The Auk 121(2):548–556, 2004
SAP-FEEDING BEHAVIOR AND TREE SELECTION IN THE ENDANGERED AKIAPOLAAU (HEMIGNATHUS MUNROI) IN HAWAII L P 1,3 J J2 2
1 Department of Environmental Studies, University of California, Santa Cruz, California 95064, USA; and U.S. Fish and Wildlife Service, Hakalau Forest National Wildlife Refuge, 32 Kinoole Street, Suite 101, Hilo, Hawaii 96720, USA
A .—The Akiapolaau (Hemignathus munroi), an endangered Hawaiian honeycreeper, drills 3–5 mm deep holes in particular ohia trees (Metrosideros polymorpha) and drinks the sap that emerges, a remarkable example of convergent evolution in sap-feeding behavior with mainland woodpeckers and Australian sugar-gliders. There has been lile research on how this species selects sap trees (“Aki trees”) and what advantages they confer. We marked the locations of and collected sap samples and microhabitat data from 101 Aki trees and 73 randomly selected control trees in Hakalau Forest National Wildlife Refuge, Hawaii. Aki trees were rare (2 ha–1), spatially clustered, and defended by Akiapolaau. Sap flow volume and speed were substantially greater in Aki trees than in controls. Aki trees also were larger, had thinner bark, and were more likely to be located on convex east-facing slopes where more light is available. Those results support the hypothesis that Aki trees are selected on the basis of high sap flow and a suite of unique microhabitat and tree characteristics. Sap may be an important energy source in times of low insect availability and a potent alternative to nectar for the Akiapolaau. Aki trees are both a fascinating example of niche specialization and a factor that should be considered when conserving or restoring habitat for this endangered species. Received 7 June 2003, accepted 27 January 2004. R .—Hemignathus munroi es una especie amenazada de mielero de Hawai que perfora agujeros de 3–5 mm de profundidad en determinados árboles de Metrosideros polymorpha y bebe la savia que emerge, lo que representa un ejemplo destacable de evolución convergente en el comportamiento de alimentación con savia con los carpinteros del continente y con Petaurus breviceps, un marsupial planeador australiano. Ha habido poca investigación sobre cómo esta especie selecciona los árboles productores de savia y qué ventajas le confieren éstos. Marcamos las localizaciones y colectamos muestras de savia y datos micro-ambientales de 101 árboles de M. polymorpha y de 73 árboles control elegidos al azar en el Refugio Nacional de Vida Silvestre Hakalau Forest, Hawai. Los árboles de M. polymorpha fueron raros (2 ha–1), estuvieron espacialmente agrupados y se encontraron defendidos por H. munroi. El volumen y la velocidad del flujo de savia fueron substancialmente mayores en los árboles de M. polymorpha que en los controles. Los árboles de M. polymorpha fueron más grandes, presentaron cortezas más delgadas y tuvieron mayor probabilidad de ser localizados en laderas convexas orientadas hacia el este, donde hay más luz disponible. Estos resultados apoyan la hipótesis de que los árboles de M. polymorpha son seleccionados sobre la base de un alto flujo de savia y un conjunto único de características micro-ambientales y de los árboles. La savia puede ser una fuente importante de energía durante períodos de baja disponibilidad de insectos y una alternativa substancial del néctar para H. munroi. Los árboles de M. polymorpha son un ejemplo fascinante de especialización de nicho y un factor que debe ser considerado a la hora de conservar o restaurar ambientes para esta especie amenazada.
