Nutrient limitation in rainforests and cloud forests along a 3000 m elevation gradient in the Peruvian Andes
Joshua B. Fisher1,*,**, Yadvinder Malhi1, Cuba Torres Israel2, Daniel B. Metcalfe1, Martine J. van de Weg3, Patrick Meir4, Silva Espejo Javier E.2, Huaraca Huasco Walter2
1 Oxford University, Environmental Change Institute, School of Geography and the Environment, South Parks Road, Oxford, OX1 3QY, UK
2 Universidad San Antonio Abad del Cusco, Department of Biology, Peru
3 Amsterdam Global Change Institute, Vrije Univesiteit, De Boelenlaan 1085, 1081 HV Amsterdam, The Netherlands
4 University of Edinburgh, School of Geosciences, Drummond Street, Edinburgh, EH8 9XP
* Present address: Jet Propulsion Laboratory, California Institute of Technology, 4800 Oak Grove Drive, Pasadena, CA, 91109, USA
** Corresponding author. E-mail address: joshbfisher@gmail.com, 1-323-540-4569
Supplemental Table 1. Individual tree data for 77 trees across all four sites (WA=3000 m, SP=1500 m, TO=1000 m, TA=200 m). Fertilization treatments are given as N (N0), N+P (NP), P (P0) and control (C). Some data were missing or unknown.
Site
|
Tree #
|
Plot
|
Fert
|
Family
|
Genera
|
Species
|
DBH (cm)
|
Height (m)
|
Leaf N (%)
|
Leaf P (%)
|
Leaf K (%)
|
WA
|
51
|
7F
|
N0
|
CUNONIACEAE
|
Weinmannia
|
crassifolia
|
8.1
|
8.0
|
1.32
|
0.11
|
0.73
|
WA
|
52
|
7F
|
N0
|
CUNONIACEAE
|
Weinmannia
|
crassifolia
|
7.2
|
7.5
|
1.27
|
0.08
|
1.02
|
WA
|
53
|
7F
|
N0
|
CLUSIACEAE
|
Clusia
|
sp
|
14.4
|
8.0
|
1.51
|
0.12
|
0.61
|
WA
|
54
|
7F
|
N0
|
THEACEAE
|
Freziera
|
parva
|
16.6
|
11.5
|
1.86
|
0.13
|
0.79
|
WA
|
55
|
7F
|
N0
|
CLUSIACEAE
|
Clusia
|
sp
|
6.2
|
6.0
|
1.80
|
0.18
|
0.94
|
WA
|
32
|
9F
|
NP0
|
CUNONIACEAE
|
Weinmannia
|
bangii
|
10.6
|
10.0
|
1.85
|
0.19
|
0.83
|
WA
|
33
|
9F
|
NP0
|
CUNONIACEAE
|
Weinmannia
|
bangii
|
15.6
|
11.0
|
1.47
|
0.16
|
0.58
|
WA
|
34
|
9F
|
NP0
|
CUNONIACEAE
|
Weinmannia
|
crassifolia
|
14.8
|
12.0
|
1.19
|
0.12
|
0.41
|
WA
|
35
|
9F
|
NP0
|
CUNONIACEAE
|
Weinmannia
|
reticulata
|
3.2
|
4.5
|
1.95
|
0.17
|
0.99
|
WA
|
11
|
11F
|
P0
|
CLETHRACEAE
|
Clethra
|
sp
|
10.4
|
7.5
|
1.22
|
0.10
|
0.81
|
WA
|
12
|
11F
|
P0
|
CLUSIACEAE
|
Cusia
|
sp
|
21.4
|
12.0
|
1.31
|
0.38
|
1.00
|
WA
|
13
|
11F
|
P0
|
CLUSIACEAE
|
Clusia
|
sp
|
12.4
|
9.0
|
1.35
|
0.23
|
0.73
|
WA
|
14
|
11F
|
P0
|
CUNONIACEAE
|
Weinmannia
|
crassifolia
|
11.3
|
8.0
|
1.17
|
0.12
|
0.55
|
WA
|
15
|
11F
|
P0
|
CUNONIACEAE
|
Weinmannia
|
crassifolia
|
11.2
|
8.0
|
1.20
|
0.09
|
0.66
|
WA
|
