FOR ONLINE PUBLICATION ONLY
APPENDIX A: Tables summarizing the porewater salinity, forest structure, growth responses, spatial
characteristics, leaf traits, and nutrients for the three study locations used in this study. These data are
from Feller and Chamberlain (2007), Feller and others (2003a, b, 2009), Lovelock and others (2005).
Distances from the fertilized trees to the mainland and upland vegetation were measured with Google
Earth Pro.
Table A1. Summary of the Explanatory Variables Related to the Canopy Characteristics of Rhizophora
mangle at Indian River Lagoon (IRL), Florida; Twin Cays, Belize; and Bocas del Toro, Panamá in Response
to Nutrient Treatment (Control, +N, +P) in Fringe and Scrub Zones
Location
Zon
e
Nutrie
nt
Salinity
(‰)
Treat
ment
IRL
Frin
ge
Scr
ub
Twin
Cays
Frin
ge
Scr
ub
Tree
Height
LAI
Growth
(cm∙yr−1∙k
g−1)
(m)
Distance to
mainland
(km)
Distance to
upland
vegetation
(m)
Con
33.0 (2.4)
5.1 (1.5)
2.3 (0.8)
9.6 (2.2)
2.67 (0.02)
122.3 (4.5)
+N
35.5 (1.0)
4.2 (1.0)
2.5 (0.5)
41.2
(16.0)
2.67 (0.02)
114.8 (3.2)
+P
31.5 (2.9)
3.9 (0.4)
2.2 (0.9)
6.4 (1.6)
2.68 (0.02)
110.0 (2.6)
Con
32.4 (1.3)
1.6 (0.3)
1.6 (0.7)
3.7 (1.2)
0.26 (0.01)
298.9 (7.9)
+N
32.8 (1.6)
2.7 (0.7)
2.0 (1.0)
51.1
(10.4)
0.26 (0.01)
298.8 (8.3)
+P
32.6 (1.3)
1.7 (0.2)
1.8 (0.4)
5.9 (4.7)
0.26 (0.01)
302.6 (6.2)
Con
36.9 (4.0)
3.5 (0.8)
2.6 (0.7)
9.3 (2.3)
15.99
(0.08)
18986.3
(91.4)
+N
36.8 (2.2)
4.1 (1.4)
3.5 (1.2)
47.0
(18.7)
16.07
(0.35)
19070.0
(82.8)
+P
36.9 (2.4)
4.3 (1.1)
3.7 (0.9)
10.0 (1.7)
15.97
(0.08)
18965.6
(83.0)
Con
39.4 (3.6)
1.2 (0.3)
1.2 (0.9)
4.7 (1.0)
15.96
(0.09)
18963.3
(91.4)
+N
39.9 (3.3)
0.9 (0.2)
1.4 (0.7)
12.3 (4.7)
15.96 (0.1)
18961.1
(98.5)
+P
40.9 (3.5)
2.2 (0.7)
4.6 (1.6)
122.7
(27.7)
15.96
(0.08)
18960.0
(82.8)
Con
33.7 (0.9)
4.6 (0.8)
2.2 (0.9)
19.4 (4.7)
8.81 (3.4)
270.0
(232.0)
+N
30.9 (4.5)
4.5 (1.2)
2.9 (0.7)
77.9
(21.4)
8.81 (3.4)
275.0
(247.6)
+P
33.9 (0.9)
4.2 (1.4)
2.6 (0.7)
31.3 (6.9)
8.8 (3.4)
253.7
(225.3)
Con
32.8 (2.8)
1.1 (0.2)
1.5 (1.4)
11.3 (3.2)
8.83 (3.0)
278.4
(256.7)
+N
33.2 (3.0)
1.3 (0.4)
1.0 (0.4)
19.2 (6.9)
9.35 (3.21)
257.3
(258.5)
+P
32.8 (1.9)
1.5 (0.2)
1.90 (0.6)
25.0 (4.0)
9.34 (3.21)
250.1
(239.7)
Nested ANOVA
F
P
F
P
F
P
F
P
F
P
F
P
Location
74.
249
0.0
00
7.89
9
0.0
01
9.5
95
0.0
00
17.
384
0.0
00
1044.
