BGBiogeosciencesBGBiogeosciences1726-4189Copernicus PublicationsGöttingen, Germany10.5194/bg-15-279-2018Evaluating the effect of nutrient redistribution by animals on the phosphorus cycle of lowland AmazoniaP redistribution by animals in AmazoniaBuendíaCorinacoribuendia@gmail.comKleidonAxelhttps://orcid.org/0000-0002-3798-0730ManzoniStefanohttps://orcid.org/0000-0002-5960-5712ReuBjörnPorporatoAmilcarehttps://orcid.org/0000-0001-9378-207XBiospheric Theory and Modelling group, Max Planck Institute for Biogeochemistry, Hans-Knöll Str. 10, 07745 Jena, GermanyCorporación Colombiana de Investigación Agropecuaria (Corpoica), km 32 vía al mar, vereda Galápagos, Rionegro-Santander, ColombiaDepartment of Physical Geography, Stockholm University, 10691 Stockholm, SwedenBolin Center for Climate Research, Stockholm University, 10691 Stockholm, SwedenEscuela de Biologia, Universidad Industrial de Santander, 680002 Bucaramanga, Santander, ColombiaDepartment of Civil and Environmental Engineering and Princeton Environmental Institute, Princeton University, Princeton, NJ, USACorina Buendía (coribuendia@gmail.com)12January20181512792951April201725April201730October201723November2017This work is licensed under the Creative Commons Attribution 3.0 Unported License. To view a copy of this licence, visit https://creativecommons.org/licenses/by/3.0/This article is available from https://bg.copernicus.org/articles/15/279/2018/bg-15-279-2018.htmlThe full text article is available as a PDF file from https://bg.copernicus.org/articles/15/279/2018/bg-15-279-2018.pdf
Phosphorus (P) availability decreases with soil age and potentially limits
the productivity of ecosystems growing on old and weathered soils. Despite
growing on ancient soils, ecosystems of lowland Amazonia are highly
productive and are among the most biodiverse on Earth. P eroded and
weathered in the Andes is transported by the rivers and deposited in
floodplains of the lowland Amazon basin creating hotspots of P fertility. We
hypothesize that animals feeding on vegetation and detritus in these hotspots
may redistribute P to P-depleted areas, thus contributing to dissipate the P
gradient across the landscape. Using a mathematical model, we show that
animal-driven spatial redistribution of P from rivers to land and from
seasonally flooded to terra firme (upland) ecosystems may sustain the
P cycle of Amazonian lowlands. Our results show how P imported to land by
terrestrial piscivores in combination with spatial redistribution of
herbivores and detritivores can significantly enhance the P content in
terra firme ecosystems, thereby highlighting the importance of
food webs for the biogeochemical cycling of Amazonia.
IntroductionThe phosphorus biogeochemical cycle
Phosphorus (P) is a crucial element for life, providing structure
to RNA and DNA and with a key function in energy transfer and storage (ATP
and ADP). In general, weathering is the main source of P to terrestrial
ecosystems. Theories on pedogenesis suggest that under humid climates and
slow tectonic uplift, rock weathering becomes negligible, preventing input of
“fresh” phosphorous to the biosphere
.
Under such conditions, without major disturbances (e.g., glaciation resetting
soil development), P availability and with it net primary productivity
decrease, leading to a so-called retrogressive phase
or terminal steady-state
. However, despite their ∼ 100-million-year-old soils
, some ecosystems in the lower Amazonian basin are among
the most diverse and productive on Earth . This raises the
question as to what prevents Amazon ecosystems from falling into a
retrogressive phase or terminal steady-state?
Amazon basin
The Amazon basin is one of the most biodiverse regions on Earth, including
highly productive ecosystems, essential to the regulation of the global
climate system. It extends over about 7 million km2, 13 % of which is
covered by the Andes, while the rest is characterized by relatively flat
topography. Over millions of years, the topographical gradient has resulted
in a gradient of soil fertility from young and nutrient-rich Andean soils to
ancient and highly weathered soils in the central and lower Amazon basin
. Consequently, rivers originating in the Andes
(called “white water rivers”) transport nutrient-rich sediments, whereas
rivers originating in the lowlands tend to be nutrient poor (“black water
rivers” if they carry organic acids and “clear water rivers” if they do not).
River floodplains cover about 30 % of the basin ;
ecosystems that are seasonally flooded by white waters are traditionally
called várzea and are characterized by a high primary productivity
and tree diversity , as compared to the ecosystems
seasonally flooded by clear or black waters, which are called igapó.
Because of nutrient transport by the white water rivers, an even steeper
nutrient availability gradient exists between várzea and the
terra firme ecosystems, which do not receive nutrients from seasonal
floods. As the Amazon River is on the Equator, its sub-basins exhibit
different seasonality, with rainy season and high waters occurring during
each hemispheric summer, that is May–August north of the Equator and
November–February south of Equator. Not only differences in nutrients but
also differences in precipitation result in diversity among Amazon
ecosystems, such as seasonally flooded rainforests, terra firme rainforests, dry forests, wetlands, and tropical savannas (Cerrado). In the lower
part of the Amazon where water is less limiting, these ecosystems sustain a
particularly high productivity and diversity of life forms
.
P dynamics in the lowland Amazon basin
Conceptual diagram of processes transferring P within the Amazon
basin's ecosystems. Conceptual diagram of processes transferring P across
ecosystems in the Amazon basin. The boxes represent the major ecoregions of
Amazonia and dashed arrows represent animal-driven fluxes and solid arrows
represent abiotic-driven fluxes. The grey tone represents the P content of
these ecoregions from dark (high P content) to light tones (lower P
content).
Here we shortly review the main processes contributing to the P budget of
lowland Amazonian ecosystems as illustrated in Fig. . We
start by discussing the inputs from the bedrock by weathering and then the
likelihood that deocclusion of P in clays could serve as a long-term P
source. Later, we discuss exogenous P input fluxes – first those mediated by
the atmosphere and then those mediated by rivers – and finally how these
inputs could reach seasonally flooded and terra firme ecosystems.
Weathering
Weathering in the central Amazon basin was estimated to be about 75 gPha-1a-1 based on data taken at the mouth of Rio Negro
river, which is an important tributary of the Amazon River draining only the
lowlands . This measurement contrast to trends observed
in soil chronosequences like the Hawaiin Islands and Franz Joseph Glacier
retrogression , where at
terminal steady state no weathering is detectable. The Amazon basin
experiences continental isostatic rebound, where the slow erosion rates are
compensated by slow uplift and weathering of new material
. However, because bedrock can be as deep as
100 m, it is not clear whether or not P released by weathering can reach the
terrestrial biotic cycle . Nevertheless, as dissolved P
reaches the rivers by groundwater flow, it can be used by freshwater
ecosystems and redistributed across sub-basins with floods.
P deocclusion
High amounts of P are found in occluded forms in the old soils of central
Amazon. Life has evolved energetically costly mechanisms, like cluster roots
and mycorrhizal associations to make some of this P available to vegetation
. In a previous paper this
possibility was explored by formulating a model that in a simple but explicit
way, accounts for physical and chemical weathering, secondary mineral
formation, P occlusion, and P deocclusion at a carbon cost. Our modeling
study suggests that because Amazonian soils are very old and the pool of
occluded P is finite, it cannot support the ecosystems in the long run.
Nevertheless, it can act as a reserve of P for the ecosystems.
Atmospheric inputs
Dust originating from African deserts carry P to the Amazon basin, but this
contribution is highly uncertain, spanning 2 orders of magnitude, from 4.8
to 11–47 gPha-1a-1 and 125–426.47 gPha-1a-1. Dust comprises only
about 7 to 17 % of atmospheric deposition, while a much larger fraction is
composed of biogenic particles (83–90 %) originating from the Amazon basin
itself.
