Land–Sea Coupling and Global-Driven Forcing: Following Some of Scott Nixon’S Challenges

Estuaries and Coasts DOI 10.1007/s12237-014-9808-3

Land–Sea Coupling and Global-Driven Forcing: Following Some of Scott Nixon’s Challenges

Ivan Valiela & Megan Bartholomew

Received: 16 December 2013 /Revised: 2 March 2014 /Accepted: 14 March 2014 # Coastal and Estuarine Research Federation 2014

Abstract Adjoined watershed–estuary–coastal ecosystems one example of early awareness of the intense, and ambivalent, are coupled by biogeochemical and hydrodynamic processes, nature of the land–sea interaction is vouchsafed in an eighteenth as Scott Nixon repeatedly argued in his many contributions. century engraving in a treatise by Bernardo Trevisan (Fig. 1), Case histories from Waquoit Bay and the Pacific Coast of showing the “opposition” of land and sea. The allegorical Panama, supplemented by information from other sites, make image depicts the interaction between Land and Sea, taking evident that the couplings that enable connectivity among place at the very edge of water and land. It is—appropriately— spatially separate landscape units, while highly subject to hard to judge whether the interaction is an embrace or a detailed local contingencies, take place in every coastal zone, struggle, but we can be sure that the interaction is an intense can be powerfully affected by human activities on land, and one. We can further extend the perhaps unwittingly prescient by global-scale forcings, as Scott Nixon often reminded us. metaphor by taking the leap to say that the interaction takes While the factors that determine the details of land–sea cou- place within the context of coasts altered by human presence, pling differ significantly from one coastal zone to the next, and under the gathering clouds of climate change. Few images estuarine systems manage, to different degrees, to furnish better capture what we know now about land–sea coupling and ecological services not only as filters or transformers of the influences of human and global-driven changes. land-derived inputs but also as exporters of energy-rich sub- Scott Nixon, whom we honor in the lead article of this sidies to coastal food webs. issue, made many contributions that advanced our knowledge about the subject of Trevisan’s allegory. Scott insisted that we Keywords Land use changes . Upwelling . La Niña . Coastal need to understand the biogeochemical and hydrodynamic – watersheds . Eutrophication . Deforestation . Estuaries . basis for land seacoupling(Nixonetal.1986;Nixon1988). Mangroves . Spatially subsidized food webs . Connectivity He showed that a number of approaches could be used to address topics underlying land–sea coupling, including meta- analysis of published data, comparisons, experiments, and models. He emphasized that clarity in definition and questions Introduction asked are key—as, for example, in his definition of eutrophication (Nixon 1995)—, and that we would be remiss if we Anyone living or thinking about the coastal zones of the world ignored the influence of external global-scale as well as local becomes keenly aware that the boundary between land and sea control processes (Nixon et al. 2009). is a critical feature, subject to powerful influences from both Land–sea coupling in the coastal zone links adjoining land- land and sea, and that the land–sea interaction through the and seascape units: watershed, estuary, wetland, and coastal coastal zone is often modified by global-driven disturbances. waters. These units are connected by exchanges of water, These interactions have long been part of human experience; nutrients, biomass (and contained energy), and sediments. Communicated by Wayne S. Gardner The exchanges are mediated largely by physical forcing by air and water, but to some degree the exchanges of materials * : I. Valiela ( ) M. Bartholomew may take place by animal and human transport (Hyndes et al. The Ecosystems Center, Marine Biological Laboratory, Woods Hole, MA 02543, USA 2014). These exchanges have been described as subsidies e-mail: [email protected] transferred among spatially apart units of landscape; there Estuaries and Coasts

