Ecology of water relations between mistletoe (Taxillus vestitus) and its host oak (Quercus floribunda)
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1 GARKOTI, AKOIJAM & SINGH 243 Tropical Ecology 43(2): , 2002 ISSN International Society for Tropical Ecology Ecology of water relations between mistletoe (Taxillus vestitus) and its host oak (Quercus floribunda) S.C. GARKOTI*, S.B. AKOIJAM & S.P. SINGH Department of Botany, Kumaun University, Nainital , India Abstract: The infestation of Quercus floribunda trees by Taxillus vestitus is common in Himalaya. Seasonal gas exchange and water relations of T. vestitus and its host Q. floribunda were studied under natural field conditions in Nainital, Indian Central Himalaya. Leaf water potential and leaf conductance were followed through the growing seasons on T. vestitus and infested Q. floribunda. Consistent with the reports elsewhere for other species of mistletoe, T. vestitus frequently transpires more rapidly than its host, and maintains a more negative water potential. Predawn and midday water potentials for Q. floribunda are in the range of -0.9 (Rainy season) to (Summer season) and -4.4 (Rainy season) to (Summer season) bars, respectively where as for that of mistletoe, it is -1.6 (Rainy season) to (Summer season) bars and -5.9 (Rainy season) to (Summer season) bars, respectively during predawn and midday. A gap in water potential between host and mistletoe occurred throughout the study period, which increased with the severity of moisture. During all seasons T. vestitus out transpired the host. It appears that the low water potential enables the mistletoe to have access to host water all the time and higher transpiration further enhances water uptake and hence possible intake of valuable elements for growth. Both the species studied showed stomatal control during the dry season, which seems to be determined by the increase of the evaporative demand. Resumen: La infestación de árboles de Quercus floribunda por Taxillus vestitus es común en Himalaya. Se estudiaron el intercambio de gases estacional y las relaciones hídricas de T. vestitus y su hospedero Q. floribunda en condiciones naturales de campo en Nainital, porción central del Himalaya en la India. El potencial hídrico foliar y la conductancia foliar fueron monitoreados durante las estaciones de crecimiento de T. vestitus y de Q. floribunda infestados. De manera consistente con los reportes para otras especies de muérdago, frecuentemente T. vestitus transpira más rápidamente que su hospedero y mantiene un potencial hídrico más negativo. Los potenciales hídricos de la madrugada y mediodía para Q. floribunda están en el intervalo de -0.9 (época de lluvias) a (verano), y de -4.4 (época de lluvias) a (verano) bars, respectivamente, mientras que para el muérdago los intervalos son de -1.6 (época de lluvias) a (verano) bars, y de -5.9 (época de lluvias) a (verano) bars, respectivamente, durante la madrugada y el mediodía. Se presentó una desigualdad en el potencial hídrico entre el hospedero y el muérdago durante todo el periodo de estudio, la cual se incrementó con la severidad de la humedad. Durante todas las estaciones T. vestitus tuvo una transpiración mayor que el hospedero. Parece que el bajo potencial hídrico permite al muérdago tener acceso al agua del hospedero todo el tiempo y la mayor transpiración incrementa todavía más el consumo de agua y por lo tanto la posible entrada de elementos valiosos para el crecimiento. Las dos especies estudiadas mostraron control estomático durante la estación seca, lo cual parece estar determinado por el incremento en la demanda evaportiva. Resumo: A infestação das árvores de Quercus floribunda pelo Taxilus vestitus é comum nos Himalaias. As trocas gasosas estacionais e as relações hídricas da T. vestitus e da sua *Corresponding Author: Department of Ecology, Assam University, Silchar , Assam, India