36
|
8/9C
|
C
|
CUNONIACEAE
|
Weinmannia
|
bangii
|
12.2
|
11.0
|
1.49
|
0.12
|
0.61
|
WA
|
37
|
8/9C
|
C
|
MYRSINACEAE
|
Myrsine
|
coriacea
|
8.0
|
8.3
|
2.17
|
0.17
|
2.59
|
WA
|
38
|
8/9C
|
C
|
CUNONIACEAE
|
Weinmannia
|
crassifolia
|
12.7
|
12.0
|
1.18
|
0.10
|
0.90
|
WA
|
39
|
8/9C
|
C
|
CUNONIACEAE
|
Weinmannia
|
latifolia
|
9.8
|
10.0
|
1.68
|
0.11
|
1.25
|
WA
|
40
|
8/9C
|
C
|
ARALIACEAE
|
Oreopanax
|
microcephalus
|
4.7
|
7.0
|
2.60
|
0.28
|
2.10
|
|
|
|
|
|
|
|
|
|
|
|
|
SP
|
312
|
1F
|
N0
|
LAURACEAE
|
Endlicheria
|
griseo-sericea
|
8.9
|
9.2
|
1.90
|
0.26
|
0.62
|
SP
|
313
|
1F
|
N0
|
MELASTOMATACEAE
|
Miconia
|
sp
|
7.8
|
7.0
|
2.22
|
0.23
|
0.73
|
SP
|
314
|
1F
|
N0
|
EUPHORBIACEAE
|
Acalypha
|
|
5.5
|
6.0
|
2.39
|
0.36
|
1.01
|
SP
|
315
|
1F
|
N0
|
EUPHORBIACEAE
|
Hyeronima
|
alchorneiodes
|
42.8
|
17.0
|
2.24
|
0.20
|
0.63
|
SP
|
316
|
1F
|
N0
|
ROSACEAE
|
Prunus
|
herthae
|
4.9
|
5.1
|
2.14
|
0.22
|
1.25
|
SP
|
291
|
3F
|
NP0
|
ANNONACEAE
|
Guatteria
|
duodecima
|
8.9
|
8.8
|
2.23
|
0.13
|
0.73
|
SP
|
292
|
3F
|
NP0
|
SAPOTACEAE
|
Sarcaulus
|
sp
|
15.8
|
15.0
|
1.87
|
0.29
|
0.48
|
SP
|
293
|
3F
|
NP0
|
SAPOTACEAE
|
Sarcaulus
|
sp
|
17.4
|
15.0
|
1.74
|
0.18
|
0.33
|
SP
|
294
|
3F
|
NP0
|
FABACEAE
|
Inga
|
|
16.0
|
13.0
|
2.72
|
0.21
|
0.77
|
SP
|
295
|
3F
|
NP0
|
SAPINDACEAE
|
Paullinia
|
|
2.5
|
3.0
|
1.82
|
0.15
|
0.65
|
SP
|
271
|
5F
|
P0
|
ARECACEAE
|
Euterpe
|
sp
|
17.9
|
13.8
|
2.01
|
0.13
|
0.36
|
SP
|
273
|
5F
|
P0
|
FABACEAE
|
Inga
|
sp
|
20.5
|
12.5
|
3.15
|
0.16
|
0.64
|
SP
|
274
|
5F
|
P0
|
RUBIACEAE
|
|
|
5.0
|
5.0
|
3.00
|
0.16
|
0.91
|
SP
|
275
|
5F
|
P0
|
ACTINIDIACEAE
|
Saurauia
|
sp
|
15.8
|
11.3
|
2.10
|
0.20
|
1.70
|
SP
|
286
|
3/4C
|
C
|
PROTEACEAE
|
|
|
3.9
|
5.9
|
2.25
|
0.29
|
1.37
|
SP
|
287
|
3/4C
|
C
|
MONIMIACEAE
|
Mollinedia
|
sp
|
6.5
|
7.0
|
2.14
|
0.27
|
1.41
|
SP
|
288
|
3/4C
|
C
|
MORACEAE
|
Pseudolmedia
|
sp
|
17.1
|
12.3
|
2.45
|
0.18
|
1.44
|
SP
|
289
|
3/4C
|
C
|
SABIACEAE
|
Meliosma
|
sp
|
28.8
|
12.0
|
1.52
|
0.10
|
0.72
|
SP
|
290
|
3/4C
|
C
|
ANNONACEAE
|
Annona
|
sp
|
10.5
|
7.5
|
2.20
|
0.12
|
0.79
|
|
|
|
|
|
|
|
|
|
|
|
|
TO
|
426
|
1F
|
N0
|
FABACEAE
|
Tachigali
|
|
13.0
|
8.7
|
2.40
|
0.14
|
0.90
|
TO
|
427
|
1F
|
N0
|
LAURACEAE
|
|
|
6.5
|
6.3
|
1.81
|
0.10
|
1.15
|
TO
|
428
|
1F
|
N0
|
EUPHORBIACEAE
|
Alchornea
|
|
15.5
|
11.1
|
3.07
|
0.24
|
1.22
|
TO
|
429
|
1F
|
N0
|
RUBIACEAE
|
Palicourea
|
|
6.0
|
5.0
|
2.96
|
0.15
|
1.68
|
TO
|
431
|
1F
|
N0
|
LAURACEAE
|
Ocotea
|
|
11.6
|
6.1
|
2.03