that alter delivery of materials from land to sea. The role of intense agricultural land uses, particularly the application of fertilizers, in enriching receiving aquatic ecosystems down- gradient, is common knowledge, with many examples from across the world. One clear example is available in series of papers by Rabelais and colleagues (summary in Rabalais 2002), who demonstrated that fertilizers used in agriculture increased nutrient deliveries from the North American Midwest, down the Mississippi River, and has resulted in a large low-oxygen dead zone in the benthos of receiving Gulf of Mexico off the mouth of the Mississippi Delta. The effects have been exacerbated by the intensive canalization of the river, which to a degree has hastened and isolated riverine flow, preventing nutrient interception in the wetlands surrounding the course of the Mississippi. This example makes clear that coupling between land and sea can exert powerful consequences, and that human activity on land may lead to shifts that can thoroughly alter coupled ecosystems. Land use practices on watersheds have been largely been forced by social and economic interests. If we knew more about the unintended effects of land uses on down-gradient waters—what we refer to here as land–sea couplings, and others have called connectivity or spatial subsidies—perhaps a better weighing of trade-offs might inform coastal landscape planning (DeFries and Eshleman 2004; Hyndes et al. 2014). Fig. 1 Allegorical engraving of the “opposition” of Land and Sea in the The impact of agricultural practices on land–sea coupling is Lagoon of Venice, taken from Bernardo Trevisan, Della Laguna di amply demonstrated by the Gulf of Mexico example. Below, Venezia, Trattato, published in 1715. Reproduced from Lasserre and we focus on the two other aspects, urbanization and defores- Marzollo (2000) tation of contributing watersheds, and use examples from temperate and tropical latitudes. are many examples that show that the exchanges affect food – webs in the coupled units of landscape (Polis et al. 1997, Heck A Temperate, Urbanizing Land Seascape: Waquoit Bay et al. 2008). In the coastal examples, the subsidies and forcing Watersheds and Estuaries may go either way (land to sea or sea to land). As will be evident below, local contingencies turn out to be paramount, In a series of papers, we have made the case that increased and the role of human activities and global-driven change are numbers of people on a watershed result in increased transfer increasingly modifying coupling mechanisms. of nutrients from watersheds to receiving estuarine waters, and In this essay, we use results from our own work in a that the receiving ecosystems have changed accordingly temperate and a tropical site, supported by observations from (Valiela et al. 1992; Valiela 2006). This of course comes as elsewhere, as a few selected examples that show that local no surprise to limnologists, who have long been aware of the contingencies and global effects may influence land–sea cou- coupling of surrounding land use to condition of receiving pling. Discussion of the examples also gives some idea of the freshwater ecosystems. We argue, however, that what we reach of Scott Nixon’s contributions in these topics. recorded in Waquoit Bay follows a broad global pattern for coastal environments. A recent enhanced night image of Europe (Fig. 2)makes two important points. First, there is a proliferation of urban Export of Water-Borne Materials from Land to Sea centers. Second, people tend to accumulate near the coasts. The image is supported by recent data that shows that we are The transfer of materials from land to sea is a natural process at a transcendent stage in human history: during the first that is often accelerated by human activities. Agriculture, decade of the twenty-first century, as human populations grew, urbanization, and deforestation all stimulate natural processes the number of urban dwellers has, for the first time, equaled Estuaries and Coasts

Fig. 4 Accumulation of people and buildings near shore, for the world Fig. 2 Mosaic of enhanced night images of the European region. From (top, Nicholls and Small 2002), and for Waquoit Bay (bottom,Valiela http://www.gsfc.nasa.gov/topstory/2003/0815citylights.html et al. 1992) the number of rural humans (Fig. 3). In addition, in much of understanding the close coupling between nutrient sources the world’scoasts—as well as in Waquoit Bay—people have and marine food webs, and confirmed that, in general, more tended to accumulate as near the coast as feasible (Fig. 4). nutrients tended to increase secondary production in receiving These trends have consequences: more people on watersheds, waters. whether at a large continental scale of at smaller, single system In Waquoit Bay, we showed that coastal watersheds re- spatial scales, result in larger transfer of land-derived nutrients ceived nitrogen inputs from atmospheric deposition, use of to receiving waters (Fig. 5). fertilizers, and disposal of human wastewater (Valiela et al. Many studies have shown that increased nutrient supplies 1997). Despite interception of 75 % of the nitrogen delivered to estuaries and coastal waters substantially change the receiv- to the watershed surface within the watershed, there was a ing ecosystems. In particular, increased dissolved inorganic substantial export of watershed-derived nitrogen to the nitrogen favors increased production of coastal producers. The effects of increased nitrogen supply are somewhat more complex, in that certain producers are favored (macroalgae and phytoplankton), while others (seagrasses, corals) decline (Valiela 2006). These changes cascade up into coastal food webs: Scott Nixon was among the first to demonstrate, using meta-analyses of published fishery data, comparative studies, and experimental mesocosms, that the stimulation of production that resulted from increased nutrient supply in turn increased secondary production, particularly of fish (arguments summarized in Nixon and Buckley 2002). Nixon’swritings through the 1980s and into this century led the way to

