Ecophysiological responses of bromelias in the restinga in simulated climate change scenarios

Respostas ecofisiológicas de bromélias na restinga em cenários simulados de mudanças climáticas

Abstract

We investigated the ecophysiological responses of the bromeliads Aechmea nudicaulis and Vriesea procera, seeking to assess their suitability to survive in a climate change scenario (optimistic scenario RCP 2.6 of the IPCC, 2021) in a Restinga environment. To carry out this investigation, we used open-top chambers (OTC). During a period of nine months (June 2022 to February 2023), the bromeliads A. nudicaulis and V. procera were subjected to the following treatments: treatment T: plants transplanted to the environmental conditions of the bare sand of the restinga and subjected to the microclimatic conditions of the OTC's; control C: plants transplanted to the environmental conditions of the bare sand of the restinga. The ecophysiological variables height, rosette diameter, relative water content, specific leaf area and total weight of the plants were evaluated. In addition, dead plants were counted. The OTC’s showed an average increase in temperature and VPD (Vapor Pressure Deficit) of 1.6°C and 0.5 Kpa, respectively, and an average reduction in RH (relative humidity) of 5.3%. The results of this study indicated that the increase in local temperature that occurred between the sixth and seventh months evaluated (November and December) created limiting conditions that exceeded the tolerance capacity of the bromeliads studied. Furthermore, the climatic conditions of the OTCs intensified the damage that occurred in the plants, verified here by the reductions in the values ​​of the ecophysiological attributes evaluated in the bromeliads studied. In addition, the high mortality rate (above 50%) reinforces the idea that the climatic conditions of the OTC’s induced the bromeliads studied to a senescence process. Therefore, these results are important, as they indicate that even the most optimistic climate change scenario (IPCC 2021 RCP 2.6) can harm the growth and development of these bromeliads, which are essential for the structure and functioning of Restinga communities.

Keywords:
climate change; growth; open top chamber; temperature; vapor pressure deficit

Resumo

Investigamos as respostas ecofisiológicas das bromélias Aechmea nudicaulis e Vriesea procera, buscando avaliar sua aptidão para sobreviverem em um cenário de mudanças climáticas (cenário otimista RCP 2.6 do IPCC, 2021) em ambiente de Restinga. Para realizar tal investigação, utilizamos câmeras de topo aberto (OTC, do inglês "Open Top Chambers"). Durante um período de nove meses (Junho de 2022 à Fevereiro 2023), as bromélias A. nudicaulis e V. procera foram submetidas aos seguintes tratamentos: tratamento T: plantas transplantadas para as condições ambientais da areia nua da restinga e submetidas às condições microclimáticas das OTC's; controle C: plantas transplantadas para as condições ambientais da areia nua da restinga. Foram avaliados as variáveis ecofisiológicas altura, diâmetro da roseta, teor relativo de água, área foliar específica e o peso total das plantas. Além disso, foram contabilizadas as plantas mortas. As OTC’s apresentaram um aumento médio da temperatura e do DPV (Défict de pressão de vapor) respectivamente de 1,6°C e 0,5 Kpa e uma redução média do URA (umidade relativa do ar) de 5,3%. Os resultados deste estudo indicaram que o aumento da temperatura local ocorrido entre o sexto e sétimo mês avaliado (novembro e dezembro) criaram condições limitantes que excederam a capacidade de tolerância das bromélias estudadas. Ademais, as condições climáticas das OTC's intensificaram os danos ocorridos nas plantas, verificados aqui pelas reduções dos valores dos atributos ecofisiológicos avaliados nas bromélias estudadas. Além disso, a elevada taxa de mortalidade (acima dos 50%) reforça a ideia que as condições climáticas das OTC’s induziram as bromélias estudadas a um processo de senescência. Portanto, esses resultados são importantes, pois indicam que mesmo o cenário mais otimista de mudanças climáticas (RCP 2.6 do IPCC 2021) pode prejudicar o crescimento e o desenvolvimento dessas bromélias, essenciais para a estrutura e o funcionamento das comunidades de Restinga.

