Enhancing restoration success of rare plants in an arid-tropical climate through water-saving technologies: a case study of Scalesia affinis ssp. brachyloba in the Galapagos Islands

Introduction

Despite occupying less than 5% of the global terrestrial area, oceanic islands are home to >20% of the planet’s terrestrial plant and vertebrate species (Courchamp et al., 2014). The Galapagos archipelago and its flora are no exception, with 37% of its plant taxa as endemic (Tye & Francisco-Ortega, 2011). Despite its globally recognized significance, the Galapagos flora is currently under high levels of degradation (Jaramillo et al., 2013) and extinction risk (Tye, 2007) which has led to Galapagos flora becoming the focus of major restoration activities in the last decade (Jaramillo et al., 2020). In the Galapagos, as in other arid tropic regions, dry forest species are some of the most threatened species due to land-use change and stochastic rainfall seasonality, which can undermine regeneration (Myers, Mittermeier & Mittermeier, 2000; Khurana & Singh, 2001; Tye & Francisco-Ortega, 2011; Gillespie et al., 2013).

The scarcity of water and high summer temperatures in arid environments are some of the main challenges of restoration programs in these climates (Cabin et al., 2002; Will et al., 2013). Although tropical climates have wet summers, climate change has altered rainfall predictability, making plants more prone to senesce when water is scarce (Nieuwolt, 1991; Anderegg, Anderegg & Berry, 2013). Water-saving technologies (WSTs) (i.e., equipment or tools that can reduce the changing levels of water balance in soil) can improve seedling survival by providing regular supplies of water and have been useful in restoration programs in other arid regions around the world (Jaramillo et al., 2020). WSTs have the potential to accelerate Galapagos plant species’ restoration by making them less susceptible to rainfall seasonality. For example, given that water limitation has been identified as a key driver of seedling survival, preliminary restoration activities with these technologies have shown promising results (Tapia et al., 2019; Negoita, Gibbs & Jaramillo, 2021).

We focused on Scalesia affinis ssp. brachyloba as a model taxon to investigate the effect of WSTs on improving species restoration. In 2013, the Charles Darwin Foundation (CDF), via the Galapagos Verde 2050 (GV2050) program, began an initiative to increase populations of Scalesia spp., with a particular focus on S. affinis ssp. brachyloba which only grows in arid-tropical conditions (Beck et al., 2018) in the south-west border of Santa Cruz Island (Harling, 1962). The species’ has evergreen leaves and a long taproot, functional characteristics for a dry environment (Atkinson, Jaramillo & Tapia, 2009), making it an ideal candidate for testing the potential value of WSTs. Results from this study may also be useful for understanding other species in this genus. Scalesia (Asteraceae) is the most diverse of seven endemic genera of the Galapagos, with 15 species and more than 20 taxa, and is often cited as a prominent example of adaptive radiation (Adsersen & Svendsen, 1986; Eliasson, 1974; Tye, 2003) from colonizing barren lava fields, to forming a forest canopy (Hamann, 1979a; Itow, 1995; Kelager & Philipp, 2008; Atkinson, Jaramillo & Tapia, 2009; Watson et al., 2009). Many Scalesia spp. are threatened by anthropogenic habitat changes, introduced species, and the changing climate (Lawesson, 1986; Caujapé-Castells et al., 2010). The population of S. affinis ssp. brachyloba (hereafter S. brachyloba) on Santa Cruz Island has dramatically declined (Atkinson, Jaramillo & Tapia, 2009). The historical distribution of the taxa was in the same area where the human settlements have established and expanded on Santa Cruz Island (Harling, 1962; Watson et al., 2009; INEC, 2015). By the year 2000 the population of S. brachyloba within the main town of Puerto Ayora was recorded at five individuals (Nielsen, 2004; Kelager & Philipp, 2008), and by 2007 all areas with previously large populations of S. brachyloba had seen population declines (Jaramillo, 2007). Low natural and assisted regeneration of the species hinders its restoration. For example, the species may reach only 17% survival 3 months after germination, and 19% one year after transplanting to the wild (Atkinson, Jaramillo & Tapia, 2009).

