary history of a specific species, and not be conserved traits ( Mayfield & Levine, 2010). In this study, the competitive ability of one species ( M. tenuiflora) which has high vegetative growth ( Figueiredo et al., 2012 ) had an impact on the experiment, so that of the three species pairs studied, the pair that contained M. tenuiflora was the only one that did not corroborate the CRH.

In this study, we consider the intraspecific treatment to represent the highest degree of niche similarity. The closely (and more functionally similar, C. glazioviana and C. oncocalyx) species pair showed the same result for both species whether in intraspecific or interspecific competition; i.e. the effect was the same whether the neighbouring plant was an individual of the same or a congeneric species. In the intermediate pair, it was possible to detect the competitive effect of M. tenuiflora. When this species grows with itself there is a negative impact on the individual of the same species, but when M. tenuiflora grows with an M. caesalpinifolia individual, the result is positive for the former and negative for the latter. Finally, the distant pair showed a classic niche differentiation response. For this pair, when the species grew in intraspecific competition there was a negative effect, and when they grew with each other, P. bracteosa demonstrated a neutral interaction and L. ferrea showed a positive interaction. Although we are looking for simplifications of the complex reality, our results partly corroborate the CRH. Only the intermediate pair did not corroborate the CRH, because competition was observed for the closely phylogenetically related pair and facilitation was found for the distantly related pair. One pair did not corroborate the CRH, meaning that other factors should be considered to better understand competition and coexistence among species.

Due to greater niche similarity, the intraspecific interactions were expected to have a more negative effect than the interspecific interactions, but the effect of this interaction was different depending on the species involved. For the congeneric species of the same clade, the intraspecific interaction was neutral, for the congeneric species of distinct clades, this interaction was competitive for M. tenuiflora and facilitative for M. caesalpiniifolia, and for the species of the same family the result was competition for both species. Once again, we note the strong competitive ability of M. tenuiflora, and that M. caesalpiniifolia, a nitrogen-fixing species ( Barros et al., 2018 ), showed a facilitative interaction in the intraspecific treatment. These results, once again, demonstrate the importance of intrinsic traits of the species involved in the interaction.

What we can synthesize from all these interactions is that facilitation is found in phylogenetically distant species and that competition is not always related to phylogenetic distance. Phylogenetically more distant species are more likely to interact positively, through facilitation ( Valiente-Banuet and Verdú, 2007). Niche partition and facilitation were found in the more distant phylogenetically related pair, and these results corroborate those reported in other studies ( Verdú et al., 2009 ; Castillo, Verdu & Valiente-Banuet, 2010; Duarte et al 2021). Facilitation, a positive interaction, usually affects the germination and establishment of coexisting species through the improvement of microenvironmental conditions and/or resource availability ( Gómez-Aparicio et al., 2004 ). The set of conditions required by a species at the time of germination and initial establishment is called the regeneration niche ( Grubb, 1977). According to Valiente-Banuet and Verdú (2007), regeneration niche traits are conserved throughout evolution, i.e., similar species require similar conditions to germinate and establish themselves and, therefore, phylogenetically distant species grow under the canopy of nurse species, and not of similar species and much less of the same species. Facilitation between distant species can be easily observed when studying shrub species facilitating cactus species (e.g., Valiente-Banuet et al., 1991 ; Drezner, 2006; Flores‐Torres et al., 2019 ). Although we studied species with the same growth form and with a certain phylogenetic relatedness in our work, facilitation was also found in species of the same family (Fabaceae, the more distantly related pair).

We were expecting that, if the functional traits were conserved and the environmental filter (water seasonality) selected the species in the semiarid region, then the phylogenetically close species would coexist and that competition would be less significant (see Webb et al., 2002 ). However, a negative interaction was found in two of the three pairs of species. We cannot fail to point out that our study was conducted in 8L pots, each containing two individuals, and therefore negative interaction was stimulated due to space limitations. Other studies evaluating competition and facilitation between species in a gradient of phylogenetic relatedness should be conducted under field conditions to get closer to reality.