|
0.11
|
0.80
|
TO
|
406
|
3F
|
NP0
|
LACISTEMATACEAE
|
Lacistema
|
|
22.5
|
18.0
|
2.56
|
0.18
|
1.58
|
TO
|
407
|
3F
|
NP0
|
MYRISTICACEAE
|
Virola
|
mollissima
|
32.2
|
17.0
|
2.34
|
0.13
|
0.70
|
TO
|
408
|
3F
|
NP0
|
LECYTHIDACEAE
|
Eschweilera
|
|
9.1
|
6.0
|
2.11
|
0.09
|
0.72
|
TO
|
409
|
3F
|
NP0
|
MORACEAE
|
Pseudolmedia
|
macrophylla
|
23.9
|
16.0
|
2.39
|
0.12
|
1.04
|
TO
|
410
|
3F
|
NP0
|
RUBIACEAE
|
Elaeagia
|
|
6.0
|
4.3
|
2.04
|
0.08
|
1.50
|
TO
|
441
|
5F
|
P0
|
CHRYSOBALANACEAE
|
Licania
|
|
14.7
|
11.5
|
1.76
|
0.10
|
0.84
|
TO
|
442
|
5F
|
P0
|
RUBIACEAE
|
Elaeagia
|
|
17.9
|
8.5
|
1.90
|
0.08
|
0.59
|
TO
|
443
|
5F
|
P0
|
VOCHYSIACEAE
|
Vochysia
|
sp
|
31.0
|
15.5
|
1.76
|
0.09
|
0.68
|
TO
|
444
|
5F
|
P0
|
FLACOURTIACEAE
|
|
|
6.2
|
4.5
|
2.49
|
0.11
|
1.17
|
TO
|
445
|
5F
|
P0
|
RUBIACEAE
|
|
|
5.6
|
6.2
|
1.67
|
0.11
|
0.63
|
TO
|
401
|
3/4C
|
C
|
MYRISTICACEAE
|
Virola
|
calophylla
|
44.7
|
22.0
|
2.22
|
0.09
|
0.71
|
TO
|
402
|
3/4C
|
C
|
FLACOURTIACEAE
|
Carpotroche
|
longifolia
|
2.4
|
3.0
|
2.28
|
0.14
|
0.78
|
TO
|
403
|
3/4C
|
C
|
FABACEAE
|
Inga
|
|
20.7
|
13.0
|
3.47
|
0.15
|
0.82
|
TO
|
404
|
3/4C
|
C
|
MORACEAE
|
Brosimum
|
utile
|
5.5
|
6.0
|
2.10
|
0.11
|
0.99
|
TO
|
405
|
3/4C
|
C
|
FLACOURTIACEAE
|
Banara
|
|
3.8
|
5.6
|
2.27
|
0.10
|
0.67
|
|
|
|
|
|
|
|
|
|
|
|
|
TA
|
1
|
1F
|
N0
|
BURSERACEAE
|
Tetragastris
|
panamensis
|
21.1
|
14.5
|
1.76
|
0.08
|
0.80
|
TA
|
2
|
1F
|
N0
|
BIXACEAE
|
Bixa
|
arborea
|
18.5
|
13.5
|
3.00
|
0.13
|
1.05
|
TA
|
3
|
1F
|
N0
|
FABACEAE
|
|
|
6.4
|
8.3
|
3.22
|
0.14
|
0.82
|
TA
|
4
|
1F
|
N0
|
MORACEAE
|
Helicostylis
|
tomentosa
|
10.8
|
12.0
|
2.47
|
0.11
|
1.27
|
TA
|
5
|
1F
|
N0
|
MYRISTICACEAE
|
Virola
|
|
5.1
|
7.4
|
2.74
|
0.11
|
0.82
|
TA
|
21
|
3F
|
NP0
|
EUPHORBIACEAE
|
Conceveiba
|
guianensis
|
9.5
|
12.2
|
2.05
|
0.13
|
0.84
|
TA
|
22
|
3F
|
NP0
|
FABACEAE
|
|
|
16.6
|
15.8
|
1.83
|
0.07
|
0.55
|
TA
|
23
|
3F
|
NP0
|
LECYTHIDACEAE
|
|
|
10.7
|
11.0
|
4.34
|
0.18
|
0.73
|
TA
|
24
|
3F
|
NP0
|
MORACEAE
|
Helicostylis
|
tomentosa
|
8.9
|
11.0
|
2.90
|
0.10
|
1.28
|
TA
|
25
|
3F
|
NP0
|
BOMBACACEAE
|
Quararibea
|
witti
|
4.8
|
7.0
|
2.72
|
0.11
|
0.89
|
TA
|
41
|
5F
|
P0
|
MELIACEAE
|
Trichilia
|
sp
|
30.0
|
18.5
|
1.91
|
0.08
|
0.65
|
TA
|
42
|
5F
|
P0
|
MYRISTICACEAE
|
Iryanthera
|
|
6.5
|
4.6
|
1.95
|
0.10
|
0.83
|
TA
|
43
|
5F
|
P0
|
LAURACEAE
|
|
|
7.8
|
10.9
|
2.03
|
0.07
|
0.44
|
TA
|
44
|
5F
|
P0
|
|
|
|
3.2
|
4.2
|
2.92
|
0.13
|
1.02
|
TA
|
45
|
5F
|
P0
|
FABACEAE
|