Redistribution of P within the Amazon basinP redistribution between and within sub-basins
Biogenic particles, such as pollen, spores, bacteria, algae, protozoa, fungi,
and leaf fragments, are generated by the forest and although to a great
extent
most of them are deposited in the forest again, some (about 19 gPha-1a-1) fall into the Atlantic Ocean
, where they become an important nutrient source to
Atlantic marine ecosystems near the continent. Fires caused by the
amplification of the agricultural frontier also contribute to the internal P
redistribution and export
. Therefore, according to
some of these estimates, the atmosphere could even drive more P losses than
inputs to whole Amazon basin.
In addition to abiotic-driven P fluxes, migratory animals, like fish,
caimans, turtles, and birds, migrate on a seasonal basis between the
Andean-influenced white waters to P-deficient lowland black and clear waters.
Animal migration thus results in a redistribution of nutrients within and
across different sub-basins. This connection between sub-basins is well
studied for some catfish species and has been shown to be significant but
difficult to quantify for the clear and black water sub-basins
(; ).
P redistribution between riverine and terrestrial ecosystems
estimated that 30 % of the Amazon basin complies with
international criteria for wetland definition. Rivers seasonally flood wide
lowland areas, providing sediments and P inputs – a concept referred to as
“flood pulse” . Despite flood pulses being
well documented , it is difficult
to quantify the magnitude of this P flux as it varies depending on the
flooding intensity, type of sediments and suspended matter transported, soil
type, and the functional composition of the várzea and
igapó ecosystems.
Painting illustrating the fauna that can be observed near the
Miritî, a black water tributary of the Caquetá river. The upper half-sphere
represents the dry season, when most of the terrestrial animals are present in
this area. The lower half-sphere represents rainy season, when animals move
deep into the terra firme forest or to the head waters. With the
beginning of the dry season animals feed on what remained from the flood and
some species (turtles and caimans) lay their eggs, which are often consumed
by terrestrial animals. This original water painting was illustrated by
Marcela and Johana Yucuna, indigenous of the Yucuna ethnic group from the
Mirití region (Caquetá, Colombia). The painting is reproduced with the permission of the artist.
Within the sub-basins, P may be transported from aquatic to terrestrial
ecosystems by animals feeding on riverine food sources, terrestrial
piscivores like the jaguar, the giant otter, and fishing birds. Figure presents an illustration of the different animals that can be
seen during the dry (lower half) and wet (upper half) seasons in a black
water rivers, as perceived by indigenous people of the Rio Negro sub-basin.
For example, an adult giant otter (Pteronura brasiliensis) consumes
about 3 kg of fish per day . Assuming fish dry
weight is 20 % and P content of fish at about 1.1–4.5 %
, an adult otter could transfer about 6.6–27 g P per day to terrestrial ecosystems (2409–9855 gPa-1).
Using the population density reported for Suriname, of 1.2 individuals per
km-2, giant otters could contribute about 28–118 gPha-1a-1. Although this species is listed as endangered,
currently there are no population density estimates available and it is
likely that population sizes have been larger than those observed today.
P redistribution between and within seasonally flooded and terra firme ecosystems
P transport by and around rivers can be complemented by terrestrial animals
including soil fauna, insects, and mammals that frequently utilize both
seasonally flooded and terra firme habitats (see Fig. ).
The movement between habitats further enhances the P redistribution potential
on finer spatial scales. In other words, animal movement generates a net
transport of P from relatively nutrient-rich to relatively nutrient-poor
areas, analogous to a diffusion process, but acting against the gradients of
physical flow processes driven by topographic relief. For example, in a study
of a woolly monkey (Lagothrix lagotricha lugens) population in
northwestern Amazon, showed that this population could
import about 1–4 gPha-1a-1 from lowland to uplands
through seed dispersal. A model based on animal movement as an agent of P
redistribution illustrated how megafauna before the Pleistocene extinction
could have sustained P cycling in this basin .
However, it has not been demonstrated that entire ecosystems involving
different trophic levels can achieve a net P redistribution effect in a
similar manner as large herbivores. Here we show, using a simple mathematical
framework, that P from seasonally flooded ecosystems can be redistributed
from the floodplains, enriching P-poor terra firme ecosystems. Because
the model accounts for different transport pathways, including contrasting
animal foraging strategies (piscivory, herbivory, and detritivory) in a
minimal parameterization, it allows us to evaluate the relative importance of
different redistribution mechanisms.
Due to the high complexity of food webs and biotic interactions, it is
impossible to consider all P fluxes driven by animal migration and movement
and the differences across ecosystems. Therefore, it is our objective to
quantitatively evaluate the importance of the different redistribution
mechanisms using a spatially lumped model synthesizing the major processes of
P cycling, including P redistribution by animals (Fig. ).
As a first approximation, rather than focusing on a single mode of transport
(as in ), we consider two foraging strategies of consumer
animals – herbivory and detritivory. Both strategies allow the spatial
redistribution of P. To assess the importance of biomass consumption by
animals on P redistribution under different environmental settings, we
parameterized our model for three contrasting Amazonian lowland sub-basins,
each subdivided into seasonally flooded (P-richer várzea or P-poorer
igapó) and terra firme areas: (1) the Caquetá-Japurá
sub-basin, a white water river rich in Andean sediments and hence relatively
rich in P; (2) the Rio Negro sub-basin, a lowland black water tributary of
the Amazon River which is regarded as P-poor; and (3) the Xingu sub-basin, a
lowland clear water tributary draining Cerrados, a dry tropical savanna
ecosystem seasonally flooded by P-poor clear waters. By doing so, we account
for the main environmental variability affecting our model results, such as
differences in P load of the flooding river (white waters vs. black and
clear waters) and differences in soil moisture regime affecting the P losses
from the ecosystem (dry vs. humid).
Modeling framework
The model includes a “local” P cycling module (based on
), a description of plant–animal and detritus–animal
interactions, and an animal-driven P redistribution mechanism between
seasonally flooded and terra firme ecosystems. The local module,
indicated by an E subscript to identify a specific ecosystem type, consists
of six ordinary differential equations representing the dynamics of
weatherable material, secondary minerals, occluded P, P in available forms
(PdE), P in vegetation biomass (PvE), and P in soil and litter
biomass (PoE). All P stocks and fluxes are normalized by the area of the
corresponding ecosystem (here we use the fractional areas AF and AU for
flooded and terra firme ecosystems, respectively). The model uses
annually averaged soil moisture content to characterize water availability,
and the processes are interpreted on the annual timescale. Since animal
dynamics are much faster than weathering and occlusion, it is safe to assume
that animal pools are in quasi-equilibrium, whereas weathered P, occluded P,
and P in secondary minerals are at steady state, thereby reducing the number
of equations in the local module from six to three. We parameterized the
system for seasonally flooded (F) and terra firme (or upland, U)
ecosystems, coupling these two ecosystems through two biotic P fluxes
representing the effect of herbivores (H) and detritivores (D; refer to
Fig. ). This distinction determines from which biomass pool
animals feed (i.e., from live or dead biomass, respectively). A summary and
description of symbols and parameters is given in Tables and . Our model assumes that herbivory and detritivory
redistribute P within a sub-basin and between both types of ecosystems
(flooded and terra firme) in proportion to the ecosystem area. As a
result of this assumption, a net P transfer occurs between the ecosystem with
higher P in the vegetation or organic matter compartment to the ecosystem
with lower P. This approximation could be relaxed in the future to account
for the fact that animals may preferably consume nutrient-rich foliage and
detritus, which is more abundantly available in the seasonally flooded forest
and hence a greater proportion of it may be
transferred to terra firme ecosystems (i.e., directional P
redistribution). Therefore, the proposed model provides a conservative
estimate of the net P transfer rate.
Description
of symbols. Subscript E may stand for either terra firme (replaced
by U) or seasonally flooded ecosystem (replaced by F).
