Conceived and designed the experiments: AWRS CAF MJL KJW. Performed the experiments: AWRS MJL. Analyzed the data: AWRS. Contributed reagents/materials/analysis tools: AWRS CAF MJL GAM. Wrote the paper: AWRS GAM.
The authors have declared that no competing interests exist.
The Intergovernmental Panel on Climate Change (IPCC) provides a conservative estimate on rates of sea-level rise of 3.8 mm yr−1 at the end of the 21st century, which may have a detrimental effect on ecologically important mangrove ecosystems. Understanding factors influencing the long-term resilience of these communities is critical but poorly understood. We investigate ecological resilience in a coastal mangrove community from the Galápagos Islands over the last 2700 years using three research questions: What are the ‘fast and slow’ processes operating in the coastal zone? Is there evidence for a threshold response? How can the past inform us about the resilience of the modern system?
Palaeoecological methods (AMS radiocarbon dating, stable carbon isotopes (δ13C)) were used to reconstruct sedimentation rates and ecological change over the past 2,700 years at Diablas lagoon, Isabela, Galápagos. Bulk geochemical analysis was also used to determine local environmental changes, and salinity was reconstructed using a diatom transfer function. Changes in relative sea level (RSL) were estimated using a glacio-isostatic adjustment model. Non-linear behaviour was observed in the Diablas mangrove ecosystem as it responded to increased salinities following exposure to tidal inundations. A negative feedback was observed which enabled the mangrove canopy to accrete vertically, but disturbances may have opened up the canopy and contributed to an erosion of resilience over time. A combination of drier climatic conditions and a slight fall in RSL then resulted in a threshold response, from a mangrove community to a microbial mat.
Palaeoecological records can provide important information on the nature of non-linear behaviour by identifying thresholds within ecological systems, and in outlining responses to ‘fast’ and ‘slow’ environmental change between alternative stable states. This study highlights the need to incorporate a long-term ecological perspective when designing strategies for maximizing coastal resilience.
Tropical mangrove ecosystems provide essential economic, geomorphological, and ecological ecosystem services by stabilizing eroding coastlines and offering protection from extreme storm surge and tsunami events. They also provide nurseries for economically valuable fishes and crustaceans, and a fuel wood source to local populations
Mangrove ecosystems consist of a series of vegetation communities dependent on an elevation gradient, comprised of mangroves, saltmarsh, and cyanobacterial microbial mats which are organized in parallel zones along the coast
The ability of an ecosystem to ‘tolerate or adapt to disturbance without collapsing into a different or qualitative state’
Resilience is a critical concept in contemporary ecology and has been applied at the local, regional, and global scale
In this study we investigate ecological resilience in a mangrove ecosystem from the Galápagos Islands. We use stable carbon isotopes (δ13C) and AMS radiocarbon dating to examine two key ecological responses in mangrove systems – community compositional change and increasing accumulation rates – to environmental changes over the past 2,700 years. Past changes in salinity are reconstructed using a diatom transfer function in order to estimate short-term tidal disturbances. Geochemical data is used to examine the long-term environmental changes that occurred at the coastal site. and results are also compared to high-resolution palaeoclimatic data from a nearby crater lake
Diablas lagoon is a 79 ha coastal lagoon situated on the south coast of the island of Isabela (0°57′6.51″S, 90°59′9.69″W). The lagoon is at sea level, and is separated from the sea by a 6 m high mangrove boundary and sandy beach, 10–300 m in width (
(A) Map of the Galápagos Islands. Diablas lagoon is located in the Diablas wetlands on the south side of Isla Isabela. (B) Satellite image of the Diablas wetlands. The coring location is marked with a circle on both satellite images and the lagoon outline has been traced (
A 4.9 m sediment core was taken in 0.8 m of water in Diablas lagoon, close to the northern fringe of
Age chronologies for each sediment sequence were developed from eight samples using bulk accelerator mass spectrometry (AMS) radiocarbon dating (
Laboratory Code | Depth (cm) | Lab ID | Modern Carbon (%) | δ13C (‰) | 14C age (yr BP) | 2σ Cal. Age (yr BP) |
OZI797 | 56 | OXR-1 | 95.7±0.5 | −10.7 | 350±40 | 285–485 |
UBA11498 | 144 | ISD_144 | 87.7±0.2 | −12.1 | 1051±17 | 860–970 |
UBA1499 | 146 | ISD_146 | 877.2±±0.2 | −24.5 | 1098±17 | 910–990 |
OZI798 | 240–242 | OXR-2 | 83.7±0.6 | −24.0 | 1430±60 | 1165–1405 |
UBA11500 | 311 | ISD_311 | 78.9±0.2 | −23.5 | 1908±18 | 1705–1865 |
UBA11501 | 387 | ISD_387 | 76.9±0.2 | −28.6 | 2114±18 | 1935–2115 |
OZI1799 | 440-443 | OXR-3 | 75.7±0.4 | −28.6 | 2240±18 | 2070–2380 |
UBA-14628 | 483 | ISD_483 | 72.34±0.3 | −26.4 | 2601±28 | 2470–2790 |
Bulk sediment accelerator mass spectrometry (AMS) radiocarbon results calibrated using the IntCal04 Southern Hemisphere Curve
The carbon isotope signature was used to detect major ecological shifts in autochthonous productivity (
Carbon isotope composition (δ13C) and C/N of the surface and core samples were measured at the NERC Isotope Geoscience Laboratory, British Geological Survey. A sampling resolution of 4 cm was used. Samples were washed in 1 mol HCl to remove carbonates, rinsed with distilled water and sieved under a vacuum using 2 µm filter paper. They were dried, crushed and then weighed into tin capsules. 13C/12C analyses were performed by combustion in a Costech Elemental Analyser (EA) on-line to a VG TripleTrap and Optima dual-inlet mass spectrometer, with δ13C values calculated to the VPDB scale using a within-run laboratory standards calibrated against NBS18, NBS-19 and NBS-22. Replicate analysis of well-mixed samples indicated a precision of ± <0.1‰ (1 SD). C/N ratios can also by measured if required, and these are calibrated against an Acetanilide standard. Replicate analysis of well-mixed samples indicated a precision of ± <0.1.