2 244 WATER RELATIONS OF HOST PARASITE RELATIONSHIP hospedeira a Q. floribunda foram estudadas sob condições naturais de campo em Nainital, no Himalaia central Indiano. O potencial hídrico nas folhas e a condutância folhear foram controladas ao longo das estações de crescimento na T. vestitus e na Q. floribunda infestada. De forma consistente com os relatórios anteriores para outras espécies de azevinho, a T.vestitus transpira frequentemente mais rapidamente que o seu hospedeiro e mantém um potencial hídrico mais negativo. O potencial hídrico de madrugada e a meio dia para a Q. floribunda situou-se no intervalo de 0,9 (Estação das chuvas) a 12,3 bares (Verão) e 4,4 (Estação das chuvas) a 20,5 bares (Verão) respectivamente, enquanto que para o azevinho foi de 1,6 (Estação das chuvas) a 14,9 bares (Verão) e 5,9 (Estação das chuvas) a 25,2 bares (Verão), respectivamente durante a madrugada e o meio dia. O gap no potencial hídrico entre o hospedeiro e o azevinho ocorreu durante todo o período do estudo e foi mais intenso com a severidade da humidade. Durante todas as estações a T. vestitus transpirou o hospedeiro. Parece que o baixo potencial hídrico possibilita ao azevinho o acesso à água do hospedeiro durante todo o tempo com a elevada transpiração a favorecer e a potenciar a absorção da água e, por esta via, um elemento importante da absorção de elementos valiosos para o crescimento. As duas espécies estudadas mostraram o controlo dos estomas durante a estação seca, o que parece ser determinada pelo aumento da evaporação. Key words: Infestation, leaf conductance, parasite, Quercus floribunda, Taxillus vestitus, water potential. Introduction Mistletoes are hemiparasites. They rely completely upon their host for water and minerals but capable of producing their own supply of photosynthate to a certain extent (Ehleringer et al. 1985; Johnson & Choinski 1993; Kuijt1969; Marshall & Ehleringer 1990). Parasitism of Quercus floribunda and other species by Taxillus vestitus is common in areas where trees are subject to lopping for fodder or other purposes. Photosynthetic rates of mistletoes is very low compared to other higher plants (Marshall et al. 1994), although transpiration rates in mistletoes are high (Davidson et al. 1989; Glatzel 1983; Goldstein et al. 1989), up to 9 times higher than those of their host (Ullmann et al. 1985). The extent to which the parasite damages the host by desiccating it is difficult to ascertain but it is likely that it plays a substantial role in disturbing the host s physiology. Early work (Glatzel 1983; Goldstein et al. 1989; Kemberling 1910; Küppers 1992; Scholander et al. 1965; Schulze & Hill 1982; Tuohy & Choinski 1991) indicated that the mistletoes had an unusually high rate of conductance compared to the host though the opposite was also found in some cases (Beserra et al. 1962; Fisher 1983; Küppers et al. 1992). Since 1965 (Scholander et al. 1965) it has been generally substantiated that mistletoes exhibit lower leaf water potential than their corresponding hosts (Ehleringer et al. 1986; Goldstein et al. 1989; Whittington & Sinclair 1988). This study was conducted with the objective to compare the responses of mistletoe, T. vestitus and the host Q. floribunda to seasonal drought and is expected to provide a critical test of generalities developed in other climates. Material and methods Kumaun and Garhawal Mountains form the central sector of Indian Himalaya continuing in the southeast into Nepalese Himalaya. The mid altitudes i.e. approximately between 1500 and 3000 m of the central Himalaya are covered with Himalayan moist temperate forests (Champion & Seth 1968) with one or more species of oaks forming climax vegetation. Quercus floribunda locally known as tilonj oak, extends westwards to Afghanistan and eastwards to Nepal, usually at the altitudes between 2000 m and 3000 m. Q. floribunda seems to prefer revine and moist areas. It is frequently gregarious and sometime reaches large size. Wood is very hard. Annual rings are marked by a dark line. Tree height usually reaches m. It reproduces very well from seed as well as by coppicing.
