I can remember my first research campaign to the mangroves. Barry Clough from the Australian Institute of Marine Science (AIMS) was leading, and we were aboard the RV Harry Messel. We sailed up from Cairns to the Daintree, arriving at the mouth of the river just after sunrise. There was a low dense fog over the river, and Cath Lovelock (then a graduate student and also new to the mangroves) and I stood on the bow as we sailed upstream. Spontaneously, we both called to mind Joseph Conrad’s Heart of Darkness, and imagined we were heading up the river looking for Kurtz.
Probably very few people have experienced this kind of introduction to their research system, and the convergence of our thoughts on Conrad is interesting in itself. But Conrad was certainly not the only one to consider tropical coastlines to be forbidding places. Friess 1, considered mangrove ecosystem services and disservices from the perspective of 19th century colonialist writers, examining 96 articles from the period. In general, he noted, the words used to describe the mangrove ecosystem were negative – impenetrable, dark, gloomy, monotonous, fetid, dismal, never-ending, and the site of “melancholy”. Mangroves harbored diseases spread by miasmatic vapors. And there were dangers from animals (snakes, crocodiles and tigers, depending on where you were), and indigenous peoples (who, understandably, had not infrequently found the colonial invaders to be undesirable).
These thoughts about mangroves persist today. Vilma, in Maryse Condé’s novel, Crossing the Mangrove (set in 1980s in Guadeloupe), says “You don’t cross a mangrove. You’d spike yourself on the roots of the mangrove trees. You’d be sucked down and suffocated by the brackish mud.” Conservation organizations seem to recognize this – in order to attract tourists to systems less charismatic than coral reefs, they construct boardwalks.
In the 19th century, the services (as opposed to disservices) that mangroves provided to European colonialists were more or less limited to extraction of resources and conversion of land to agriculture. That approach was, however, not limited to European colonialists; mangroves from East Africa had been exported to the Arabian peninsula for more than 800 years prior, and locally, mangroves as timber and fuel were certainly important. And they still are. Local inhabitants of the coastal zone have sustainably and efficiently used mangroves for fuel, timber, agriculture and coast line protection for centuries.
Nevertheless, as early as 1875, there was some appreciation of other services, e.g. mangroves in the Rufiji Delta (Tanzania) were understood to attenuate wave energy by “grasping the depths and grappling with the floods.” 1 Following the tsunami in 2004, field surveys confirmed the value of this service 2, but well before that, villagers (in, for example, northern Tanzania where sea fronts had been cleared, usually by some “developer” who dreamed of building a “resort”) knew that their shoreline was eroded when the mangroves were cut.
Less tangible, or at least less identifiable by scientific study are cultural ecosystem services, a term that refers to a range of social benefits, including tourism and recreation, but also sense of place, and spiritual and aesthetic value. Clearly, this service is provided by numerous other ecosystems, usually without recognition until the affected community protests against its loss.
In the last 20 years or so, scientists (“We”) have come to appreciate the services mangroves provide as breeding, spawning, hatching and nursing grounds for reef and pelagic species. As some 50% of all mangroves disappeared during the last half of the 20th century, the loss of this service was only slowly noted, similar to the losses of marine and freshwater fisheries during the same period. 2
What are mangroves?
Mangroves are a special class of halophytes – trees and shrubs which inhabit intertidal zone, i.e. the fringe between the ocean and land. They are found throughout the world on tropical coasts. Today, “We”, in the scientific and conservation communities, recognize that this placement gives them an important role in both terrestrial and ocean ecology. But as global communication approached the instantaneous in the past few decades, We have also become aware just how rapidly they are being decimated. The culprits include all the “usual suspects” – over exploitation, land conversion to uses more profitable in the short term (usually to outside interests), and climate change. At the same time, We have become aware of the critical services they provide and how those are falling by the wayside, adversely affecting both the human and non-human elements of the mangrove ecosystem.
Fortunately, over the years, mangrove systems have become the targets of a number of concerted conservation efforts directed specifically toward protecting and restoring them. Notable among these are the Mangrove Action Project, the Chinese Mangrove Conservation Network, the Nature Conservancy‘s Nature Works program, and the Papua New Guinea Wildlife Conservation Society‘s Rehabilitation and Protection initiative.