809
0.0
00
1215.
064
0.0
00
Zone/Location
6.6
94
0.0
00
205.
330
0.0
00
18.
152
0.0
00
6.8
57
0.0
00
42.73
4
0.0
00
10.48
0
0.0
00
Treatment/Zone/Locatio 1.2
n
89
0.2
33
6.80
3
0.0
00
7.4
12
0.0
00
12.
176
0.0
00
0.031
1.0
00
0.039
1.0
00
Bocas
del Toro
Frin
ge
Scr
ub
Values are means ± 1 SD with the F- and P-values for the nested ANOVAs below.
Table A2. Summary of the Explanatory Variables Related to Leaf Traits of Rhizophora mangle at Indian
River Lagoon (IRL), Florida; Twin Cays (TC), Belize; Bocas del Toro (BdT), Panamá in Response to Nutrient
Treatment (NE) as (Control (Con), +N, +P), in Fringe (F) and Scrub (S) Zones (Z) at Each Location (Loc)
*
Lo Z N
LMA
%C
%N
%P
%K
C:N
C:P
N:P
Mean
Mean
Mean
Mean
Mean
Mean
Mean
Mean
c
IR
L
T
C
B
d
T
E
(SD)
(SD)
(SD)
(SD)
(SD)
(SD)
(SD)
(SD)
F C
o
n
0.016
(0.001)
45.1 (0.9)
1.26
(0.19)
0.10
(0.01)
0.74
(0.10)
36.5
(6.0)
473.8
(58.8)
13.1
(1.0)
+
N
0.015
(0.001)
46.3 (1.0)
1.53
(0.13)
0.11
(0.00)
0.81
(0.09)
30.5
(2.5)
441.0
(23.5)
14.5
(1.5)
+
P
0.017
(0.002)
46.3 (0.6)
1.23
(0.28)
0.09
(0.02)
0.67
(0.06)
39.4
(9.9)
521.5
(102.7)
13.4
(4.5)
S C
o
n
0.021
(0.002)
44.3 (1.1)
1.15
(0.07)
0.09
(0.01)
0.78
(0.11)
38.5
(2.8)
474.0
(41.0)
12.3
(1.0)
+
N
0.021
(0.001)
44.5 (0.6)
1.04
(0.06)
0.10
(0.01)
0.80
(0.14)
42.9
(2.2)
463.9
(70.2)
10.9
(2.1)
+
P
0.020
(0.002)
43.9 (0.9)
1.10
(0.04)
0.10
(0.01)
0.72
(0.07)
40.0
(1.7)
452.3
(29.5)
11.6
(1.1)
F C
o
n
0.022
(0.003)
43.4 (0.6)
0.90
(0.19)
0.06
(0.01)
0.71
(0.05)
50.5
(10.9)
749.8
(122.1)
15.3
(4.3)
+
N
0.020
(0.002)
44.0 (1.2)
1.05
(0.16)
0.06
(0.01)
0.79
(0.17)
42.8
(6.5)
762.1
(74.4)
18.0
(2.7)
+
P
0.021
(0.001)
44.0 (1.3)
0.91
(0.25)
0.06
(0.01)
0.75
(0.19)
50.4
(10.1)
689.6
(77.9)
14.4
(4.8)
S C
o
n
0.027
(0.001)
43.6 (1.2)
0.96
(0.16)
0.04
(0.00)
1.10
(0.22)
46.4
(7.5)
1087.8
(90.3)
24.0
(4.6)
+
N
0.027
(0.001)
44.7 (1.7)
1.25
(0.20)
0.04
(0.00)
1.16
(0.20)
36.7
(6.2)
1182.6
(143.4)
32.9
(5.2)
+
P
0.021
(0.001)
44.6 (1.6)
1.02
(0.15)
0.08
(0.01)
0.52
(0.05)
44.4
(5.5)
583.8
(48.4)
13.3
(1.6)
F C
o
n
0.022
(0.001)
47.0 (0.9)
1.12
(0.08)
0.07
(0.01)
0.60
(0.07)
42.1
(2.5)
695.1
(74.0)
16.5
(1.5)
+
N
0.023
(0.001)
46.4 (0.7)
1.15
(0.09)
0.06
(0.01)
0.65
(0.09)
40.6
(3.1)
752.8
(76.7)
18.7
(2.3)
+
P
0.023
(0.001)
47.4 (0.8)
1.09
(0.06)
0.07
(0.00)
0.62
(0.06)
43.6
(2.4)
702.3
(52.8)
16.1
(1.3)
S C
o
n
0.025
(0.002)
46.5 (0.9)
1.14
(0.04)
0.05
(0.01)
0.72
(0.08)
40.8
(1.9)
899.4
(101.9)
21.7
(2.4)
+
N
0.026
(0.002)
47.2 (0.6)
1.41
(0.18)
0.05
(0.00)
0.75
(0.11)
33.9
(4.3)
984.3
(75.5)
29.5
(4.4)
+
P
0.024
(0.001)
47.1 (0.7)
1.02
(0.09)
0.07
(0.01)
0.60
(0.05)
46.7
(3.8)
639.9
(74.1)
13.8
(1.4)
Nested
ANOVA
F
P
F
P
F
P
F
P
F
P
F
P
F
P
F
P
Loc
153
.55
9
0.
