Linkages between Aquatic Sediment Biota and Life Above Sediments as Potential Drivers of Biodiversity and Ecological Processes

Abstract

A great deal of attention has been given to declining species diversity in terrestrial systems, and certainly the rate of species loss in tropical forests is staggering. Recently, increasing attention has been focused on the loss of species in aquatic ecosystems. Indeed, Ricciardi and Rasmussen (1999) report that freshwater extinctions in North America far exceed extinctions in terrestrial environments. For example, an increasing number of freshwater fish and bivalves are being added to endangered species lists (Angermeier and Schlosser 1995, Strayer et al. 1996). In contrast to our knowledge of fish and bivalves, information on species extinctions or even inventory lists are lacking for most inhabitants of the bottom sediments of lakes, streams, ground waters and wetlands, even though these “invisible” habitats harbor diverse and abundant biota (e.g., estimated at more than 100,000 species of sediment invertebrates globally, 10,000 species of algae, and more than 20,000 species of protozoans and bacteria; Palmer et al. 1997). Although the local and global environmental consequences of species extinctions in aquatic sediments are not fully understood, many sediment species are likely to play important functional roles in freshwater ecosystems (Covich et al. 1999). Sediment biota not only mediate biogeochemical transformations of global significance but are essential to the maintenance of clean water, the decomposition of organic material (often added in excess to our water bodies), the uptake and transfer of materials (including sediment-bound contaminants), and primary production (Freckman et al. 1997). Land-use changes and concomitant changes in the quality of water overlying aquatic sediments are contributing to the loss of sediment-dwelling species in freshwater ecosystems. Riparian plant communities are dwindling as urbanization and agriculture alter land use, and this decline in riparian zones has dramatic effects on nearby water bodies and their bottom sediments. Invertebrates that were previously abundant in lakes and streams are disappearing as the quality and quantity of groundwater and surface waters diminish (Richter et al. 1997). In North America alone, freshwater mussels are expected to experience future extinction rates of more than 6% per decade, and freshwater crayfish of nearly 4% per decade (Ricciardi and Rasmussen 1999). Taxa such as freshwater mussels and crayfish living on or near the surface of bottom substrates have been reasonably well studied. In contrast, there are so few data on the more cryptic freshwater sediment dwellers (e.g., worms, insect larvae) that estimates of extinction rates are not possible and mechanisms leading to extinction are poorly understood. The relationship between the loss of terrestrial and water-column species and the loss of aquatic sediment species is unknown. Are species losses in aquatic sediments linked to biotic processes and patterns aboveground? Is biodiversity in aquatic sediments threatened by the loss of species in adjacent terrestrial habitats or in the overlying water? Conversely, if sediment-dwelling species were lost, would the result be subsequent losses of flora and fauna in the water or in nearby terrestrial regions? We explored such questions during a series of working groups organized by the Scientific Committee on Problems in the Environment (SCOPE). These questions are difficult to answer because research has not focused directly on links between biodiversity above ground and biodiversity in aquatic sediments, and because there are few quantitative studies on the diversity and functional roles of biota in aquatic sediments. In this article, we identify potential mechanisms that could lead to a coupling of above-sediment (terrestrial and water column) biota and the biota of aquatic sediments (sediment biota). We hypothesize direct and indirect physical, chemical, and biological linkages between the flora and fauna living above sediment and the species composition in aquatic sediments. Because the magnitude of these linkages is largely unknown, parts of this article are speculative and meant to stimulate experimental studies or syntheses of existing data to explore this issue. If there is a tight coupling of above-sediment and sediment biodiversity in fresh waters, there may be a need to examine land management practices in the light of this knowledge. Further, if the diversity of aboveground species such as littoral plants is predictive of the diversity of aquatic sediment biota, then scientists may be able to use above-sediment diversity as a surrogate indicator of species diversity for aquatic sediments. This is attractive because sampling and identifying cryptic sediment biota is extremely difficult. The belowground habitats of freshwater systems include the sediments of both running waters (streams and rivers) and standing or semi-standing waters (wetlands, marshes, ponds, lakes, and ground waters) (Figure 1). The term “sediment” is broadly defined to include all unconsolidated material that makes up the bottom of aquatic ecosystems, including fine silts, sands, loose cobble, boulders, and partially or fully buried organic matter. All freshwater bodies are more or less connected to ground water through the hyporheic zone (the saturated sediments