Palavras-chave:
mudanças climáticas; crescimento; câmera de topo aberto; temperatura; déficit de pressão de vapor

1. Introduction

Restinga is an ecosystem associated with the Atlantic Forest domain that features diverse vegetation and a variety of plant formations (Assis et al., 2011; Pereira and Menezes, 2023). Within this ecosystem, one can find everything from herbaceous vegetation near the beach to forest formations in continental areas (Pereira and Araújo, 2000; Scarano, 2002)

Although these vegetation formations are distributed along a wide longitudinal range of the coastal plain, they are similarly subject to adverse environmental conditions such as high light, temperature, salinity, unstable sediments, and strong winds (Magnago et al., 2010; Menezes and Araújo, 2005). To establish themselves in these challenging environments, plant species must possess a series of adaptive mechanisms to regulate their growth and development (Carlucci et al., 2021; Gray and Brady, 2016). However, the rapid climate changes occurring in the Anthropocene threaten the adaptive capacity of living organisms, and consequently, the resilience of ecosystems (Becklin et al., 2016; Shaw and Etterson, 2012).

In this context, the discussion arises about the impact of these changes on plant species that inhabit extreme environmental conditions, such as those found in Restinga (Inague et al., 2021). Given this scenario, it is essential to conduct studies that evaluate the adaptive plasticity of species present in Restinga in the face of climate change (Inague et al., 2021). Studies like these are crucial to understanding how plants can respond to environmental transformations, contributing to the conservation of biodiversity and the sustainability of these unique ecosystems (Martin and Watson, 2016; Upson et al., 2016).

In Restingas, the Aechmea nudicaulis (L.) Griseb. and Vriesea procera (Mart. ex Schult. & Schult. F) bromeliads stand out for their dominance in the understory of the phytophysiognomic open shrub formation (Assis et al., 2004; Sampaio et al., 2002; Scarano, 2002). These bromeliad species share common ecophysiological mechanisms and survival strategies. Both are facultative epiphytes (mainly terrestrial in the Restinga), have tank-forming leaves adapted to store water, possess CAM (Crassulacean Acid Metabolism) photosynthetic metabolism, and rely on clonal growth as their main propagation strategy in the Restinga (Costa et al., 2014; Sampaio et al., 2002, 2005; Uribbe et al., 2020). These species constitute an important component of this plant community, particularly due to their role in ecological succession, acting as facilitator species by providing resources and shelter for other plants (Costa et al., 2014; Martinelli et al., 2008; Sampaio et al., 2002, 2005). Therefore, given the relevance of these key species, it is essential to conduct studies that simulate the effects of predicted climate changes on them.

In this context, the use of open top chambers (OTC’s) emerges as an alternative to investigate the effects of changes in climatic factors, such as temperature, humidity, and vapor pressure deficit (VPD), on the ecophysiological responses of plant species (De-Frenne et al., 2010; Welshofer et al., 2018). In this way, OTC’s represent a promising and efficient tool to advance the understanding of the impacts of climate change on native plant species and their ecosystems (Norby et al., 1997; Welshofer et al., 2018).

Therefore, this study aims to test the hypothesis that the changes generated by open-top chambers, simulating the climate changes predicted by the optimistic scenario RCP 2.6 of the IPCC (Intergovernmental Panel on Climate Change), considering the climatic factors temperature, relative humidity and vapor pressure deficit, can harm the ecophysiological performance of the bromeliads A. nudicaulis and V. procera, thus compromising their survival.

2. Material and Methods

2.1. Study area

The study was carried out at the Paulo Cesar Vinha State Park (Research authorization No. 004-2022; Process No. 2021-GQHQR), located in the municipality of Guarapari, in the state Espírito Santo (20º33'-20º38'S and 40º23'-40º26'W). The park has an area of approximately 1,500 acres that encompasses the Restinga ecosystem. The phytophysiognomy of the study site is classified as non-floodable open shrub formation (Pereira and Menezes, 2023). The region's climate is tropical Aw, according to the Köppen classification, with hot and rainy summers and dry winters. The average annual temperature is 24ºC, the average annual precipitation is 1.270 mm, and the average annual relative humidity is 80%.

2.2. Experiment setup and conditions

Were randomly selected 26 vegetative branches of each bromeliad species (A. nudicaulis e V. procera), coming from different clonal modules located in the understory of the vegetation. For standardization, were seleted ramets in the vegetative stage located in the penultimate position of the rhizomes of the clonal modules for both species. Only ramets with weight variation of less than 10% and without signs of disease or herbivory were chosen.