TypeSymbolMathematical descriptionDescriptionUnitsPoolsPvEphosphorus in vegetationgPm-2PoEphosphorus in soil biomassgPm-2PdEphosphorus in soil solutiongPm-2FluxesOoEkcPdEphosphorus occlusiongPm-1a-1FdvEPdEηsEnZrsEphosphorus uptake by vegetationgPm-2a-1FvoEPvEkvphosphorus losses from vegetationgPm-2a-1FodEPoEkdsET20phosphorus mineralizationgPm-2a-1LossesOoEPoE(kf+krklsEc)phosphorus in organic formgPm-2a-1OdEPdEklsEcnZrsEphosphorus in soil solutiongPm-2a-1Animal fluxesAOoEkDPoEdetritivores consumption of PoEgPm-2a-1AOvEkHPvEherbivores consumption of PvEgPm-2a-1AIodEkDMkD(AFPoF+AUPoU)detritivores mineralized inputs of PvEgPm-2a-1AIooE(1-kDM)kD(AFPoF+AUPoU)detritivores inputs of PvEgPm-2a-1AIvdEkHMkH(AFPvF+AUPvU)herbivores mineralized input of PvEgPm-2a-1AIvoE(1-kHM)kH(AFPvF+AUPvU)herbivores organic inputs of PvEgPm-2a-1Herbivory and detritivory
Two P consumption pathways control P redistribution by terrestrial animals –
one that is supported by live vegetation biomass (herbivory) and one that is
supported by litter and soil organic matter (detritivory). The rate of
vegetation P (PvE) consumption by herbivores is described by a first-order process with a rate constant kH.
This foraging strategy is
characteristic of, e.g., monkeys, birds, and leaf cutter ants together with
their supported food webs (see Fig. ). The rate of organic
matter P (PoE) consumption by detritivores is also modeled as a first-order process with rate constant kD.
This foraging strategy is adopted
by species such as termites, soil fauna, and their food webs. These P
consumption and redistribution fluxes are defined mathematically in the
following.
With reference to Fig. , we can define the rate of
herbivory per unit area in a generic E ecosystem as AOvE=kHPvE
(where AO stands for animal-driven output). When accounting for the areal
extent of each ecosystem, herbivores consume kH(AUPvU+AFPvF). Phosphorus is then released by animals in proportion to the area of
the receiving ecosystem. The flux of P returned to a generic ecosystem is
then calculated as the rate of consumption over the whole basin weighed by
the area receiving P (i.e., kHAE(AUPvU+AFPvF)). Therefore,
the area-normalized input P fluxes to each ecosystem are obtained as
AIvE=kH(AUPvU+AFPvF) (where AI stands for animal-driven
input).
Of this P input to an ecosystem, animals mineralize a fraction kHM
(transferred to the dissolved pool PdE), whereas the remaining fraction
(1-kHM) is transferred to the soil organic matter pool PoE. This
choice is motivated by the fact that animals have limited assimilation
efficiency, resulting in excretion of P in easily available forms (i.e.,
reaching the dissolved pool Pd; ). Based
on these assumptions, the non-mineralized organic inputs to both ecosystems
from herbivores (first subscript v) and detritivores (first subscript o)
are, respectively, expressed as
The inputs in mineralized forms to the PdE compartments are similarly
described as
AIvdE=kHMkH(AUPvU+AFPvF),AIodE=kDMkD(AUPoU+AFPoF).
The net P flux from flooded to upland ecosystems mediated by herbivores can
be also calculated on a whole-basin area basis as
HF→U=AU(AIvU-AOvU)=AF(-AIvF+AOvF).
Using the definitions of P fluxes, HF→U is thus found as
HF→U=kHAU(1-AU)(PvF-PvU).
This equation demonstrates that herbivores mediate a net P transport from
ecosystems with more vegetation P to ecosystems with less vegetation, thus
dissipating P gradients across the landscape. Interestingly, the more uniform
the partition between flooded and upland ecosystems, the larger the flux is,
because AU(1-AU) is maximized at AU=0.5. The same reasoning can be
applied to detritivory, and the corresponding equations are obtained by
substituting the subscript H by D.
Description of model parameters.
TypeParameterDescriptionValueUnitsReferenceAFfraction of seasonally flooded area0.3unit-lessAUfraction of upland or terra firme area0.7unit-lesscommonηmaximum transpiration rate5mm day-1Ttemperature25Celsiuscexponent of runoff leakage function3unit-lessZreffective soil depth1mnporosity0.4dimensionlesskcphosphorus occlusion rate0.00001m2a-1g-1re-calibratedkewind and gravitational-driven losses0.00001a-1klrunoff/leakage rate at saturation0.1a-1kdmineralization rate0.19a-1kvlitter fall rate0.20075a-1krlosses regulation rate0.002a-1kuactive uptake by vegetation10dimensionlesskfwind, animal, fire losses rate0.0001a-1Iwweathering80gPha-1a-1steady-state solutionIdatmospheric deposition of dust5, 11–47gPha-1a-1
Note that, if herbivore consumption is set to 10 % per year, the model
assumes that the same amount of biomass of both seasonally flooded (F) and
terra firme ecosystems (U) is consumed. Therefore, the magnitude of
the redistribution linearly depends on the P stocks in each ecosystem. Animal
population dynamics are effectively neglected here (e.g., the model would not
properly describe herbivore outbreaks that defoliate large areas), although
other approaches to modeling herbivory include an animal pool and employ
nonlinear consumption kinetics (e.g.,
). The advantage of our minimal
approach is that it does not require any parameter except the consumption
rate of vegetation and detritus, for which we show sensitivity analyses, and
the partitioning of animal P to organic and available pools, which does not
play a major role at steady state.
Model structure diagram representing the redistribution of P due to
herbivory and detritivory. Diagram of model structure representing P fluxes
and pools. Black arrows represent the P fluxes among pools representing the
basin dynamics of the P cycle and color arrows represent the P fluxes due to
animal consumption and dual habitat use: green arrows for herbivory fluxes
and brown arrows for detritivory fluxes; red arrow for terrestrial
piscivores.
Model parameterization and inputsWeathering inputs
For the weathering input Iw, we assumed an average molar P concentration
in the bedrock of 75 mol P m-3 and a tectonic
uplift rate for the lowland basin of 0.0057 mm a-1. We assumed that uplift rates are the same for the
lowland basin and that only 60 % of the material in the rock is weatherable.
The steady-state solution corresponds to a weathering flux of about 80 gPha-1a-1. Furthermore, we assume that the P from
weathering is available for plants.
Atmospheric input Id
While P in gaseous phase forms is not common, the atmosphere can transport P-carrying particles. As it has already been discussed in the
Introduction,
deposition of Saharan dust has been found to contribute to the P budget of
the Amazon basin and we chose to work with 5 gPha-1a-1.
The atmospheric deposition of biogenic particles, which accounts for the
highest percentage of atmospheric deposition (about 80 % in the Amazon),
should not be considered as a system input but rather as a sub-basin
recycling process . It should be noted that the term
identified in our model as detritivory could also be considered as a
sub-basin recycling process. Hence, the production of biogenic particles by
forests has a similar effect as detritivore redistribution within the basin.
Flooding inputs
To constrain the range of parameter values in the sensitivity analyses, we
estimate the maximum possible P input based on weathering estimates of a
lowland sub-basin compared to the Amazon basin. The calculation is based on
the assumption that the P cycle is at steady state, i.e., P transport by
rivers out of the basin equals the weathering rate as it was explained in the
introduction.
estimated the P weathering rate for the Amazon and Rio
Negro basins to be 457 and 242 molPkm-2a-1,
respectively. Assuming that the lowlands of the Amazon have a similar
weathering rates as the Rio Negro sub-basin, which is a black water
tributary draining only the lowland, and taking into account that lowlands
occupy about 87 % of the whole basin, their contribution to the total is
about 242×0.87=210.54molPkm-1a-1. Hence, the
Andes contribute with the remaining 457-210=246molPkm-2a-1.