under and laterally adjacent to freshwater bodies where there is active exchange between ground water and surface water). The sediment-water interface is where the water-saturated sediment meets the water column. In aquatic ecosystems such as lakes, this interface may be obvious, whereas the distinction between the sediment and the water column is less clear and more variable over time in high-energy streams and rivers. While many aquatic organisms spend their entire lives in the sediment or in the water, many others live at the interface or spend part of their time in the water column and part in the saturated sediments. Further, some aquatic fauna (especially insects) spend part of their life cycle on land or in the air. In this paper, we broadly define sediment biota as those organisms living within aquatic sediments, on aquatic sediments, or closely associated with aquatic sediments at some stage of their life. Thus, organisms that burrow in stream and lake beds, such as dipteran larvae, are sediment organisms, even though they may make diel migrations into the water column and spend their adult life flying and mating in the air or on trees. Similarly, organisms living on and among rocks in a stream are sediment biota because rocks are part of the unconsolidated stream bed. The definition of above ground biota seems relatively clear in terrestrial systems: grasses, trees, and animals that tower over the soils are clearly above ground. For freshwater ecosystems, the distinction between “above” and “below” is not as obvious because aquatic sediments may be covered by water (e.g., lakes) or by soil and plants, as in groundwater sediments and wetlands. Thus, organisms continuously inhabiting the water column (fish, plankton, macrophytes) above freshwater sediments are above-sediment biota. Likewise, terrestrial flora and fauna that border waterways or are in contact with the ground water that directly feeds the waterways are above-sediment biota. Macrophytes have roots that penetrate freshwater sediments and thus also could be considered sediment biota; however, by analogy with trees and other terrestrial plants that are considered part of the aboveground landscape (Hooper et al. 2000), ecologists treat macrophytes as above-sediment biota. Biodiversity in aquatic sediments is poorly known, particularly for the smallest biota. For some freshwater systems, there is information on the number of sediment species for a few taxonomic groups (e.g., Bivalvia, Crustacea) or a few functional groups such as primary producers, but usually little more is known. The most numerous taxa in aquatic sediments (Table 1) are microscopic and often live deep within the sediments, making them difficult to sample. Even if samples can be obtained, few scientists have sufficient taxonomic expertise to identify collected specimens. Attention given to the Archaea, fungi, protozoans, and small, soft-bodied invertebrates of aquatic sediments has been especially inadequate (Palmer et al. 1997). Global estimates of microbial biodiversity in aquatic sediments remain highly controversial (Fenchel and Finlay 1995) and there are only a few published accounts of the genetic diversity of freshwater sediment bacteria and Archaea (Miskin et al. 1998, 1999). Instead, functional groups are active are the of biogeochemical (e.g., but these groups are linked to diversity or even species and 1999). In this article, we a to aquatic sediment making use of the many diversity (e.g., species species functional diversity and the air and the in the between above sediment and aquatic sediment biodiversity are that freshwater systems and primary and species composition in aquatic sediments largely the the rate of decomposition in fresh water are also closely to the and the air because these may the of such as and These may the species composition and of aquatic sediment that decomposition links between land and water may also species composition in aquatic sediments. For example, the of and soil in many aquatic systems, and is a variable in making water to a of In the landscape is important because between the terrestrial or water column biota and sediment biota may to a on the by and Because information is lacking for sediment biota, a functional is for among aquatic sediment organisms and those living above sediments (Table For example, the diversity of above-sediment primary near may be linked to the diversity of sediment biota because the many in biota living in may organisms in the other is difficult because there are numerous direct and indirect linkages between the biota and the processes (Figure For example, the roots of macrophytes may for sediment biota and thus have a direct on sediment and roots can also lead to an in of aquatic sediments, into sediment indirect that sediment biota). This sediment microbial and direct biotic may in alter microbial and can all biodiversity above and within the sediments. these an that direct indirect effects and biological and effects is a for identifying and links between aboveground biota and sediment biota (Figure For example, to diverse fish are associated with diverse sediment fauna because a diverse sediment fauna a of for the or because in sediment and a of habitats that may be by The of terrestrial plants, especially those in the riparian zones of streams, and the of macrophytes in aquatic processes have been and et al. and 1997). For this we numerous mechanisms