DOI: 10.5061/dryad.m37pvmd34
title: Data from: Insectivorous birds reduce herbivory but do not increase mangrove growth across productivity zones

description: Top-down effects of predators and bottom-up effects of resources are
 important drivers of community structure and function in a wide array of
 ecosystems. Fertilization experiments impose variation in resource
 availability that can mediate the strength of predator impacts, but the
 prevalence of such interactions across natural productivity gradients is
 less clear. We studied the joint impacts of top-down and bottom-up factors
 in a tropical mangrove forest system, leveraging fine-grained patchiness
 in resource availability and primary productivity on coastal cays of
 Belize. We excluded birds from canopies of red mangrove (Rhizophoraceae:
 Rhizophora mangle) for 13 months in zones of phosphorus-limited, stunted
 dwarf mangroves, and in adjacent zones of vigorous mangroves that receive
 detrital subsidies. Birds decreased total arthropod densities by 62%,
 herbivore densities more than fivefold, and reduced rates of leaf and bud
 herbivory by 45% and 52%, respectively. Despite similar arthropod
 densities across both zones of productivity, leaf and bud damage were 2
 and 4.3 times greater in productive stands. Detrital subsidies strongly
 impacted a suite of plant traits in productive stands, potentially making
 leaves more nutritious and vulnerable to damage. Despite consistently
 strong impacts on herbivory, we did not detect top-down forcing that
 impacted mangrove growth, which was similar with and without birds. Our
 results indicated that both top-down and bottom-up forces drive arthropod
 community dynamics, but attenuation at the plant-herbivore interface
 weakens top-down control by avian insectivores.
description: We established our field experiment on Twin Cays, Belize (16.82°
 N, 88.10° W), a 92-ha archipelago of peat-based mangrove islands,
 approximately 12 km from the mainland. Island vegetation is dominated by
 mangroves, the majority of which are <em>Rhizophora
 mangle</em>. Black mangroves (<em>Avicennia germinans
 </em>(L.)) are locally common in some areas, while white mangroves
 (<em>Laguncularia racemosa</em> (L.) C.F. Gaertn.) are
 scattered and relatively rare. A narrow 5-20m band of large, productive
 <em>R. mangle</em> trees (5-6m tall) lines the island
 perimeters, while interior ponds are inhabited by old-growth stands of
 dwarf <em>R. mangle</em> (&lt;1.5m tall) that are
 short-statured primarily due to phosphorus (P) limitation.
 Two main islands (“West island” and “East island”) constitute
 most of Twin Cays’ landmass, and we established one study site on each of
 these islands ("Dock" and "Boa" respectively). Site
 locations were chosen based on accessibility and on the co-occurrence of
 fast-growing floc-associated R. mangle on pond edges and dwarf
 <em>R. mangle</em> within ponds. The two sites we selected
 were approximately 0.7km apart and differed somewhat in their hydrological
 conditions and spatial patterns of floc deposits.
 Experimental design Experimental manipulations
 were established 7-12 January 2010. At each of two sites, we selected 20
 experimental units: 10 <em>R. mangle</em> dwarf trees (low
 resource treatment) and 10 branches on different <em>R.
 mangle</em> trees near flocculent organic deposits (high resource
 treatment, hereafter “floc trees”). Vigorous floc trees were much larger
 than the dwarf <em>R. mangle</em> in interior ponds.
 Therefore, we manipulated only portions of the floc trees of similar size
 to dwarfs, in order to standardize the size of our experimental units. We
 built 1-m3 frames of ¾” PVC around each experimental unit and randomly
 selected half of the frames around dwarfs and floc trees to be covered in
 polypropylene netting (2x2cm openings; Dalen Deer-X netting) to exclude
 vertebrates but not arthropods. Thus, each combination of resource
 treatment (floc vs. dwarf tree) by bird access treatment (no net vs. net)
 had a total replication of n=10 (5 per site). Nets did not extend
 underwater to the sediment surface, rather they stopped at the height of
 high tide so that they allowed floating detritus movement but not bird
 access. Experimental units were chosen so that they were all at least 5m
 apart, had 10-20 terminal shoots and could be oriented within frames so
 that they would not contact net coverings. Three terminal stems were
 haphazardly chosen on each experimental unit and marked with aluminum
 tags. These stems were later used to quantify plant growth and rates of
 herbivory (see below). Nets and frames were checked and repaired if needed
 at 2, 4, and 8 months after initiation of treatments. After 13 months
 (10-16 February 2011), we measured all final response variables.
