Indirect paleo-seagrass indicators (IPSIs): A review
Introduction
The deeper understanding of paleo-habitats and their successful recognition in the geological past help us to investigate their ecological responses to small- and large-scale environmental changes, such as climate change and sea-level fluctuations. In order to evaluate the development of coastal biodiversity through time it is necessary to reliably discriminate different marine habitats, because species numbers and assemblage compositions may vary considerably between environments (Gray, 2001, Bouchet et al., 2002). Therefore, the successful recognition and discrimination of paleohabitats are an indispensable basis for studies on biodiversity, climate and sea level history.
Here the terms ‘seagrass habitat’, ‘seagrass meadow’, etc. refer to environments with an area-wide vegetation cover (10s to 100s of m2) dominated by marine angiosperms. Patchy seagrass occurrences in other, for instance coral-dominated, environments are not further considered, because the recognition of dispersed seagrass vegetation appears to be limited, although not impossible (Zuschin and Hohenegger, 1998, Kusworo et al., in press).
Seagrass meadows are distributed worldwide from Australia and New Zealand to Iceland, Norway and Greenland, spanning the coasts of Africa, India, The Middle East, North and South America and Europe with the exception of Antartica (Fig. 1). The habitat is characterized by a three-dimensional structuring of marine angiosperms and associated macroalgae.
Seagrasses are a polyphyletic functional group comprising approximately 60 species in 13 genera, assigned to five different plant families (Les et al., 1997). They are the only angiosperms that live permanently in fully marine environments, involving several physiological adaptations (Touchette and Burkholder, 2000). The highest diversity of seagrass species is found in the tropical Indo-West Pacific around the Philippines, New Guinea, and Indonesia (Mukai, 1993, Green and Short, 2003). Marine angiosperms predominantly occur in the tidal and shallow subtidal zone down to about 15 m, but have also been reported from depths down to 90 m, depending on seagrass species and light attenuation (Duarte, 1991). In the tropics seagrasses often grow on reef flats and form compound associations with corals in the transition zone between intertidal meadows and subtidal reefs (Nienhuis et al., 1989, Hoeksema, 2007). In the Caribbean the presence of fringing reefs, which have been the dominant reef type in that region since the Plio–Pleistocene, is critical for sheltering and facilitating the accumulation of back-reef seagrass meadows and landward fringes of mangroves (Budd et al., 1996, Spalding et al., 2001, Johnson et al., 2007). Where the three components are present, seagrasses, coral reefs, and mangroves are intimately linked both in terms of the genesis of the wider reef system and its sedimentation patterns, and chemically through nutrient transfer (McCoy and Heck, 1976, Ogden, 1997).
Seagrass meadows provide a number of functions that make them an ecologically highly valuable habitat. Constanza et al. (1997) estimated the commercial value of ecosystems based on the ecological functions they provide, and rated seagrass meadows as one of the most valuable biotopes in the world. They contribute significantly to the oceanic primary production on a global scale and play an important role in the oceanic carbon cycle, especially in carbon storage (Duarte and Chiscano, 1999, Hemminga and Duarte, 2000). Due to their ability of rapid nutrient uptake in combination with slow decomposition rates, they can reduce eutrophication, bind organic pollutants and therefore play an important role in nutrient cycling (Spalding et al., 2003). Because seagrasses, in contrast to other marine macrophytes, have true roots, they trap and stabilize sediments and therefore prevent coastal erosion even under extreme conditions such as hurricanes (Ball et al., 1967, Scoffin, 1970). Seagrass meadows support local biodiversity by providing food, stable sediment conditions, and a three-dimensional structuring, offering attachment surfaces and shelter against predation, for numerous associated organisms (e.g., Boström and Bonsdorff, 1997). Seagrasses form complex ecosystems that consist of several microhabitats for different groups of organisms, i.e., the infauna in the sediment, the benthic community on the sediment surface, the epiphytic community, and planktonic as well as nektonic organisms in the water column (Den Hartog, 1979). Meadows are also an important nursery habitat for fish, crustaceans, mollusks and echinoderms, including reef-associated and economically important species (Hemminga and Duarte, 2000). Therefore, species richness and abundance are often higher in seagrass meadows than in adjacent unvegetated areas that lack a three-dimensional structuring (Brasier, 1975, Mikkelsen et al., 1995, Hemminga and Duarte, 2000, Barnes and Barnes, 2012). However, diversity often does not exceed that of other shallow marine phytal habitats, such as mangrove forests or algal mats, or that of nearby coral reefs (Hemminga and Duarte, 2000, and references therein; Sheridan, 1997). Like other coastal marine ecosystems, seagrass meadows are severely threatened by climate change, eutrophication, over-exploitation, and mechanical disturbance (Short and Neckles, 1999, Jackson, 2001, Orth et al., 2006, Hughes et al., 2009, Waycott et al., 2009, Rasheed, 2011).