by above-sediment plants may aquatic sediment have direct effects on aquatic sediment they may to the and the and microbial (Figure and plants and to existing sediment The of plant in the water the of the sediment-water and and and may the diversity of sediment particularly and is likely that microbial biodiversity is if Indeed, an of may be associated with microbial diversity because such as and or and live in (Fenchel and Finlay also directly sediment biota because plant and roots and sediment in aquatic The of aquatic plants is associated with an in the or species of many sediment-dwelling invertebrates and and In may to the of sediment fauna of and (e.g., the of protozoans and invertebrates is in the of In running waters, roots also to sediments can then a more diverse biota than sediments that are continuously by Thus, the of plants in freshwater ecosystems is to diversity of sediment fauna terrestrial plants also environmental in lakes and streams by diverse bottom the of in freshwater systems is usually associated with an in biodiversity of stream bottom invertebrates et al. and The may of sediments, or the may alter the and patterns to of fine sediments with of In streams, the result may be an in species diversity of sediment-dwelling invertebrates to stream with sediments (Palmer et al. Because of the in freshwater systems is habitats for many hyporheic and invertebrates and et al. and associated and bacteria may also be by that would not be in aquatic sediments et al. 1999). and riparian plants the and quality of light nearby fresh waters and The of of streams and standing waters is a of the and composition of terrestrial et al. If of are functional groups of sediment biota such as invertebrates may a decline in sediment of even a few species of plants may have direct effects on sediment biodiversity through the loss of species or the loss of sediment biota and plants, particularly algae, also effects that can sediment in may have effects running water and lake and sediments are linked to terrestrial soils and to surface waters through between the ground water and the surface These processes are to the and species composition of aboveground in have effects on the of water and materials in may thus or processes in lakes, streams, and by the quality and quantity of water that have through the adjacent soils et al. et al. In running water systems, macrophytes can local and zones in the sediments that may have effects on the hyporheic and The biota of aquatic sediments are to be extremely to changes in species and functional composition and are expected with changes in water and groundwater quality and and et al. 1998, and The of many aquatic ecosystems are largely by of plant material the landscape (Figure the and diversity of sediment-dwelling and invertebrates in freshwater et al. and et al. 1997). For example, stream bottom invertebrates are by the composition of riparian and some have with macrophytes or and et al. et al. 1999). Although experimental are in is that plant diversity above ground (e.g., in riparian and in the water may diversity in aquatic sediments effects (Figure This the that a diverse of plants the during is to aquatic the diversity of and the diversity of organic in microbial diversity to the diversity of organic to the diversity of sediment biota is difficult because of the many potential mechanisms linkages and because many other than these linkages biodiversity in aquatic sediments. studies that some stream invertebrates have and rates species of and et al. Palmer et al. 2000), the that a diversity of aboveground plants may biodiversity in aquatic sediments. This is certainly an in are of live may also be an important of aquatic sediment In and lakes, many species of sediment invertebrates use and as or as on to or The of aquatic plants and microbial communities that as an for even many sediment dwellers and Sediment biota that make of the sediments may of the plants as or may on the and on the plant studies and diversity have focused on invertebrates living on plants not on invertebrates living in the sediments Thus, or not a diversity of aquatic plants a of sediment biota to be not only the of water to aquatic sediments but also the composition of water into nearby water in plant species can alter water particularly the and of and may in the sediment-dwelling biota and and and 1997). of and near bodies of water may be on plant and of and For example, et al. that rates of in ground water were in than in or Similarly, species of macrophytes are to the water both by into organic and by as on the These can lead to the of and sediments may have have not explored the relationship between plant species and water but clearly plant species composition has effects on the of aquatic sediments. Because bacteria to changes in their we by the aquatic sediment microbial to in plant species that sediment of and into freshwater sediments stimulate and sediment and Similarly, changes in have been to have effects on the species composition of aquatic sediment-dwelling et al. in microbial may to and 2000), microbial biodiversity may also to changes in sediment that are linked to above-sediment plants (Figure The to microbial biodiversity is speculative at this because the of microbial species composition in aquatic sediments and to microbial is in and are abundant both in water than and in aquatic sediments than et al. not all bacteria are active