 Measurements of flocculent detritus The depth
 of the floc near the base of each experimental unit was measured
 repeatedly; once at the start of the experiment and again after 2, 4, and
 8 months. At each time point, an extending ruler was used to measure the
 depth of floc at five locations within the base of each frame. All floc
 depth measures were averaged to create a single floc depth value for each
 tree. At four sites (two on each island) where
 accumulations of floc were present and associated with bands of rapidly
 growing <em>R. mangle</em>, we collected three floc samples
 and three substrate (i.e., mostly peat) samples. Floc samples were
 collected every 5m along a pond edge where floc was accumulating, and peat
 was collected 10m toward the pond’s interior from each floc sample (where
 only trace amounts of floc were present). Substrate %P by mass was
 determined by placing a known mass (~2 mg) of dried, ground material in a
 muffle furnace at 550°C for two hours, followed by colorimetric analysis
 using the ammonium molybdate method. Assessing growth
 and plant traits We assessed the growth of experimental
 units throughout the experiment by quantifying the length and number of
 leaves present on three marked twigs, as well as recording the total
 number of live terminal stems present. As marked twigs branched, we summed
 the lengths of all shoots and shoot segments distal to a marked point to
 calculate length values. Measurements of total twig length and overall
 terminal shoot abundance were taken 0, 2, 4, 8, and 13 months after
 treatments were imposed, while twig leaf abundance was measured 2, 4, 8,
 and 13 months after treatments were imposed. To create a single value
 summarizing the rate of change in each of these variables, we subtracted
 the last collected measure from the earliest collected measure for each
 variable and then divided these differences by the number of months that
 elapsed between them. Data collection errors led 3/120 marked twigs to
 have earliest measures later than the start of the experiment while twig
 death led to 6/120 marked twigs to have their latest measures before the
 end of the experiment (three of these were on an experimental unit that
 died between months 8 and 13). After means for each experimental unit were
 calculated for marked twig values, we performed a principal components
 analysis (PCA) on the three growth rate variables, first centered and
 scaled to unit variance, to create a synthetic variable representing the
 overall growth of each plant (PCA axis 1). The first PCA axis captured
 87.9% of the total variance in the growth-related measurements, and
 loadings were similar across measured variables (0.54-0.6).
 To assess the toughness and nutrient content of leaves on our
 manipulated trees, we collected three leaves from different terminal stems
 which were growing in full sun and members of the newest fully expanded
 pair of leaves on each stem. We used a Wagner FT penetrometer (Wagner
 Instruments) to measure the amount of force required to punch through each
 leaf. The penetrometer was pushed through the leaf at the midpoint between
 a leaf edge and the midrib halfway down the length of the leaf. The leaves
 were oven-dried at 60°C until constant weight and then the three leaves
 from each plant were separately ground and homogenized. Leaf %P was
 determined using the protocol outlined above for substrate samples. We
 measured leaf %C and %N by packing tin cups with known masses of dried
 ground leaf material (~4mg) and using a Flash EA series 1112 NC soils
 analyzer. Internal lab standards measured along with experimental leaf
 samples were used to confirm the validity of nutrient analyses.
 To quantify leaf morphology (leaf mass per area, or LMA), we
 collected single leaves from experimental units at the East island site
 only, due to logistical constraints. The leaves were growing in full sun
 and were part of the newest fully expanded pair of leaves on a terminal
 stem. We took digital photographs of each leaf, used ImageJ v.1.49 to
 measure their surface area, oven dried the leaves to constant mass at 60°C
 and measured leaf biomass using an electronic balance. We subsequently
 calculated LMA by dividing leaf biomass by dry leaf area
 (mg/cm2). Quantifying arthropod density and
 herbivory At the experiment’s end, we exhaustively
 searched each experimental unit, collected all arthropods that were
 discovered using handheld aspirators, and identified them to order. Half
 of the foliage and branches on each plant/branch were clipped into plastic
 bags and searched in the lab while the remaining plant parts were searched
 in the field. The number of terminal shoots on the branches collected from
 each plant were noted and their dry mass was measured to quantify the
 relationship between biomass and terminal shoot abundance. One floc-tree
 experimental unit was damaged in a storm and died between months 8 and 11
 of the experiment, so this replicate, to which birds had access, did not
 contribute to the arthropod and herbivory datasets. To
 quantify herbivory rates on leaves, one of the newest fully expanded
 leaves and one of the oldest fully expanded leaves from each of the three
 marked stems on all experimental units were digitally photographed. We
 used ImageJ v.1.49 to measure the area of each leaf that had been damaged
 by herbivores and averaged the percent damage values for the six leaves
 from each tree. Leaf lifespan in <em>R. mangle</em> is
 approximately 18 months, thus the oldest leaves on each stem likely
 originated before the start of our experiment and were exposed to the
 entire duration of our experiment treatments. The young leaves that we
 sampled, on the other hand, likely originated during our experimental
 treatments and were exposed to varying durations of our bird access
 treatments. Both young and old leaves were included in our measurements of
 herbivory, despite the possibility that old leaves may have been damaged
 before the experiment began, because the dominant folivore of <em>R.
 mangle</em>, <em>Aratus pisonii</em>, preferentially
 feeds on older leaves. To quantify rates of herbivory
 on buds, we counted the number of buds with herbivore damage on each
 experimental unit as well as the number of leaf pairs in which both leaves
 were symmetrically damaged and/or deformed, indicating the damage occurred
 when they were rolled within a bud. We summed the number of damaged buds
 and symmetrically damaged leaf pairs as an index of bud herbivory. Dead
 buds were not counted as “damaged” if cause of death could not be
 determined. All statistical analyses were performed in
 R v. 3.2.3.
description: Please refer to ReadMe file.