Fundamental to studies of seagrass habitats in deeper time is the assumption that seagrass meadows in the geological past since their Late Cretaceous origin provided habitat functions comparable to modern seagrass meadows and were inhabited by a comparable community of associated organisms. Despite their ecological importance, our knowledge of the biodiversity of modern seagrass habitats remains surprisingly limited, with faunal inventories often being restricted to specific groups, such as fish or arthropods (e.g., Heck et al., 1989). Other studies focus on the macrobenthic invertebrate community, often combined with an assessment of the infauna (e.g., Boström and Bonsdorff, 1997, Barnes and Barnes, 2012), or that of epiphytes (e.g., Marsh, 1973). Studies of the composition and diversity of the entire macrofauna present in Recent seagrass meadows are comparatively scarce (Brouns and Heijs, 1985). Likewise, detailed studies of distribution patterns of seagrass meadows and their response to environmental change during the Cenozoic are very few in number (Brasier, 1975, Eva, 1980, Domning, 2001, Vélez-Juarbe, 2014). There are no studies examining patterns of biodiversity change of seagrasses and associated organisms over global or regional scales. One likely explanation is the challenge of reliable identification of seagrass meadows in the fossil record. Seagrasses easily disintegrate, therefore marine angiosperm macrofossils are rare (Brasier, 1975). In contrast to most land plants, the pollen of seagrasses is prone to decay, because it lacks the resistant pollen wall used by land plants for protection against dehydration (Hesse et al., 1999). Therefore, a widely used approach has been to infer the former presence of paleo-seagrass vegetation through sedimentological and taphonomic indicators, and the presence of fossil organisms that are interpreted as typical for seagrass associations (Brasier, 1975, Eva, 1980, Domning, 1981, James and Bone, 2007, Reuter et al., 2010). All these indicators can only provide indirect evidence of seagrass meadows and are therefore here referred to as IPSIs (Indirect Paleo-Seagrass Indicators). IPSIs have often been of limited use because of their low fossilization potential, limited geographical distribution, or occurrences in habitats other than seagrass meadows. To date no comprehensive summary of indirect paleo-seagrass indicators is available, neither is an assessment of the value of those indicators.
In this study we review previous studies of seagrass meadows in the Late Cretaceous and Cenozoic, focusing on the methods used to identify this habitat. Our aim is to provide an overview of previously used IPSIs, to assess their usefulness, and to identify which indicators or combinations of them are most reliable to infer paleo-seagrass vegetation in the geological record.
Section snippets
Material and methods
This study is largely based on a review of the available literature on modern seagrass meadows, previously identified paleo-seagrass meadows, and IPSIs of various kinds. Observations made on our own (in part unpublished) material and results are included. Specimens deposited in the Naturalis Biodiversity Center, Leiden, the Netherlands are indicated by RGM numbers. Specimens deposited in the Natural History Museum in London, UK are indicated by NHMUK numbers.
We provide a classification for each
Seagrass associations in the fossil record
Seagrass associations in the fossil record can be divided into two categories: 1) associations with seagrass preservation (see Section 3.1), and 2) associations identified based on IPSIs. In addition, the presence of IPSIs can strengthen the interpretation of a sedimentary deposit containing only rare remains of seagrasses or of ‘seagrass-like’ plants that cannot be reliably identified (Collinson, 1996). Studies on fossil associations including preserved seagrass remains reveal similarities to
Benthic foraminiferal assemblages
The assemblage composition of foraminifera and the occurrence of individual species associated with seagrasses have received considerable attention (e.g., Langer, 1993, Semeniuk, 2001). Worldwide, numerous species (> 100) are reported in association with seagrasses. Species numbers per seagrass leaf can be up to 24 (Richardson, 2004), and typical densities range from 14 to 80 specimens/cm2 (Richardson, 2000, Richardson, 2004, Wilson, 1998; W. Renema, unpublished data on various seagrass meadows
Occurrence of unsorted fine sediments
In modern seagrass meadows: Sedimentological features of seagrass meadows are linked to the ability of seagrasses to baffle currents and trap and stabilize sediments. Reduced resuspension promotes the accumulation of fine-grained sediments, partly sourced from the in-habitat production of skeletal carbonate (Scoffin, 1970, Nelsen and Ginsburg, 1986, Fornos and Ahr, 1997). As observed in seagrass meadows in the Mediterranean, seagrass-associated sediments are usually poorly sorted, with abundant
Discussion and conclusions
The strength of an IPSI is context-dependent. We have yet to find an IPSI that can provide straightforward identification of paleo-seagrass habitats on a global scale throughout the stratigraphic range of seagrasses and that is common in the fossil record. In addition, our characterization of IPSIs is based on perfectly preserved material and poorer preservation will hamper the use of individual IPSIs by differing amounts.
The record of paleo-seagrass facies is strongly biased towards the
Acknowledgments
This research was funded by the Marie Curie Actions Plan, Seventh Framework Program of the European Union (Throughflow, grant no. 237922). Many colleagues helpfully provided their knowledge on various aspects of this study. We thank J. Cottrell, A. Cutler, J.W. de Leeuw, S. Donovan, R. van der Ham, R.D. Pancost, G. Stringer, P.D. Taylor, and M. Yasuhara. Special thanks go to J.C. Braga and K.G. Johnson for their helpful comments and the additional provision of photographs. Furthermore, we would
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