In conclusion, phylogenetic distance alone cannot be used to determine the type of interaction in species associations, and the competitive ability of each species should also be considered when evaluating species coexistence. The coexistence mechanisms can be used to predict biological invasions and to determine better species combinations for the restoration and recovery of degraded areas.

REFERENCES

• ALEXANDROU, M. A.; CARDINALE, B. J.; HALL, B. J. D; DELWICHE, C. F.; FRITSCHIE, K.; NARWANI, A.; VENAIL, P. A.; BENTLAGE, B.; PANKEY, M. S.; OAKLEY, T. H.. Evolutionary relatedness does not predict competition and co-occurrence in natural or experimental communities of green algae. Proceedings of the Royal Society B: Biological Sciences 282: 20141745, 2015.
• Armas, C.; Ordiales, R.; Pugnaire, F. I. (2004). MEASURING PLANT INTERACTIONS: A NEW COMPARATIVE INDEX. Ecology, 85(10), 2682–2686. doi:10.1890/03-0650
  » https://doi.org/10.1890/03-0650
• BARTLETT, M.; SCOFFONI, C.; SACK, L. The determinants of leaf turgor loss point and prediction of drought tolerance of species and biomes: a global meta-analysis. Ecology Letters, v. 15, p. 393–405, 2012.
• BARROS, F. M. R.; FRACETTO, G. G. M.; FRACETTO, F. J. C.; MENDES JÚNIOR, J. P.; ARAÚJO, V. L. V. P.; LIRA JUNIOR, M. A. Silvopastoral systems drive the nitrogen-cycling bacterial community in soil. Ciência e Agrotecnologia, v. 42, p. 281-290, 2018.
• BLOMBERG S. P.; GARLAND Jr T. (2002) Tempo and model in evolution: Phylogenetic inertia, adaptation and comparative methods. J Evol Biol 15:899-910.
• BLOMBERG SP, GARLAND T and IVES AR (2003) Testing for phylogenetic signal in comparative data: Behavioral traits are more labile. Evolution 57:717-745.
• BURNS JH & STRAUSS SY, 2012. Effects of competition onphylogenetic signal and phenotypic plasticity in plant functional traits. Ecology, 93:S126-S137. http://dx.doi.org/10.1890/11-0401.1
  » https://doi.org/10.1890/11-0401.1
• CAHILL, J. F.; KEMBEL, S. W.; LAMB, E. G.; KEDDY, P. A. Does phylogenetic relatedness influence the strength of competition among vascular plants? Perspectives in Plant Ecology Evolution and Systematics, v. 10, p. 41–50, 2007.
• CASTILLO, J. P.; VERDÚ, M.; VALIENTE-BANUET, A. Neighborhood phylodiversity affects plant performance. Ecology, v. 91, p. 3656–3663, 2010.
• CAVENDER-BARES, J.; KOZAK, K. H.; FINE, P. V. A.; KEMBEL, S. W. The merging of community ecology and phylogenetic biology. Ecology Letters, v. 12, p. 693–715, 2009.
• CHESSON, P. Mechanisms of maintenance of species diversity. Annual Review of Ecology Evolution and Systematics, v. 31, p. 343–366, 2000.
• DARWIN, C.; KEBLER, L. On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life. London: J. Murray, 1859. 502p.
• DREZNER, T. D. Plant facilitation in extreme environments: The nonrandom distribution of saguaro cacti (Carnegiea gigantea) under their nurse associates and the relationship to nurse architecture. Journal of Arid Environments, v. 65, p. 46-61, 2006.
• DUARTE, M.; VERDÚ, M.; CAVIERES, L. A.; BUSTAMANTE, R. O. Plant–plant facilitation increases with reduced phylogenetic relatedness along na elevation gradient. Oikos, v. 130, p. 248-259, 2021.
• EVANS, J. R.; SANTIAGO, L. S. PrometheusWiki gold leaf protocol: gás exchange using Li-COR 6400. Functional Plant Biology, v. 41, n. 3, p. 223-226, 2014.