Fig. 5 Discharges from watersheds to receiving coastal waters, in relation Fig. 3 Estimated (black points) and projected (white points)totalworld to human density on the watersheds, for European watersheds (in terms of population, 1950–2050, and partition of the total population into people N(black)andP(open symbols)) (top, from Garnier et al. 2002), and for living in urban and rural environments. Data from FAO, http://www.fao.org Waquoit Bay (bottom, from Valiela et al. 2000) Estuaries and Coasts receiving water columns. Land covers and population on the It is harder to qualitatively evaluate whether the changes urbanizing watersheds mediated the export. Wastewater pro- we can clearly document are favorable or negative, an ambi- vided the larger contribution of nitrogen entering the estuaries, guity that fits neatly with the ambivalence of the Land-Sea and since wastewater disposal was a function of people living interaction in the allegory of Fig. 1. Exports from land to on the watershed, more people led to larger nitrogen inputs to sea—land–sea coupling—create a gradient of effects. On the the estuaries. The amount of export, and hence the relative one hand, as Nixon showed in seminal meta-analyses of data effect on the receiving aquatic ecosystems, differed signifi- from many sites, more nutrients support higher primary pro- cantly, depending on local conditions, such as human density, duction, and greater primary production is associated with land covers, and hydrodynamics of the receiving water body. larger fish catch (Nixon 1988). Fish yields from estuarine We can add that infrequent weather events may include regions were similar or larger than yields from well-known different mechanisms that alter transfer of materials between upwelling areas. We can safely conclude that nutrient exports land and sea, and even shift the direction of influence. from land, flowing through estuaries, support coastal fisheries. Ammonium concentrations in the water column of Waquoit To a certain level, nutrient subsidies from land support fish Bay increased significantly after passage of Hurricane Bob production and catches, but larger nutrient exports from land (Valiela et al. 1996, 1998). The mechanism behind the in- can reach tipping levels that have deleterious effects on the creased ammonium appeared to be that salt aerosols fell on receiving estuarine ecosystems. Increased nutrient loads may land and leached ammonium from solids, which the larger not only lower water quality for human uses, but may be than usual rainfall recharge then transported to the estuaries. deleterious to certain community elements, as for example, This was an unusual occurrence, with the sea playing the part to seagrass meadows. In the case of the Gulf of Mexico, of the driver. If we face a future with more frequent intense terrestrial nitrogen inputs obviously exceeded a tipping point, storms, such occurrences might become more common. and the marine end-member has been degraded. Within the Waquoit estuaries, larger land-derived nitrogen Scott Nixon thought much about these matters in regard to inputs, in general, led to increased nitrogen concentrations in fish yields, and he and his student Autumn Oczkowski found a the water column, which fostered larger canopies of system where they could assess the relative effect on fish macroalgae and phytoplankton, and much reduced stands of yields from populations exposed to a large range of land- seagrass (Valiela et al. 1992;Hauxwelletal.1998, 2003). derived nitrogen loads. They compared fish catches from a These consequences of land-derived nutrient loads have a series of lagoons on the Nile Delta, where estimates of nitro- cascade of further influences. Phytoplankton cells moving gen supply and fish yields were obtainable (Oczkowski et al. down-estuary take up ammonium preferentially in the upper 2009). They found that, as expected, initially, catch increased reaches of the estuaries, and transport the nitrogen down- as inorganic nitrogen concentration in the lagoons increased estuary, eventually reaching coastal waters (York et al. (Fig. 6). Beyond a certain point in the gradient of nitrogen 2006). The shallow estuaries, at least in New England, are loading, fish catch decreased markedly. Apparently, beyond usually warmer than the coastal sea, so that the export of this tipping point, increased nitrogen was associated with enriched phytoplankton cells could prime the start of plankton lower water quality, with algal blooms and hypoxia, and cycles in winter. Land-derived nutrient loads exerted different conditions apparently deteriorated enough to reduce fish effects on macroalgae and seagrasses. More nitrogen fostered macroalgal growth, which actively shade sea grasses. Seagrass meadows are preferred habitats for several shellfish and finfish species of commercial and ecological importance; loss of seagrass meadows was followed by a sharp reduction, for example, of scallops, a bivalve closely dependent on seagrass meadows (Valiela et al. 1992). It is evident, therefore, that changes in land use and increased numbers of people on Waquoit Bay watersheds fostered greater delivery of the critical limiting element to estuaries, and there stimulated pervasive changes in the food webs as well as in water quality. Much as in the case of the marine consumers reported by Scott Nixon, the shifts in the coupling of land to sea were consequential enough to transform even Fig. 6 Fish yields from Nile Delta lagoons, plotted versus the mean the upper parts of food webs in the receiving ecosystems. We concentration of inorganic nitrogen measured in the lagoon water col- therefore have sufficient evidence to say that in well- umns. Data from Oczkowski et al. (2009). Catch per unit effort data are lacking, but catch per fisher, or per boat, in relation to area fished, were populated watersheds in temperate latitudes, land to sea cou- reasonably similar in the different lagoons (A. Oczkowski, personal pling is