Tachigalli
|
poliphylla
|
21.3
|
19.0
|
2.67
|
0.11
|
0.79
|
TA
|
27
|
3/4C
|
C
|
|
|
|
35.0
|
24.5
|
3.08
|
0.14
|
0.82
|
TA
|
28
|
3/4C
|
C
|
SIPARUNACEAE
|
Siparuna
|
decipiens
|
9.0
|
9.0
|
2.55
|
0.10
|
2.09
|
TA
|
29
|
3/4C
|
C
|
CLUSIACEAE
|
Calophyllum
|
brasiliensis
|
7.5
|
8.0
|
2.21
|
0.08
|
1.47
|
TA
|
30
|
3/4C
|
C
|
FABACEAE
|
|
|
6.0
|
8.0
|
1.78
|
0.07
|
0.74
|
Supplemental Figure Captions
Supplemental Fig. 1. Study sites with inset from Google Earth. Clouds (not snow) cover much of the mountains in the image.
Supplemental Fig. 2. The experimental set up for the fertilization experiment (shown here at the 1500 m site for example). The long-term 100 x 100 m plot is surrounded on three sides by 10 x 110 m transects consisting of 10 x 10 m sub-plots. Within each transect, two sub-plots were fertilized with N, two with P, two with both N and P, and six controls separated each fertilized sub-plot. Of those fertilized sub-plots within each transect, half began fertilization in the first year (N0, NP0, P0) and the other half in the second year (N1, NP1, P1).
Supplemental Fig. 3. a) Leaf nitrogen (N), b) leaf phosphorus (P), and c) leaf N:P ratio from three canopy heights (top, middle, and bottom) for all four sites (200 m, 1000 m, 1500 m, and 3000 m) and all four treatments (control, N, N+P, and P) in 2008 as mean ± SE.
Supplemental Fig. 4. The mean relative growth rate (RGR) averaged for each Family by treatment type. Data would naturally increase substantially if presented by Genera or Species. Not all Families had all 4 treatments. It is possible to see treatment differences in, for example, Rubiaceae, where the RGR for the Control (black) is less than that for the N treatments (green), which is less than that for the P treatments (purple), which is less than that for the N+P treatments (orange).
Supplemental Fig. 5. Soil respiration contribution for control and fertilized sub-plots from litter, roots, fungal hyphae and microbes in 2009. The top three (Y1) panels are from the sub-plots that received fertilization starting in the first year (2007), and the bottom three (Y2) panels are from the sub-plots that received fertilization starting in the second year (2008).
Supplemental Fig. 1.
Supplemental Fig. 2.
Supplemental Fig. 3.
Supplemental Fig. 4.
Soil respiration partitioning (%)
|
|
Control
|
|
Nitrogen – Y1
|
Nitrogen+Phosphorus – Y1
|
Phosphorus – Y1
|
Nitrogen – Y2
|
Nitrogen+Phosphorus – Y2
|
Phosphorus – Y2
|
|
Site
|
Supplemental Fig. 5. |