Since the Andes cover 13 % of the total basin, the in situ weathering must be
around 1895.84 molPkm-2a-1. Because our goal here is
to define an upper limit for the sensitivity analysis, we assume that all the
P from Andean weathering is deposited through flooding to the
seasonally flooded areas. These areas occupy 30 % of the drained area, so
that the total amount of P that is deposited amounts to 1895/0.3=6316 mol P molPkm-1a-1
(i.e., 1957 gPha-1a-1). Following similar calculations, for igapó ecosystems the
deposition rate is estimated as 700 mol P molPkm-2a-1
(i.e., 217 gPha-1a-1). Considering that most of the
material is transported during the raining season, flood plains are
inundated during some months the year, and P can recycle within the basin more
times before it is discharged into the ocean, we let the flooding input for
the várzeaIfw be 80 % of the estimated 1566 gPha-1a-1 and the flooding input to the igapóffB 90 % of estimated 196 gPha-1a-1.
Terrestrial piscivores
In addition to flooding, terrestrial animals that transport P from river to
flooded ecosystems, for example giant otters, fishing birds, and humans, are
represented here as annual fluxes of P to flooded areas as the animals will
probably use terra firme areas close to the rivers.
For the animal P flux from rivers to the flooded areas, simulations with
three different P inputs were run, with values of 0, 72, and 242 gPha-1a-1. The first value simulates a scenario with no
animals, the second simulates a scenario in which P transfer is like the one
estimated for giant otter (Pteronura brasiliensis; see calculation in
the introduction), and the last one simulates a scenario in which otters and
other animals contribute; since this contribution is unknown, the limit for
the sensitivity analysis was set to a value between 3 to 4 times the second
estimate, 242 gPha-1a-1.
Balance equations
The following equations represent the P balances of a generic ecosystem
(subscript E). The specific equations for terra firme and seasonally
flooded ecosystems are obtained by replacing subscript E with U for upland
and F for flooded. The parameters used for seasonally flooded
and terra firme ecosystems are the same, with the exception of yearly
averaged soil moisture sE and the ecosystem spatial extent (AU and
AF). Vegetation obtains P from available forms in the soil (PdE)
through water uptake (passive mechanism) and symbiotic organisms (FdvE); losses are due to herbivory
(AOvE) and litterfall (FvoE;
see Fig. ):
dPvEdt=FdvE-FvoE-AOvE.
Soil and litter organic biomass (PoE) increase due to litterfall (FvoE) from the same ecosystem as well
as from the connected ecosystem due
to the contribution of herbivores (AIvoE), detritivores (AIooE),
and terrestrial animals feeding on riverine food sources (piscivores) that
transport P to flooded ecosystems (IaoF). P release due to
mineralization of soil organic matter is a function of soil moisture and
temperature. Detritivores also induce mineralization and redistribution of
PoE through the flux AOoE. Accordingly, the mass balance equation
for organic matter P reads
dPoEdt=IaoF+FvoE-FodE-OoE-AOoE+AIvoE+AIooE.
P in available forms (Pd) receives inputs from atmospheric dust deposition
(Id), weathering (Iw), flooding in seasonally flooded ecosystems
(IfF), terrestrial piscivore imports to flooded ecosystems (IadF),
mineralization of PoE (FodE), and mineralization and
redistribution through animals (AIodE+AIvdE). Losses are driven
mainly by runoff and leaching OdE, vegetation uptake FdvE, and
occlusion OdcE, so that the mass balance equation for available P can
be written as
dPdEdt=Id+Iw+IfF+IadF+FodE-[FdvE+OdcE+OdE]+AIodE+AIvdE.
Sensitivities to parameters like soil moisture, vegetation active uptake, and
runoff are presented in , and the values chosen for
simulations are listed in Table 1.
Description of model parameters that are site
specific.
TypeParameterDescriptionValueUnitsReferenceSite specificAUfraction of land covered with terra firme ecosystems0.7dimensionlessAFfraction of land covered with flooded ecosystems0.3dimensionlesssUyearly averaged soil moisture0.2–0.6dimensionlessvariableof terra firme ecosystemssFyearly averaged soil moisture0.7dimensionlesschosenseasonally flooded ecosystemsIfWinputs by seasonal flooding to várzea ecosystems1566gPha-1a-1chosenIfBinputs by seasonal flooding to igapó ecosystems196gPha-1a-1chosenIaFinputs from river to land by animals0, 72, 242gPha-1a-1variableAnimal-drivenkDlitter and soil organic matter0–0.3a-1variableconsumption by detritivoreskHvegetation consumption by herbivores0–0.1a-1variablekDMmineralization fraction due to herbivory0.5a-1chosenkHMmineralization fraction due to herbivores0.5a-1chosenParameterization of animal dynamics
The parameterization of animal dynamics requires only a few parameters. P
from animal turnover and excreta is assumed to be transferred equally to
either available P and soil organic matter P (i.e., kHM=kDM=0.5).
Altering this assumption did not significantly affect the results. Herbivore
and detritivore consumption rate constants (kH and kD) are varied in a
sensitivity analysis over a range consistent with observations
Scenarios for Amazonian sub-basins
To assess the importance of biomass consumption by animals on P
redistribution under different environmental settings, we parameterized our
model for three contrasting Amazonian lowland sub-basins: (1) the
Caquetá-Japurá sub-basin, a white water river rich in Andean sediments
and hence relatively richer in P; (2) the Rio Negro sub-basin, a lowland
black water tributary of the Amazon River which is generally poor in P; and
(3) the Xingu sub-basin, clear water tributary of the Amazon, draining mainly
Cerrados, dry tropical savanna ecosystem.
On the regional scale, the average fluxes are calculated with the assumption
that 30 % of the terrestrial area is seasonally flooded and the 70 % is
terra firme (non-flooded; Junk et al., 2011). We run the model for
terra firme ecosystems (U) using yearly averaged relative soil water
content (sU) of 0.35 for the Cerrado , and 0.6 for
the Caquetá-Japurá and Rio Negro sub-basins. Furthermore, for all
seasonally flooded areas in the three sub-basins (F), we assumed yearly
averaged soil water content (sF) of 0.7.
Simulation setup
The solution of the system of six ordinary differential equations was
obtained using the deSolve package in R . The model
approaches steady state at around 7000 simulation years. Since the initial
state of the system is not known, we use here only the steady-state solutions
for our results.
Simulation results
Herbivores and detritivores affect the P cycle in the simulated sub-basins in
multiple ways, as illustrated in Figs. 4 and 5. These figures show contour
plots of the parameter of interest (P fluxes in Fig. and P
stocks in Fig. ), as a function of herbivore and detritivore
consumption rates. These patterns are described first regarding the more
humid sub-basins (Caquetá/Japurá, Rio Negro) and then to explore different
climatic conditions using the Xingu sub-basin as a case study. The two
subsequent Figs. () and () show the effect of either
herbivory or detritivory (respectively), while also considering
piscivore-mediated P redistribution.
Sensitivity of P fluxes of the model at steady state to herbivore
and detritivore consumption rates. The first row of panels show the net P
input to terra firme due to herbivory and detritivory (total animal
input to TF – animal output of TF). The second row shows the P dissolved
losses to the terra firme and the last row the sub-basin total losses.
This simulation assumes a terrestrial piscivore input to the seasonally
flooded ecosystem of 72 gPha-1a-1.
Our model results show that at steady state, in general, terra firme
ecosystems have less P in biomass than their associated seasonally flooded
ecosystem (Fig. , middle row), this is expected due to the P
inputs with seasonal flooding. The gradient between the coupled ecosystems is
steeper when P inputs are higher, and therefore Caquetá/Japurá receiving Andean
sediments flooding inputs has the steepest gradient. The redistribution of P
due to animals (herbivores and detritivores) helps to dissipate the P
gradient between the coupled ecosystems, resulting in a net P transfer from
seasonally flooded to terra firme ecosystems (Fig. , top row).