For the experiment, half (13 ramets) of the 26 ramets of each bromeliad species were randomly selected and transplanted into a bare sand environment of the Restinga in full sun and subjected to the microclimatic conditions of the OTC’s, representing the treatment (T) (Figure 1). The other 13 ramets were transplanted into a bare sand environment of the Restinga in full sun, representing the control (C) (Figure 1). The ramets were transplanted into holes approximately 10 centimeters deep, positioning an individual subjected to the treatment and control in a perpendicular line relative to the movement of the sun (East-West) at a distance of one meter between them.

Figure 1
A: V. procera plants and B: A. nudicaulis plants subjected to treatment T = inside the OTC’s; control C = outside the OTC’s.

The experiment was conducted over a period of 9 months (June 2022 to February 2023), with monthly assessments of ecophysiological attributes. To carry out these assessments, 10 individuals were randomly selected from the 13 subjected to the treatment conditions, and in the same way for the control. The analyses that required the collection of leaf material were carried out quarterly, randomly selecting 6 individuals for both the treatment and control groups.

2.3. Open-top chambers (OTC)

The OTC’s were designed to simulate the climate conditions predicted by the optimistic scenario (RCP 2.6) of the Representative Concentration Pathways proposed by the IPCC (2021). According to this scenario, a gradual increase in temperature of 1.5°C to 2°C and a 15% increase in rainfall are estimated for the southeastern region of Brazil (IPCC, 2021).

The OTC’s were built in the shape of a frustum, with dimensions of 35 centimeters in diameter at the largest base, 20 centimeters in diameter at the smallest base, and 50 centimeters in height, surrounded by a transparent PVC (polyvinyl chloride) cover that is 0.40 mm thick. In each side quadrant of the OTC’s, there were two air ventilation channels measuring 6.5 centimeters in diameter.

2.4. Climatic conditions between treatment and control

Was collected climate data between these two environments (inside and outside OTC's), with the aid of external data logger type devices of the model HOBO U12 (Onest® HOBO data loggers, Bourne, MA, USA) with recording programmed every 1 minute. This information was collected over a period of 24 hours, starting at 7:35 am on the 25/02/23 and ending at 7:35 am on the 26/02/23.

2.5. Climatic conditions of the study area

The climate data of the study area were obtained from the INMET (National Institute of Meteorology) (Brasil, 2022) meteorological station A634 located in the city of Vila Velha-ES (20°28' S and 40°24' W), located 21.9 kilometers from the study area.

2.6. Analyzes of ecophysiological attributes

We measured the height of the aerial part monthly, from the soil surface to the highest position reached by the leaves, the diameter of the rosette, and the length and width of the leaves using a measuring tape and a digital caliper (accuracy of 0.01 mm). The fresh mass of the plants was also weighed at transplanting and at the end of the study.

2.7. Leaf area

The leaf area (LA) of the studied plants was determined using a first degree linear regression equation model: Y= ax + b, according to Cristofori et al. (2007).

Where, Y = leaf area; a = slope of the line; x = product of multiplying length and width (LW); b = point of intersection of the line.

To determine the slope and the intersection point of the model line, 20 leaves were collected from 4 individuals for each species in different positions of the leaf rosette, from the smallest leaves to the largest leaves in the rosette. The length and width of each leaf were then measured, as well as its leaf area, with the aid of the model area meter LICOR LI-3100 (LI-COR, Inc. Lincoln, Nebraska, USA). The resulting Equations for each species were: A. nudicaulis: Y = 1.56x – 10.88 and V. procera: Y = 0.86x – 1.48.

From these data, a scatterplot of the LW of the leaves with their respective LA was plotted. The high value of the correlation coefficient (R²) allowed confirming the accuracy of the model used to determine the LA (Figure 2).

Figure 2
Scatter diagram of leaf area (LA) with the product of the multiplication of the length by the width of the leaves (LW) to create a leaf area estimator model. A: Leaves of A. nudicaulis n= 20 and B: Leaves of V.procera n= 20.

2.8. Quarterly analysis

Were collected quarterly leaf samples from the same that were carried out as monthly ecophysiological analyses. The leaf samples were placed in black plastic bags and sealed until laboratory analysis was performed approximately 2:30 hours after collection. Was analyzed the relative water content in the leaves (RWC) expressed as percentage, determined by equation: RWC = [(FW-DW) / (TW-DW)] * 100. Where FW = fresh weight; DW = dry weight e TW= turgid weight. It also analyzed the specific leaf area (SLA), obtained through the ratio between the leaf area and its dry mass (cm². g^-1).

