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Seed Chemistry of Sophora chrysophylla (Mamane) in Relation to Diet of Specialist Avian Seed Predator Loxioides bailleui (Palila) in Hawaii

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Abstract

This study describes the chemical ecology of a tritrophic interaction among species endemic to the island of Hawaii, USA: a tree (Sophora chrysophylla: mamane), an endangered bird (Loxioides bailleui; palila), and moth larvae (Cydia spp.). Palila and Cydia both specialize on the seed embryos of mamane but avoid eating the seed coats. Palila actively seek out and feed mamane embryos and Cydia larvae to their nestlings. Because mamane embryos contain potentially toxic levels of alkaloids, including broadly toxic quinolizidine alkaloids, and because insects often sequester alkaloids from their food plants, we focus on the questions of why palila forage upon mamane embryos and why they supplement their diet with Cydia larvae. Our data show that mamane embryos contain high amounts of potentially toxic alkaloids, but are well balanced nutritionally and contain lipids, carbohydrates, proteins, amino acids, and minerals at levels that are likely to be sufficient for maintenance and breeding. Mamane seed coats contain lower levels of alkaloids and nutrients, somewhat higher levels of phenolics, and much higher levels of nondigestible fiber. Taken together, these results suggest that palila have evolved tolerance to high levels of alkaloids and that they forage upon embryos primarily because of their availability in the habitat and high nutritional reward. Our data also suggest that Cydia are used by palila because they are readily accessible, nontoxic, and nutritious; the larvae apparently do not sequester alkaloids while feeding upon mamane seeds. Our results are interpreted with respect to the likelihood of current and historical coadaptive responses in this ecologically isolated and simplified island setting.
... One surviving species is the palila (Loxioides bailleui). Palila are a species of finch-billed Hawaiian honeycreeper specializing in seed-eating (Banko et al., 2002b), predominately mamane (Sophora chrysophylla) seed pods (Banko et al., 2002a). ...
... Palila currently live in upland dry forest dominated by mamane (Sophora chrysophylla) and naio (Myoporum sandwicense) trees above the inversion layer where the climate is cool and dry (Press et al. 2006). Mamane trees are an important food for palila and for their native invertebrate prey (Banko et al., 2002a(Banko et al., , 2002b. Palila consume the flowers, buds, young leaves, and immature seeds from within pods. ...
... Palila consume the flowers, buds, young leaves, and immature seeds from within pods. Palila also consume the moth larvae of Cydia spp., Scotorythra (Geometridae) and Uresephita polygonalis virescens (Butler) [Crambidae] (Banko et al., 2002a). Cydia spp. the most important invertebrate prey species for palila (Brenner et al., 2002) also feed on the mamane seeds (Banko et al., 2002a). ...
Thesis
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The remaining population of palila (Loxioides bailleui), which is tied closely to mamane (Sophora chrysophylla) and naio (Myoporum sandwicense) tree species, has been in long-term decline. This decline is caused by black rats (Ratus ratus), malaria, predation, and parasitism of moth species that palila consume, and the destruction of the mamane naio woodland by ungulate browsing and invasive flora. Using LiDAR and hyperspectral data collected in 2009, this study derived measures of the mamane and naio habitat. Using Bayesian information criterion (BIC) stepwise selection this study found that LiDAR ground return intensity, area of mamane trees and water band index (WBI) were the best explanatory variables of palila bird count data and that mamane and naio may be used at different scales. The browsing and area of mamane variables support existing knowledge; the canopy water content however suggests a problem for palila in wetter areas, contra to established expectation.
... In the seed dispersal system, seed predators/dispersers play an important role in dispersing seeds and facilitating seedling establishment of plants bearing large seeds (Vander Wall 1990;Wang et al. 2014;Steele et al. 2015). During the seed dispersal process, seed-eating animals tend to consume a great proportion of seeds that contain proteins, lipids, carbohydrates, minerals and water (Díaz 1996;Banko et al. 2002;Carrillo et al. 2007). It is assumed that plants need not only to evolve high nutritional quality to attract seed consumers for seed dispersal (Lai et al. 2014;Whitehead et al. 2015), but also to counter predation by animals through a variety of evolutionary strategies (e.g., physical and chemical defenses, rapid germination and seed masting) (Vander Wall 2001;Steele et al. 2006;Schnurr et al. 2014;Zungu and Downs 2015). ...
