Epicaulous, Nitrogen-Fixing Microepiphytes in a Tropical Mangal Community, Guadeloupe, French West Indies

Abstract

The mangal community fringing the Grand Cul-de-Sac Marin of Guadeloupe, French West Indies is composed of Rhizophora mangle (red), Avicennia germinans (black), and Laguncularia racemosa (white mangrove). These species form six discrete vegetation zones along a Canal Perrin transect. A. germinans supports dense epicaulous crusts of nitrogen-fixing cyanobacteria which cover the bole and even the finest branchlettes. Crusts on red and white mangrove were less dense. Acetylene reduction activity (ARA) recorded for these previously unreported crusts ranged from 174 to 2012 nmol C2H4 mg Chl.a-1 hr-'. The ARA in the aerial stratum represents a potentially important source of nitrogen to this mangal community. Preliminary data showed that the 42.3 g N m-2 yr-I biologically fixed by cyanobacteria growing epiphytically on Avicennia in zone IV of the Canal Perrin Transect was 3.2 times greater than the total nitrogen budget of an Avicennia community in Southern Australia. The rate-controlling effects of crust hydration and salinity on the ARA and the recovery rate of nitrogenase activity following a period of dehydration are reported. MANGAL COMMUNITIES ARE CIRCUMPOLAR, they occupy approximately 75 percent of the tropical coastlines and often extend inland along the banks of rivers (Zuberer & Silver 1978). The paradox of the high productivity of mangal communities situated in nutrient limited coastal lowlands (Ryther & Dunstan 1971) may be resolved by studies concerning the role of symbiotic cyanobacteria in both the substrate and aerial levels of the community. Although the literature on mangroves in 1981 included over 6000 citations (Rollet 1981), certain aspects of mangrove ecology such as mineral cycling and the contribution of N by nitrogen fixation are poorly understood (Lugo & Snedaker 1974; Walsh 1974; Chapman 1976, 1977; van der Valk & Attiwill 1984; Tomlinson 1986). Investigations of biological nitrogen fixation in mangal communities have been confined to the substrate layer. Rates of nitrogen fixation measured in estuarial muds were low (Brooks et al. 1971, Patriquin & Knowles 1972, Bohlool 1978), while those of mangrove sediments were higher (Zuberer & Silver 1978). Decaying leaves at the substrate surface in New Zealand exhibited a mean acetylene reduction activity (ARA) of 32.4 nmol C2H4 gdw-l hr-I (Hicks & Silvester 1985). These same authors also reported high ARA rates by the cyanobacterium Calothrix (100-500 nmol C2H4 . pneumatophoreI yr'-). N-fixation in leaf litter plus the root and sediment layers contributed 42 percent of the total mangal nitrogen requirement of 13 g N m-2yr-l (van der Valk & Attiwill 1984). Anaerobic fixation in R. mangle litter in Key Biscayne, Florida contributed 11 ,ug N gdw-I hr-I (Gotto & Taylor 1976). Light-independent nitrogenase activities have been detected in the surface sediments of mangrove forests in New Zealand (Hicks & Silvester 1985), Southern Australia (van der Valk & Attiwill 1984) and in decaying leaves of Rhizophora mangle at Key Biscayne, Florida (Gotto & Taylor 1976); whereas, the light dependent ARA by cyanobacteria and members of the Rhodospirillaceae in mangal sediments also occurs (Gotto & Taylor 1976; Zuberer & Silver 1978; Potts 1979, 1980). In general, mangal community muds are anaerobic with high rates of denitrification (Nedwell 1975). The only reported epicaulous ARA resulted from bacteria (812 nmol C2H4 gfw of bark-l'hr-') on the warty bark of Bruguiera gymnorrhiza (Uchino et al. 1984). This paper reports a study of cyanobacterial, epicaulous crusts that reduce acetylene at rates representing a potentially substantial contribution of nitrogen to the Canal Perrin mangal community on the island of Guadeloupe, Lesser Antilles, French West Indies (16?40'N, 61?10'W). It is the first report on epicaulous nitrogenase activity due to cyanobacteria on mangrove species. This mangal community, which borders the shore of the Cul-de-Sac Marin, consists of Rhizophora mangle, Avicennia germinans and Laguncularia racemosa (Imbert & Portecop 1986, Imbert 1985). The trunks and even i Received 30 June 1990, revision accepted 15 March 1991. 2 Formerly R. Fritz-Sheridan.