consequential. communication) Estuaries and Coasts populations and catch. This was an important result, certainly research results to manage or restore these adjoined and anticipated from many earlier reports from a variety of differ- interlinked land and aquatic ecosystems (Duarte this issue). ent estuaries that were subject to different levels of enrich- In temperate latitudes, therefore, we deal with land–sea ment. The Oczkowski et al. (2009) study, however, put the coupling that is strongly affected by watershed-scale local pieces of the puzzle together. That study made the point that human activities, including agriculture, and urbanization. land-to-sea coupling indeed had a major role in structuring These linkages are, in turn, affected by the trends driven by food webs in receiving waters, and that some increases in larger external variables, which are substantial enough to nutrient exports were beneficial, but that there were clear restructure the effects of local variables, and which are subject limits, above which detrimental effects became apparent to long-term shifts in baseline conditions. (much as in the case of the dead zones of the Gulf of Mexico). The tipping points, however, are most likely so An Example from Tropical, Subsistence-Level Watershed– subject to local contingencies, that it is improbable that we Estuaries from the Pacific Coast of Panama can define generalizable thresholds for land-derived nutrient loads. Loss of forests is a major agent of ecological and biogeochem- Land–sea coupling does not exist in a historical vacuum, ical change in most of the tropical world, as is evident in many and as is widely known, there are major global climate chang- publications. What is less understood is whether conversion of es taking place. Changes in seawater temperature, sea level, tropical forests to other land covers changes the coupling of and other variables are taking place alongside the demograph- land cover on watersheds to receiving stream, estuary, and ic and economic shifts that alter land covers on coastal water- coastal waters. To examine the possible effects of deforesta- sheds. Scott Nixon and his colleagues at the University of tion on delivery of materials down-gradient to receiving man- Rhode Island early noted such shifts. In a summary paper, grove estuaries and to coastal waters, we located a series of they documented what seemed to be substantial shifts in the coupled watershed–estuary units on the Pacific coast of nitrogen cycle and primary production processes in Panama. The degree of deforestation on these watersheds Narragansett Bay (Nixon et al. 2009). It did appear as if during resulted in a range of 23 to 92 % forest cover (Valiela et al. recent decades, the relative eutrophication of the Bay de- 2013a, b, c). creased, in parallel with warmer temperatures. In addition, These Panamanian watersheds are a world apart from the other major external variables are changing. For example, urbanizing watersheds of Waquoit Bay, and are inhabited by nitrogen concentrations and nitrogen loads delivered to wa- few people, living at a near-subsistence level in a few villages. tersheds and estuaries in NE US by atmospheric deposition The major land-cover shift is that villagers cut and burn the have declined by about half since 2000 (Lajtha and Jones wet rainforest to create and maintain pastures that they in turn 2013, http://epa.gov/castnet/javaweb/index.html). Such a rent for a pittance to absentee livestock owners. Human pop- reduction could have significant consequences for the ulation densities in the region were so low that direct contri- receiving aquatic ecosystems. bution of wastewater was trivial. The soils in the region are not Climate-driven changes are likely in many coastal systems conducive to agriculture. These watersheds were therefore (Lloret et al. 2008). In Waquoit Bay, we find that the canopies convenient for our purposes, which centered on assessing of macroalgae that were so prominent during the 1970s into whether degree of deforestation on watersheds indeed affected the 1990s have actually decreased more recently (unpublished coupling down-estuary and into coastal waters. data). We need to know if these decreases result from climate- related shifts in the nitrogen cycle (responses by temperature- Export of Water-Borne Nutrients from Watersheds As in the sensitive processes, such as denitrification, for example), case of Waquoit Bay, atmospherically delivered nutrients were whether land-derived nitrogen loads have decreased following largely retained within the watersheds with relatively high more careful wastewater management on land, or if some retention values, similar to those reported for other tropical other explanation (for instance, lower atmospheric deposition) sites (Valiela et al. 2013a, b, c). In spite of the generally is responsible. effective retention of nitrogen within the Panama watersheds, The salient point here is that coupling of land and sea takes however, concentrations of dissolved inorganic nitrogen place along historical contexts, and that external (global emerging from watersheds into receiving upper reaches of change) and internal (land use changes, better wastewater freshwater streams bore a significant imprint of watershed management) mechanisms change with time. Thus, as land cover (Fig. 7 top left panel). Contrary to what might be Duarte et al. (2009) noted, there are powerful changing cli- expected, larger concentrations of dissolved inorganic nitro- matic conditions that are changing the baselines that govern gen emerged from watersheds with greater forest cover. DIN dynamics of coastal environments. These changing baselines concentrations discharged from the most forested watersheds must be recognized as the inconstant context for research to were two to three times larger than those emerging from the understand land–sea coupling, as well as in application of most deforested watersheds (Fig. 7 top left). Concentrations of Estuaries and Coasts