Here we aim to use S. brachyloba both as a study taxon for evaluating the effect of a water-saving technology (Groasis Waterboxx®, hereafter just “Groasis”) on dry forest species, but results may also inform future restoration efforts of this species on Santa Cruz Island, Galapagos. Through this process we also account for the influence of the two main factors that shape arid-tropical climates: precipitation and maximum temperature.

Materials & Methods

Through regular monitoring over six years, we collected data on the survival of S. brachyloba seedlings that were planted (under National Park permission N° PC-10-21) using treatments that included Groasis and controls (no technology). We also used available data from associated environmental conditions (Jaramillo et al., 2020).

Study area, sites, and target species

Our study sites were based on the southwest border of Santa Cruz Island (−0.7351, −90.3089)—the second largest island on the Galapagos archipelago (Helsen et al., 2009), in the dry lowland zone of the island. The climate in this zone is arid tropical with a median annual rainfall of 227 mm, though 71% of this precipitation occurs during the wet season months of January through May and mean monthly temperature ranging from 19° to 30.5 °C (Beck et al., 2018; Trueman & D’Ozouville, 2010). Vegetation community is mostly xeric, composed by S. affinis, Oputia echios and Croton scouleri (Huttel, 1986). Soils are mainly clay or clay-loam (Hengl et al., 2017). We studied S. brachyloba at six sites which totaled an area of one hectare and were all locations where S. brachyloba had been historically found—locations that were confirmed by samples in the CDF Herbarium (Jaramillo et al., 2018), observations, and photographs (Jaramillo, 2007; Atkinson, Jaramillo & Tapia, 2009) (Table 1, Fig. 1). Two sites correspond to natural populations: one site was an enclosed area of national park land in an area called ‘Garrapatero’ in the southeast of the island and another site called ‘Mirador’ was on public land in Puerto Ayora (Jaramillo, Tapia & Tye, 2018). The other four sites were all small gardens located in Puerto Ayora, Galapagos at the Biosecurity Agency (GBA), the Galapagos National High School, the offices of the Galapagos National Park Directorate (GNPD), and the Charles Darwin Research Station (CDRS) (Fig. 1).

Table 1:

Planting age summary of Scalesia affinis ssp. brachyloba by study site, treatment and planting date.

Site	Treatment	Count	Mean		SD	Median	CI_Lower	CI_Upper
GBA	Control	1	124,0	±	NA	124	NA	NA
	Groasis	30	510,7	±	560,6	124	301,4	720,1
CDF	Control	3	456,7	±	456,8	305	0,0	1591,4
	Groasis	22	650,2	±	539,6	407	410,9	889,4
Galapagos College	Groasis	4	1277,0	±	8,0	1273	1264,3	1289,7
Garrapatero	Control	25	60,6	±	29,3	42	48,6	72,7
	Groasis	155	350,8	±	255,0	297	310,4	391,3
GNP	Control	1	1352,0	±	NA	1352	NA	NA
	Groasis	5	844,2	±	564,2	1130	143,7	1544,7
Mirador	Control	18	131,9	±	308,5	46	0,0	285,3
	Groasis	110	625,3	±	476,4	583	535,3	715,3

DOI: 10.7717/peerj.16367/table-1

Notes:

Count = number of plants used. Summaries are mean planting age (days ± SD) and median planting age plus the lower and upper limit for its 95% confidence interval.

Results

Plants grown with Groasis generally had a greater planting age at death than those grown without Groasis, with a median survival of at least 1.25 years (455 days, 335 to 569 95% CI) for Groasis compared to 46 days (42 to 95 95% CI) for controls (Fig. 2). This difference in survival was marked predominantly in the first two years. By 3.7 years of monitoring, both treatments had become more stable, with a three-fold higher survival of Groasis at 16% (± 2% s.e.) compared with controls at 5.1% survival (±3.3% s.e.) (Fig. 2). For controls, this corresponds to only one plant surviving, in GNP gardens (Table 1).

