Mangroves in the Sky

Evolution of mangroves interests me and in this blog I have often written about the specific situations that may give rise to new mangrove species.  I am fairly convinced that mangrove soils are just as big a barrier to mangrove evolution as salinity.  The US Government actually maintains a database of salinity resistant plants with several thousand species in it so why don't these species dominate our shores?  What if plants could adapt to mangrove soils first and later learn to live in the intertidal zone where they are exposed to high levels of salinity?  Evolving in two steps rather than one might greatly reduce the entry barrier to mangrove evolution.  I know of a place where this process is possible, where mangrove soils have risen out of the sea and have become mountains of mud – Gulf Province in Papua New Guinea.

Small plateau with near vertical sides are common and landslides are frequent

At 125 m above sea-level and about 50 kilometres inland, I was looking at the stream banks and realised that the patterns in the rocks were the preserved burrows in marine invertebrates, probably yabbies and crabs and worms similar to those that are found in tropical estuaries today.  In fact the rocks are not even really rocks, they are just compressed sandy marine mud and you can break the rocks with your hands.  Trapped beneath about 2 km of this marine mud is the gas field that InterOil is developing.  It is the highest pressure gas field in the world as the soft mud is not self supporting like stone but transfers its full weight onto the gas below creating the highest lithostatic pressure of any production gas field in the world. This place really is a mountain of mangrove mud.

Testing the gas flow rate at the gas field - all the other photos were taken with a few kilometres of this place.
Photo from DrillingAhead.com

On the crest of a nearby hill, soil development was less than a metre thick then almost unaltered grey marine mud

Fossil cockles could be found in some of the stream banks.  Many types of mollusc shell could be found but I could not find any crustacean body parts.  I began talking to local tribesmen to ask if they had ever seen any crocodile or sharks teeth in the ground and at that very moment, I found a megalodon tooth in the ground where we were standing.  Megalodon sharks were largest and most dangerous shark that ever lived and they lived between 1 and 25 million years ago, so I had an upper and lower limit for age of the fossils I was finding.

This looks like fresh dredge spoil but is actually sub-fossils that are millions of years old

Broken Megalodon tooth - Gulf Province PNG

Fossil marine animal burrows in river stones

Even after millenia, the mangrove mud had not lost its characteristic appearance.  Unfortunately I did not test it for salinity or hydrogen sulfide. Only a shallow band of reddish soil had developed even in the most aerated parts of the landscape.  In North Queensland, weathering has created soil profiles up to 30 m deep, even on recent volcanic lava flows so the contrast between the soils of tropical Australia and PNG is extreme.  Near the coast, there are also coral reefs that have been uplifted and are now coastal headlands.

So the gradual uplift of PNG has created a situation where marine substrates are lifted above sea-level and the character of the soils remains essentially marine for millenia.  In theory, plants could adapt to these soils over time and then be dispersed downstream to colonise the lower catchment and possibly even mangrove areas.  So are new mangroves evolving here?  I have not had the pleasure of looking the area over.  It is said to be full of pirates armed with automatic weapons so one can't just go there.  There is at least one mangrove species which is unique to this region, which suggests that it may have evolved there.  A word of caution though, rapidly rising and falling sea level over geological time has sent many mangroves species locally extinct and some mangrove species now only occur in areas away from their birth places.

The mangrove (Camptostemon schultzii) only occurs on Cape York Peninsula and in the Gulf of Papua - could it have come from the uplifted marine deposits?

Camptostemon mangroves have giant sized knob roots.

The extreme rainfall of Gulf Province, about 9 m per year prevents the soils from drying out and is probably the reason why there is mangrove mud in the mountains.  The mud has many consequences, mountain streams flow with turbid water, trees are shallow rooted and easily fall over.  When I was in the forest, a strong trade wind blew over the forest, perhaps 40 km/hr and big trees started to fall.  We had to leave the primary rainforest with the big trees and head for secondary forest which is regenerating after a landslip as the risk from big falling trees was considerable.  In north Queensland, trade winds blow for more than half the year and the big trees are unaffected.  Palms, bamboo and large lilies do well in the soft muddy soils and eternal wetness.  Only a few plants in here have mangrove relatives.  This part of PNG is perhaps too wet to provide an ideal nursery for mangroves as tolerance to drought stress is also an important mangrove characteristic.

