Ten mineral elements were determined in green D. guamense leaves, and only potassium was unaffected by host tree species. All of the nine elements that were influenced by host tree species behaved in a manner that the concentrations from the two host trees with horizontal stems separated from the concentrations from the four host trees with vertical stems. Therefore, the results confirm my hypothesis for every element that exhibited significant differences among the host trees.
There are no published orchid nutrition papers from the Mariana Islands to compare with my results. However, the relatively low concentrations of leaf macronutrients reported here were comparable to a range of epiphytic orchid species from Panama [13
]. Stoichiometric variables indicated nitrogen was most limiting, yet nitrogen resorption efficiency was extremely low compared to phosphorus and potassium resorption efficiencies. These enigmatic relations were also shown for several epiphyte orchid species from Panama [14
The highly stable potassium concentrations indicated D. guamense
exerts greater control over leaf potassium homeostasis than any other essential element. The function of this element in maintaining leaf physiology and plant turgidity [15
] may explain the need for this epiphyte species to control potassium concentrations within a narrow range to maintain desiccation tolerance. Moreover, nutrient budgets for the epiphytic orchid Dimerandra emarginata
(G. Meyer) Hoehne revealed that fruit demands for potassium were substantial [13
], and the potassium pool in vegetative organs may serve as a source to satisfy this need.
The manner in which epiphytic orchid plants influence habitat-level nutrient budgets and cycling cannot be fully understood without considering the bulk movement of elements from the living plant canopy to the soil. The transfer of nutrients that are sequestered in vegetation to the soil is mostly controlled by falling leaves and other plant parts. With time, the nutrients within these components of the litter layer are leached and released during decomposition. In addition to this phenomenon, precipitation causes the movement of nutrients from the vegetation to the soil as throughfall and stemflow [18
]. Throughfall is the precipitation that is intercepted by a plant, then drips from the surfaces of components of the canopy. Stemflow is the intercepted rainfall that is transferred to the soil by running down the vertical stems. Throughfall and stemflow cause an increase in nutrient deposition in relation to precipitation because they contain nutrients that are leached from the vegetation canopy and nutrients that have accumulated on the surfaces of the canopy organs since the previous rainfall event [23
]. In contrast to the nutrients that are locked up in freshly fallen litter, these nutrients are available immediately. Throughfall and stemflow significantly contribute to soil nutrition in many ecosystems, and may be particularly important sources of input of severely limiting nutrients [25
My results indicate nitrogen, calcium, iron, manganese, zinc, and boron may be more available to D. guamense plants via interception of stemflow solutions. In contrast, phosphorus, magnesium, and copper may be more available to D. guamense plants via development of a microbiome in the rhizosphere of canopy debris that accumulates on the top of plagiotropic branches. An attempt to separate the direct influences of host tree stem orientation from host tree species on D. guamense leaf nutrient traits is beyond the scope of this study. Furthermore, my dataset does not contain the continuum of host stem orientation from horizontal to vertical. The direct role of orientation could be directly tested with regression analysis by including a full range of stem orientations from horizontal to vertical within the same host tree species. Eudicot trees such as E. joga and G. speciosa would be required for this endeavor because the stems for the other host trees in this study are always ageotropic and therefore restricted to vertical orientation.
Several studies have focused on stemflow of palm species. A Brazilian forest dominated by the palm Orbignya phalerata
Mart. exhibited stemflow that was 8% of incident rainfall, yet the total basal area of vegetation was only 0.3% of the plot area [26
]. Comparisons of palms and eudicot tree species in Brazil showed palm trees to exhibit greater volumes and nutrient transfers in stemflow than the eudicot species [27
]. The nutrient budgets of the palm Rhopalostylis sapida
H. Wendl. &Drude were determined to show that stemflow contributed enough calcium, magnesium, and potassium to the base of the plant to meet all of the annual nutrient needs [29
]. Lodoicea maldivica
(J.F. Gmel.) Pers. was studied to show that the radiating leaves of a palm tree create an effective trap and funnel that intercepts aerosol particles including pollen, then transfers these particles to the soil as stemflow [30
]. The canopy funnel trap phenomenon was further developed for the palm Asterogyne martiana
Wendl. Ex Hemsl. by describing how copious amounts of alien litter were trapped then contributed nutrients to stemflow [31
]. The electrical conductivity of stemflow varied almost three-fold among six palm species in a single location, illuminating the strong influence of canopy traits on stemflow chemistry [32
The presence of epiphytes in a tree canopy can significantly reduce the volume of throughfall and stemflow [33
] illuminating the ability of epiphytes to intercept rainfall, throughfall, and stemflow. The orchid velamen is highly efficient in capturing nutrients within solutions that are ephemerally available on stem surfaces. These nutrients can be absorbed in seconds whenever they become available on the stem surface [2
]. Charged ions are retained after the rapid absorption while uncharged compounds are subsequently lost from the velamen. This form of nutrient absorption by D. guamense
plants may be greater on vertical host stems because of the greater stemflow. Alternatively, the buildup of organic debris in microsites of tree canopies such as the top of large horizontal stems is referred to as “crown humus” or “canopy soil” and may occur in microsites in canopy trees where trapped organic matter becomes heavily decomposed [2
]. Epiphyte roots that are able to access the nutrients that are released from this crown humus may have access to more available nutrients than epiphyte roots attached to vertical host stems. The rhizosphere of an epiphyte’s roots within this humus may be extensively colonized by microorganisms to create canopy hot-spots in which the interactions between organisms reach a very complex level. These contrasts of stemflow versus crown humus may explain my D. guamense
Stoichiometric relations among macronutrients have been used to estimate which elements are most limiting of plant health. The nitrogen:phosphorus mean of 7.35, the nitrogen:potassium mean of 0.55, and the potassium:phosphorus mean of 11.32 indicate that nutrient limitations for these D. guamense
plants were greatest for nitrogen, least for potassium, and intermediate for phosphorus [35
]. Moreover, nitrogen was more limiting in plants growing on horizontal host stems, and less so for plants growing on erect host stems. The inclusion of carbon in the relationships magnifies our ability to understand stoichiometry, as long-lived leaves tend to contain greater carbon construction costs which may dilute the mineral elements. The global C:N:P mean of 469:13:1 [40
] was not similar to the 679:11:1 for the D. guamense
plants growing on erect host stems or the 387:4:1 for the D. guamense
plants growing on horizontal host stems (calculated from Table 1
). However, the difference of this metric for the D. guamense
plants growing on erect host stems versus D. guamense
plants growing on horizontal host stems provides more evidence of the direct influence of host plant on this orchid’s leaf nutrition.