T (D ) of the Hawaiian Archipelago are a classic example of adaptive radiation and convergent evolution. Several original colonizers gave rise to >50 species by evolving the remarkable behavioral and
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morphological diversity that enabled them to exploit novel food resources (Freed et al. 1987, James and Olson 1991). One of the most spectacular examples of niche specialization is the Akiapolaau (Hemignathus munroi), which fills a woodpecker-like niche on the island of Hawaii (Ralph and Fancy 1996). Akiapolaaus drink sap from particular trees, a foraging behavior that is
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convergent with other sap feeders, such as the Yellow-bellied Sapsucker (Syphyrapicus varius) and the yellow-bellied glider (Petaurus australis), a marsupial (Eberhardt 2000, Goldingay 2000). Akiapolaau sap-feeding behavior has been described (Pra et al. 2001); but there has been lile research on how Akiapolaaus select sap trees, how that behavior compares to mainland sap-feeding species, and what advantage trees confer. Akiapolaaus have a long, flexible, strongly decurved upper bill and a short, sharp lower mandible (Fig. 1). This bill allows them to drill holes in trees using the stout lower mandible and then use the slender upper bill as a hook or probe. Akiapolaaus forage primarily for lepidopteran and cerambicid larvae under the bark surface of koa (Acacia koa). They are one of the few honeycreepers in Hawaii that do not regularly drink nectar. Perhaps as an alternative to nectar, Akiapolaaus feed on ohia (Metrosideros polymorpha) sap year-round by drilling 3-mm deep holes through the bark and into the phloem (Fig. 1). They gather sap by tilting back the head, inserting the bill partway into the hole, and collecting sap with the tongue. Whereas other sap-feeding species, such as Yellowbellied Sapsuckers, exploit multiple species of trees (Kilham 1964), Akiapolaaus drink phloem sap only from ohia. Phloem sap of all trees is composed primarily of sucrose (Snyder 1992). The sap is well protected from herbivores by a thick layer of bark, and by an injury-induced response that releases proteins to prevent continued bleeding from injured sieve tubes (Cras and Crisp 1971, Flowers and Yeo 1992). The few organisms that are able to overcome those defenses and exploit the resource choose their target trees selectively (Eberhardt 2000). Sap-feeding species presumably forage on particular trees because they provide more sap (Goldingay 1991), have higher quality sap (more sugar, proteins, and minerals) (Foster and Tate 1966, Snyder 1992), or because the sap is more accessible. Individual tree characteristics, such as bark thickness (Mackowski 1988), microhabitat variables (Rohrbaugh and Rice 1949, Har 1967, Cras and Crisp 1971, Lambers et al. 1998), genetic variation in sap content (Crawley 1983), and the presence of secondary chemicals, could all influence how available the sap is to the animal (Snyder
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F . 1. A male Akiapolaau drilling for phloem sap on an Aki tree. Note that the bird is drilling with the stout lower mandible, while holding the upper bill out of the way, and that it has drilled some holes in roughly horizontal rows on the trunk.
1992). Although factors determining sap-tree selection remain poorly understood, previous research on sap-feeding species suggests that multiple mechanisms influence sap flow and content and affect tree choice by the organism (Goldingay 1987). Research on yellow-bellied gliders, which feed by making incisions in particular Eucalyptus species and licking the exudate, has shown that gliders choose sap trees based on higher sap flow, smoother bark, and larger size (Goldingay 1987, Mackowski 1988, Goldingay 1991). Kilham (1964) and Eberhardt (2000) concluded that Yellow-bellied Sapsuckers select trees for individual characteristics such as poor health. Snyder (1992) found that Abert’s squirrels (Sciurus aberti) select particular ponderosa pines (Pinus ponderosa) as sap trees on the basis of significantly higher levels of sugars and lower concentrations of deleterious compounds.
