Oxygen microgradients in the rhizosphere of the mangrove Avicennia marina

Oxygen concentration was measured in aerial roots (pneumatophores), horizontal cable roots and surrounding sediment of the tree Avicennia marina (Forsk.) Vierh. in a mangrove swamp at Ao Nam Bor, on the southeast coast of Phuket Island, Thailand. The O2 measurements were made in the field with a polarographlc oxygen minielectrode. The O2 concentration inside pneurnatophores was 63 to 88 % of air saturation, whereas the cable roots showed a lower concentration (62 to 73 %) indicating an O2 gradlent from the emerging parts to the subsurface roots. The O2 concentration in the roots was highest in the outer part of the aerenchyma. The oxic zone of the sediment around roots was thin (ca 0.5 mm) which may indicate that very litte O2 is released from the roots. Recording around a fiddler crab (Uca sp.) burrow revealed, for comparison, that the oxic layer of the burrow wall was ca 1 mm thick. The penetration depth for O2 at the surface of this tropical mangrove sediment (1.5 to 3 mm) was similar to that measured in temperate coastal sediments. Sediments in mangrove swamps are in general 0 2 depleted, with only a thin oxic surface layer (Kristensen et aL unpubl.). Mangroves therefore possess special adaptations for supplying O2 to the respiring root system. Hence many mangroves have negatively geotropic roots that emerge above the sediment surface, and these contain well-developed aerenchyma tissue. Pneumatophores (aerial roots), which are found for example in Avicennia and Sonneratia, have long been considered as organs responsible for gaseous exchange between the atmosphere and the internal tissues of mangroves (Goebel 1886). Other genera as Bruguiera and Lumnitzera have emerging kneelike bends on their lateral roots. In Rhizophora spp. the prop roots are responsible for gaseous exchange (Chapman 1976). Chapman (1976) gives a review of the relatively few experimental studies that have been made on the function of the pneumatophores. These studies were made more than 30 yr ago, often with manometric techniques and on cut and isolated root parts. Scholander et al. (1955) found that the O2 concentration in Rhizophora O Inter-Research/Printed in F. R. Germany prop roots approached that of the atmosphere (14 to 19 %) whereas the CO2 concentration was higher (4 to 6 %). The same authors also studied mechanisms for gas transport in the root systems of Avicennia. The purpose of the present study was to measure O2 concentrations around and inside intact pneumatophores and cable roots of Avicennia marina in the field. If significant amounts of O2 are released from the gastransporting roots, an oxic zone outside the roots would be expected. For comparison we measured O2 profiles around an air-filled burrow of a fiddler crab (Uca sp.). Materials and methods. The investigation was cdrried oul in January i387 iri the Ao Narri Bor I I I ~ I I grove on the southeast coast of Phuket Island, southwest Thailand (Frith et al. 1976, Christensen 1978). This mangrove forest is ca 200 m wide at the study site and is bordered by a ca 500 m wide tidal flat without vegetation. The measurements were made around an isolated Avicennia manna (Forsk.) Vierh. tree at the seaward edge of the mangrove forest and around a fiddler crab (Uca sp.) burrow situated 5 m from the tree on the tidal flat. The sediment and pneumatophores were covered by 60 to 70 cm water at high tide. The tidal range in the area was ca 2 m. Salinity of the seawater was 35 %O and water temperature was 28 "C. However, the temperature of the sediment surface may rise to 35 to' 38 "C at low tide when the sediment is exposed to direct sun. Oxygen concentration was measured with a polarographic needle minielectrode (2.5 cm long, 0.7 mm o.d., Diamond Electro-Tech) covered with a DePeX membrane. The spatial resolution of the electrode was less than 0.5 mm. Pretreatment and calibration of the oxygen electrode was carried out according to Helder & Bakker (1985). A calomel electrode (Radiometer) was used as a reference. The electrodes were connected to a pico-ammeter (Keithly 480) and the signal recorded 202 Mar. Ecol. Prog. Ser. 44: 201-204, 1988 on a battery-driven recorder (Minigor RE501, Goerz Electro). The oxygen electrode was mounted on a manually operated micromanipulator. Oxygen profiles were measured in the field around the root system of the tree (2 m from the trunk) and around a fiddler crab (Uca sp.) burrow. The tree was ca 3 m high, the crown 2 m wide and the root system with pneumatophores extended 2 to 3 m from the trunk. All measurements were made during daytime with exposed sediment surface. Vertical profiles were measured to describe the oxygen gradient at the sediment surface and at horizontal roots. Profiles with a 45" angle to the sediment surface were made to determine oxygen gradients around vertical structures. After the O2 measurements, the roots were dug up from the sediment and cut where the electrode had entered the root. The thickness of the cut root was measured with a ruler (precision 0.5 mm). Drawings of transverse sections of the roots were made using a Wild M7 microscope equipped with a drawing apparatus. Copies of the drawings were cut and weighed, and the aerenchyma part was calculated relative to the total area of the transverse section. Results. The O2 measurements showed high concentrations inside the roots compared to the surrounding sediment (Fig. 1). The pneumatophore contained between 63 and 88 O/O of O2 saturation (mean 78 %) at l l to 19 mm below the sediment surface (Fig. 1A) The O2 concentration was highest in the outer part of the pneumatophore just inside the epidermis. A minimum surrounded by minor peaks was recorded in the center of the pneumatophore. The cable root deeper in the sediment (66 to 78 mm) showed a lower O2 concentration (62 to 73 %, mean 65% saturation) than the pneumatophores (Fig. 1B). The highest O2 concentrations in the cable roots were also found just inside the epidermis. Another measurement on a different root system showed a similar difference in O2 concentration between the pneumatophore (75 to 86 % , 10 mm below the sediment surface) and the cable root (61 to 74 %, 47 mm below the sediment surface). The O2 gradients around both pneumatophores and cable roots were very steep (ca 0.5 mm). It is difficult to know exactly when the O2 probe is inside or outside the roots and thus, if the recorded gradient is in the outer part of the root or in the surrounding sediment. The outer