Are saltmarshes younger than mangrove swamps?

Abstract Temperate saltmarshes and tropical mangrove swamps (mangals) are marine‐influenced, productive ecosystems that enhance nutrient transfers between land and sea and facilitate colonization of lineages between terrestrial and marine habitats. Mangals have existed since the late Cretaceous, but the time of origin of saltmarshes is less clear. On the basis of phylogenetic and fossil evidence for plants and molluscs specialized to these ecosystems, I propose that saltmarsh vegetation of angiosperms began during the latest Eocene to Early Oligocene (35–30 Ma), at least 34 m.y. after the origin of mangals. The plants that colonized saltmarshes then and later have mainly temperate origins, contrasting with the tropical‐forest origins of mangroves. Unlike the plants, the few saltmarsh‐specialized molluscs are derived from tropical lineages and reflect recent colonizations. The development of saltmarshes during the Neogene enhanced near shore productivity along temperate and Arctic coastlines.


| INTRODUC TI ON
Temperate saltmarshes and tropical mangrove swamps (mangals) are important marine-influenced wetlands whose primary producers are overwhelmingly angiosperms of terrestrial origin. These highly productive ecosystems at the transition between land and sea enrich nearby marine habitats with nutrients and facilitate colonization of lineages from land to sea or vice versa. Both marine and terrestrial animals have become specialized for life on or under mangroves and saltmarsh vegetation.
Although comprehensive descriptions of these ecosystems have long been available (Chapman, 1960;Greb et al., 2006;Macnae, 1968;Saintilan, 2009;Visser et al., 2019;Walsh, 1974), and numerous taxonomic and ecological studies of resident taxa have been published, differences in the times of origin between mangals and saltmarshes have gone unnoticed. These are nonetheless important because they might indicate that temperate gains in productivity in coastal vegetations are much more recent than those in tropical mangals.
Mangals and saltmarshes have in common that both thrive on and create muddy or sandy soils in wave-sheltered tidal environments. Nevertheless, their taxonomic compositions differ strikingly, potentially reflecting contrasting times and places of origin. Here, I propose the hypothesis that saltmarshes are much younger than mangals, that the plant inhabitants of saltmarshes derive from lineages almost entirely different from the lineages of mangrove species, and that specialization of molluscs to mangrove swamps and saltmarshes mirror these contrasting histories.

| MATERIAL S AND ME THODS
Plants were considered to be adapted to mangals or saltmarshes if they are regularly or occasionally inundated by seawater. Molluscs were considered to be specialized to mangroves or saltmarshes if they either routinely climb on vegetation or are attached to vegetation. Many species live on the sediment beneath vegetation or are found on hard surfaces in addition to the vegetation; these were not considered to be specialized mangal or saltmarsh species.
Phylogenetic and fossil evidence for times of origin were gleaned from the published literature. I searched for relevant phylogenetic and paleobotanical papers for each family of angiosperms with representatives in saltmarshes and then consulted the reference list in the papers as well as the papers that cited those I found. Search terms other than family names were judged inadequate or too general to be useful. Divergence times were accepted as inferred in the studies cited. Given their consistency among papers, variations in the protocols used should have a little effect on the interpretations made herein. Primulaceae. Specialization to these saline coastal environments has occurred more than once in most of these families (Bennett et al., 2013;Dassanayake & Larkin, 2017;Ellison et al., 1999;Flowers et al., 2010;Ricklefs & Latham, 1993;Sahu et al., 2016). Only one family (Plumbaginaceae) includes representatives in both habitats, but mangal and saltmarsh species belong to separate lineages. There is no genus-level overlap between mangrove and saltmarsh plants.
A second striking contrast between angiosperm-dominated mangals and saltmarshes is the time of origin of these ecosystems.