... Most importantly, high levels of chemical nutritional characteristics in nuts are assumed to attract seed-eating animals and then promote seed dispersal and seedling establishment . On the other hand, nuts in Fagaceae are characterized by a number of chemical defense compounds such as tannins, which bind to protein to impede seed digestion and incur toxicity to certain seed consumers (Twigg and Socha 1996;Banko et al. 2002). In addition, cellulose has been regarded as another defensive component in seeds to cope with seed predation by animals . ...
Article
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Seeds usually exhibit physical and chemical defensive properties; however, it is still debated whether there is trade-off between the two defensive traits. Moreover, the relationship between nutritional and defensive properties of seeds is rarely investigated. In this study, we measured chemical compositions and physical properties of 29 species/varieties in Fagaceae with different seed traits, to investigate variations in nutritional and defensive properties at interspecific level. Our study provided evident nutritional trade-off in Fagaceae nuts, i.e., the concentration of protein and fat was negatively correlated with that of starch. However, no clear trade-off between physical and chemical defensive traits was found, indicating coordinated defense syndromes in these Fagaceae species. Chemical defense in Fagaceae nuts was positively associated with fat and protein but negatively with the content of starch. The congruence between phylogenetic tree and seed trait cladogram indicated conservative evolution of seed traits. In addition, large nuts had high concentration of protein and fat, resulting in a positive relationship between seed coat thickness and caloric values. Fagaceae nuts with high nutrition tended to invest more energy into physical defenses, indicating that the trade-off between chemical and physical defenses might be seed size dependent across plant species.
... For example, intermediate seed sizes are most strongly selected and impacted by generalist rodent seed predators globally, and this has flow on effects to plant recruitment and community composition (Dylewski, Ortega, Bogdziewicz, & Pearson, 2020). Island seed predators may also have acted as a selective force in the evolution of plant reproductive traits, for example high levels of alkaloid defensive compounds within seeds of species such as Sophora (Banko et al., 2002). In addition, assessing the consequences of altered seed predation interactions for plants is incomplete without examining seed predation by invertebrates (Gripenberg et al., 2019). ...
Article
1. Human colonization of islands has resulted in the reduction or loss of many native species, and the introduction of non-native species, producing novel ecosystems. The impacts of these changes on mutualistic plant-animal interactions have received considerable attention, but the potential effects on some antagonistic interactions, such as seed predation, are less thoroughly understood, and often overlooked. 2. Using three archetypal island groups-New Zealand, the Mascarenes and Hawaiʻi-we compare the taxonomic richness and functional diversity of vertebrate seed predators from prehuman and contemporary ecosystems. We scored species on several traits relevant to seed predation, then clustered species into functionally similar groups using hierarchical clustering. 3. These archipelagos once supported between 19 and 24 species of exclusively avian seed predators (representing two to four orders) ranging from large, flight-less herbivores to small, volant finches and parrots. Following human arrival, 63%-89% of these species went extinct, and between 12 and 23 non-native seed predators were introduced. Contemporary seed predator faunas consist of between 14 and 26 species (representing six to seven orders), dominated by non-native granivorous birds and omnivorous mammals. 4. Our results reveal several examples in which non-native species may be functionally similar to extinct seed predators, but most non-native species are functionally different from extinct species, and therefore may be introducing novel seed predation pressures for insular ecosystems. Mammalian seed predators are especially functionally different from the native avian seed predators, as their teeth and widespread habitat distribution allow them to destroy a more diverse range of seeds, including the largest seeds.5. We highlight the need to understand how these altered seed predator communities are affecting native plant populations, particularly in the context of reduced pollination and seed dispersal. More broadly, we argue that antagonistic interactions are an integral part of any ecosystem, and therefore must be understood if we are to achieve more holistic restoration frameworks for insular ecosystems.
... Con tienen proteinas, lipidos, carbohidratos, minerales y agua [1] [2] [3]. La capacidad de las aves de comer ciertos tipos se millas esta condicionada en gran medida por el tamafio del craneo y la forma del pica [2] [4] [5] [6]. Asimismo, la du reza de las semillas cumple un papel fundamental. ...