The selected model had a better performance than all other models tested (Table 2), and we found that all interaction effects were significant predictors of S. brachyloba survival [χ² = 116.28 (df = 7, n = 374), p < 0.01 to χ² = 15.5 (df = 3, n = 374), p < 0.01, depending on the models compared]. When controlling for all other factors we found that treatment was a significant predictor of S. brachyloba when grown with Groasis (Fig. 3) (χ² (df = 1, n = 374) = 48.67, p < 0.01), showing a high variation when grown without the technology (control). Since these effects come from a 3-way interaction model, their independent significance should be interpreted with caution, as the main effects are marginal to the full interaction. Treatment remained significant when the interaction was removed on a type II Wald Chi Square test, and when the dataset was balanced by resampling Groasis and controls (48 each) (Fig. 3; inset graph). The interaction between the three factors included in the model had an overall positive effect with odds ratio −1 of 16.585 (Table 3). When maximum temperature is segregated in two groups, total precipitation had a positive effect on predicted survival of controls (Fig. 4), particularly under conditions of 27 °C or below. On the contrary, predicted survival of plants growing with Groasis technology showed a neutral or slightly negative trend with increasing temperature and precipitation. We included planting age to account for any change due to age-related factors, and its trend was negative (Table 3, Fig. S1; coef = −0.41) but its overall effect was non-significant.

Discussion

Our results suggest that water limitation is an important factor for the early-stage survival and restoration of S. brachyloba. We found that water availability through precipitation increases the survival of this species and the use of Groasis consistently improved survival (Table 3, Figs. 3 and 4), probably by providing a balanced input of water. However, survival differences between control and Groasis narrowed two years after planting (Fig. 2). This coincided with when most Groasis boxes were removed, suggesting that S. brachyloba plants may benefit from a longer application of this technology. Additionally, as the study was part of a large-scale restoration project framework, there were certain limitations in the experimental design because not all combinations of treatments could be applied (e.g., applying the same volume of water to Groasis and controls), thus, effects of water availability presented here confounded the application of the Groasis technology.

Individuals of S. brachyloba usually exhibit resilience in their survival during extended periods of reduced water-availability. Having evolved with regular drought, arid-tropical species such as S. brachyloba may be resilient to such conditions (Hamann, 1979b; Riedinger et al., 2002). The Galapagos archipelago’s location is within the El Niño Southern Oscillation (ENSO) region making it subject to drought and rainfall cycles that are especially pronounced during strong events, with some years seeing up to 3 m of annual precipitation (Trueman & D’Ozouville, 2010). Many plant species in Galapagos, including Scalesia spp., benefit from short-term increases in rainfall associated with El Niño events (Tye & Aldáz, 1999), as seen in other arid-tropical plant populations following an El Niño event (Polis et al., 1997). This period is followed by a large spike in mortality of adults from long-term exposure to water via precipitation. This may explain why the plants grown with Groasis showed a weak negative trend with increasing precipitation (Fig. 4), indicating that the water added to the technology plus high levels of rainfall may be more than the amount that S. brachyloba can withstand. Nonetheless, even the lowest values of predicted survival in Groasis were close to the maximum predicted survival for controls (Fig. 4), indicating that even in extremely humid events, too little water has a more detrimental effect on S. brachyloba than too much water, providing a support to the value of using Groasis despite intense rainfall events.

The Galapagos hot season (i.e., warmer land and sea surface temperatures from January to May and high rainfall variability) principally determines dry-zone species’ annual productivity, such as that of S. brachyloba (Snell & Rea, 1999; Trueman & D’Ozouville, 2010; Larrea & Di Carlo, 2011). Our results similarly show that predicted survival was associated with rainfall, and that under lower maximum temperatures (in the June-December cold season) this interaction is more evident (Fig. 4). Although the test of temperature above or below 27 °C in this study was arbitrary and only for visualization purposes, one possible explanation is that S. brachyloba may be more active below certain temperature thresholds. Many tropical forest species are known to have a threshold around 27–29 °C where photosynthesis starts to decline but respiration increases (Mau et al., 2018). Further research addressing temperature threshold for Galapagos’ plant species is needed to evaluate this hypothesis.