00
0
108
.39
1
0.
00
0
20.
64
9
0.
00
0
361
.01
4
0.
00
0
26.
17
8
0.
00
0
16.
66
1
0.
00
0
270
.15
6
0.
00
0
91.
91
3
0.
00
0
Z/Loc
80.
112
0.
00
0
9.7
98
0.
00
0
12.
86
9
0.
00
0
16.
088
0.
00
0
6.8
79
0.
00
0
6.7
25
0.
00
0
42.
239
0.
00
0
34.
67
7
0.
00
0
T/Z/Loc
11.
045
0.
00
0
1.6
34
0.
09
0
6.1
75
0.
00
0
22.
793
0.
00
0
14.
65
9
0.
00
0
4.8
23
0.
00
0
31.
876
0.
00
0
25.
47
6
0.
00
0
*LMA = leaf mass per unit area; C = carbon; N = nitrogen; P = phosphorus; K = potassium
Values are means (± 1SD). F- and P-values for the nested ANOVAs are listed below.
LITERATURE CITED FOR APPENDIX A
Feller, I.C., and A.H. Chamberlain. 2007. Herbivore responses to nutrient enrichment and landscape
heterogeneity in a mangrove ecosystem. Oecologia 153: 607-616.
Feller, I.C., C.E. Lovelock, and C. Piou. 2009. Growth and nutrient conservation in Rhizophora mangle in
response to fertilization
Feller, I.C., K.L. McKee, D.F. Whigham, and J.P. O'Neill. 2003a. Nitrogen vs. phosphorus limitation across
and ecotonal gradient in a mangrove forest. Biogeochemistry 62: 145-175.
Feller, I.C., D.F. Whigham, K.L. McKee, and C.E. Lovelock. 2003b. Nitrogen limitation of growth and
nutrient dynamics in a disturbed mangrove forest, Indian River Lagoon, Florida. Oecologia 134: 405-414.
Lovelock, C.E., I.C. Feller, and K.L. McKee, and R. Thompson. 2005. Forest structure of the extensive
Caribbean mangrove forests of Bocas del Toro, Panama. Caribbean Journal of Science 41: 456-464.
APPENDIX B: Descriptions of the three sites sampled for the effects of nutrient enrichment on
herbivory in mangrove forests along a latitudinal gradient from a warm temperate climate in
central Florida to tropical in Belize and Panamá.