2.9. Experimental design and statistical analysis

The experiment was conducted in completely randomized blocks, with each block represented by one individual from the treatment and one from the control (Figure 1). The treatment and control were compared using Student's t-test for independent samples at the 5% and 1% significance levels. Due to plant death during the study period, the sample size of the treatment and control changed from ten to nine plants in January and seven plants in February for the species A. nudicaulis, and to six plants in February for the species V. procera.

3. Results

3.1. Climatic conditions during the evaluated months

The climatic conditions during the experimental period (June 2022 to February 2023) were consistent with the region's expected climate pattern according to the Köppen classification (Figure 3). Two distinct climatic periods can be identified. The period from spring to winter (June to September) had milder temperatures (average temperature: 22.39°C), lower averages of relative humidity and precipitation (77.67% and 18.75 mm, respectively), and accumulated precipitation of 74.20 mm (Figure 3). In contrast, the period from autumn to summer (October to February) had higher temperatures (average temperature: 25.72°C), higher averages of relative humidity and precipitation (88.65% and 154.64 mm, respectively), and accumulated precipitation of 773.20 mm (Figure 3).

Figure 3
Relative humidity, precipitation and average average temperature for the months of June 2022 to February 2023. Source: Brasil (2022) data adapted.

3.2. Climatic conditions inside and outside OTC’s

The OTC’s increased the average temperature by 1.92°C during the day and 1.29°C at night (Table 1). The OTC’s reduced the average relative humidity by 5.75% at night and 4.06% during the day (Table 1). The OTC’s also increased the average vapor pressure deficit (VPD) by 0.81 Kpa during the day and 0.19 Kpa at night (Table 1). Considering the entire day, the average increase in temperature was 1.61°C, the VPD was 0.49 Kpa, and the average reduction in relative humidity was 5.37% (Table 1).

Table 1
Average, maximum and minimum values of temperature, relative humidity, luminosity and vapor pressure deficit (VPD) treatment inside the OTC's (T) and control outside the OTC's (C) during the entire day period (7:35 hours from 02/25/23 to 7:35 am on 02/26/23), during the day (7:35 am to 6:15 pm) and at night (6:16 pm to 5:50 am).

Period		Temperature (c°)		Difference between	Relative humidity (%)		Difference between	Luminosity (lum/ft2)		Difference between	VPD		Difference between
		T	C	T and C	T	C	T and C	T	C	T and C	T	C	T and C
Entire day (24 hours)	Average	33.12	31.51	1.61	63.90	69.27	5.37	1,010.01	1,061.38	51.37	2.86	2.36	0.49
	Maximum	48.14	46.67	1.47	91.92	96.71	4.79	2,998.90	2,998.90	0.00	8.30	7.31	0.99
	Minimum	23.21	21.96	1.25	25.76	28.51	2.75	0.40	0.40	0.00	0.23	0.09	0.14
At day (7:35 am to 6:15 pm)	Average	42.74	40.82	1.92	36.88	40.94	04.06	2,220.15	2,305.64	85.50	5.78	4.97	0.81
	Maximum	48.14	46.67	1.47	74.53	81.75	7.22	2,998.90	2,998.90	0.00	8.30	7.31	0.99
	Minimum	27.95	26.52	1.43	25.76	28.51	2.75	7.00	2.60	4.40	0.96	0.63	0.33
At night (6:16 pm to 5:50 am)	Average	24.32	23.02	1.29	89.42	95.18	5.75	0.40	0.40	0.00	0.32	0.14	0.19
	Maximum	25.99	24.75	1.24	91.92	96.63	4.71	0.40	0.40	0.00	0.50	0.26	0.24
	Minimum	23.21	21.96	1.25	85.04	91.75	6.72	0.40	0.40	0.00	0.23	0.09	0.14

There was no significant difference in luminosity between treatment and control (Table 1). The biggest difference between treatment and control was during the day, representing a difference of only 3.70% (maximum difference of 85 lum/ft²), indicating that the OTC coating did not interfere with luminosity.

3.3. Growth

V. procera presented significantly lower height values in the treatment during the months of December, January, and February, with reductions of 14.55%, 19.97%, and 26.25%, respectively (Table 2). For the height of A. nudicaulis, there was a significant difference between treatment and control only in February, with the treatment showing lower values by 15.98% (Table 2).

Table 2
Growth attributes of A. nudicaulis and V. procera plants during the months of evaluation in treatment inside the OTC's (T) and control outside the OTC's (C).