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Although Akiapolaaus share that sap-feeding niche, it is not clear that they are receiving the same benefits and that the mechanisms for tree selection are the same. It is particularly important to understand sap feeding in Akiapolaaus, because they are an endangered species with an estimated total population of 1,200 individuals (Fancy et al. 1996). The decline of the Akiapolaau can be aributed to habitat loss, effects of introduced predators and disease, and some unique life-history characteristics, including a low reproductive rate (Banko and Williams 1993), long parental care period, large home ranges, and a unique foraging ecology (Pra et al. 2001). Because invertebrate prey populations may be seasonally unreliable, and this species does not feed regularly on nectar, drinking sap may provide an important year-round supplementary food source. Describing sap-feeding behavior and determining how and why Akiapolaaus choose particular ohia trees (“Aki trees”), therefore, not only will contribute to understanding the ecology and evolution of this unique dietary niche, but also has conservation relevance. We measured microhabitat and individual characteristics of Aki trees and control trees to test the following hypotheses about factors influencing sap-tree selection in the Akiapolaau: (1) Availability: sap flows more readily in Aki trees than in control trees, and thinner bark allows easier access to sap. (2) Quality: Aki sap has a higher percentage of sucrose and a different composition of compounds than other ohia, perhaps providing a higher quality food source with fewer harmful secondary chemicals. (3) Microhabitat and tree characteristics: Aki trees are larger (more leaf surface area for photosynthesis) and are located in areas where more light and moisture are available. (4) Density and distribution: Aki trees are rare and nonrandomly distributed over the landscape. S A M Study area.—The study was conducted in mesic rainforest at 2,000 m in Hakalau Forest National Wildlife Refuge (HFNWR) on the island of Hawaii (19’50’N, 155’20’W). Aki trees (n = 101) and control trees (n = 73) are located in the Pua Akala and Nauhi tracts of HFNWR. Those sites are ∼6 km apart and consist of mature koa-ohia forest recovering from a history of cale grazing and disturbance from other feral ungulates. Those sites receive ∼2,000 mm of rain annually (Hart and Freed 2003). Each study area is defined by
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the home ranges of 10 Akiapolaau family groups as part of a larger project on Akiapolaau habitat selection and population biology. Aki trees were identified during three field seasons: July–September 2000, April– August 2001, and April–October 2002. Measurements and samples for Aki trees and controls were collected in October 2002 when sufficient Aki trees had been located. There is no reason to believe that that resource is strongly seasonal, because ohia is a tropical evergreen species, and Akiapolaaus have been observed foraging on Aki trees throughout the year. Identifying Aki trees and controls.—Aki trees were located either by following Akiapolaaus or by randomly scanning ohia. All birds from the study population were followed weekly and would occasionally lead the observer to a new Aki tree. When searching for Akiapolaaus or moving through the study sites for any purpose, we systematically scanned ohia for sap holes. Each newly discovered Aki tree was flagged, and universal transverse mercator (UTM) coordinates were recorded using a Garmin 12 global positioning system (Garmin, Olathe, Kansas). Control trees were selected using a grid of vegetation plots that were 20 m in diameter and evenly spaced every 100 m throughout the study sites. Number of Aki trees and control trees in the study are not equal because of the limited number of vegetation plots (n = 73). The closest live ohia tree to the center of each plot that was >10 cm in diameter and did not have Aki holes was chosen as a control. Because we knew a priori that all Aki trees in the study were canopy trees, a minimum diameter of 10 cm was used to avoid choosing ohia saplings, which would be subject to very different light conditions. Minimum diameter of controls was not larger than 10 cm because we wanted to test if the diameter of Aki trees was different from the average diameter of all available ohia. Measuring sap flow and sap content.—To mimic Akiapolaau foraging techniques, we collected sap from Aki trees and controls using a hammer and a nail approximately the same diameter as the bird’s lower mandible. We measured sap flow volume by making 10 holes 0.5–2 m above the ground on each tree and collecting all the sap that emerged with glass capillary tubes (flow generally ebbed within 5 min). We blew the sap into plastic containers, measured total volume collected from each tree, and froze the samples for later analysis. Some sap samples (n = 12) were analyzed in April 2003 for relative composition of compounds in Aki trees and controls using high-performance liquid chromatography (HPLC). Sap was dissolved in 5 mg mL–1 of MeOH and injected on a reverse phase analytical “C-18” column in a 10:90 (acetonitrile:water ratio) solvent >50 min using a Waters 996 photo diode array UV detector (Waters Corporation, Milford, Massachuses). On a subset of Aki trees and controls (n = 47), we drilled one additional hole to measure solute (principally sucrose) concentration using a handheld light refractometer (Southwick and Southwick