Animals mediate this P transfer, but the feedbacks of animal consumption on
the various P pools in the model make the role of animals non-trivial –
involving both positive and negative effects on vegetation P depending on the
intensity of herbivory and detritivory.
Sensitivity of P states of the model at steady state to herbivore
and detritivore consumption rates. The first row of panels show the status of
P in terra firme due to herbivory and detritivory. The second row
shows the difference between P in vegetation in terra firme ecosystem
and in seasonally flooded ecosystem to represent the P gradient and how this
differentially gets dissipated with herbivory and detritivory (AFPvF-AUPvU). The last row shows total P at the sub-basin (AF(PvF+PoF+PdF)+AU(PvU+PoU+PdU)). This simulation
assumes a terrestrial piscivore input to the seasonally flooded ecosystem of
72 gPha-1a-1.
In humid sub-basins, increasing consumption rates by either herbivores or
detritivores speeds up the P cycle by increasing cycling and mineralization
of organic P. The effect is similar for P-rich (left columns in Figs. –) and P-poor sub-basins (middle columns), despite
the latter showing smaller P stocks and fluxes than the P-rich systems. On
one hand, this enhanced P cycling increases P transfer from the flooded to
the terra firme ecosystem (Fig. , top row); on the other
hand, due to the larger available P pool, P losses from the terra firme
ecosystem and overall on the sub-basin scale also increase (Fig. , middle row). Despite the enhanced P losses, the net transfer of
P from flooded to terra firme ecosystems sustains a larger terra firme
vegetation than in absence of herbivores and detritivores (Fig. , top row). The two consumption pathways appear largely
complementary, as indicated by approximately hyperbolic contour curves for
these fluxes (left two columns in Fig. ). Under the humid
conditions of the Caquetá/Japurá and Rio Negro sub-basins, both strategies
acting simultaneously enhance P in vegetation at low herbivory and
detritivory rates (< 1.5 % per year), whereas intensifying herbivore
consumption eventually decreases the vegetation P stocks, especially at high
detritivore consumption rates (Fig. , top row). Therefore,
animal contribution to P redistribution is optimal for vegetation P in the
terra firme at intermediate values of herbivore consumption (1–2 % per
year) and only under low to moderate detritivore consumption rates (< 3 % per
year).
While a rate of herbivore consumption of 1–2 % maximizes P in living biomass
of the terra firme ecosystem, a rate of only 1 % or less maximizes the
P status of the whole sub-basin (Fig. , bottom row), and this
maximum only occurs at low detritivore consumption rates. This difference
originates from the P gains of the terra firme ecosystem but also takes into
account the losses of the seasonally flooded ecosystem that occupies 30 % of
the sub-basins area. Therefore, despite larger vegetation P under certain
combinations of consumption rates, the steady-state total P stocks on the
sub-basin scale tend to decrease with increasing consumption rates, except at
very low consumptions rates (Fig. , bottom row) due to the
corresponding increasing P losses.
Herbivory and detritivory affect the P status of vegetation in the
terra firme ecosystems in a different way under more arid conditions,
suggesting a potentially important role of climate in mediating P
redistribution, as illustrated in Figs. and
(right columns). In the dry Xingu sub-basin, patterns are more complex than
in the moister sub-basins. There, the effect of the two consumption pathways
on the net P transfer between flooded and terra firme ecosystems is
mainly additive (rather than complementary as in the humid sub-basins), as
shown by the monotonically increasing contour curves in Fig.
(top-right panel). Despite the positive effect of both consumption pathways
on P transfer, the steady-state vegetation P in the terra firme
ecosystem does not increase monotonically with increasing consumption rates
(Fig. , top right). Intermediate values of herbivory (1–2 % per
year) maximize vegetation P for detritivory rates below 6 % per year, while
no maximum occurs under very intense detritivore consumption. For a given
herbivory rate, increasing detritivore consumption increases vegetation P, at
low kD, but has a negative at high kD values (top right panel in Fig. ).
Sensitivities of herbivory on P in vegetation for the three
sub-basins with different terrestrial piscivores P inputs. Effect of
herbivory rates on P in vegetation (gPm-2) for the three
sub-basins (columns) at seasonally flooded and terra firme ecosystems
and on the sub-basin scale (rows). The different line types refer to
different input estimates to the flooded ecosystem by terrestrial piscivores
(none, otters only, otters and other species). Simulations were run without
detritivory.
Sensitivities of detritivory on P in vegetation for the three
sub-basins with different terrestrial piscivores P inputs. Effect of
detritivory on P in vegetation (gPm-2) for the three sub-basins
(columns) with different terrestrial piscivores P inputs. P in vegetation is
shown for seasonally flooded and terra firme ecosystems and on the
sub-basin scale (rows). The different line types refer to different
mechanisms of P input to the flooded ecosystem by terrestrial piscivores
(none, otters only, otters and other species). Simulations were run without
herbivory.
In Figs. and we also tested the role of P
transport by piscivores from the rivers to the flooded areas, from which it
may be transported further inland by detritivores and herbivores as described
above. In all sub-basins, piscivore activity (solid and dotted lines compared
to the dashed line) significantly improves the P status of both flooded and
terra firme ecosystems. In particular, higher piscivore activity
emphasizes the maximum in vegetation P in terra firme ecosystems at
intermediate levels of herbivore grazing pressure.
Discussion of simulation results
We explored the effect of P redistribution through herbivory and detritivory
on P availability in three different sub-basins within the Amazon basin. We
also considered different P inputs originating from terrestrial piscivores
and we investigated the interactions between herbivory and detritivory,
flooding regime, and the role of soil moisture. Our results highlight four
important points: first, plants growing in terra firme ecosystems can
gain P from redistribution induced by both herbivory and detritivory. Second,
animal-driven redistribution leads to contrasting P in vegetation depending
on herbivore grazing pressure. While small herbivory rates significantly
enhance the P in vegetation in terra firme ecosystems with a maximum
around 1–2 %, detritivory monotonically increases the P availability in these
ecosystems, resulting in a saturation at high consumption rates. Third,
differences in soil moisture conditions as well as in P input through
flooding across the three sub-basins lead to differences in the absolute
amount of P in vegetation and to different responses to herbivory and
detritivory. Fourth, terrestrial piscivores importing P to flooded ecosystems
in combination with the redistribution by detritivores and herbivores can
fertilize terra firme ecosystems. For terra firme at the dry
Xingu, the extra P input by piscivores switches the redistribution effect of
herbivory and detritivory from decreasing to increasing vegetation P (Figs. and ).
Our results show that herbivory annual consumption rates of 1–2 % led to a
maximum in P availability in the terra firme ecosystem. In a
terra firme forest in the Rio Negro basin, leaves account for about
0.51 gPm-2, stems 2.60 gPm-2, and roots 1.71 gPm-2, adding up to
about 5 gPm-2(a value consistent with those obtained in our
simulations; Fig. ). Leaf cutter ants in the tropical forest of
Barro Colorado Island (Panama) consume about 10 % of foliar biomass per year
. Assuming that ant consumption rates are
similar across tropical terra firme forests, 10 % of the foliage
consumed in the Rio Negro basin leads to an overall P annual consumption rate
of 1 % of vegetation biomass. Considering the presence of other herbivores,
the overall consumption rate probably ranges between 1 and 3 % per year,
which is also in agreement with the predicted range that maximizes vegetation
P in the terra firme ecosystem, and in the upper range of our estimate
of 1 % herbivory, maximizing the P status on the sub-basin scale (Fig. ). Moreover, our model suggests that herbivory rates greater
than 2.5 % exert a negative effect on P availability in ecosystems that lack
substantial sources of P (like the Rio Negro basin).