3 GARKOTI, AKOIJAM & SINGH 245 The study was conducted in Q. floribunda forest in Nainital (29 24 N 1at. and E long.). The area is latitudinally located within the subtropical belt and is influenced greatly by the southwest monsoon. A temperate environment prevails because of the high elevation, and the functional behaviour of vegetation represents a transition between strongly seasonal tropical & temperate conditions (Singh & Singh 1992). A survey made in and around Nainital revealed that upto 90% trees of Q. floribunda were infested with mistletoes. Due to lopping of branches, light availability and cut surfaces for seed attachment increase, resulting in proliferation of mistletoes in most of the disturbed oak forests. The year is divisible into three main seasons; rainy (mid June-September); winter (October- March); and summer (April-mid June). Of the total annual rainfall of 1963 mm, 90% occurs in the rainy season. The mean daily temperature ranges between 7 and 19.3 C. For observations on water relations, six average sized trees (about 50 cm diameter at breast height) of Q. floribunda infested by mistletoe were selected in a typical Q. floribunda forest site in Nainital. Fully illuminated adjacent twigs/leaves of host and parasite located on the periphery of the crown were sampled. Leaf water potential (ψ) was measured on leafy shoot sampled from parasitized branches using a pressure chamber (Model 1000 PMS Instrument CO, Corvallis). Water potential (ψ) was measured as described by Zobel & Singh (1995), Garkoti et al. (2000) before dawn when plant ψ should be maximum and at equilibrium with soil moisture and at midday when plant ψ should be minimum. Stomatal conductance (m mol m -2 s -1 ) of host and parasite was assessed at 9 AM & 1 PM by using Ap4-type porometer (Delta-T Devices, Cambridge, England). Data from two to three leaves from each plant were averaged while interpreting the results. Foliage was maintained in natural orientation during conductance measurements. However, for larger trees or in case of infestation on the crown top large twigs were cut for measurements. Soil ψ was measured once per sample date at two depths (10 cm and 60 cm) for three representative locations using a thermocouple psychrometer (SC10A, Decagon Devices, Pullman, WA, USA, with NT3 micro voltmeter). Water relations attributes were sampled during five seasons: rainy-hot but wet, autumn-with high soil moisture and cooling weather; winteroften with freezing weather, spring-just before initiation of new leaf crop; summer seasonssupporting most production of new leaves. Results and discussion Across the seasons an increase in soil water potential (Soil ψ) was observed with increase in soil depth. At 10 cm soil depth it varied between > -2.0 bars in rainy season and bars in summer season while at 60 cm soil depth the Soil (ψ) was between > -2.0 bars in rainy seasons and bars in summer season (Table 1). On all sampling dates both predawn and midday plant water potentials (ψ) were more severe for the mistletoe than for the host (Fig. 1a & b). This enables the parasite to have access to host water in all seasons, even if the host is under considerable water stress. Although the water potentials of the mistletoe shoots were consistently lower than those of the host, the potential difference was not consistent (Fig. 1a & b). It seems that the parasite employs a more efficient osmotic adjustment for maintaining an unbroken supply of water from the host with higher water potentials. Consistent with the observations of Garkoti et al. (2000) and Zobel et al. (2001) the daily range of ψ ( ψ = predawn ψ - midday ψ) in both mistletoe and the host in general, showed a similar pattern (Table 2). In both the cases the maximum difference between predawn & midday ψ ( ψ) was found in summer season when the soil ψ was lowest (Table 1) and plants were at the peak of the growth phase, and the minimum difference was observed in winter season when all plant activities are at minimum. The mistletoe out transpires its host in all seasons. The transpiration rates observed for mistletoes were usually many times the rates of the host particularly when host stress was greater. Accord- Table 1. Seasonal variation in soil water potential (-bars) in Q. floribunda forest. Seasons Soil Depth 10 cm 60 cm Rainy > 2.0 > 2.0 Autumn Winter Spring Summer