Fig. 7 Left panels, concentrations of dissolved inorganic nitrogen measured in water from fresher (<5 ‰), intermediate (5–25 ‰), and saltier (>25 ‰) salinities, in the stream–estuaries receiving inputs from the Panamanian watersheds with different degree of forest cover. Right panels,same,except for N/P, calculated as the ratio of dissolved inorganic nitrogen to phosphate concentrations. Adapted from Valiela et al. (2013a)

dissolved organic nitrogen and phosphate emerging from nitrogen or phosphate to streams (Fig. 8 middle and bottom). watersheds showed no land cover-related effects (Valiela The percent discharge of DON from these watersheds were et al. 2013a, b, c). more variable, but of similar magnitude to the export of DIN The DIN/P in water discharged from the Panama watersheds into streams were low in deforested watersheds and rose in forested watersheds to near Redfield levels (Fig. 7 top right). The land cover-related effect was largely owing to differences in DIN. The range and trend in N/P values were similar to those reported for other tropical sites (Valiela et al. 2013a, b, c). The trends in concentrations (Fig. 7 left panels) and in N/P (Fig. 7 right panels) suggest that first, even though there are reports of conservative N cycles and nitrogen-limited conditions of tropical wet lowland forests (Williams et al. 1997; Wullaert et al. 2010; Parron et al. 2011), these ecosystems leak biologically available nitrogen (Downing et al. 1999; Templer et al. 2008; Brookshire et al. 2012), while grass-covered parcels more effectively retain DIN (Chaves et al. 2009; Corre et al. 2010). Second, during transit down-estuary, concentrations vary but the watershed imprint is lost. N/P varies, but on average remains within Redfield ratio values. Growth of producers growing in the freshwater upper reaches of streams receiving inputs from forested tracts might be limited by phosphorus supply. To estimate the relative water-borne export of dissolved nutrients from the different watersheds, we calculated fluxes of rain-delivered nutrients relative to discharged dissolved nutrients, allowing for evapotranspiration, dry deposition, and assuming conservation of water mass once rain enters the aquifers (Valiela et al. 2013a, b, c). Watersheds with greater proportion of forested land cover exported larger pro- Fig. 8 Percentages of external inputs of DIN, DON, and PO4 that were portions of atmospherically delivered dissolved inorganic ni- discharged from watersheds into receiving streams, for watersheds with different percentages of forest cover (data from Valiela et al. 2013a, b, c, trogen than the more deforested watersheds (Fig. 8 top). and in preparation). Percentages calculated on the basis of mass fluxes Deforestation had no effect on export of dissolved organic (concentrations×water flow) Estuaries and Coasts