It would be interesting to assess whether other models of nutrient redistribution
exhibit a similar transition from positive to negative effects (for example,
in the case of megaherbivores before the megafauna extinction; see
). It is worth noting in this context that in about 50 %
of the world ecosystems, the fraction of biomass consumed by herbivores is
indeed lower than 5 % .
Furthermore, our model simulations suggest that P redistribution through
detritivores is in general of similar importance than that of herbivores.
Observations from central Amazonian forests showing that the proportion of
animals feeding on living plant material is rather small (about 7 %) while
the proportion of animals feeding on detritus is about half of the total
are in agreement with our finding that higher
detritivory than herbivory is necessary to maximize P in vegetation. For
example, termites are present in most Amazonian ecosystems
, where they abandon nests at a rate of approximately 165 nests ha-1a-1. In terms of P, this rate translates to a
turnover rate of about 600 gPha-1a-1, comprising 95 %
woody turnover and 8.5 % total litter turnover
.
These dynamics create micro-sites of fertility, but over larger scales and in
the long-term they offer a mechanism for P transfer from flooded to terra firme ecosystems. The study of on abandoned raised
agricultural fields in a seasonal flooded ecosystem found a positive
correlation between P content of the fields and the number of termites, ants,
and worms. This is consistent with our model finding that redistribution is
key to the P budget of the terra firme ecosystems and that
detritivores are particularly important in this process
(Figs.
and ).
P dynamics of the Amazon basin and its implications
Our results follow from the assumption that herbivores and detritivores can
effectively transport P deep into the terra firme ecosystems. Is this
assumption reasonable, considering current Amazonian fauna? Amazonian food
webs are poorly understood from the perspective of modern science, but
communities inhabiting the Amazon have a deep understanding of how they
function. As an example Fig. illustrates some of the animals
(birds, insects, snakes, and big cats) that are driving the P transfer
associated with the Mirití, a black water tributary to the Caquetá, based
on the personal experiences of the native people.
Leaf cutting ants, although not herbivores in the strict sense, take amounts
of leaves much greater than one would assume based on their body size. This
is because ants do not directly feed on leaves but on the fungi they grow
with them. Other animals in turn feed on ants, like birds, anteaters, and
monkeys, which in turn are eaten by large predators like the jaguar (Fig. ). Thus leaf P can be later excreted by a jaguar in the deepest
part of the terra firme ecosystems due to the activity of the whole
food web. This means that a complex food web may allow P transport to areas
far away from seasonally flooded ecosystems and rivers. To illustrate this
process, one may consider it in analogy to a wave: a wave moves over long
distances, but the particles (animals in our context) transfer the energy (P)
from particle to particle. It is not necessary that a single animal moves
far, but it is the total action of the movement that could result in a net
input of P to the P depleted regions. We can imagine how a P atom may travel
in complex ways across the Amazon, but a deterministic model of such
movement is unfeasible. Animal movement due to dual habitat use is not
restricted to invertebrates as in the example above, but it is also
documented for fructivorous vertebrates, which use both seasonally flooded
and terra firme habitats. Some animals move on a daily basis, while
others move on a seasonal basis.
showed that this
movement is related to spatial variations in fruit availability. The arboreal
species take advantage of the newly available immature and mature fruits,
while terrestrial vertebrates mainly profit from fruits remaining after the
flood. As we already mention in the introduction, a study on a population of
woolly monkeys (Lagothrix lagotricha lugens) shows that their dual
habitat use results in a net P flux of 1–4 gPha-1a-1 from
seasonally flooded forest to terra firme forest
. The magnitude of P imported by this single monkey
population is of the same order of magnitude of the P inputs through the
atmosphere originating from the Saharan desert. Hence, the finding of our
model that animals contribute substantially to P redistribution in the Amazon
basin appears reasonable.
Our results also illustrate how terrestrial animals and the associated food
webs that feed on riverine sources of food together with herbivores and/or
detritivores can fertilize terra firme ecosystems (Figs. and ). Those P imports are particularly important in
sub-basins drained by clear and black water rivers, which do not receive
large amounts of P because the waters that flood those sub-basins are very
poor in P (as illustrated in Fig. ). This flow of P associated
with the Amazonian food webs has implications for human effects on the Amazon
basin. Humans have inhabited the Amazon basin for at least 19 000 years and
also rely in riverine sources of food. They have created a soil of high
fertility, the terra preta, which has been shown to be widespread in
the western part of the Amazon and it is associated with clear and black water
rivers . The population density of pre-Colombian
societies in the Amazon before European arrival is still highly uncertain.
However, one could imagine that humans were and to some degree are still are
as important as other predators for the transfer of P from rivers to land.
So far, we solely considered the transfer of P from rivers to land, but not
the P transfer between sub-basins. Although this is not included in our
model, fish migration in the Amazon River network constitutes an important
mechanism transferring P from the nutrient-rich white waters to the
nutrient-poor black and clear water rivers . Large
predator species such as the catfish and detrital-feeding fish species
migrate from rivers relying on the Andean nutrient supply to rivers that
drain nutrient-poor lowlands (; ).
Although fish migrations are well studied, the reasons why they occur remain
unclear. One reason might be stoichiometric constraints during ontogenesis
. Juveniles migrate to the estuaries
, where P is abundantly available due to the
mixture of sediments with saltwater. There, they can feed on nutrient-rich
resources for growth. Adults mainly require energy and locations for
reproduction, which are mainly found upstream in small rivers in the forests
. This migration potentially results in a
depletion of the P gradient between rivers originating in the Andes, the
mouth of the Amazon River, and the black water lowland rivers
. Using information on the productivity of the forest
and how fish change their nutritional needs through the life cycle could help
to better understand this remarkable animal-driven P redistribution
mechanism.
Comparison with other modeling approaches
A publication presenting a model of P redistribution due to herbivory in the
Amazon basin by argued that the last extinction of
megaherbivores, about 13 000 years ago, decreased significantly P
redistribution within the Amazon basin. They suggest “major human impacts on
global biogeochemical cycles stretch back to well before the dawn of
agriculture. Aspects of the Anthropocene may have begun with the Pleistocene
megafaunal extinctions”. Our results agree with those of
in identifying animals as important drivers of the P cycle and therefore
essential to Amazon productivity. However, we obtain different insights about
P dynamics in the Amazon and how important herbivory and detritivory might
be. We find that excessive herbivory can have negative effects of the P
budget. Thus the expansion of cattle farming in the Amazon (i.e., human
associated megafauna) is not only a driver of deforestation but may also
have long-term effects on biogeochemical cycling of the Amazon. If cattle
feeds on vegetation in the basin, but is transported elsewhere for
consumption, it represents a net P loss from the system. Locally, cattle
movement can concentrate P around drinking or resting areas, thus
substituting the natural redistribution processes with a P concentration
mechanism. P would then be easily lost via leaching from these biogeochemical
hot spots, which would also represent a net loss, but via a different route.
In contrast to our approach, only consider herbivores
feeding in the seasonally flooded ecosystems, and base their model on the
behavior of current large herbivores living in African savannas. Herbivore
movement is approximated by a Brownian motion and the redistribution of P is
assumed to be proportional to the size of the herbivore
. Therefore, the effects of detritivores
and small organisms, such as leaf cutter ants that harvest a
disproportionately large amount of biomass compared to their size, are
neglected, and the role of complex food webs that may allow long-distance
transport may be underestimated. This model also does not consider
terrestrial animals feeding on riverine food sources, like birds, humans, and
otters, which our model shows to be very important in terms of P
redistribution.
At the same time most of the megaherbivores went extinct (as assumed by
Doughty et al., 2013), pre-Columbian societies would have shifted their diet
towards fish and thereby would have enhanced the flux of P from rivers to
land. Terra preta soils widespread in many terra firme
ecosystems in western Amazonia are evidence for this human action. Moreover,
pre-Colombian societies may have increased the contact areas with rivers by
creating ponds and channels (so-called earthworks, or geoplyphs), which may
have increased nutrient input by flooding . Taking this one
step further, one may speculate whether pre-Columbian cultures of the Amazon
intentionally enhanced the nutrient flux from river to terrestrial ecosystems
and whether they did this by creating channels, feeding primarily on riverine
sources of food, and keeping their waste on land.