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1980). Sample sizes for the HPLC and refractometer analyses were limited, because relatively few control ohia gave sufficient sap. Sap flow speed was measured as latency to first sap flow rather than flow rate. Before sampling from Aki trees, we also recorded whether there were previous Akiapolaau holes where we were sampling, at what height the holes began, and the extent and density of holes (high = holes densely covering the majority of tree surface area, medium = holes covering about half of tree surface, low = holes present on a small fraction of tree surface and diffuse). Time of day, cloud cover, and precipitation are known to effect photosynthesis and sap flow (Lambers et al. 1998). It was not logistically possible to sample all Aki trees and controls at the same time of day and under the same environmental conditions. To minimize the effect, however, we sampled trees only between 0900 and 1700 h; we never sampled during rainfall. Time of day and cloud cover did not significantly affect sap flow in the study (time: χ2 = 3.34, df = 2, P = 0.19; cloud cover: χ2 = 1.47, df = 3, P = 0.69). Microhabitat and tree characteristics.—We measured the following microhabitat and tree characteristics: aspect, terrain shape index (TSI), diameter at breast height (DBH), height, bark thickness, trunk straightness, forking, and number of trunks. Aspect and TSI are measures of the amount of sunlight and moisture available to the tree. Aspect was recorded using a compass, and TSI was measured by averaging the slopes from the focal tree to a point 10 m in each cardinal direction. Terrain shape index is a quantitative expression of the geometric shape of the land surface, indicating whether the tree is on convex (–), linear (0), or concave (+) terrain. The TSI may influence sap flow, because land surface geometry affects the moisture and light available to the tree (McNab 1989). Although soil characteristics, including soil moisture, certainly could influence sap flow, we did not sample soil, because it is likely to be relatively homogeneous throughout the site (all trees are on the same-age lava flow). In addition, soil moisture is influenced by precipitation, which is variable over time and space. Given the number of trees and the size and terrain of the study area, it would not have been possible to sample all trees on the same day and under the same weather conditions. Diameter at breast height and height are generally indicative of total canopy cover (surface area available for photosynthesis) and influence the hydrostatic gradient and rate of sap unloading at sinks, such as Akiapolaau drill holes (Cras and Crisp 1971, Mueller-Dombois and Ellenberg 1974). The DBH was measured at 1.3 m and height was measured using a clinometer. Thinner, smoother bark has been associated with sap-tree selection in other taxa, probably because it allows the organism easier access to phloem (Mackowski 1988). We visually scanned each tree and
assigned it a bark thickness category of “smooth” (bark uniformly 15 mm thick). The overall architecture of the tree (i.e. trunk straightness, forking, and number of trunks) may also affect sap flow. We recorded that the tree was straight unless it was leaning 20° or more in any direction. We recorded number of trunks and whether the tree forked below 10 m. Data analysis—We used chi-square to test for differences between Aki trees and controls for the categorical variables—aspect, bark thickness, straightness, forking, and number of trunks. For the continuous variables— sap flow, sap speed, TSI, DBH, and height—we used either ANOVA or t-tests, depending on the number of treatment levels. We also tested for a relationship between sap flow in Aki trees and denseness of holes on the tree, and between sap flow and presence or absence of holes where we collected the sap sample. When assumptions of parametric statistics could not be met, data were analyzed using the Wilcoxon twosample test and the Kruskall-Wallis test for multiple levels of independent variables (Zar 1999). Stepwise logistic regression and the log-likelihood ratio were used to determine how well Aki trees and controls can be predicted given the microhabitat and tree characteristic variables that we measured. Status as an Aki tree or control was the response variable; aspect, TSI, DBH, bark thickness, straightness, forking, and number of trunks were the independent terms in the model (height was excluded because it is correlated with DBH). We used multiple regression to determine if any variables influence relative sap flow among Aki trees. Sap flow was the dependent variable; hole denseness and hole presence or absence at sampling location were included as explanatory variables, along with the same microhabitat and tree characteristic variables discussed above. We determined Aki tree density and distribution by creating minimum convex polygons and using the nearest-neighbor method in ARCVIEW 3.2 (Environmental System Research Institute, Redlands, California) (Krebs 1989).
R Sap flow.—Aki trees produced substantially more sap (Z = –0.22, df = 1, P < 0.0001) and produced sap faster (Z = 2.14, df = 1, P = 0.03) than control ohia (Fig. 2). About 86% of Aki trees gave sap; only 20% of controls gave sap. Nearly 11% of Aki trees gave >1 mL of sap per 10 holes, in contrast to 0% in controls (Table 1). All sap holes, both artificially and birdmade, stopped producing sap within 5 min of drilling. Volume of sap produced from Aki trees was associated with denseness and ex-
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T
1. Percentage of Aki trees and control trees that produced sap, categorized by sap volume. Volume of sap flow (mL) 0 0.01–0.1 0.11–1.0 >1.0
Aki trees (n = 101) 13.9% (14) 28.7% (29) 46.5% (47) 10.9% (11)
Controls (n = 73) 79.4% (58) 19.2% (14) 1.4% (1) 0% (0)
T
2. Lowest height of previously drilled Akiapolaau holes on Aki trees.
F . 2. Average volume of sap (± SE) produced from Aki trees (n = 101) and control trees (n = 73).