Nutrient resorption is a critical behavior among plants enabling a recycling of limiting elements prior to organ senescence [9
]. This behavior affects plant processes by reducing the dependence on the rhizosphere to satisfy ongoing needs of mineral nutrition. Additionally, the behavior affects biogeochemical cycling by increasing elemental residence time within the plant body and reducing the minerals that are deposited into the litter layer when senescent organs are abscised from a plant. On average, plants withdraw 50% to 60% of leaf nitrogen and phosphorus prior to leaf abscission, and withdraw about 70% of the leaf potassium prior to leaf abscission [8
]. Despite the relatively low green leaf concentrations, the D. guamense
plants in this study were unable to adequately mobilize these three nutrients during leaf senescence, as the resorption efficiencies of nitrogen and phosphorus were less than 35% and that of potassium was only 50%.
] introduced the term resorption proficiency to describe the basal levels to which each nutrient was reduced in senesced leaves. Among woody perennials, a nitrogen resorption proficiency of <7 mg·g−1
and a phosphorus resorption proficiency of <0.5 mg·g−1
indicates complete withdrawal. Our resorption proficiencies did not approach these lower limits, confirming the conclusions from the resorption efficiencies that these orchid plants are not adept at recovering leaf nutrients during senescence.
Green leaf nutrient levels combine with resorption traits to mediate the litter quality upon leaf senescence. The relations among carbon and macronutrients exert profound influence in litter decomposition speed, with greater carbon:nitrogen indicating slower decomposition [44
]. In this study, the influence of host tree on D. guamense
leaf litter chemistry exerted robust changes in these traits. The species with vertical stems produced orchid litter with carbon:nitrogen averaging 105, while the E. joga
trees produced orchid litter that was 1.5-fold greater and the G. speciosa
trees produced orchid litter that was 2.0-fold greater than the species with vertical stems. Parasitic plants such as mistletoe have been shown to influence litterfall quality, quantity, seasonality, and spatial heterogeneity in a manner that alters habitat nutrient cycling [46
]. In this light, my results indicate that host tree identity may exert a direct effect on how the epiphytic D. guamense
influences nutrient turnover via litterfall. On average, the orchid plants growing on palms, cycads, and pandanus trees will contribute higher quality litterfall to the ecosystem than plants growing on E. joga
or G. speciosa
trees. These differences potentially improve habitat health by creating more spatial heterogeneity in soil nutrient status.
Conserving species-at-risk is often plagued with uncertainties and a failure to understand multi-species interactions. The conservation issues related to an epiphyte are magnified beyond direct threats to the plant in need of conservation. The requirement of a suitable host for an epiphyte indicates that threats to the range of host tree species also indirectly threatens an epiphyte species. The threats to C. micronesica
illustrate this phenomenon. This tree was once the most abundant tree on Guam [48
], illuminating the value in serving as potential host for D. guamense
. However, an armored scale [49
] and several other non-native specialist insects [50
] have killed more than 90% of the tree population since 2003 [51
]. This case study reveals the need to conserve host tree species as a component of a comprehensive conservation plan designed to conserve a threatened epiphyte species such as D. guamense
More research is needed on tropical orchid species to fully understand the symbioses between the host plant and the orchid mycorrhizal fungi and other root endophytes [52
]. My results illuminate two more research agendas that would benefit from the inclusion of more tropical orchid species. First, epiphytic orchid species with broad host tree range provide case studies to determine the influence of host tree on orchid nutritional status. My approach was to use two groups of host trees with highly contrasting stem orientations, but there are other host tree traits that could also be studied in the context of orchid plant nutrition. For example, more direct measurements of stemflow and throughfall volume and chemistry among host trees would illuminate the differences among host trees. Second, much of the stemflow research has focused on canopy inputs to the solution that flows down the vertical stems. My results indicate epiphyte plant removal of nutrients from stemflow solutions should also be explicitly considered in the nutrient and water budgets during experimental design. In other words, what makes it into the solution at the canopy level may not be present when the stemflow enters the soil, especially in the case of epiphytic host tree species. The same may be said of throughfall, where mid-strata epiphytes may intercept and remove nutrients from throughfall that originates in the upper canopy. Collection of throughfall at more than one strata within the canopy would be able to quantify this function of canopy epiphytes in future throughfall research.