Overall, most high mortality rates in S. brachyloba appeared either after periods of cold temperature and high rainfall (>50 mm per week, maximum temperature <27 °C) (Fig. S2) or after periods of warm temperature and low rainfall (<50 mm per week, maximum temperature >27 °C), indicating two extreme conditions that may constrain species development. The link between high water availability and other Scalesia species’ mortality has been attributed to root rot, high winds, and vine overgrowth (Tye & Aldáz, 1999; Hamann, 2001; Larrea & Di Carlo, 2011). While temperature and rainfall influence the species’ survival, the causal mechanism was not addressed in this study. Further research is needed to establish how weather conditions directly shape S. brachyloba seedling survival. Research on S. pedunculata has shown that large-scale, rainfall-induced mortality makes way for the next cohort of young plants (Itow & Mueller-Dombois, 1988; Itow, 1995; Tye & Aldáz, 1999; Hamann, 2001; Larrea & Di Carlo, 2011; Jäger et al., 2017). Rainfall, especially during extreme weather events, may thus influence the natural regeneration cycles of related species. Similar patterns, though less pronounced, have been found in the mortality and regeneration of five dry-zone Scalesia species in response to the high rainfall of El Niño events (Tye & Aldáz, 1999; Hamann, 2001; Larrea & Di Carlo, 2011). All in all, the results of this study are informative in addressing potential planting windows for S. brachyloba by avoiding the most extreme conditions.

Our study only applies to the first few years of growth in young S. brachyloba, a period less than both the species life expectancy and ENSO events; therefore, future research should consider longer-term demographic changes in response to weather conditions. Other challenges of the current study include the large variability between sites. Evaluating site differences were beyond the scope of the study since our goal was to extract general trends on the use of WSTs for the focal species. Nonetheless, future work should seek to further examine the importance of local conditions. For example, no plants survived more than 851 days at the Garrapatero site, which may be due to its much more rural location, where plants may be more susceptible to pest attacks (P Jaramillo, pers. obs., 2019). The overall low sample and imbalanced design is also a fundamental limitation of this study. This is largely due to the focus on conservation of a rare species that is already limited in sample size (i.e., restoring S. brachyloba), and retrospective nature of the study (the study was conducted using data that were collected prior to a central experimental design). These limitations reduce the strength with which our results can be generalized, and it is imperative that additional prospective studies are conducted for further assessing the best tools for effectively restoring S. brachyloba and other species of conservation concern in Galapagos.

Galapagos arid-zone rainfall is largely determined by sea-surface temperatures, and global climate change is expected to create a wetter and warmer climate in the Galapagos (Trueman & D’Ozouville, 2010; Larrea & Di Carlo, 2011). It is more important to understand how these changes may affect endangered species in the Galapagos, especially by examining the effect of water availability and temperature on their survival and growth. This study gives insights into the effects of both factor on the early growth of S. brachyloba and shows promise in the use of water-saving technologies to improve survival in the face of climatic fluctuations. However, further investigations into the life cycle of S. brachyloba across more conditions and larger time frames are necessary to inform a more complete restoration plan for this species.

Conclusions

The restoration of endemic species in tropical dry forest ecosystems is needed to prevent the continued degradation of these habitats (Gillespie et al., 2013). Water-saving technology has the potential to increase the survival of dry forest plant species, such as Scalesia affinis ssp. brachyloba. This study investigated S. brachyloba’ relationship with two main weather conditions in arid-tropical climates: precipitation and maximum temperature, and from this, has been able to determine the effectiveness of a WST on its survival. Application of similar experimental efforts using WSTs on endangered dry forest species may produce similar positive successes, but understanding other factors that impact the species’ early establishment is essential for contributing to the recovery of a globally threatened ecosystem.

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