tent of Akiapolaau holes on the tree (χ2 = 7.34, df = 2, P = 0.03). Trees with densely spaced holes covering most of the tree surface gave more sap than either medium- or low-density trees (Z = 2.47, df = 1, P = 0.01). High-density trees also had significantly smoother bark (χ2 = 18.98, df = 1, P < 0.0001). Presence or absence of Akiapolaau holes where samples were collected was associated with amount of sap produced (Z = –2.34, df = 1, P = 0.02). On nearly 50% of trees, Akiapolaau-drilled holes started below 1 m on the trunk. On all other trees, Akiapolaau holes were too high on the trunk and we could not get to those locations for sap sampling (Table 2). None of the microhabitat or tree-characteristic variables significantly explained sap flow volume among Aki trees in the multiple regression model (R2 = 0.06, P > 0.05 in all cases). Sap content.—Mean solute (primarily sucrose) concentration was 15.12% in all ohia sampled (range = 13.2–17.6, n = 47). There was no difference in solute concentration between Aki trees and controls (t = 0.62, df = 46, P = 0.5416). Highperformance liquid chromatography analysis of equal numbers of sap samples from Aki trees and controls (n = 12) showed a total of 13 compounds in ohia phloem sap. Eight of those compounds were found in both Aki trees and controls; the other five compounds were found only in control trees. Those five compounds found only in control trees were rare, but each was in at least two different samples. It was not possible to isolate and identify those compounds, because of funding constraints and the relatively small volume of sap samples. Microhabitat and tree characteristics.—Aspect,
Height of lowest holes (m) 0–1 1–4 5–9 10–14 15–18
Aki trees (%) (n = 101) 46.5 15.8 15.8 10.9 10.9
TSI, DBH, height, and bark thickness were all strongly significant factors for Aki tree selection (Table 3). Aki trees were more likely to be found on east-facing slopes, and controls were more oen found on south-facing slopes (χ2 = 6.46, df = 2, P = 0.04). No trees in the study were on west-facing slopes, because both sites are on the eastern flank of Mauna Kea volcano. Aki trees had a more negative TSI than control trees, which indicates that they are more likely to be found on convex land surfaces (t = –2.71, df = 173, P = 0.0075). Aki trees had larger diameters (DBH: Z = –3.99, df = 1, P < 0.0001) and were taller (height: t = 7.15, df = 172, P < 0.0001); however, those two variables are closely correlated (P < 0.0001). Sixty-one percent of Aki trees had smooth bark, in contrast to 11% of controls (χ2 = 66.80, df = 2, P < 0.0001). Tree architecture variables were not significantly different in Aki trees and controls (straightness: χ2 = 1.19, df = 1, P = 0.28; forking: χ2 = 0.16, df = 1, P = 0.69; number of trunks: χ2 = 2.52, df = 1, P = 0.11) (Table 3). Stepwise logistic regression demonstrated that four of the significant variables (TSI, DBH, aspect, and bark thickness) were reasonably good predictors for determining whether a particular ohia was an Aki tree or a control (χ2 = 104.03, df = 4, P < 0.0001). The logistic model correctly predicted Aki trees 85.9% of the time and controls 76.1% of the time (Table 4). Density and distribution.—We found 103 Aki trees during 3,600 h of fieldwork in the study
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3. Microhabitat and tree characteristics of Aki trees and control trees.
Variable Aspect (%) North East South TSI (0 = level surface) DBH (cm) Height (m) Bark thickness (%) Smooth Medium Rough Straight trunk (%) Forking (%) Trunks (% with one)
Aki tree Mean ± SE (n = 101)
Control Mean ± SE (n = 73)
13 81 6 –0.030 ± 0.008 52.11 ± 1.89 23.1 ± 0.4
13.9 68.1 18.1 –0.001 ± 0.010 42.62 ± 3.04 18.2 ± 0.6
60.8 39.2 0.0 89.2 57.8 88.2
11.0 50.7 38.4 83.6 54.8 79.5
P 0.04
0.0075