at time and in functional of (Table is at some time and in nearly freshwater research of a and a in stream sediments has that the of microbial processes over of or less et al. 1999). and all to over these These that a diverse of functional groups in freshwater sediments. of these groups are active may on plant biodiversity above the sediments, because plants sediment by et al. has that the of of and in ground water microbial composition and in freshwater sediments. the or more microbial functional groups may active and et al. 1999). Thus, functional and species of freshwater sediment be over time and and may to changes in water by changes in the overlying plant species or not effects on the microbial have effects on the sediment-dwelling biota is an The is for studies microbial diversity or and 1995) and the by microbial for into sediment biodiversity is to aboveground plant in the species or functional diversity of sediment could the species composition of sediment-dwelling particularly less than that on such as and protozoans and and Palmer Because freshwater may be by there is the potential for water effects to the bacteria to the and to the and to the effects of plants, we of terrestrial and animals aquatic sediment biota. terrestrial animals that in or through fresh waters, such as or may have dramatic effects on entire aquatic ecosystems, including the sediment biota. other above-sediment biota (e.g., may alter the biodiversity of aquatic sediment biota through their direct and indirect and biological terrestrial or animals sediment biota through their effects on aquatic and fish can for sediment biota through their and and et al. is to the diversity of aquatic sediment biota; however, some animals that or streams (e.g., the sediments so that effects on sediment biodiversity are in fresh waters and an in sediment particularly because species of and are In such only a few species of highly fauna (e.g., larvae, may the aquatic sediments. While the effects of above-sediment fauna as have been for a few links between the diversity above sediment and in the sediment have not been their may the of fine to bottom sediments, for and that loss to the in with than in those because there a in the microbial in of can also microbial diversity in aquatic sediments by increasing the of in the microbial Because of they also and effects may have to changes (often in diversity et al. In with et al. there were in the diversity of some insect groups (especially and other sediment biota (especially were more abundant or in the species diversity of sediment biota may be linked to the of above-sediment biota. This can be in and and may to the bottom For example, et al. that water effects on primary production of freshwater algae, in effects on species of both and sediment-dwelling terrestrial and flying biota can also the of aquatic sediment-dwelling species that The may be by above-sediment biota, in their and be in freshwater systems as the biota are the most important above-sediment that direct biotic effects on aquatic sediment biota. fish and invertebrates on many sediment species for their and the dramatic of these on the diversity of sediment biota is extremely well in freshwater systems fauna also have effects on as they often the sediment and can and species composition in or on aquatic sediments 1996). Further, the of may alter the of in aquatic sediments and the sediments to the water or littoral or riparian zone and 1995, and 1996). Because many have for sediment they can have dramatic on the and of species The of macrophytes can mediate the of on sediment biota in fresh waters because the plant may and near the et al. The effects of some above sediment organisms (e.g., can thus be by the effects of other above-sediment life (e.g., biota may also biodiversity of linkages among life For example, fish may diversity because many freshwater bivalves that fish species as and are important above-sediment of life that may have a dramatic on sediment especially For example, the and the of that to the bottom the of that as for invertebrates and substrates for and 1996). The in lakes is by a of especially during and are in and are considered a for sediment-dwelling invertebrates et al. et al. 1997). The of species the of transfer and may sediment biota in may or alter the water both of can have direct effects on sediment life or up in a littoral The mechanisms by life above the sediments are less numerous and more difficult to identify than those by the above-sediment biota sediment life. The most important effects of biota on the terrestrial are to water organisms that sediments alter the of and into the water, the composition of bacteria and et al. and 1996). in water are also likely to and fauna living the of water however, this has not been macrophytes living in aquatic sediments be by biotic that alter sediment or et al. biota living deep within sediments are well to the of that may alter of algae, and effects of biota have been less in freshwater systems than in systems and Palmer 1999). there are dramatic of by freshwater biota living at the sediment-water the of mussels to water bodies in the an in and dramatic changes in and species composition were for the et al. Strayer et al. et al. Sediment biota also to the decomposition of organic this in rates and to and and the of organic material et al. 1997). organic and the both of processes decomposition and of sediment