(Fig. 8). The relative water-borne exports of nitrogen in Fig. 8 net inputs to watershed surfaces might add about an additional suggest significant retention of atmospheric-derived nitrogen 25 % to the amounts of N contributed by atmospheric depo- within the Panama watersheds. The salient feature here, how- sition. This suggests that the actual percentage nitrogen ex- ever, is that deforestation altered retention and discharges of port, relative to inputs to the ecosystems, through discharges DIN. from watersheds to receiving streams and estuaries may be There is a substantial literature on nutrient releases from lower than we show in Fig. 8. Moreover, our nutrient export tropical land covers, reporting various results, some which estimates based merely on water-borne processes most likely find that forest land covers allow more nitrogen to pass are under-estimates, and the leaps of faith involved in through (Chaves et al. 2009;Deeganetal.2010;Brookshire assessing the gaseous exchanges make clear that developing et al. 2012), much as we report for the Panamanian water- comprehensive nitrogen budgets seems a high priority for sheds. The mechanisms underlying differential discharge of understanding the role of tropical forests in land–sea coupling. nitrogen remain to be understood, but we can offer some What we can show, however, is that, at least for water- conjectures. The C4 grasses that grow aggressively in the borne DIN, the degree of forest cover on Panama watersheds Panama pastures may be adept at effective retention of affects concentrations and loads discharged to receiving wa- nitrogen. Tropical forests hold far more biomass that could ters (Valiela et al. 2013a, b, c, and Fig. 8). Watersheds with be leached of nitrogen by rain, include far more free-living >90 % forest cover discharged about 40 % of atmospheric nitrogen fixing potential in soils, and symbiotic fixers in deposition inputs; watersheds with <30 % forest cover epiphytes, lichens, legumes, orchids, and bromeliads. discharged less than 20 % of such inputs (Fig. 8). So far we focused on water-borne inputs and outputs, but in Deforestation therefore imparted a detectable imprint on the fact, there are other mechanisms of gains and losses of nitrogen mix of nutrient exports to receiving waters. that involve gas exchanges, such as nitrogen fixation and denitrification. Both these mechanisms have been hard to Fate of Dissolved Nutrients Within Stream– measure comprehensively at the watershed spatial level, but Estuaries Freshwater derived from watersheds mixes with may involve substantial amounts of nitrogen in tropical forests. seawater during transit down streams and into estuaries, and Free and symbiotic nitrogen fixation could contribute about complex transformations affect nutrients traveling down- half as much nitrogen to the Panama watersheds as added by estuary. The significant imprint of watershed deforestation atmospheric deposition, with mean=57 %, range=47–62 %, that was detectable on nutrient concentrations and N/P from Valiela et al. (in preparation), values based on compila- (Fig. 7 top panels) in the fresh upper reaches were erased tions of measurements in tropical watersheds (Roggy et al. down-estuary as salinity increased (Fig. 7 middle and bottom 1999; Cusack et al. 2009;Reedetal.2011; Batterman et al. panels). Major biogeochemical transformations therefore take 2013). The values we offer here must surely be underesti- place within mangrove estuaries, transformations strong mates, since almost no one has comprehensively measured all enough to erase land cover influences and impart their own fixation sources in wet tropical forests because of the variety characteristics to down-gradient transport of dissolved of sites of fixation and spatial heterogeneity. nutrients. There are too few direct estimates of denitrification for To track changes in nutrients down-estuaries, we plotted tropical forests (Xu et al. 2013)toobtainevenanapproximate water column nutrient concentrations from the different man- balance of nitrogen inputs and outputs that might be appro- grove estuaries versus salinity (Fig. 9). Since we had evidence priate. Some suggest that owing to oxidized state, and low that the watershed imprints were erased down-estuary, for the supply of nitrate in forest soils, rates of denitrification in purpose of this figure we pooled data from all the estuaries. tropical forest habitats might be quite low (Templer et al. These pooled data provided a detailed view of down-estuary 2008). Others argue that denitrification might process patterns, as well as allowed us to examine temporal amounts of nitrogen comparable to 24–53 % of atmospheric differences. deposition on tropical forests, judging from stable isotopic First, we consider ammonium and nitrate gradients as evidence (Houlton et al. 2006). A highly speculative guess examples of down-estuary patterns. During most sampling about denitrification, based on stable isotopic data in gaseous dates (Fig. 9 left panels), ammonium increased up to about losses from Hawaii rainforests (Houlton et al 2006), for sites salinity 15 ‰, and then decreased across saltier samples. This with rainfall similar to that falling of the Panama watersheds, suggests that regeneration or other processes added ammoni- −1 −1 might be that about 7 kg N ha year are lost via N2 and N2O um down gradient; the net addition was insufficient to counter releases. This rate of gaseous N loss is about 25 % of our mean dilution with ammonium-poor seawater and actual loss mech- estimateof30kgNha−1 year−1 that were delivered by anisms farther down the estuaries. Nitrate concentrations di- atmospheric deposition to the Panama watersheds. minished down-gradient, suggesting net losses throughout the From our rather speculative guesses about the magnitude of estuarine gradient, probably related to denitrification or other nitrogen fixation and denitrification, we venture that gaseous mechanisms in sediments. Estuaries and Coasts