Mangal ecosystems have expanded and contracted throughout the
Cenozoic in all parts of the tropics, but their highest diversity of plant species is achieved in the inner Indo-West Pacific region of southeast Asia (Ellison et al., 1999;Guo et al., 2017;Walsh, 1974;Woodroffe & Grindrod, 1991).
The history of saltmarsh lineages is less well known, but divergence times inferred from molecular sequences indicate that saltmarshes are no older than the latest Eocene to earliest Oligocene
Species in at least 10 gastropod families live on or under vegetation in saltmarshes, but only one species, the northwest Atlantic Littoraria irrorata, occurs on saltmarsh plants (Reid et al., 2010). Many gastropods have populations in both mangals and saltmarshes, but again, most of these do not climb on vegetation.

Plant-climbing species of Palustorina (Littorinidae) in China and
Littorinopsis in Australia live in saltmarshes but are primarily associated with tropical mangroves (Dong et al., 2015;Reid, 1986).
No saltmarsh gastropods that can climb plants have temperate origins. Northern-hemisphere populations of Littorina occur in saltmarshes, but they belong to species with very broad ecological distributions including wave-swept rocky shores (Reid, 1996). The only bivalve that appears to be specialized for life in saltmarshes is the byssate semi-infaunal mytilid mussel genus Geukensia, with two allopatric northwest Atlantic species (Sarver et al., 1992).
Geukensia in the sister group of the tropical and warm-temperate western Atlantic genus Ischadium in the subfamily Brachidontinae, which occurs widely in mangals and on other hard substrata including oysters (Trovant et al., 2015).

Mangrove-associated littorinids and potamidids date to the Early
Eocene (Dominici & Kowalke, 2014;Reid et al., 2008Reid et al., , 2010, but the tree-climbing potamidid Cerithidea, Clypeomorus (Cerithiidae), and muricids are no older than the Miocene (see also Claremont et al., 2013;Houbrick, 1985). The saltmarsh-specialized Littoraria irrorata is a known fossil from the Late Miocene and Pliocene and diverged from its sister species L. varia at about this time (Reid et al., 2010). The littorinids with well-established saltmarsh populations in the North Atlantic (Littorina littorea and L. saxatilis) arrived from the North Pacific during the Pliocene (Reid, 1996). There is no pre-Pleistocene record for the mussel genus Geukensia. The meager record of saltmarsh molluscs is therefore consistent with the hypothesis that saltmarsh ecosystems are much younger than mangals and that specialization to saltmarshes is much less common than that to mangroves.  Falcon-Lang, 2005;Greb et al., 2006). The peculiar lycophyte

| G ENER AL D ISCUSS I ON
Pleuromeia from the Early and Middle Triassic appears to be halophytic (Krassilove & Zakharov, 1975;Retallack, 1975), as are some conifers of the Middle Jurassic and Early Cretaceous in the family Cheirolepidiaceae, the Middle Jurassic conifer Brachyphyllus, and the Late Jurassic fern Pachypteris (Alvin, 1982 The hypothesis proposed here can be further tested and elaborated by considering other animal groups that have become specialized to live on mangrove trees or in saltmarshes. These groups especially include brachyuran crabs as well as herbivorous insects and some terrestrially derived vertebrates. Geographical differences in specialization and in diversity of mangal and saltmarsh specialists could illuminate aspects of evolution in these habitats. For example, Indo-West Pacific mangrove plants, molluscs, and crustaceans are more than 10 times richer in species than their Atlantic-East Pacific counterparts (Ellison et al., 1999;Vermeij, 1973;Walsh, 1974), perhaps reflecting the geographical extents of suitable habitats in the past (Ricklefs & Latham, 1993). Differences in saltmarsh specialization between regions have not been investigated, but the northwest Atlantic and perhaps Australia appear to harbor more specialists than other parts of the world.
These historical and comparative aspects of ecology can be fruitfully applied to other ecosystems as well, especially systems that develop at major transitions among terrestrial, freshwater, and marine environments. Although such studies may not have immediate practical applications, they offer an important historical perspective with long-term implications for the health and sustenance of systems that have been strongly affected.

ACK N OWLED G M ENT
I thank Tracy Thomson for technical assistance.

CO N FLI C T O F I NTE R E S T
I wrote the paper, and I have no conflicts of interest.