V. Procera	Months	Height (cm)		p-value	Rosette diameter (cm)		p-value	Leaf area (cm2)		p-value
		T	C		T	C		T	C
	June	29.23±3.28	29.78±3.81	0.73	27.84±3.53	25.61±4.54	0.2367	53.59±5.32	54.70±6.15	0.6720
	July	30.45±1.46	30.62±4.26	0.9072	29.01±4.58	27.39±4.98	0.4619	48.14±6	49.64±6.64	0.6027
	August	31.09±1.93	32.58±3.32	0.2360	29.07±3.86	28.45±3.17	0.6998	67.78±12.81	66.79±9.65	0.8483
	September	31.9±1.80	33.18±2.11	0.1624	28.41±2.71	28.56±3.37	0.9140	66.24±5.08	67.52±5.13	0.5812
	October	32.52±1.86	34.01±2.59	0.1579	27.883.65	28.79±4.42	0.6221	65.84±9.33	63.17±8.86	0.5207
	November	29.04±2.55	32.1±4.87	0.0957	24.65±3.95	23.47±2.93	0.4581	57.35±4.94	58.69±6.36	0.6060
	December	26.42±2.99	30.92±2.70	0.0024**	24.56±2.83	23.32±2.12	0.2822	52.88±4.61	51.97±5.8	0.7040
	January	23.8±5.00	29.74±3.65	0.0072**	21.27±2.64	23.87±2.57	0.0391*	45.15±3.96	54.83±7.91	0.0028**
	February	21.85±2.34	29.63±1.49	0.0001**	20.18±1.22	23.75±1.40	0.0009**	30.96±2.73	54.44±9.6	0.0012**
A. Nudicaulis	June	29.94±3.81	27.32±4.58	0.1814	13.01±1.42	12.47±1.36	0.3981	157.95±26.04	155.11±29.24	0.8225
	July	32.12±3.77	30.29±4.32	0.3271	12.75±1.72	12.03±0.79	0.2526	188.78±36.68	186.19±41.57	0.8843
	August	33.21±4.80	31.08±2.33	0.2298	12.83±2.14	12.92±2.26	0.9283	177.94±30.55	172.31±31.91	0.6915
	September	33.83±4.01	31.72±1.99	0.1586	13.08±1.34	12.91±1.43	0.7876	187.19±22.88	183.83±20.71	0.7351
	October	34.13±4.26	32.74±4.79	0.5020	13.17±2.54	12.89±2.21	0.7962	182.70±26.92	179.45±26.39	0.7880
	November	33.36±5.92	33.63±5.61	0.9179	14.63±2.66	13.83±1.97	0.4527	200.83±41.6	197.85±41.7	0.8748
	December	32.03±3.62	32.97±4.58	0.6195	13.82±2.52	12.91±2.57	0.4339	188.97±41.56	200.17±33.57	0.5161
	January	29.853.11	31.06±3.97	0.4822	11.47±3.43	13.78±2.21	0.1096	142.06±28.34	204.15±33.69	0.0006**
	February	29.02±1.41	34.54±5.33	0.0331*	12.71±0.92	12.82±2.40	0.9096	112.63±17.73	202.37±31.24	0.0001**

• Footer: P-values followed by * indicate significant differences between treatment and control by Student's T test at *≤5% significance (0.01< P-value <0.05) and **≤1% significance (P-value <0.01). Data correspond to mean values ± standard deviation.
• For A. nudicaulis from June to December n=10; January n=9; February n=7. For V. procera from June to January n=10; February n=6. Os valores seguidos de * apresentam níveis de significância menor que 5% e maior que 1% ( 0.01< P-value <0.05), enquanto valores reguidos de ** apresentam níveis de significância menor que 1% (P-value <0.01).

Regarding the diameter of the rosette, only V. procera presented significantly lower values in the treatment during January and February, with reductions of 10.89% and 15.03%, respectively (Table 2).

The leaf area (LA) of both species showed significant differences between treatment and control in January and February (Table 2). During these months, the treatment presented lower values by 14.26% and 43.13% in V. procera, and by 30.46% and 45.12% in A. nudicaulis (Table 2).

3.4. Relative water content (RWC) and specific leaf area (SLA)

The relative water content (RWC) showed a significant difference between treatment and control in plants of both species in December and February (Table 3). In these months, the treatment in V. procera presented lower values of 12.28% and 17.82%, respectively, while in A. nudicaulis, the treatment presented lower values of 9.27% and 8.62%, respectively (Table 3).