This study was conducted at three locations along the Atlantic and Caribbean coasts from
Florida to Panama (Figure B1). These locations represented a climatic gradient from a warm
temperate climate in central Florida to the tropics in Belize and Panama over more than 2050 km
and 18.4º of latitude at: 1) Indian River Lagoon, Florida; 2) Twin Cays, Belize; 3) Bocas del
Toro, Panama. The three locations were located at sea level and had similar forest structure,
which was characterized by complex gradients in tree height that included a narrow seaward
fringe of pure stands of uniformly tall (5–6 m) R. mangle, varying in width from 5–20 m wide
(Figure B2). Tree height decreased rapidly to landward with interior areas dominated by oldgrowth stands of low stature, or ‘scrub’, (≤1.5 m tall) trees. The black mangrove (Avicennia
germinans L.) and the white mangrove (Laguncularia racemosa (L.) Gaertn. f.) were also
present in each of these locations, primarily near the landward ecotone. The hydrogeomorphic
settings were variable among the three locations (Table B1). IRL and Bocas del Toro were
continental in contrast with Twin Cays, which was an offshore archipelago of small mangrove
cays. However, the mineralogies of Twin Cays and Bocas del Toro were more similar (Phillips
and others 1997; Macintyre and others 2004; Coates and others 2005), with mangrove forests
developing atop carbonate platforms and forming deep peat deposits. All sites were microtidal
with mixed semidiurnal tides (Kjerfve 1982; Kaufman and Thompson 2005). The fringe zones at
the three locations were similarly well-flushed, but the hydrologies of the scrub zones varied. At
IRL, the scrub R. mangle stands drained completely at low tide during the summer, but remained
inundated for days during the winter (Feller and others 2003b). At Twin Cays, many of the scrub
R. mangle stands in the interior portions of the island were waterlogged and perennially flooded
except at unusually low tides (McKee and others 2007). In contrast, the scrub zone at Bocas del
Toro regularly drained completely at low tide (Lovelock and others 2005).
At the IRL, our experimental sites were situated on the lagoon side of two barrier islands. The
fringe site was in Avalon State Park on North Hutchinson Island, St. Lucie County; the scrub site was in
the Hobe Sound National Wildlife Refuge on Jupiter Island, Martin County. These sites were previously
impounded for mosquito control. In this area, soil was composed primarily of sand with mangrove
forests adjacent to coastal strand vegetation and maritime hammocks. Descriptions of forest structure,
hydro-edaphic conditions, growth, nutrient dynamics, and photosynthesis at the Avalon State Park site
were previously reported (Feller and others 2003a; Lovelock and Feller 2003). At Twin Cays, our fringe
and scrub sites were located on the two largest cays in this 92-ha mangrove archipelago. Descriptions of
forest structure, biogeochemistry, ecophysiology, growth, and nutrient dynamics were previously
reported (McKee and others 2002; Feller and others 2003b, 2007; Lovelock and others 2006a,b,c,d).
These offshore islands were underlain by deep mangrove peat 8–12 m thick (Macintyre and others
2004; McKee and others 2007). At Bocas del Toro, fringe and scrub sites were located on three islands
(Isla San Cristobal, Isla Solarte, Isla Popa) in Almirante Bay and the Chiriqui Lagoon in a vast network of
mangrove islands and mainland peninsulas covering approximately 2885 km2 (D’Croz 1993; Guzman and
others 2005; Lovelock and others 2004, 2005). Here, mangroves occurred adjacent to tropical
rainforests and grew on peat about 5 m deep over ancient coral reef limestone (Phillips and Bustin 1996;
Phillips and others 1994, 1997). Bocas del Toro was outside the hurricane belt, but flooding was
common. Episodic earthquakes were the major non-anthropogenic disturbance regime influencing these
forests.
LITERATURE CITED FOR APPENDIX B
Coates, A.G., D.F. McNeill, M.P. Aubry, W.A. Berggren, and L.S. Collins. 2005. An
introduction to the geology of the Bocas del Toro Archipelago, Panama. Caribbean Journal of
Science 41: 374-391.
D’Croz, L. 1993. Status and uses of mangroves in the Republic of Panama. Pp. 115-127 in
Technical report of the project conservation and sustainable utilization of mangrove forests in
Latin America and Africa regions. Part 1. Latin America. L.D. de Lacerda (Ed.). International
Society for Mangrove Ecosystems and International Tropical Timber Organization.
Feller, I.C., K.L. McKee, D.F. Whigham, and J.P. O'Neill. 2003a. Nitrogen vs. phosphorus limitation across
and ecotonal gradient in a mangrove forest. Biogeochemistry 62: 145-175.
Feller, I.C., D.F. Whigham, K.L. McKee, and C.E. Lovelock. 2003b. Nitrogen limitation of growth and
nutrient dynamics in a disturbed mangrove forest, Indian River Lagoon, Florida. Oecologia 134: 405-414.