Conference Paper
This project describes the investigation, devel­ opment and implementation of an electronic device that measures the re q uired force to break a seed. The device is based on a load cell which measures the force applied to the solid. The device detects the instant when the sample breaks. The obtained hardness values are stored in the device internal memory and are visualized in a li q uid crystal display. Also, the device can be connected to a computer to show on a graphic the instantaneous force values applied to a seed or to download the hardness values. The device performance was verified through sample measurements with statistically known hard­ ness values. Resumen-Este trabajo describe la investigacion, desarro­ llo e implementacion de un dispositivo electronico capaz de medir la fuerza re q uerida para romper una semilla. EI disposi­ tivo se basa en una celda de carga q ue mide la fuerza aplicada al solido. Se detecta el in stante en q ue la muestra se rompe, luego los valores de dureza obtenidos se almacenan en la me­ moria intern a del dispositivo y se visualizan a traves de una pantalla de cristal Hquido. Ademas, el instrumento po see co­ nectividad a una computadora para visualizar graficamente los valores de fuerza instantaneos aplicados a la semilla 0 para descargar las ad q uisiciones. EI funcionamiento del instrumen­ to se verifico mediante mediciones de muestras con valores de dureza estadisticos conocidos. I. TNTRODUCCION Las semillas son una fuente completa de nutrientes. Con­ tienen proteinas, lipidos, carbohidratos, minerales y agua [1] [2] [3]. La capacidad de las aves de comer ciertos tipos se­ millas esta condicionada en gran medida por el tamafio del craneo y la forma del pica [2] [4] [5] [6]. Asimismo, la du­ reza de las semillas cumple un papel fundamental. Si la se­ milia es dura, las aves no tendrian acceso a los nutrientes 0 por caso demoraria el acceso a esos nutrientes. Algunos estudios establecieron que ciertos tipos de semi­ lIas de la zona del desierto del Monte Central en Mendoza, Argentina, son consumidas en mayor 0 menor proporcion por su alto contenido en almidon 0 por su bajo contenido en compuestos secundarios de plantas [6]. Sin embargo, hasta el momenta el efecto de la dureza no ha sido establecido ni para estas semillas, ni para otras en otros ambientes y eco­ sistemas en Argentina. Para realizar estudios sobre la dureza de semillas consumidas por las aves, es necesario contar con un instrumento especffico que permita medir la fuerza nece­ saria para alcanzar el punto de quiebre de una muestra. En la actualidad, existen pocos desarrollos sobre instrumentos portatiles para este proposito. ComUnmente, se emplean instrumentos analogicos construidos con un resorte de pre­ sion (similar a un dinamometro) montado en una pareja de tenazas [7]. En este tipo de instrumentos, la medicion de dureza requiere de la destreza del usuario para determinar la posicion a la que llega una aguja del reloj antes de quebrarse la semilla [8]. En este proyecto se desarrolla un instrumento digital donde la obtencion del valor de la fuerza en el momenta de ruptura de la semilla esta automatizada. Este instrumento permitira a biologos y ecologos conocer el impacto de la dureza de las semillas en la ecologia nutricional y compor­ tam ental de aves. EI dispositivo desarrollado en este trabajo permitira in­ corporar la dureza de semillas al conjunto de variables que determinan la seleccion de semillas por aves. En particular, sera utilizado principalmente para conocer como la dureza afecta la seleccion de las semillas por las aves graminivoras del Monte Central en Argentina. Ademas, las implicancias de este desarrollo, se extienden al conocimiento de la dureza de semillas de plantas cultivables, su imp acto en especies plagas de aves y su efecto en el rendimiento de las cosechas. IT. COMPONENTES DEL SISTEMA DE MEDICION Las especificaciones de diseiio del instrumento fueron definidas en base a los requerimientos de los futuros usua­ rios, teniendo en cuenta las caracteristicas de las semillas que deben medirse, los metodos actuales de tomas de mues­ tras, la precision requerida, etc. De esta manera, se plantea­ ron las siguientes especificaciones deseadas para el disefio: • Variable a medir: Fuerza. • Unidad de medicion: Newton. • Rango de medicion: 0 N-150 N. • Precision: 0,5 N. • Capacidad de almacenamiento minima: 100 muestras • Portable: Alimentacion con baterias con una dura­ cion minima de 4hs, tamafio compacto. •
... We may hypothesize that this adaptation originally developed in order to cope with plant alkaloids. The ability of grani-, frugi-and nectarivorous birds to cope with alkaloids as the secondary plant metabolites deposited in seeds or nectar has been shown several times (Díaz 1996;Levey & Cipollini 1998;Banko et al. 2002;Matson et al. 2004;Ríos et al. 2012), though various bird species may significantly differ in their ability to ingest alkaloids (Lerch-Henning & Nicolson 2013, 2015. There is no study comparing the effect of plant and insect alkaloids on the bird metabolism (see Fu et al. 2004 for review), so we may only hypothesize that the ability to deal with chemical alkaloids was predisposed by the ability to deal with plant alkaloids. ...