Fig. 9 Concentrations of ammonium and nitrate measured in the Panama estuaries, plotted versus salinity, for sampling dates with no unusual conditions (left panels), and on dates where La Niña-driven upwelling (March 2009) and unusually large rainfall (December 2010) occurred. Adapted from Valiela et al. (2012, 2013a)

Second, the data discussed so far (Fig. 9 left panels) estuary transformations, on SPM, we pooled the data into were collected on sampling times during which the region three bins of percent forest cover and three bins of salinity experienced what could be considered “normal” seasonal (Fig. 10 left panels). regimes. In contrast, during two of the samplings, we Concentrations of SPM were larger in streams with less encountered less common, global-driven conditions forested watershed land cover (Fig. 10 left panels). SPM (Fig. 9 right panels). increased farther down-estuary, probably a result of resus- The first unusual sampling took place during March 2009, pended particles entrained by net flow downstream. There when a strong La Niña, with very low associated rainfall, held was no effect of the upwelling event (these data were therefore sway in the southern part of the sampling area, and created a included in the top left panel of Fig. 10), but the rather marked upwelling of ammonium-rich water (the water mass substantial rainfall during December 2010 markedly diluted was to a degree hypoxic). In contrast to the usual pattern seen concentrations of SPM (note in Fig. 10 left bottom panel that in Fig. 9 (left panels), we recorded remarkably high ammoni- there were no samples with salinity >25). We should add that um concentrations being driven from the sea into the estuarine we did not sample immediately after the onset of the La Niña gradients (Fig. 9 top right). The ammonium was actively rains, when we fully expect, from much visual evidence of nitrified within the estuaries, as can be seen in the nitrate widespread erosion of the estuary shoreline, that there was gradient into the estuaries (Fig. 9 bottom right). substantial initial SPM transport. The second unusual event took place during December We conclude, from Fig. 9, that SPM concentrations in 2010, when another La Niña affected the entire region, but streams and estuaries (a) were consistently larger throughout this event was accompanied by very large rainfall (Valiela the estuarine gradient, by factors of 5, 2, and 1.8 as salinity et al. 2012). The unusual volume of rain lowered both ammo- increased from <5 to >25; and (b) increased by factors of 2.5, nium and nitrate concentrations (Fig. 9 right panels). Clearly, 2, and 8.5 down-estuary, for estuaries whose watersheds sup- globally driven climate shifts considerably modified the more ported low, intermediate, and high forest land cover percent- usual nutrient regime of the Panama estuaries during the two ages. Down-estuary entraining of suspended matter was there- La Niña episodes. These re-castings of the dissolved nutrient fore active in all estuaries, the overall SPM load was higher in data showed that there was substantial variation taking place estuaries with deforested land cover, but, surprisingly, the rate down estuarine gradients, and that external, global-scale phe- of entrainment was more marked in estuaries with more nomena could re-shuffle gradients in powerful fashion. forested land cover.

Transport and Transformations of Suspended Particulate Export of Dissolved Nutrients to Coastal Waters Many pub- Matter Down-estuary Down-estuary patterns of concentra- lished sources maintain that mangrove estuaries export mate- tions of suspended particulate matter (SPM) differed greatly rials to coastal waters (Dittmar et al. 2001;Jennerjahnand from those of the dissolved nutrients (Figs. 8 and 9, and Ittekkot 2002; Mallela and Harrod 2008). To ascertain wheth- Valiela et al. 2013b). To simplify presentation of results re- er, in fact, concentrations of dissolved nutrients leaving the garding the effects of watershed forest cover, as well as down- Panama mangrove estuaries were larger than those found in Estuaries and Coasts

Fig. 10 Summary of concentrations of suspended particulate matter and high (91–92 %) watershed forest cover. The upper panels show data (SPM), measured in water from six stations within (left panels) and three collected during samplings without unusual amounts of rain; the lower stations outside (right panels) the Panama estuaries. To show the effects panels show data collected during the December 2010 period of unusu- of different degree of forest covers on the contributing watersheds, the ally large rainfall. Adapted from Valiela et al. (2013b) data were binned into strata with low (23–29 %), intermediate (47–73 %), the near-shore water column, we pooled all the data from the estuarine gradient, and exited the estuaries, could still be different estuaries and compared nutrient concentrations recognized in the near-shore water column. A hint of the emerging from the estuaries relative to concentrations in watershed land cover imprint appears even in the sampling the receiving coastal waters outside the estuary mouths during the very rainy La Niña event of December 2010 (Fig. 11). This comparison aimed to furnish some notion (Fig. 10 bottom right). of the potential export of nutrients from the mangrove Transport of SPM from these estuaries to coastal waters estuaries. seems sufficient to materially couple land and coastal ecosys- Ammonium and nitrate concentrations leaving the man- tems (Valiela et al. 2013b,andFig.12). The colored boxes in grove estuaries were large, up to 2 orders of magnitude higher Fig. 12 show the ranges of δ15Nandδ13C measured in various than concentrations in the receiving coastal waters, thus sug- sources of organic materials in tropical estuaries and coastal gesting potential exports of dissolved inorganic nitrogen. waters. The point symbols show the isotopic values for SPM Differences for phosphate and DON concentrations were not collected, with data binned into three forest cover and three evident. These Panamanian estuaries therefore seemed likely salinity groups. to be exporting dissolved inorganic nitrogen to coastal waters. The potential export of DIN was not affected by the contributing watershed land cover (Fig. 11) and took place in spite of evident within-estuary transformations that managed to erase the watershed imprint (Fig. 7). The DIN that managed to be discharged from the estuaries was probably biologically important because of the impoverished nutrient regimes of the regional coastal water column, at least during the large major- ity of time during the year when there was no coastal upwelling. In addition, the dissolved N/P in water that was about to be discharged from the estuaries to sea (Fig. 7, bottom right panel) was approximately in the Redfield ratio needed by producers.