4 246 WATER RELATIONS OF HOST PARASITE RELATIONSHIP Fig. 1. Seasonal courses of leaf conductance and water potential for: Q. floribunda and T. vestitus a = predawn (9 AM for leaf conductance), b = midday; R = rainy, A = autumn, S & S are spring and summer seasons, respectively. ing to Schulze et al. (1984) high transpiration rates of mistletoe leads to enhanced assimilation of nitrogen from the host xylem sap which might be necessary for the growth of mistletoe. Because xylem-tapping mistletoes have no direct access to nitrogen, which may be present in the host phloem, they are entirely dependent on the dilute nitrogen they parasitize from host xylem sap (Marshall et al. 1994). Though in present study parasitic carbon gain has not been evaluated, studies indicate that the high transpiration rates in mistletoes also results to carbon gain in addition to nitrogen. Press et al. (1987) and Marshall & Ehleringer (1990) noted that mistletoes must obtain a substantial carbon subsidy from passive uptake and assimilation of carbon compounds dissolved in the xylem sap of the host. The proportion of carbon in mistletoe derived from host is reported to be between 5 and 60%. A mistletoe with high nitrogen status would have high photosynthetic rate. So, increased import of nitrogen through high transpiration may reduce the dependence of mistletoe on host for carbon. High transpiration rates exhibited by T. vestitus in present study may partly be related to the strategy for increasing net autotrophic (mistletoe s own production) carbon through increased passive N uptake. In present study both host and parasite suffered on account of long drought that follows the monsoon months, as it reduced their water potentials and leaf conductance. However, while the decline in the water potential occurred earlier in the parasite than the host, it was relatively delayed for leaf water conductance (Fig. 1a & b). Although
5 GARKOTI, AKOIJAM & SINGH 247 Table 2. Patterns of seasonal difference in predawn & midday water potential in Q. floribunda and T. vestitus. Seasons T. vestitus Q. floribunda Rainy Autumn Winter Spring Summer both host and parasite could have high capacity to keep stomata open during drought, the parasite perhaps keeps stomata more open than the host up to considerably lower water potential. Since access to water contained in the host tissues remains unbroken presumably due to lowered osmotic potential, the parasite is not required to avoid drought by closing down stomata. On a day that followed a long rainless period, and when relative humidity was less than 25% throughout the day the parasite exhibited a three fold higher photosynthetic rate (Garkoti & Singh, unpublished data). For maintaining high rates of photosynthesis the mistletoe continues to extract water and minerals from the host, even during drought and causes severe stress to the host. Thus, the parasite adversely affects the host through disrupting water relations. One time observations made in summer season on healthy as well as infested Q. floribunda trees growing at nearby site also confirm the statement. The healthy trees had early morning leaf water conductance of m mol m -2 s -1 compared to 57 m mol m -2 s -1 in the infested tree. Leaf conductance measurements show that Q. floribunda does not close its stomata completely during period of increasing water stress, only enough to prevent further dehydration. Presumably the stomata were open at a level where transpiration was equal to water flow into the leaf from the xylem pathway. For any level of water availability, T. vestitus is able to tolerate a greater stomatal opening, hence more transpiration than Q. floribunda. Glatzel (1983), Schulze et al. (1982) and