A stable isotope mixing model
(A) C/N and δ13C results of surface samples of mangroves and microbial mats in Diablas; (B) Comparison between linear fitting (dashed line) and the logistic curve (full line) fitting methodology used in our model. (C) Stable isotope values and (D) mixing model output for Diablas lagoon.
A logistic curve was fitted to these values using least squares regression (
In this model, the dominant source of organic material is assumed to be autochthonous. Therefore, the model reflects the accretion of organic material growing in the lagoon at the sampling point. In terms of biological distributions, an index value of 0 indicates an open water lagoon with no mangroves living at the coring site. Conversely, an index value of 1 indicates that the site was completely covered by mangroves above the surface; i.e an expansion of mangroves growing within the lagoon.
Changes in the abundance of elements in a sediment profile can be used to infer past changes in palaeoecological and palaeoclimatic conditions (
Geochemical variations in 18 rare earth elements from the core from the Diablas lagoon. The dashed-red line denotes the major sediment transition identified in
Traces of geochemical elemental concentrations were measured at 4 cm intervals on 0.2 g of dry sediment using ICP-AES (Inductively Coupled Plasma-Atomic Emission Spectrometer) after applying a bulk sediment digestion technique
Salinity changes were estimated using a Weighted Average (WA) diatom transfer function with downweighting for rare species
One cm3 diatom samples were taken from both surface material and from sediment cores. The sediment core was subsampled at a resolution of 4 cm. Samples were prepared using the standard diatom digestion preparation procedures
Shorelines in the Galápagos have varied on glacial-interglacial timescales, with sea levels approximately 120 m lower during the Last-Glacial Maximum (LGM) due to an increased proportion of the global water budget locked in terrestrial ice caps
Note that for the RSL data, seven different modelling parameters are provided (see methods section). The medium parameter model is marked by the thick-blue line. Grain size data is from El Junco crater-lake, San Cristobal (see ref. 19).
Climatic conditions in the Galápagos are driven by variability in the El Niño Southern Oscillation (ENSO), which results in a close correlation in weather patterns across different lowland sites (
The core is separated into two major stratigraphic sections, an upper section (top-145 cm) of composed of pink, gelatinous sediment which is indicative of a microbial mat (
Radiocarbon dating results are provided in
There is a transition from low (approx – 27‰) to high (approx – 12‰) δ13C at 940 cal yr BP (
The major stratigraphic and isotopic changes observed above are easily identifiable in the geochemical signature of the Diablas core (
Mg, Mn, and Li were found in higher abundances at the top of the sequence and were therefore associated with the microbial mat. The reduction of Mn is the first decompositional process used to gain energy from organic matter in anaerobic sediments
Between 2020–1600 cal yr BP, there were peaks of Fe, Al, and Ti in the sedimentary sequence (
The core is generally composed of benthic brackish water diatoms and experienced a transition of species from the base of the record to the present day (
Output from the GIA model indicates that sea level increased steadily at our study location, and reached a small highstand of between 0.1–0.4 m between 2000 and 1000 cal yr BP. The predicted amplitude of the highstand is dependent on the adopted Earth viscosity model. This pattern of RSL change was observed in all but one of the model runs (that with a relatively high lower mantle viscosity of 5×10221Pas), which showed a steadily rising RSL for the past 3,000 years. The predicted change from a RSL rise to fall is due to the reduction in (predominantly Antarctic) ice melt rate during the late Holocene
Sedimentation at the coring site in Diablas began at 2,670 cal yr BP and is probably linked to the fact that relative sea levels were approaching their highest since the Last Glacial Maximum
2020–1600 cal yr BP was an important period of environmental change at Diablas lagoon. Modelling results indicate that sea levels reached a maximum at around this time (between 0.15–0.4 m above present day levels), whilst a number of shorter term, higher energy events were also observed in the record and are the result of a breaching of a seaward barrier (
Despite the increasing exposure to tidal surges, mangroves remained the dominant source of biogenic accumulation at the coring site over this 400 year period. An interesting result is the fact that, at the same time that diatoms were removed from the record through tidal disturbance, and when salinities in the lagoon began to increase dramatically, mangrove accumulation rates had peaked at around 5.7 mm yr−1. In this way, the mangroves were able to accrete vertically in line with the tidal inundations, a common response which encourages the stability of the canopy through time (see below).