Flood plain forest and creek

Inside the forest - most of the big trees have plank buttress roots

Secondary forest, which is where you want to be when the big trees fall.

Creek meanders often have bamboo, gingers and palms, plants that don't fall over in soft ground.

Even in the hills are signs of marine life

A creek in undisturbed, uninhabited rainforest on a hillside is completely brown with sediment and full of fallen trees

As far as I am aware, there has been no formal research into evolution of new mangroves in response to tectonic uplift.  Maybe this is something for you to research?

The coastal plains with grasslands, forests and tidal influence may not have been properly explored.

When is a mangrove not a mangrove?

When it is a mangrove associate. Mangrove associates are plants that grow along or just below highest astronomical tide level. The term mangrove associates is used more widely used but is sort of a non-category that fails to respectfully identify this interesting group of plants.  Others have also struggled with this issue and was seems to be lacking is a good simple name for these species.  In particular, there is no good name for species which can grow in saline mud together with exclusive mangrove species.  Supra-littoral forest is the place where these plants occur. Let me call these species opportunistic mangroves.  The term mangrove associates covers a broad range of species, but is mixed grab bag of species as it includes species from all types of transition zone, including rocky mangrove coasts, sandy levees and beach ridges and within freshwater backswamps.  Let me define opportunistic mangroves as species that will take opportunities to grow below the high tide line on mangrove soils in places that experience fully saline conditions for at least one event each year.  The opportunities to grow in the mangrove edge are common but never abundant and opportunistic mangroves are always limited to small stands or scattered individuals.

Opportunistic mangroves are salinity tolerant trees and shrubs which can grow in the supra-littoral zone, which is defined as the zone above normal high tide level. The roots of these species are covered by seawater on a few occasions every year so they have to be halophytes (salt tolerant species).  To be exposed to raw seawater, the opportunistic mangroves have to be located in places with a dry season and with a large tidal range.  They also need to be in places where fresh groundwater seepage does not fill or flush the ground, protecting the trees from exposure to salt.  Often these places are very dry during prolonged dry conditions.  A final criterion would be that the trunk of the plant is located in a place with an unambiguous mangrove understorey, usually bare ground with crab holes or bare sand that is washed over by tides.

For comparison, some rivers which have freshwater baseflow all year round have freshwater tidal zones and river bank and freshwater swamp plants often dominate these places. These places are about as close as you can get to Pandora in the movie Avitar. There are several specialised mangroves species that live in tidal freshwaters but most of the plants live there are not referred to as mangroves as they can also be found in lowland rainforests other non-saline wetland habitats.  Which of these mangrove transition zones is an incubator for new mangrove species?

A tidal freshwater system near Cooktown, complete with beasts that squat in the mud and want to kill you.

Opportunistic mangroves are not restricted to growing near tidal waterways. Some can even grow on elevated inland areas as paradoxically the same adaptations that work in swamps make plants tolerant to swings between seasonal drought and waterlogging. Indeed one of the main minor supra-littoral mangroves around Cairns, Acacia oraria is common on the western flank of the Great Dividing Range.  The label opportunistic mangrove describes a capacity to grow on tidally affected land and is a functional category. Weeds are now defined as plants growing where they are not wanted. Calling a species a weed is discouraged, as a given species can be a weed in one context and a desirable plant in another. The term opportunistic mangrove should be similar, it describes plants than can grow in tidally affected areas with heavy soils and not just plants that have to grow there.

The definition of opportunistic mangroves solves a issue for me as the separation between mangrove and non-mangrove vegetation can be indistinct in areas with very flat terrain and places with moderate to high rainfall. Some species are classed as mangroves, yet other species with similar appearances and very similar habitat preferences are not. The concept of opportunistic mangrove lets me sidestep this issue.

In the Barron River Delta, near Cairns, some hectare-sized areas with opportunistic mangroves can be found on flat expanses just below highest astronomical tide level. These places have vegetation that is intermediate between mangroves and littoral rainforest. The largest supra-littoral areas are only a few tens of metres wide but may more than one hundred of metres long as they follow the tide line.  Unlike the landward zone of the mangrove swamp which has larger than normal mangrove trees, the trees in the supra-littoral mangrove area are usually short and shrubby.  Some supra-littoral areas are isolated low rises located deep in the mangroves which have no terrestrial habitat at all.  Only seasonal rainfall stops these areas from being salt pans. 