Following this reasoning, landscape changes that are currently occurring in
the Amazon region, such as the construction of dams, canalization of the main
channels, and land-use changes towards pastures and crops will likely have
impacts on the intermediate and long-term P dynamics of Amazonia and,
consequently, its productivity and ecosystems dynamics. For example, the
canalization of rivers reduces the contact area between rivers and the
terrestrial ecosystems, thereby reducing flood plains that constitute
important fertility hotspots. Dams disrupt fish migrations, thus reducing the
P flux from nutrient-rich freshwater ecosystems like the Caquetá-Japurá
river to nutrient-poor rivers like the Xingu. Fish overexploitation,
particularly for export, has a similar effect. Land-use changes are major
drivers of biodiversity loss and may thus reduce the ways P is redistributed
across the basin and thus terra firme ecosystem productivity.
Therefore, a more holistic exploration of P fluxes associated with animals
seems necessary for better understanding the mechanisms that prevent the
Amazon region from reaching P depletion.
Conclusions
We used a simple model to illustrate and discuss our hypothesis that animals
may significantly contribute to the internal redistribution of P within the
Amazon basin by reducing P availability gradient across the landscape. While
rivers tend to dissipate the large-scale P gradient between the Andes and the
lowlands , animals do the same across sub-basins and on
the landscape scale between river, seasonally flooded, and terra firme
ecosystems. Our model assumes that the P from the Andes that is redistributed
by rivers and animals could prevent Amazon lowland forests from falling into
a retrogressive phase despite deeply weathered and nutrient-poor
soils. This is in contrast to previous studies that mainly attribute high
Amazonian productivity to exogenous atmospheric P imports. We advocate the
view that redistribution processes within the Amazon basin are at least as
important as exogenous inputs, based on a synthesis of the available
information and a modeling exercise for the three major ecosystem types
within Amazonia. Keeping in mind future empirical tests and investigations, we
summarize our results as follows.
Flooding not only provides P but also takes it away, especially through
biomass removal. Therefore not only the strength of the P gradient between
seasonally flooded and terra firme ecosystem is important but also the
soil moisture regime and the duration of flooding when comparing different
locations or sub-basins.
Herbivores dissipate the P gradient between seasonally flooded and
terra firme ecosystems much more efficiently than detritivores, while
consumption rates of detritivores can be an order of magnitude higher than
consumption rates of herbivores. Herbivory annual consumption rates of 1–2 % led to a maximum in P availability in the terra firme ecosystem.
Herbivory and detritivory are complementary pathways enriching the P content
of terra firme ecosystems. To understand P Amazon dynamics it
would be important to quantify those effects in the field, e.g., by measuring
the consumption rates of herbivores and detritivores along a P availability
gradient.
All information necessary to reproduce the results is
included in the model description; additionally, the model R code is shared in the Supplement.
The supplement related to this article is available online at: https://doi.org/10.5194/bg-15-279-2018-supplement.
Statement of authorship: CB, AK, and AP defined the research question; CB and SM designed the model; CB and BR
performed model simulations and analyzed the results; CB wrote the first draft of the manuscript; and all authors contributed substantially to revisions.
The authors declare that they have no conflict of interest.
Acknowledgements
Corina Buendía would like to thank Alvaro Buendía, Carlos Rodriguez,
Johana Yucuna,
and Marcela Yucuna for pointing out ways animals transport P; Carlos Sierra
for comments on model structure; Lee Miller and Kerry Hinds for comments on
manuscript structure and language; Thomas Hickler for comments and
corrections of the manuscript; Natalie Mahowald and Carlos Jordan for
pointing out some important aspects of the Amazon P cycle; and the Max Planck
Society for supporting Corina Buendía with a doctoral scholarship and Amilcare Porporato by the
Agriculture and Food Research Initiative from the USDA National Institute of
Food and Agriculture (2011-67003-30222) and the National Science Foundation
(CBET-1033467, FESD 1338694, and EAR 1331846 for the Calhoun Critical Zone
Observatory). We also thank the two reviewers for constructive criticism.
The article processing charges for this open-access publication were covered by the Max Planck Society.
Edited by: Akihiko Ito
Reviewed by: two anonymous referees
References
Andersen, T., Elser, J. J., and Hessen, D. O.: Stoichiometry and population
dynamics, Ecol. Lett., 7, 884–900, 2004.
Antonelli, A. and Sanmartín, I.: Why are there so many plant species in
the Neotropics?, Taxon, 60, 403–414, 2011.
Artaxo, P. and Hansson, H.: Size distribution of biogenic aerosol particles
from the Amazon Basin, Atmos. Environ., 29, 393–402, 1994.
Barthem, R. and Goulding, M.: The catfish connection: ecology, migration, and
conservation of Amazon predators, Columbia University Press, 1997.Bristow, C. S., Hudson-Edwards, K. A., and Chappell, A.: Fertilizing the
Amazon and equatorial Atlantic with West African dust, Geophys. Res. Lett., 37, L14807, 10.1029/2010GL043486, 2010.Buendía, C., Kleidon, A., and Porporato, A.: The role of tectonic uplift,
climate and vegetation in the long-term terrestrial phosphorus cycle,
Biogeosciences, 7, 2025–2038, 10.5194/bg-7-2025-2010, 2010.Buendía, C., Arens, S., Hickler, T., Higgins, S. I., Porada, P., and Kleidon, A.: On the potential vegetation
feedbacks that enhance phosphorus availability – insights from a process-based model linking geological and ecological
timescales, Biogeosciences, 11, 3661–3683, 10.5194/bg-11-3661-2014, 2014.
Carter, S. and Rosas, F. C.: Biology and conservation of the giant otter
Pteronura brasiliensis, Mammal Rev., 27, 1–26, 1997.
Cebrian, J. and Lartigue, J.: Patterns of herbivory and decomposition in
aquatic and terrestrial ecosystems, Ecol. Monogr., 74, 237–259,
2004.
Chadwick, O. A., Derry, L. A., Vitousek, P. M., Huebert, B. J., and Hedin, L.:
Changing sources of nutrients during four million years of ecosystem
development, Nature, 397, 491–497, 1999.
Crews, T., Kitayama, K., Fownes, J., and Riley, R.: Changes in soil phosphorus
fractions and ecosystem dynamics across a long chronosequence in Hawaii,
Ecology, 75, 1407–1424, 1995.
de Mazancourt, C. and Schwartz, M. W.: A resource ratio theory of
cooperation, Ecol. Lett., 13, 349–359, 2010.Doughty, C. E., Wolf, A., and Malhi, Y.: The legacy of the Pleistocene
megafauna extinctions on nutrient availability in Amazonia, Nat. Geosci., 10.1038/NGEO1895, 2013.Duplaix, N., Waldemarin, H., Groenedijk, J., Munis, M., Valesco, M., and
Botello, J.: Pteronura brasiliensis: In IUCN Red List of Threatened
Species, 2008.
Fittkau, E. J. and Klinge, H.: On biomass and trophic structure of the central
Amazonian rain forest ecosystem, Biotropica, 2–14, 1973.
Gardner, L.: The role of rock weathering in the phosphorus budget of
terrestrial watersheds, Biogeochemistry, 11, 97–110, 1990.
Gentry, A. H.: Tropical Forest Biodiversity: Distributional Patterns and Their
Conservational Significance, Oikos, 63, 19–28, 1992.
Haugaasen, T. and Peres, C. A.: Vertebrate responses to fruit production in
Amazonian flooded and unflooded forests, Biodivers. Conserv., 16,
4165–4190, 2007.Haugaasen, T. and Peres, C. A.: Population abundance and biomass of
large-bodied birds in Amazonian flooded and unflooded forests, Bird Conserv. Int., 18, 87–101
10.1017/S0959270908000130, 2008.