In addition to this vertical accretion, between 1960–1270 cal yr BP, stable isotope evidence indicates a shift to more variable, heavier isotopes of carbon. Benthic microbial mats are common at the surface of scrub mangrove forests, and it is likely that this represents a reduction or opening of the canopy as following the higher-energy tidal inundations
At 940 cal yr BP, there was a rapid ecological transition from mangroves to a microbial mat, as evidenced by both stable isotopic, geochemical, and stratigraphic evidence (
The Diablas wetlands have been highly dynamic for the past 2,700 years experiencing significant environmental and ecological changes linked to GIA, high-energy tidal disturbance events and climatic change. These can be organized into a series of ‘fast’ (<50 years, the lowest average resolution available between three samples in our record) and ‘slow’ (>50 years, i.e. decadal-centennial, e.g.
Taking the predictions from the GIA model with intermediate parameters, a sea-level highstand of around 0.15 m occurred at 2000 cal yr BP. Since, sea levels were predicted to have changed at an order of magnitude lower than the sedimentation rates observed in our record, the rapid sediment accumulation rates must be associated with other, long-term, geomorphological processes. It is likely that the 4.9 m accumulation resulted from the infilling of the basin as it experienced increasing tidal influence and RSL rise (
Alternatively, some of the additional sediment accumulation may also have resulted from tectonic subsidence. This is common in volcanic archipelagos such as the Galápagos, where active islands to the west of the archipelago (Isabela) can experience local-regional scale changes in land elevation through gradual subsidence or sudden landslip events
The system was also punctuated by a series of higher-energy disturbance events associated with above-ground tidal surges (
Palaeoclimatic evidence from El Junco crater lake from the highlands of San Cristobal indicate frequent changes in the strength and magnitude of ENSO over the past 2,700 years, resulting in changes in the precipitation regime on annual-decadal timescales
Non-linear responses to environmental change occur as a result of negative feedback processes which maintain a system in an equilibrium state. A key negative feedback identified in mangrove ecosystems is the accumulation of organic material in response to a tidal influx
A) Stable isotope mixing model results indicating the main ecological changes at the Diablas lagoon. B) Phase plot to indicate the presence of alternative stable states (mangroves and microbial mat) in the lagoon system. The point at which the threshold between the two states was crossed is marked by a red dashed line. Detailed chronological summary is as follows. (i) 2770 cal yr BP- resilient mangrove stand at the coring site; (ii) 2000 cal yr BP- increase in sediment accumulation rates denotes feedback response of resilient mangroves in response to environmental disturbances; (iii) 1400 cal yr BP- opening of the mangrove canopy due to preceding tidal disturbance events, eroding resilience over time; (iv) (940 cal yr BP) Drier background climatic conditions and slightly decreasing RSL combine, resulting in threshold transition to microbial mat; (v) present day; contemporary lagoon conditions with cyanobacterial mat at the sediment surface.
According to resilience theory, the accumulation of slow processes can result in an erosion of resilience over time, making a system more susceptible to smaller perturbations and environmental changes. We propose that the historical period of disturbances occurring after 2000 cal yr BP, which had the effect of the opening up the mangrove canopy, caused an erosion of resilience at our study site (
Indeed, the transition to a microbial mat in Diablas occurred at a time of drier climatic conditions in the EEP
These findings have important consequences in our understanding of the ecological response of mangrove ecosystems to future environmental change. Future predictions on the rates RSL rise linked to climate change are uncertain, but the central estimate of the rate of rise at the end of the 21st century is 3.8 mm yr−1
However, in our study the resilience of mangroves was eroded by a series of historical processes and, as a result, a combination of arid conditions and slow RSL change eventually resulted in a threshold transition to an alternative stable state. Thus, our study implies that in this system, understanding the patterns of past historical processes are essential for determining baselines and for investigating ecological responses. The study highlights the need to incorporate a long-term ecological perspective when designing strategies for maximizing coastal resilience.
Palaeoecology is increasingly being applied as a tool to identify long-term baselines and thresholds in ecosystems at the local-regional scale
(EPS)
(EPS)
(DOC)
The authors thank Simon Haberle, Iona Flett, Jim Neale, Henk Heijnis, Iain Robertson, Emily Coffey, Benson Schleisser, and Salome Maldonado for their tireless efforts in the field. We thank Keith Bennett for providing the funding for 5 of the 8 radiocarbon dates. The palaeoclimate data was donated by Jessica Conroy (University of Arizona). Thanks also to Kaarina Weckström (University of Copenhagen) for supplying the MOLTEN surface data for the diatom transfer function and Maarten Blaauw (University of Belfast) for modifying the code in his CLAM software in order to estimate sedimentation rates. ICP-AES analyses were performed at the NERC ICP facility based at Royal Holloway University of London. This is publication number 2039 from the Charles Darwin Research Station, Puerto Ayora, Galápagos.