A mangrove with a light trunk surrounded by poor littoral rainforest. 

A stilt mangrove growing around a rainforest tree and an acacia (trunk at the back).

In my naval gazing about how mangroves evolved, these places seem to be one of the potential sites of crossover from a terrestrial to intertidal existence. Last week, I examined beach ridges and found that most of the species on beach ridges shrivel when exposed to seawater. Opportunistic mangroves seem to have much greater salt tolerance. Indeed the few millimetres of sea level rise that is now occurring has already greatly increased the exposure of many of these species to regular tides. Even without sea level rise, the land surface in these places is falling fast. As leaf-litter is swept away by tides and eaten by crabs, the ground is unprotected and tropical deluges spatter the surface and carry away the loosened material. Tonnes of material are lost every year, particularly in areas with overland flow. Imagine an extensive, slowly falling ground surface covered with opportunistic mangroves, would that not be an ideal environment for mangrove evolution? Each new generation of trees would encounter an environment that is slightly more marine than before. My horticultural experience tells me that the worst growing conditions of all is salty, dry and shady, with intense root competition from surrounding trees so this may not be the case. I have seen that combination around saltwater swimming pools, under stands of coconut palms and in the landward zones of mangrove swamps. The clear understorey in most of the transitional areas suggest that horticultural combination of death often applies to this zone and this may be why healthy existing opportunistic mangroves do not leave many seedlings.

Seedlings of mangroves, ixora (I. timoriense) and mock orange (Atractocarpus fitzalanii) were common in this thirsty contested zone.

Another factor may prevent trees from passing through the supra-littoral portal into the mangrove zone. One of the current theories of evolution, is known as punctuated equilibrium. This theory notes that species stay the same for long time scales and then new species rapidly evolve. A key part of this theory is the idea that small reproductively isolated populations are required, as large populations that are spread over wide areas are subject to evolutionary pressures the pull in opposing directions. A tree might be selected for seed dormancy in one part of its range and for seeds that germinate and take root as soon as they touch the ground in another. The result of these opposing pressures is that the species as a whole does not change. With some species of opportunistic mangroves, the bulk of the population lies in the terrestrial environment and this limits their ability to adapt to mangrove life. In some cases, the mangrove fringe often has small populations of plants that are very far from their terrestrial kin (Myoporum montanum, Bauhinia binatum, and Cathormion umbellatum to name a few. Perhaps genetic research will find the legendary reproductively isolated small population that is undergoing rapid change and the mangrove fringe would be one of the first places I would look.

A paperbark and a stilt mangrove are as close as old mates, surely they experience similar conditions.

A tuckeroo (front), probably Brisbane's most common street tree grows in the same saline muddy environment as a giant sized white mangrove (back).

Further Reading:

• List of well known mangrove associates
• Description of mangrove associates and broad types of mangroves

Did Mangroves Evolve from Beach Vegetation?

Mangroves are not the only trees with floating seeds that are dispersed by sea.  Plants growing in tropical sandy foredunes also have floating seeds and fruit.  The most famous of these plants is the coconut.  Despite growing side by side with mangroves, there seems to be a strong ecological barrier that prevents plants from the foredune from evolving into mangroves.  Others have noted this barrier but there is only vague speculation on what the nature of this barrier is.  In this post, I will investigate the barrier between mangroves and beach vegetation.

Strand vegetation near Cairns with taller dark green littoral rainforest behind

I refer to vegetation dominated by plants with seeds that are dispersed by sea as strand vegetation.  Wikipedia defines strand vegetation as ‘a plant community of flowering plants that form along the shore in loose sand just above the high tide line.’  It goes on to describe the key features of this habitat.  “Many plants that grow in this area are endemic to the strand. The community has low species diversity because so few plants can tolerate the harsh conditions of high winds, battering salt spray, and extreme high temperatures in the summer. Plants must also be adapted to sandy saline soils, with extremely low nutrient loads, and low water holding capacity.”  Although this definition was crafted for North American strands, the term strand vegetation is also used in the same way from Africa to Asia.  In Australia, the term foredune vegetation is often used, however I tend to associate this term with the high energy surf beaches and not the relatively calm tropical coasts.  There are several distinct vegetation communities that occur beside the high tide line, so vegetation community names should be used with care.  For example, strand forests often occur beside littoral rainforests but littoral rainforest trees are almost all bird dispersed and littoral rainforests create and grow on soils rich in humus and depend on efficient nutrient recycling.