in a of sediments, the of the The result is et al. and a more of organic and of to the overlying water et al. These effects may be particularly important in the of the of such as and primary the functional of biota living in aquatic sediments and the of their diversity and (Palmer et al. is that we so little linkages between sediment biodiversity and diversity above sediments. research on the and functional roles of species is to the of environmental changes above ground on aquatic sediment biota. Because plants play chemical, and biological roles in the species composition and of sediment-dwelling organisms in lakes, wetlands, and running waters, attention be focused on the sediment The and diversity of terrestrial and aquatic may biodiversity in freshwater sediments (Figure but this The of terrestrial and animals such as and fish on aquatic sediment communities can be both and diversity or of sediment biota may decline or be The in knowledge with to linkages between aboveground plants or animals and aquatic sediment biota to the microbial is the diversity of bacteria and protozoans in aquatic sediments, and less microbial are by the diversity of plants or animals living above the sediments. Thus, a research be to patterns in microbial biodiversity in aquatic sediments, particularly in where terrestrial plants and animals are well important research be to our of the functional roles of sediment-dwelling including the smallest and to to above-sediment biodiversity to nearby aquatic sediment communities in these is important because there are environmental management if linkages between above-sediment life and aquatic sediment biodiversity are (Table that or the transfer of material (e.g., organic sediments, terrestrial to fresh waters or that the landscape adjacent to water bodies may need use is expected to have a dramatic global on biodiversity over the et al. and this be most in freshwater ecosystems because live near waterways and on them for and water may be to groundwater if such the of soils to fresh waters (often the hyporheic Land-use and management practices may need to be to on the maintenance of plant diversity adjacent to freshwater not only on the maintenance of a plant near fresh waters may result in dramatic in aquatic sediment because diverse plant communities diverse and for sediment biota. in aquatic sediment biodiversity are also expected if near water bodies is not in because with groundwater and because may be associated with an in the of plant and and of organisms into freshwater lakes is the to aquatic management for associated with species is difficult (Figure in et al. the of species into fresh waters, the loss of sediment species that play a in processes in fresh waters species or is of (Palmer et al. et al. 1999). While the local and global consequences of the loss of biota and of linkages between above-sediment and sediment biota are not fully understood, scientists that the decline of biodiversity in many fresh waters is staggering. to the linkages and their consequences are We to the for the that to this paper, and for their and for for this are in part on research by on and the of the and and for to the and were by the by and by the of of freshwater sediment biota. The number of species between to species of invertebrates at a lakes and species at a and at a also within a over time for example, diversity in streams during and of diversity the entire local species Palmer et al. and functional groups of freshwater sediment bacteria and are not because they into this groups are and groups are A functional to the of above-sediment biota and aquatic sediment biota on processes in the adjacent many aquatic sediment species to functional groups or in to environmental or life the species composition within a functional is not considered to the maintenance of important linkages between freshwater sediment biota and life above the sediments. of the has management however, research on sediment biota and they to a in above-sediment biodiversity is and that are considered above sediment and those considered as aquatic sediments. The is an of the freshwater systems: lakes, streams and groundwater wetlands. The bottom is a of a lake or stream the above-sediment and aquatic sediment For the above-sediment the flora (terrestrial and fauna (fish, are The water column is considered an above-sediment the hyporheic and groundwater zones are considered aquatic sediment habitats of linkages between above-sediment biota and aquatic sediment biota and between that direct effects may lead to indirect effects in some that may also have dramatic effects on the sediment biota of material the of many freshwater ecosystems such as this may but are and into aquatic sediments by and mechanisms by diverse terrestrial and aquatic plant communities may lead to an in the biodiversity in aquatic sediments. organic of in for diversity of number of of organic contributing to the (e.g., species that are and microbial number of functional or genetic groups of fungi, and in is of a stream with diversity of aquatic invertebrates and mechanisms by diverse terrestrial and aquatic plant communities may lead to an in the biodiversity in aquatic sediments. organic of in for diversity of number of of organic contributing to the (e.g., species that are and microbial number of functional or genetic groups of fungi, and in is of a stream with diversity of aquatic invertebrates and