Export of Particulate Suspended Matter The SPM data from Fig. 11 Comparison of dissolved nutrient concentrations measured as sampling stations outside the estuaries (Fig. 10 right panels) they exited the Panama estuaries, compared to concentrations in water suggest that the watershed imprint we found throughout the collected off the estuaries. Adapted from Valiela et al. (2013a) Estuaries and Coasts

Within-mangrove estuary processes—such as denitrification and ammonium regeneration—are active enough to erase the watershed land cover imprints on the mix of dissolved nutrients moving down-estuary. These within-estuary transformations impart their own signatures on down-estuary and to-sea exports of dissolved nutrients. In spite of the significant watershed retention and within- estuary transformations, mangrove estuaries nevertheless manage to export nutrients in concentrations that greatly exceed those in receiving coastal waters. The exports thus must make biologically meaningful contributions that subsidize coastal production. In addition, the transport and export of Fig. 12 Values of stable isotopes of nitrogen and carbon measured in suspended particulate matter plays an important role in medi- samples of suspended particulate matter (pooled into bins as in Fig. 10), in ating the linkages coupling land–estuaries–coastal sea in the relation to the nitrogen and carbon isotopic ranges of possible sources of Panama coastal zone. SPM in the Panama estuaries and coastal waters. The many sources of All the mechanisms mediating coupling between land data used in this figure are listed in Valiela et al. (2013b) and sea in this region of Panama are occasionally altered by events influenced by global-scale processes. The pattern that emerges is that mangrove trees appear to Under certain circumstances, La Niña-related upwelling be the sources of upstream particulates (open symbols, inserts marine dissolved inorganic nitrogen into the Fig. 12). The particles are then transported down-estuary, mangrove estuaries. On other instances, La Niña-inten- and their stable isotopic values (particularly for the samples sified rainfall severely freshens estuarine waters, altering with higher salinity) converge on values of coastal sediments. conditions for biota, dilutes deliveries of nutrients to Parenthetically, we note that δ15Nandδ13C of SPM of fresher sea, and freshens upper layers of the coastal water water bear a significant land cover imprint that is not apparent column, which impairs upwelling. in Fig. 12; that imprint was lost by the time SPM reached the estuary mouths (cf. Fig. 4 in Valiela et al. 2013b). The δ15Nandδ13C values of SPM included in Fig. 12 Land–Sea Coupling Through Exchanges by Animals suggest that there is a linkage between mangrove tree and and Humans coastal sediments, mediated by transport of SPM. All other potential sources seem likely to make minor (forest trees), or Most of the foregoing concerned water-borne transport that unlikely contributions (forest or pasture soils, grasses). potentially couples land and sea, but there are additional Therefore, from Fig. 10 (top left panel) and Fig. 12,wecould transport mechanisms (Hyndes et al. 2014). In the case of infer that there is estuarine export of SPM that reaches the sea. Waquoit Bay, we already mentioned the mechanisms involv- Of course, the SPM isotopic data could merely indicate a ing marine salt carried by storm-driven aerosols unto water- passive mixing of estuary and coastal sedimentary material, sheds. One other transport mechanism that has is potential but δ34S information for the SPM showed that in fact one animal involvement in land sea exchanges. Schmitz et al. direction of exports—from estuaries to sea—dominated the (2013) highlighted that animal transport of carbon could be linkage, with little role left for import of marine particles into significant compared to other transfers, such as human fossil estuaries (Valiela et al. 2013b). We conclude that in these fuel emissions, for example. Polis et al. (1997)compiledother adjoined ecosystems, the coupling of land to estuary to sea examples of exchanges among spatially-separate landscape (particularly to coastal sediment, in this case) may largely be units. The exchanges of animal-borne carbon (and of other implemented by down-gradient transport of suspended partic- elements such as nitrogen) via movement and transport of ulate matter. stocks therefore merit attention. From the above considerations, it seems clear that There is a substantial literature that demonstrates that many there is substantial retention of dissolved nutrients with- fish and crustaceans use estuaries as nurseries, and that the in these tropical watersheds. Deforestation diminishes— high food abundance in these environments supports fast counter-intuitively—discharge of dissolved inorganic ni- growth of larvae and juveniles. These early life stages grow, trogen, but nevertheless there are still sufficient dis- and at certain stages of development move to deeper coastal charges of dissolved nutrients to have significant bio- waters: the biomass embodied by these exports thus is a logical effects. Deforested watersheds somehow increase potential mechanism that could couple estuaries to receiving the release of suspended particulate matter that can be coastal waters. It is difficult to assess these exports, but some entrained down streams and estuaries. estimates have been made. Deegan (1993), for instance, Estuaries and Coasts estimated that juvenile fish could export about 20 % of pri- on to make the case that some generalities exist. From our mary production from a Louisiana salt marsh estuary to the knowledge of his writings and conversations, we can aver that Gulf of Mexico. Nelson et al. (2013) concluded that prey he would not be surprised by what we conclude below. organisms in shallow estuarine seagrass flats may support up In all such coastal land to sea systems, temperate or trop- to 25 % of fish production in the nearby adjacent Gulf of ical, subsistence or urban, land–sea couplings play a major Mexico region. role. The couplings are largely carried out by biogeochemical Other studies have suggested that animal-borne biomass transformations and exports, which are mainly hydro- can invert the usual transport direction and move marine- dynamically mediated. Estuaries, curiously, exert a dual func- derived materials into coastal watersheds. Marine nitrogen is tion, furnishing ecological services that may at first glance moved to land-based rookeries by roosting seabirds (Onuf appear incompatible. Estuaries act as filters that decouple sea et al. 1977; Anderson and Polis 1999; McCauley et al. from terrestrial inputs, while also often exporting energy-rich 2012). Accumulation of guano from roosting sea birds can subsidies to coastal food webs. be impressive and was the basis of the guano fertilizer industry Estuarine systems interposed between land and sea act as up into the nineteenth century. Pacific salmon grow in the sea filters or transformers within a certain range of terrestrial but migrate to spawn in upland streams, where salmon serve exports. Within that range, estuarine transformations diminish as food for terrestrial carnivores and scavengers. The con- transport of land-derived materials to sea, and hence un- sumers then spread the marine N throughout the landscape. couple coastal ecosystems from inputs from land. At the same Marine-derived nitrogen that was contained in the salm- time, the biogeochemical transformations taking place within on has been found in vegetation and soil of the water- estuaries create conditions where energy-rich materials (am- sheds surrounding the spawning streams (Naiman et al. monium, organic compounds) can be exported to sea by 2002). This transfer of marine-derived nitrogen to ter- hydrodynamic exchanges. In most circumstances, the restrial watersheds was unambiguously determined by exported estuarine waters bear concentrations of materials that stable isotopic evidence. Another example of marine are larger than those in the receiving seawater, and hence materials transported to land is consumption of intertidal estuaries, in turn, subsidize coastal food webs. polychaetes by ants (Palomo et al. 2003). Substantial As we have transitioned from subsistence to intense urban sea-to-land fluxes involving ants have been reported in and agricultural presence on coastal watersheds, human activ- several sites (Palomo et al. 2003 and many earlier ities invariably and powerfully accelerate fluxes from land to references therein; Piovia-Scott et al. 2011) sea. These fluxes may reach tipping points that exceed ability Humans are involved in another, much larger-scale transfer of within-estuary processes to intercept and minimize exports of materials from sea to land. Maranger et al. (2008), based on to coastal waters. Where human populations and activities surveys of world fishery hauls, argued that the commercial increase, land-derived loads not infrequently pass critical tip- fish catch brings large amounts of marine nitrogen to land. ping points, to create critical environmental effects in coastal The estimates were that the nitrogen content in the world fish waters. catch that is consumed by people on land might amount to as DeFries et al. (2004) and Mustard et al. (2005)conveythe much as 20 % of nitrate exported from land to sea (Maranger sequence of events and associated land use changes that et al. 2008). follow the progression from human subsistence use of land- While most studies about land–sea coupling have focused scapes to intense urban or agricultural land use. The sequence on hydrodynamic and biogeochemical mechanisms, it seems of increasing pressure on environments inexorably follows as appropriate to note that exchanges via animal and human more people accumulate on parcels of landscape, regardless of transport of fish catch may be significant, and the direction the latitude where the transition from subsistence to urban of transfer may differ depending on the specific situation and takes place. In our examples, we dealt with the near- site. More concerted study will be needed before we can offer subsistence Panama situation, with minor, yet detectable ef- a comprehensive picture of the net magnitude and direction of fects on export of materials from land, to the more densely these complicated and quite specific transfers. populated, urbanized Waquoit Bay and Nile Delta examples, with the influence of land exports exerting much larger pres- sures on receiving aquatic ecosystems. As human population Discussion pressure builds, we can certainly expect that the relative forcing from land towards sea in any of these coastal settings From the exposition above, it is evident that local conditions will increase. in land use, hydrodynamics, global drivers, and more lead to In addition, we can also be sure that the land–sea coupling contrasting sets of contingencies that make one coupled land– taking place in such increasingly human-dominated coastal sea unit of adjoined ecosystems quite different from the next. zones will be further affected by large-scale global-driven Scott Nixon would surely have agreed, but quickly would go agents of change such as warmer temperatures, sea level rise, Estuaries and Coasts more intense storms, acidification, and more. These global Garnier, J., G. Billen, E. Hannen, S. Fonbonne, Y. Videnina, and M. factors will shift baselines and alter the time trajectories of Soulie. 2002. 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