• FELSENSTEIN, J. Phylogenies and the comparative method. American Naturalist, v. 125, p. 1-15, 1985.
• FIGUEIREDO, J. M.; ARAÚJO, J. M.; PEREIRA, O. N.; BAKKE, I. A.; BAKKE, O. A.. Revegetation of degraded caatinga sites. Journal of Tropical Forest Science, v. 24, p. 332-343, 2012.
• FLORES‐TORRES, A.; MONTAÑA, C.; FRANCO, M. Coexistence and the niche in a nurse–cactus interaction: Is cyclic dynamics justified? Journal of Ecology v. 107, p. 407–417, 2019.
• FRITSCHIE, K. J; CARDINALE, B. J.; ALEXANDROU, M. A.; OAKLEY, T. Evolutionary history and the strength of species interactions: testing the phylogenetic limiting similarity hypothesis. Ecology, v. 95, p. 1407–1417, 2014.
• GODOY, O. Coexistence theory as a tool to understand biological invasions in species interaction networks: Implications for the study of novel ecosystems. Functional Ecology, v. 33, p. 1190-1201, 2019.
• GÓMEZ-APARICIO, L.; ZAMORA, R.; GÓMEZ, J. M.; HÓDAR, J. A.; CASTRO, J.; BARAZA, E. Applying plant facilitation to forest restoration in Mediterranean ecosystems: a meta-analysis of the use of shrubs as nurse plants. Ecological Applications, v. 14, p. 1128–1138, 2004.
• GRUBB, P. J. The maintenance of species richness in plant communities: the importance of the regeneration niche. Biological Reviews, v. 52, p. 107–145, 1977.
• HILLERISLAMBERS, J.; ADLER, P. B.; HARPOLE, W. S.; LEVINE, J. M.; MAYFIELD, M. M. Rethinking Community Assembly through the Lens of Coexistence Theory. Annual Review of Ecology, Evolution, and Systematics, v. 43, p. 227–48, 2012.
• HOISS. B.; KRAUSS, J.; POTTS, S.; ROBERTS, S.; STEFFAN-DEWENTER, I. Altitude acts as an environmental filter on phylogenetic composition, traits and diversity in bee communities. Proceedings of the Royal Society, v. 279, p. 4447-4456, 2012.
• KRAFT, N. J. B.; GODOY, O.; LEVINE, J. M.. Plant functional traits and the multidimensional nature of species coexistence. Proceedings of the National Academy of Sciences of the United States of America, v. 112, p. 797–802, 2015.
• LOSSOS, L. B. Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. Ecology Letters, v. 11, p. 995–1007, 2008.
• LYU, S.; LIU, X.; VENAIL, P.; ZHOU, S. Functional dissimilarity, not phylogeneticrelatedness, determines interspecifc interactions among plants in the Tibetan alpine meadows. Oikos, v. 126, p. 381–388, 2017.
• MACARTHUR, R.; LEVINS, R. The limiting similarity, convergence, and divergence of coexisting species. The American Naturalist, v. 921, p.377-385, 1967.
• MAHERALI, H.; KLIRONOMOS, J. N. Influence of Phylogeny on Fungal Community Assembly and Ecosystem Functioning. Science, v. 316, p. 1746-1748, 2007.
• MARTINEZ-VILALTA, J.; POYATOS, R.; AGUADE, D.; RETANA, J.; MENCUCCINI, M. A new look at water transport regulation in plants. New Phytologist, v.204, p. 105–115, 2014.
• MAYFIELD, M. M.; LEVINE, J. M. Opposing effects of competitive exclusion on the phylogenetic structure of communities. Ecology Letters, v. 13, p. 1085–1093, 2010.
• NARWANI, A.; ALEXANDROU, M. A.; OAKLEY, T. H. ; CARROLL, I. T.; CARDINALE, B. J. Experimental evidence that evolutionary relatedness does not affect the ecological mechanisms of coexistence in freshwater Green algae. Ecology Letters, v. 16, p. 1373–1381, 2013.