Table 3
Relative water content (RWC) and specific leaf area (SLA) in the leaves of V. procera and A. nudicaulis plants in treatment inside the OTC’s (T) and control outside the OTC’s (C).

V. procera	Months	RWC (%)		p-value	SLA (cm2. g-1)		p-value
		T	C		T	C
	June	84.92±2.09	83.61±4.16	0.5070	308.54±21.02	306.82±21.59	0.9529
	September	81.19±3.41	82.09±5.01	0.7239	256.84±15.19	254.29±30.76	0.8589
	December	60.26±3.84	72.54±5.68	0.0014**	257.56±23.22	262.01±14.83	0.7008
	February	41.27±3.59	59.09±2.18	0.0001**	286.44±8.64	278.31±13.90	0.2518
A. nudicaulis	June	89.25±4.48	92.94±3.84	0.1578	136.56±13.45	137.71±4.67	0.8492
	September	84.79±7.98	83.61±9.68	0.8222	183.31±14.06	188.17±16.77	0.5976
	December	67.44±5.31	76.71±2.97	0.0039**	194.34±18.54	189.65±9.52	0.5935
	February	56.96±4.90	65.58±2.98	0.0043**	204.55±20.53	209.63±15.54	0.6394

• Footer: P-values followed by * indicate significant differences between treatment and control by Student's T test at *≤5% significance (0.01< P-value <0.05) and **≤1% significance (P-value <0.01).
• Data correspond to mean values ± standard deviation. For A. nudicaulis from June to December n=10; February n=7. For V. procera from June to December n=10; February n=6.

The specific leaf area (SLA) of plants of both species showed no significant difference between treatment and control in any of the months evaluated (Table 3). However, comparing the SLA between the first and last month evaluated, V. procera showed a reduction in both treatment and control of 7.16% and 9.29%, respectively (Table 3). In contrast, A. nudicaulis showed an increase in both treatment and control of 33.24% and 34.31%, respectively (Table 3).

3.6. Plant weight

There was no significant difference in initial weight (IW) and the initial weight of the surviving plants (IWS) between the treatment and control of both species (Table 4). However, in the final weight of the surviving plants, there was a significant difference between treatment and control in both species (Table 4). The treatment showed higher values in V. procera and A. nudicaulis, with increases of 37.73% and 22.03%, respectively (Table 4).

Table 4
Weight of A. nudicaulis and V. procera plants. Footer: P- values followed by * indicates significant difference between treatment and control by Student's t test.

Species	Treatments	IW (g)	p-value	IWS (g)	p-value	Final weight (g)	p-value
V. procera	T	184.76±19.45	0.7789	186.7±2.75	0.2623	121.83±29.28	0.0018**
	C	182.84±14.65		183.21±6.64		195.66±31.27
A. nudicaulis	T	64.48±5.97	0.4478	65.78±5.45	0.4549	58.14±16.22	0.042**
	C	62.66±6.01		63.84±3.79		74.57±10.08

• ^*
  ≤5% significance and **≤1% significance. Data correspond to mean values ± standard deviation.
• IW: initial weight of plants (n=13), IWS: initial weight of surviving plants (n= V. procera 6; A. nudicaulis 7).

Comparing IWS to their final weight, it was observed that V. procera experienced a weight loss of 34.74% in the treatment and a gain of 6.79% in the control (Table 4). In A. nudicaulis, there was a weight loss of 11.61% in the treatment and a gain of 16.80% in the control (Table 4).

3.7. Dead plants

The first dead plants appeared in December (Table 5). In this month, A. nudicaulis had two dead plants in the treatment (Table 5). In January, V. procera had two dead plants and A. nudicaulis had four dead plants, both in the treatment (Table 5). In February, V. procera had seven dead plants in the treatment and one in the control, while A. nudicaulis had six dead plants in the treatment and two in the control (Table 5).

Table 5
Relative and absolute values of dead A. nudicaulis and V. procera plants.