Haugaasen, T. and Peres, C. A.: Interspecific primate associations in
Amazonian flooded and unflooded forests, Primates, 50, 239–251, 2009.
Hoorn, C., Wesselingh, F. P., ter Steege, H., Bermudez, M. A., Mora, A., Sevink, J., Sanmartín, I., Sanchez-Meseguer, A.,
Anderson, C. L., Figueiredo, J. P., Jaramillo, C., Riff, D., Negri, F. R., Hooghiemstra, H., Lundberg, J., Stadler, T.,
Särkinen, T., and Antonelli, A.: Amazonia through time: Andean uplift, climate change, landscape
evolution, and biodiversity, Science, 330, 927–931, 2010.
Hudson, T. M., Turner, B. L., Herz, H., and Robinson, J. S.: Temporal patterns
of nutrient availability around nests of leaf-cutting ants (Atta colombica)
in secondary moist tropical forest, Soil Biol. Biochem., 41,
1088–1093, 2009.
Junk, W. J. (Ed.): The central Amazon floodplain: ecology of a pulsing system,
Vol. 126, Ecological Studies, 1997.
Junk, W. J., Bayley, P. B., and Sparks, R. E.: The flood pulse concept in
river-floodplain systems, Canadian special publication of fisheries and aquatic sciences, 106, 110–127, 1989.
Junk, W. J., Piedade, M. T. F., Schöngart, J., Cohn-Haft, M., Adeney,
J. M., and Wittmann, F.: A Classification of Major Naturally-Occurring
Amazonian Lowland Wetlands, Wetlands, 31, 623–640, 2011a.
Junk, W. J., Piedade, M. T. F., Schöngart, J., Cohn-Haft, M., Adeney,
J. M., and Wittmann, F.: A Classification of Major Naturally-Occurring
Amazonian Lowland Wetlands, Wetlands, 31, 623–640, 2011b.
Kronberg, B., Fyfe, W., Leonardos, O., and Santos, A.: The chemistry of some
Brazilian soils: Element mobility during intense weathering, Chem. Geol., 24, 211–229, 1979.
Lambers, H., Raven, J. A., Shaver, G. R., and Smith, S. E.: Plant
nutrient-acquisition strategies change with soil age, Trends Ecol. Evol., 23, 95–103, 2008.Mahowald, N. M., Artaxo, P., Baker, A. R., Jickells, T. D., Okin, G. S.,
Randerson, J. T., and Townsend, A. R.: Impacts of biomass burning emissions
and land use change on Amazonian atmospheric phosphorus cycling and
deposition, Global Biogeochem. Cy., 19, GB4030, 10.1029/2005GB002541, 2005.
Mann, C. C.: Ancient Earthmovers Of the Amazon, Science, 321, 1148–1152,
2008.
McClain, M. E. and Naiman, R. J.: Andean influences on the biogeochemistry and
ecology of the Amazon River, BioScience, 58, 325–338, 2008.
McKey, D., Rostain, S., Iriarte, J., Glaser, B., Birk, J. J., Holst, I., and
Renard, D.: Pre-Columbian agricultural landscapes, ecosystem engineers, and
self-organized patchiness in Amazonia, P. Natl. Acad. Sci. USA, 107, 7823–7828, 2010.McMichael, C. H., Palace, M. W., Bush, M. B.and Braswell, B., Hagen, S., Neves,
E. G., Silman, M. R., Tamanaha, E. K., and C., C.: Predicting pre-Columbian
anthropogenic soils in Amazonia, P. R. Soc. B, 22, 281, 1471–2954,
10.1098/rspb.2013.2475, 2014.Metcalfe, D. B., Asner, G. P., Martin, R. E., Silva Espejo, J. E., Huasco,
W. H., Farfán Amázquita, F. F., Carranza-Jimenez, L., Galiano Cabrera,
D. F., Baca, L. D., Sinca, F., Huaraca Quispe, L. P., Taype, I. A., Mora,
L. E., Dávila, A. R., Solórzano, M. M., Puma Vilca, B. L., Laupa Román,
J. M., Guerra Bustios, P. C., Revilla, N. S., Tupayachi, R., Girardin, C.
A. J., Doughty, C. E., and Malhi, Y.: Herbivory makes major contributions to
ecosystem carbon and nutrient cycling in tropical forests, Ecol. Lett.,
17, 324–332, 10.1111/ele.12233, 2014.Pauliquevis, T., Lara, L. L., Antunes, M. L., and Artaxo, P.: Aerosol and precipitation chemistry measurements in a
remote site in Central Amazonia: the role of biogenic contribution, Atmos. Chem. Phys., 12, 4987–5015, 10.5194/acp-12-4987-2012, 2012.
Porder, S., Vitousek, P. M., Chadwick, O. A., Chamberlain, C. P., and Hilley,
G. E.: Uplift, Erosion and Phosphorus limitation in Terrestrial Ecosystems,
Ecosystems, 10, 158–170, 2007.
Porporato, A., D'Odorico, P., Laio, F., and Rodriguez-Iturbe, I.: Hydrologic
controls on soil carbon and nitrogen cycles. I. Modeling scheme, Adv. Water Resour., 26, 45–58, 2003.
Rückamp, D., Amelung, W., Theisz, N., Bandeira, A. G., and Martius, C.:
Phosphorus forms in Brazilian termite nests and soils: relevance of feeding
guild and ecosystems, Geoderma, 155, 269–279, 2010.
Runyan, C. W. and D'Odorico, P.: Hydrologic controls on phosphorus dynamics: A
modeling framework, Adv. Water Resour., 35, 94–109, 2012.
Salick, J., Herrera, R., and Jordan, C. F.: Termitaria: nutrient patchiness in
nutrient-deficient rain forests, Biotropica, 15, 1–7, 1983.
Soetaert, K., Petzoldt, T., and Setzer, R. W.: Solving Differential Equations
in R: Package deSolve, J. Stat. Softw., 33, 1–25, 2010.
Sterner, R. W. and Elser, J. J.: Ecological stoichiometry: the biology of
elements from molecules to the biosphere, Princeton University Press, 2002.
Stevenson, P. R. and Guzmán-Caro, D. C.: Nutrient transport within and
between habitats through seed dispersal processes by woolly monkeys in
north-western Amazonia, Am. J. Primatol., 72, 992–1003,
2010.
Swap, R., Garstang, M., Greco, S., Talbot, R., and Kållberg, P.: Saharan
dust in the Amazon Basin, Tellus B, 44, 133–149, 1992.
Uhl, C. and Jordan, C. F.: Succession and Nutrient Dynamics Following Forest
Cutting and Burning in Amazonia, Ecology, 65, 1476–1490, 1984.
Walker, T. W. and Syers, J. K.: The fate of phosphorous during pedogenesis,
Geoderma, 15, 1–19, 1976.Wardle, D. A.: Ecosystem Properties and Forest Decline in Contrasting Long-Term
Chronosequences, Science, 305, 509–513, 10.1126/science.1098778, 2004.
Wardle, D. A., Bellingham, P. J., Bonner, K. I., and Mulder, C. P. H.: Indirect
effects of invasive predators on litter decomposition and nutrient resorption
on seabird-dominated islands, Ecology, 90, 452–464, 2009.
Wittmann, F., Schöngart, J., Montero, J. C., Motzer, T., Junk, W. J.,
Piedade, M. T. F., Queiroz, H. L., and Worbes, M.: Tree species composition
and diversity gradients in white-water forests across the Amazon Basin,
J. Biogeogr., 33, 1334–1347, 2006.Wolf, A., Doughty, C. E., and Malhi, Y.: Lateral Diffusion of Nutrients by
Mammalian Herbivores in Terrestrial Ecosystems, PloS one, 8, e71352, 10.1371/journal.pone.0071352, 2013.