“Intertidal” does not, alone, say anything about the species involved, their relationships to each other, their evolution, their physiology or the structure and function of their genomes. Table 1 (see 3) lists some 62 species of mangroves, in 26 genera, 18 families and 11 orders. These include one monocot (Nypa fruticans) and one fern (Acrosticum aureum). Fifteen species and 4 hybrids are in the Rhizophoracea, the largest family. The borders of this list are unclear, partly because of continuing attempts to distinguishing between “true” mangroves and mangrove “associates”.4
The broad phylogenetic distribution of mangroves serves to emphasize the importance of convergent evolution in their origin. Broadly, mangroves share a tolerance of salinity from freshwater at least up to seawater levels, and of fluctuations in salinity with tidal and seasonal conditions.They are tolerant of high irradiance and high temperatures (but not low temperatures). They tolerate at least intermittent anoxia, associated with tidal flooding and growth in thick, mucky “soils”. They are well protected, chemically, against herbivores and pathogens. With respect to reproduction, both the world-wide distribution of mangroves and the low genetic diversity shown by a single species over a wide geographical range reflects the dispersal of their propagules by water.
As for the eXtreme credentials of mangroves, the most important may be that they are able to withstand and dissipate the energy associated with both normal and extreme storm-tide events, such as those associated with cyclones/hurricanes. In at least some species, e.g. the Rhizophoras, floating propagules can sink, root, and establish under water. Alternately, they can also sometimes establish on solid rock, in the manor of chasmophytes.
Mangroves arose on the borders of the extensive, ancient, tropical Sea of Tethys. Their subsequent dispersal depended on continued water passages between continents. Over the period involved, particularly in the late paleocene and eocene, those passages changed continuously and dramatically due to plate tectonics and continental drift. Around 18 MYA, dispersal was seriously restricted by the closure of the Mediterranean and the collision of Africa and Asia Minor. After that, the Indo West Pacific (IWP) and American East Pacific (AEP) mangrove flora developed independently. The Atlantic and eastern Pacific flora became isolated following the closure of the Panama gap ca. 3 MYA but that was recent enough that the genetic divergence of the American mangroves has not been major.
None of this, however, says anything definitive about the actual centers of origin of the different clades. Saenger 5summarized four proposed scenarios, concluding that Rhizophora and possibly Avicennia originated at the eastern, Indo-Pacific, end of the Tethys and dispersed westward through the Mediterranean. Aegialitis, Campostemon, and Scyphiphora arose in the same area, although somewhat later. Nypa and the mangroves in the Combretaceae, on the other hand, arose in the western (proto-Atlantic) Tethys, while Sonneratia (first), and Heritiera, Pelliciera and Aegiceras (later) are from the central (Mediterranean) Tethys region. By the mid Eocene, the extant flora had converged in what is now France and England. Subsequent migrations and local extinctions were determined by sea level changes and a late Eocene period of climatic cooling. The latitudinal ranges of individual species today are closely associated with rainfall and temperature patterns.6
From ecology to physiology
For good and obvious reasons, ecologists and managers look at mangrove forests as communities, with major questions directed at the population, community, or sometimes system levels. The forests themselves are, however, composed of individuals. Normal life in the best of times for any plant is a complex balancing act but ecosystem degradation brings with it new stresses and threats, new invaders, and new edaphic, atmospheric, and hydrologic problems. Plant communities which have co-existed with human communities for centuries are destabilized; their continued existence is far from assured.
Just as uncertainties in human societies call attention to the behaviors, responses and capacities of individuals, so do uncertainties in ecosystems. For plants, these are enabled by physiological plasticity and manifested in physiological performance. Performance in response to challenges allows us to witness and understand the complexity of organismal integration central to survival as an individual.
Because physiologists are concerned with what an individual plant has to accomplish in order to live where it does, they are concerned with suites of physiological characteristics, sometimes called “strategies”, that allow plants to overcome environmental constraints.7 Thus, for mangroves or any other eXtreme system, physiologists contribute importantly to the understanding of what happens – at the organismal and biochemical levels – when a plant does, or does not, maintain its place in the ecosystem.