Nature provided a natural experiment which helped me to see the barrier between mangroves and beach vegetation.  Some recent weather events effectively raised the normal high tide level by twenty or thirty centimetres and the strand vegetation was subject inundation with sea water.   Cyclone Dylan came to visit in January 2014, however Cairns being on the northern side of the system had offshore winds and the sea was quite calm save for a low swell.  The low atmospheric pressure associated with cyclones can lift the surface of the sea by approximately one metre.   In the Cairns area, the cumulative effect of the lower air pressure and high spring tides was to raise the sea by approximately 30 cm above normal (~3.6-3.8 m AHD) and the lower parts of the foredune were inundated.

High sea levels associated with Cyclone Dylan and swells gently swashing over the foredune

Some low lying coastal parks and some freshwater swamps were also inundated.  In the parks, fig trees dropped their leaves from the shock of salt water.  Freshwater swamps usually occur in basins such as old billabongs and swales.  As the seawater has trouble draining back out of the basins, many of the freshwater swamps were badly or permanently damaged with large paperbark trees and groundcover vegetation being killed.  Many of these swamps will change into mangrove swamps with time, especially as erosion of the barrier between the swamp and sea is often reduced by these events.

A park tree (Ficus lyrata) dropped its leaves due to a short period of saltwater inundation.

Seawater gets into some freshwater swamps but can't get out and kills all the vegetation.

A freshwater swamp turning into a mangrove swamp, Redden Island.

It turns out that even though strand plants live by the sea, most of them are also sensitive to saltwater inundation.  Many species drop their leaves.  In mangroves, salt is accumulated in old leaves before they are dropped.  I am not sure that this is the case with other species.

A beach almond dropping leaves after saltwater inundation.

Beach creepers were complete defoliated.

Cyclones are not the only reason plants suddenly find themselves exposed to seawater.  Sometimes erosion removes the land from around the trees.  Other times, plants become established on low lying ground and grow for months before encountering very high tides and rough seas from trade winds that put swash across the beach.  

Beach Cabbage (Scaevola taccada) with signs of salinity stress

Crinum lily damaged by exposure to seawater

Severe wilting of Cordia subcordata seeding on a sand bar in a mangrove swamp.

However not all strand trees are impacted as severely by salinity.  Some species hardly seem to notice.  Beach casuarinas are a bit special.  They drip concentrated saltwater from their leaves and are perhaps the only sandy soil specialist to easily cope with high loads of salt.  Most other species which cope with seawater inundation can also survive on riverbanks with dense silty soils and clays so I think there is a link between soil type preference and reaction to salinity.  Beach hibiscus (H. tiliaceus) , Portia trees (Thespesia populena) and Pongamia (Milletia pinnata) keep on growing until the sea physically washes them away. In one small section of swamp, I counted more than twenty living Portia trees suspended by mangrove roots.  They can almost teach mangroves tricks about living in salt water.

Beach casuarina growing at approximately neap high tide level.

A Pongamia tree survives where other trees have perished.

A leaning Portia tree perched in the mangroves well below spring high tide level.

Portia trees continue to grow and fruit despite exposure to the sea. 

In summary, salinity has dire effects on most vegetation.  However some species seem to cope easily with high levels of salinity and have seeds dispersed by sea, yet are not mangroves.  My conclusion is that most species that are specialised for growing in clean sand are likely to have adaptations that seem to make them susceptible to salinity. Mangroves are unlikely to have evolved from strand species.  A few of the species present in strand vegetation also grow around the terrestrial margins of salt flats or adjacent to the landward zones of mangrove swamps where soils are heavy silts and clays.  These species handle seawater inundation better.  I suspect that mangroves evolved in river deltas, rather that from beach species that crossed over the high tide line.

How did Mangroves Evolve?

When I Google mangrove evolution all I find are a few pithy generic statements and no real information.  I think that if all the mangroves we currently have were to disappear, other plants would race to fill the ecological vacuum.  Next time you are in the mangroves, look for non-mangrove trees that are dipping their toes in saltwater.  It is surprising how many there are and how many species can actually survive in the edges of mangroves swamps, where they are surrounded on all sides by mangroves and are growing in mud.  The question is why are these species not completing the transition?  That is a very big question so lets investigate a small part of it, how mangrove stilt roots may have developed.