Article
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Growing evidence exists that aposematic and toxic prey may be included in a predator's diet when the predator experiences physiological stress. The tree sparrow Passer montanus is known to have a significant portion of aposematic and toxic ladybirds in its natural diet. Here, we present experiments testing the attack and eating rate of the tree sparrow towards the invasive aposematic harlequin ladybird Harmonia axyridis. We wondered whether the sparrow's ability to prey on native ladybirds predisposes them to also prey on harlequin ladybirds. We compared the attack and eating rates of tree sparrows of particular age and/or experience classes to test for any changes during ontogeny (hand-reared x young wild-caught × adult wild-caught) and with differing perceived levels of physiological stress (summer adult x winter adult). Winter adult tree sparrows commonly attacked and ate the offered ladybirds with no evidence of disgust or metabolic difficulties after ingestion. Naïve and wild immature tree sparrows attacked the ladybirds but hesitated to eat them. Adult tree sparrows caught in the summer avoided attacking the ladybirds. These results suggest that tree sparrows are able to cope with chemicals ingested along with the ladybirds. This pre-adaptation enables them to include ladybirds in their diet; though they commonly do this only in times of shortage in insect availability (winter). Young sparrows showed avoidance towards the chemical protection of the ladybirds.
... At the same time, measuring geographic variation in other chemical (e.g. alkaloids; Banko et al. 2002) and physical traits (e.g. toughness; Marquis, Ricklefs & Abdala-Roberts 2012) across tissues would be useful in order to determine the generality of tissue-specific patterns. ...
Article
Geographic variation in abiotic factors and species interactions is widespread and is hypothesized to generate concomitant patterns of species trait variation. For example, higher rates of herbivory at lower latitudes are thought to select for increased plant defences, although latitudinal variation in defences may also be influenced directly by abiotic factors and indirectly by predators and parasitoids reducing herbivore pressure. We measured defences of the herb Ruellia nudiflora among 30 populations spanning a latitudinal gradient from northern Yucatan to southern Belize that vary substantially in leaf herbivory (fourfold), seed herbivory (25-fold) and seed herbivore parasitism (14-fold). These surveyed populations span one-third of the species' latitudinal distribution (5° of latitude), the entire precipitation gradient of its distribution, and one-third of the temperature gradient of its distribution. Our prior work showed that leaf herbivory decreased with latitude and that seed herbivory increased with latitude. Here, we measured leaf trichome density and leaf and seed phenolics and tested whether latitudinal variation in climate, herbivory and parasitism explained latitudinal variation in these defensive traits. Patterns of variation in leaf trichomes fully supported predictions, with trichome density increasing with a parallel increase in herbivory towards lower latitudes. While seed phenolics were positively associated with herbivory, and seed herbivory tended to increase with latitude, the predicted (positive) association between latitude and defence was not detectable. There was no detectable association between parasitoids and seed defences. In addition, the association between leaf herbivory and phenolics was weak, and leaf phenolics were not associated with latitude. Importantly, variation in the abiotic environment was associated with plant defence, indicating that abiotic factors can play a major role in shaping plant defences, independently of herbivory. Synthesis. Latitudinal variation in abiotic factors may drive concomitant patterns of variation in plant defences, independently of herbivory. Collectively, these findings highlight the need for assessing geographic variation in plant defences from a multi-factorial perspective, testing for the simultaneous influence of biotic and abiotic factors.
... Understanding the range of naturally induced rainfall variability in this region that is rich in endemic plant (e.g., Price, 2004) and animal (e.g., Case, 1996) species, and is particularly vulnerable to projected human-induced climate change (Benning et al., 2002;Duffy, 2011;Lal et al., 2002), is crucial. Here we present high-resolution, intra-ring δ 13 C data across the unique nitrogen fixing and drought-resistant tree, māmane (Sophora chrysophylla), which provides the main habitat for endangered palila birds (Loxioides bailleui) (Banko et al., 2002;. The wide geographical and environmental extent of māmane, which spans from near sea level to the high-elevation tree line in Hawai'i (Little and Skolmen, 1989), makes it an excellent species for reconstructing past precipitation variations in the region. ...