Feller I.C., C.E. Lovelock, and K.L. McKee. 2007 Nutrient addition differentially affects ecological
processes of Avicennia germinans in nitrogen vs. phosphorus limited mangrove ecosystems. Ecosystems
10: 347-359.
Guzman, H.M., P.A.G. Barnes, C.E. Lovelock, and I.C. Feller. 2005. CARICOMP mangrove, seagrass and
coral reef sites in Bocas del Toro, Panama. Caribbean Journal of Science 41: 430-440.
Kaufman, K.W. and R.C. Thompson. 2005. Water temperature variation and the meteorological
and hydrographic environment of Bocas del Toro, Panama. Caribbean Journal of Science 41:
392-413.
Kjerfve, B. 1982. Water exchange across the reef crest at Carrie Bow Cay, Belize. Smithsonian
Contributions to Marine Science 12: 59-62.
Lovelock, C.E. and I.C. Feller. 2003. Photosynthetic performance and resource utilization of two
mangrove species coexisting in hypersaline scrub forest. Oecologia 134: 455-462.
Lovelock, C.E., I.C. Feller, K.L. McKee, B.M.J. Engelbrecht, and M.C. Ball. 2004. The effect of
nutrient enrichment on growth, photosynthesis and hydraulic conductance of dwarf mangroves in
Panama. Functional Ecology 18: 25-33.
Lovelock, C.E., I.C. Feller, and K.L. McKee, and R. Thompson. 2005. Forest structure of the
extensive Caribbean mangrove forests of Bocas del Toro, Panama. Caribbean Journal of Science
41: 456-464.
Lovelock, C.E., M.C. Ball, B. Choat, B.M.J. Engelbrecht, N.M. Holbrook, and I.C. Feller.
2006a. Linking physiological processes with mangrove forest structure: phosphorus deficiency
limits canopy development, hydraulic conductivity and photosynthetic carbon gain in dwarf
Rhizophora mangle. Plant, Cell and Environment 29: 793-802.
Lovelock, C.E., M.C. Ball, I.C. Feller, B.M.J. Engelbrecht, and M.L. Ewe. 2006b. Variation in
hydraulic conductivity of mangroves: Influence of species, salinity, and nitrogen and phosphorus
availability. Physiologia Plantarum 127: 457- 464.
Lovelock, C.E., I.C. Feller, M.C. Ball, B.M.J. Engelbrecht, and M.L. Ewe. 2006c. Differences in
plant function in phosphorus and nitrogen limited mangrove ecosystems. New Phytologist 172:
514-522.
Lovelock, C.E., R.W. Ruess, and I.C. Feller. 2006d. Fine root respiration in the mangrove
Rhizophora mangle over variation in forest stature and nutrient availability. Tree Physiology
26:1601–1606.
Macintyre, I.G., M.A. Toscano, and G.B. Bond. 2004. Modern sedimentary environments, Twin
Cays, Belize, Central America. Atoll Research Bulletin 509: 1-12.
McKee, K.L. I.C. Feller, M. Popp, and W. Wanek. 2002. Mangrove isotopic fractionation (δ15N
and δ13C) across a nitrogen versus phosphorus limitation gradient. Ecology 83: 1065-1075.
McKee, K.L, D. Cahoon, and I.C. Feller. 2007. Caribbean mangroves adjust to rising sea-level
through biotic controls on soil elevation change. Global Ecology and Biogeography 16: 546-556.
Phillips S. and R.M. Bustin. 1996. Sedimentology of the Changuinola peat deposit: Organic and clastic
sedimentary response to punctuated coastal subsidence. Geological Society of America Bulletin 108:
794-814.
Phillips S., R.M. Bustin, and L.E. Lowe. 1994. Earthquake induced flooding of a tropical coastal peat
swamp: A modern analogue for high-sulfur coals? Geology 22: 929-932.
Phillips S., G.E. Rouse, and R.M. Bustin. 1997. Vegetation zones and diagnostic pollen profiles of a
coastal peat swamp, Bocas del Toro, Panama. Paleogeography, Paleoclimatology, Paleoecology 128:
301-338.