• OLIVEIRA, L. S.; MORO, M. F.; NIC LUGHADHA, E. M.; MARTINS, F. R.; MELO, A. L.; ESSER, H. J.; SALES, M. F. Hidden in the dry woods: Mapping the collection history and distribution of Gymnanthes boticario, a well-collected but very recently described species restricted to the dry vegetation of South America. Phytotaxa, v. 97, p. 1–16, 2013
• MÜNKEMÜLLER, T.; LAVERGNE, S.; BZEZNIK, B.; DRAY, S.; JOMBART, T.; SCHIFFERS, K.; THUILLER, W. How to measure and test phylogenetic signal. Methods in Ecology and Evolution, v. 3, p. 743-756, 2012.
• PENNINGTON, R. T.; LAVIN, M.; OLIVEIRA-FILHO, A. Woody Plant Diversity, Evolution, and Ecology in the Tropics: Perspectives from Seasonally Dry Tropical Forests. Annual Review of Ecology, Evolution, and Systematics, v. 40, p. 437–457, 2009.
• PÉREZ-HARGUINDEGUY, N.; DÍAZ, S.; GARNIER, E. New handbook for standardised measurement of plant functional traits worldwide. Australian Journal of Botany, v. 61, p. 137–234, 2013.
• SAMPAIO, E. V. S. B. Overview of the Brazilian Caatinga. In: Bullock, S. H.; Mooney H. A.; Medina, E. Seasonally dry tropical forest. Cambridge University Press, 1995. p. 35-63.
• SIMON, M. F.; GRETHER, R.; QUEIROZ, L. P.; SÄRKINEN, T. E.; DUTRA, V. F.;HUGHES, C. E. The evolutionary history of Mimosa (Leguminosae): Toward a phylogeny of the sensitive plants. American Journal of Botany, v. 98, p. 1201-1221, 2011.
• STRAUS, S. Y.; WEBB, C. O.; SALAMIN, N. Exotic taxa less related to native species are more invasive. Proceedings national academy of sciences, v. 11, p. 5841 5845, 2006.
• TYREE, M. T.; HAMMEL, H. T. Measurement of turgor pressure and water relations of plants by pressure bomb technique. Journal of experimental Botany, v. 23, p. 267–282, 1972.
• VALIENTE-BANUET, A.; VITE, F.; ZAVALA-HURTADO, J. A. Interaction between the cactus Neobuxbaumia tetetzo and the nurse shrub Mimosa luisana. Journal of Vegetation Science, v. 2: 11-14, 1991.
• VALIENTE-BANUET, A.; VERDÚ, M. Facilitation can increase the phylogenetic diversity of plant communities. Ecology Letters, v. 10, p. 1029–1036, 2007.
• VALIENTE-BANUET, A.; VERDÚ, M. Temporal shifts from facilitation to competition occur between closely related taxa. Journal of Ecology, v. 96, p. 489–494, 2008.
• VENAIL, P. A.; NARWANI, A.; FRITSCHIE, K.; ALEXANDROU, M. A.; OAKLEY, T. H.; CARDINALE, B. J. The influence of phylogenetic relatedness on species interactions among freshwater green algae in a mesocosm experiment. Journal of Ecology, v. 102, p. 1288–1299, 2014.
• VERDÚ, M.; REY, P. J.; ALCÁNTARA, J. M.; SILES, G.; VALIENTE-BANUET, A. Phylogenetic signatures of facilitation and competition in successional communities. Journal of Ecology, v. 97, p. 1171–1180, 2009.
• VERDÚ, M.; GOMEZ-APARICIO, L.; VALIENTE-BANUET, A. Phylogenetic relatedness as a tool in restoration ecology: a meta-analysis. Proceedings of the Royal Society of London Series B: Biological Sciences, v. 279, p. 1761–1767, 2012.
• VIOLLE, C; NEMERGUT, D. R.; PU, Z.; JIANG, L. Phylogenetic limiting similarity and ompetitive exclusion. Ecological Letters, v. 14, p. 782–787, 2011.
• WEBB, C. O.; ACKERLY, D. D.; MCPEEK, M. A.; DONOGHUE, M. J. Phylogenies and community ecology. Annual Review of Ecology and Systematics, v. 33, p. 475–505, 2002

Publication Dates

• Publication in this collection
  16 Dec 2022
• Date of issue
  2022

History

• Received
  03 Dec 2021
• Accepted
  10 May 2022