Article
Determination of carbon isotope (δ13C) values of tree-ring tissue is a well-established method to reconstruct past climate variability at annual resolution, but such records are limited in tropical latitudes due to the lack of well-defined annual growth bands. Recent work has demonstrated the potential for high-resolution, intra-ring δ13C records to help define ring boundaries in tropical environments and provide additional climate information at sub-annual resolution. Here we present a high-resolution, intra-ring carbon isotope (δ13C) record of the Hawaiian endemic species Sophora chrysophylla (also known as “māmane”) in order to assess the ability to extract seasonal climate information from these drought tolerant trees. Tree cores were sampled from high-elevation māmane trees growing on the west side of Mauna Kea, Big Island. Across our entire dataset (1986–2008), we identified a notable decreasing linear trend in the δ13C record of 0.061‰/year that can be attributed to changes in the δ13C value of atmospheric CO2 and pCO2 concentration associated with fossil fuel burning. Correcting for these affects yields a nearly flat δ13C record with a slope of − 0.0075‰/year, suggesting no long-term trends in climate across the study period. We observe a quasi-periodic change in the δ13C values [Δ(δ13C)] measured within each ring that averages 1.09 ± 0.50‰ (± 1σ, n = 23) in amplitude. These variations are interpreted as the intra-annual isotopic signal in tree photosynthesis. The δ13C variability correlates with the visible ring structure of the sample, suggesting the presence of annual growth rings at this tropical high elevation site.
... While the importance of māmane to Palila movement, breeding, and survival has been well documented (van Riper 1978(van Riper , 1980aScott et al. 1984;Fancy et al. 1993;Lindsey et al. 1995;Hess et al. 2001), our results further underscore the specific significance of māmane pods in the diet of Palila. Māmane seeds have high nutritional value (Banko et al. 2002c) and contribute the largest proportion of food mass in the diet of Palila (Banko et al. 2002a). Densities of Palila were previously found to be related to pod availability but not flower availability (Hess et al. 2001). ...
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Seeds and flowers of the leguminous māmane (Sophora chrysophylla) tree are the primary food resource of the federally endangered Palila (Loxioides bailleui; Fringillidae: Drepanidinae), which is now restricted to dry subalpine woodland on Mauna Kea Volcano on the island of Hawai‘i because of centuries of habitat degradation by non-native ungulates. Palila are morphologically and behaviorally adapted to consume māmane seeds by grasping seed pods with their feet and opening pods with stout bills and demonstrate limited ability to exploit alternative food resources. This degree of single species dependency is rare among birds and illustrates unique adaptations that also occurred in other Hawaiian species that are now extinct. In mixed-woodland with co-dominant naio (Myoporum sandwicense), Palila spent 1.7–3.9 times longer in māmane than in naio during foraging observations where naio was 1.3–4.6 times as dense as māmane. Naio fruit was readily available, but it comprised proportionally <11% of food items taken by Palila. Although māmane flowers were more abundant than māmane pods throughout this study except at one lower-elevation mixed-woodland site, Palila spent more time foraging on pods than flowers in both māmane woodland and mixed-woodland, but consumed more flowers than pods in mixed-woodland. Insects, which have been reported as an important component of the diet of Palila, were apparently taken rarely in this study. Protecting and restoring māmane in woodlands adjacent to the current range of Palila will benefit their recovery, allowing them to exploit increased food availability in areas of their former range.
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A new species of Hawaiian finch is described from two fossil maxillae recovered from Holocene lacustrine sediments in Makauwahi Cave, island of Kaua‘i. The new species is assigned to Loxioides on the basis of characters defined in a previous study of drepanidine phylogeny. The maxilla of the new species resembles that of L. bailleui (the only other member of the genus) in its distinctly foreshortened shape, but differs in size and several qualitative characters. The species was sympatric with Loxioides cf. bailleui during the Holocene on Kaua‘i. Like L. bailleui, it may have been a resource specialist feeding mainly on leguminous pods. The radio-carbon chronology of the Makauwahi site indicates that the species became extinct in the late Holocene and, more tentatively, that it may have survived well beyond the time when humans first discovered and colonized Kaua‘i. Una Nueva Especie de Pinzón de Hawaii (Drepanidini: Loxioides) de la Cueva Makauwahi, Kaua‘i
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Chapter
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