Dead plants
Species	Treatments	December		January		February
		Absolutes	Relatives (%)	Absolutes	Relatives (%)	Absolutes	Relatives (%)
V. procera	T	0.0	0.0	2.0	15.4	7.0	53.8
	C	0.0	0.0	0.0	0.0	1.0	7.7
A. nudicaulis	T	2.0	15.4	4.0	30.8	6.0	46.2
	C	0.0	0.0	1.0	7.7	2.0	15.4

4. Discussion

The results of this study indicate that both bromeliad species studied acclimatized to the new climatic conditions of the treatment and control until around the fifth and sixth month evaluations (October and November), during which the bromeliad species showed positive growth rates. However, between the sixth and seventh months evaluated (November and December), both species under treatment and control conditions exhibited a growth interruption. This phenomenon suggests that the increase in local temperature during this period created limiting conditions for the studied bromeliads.

Although the growth metrics, the water status of the leaves (assessed here by the RWC), and the total mass of the plants indicate damage in both species under treatment and control, it was evident that the damage occurred initially and more severely in bromeliads exposed to OTC conditions. This is due to the summative effect of the increase in local temperature and the climate changes generated by the OTC’s, particularly the rise in temperature and VPD.

When temperatures exceed the tolerance limits of plant species, damage to growth and development can occur, which, if persistent, may become lethal (Hajiboland, 2012). Exposure to extreme temperatures leads to excess energy production during the photochemical stage of photosynthesis, which, if not used by the photosynthetic pathways, can result in the production of reactive oxygen species (ROS) and subsequent oxidative damage to plant cells (Imlay, 2003; Perales-Vela et al., 2007).

Another indication of severe damage in both bromeliad species under OTC conditions was the drastic reduction in RWC in the leaves. RWC reflects the hydration status of bromeliads, providing crucial information about their health (Freschi et al., 2010). Therefore, the low RWC values in the bromeliads studied, especially in the last month evaluated, indicate that OTC conditions induced the bromeliads to a progressive state of senescence.

Although the SLA of both species did not show significant differences between treatment and control, a distinct behavior was observed when comparing its variation over the months evaluated. While V. procera exhibited a gradual decrease in SLA, A. nudicaulis showed a gradual increase. SLA values are often associated with the resource acquisition and investment strategies of plants (Bongers and Popma, 1990; Pérez-Harguindeguy et al., 2013). Plants with high SLA tend to adopt more "acquisitive" strategies, investing less in leaf dry matter and exhibiting higher photosynthesis and growth rates (Pérez-Harguindeguy et al., 2013). Conversely, plants with low SLA tend to adopt "conservative" strategies, investing more in dry matter in leaves and having lower rates of photosynthesis and growth (Pérez-Harguindeguy et al., 2013). Therefore, this result suggests that V. procera may have adopted a more "conservative" strategy, while A. nudicaulis adopted a more "acquisitive" strategy.

Furthermore, the observed reductions in the biomass of the bromeliads studied are probably associated with the increased demand for energy reserves mobilized for stress tolerance mechanisms and the reduction in photosynthetic activity (Schrader et al., 2007). Zani et al. (2023) evaluated the ecophysiological performance of Allagoptera arenaria (Gomes) Kuntze, a palm found in the habitat of the bromeliads studied here, under simulated climate change conditions using passive OTC’s, and also observed reductions in plant biomass.

The significant mortality that began in December and reached around 50% in February for both bromeliad species was a consequence of the advanced state of senescence. These results highlight the permanent damage caused by the environmental conditions created by the OTC’s.

However, it should also be noted that the bromeliads were transplanted to the treatment and control conditions without their clonal rhizomes. Rhizomes allow plants to share resources such as water, nutrients, and chemical signals, which increases the survival chances of clonal modules in stressful environments (Liu et al., 2016).

5. Conclusion

The bromeliad species A. nudicaulis and V. procera were able to acclimate to the environmental conditions of the bare sand of Restinga and the OTC’s during a period of milder climate (June to September). However, when the conditions became more extreme (October to February), they stopped growing and suffered ecophysiological damage. The conditions of the OTC’s aggravated this damage, leading to senescence. A. nudicaulis showed greater tolerance to the stresses of the OTC’s compared to V. procera. These results are important, as they indicate that even the most optimistic climate change scenario (RCP 2.6 of the IPCC, 2021) can impair the growth and development of these bromeliads, which are essential for the structure and functioning of the Restinga communities.

Acknowledgements

The authors thank Universidade Federal do Espírito Santo (UFES). This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001. To Paulo Cesar Vinha State Park for allowing these activities to be carried out in that conservation unit.

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Publication Dates

• Publication in this collection
  21 Oct 2024
• Date of issue
  2024

History

• Received
  27 Mar 2024
• Accepted
  29 Aug 2024