Whittington & Sinclair (1988) suggested that mistletoes can control stomatal apertures. The claims that mistletoes have little control over stomatal conductance (Calder et al. 1979; Fisher 1983) is not supported by this study, as stomata of both the species responded to water stress by lowering their conductances (Fig. 1a & b). Montilla et al. (1980) also reported that the mistletoe shows stomatal control during the dry season, which they have linked to the increase of evaporative demand. Present pre-dawn water potential values for mistletoe are higher than those reported for Amyema miquelli (-13.4 to bars; Whittington & Sinclair 1988) and are generally comparable or lower than those reported for other mistletoes; bars for Viscum album; -4.0 to -9.5 bars for Loranthus europaeus (Schulze et al. 1984), -4.0 to -8.0 bars for Loranthus europaeus (Glatzel 1983). The water potentials for Q. floribunda are generally in between the range reported for Eucalyptus fasciculosa (Whittington & Sinclair 1983) (-6.0 to bars) and higher than those reported for some other eucalyptus (-16.3 to bars; Myers & Neals 1984). Values ranging from -4.0 to bars for E. fasciculosa from a site with higher rainfall were reported (Sinclair & Venables 1983). These values are well within the range of the present study. A pre-dawn gap in water potential between host and mistletoe occurred throughout the study period, which increased from high water availability conditions to dry periods. Study made on E. fasciculosa and its parasite (Whittington & Sinclair 1988) shows that E. fasciculosa rehydrated relatively rapidly reaching an equilibrium water potential by about pm, the water potential of A. miquelli (parasite) increased gradually throughout the night indicating a large hydraulic resistance perhaps associated with haustorial junction. This hydraulic resistance reduced the rate of rehydration of mistletoe to such an extent that a large gap in water potential between host and parasite was maintained at dawn. The result obtained in this study can be explained in terms of large resistance at the haustorial junctions and a large capacitance of the mistletoe leaf compared to its host. The high and possibly variable haustorial resistance slows night time rehydration of the mistletoe so that it does not have time to reach equilibrium with the host by dawn. The large leaf capacitance caused considerable hysteresis in the relationship between transpiration and water potential. It is suggested that a large haustorial resistance, which is in some ways hazardous to Taxillus may benefit it in other ways, as the long-term survival of the mistletoe is dependent upon the survival and health of the host.
6 248 WATER RELATIONS OF HOST PARASITE RELATIONSHIP Acknowledgement We thank Prof. D.B. Zobel for his valuable help and suggestions. References Beserra, De Oliveira, J.G., I.F. Marques Valio, G.M. Felippe & S.M. Campos de Balanco d agua do hemiparasito Struthanthus vulgaris Mart.: 1. Estudo comparativo co seu hospedeiro Erythrina speciosa Andr. Na Estaeao chuvosa (Sao Paulo, SP, Brasil). An Acad Bras Cienc 34: Calder, D.M., R.W. Eager & P. Bernhardt Introduction to the ecology and floral biology of Amyema (Lorenthaceae) in southeastern Australia. pp In: L.T. Musselman, A.D. Worsham & A.D. Eplee (eds.) Proceedings of the Second Symposium on Parasite Weeds. North Carolina State University, Raleigh, NC. Champion, H.G. & S.K. Seth A Revised Survey of the Forest Types of India. Government of India Publication, New Delhi. Davidson, N.J., K.C. True & J.S. Pate Water relations of the parasite: host relationship between the mistletoe Amyema linophyllum (Fenzal) Tieghem and Casuarina Obesa Miq. Oecologia 80: Ehleringer, J.R., C.S. Cook & L.L. Tiezen Comparative water use and nitrogen relationships in a mistletoe and its host. Oecologia 68: Ehleringer, J.R., E.D. Schulze, H. Ziegler, O.L. Lange, G.D. Farquhar & I.R. Cowan Xylem tapping mistletoe: Water or nutrient parasite? Science 227: Fisher, J.T Water relations of mistletoes and their hosts. pp In: M. Calder & P. Bernhardt (eds.). The Biology of Mistletoes. Academic Press, New York. Garkoti, S.C., D.B. Zobel & S.P. Singh Comparison of water relations of seedlings and trees of two Himalayan oaks. International Journal of Ecology and Environmental Sciences 26: Glatzel, G Mineral nutrition and water relations of hemi parasitic mistletoes: a question of partitioning experiments with Loranthus Europaeu on Quercus petraea and Quercus robur. Oecologia 56: Goldstein, G., F. Rada, O. Zabala, A. Azocar, M.F. Canales & A. Celis Gas exchange and water balance of a mistletoe species and its mangrove hosts. Oecologia 78: Johnson, J.M. & J.S. Choinski Jr Photosynthesis in Tapinanthus Diplorhynchus mistletoe host relationship. Annals of Botany 72: Kemberling, Z Verdunstunguersuche mit tropischen Loranthaceen. Berichte der deutschen Botanischen Gesellschaft 32: Kuijt, J The Biology of Parasitic Flowering Plants. University of California Press, Berkeley. Küppers, M Carbon discrimination, water use efficiency nitrogen and phosphorous nutrition of the host/mistletoe pair Eucalyptus behriana F. Muell and Amyema miquelii (Lehm. Ex Miq) Teigh at permanently low plant water status in the field. Trees 7: Küppers, M., B.I.L. Küppers & A.G. Swan Leaf conductance and xylem pressures of the host/mistle toe pair Eucalyptus behriana F. Muell and Amyema miquelii (Lehm. Ex. Miq.) Teigh at permanently low plant water status in the field. Trees 8: Marshall, J.D. & J.R. Ehleringer Are xylemtapping mistletoes partially heterotrophic? Oecologia 84: Marshall, J.D., J.R. Ehleringer, J.R. Schulze, E.D. Schulze & G.D. Farquhar Carbon isotope composition, gas exchange and heterotophy in Australian mistletoes. Functional Ecology 8: Montilla, M., A. Azocar & G. Goldstein Effects de la hemiparasita Phthirusa pyrifolia sobre el balance hidrico de dos hospedantes. Acta-Oecologica, Oecologia-Plantarum 10: Myers, B.A. & T.F. Neals Seasonal changes in the water relations of Eucalyptus behriana. F. Muell and E. microcarpa (Maiden). Australian Journal of Botany 23: Press, M.C., N. Shah, J.M. Tuohy & G.R. Stewart Carbon isotope ratios demonstrate carbon flux from C4 hosts to C3 parasite. Plant Physiology 85: Scholander, P.F., H.T. Hammel, E.D. Brandstreet & E.A. Hemmingsen Sap pressure in vascular plants. Science 148: Schulze, E.L. & A.E. Hall Stomatal responses, water loss and CO2 assimilation rates of plants in contrasting environments. pp In: O.L. Lange, P.S. Nobel C.B. Osmond & H. Ziegler (eds.). Physiological Plant Ecology II Water relations and carbon assimilation. Encyclopedia of Plant Physiology. Springer Verlag Berlin. Schulze, E.D., N.C. Turner & G. Glatzel Carbon, water and nutrient relationships of two mistletoes and their hosts: a hypothesis. Plant Cell and Environment 7:
7 GARKOTI, AKOIJAM & SINGH 249 Sinclair, R. & W.N. Venables An alternative method for analyzing pressure volume curves produced with the pressure chamber. Plant Cell and Environment 6: Singh, J.S. & S.P. Singh Forests of Himalaya: Structure Functioning and Impact of Man. Gyanodaya Prakashan, Nainital. Tuohy, J.M. & J.S. Choinski Jr Water relations and photosynthesis in the mistletoe Tieghemia bolusii and its host tree Diplorhynchus condylocapon pp In: J.K. Ransom, L.J. Musselman, A.D. Worshma & C.J. Parker (eds.) Proceedings of the 5th International Symposium of Parasitic Weeds. Nairobi, Kenya. Whittington, J. & R. Sinclair Water relation of the mistletoe Amyema miquelii and its host Eucalyptus fasciculosa. Australian Journal of Botany 36: Ullmann, I., O.L. Lange, H. Ziegler, J. Ehleringer, E.D. Schulze & I.R. Cowan Diurnal courses of leaf conductance and transpiration of mistletoes and their hosts in central Australia. Oecolgoia 67: Zobel, D.B. & S.P. Singh Tree water relations alongwith vegetational gradient in the Himalayas. Current Science 68: Zobel, D.B., S.C. Garkoti, S.P. Singh, A. Tewari & C.M.S. Negi Patterns of water potential among forest types of the central Himalaya. Current Science 80:
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