Thus, for more than a century there has been extensive physiological work on mangroves – on their water relations including hydraulic conductivity and the repair of cavitation/embolisms8, on acquiring and allocating to nutrients, especially in oligotrophic environments 9, on responses to flooding, both in the short term and associated with global change10, on photosynthesis and the allocation of photosynthate to multiple tasks11, on photoprotection12, on secondary chemistry including the production of tannins, phenolics and their roles1314, on management of salt contents, both by excretion and by exclusion. 1516 Each of these is highly variable between species. Table 2 shows a simple example of this, comparing 4 non-excreting mangroves from one hypersaline site in the Daintree River.
From physiology to molecular genetics
Having established a progression – historical and biological – from the ecosystem/community level through the physiological level to the subcellular, it is understandable that an emphasis on molecular genetics has come to mangrove studies. This was really made possible first by “next-gen” sequencing, and then by single large molecule sequencing and ever falling sequencing costs. For mangroves as for all other eXtreme plants, however, the importance of the subject can easily be lost in the excitement of, for example, being the first to sequence x, or of publishing the stats associated with the sequencing and assembly, or of identifying GO categories or KEGG pathways more heavily represented than in Arabidopsis.
The first big sequencing effort devoted to mangroves was that by Boping Ye and Wei Sun who sequenced and deposited 22400 ESTs for Bruguiera gymnorrhiza in 2008. There was apparently no publication associated with this. This was followed in 2009 by the first large scale 454 GS FLX de novo transcriptome analysis of two mangroves, Heritiera littoralis and Rhizophora mangle by Maheshi Dassanayake and co-workers. 17 Importantly, they normalized the samples, reducing the representation of some very abundant transcripts and uncovering the representation of rare transcripts. Associated with this, the authors also annotated all then-available mangrove sequences 18 and made them available in the mangrove transcriptome database. Unfortunately, that database has seen only minor updating since 2010.
Concentrating only on more recent efforts that have been associated with publications, much – even most – of the work has originated in the lab of Suhua Shi (Sun Yat-Sen University, Guangzhou, China). For a complete list of her mangrove-related publications at PubMed, click here.
Continuing the “lifestyle” consideration initiated by Dassanayake et al., Wen et al. 19 examined the small RNA transcriptomes of Bruguiera gymnorrhiza and Kandelia candel, finding both conserved and mangrove-specific miRNAs and targets. Differential expression between the mangroves and non-halophytes called to mind responses to “stress” reported for Arabidopsis under Petri dish conditions. B. gymnorrhiza, emphasized more heavily in this study, showed some highly abundant but less conserved trans-acting siRNAs and an expanded set of potential targets. The authors hypothesized that the results reflected the “evolutionary alteration of sRNA expression levels and the rewiring of sRNA-regulatory networks”, putatively associated with stress adaptation. Similar results were reported separately for Avicennia marina.20
As noted above, all but a very few mangroves are dicot trees. Of the others, two mangrove ferns, Acrostichum aureum and A. speciosum. have been sequenced at the transcriptome level, but could only partially be annotated using public databases. 21 This undoubtedly reflects the paucity of sequencing data for ferns. A Nypa transcriptome sequencing project has been deposited but not published.
A number of other sequencing projects have been deposited in NCBI and other data bases, but without associated publications. Please see Genome Resources to access their details.
The number of mangrovelers working at the molecular level is very small and the long life cycle and complexity of mangrove field conditions makes any study of them, at any level of organization, difficult. To date, in publications, there has been a pronounced tendency to dwell on the mechanical and statistical details of the sequencing project, with much less consideration of real biological problems. Nevertheless, the number of deposited datasets at the transcriptome and, more recently, microbiome levels is growing. As the quality and quantity of reference transcriptomes grows, there is real promise of more complex, treatment-based expression studies, even under field conditions.
[This page was written by John Cheeseman who gratefully acknowledges more than 30 years of collaboration and collegiality from the world-wide community of mangrovelers.]