The one scientific paper on mangrove evolution that I could get for free (most are locked up behind science journal paywalls) was about the biogeography of mangrove evolution and it said that almost all the mangroves present today evolved in the Tethys Sea which was sort of where Arabia and India are today.  The earliest species were Acrostichum, the mangrove fern and Nypa, the mangrove palm.  These species like lower salinities so that is a clue.  The main mangrove species (Avicennia and Rhizophora) were around 50-70 million years ago so forests just like those lining the worlds tropical oceans today would have seen dinosaurs.  Perhaps the Tethys Sea was like the sea between Australia and the island of New Guinea is today.  The information from the paper tells me what evolved and where but does not tell me how the plants evolved.  If I knew how mangroves evolved, then perhaps I would be able to understand the barrier that is preventing more mangroves from evolving.

Recently I have been seeing stilt roots on some species of mangrove that normally do not have them.  These mangroves usually have pneumatophores which are breathing roots that protrude from the mud.  If the trees have a choice of stilt roots or pneumatophores, why do they choose pneumatophores?  Fortunately it is possible to collect evidence on conditions that favour stilt root development.

In a swale, which is a shallow valley between sand ridges, I found several white mangroves (Avicennia marina var. eucalyptifolia) with stilt roots instead of the usually pencil roots.  This is very strange as Avicennia is the champion producer of pneumatophores. The stilt roots are not as well developed as those of stilt mangroves (Rhizophora) but are clearly stilt roots none-the-less.  

Avicennia tree with stilt roots instead of pencil roots (pneumatophores)

The swale traps a pool of freshwater in the wet season and saltwater in the dry season.  I happened across the swale on one of the few days when it was completely dry.  During the wet season, the swale appears to be a window lake, which means that the freshwater table is above ground level.  Several large paperbarks live or lived among the mangroves.  However as sea level rises by a few millimetres each year and the drainage line to the sea expands due to tidal and storm water flows, the ingress of seawater is increasing and the paperbarks are declining. 

Mangroves growing around a paperbark tree (Melaleuca leucadendra) 

Two days later a full moon brought in one of the highest tides of the year and flooded the swale and covered the entire stilt root system of the Avicennia trees.  It seems that in the centre of the swale the water is just too deep for pneumatophores.  Avicennia on the margins of the swale grow thickets of pneumatophores.  

Mangrove swale with standing water at full depth

Stilt roots and a few pneumatophores when pool is full

Avicennia can also grow adventitious roots (roots growing from the trunk above ground level) in more exposed situations, such as river mouths, where regular tides are experienced. In these areas, however the adventitious roots rarely become stilt roots.

Adventitious roots on tree a creek mouth

Another mangrove species that can also form stilts instead of pneumatophores is the black mangrove (Lumnitizera racemosa).  Normally, black mangroves have very few pneumatophores unless they are in areas with freshwater seepage, then they grow strange root loops.   In one special place, near Pormpuraaw in the Gulf of Carpentaria, I found a forest where black mangroves have stilt roots instead.  The Gulf has only one high tide per day, whereas the east coast of Australia has two high tides each day.  There is much less tidal exchange of water and the headwaters of rivers probably remain brackish longer than their east coast equivalents.  Upstream of the tidal creek is a vast flat swampy plain that slowly drains into the mangroves for several months a year, creating freshwater tides for part of the year. It is these special conditions which create this strange forest.

Lumnitzera mangroves in headwaters of a creek which has strong seasonal freshwater flows

Lumnitzera on stilts with super long Avicennia pneumatophores

Brackish water swamps with still pools of water do not foster stilt roots, in these places pneumatophore development goes crazy.  In a back swamp close to the black mangroves is a brackish water swamp with pools of water surrounded by mangroves and reeds.  The mangrove pneumatophores are exceptionally long and dense.

Avicennia around a brackish pool with Baumea reeds

The Avicennia pneumatophores are as dense as the reeds

So my concluding conjecture is that stilts seem develop more in areas with seasonal freshwater flooding or tides.  In fact this is just the type of place that the forest mangrove grows.  The forest mangrove (Carallia brachiata) is the only non-mangrove member of the stilt mangrove family in Australia. Carallia has a propensity to grow masses of adventitious roots even when it is in rainforest on wet foot hills, so perhaps the stilt mangrove families propensity for this type of root structure combined with an opportunity is what lead to stilt mangroves.