Microbial activity in soils of oligotrophic, arid zone mangroves is likely strongly limited by carbon (C) and nutrient availability, where even small changes in microbial activity could result in significant shifts in ecosystem functioning. We hypothesised that microbial respiration in arid mangrove ecosystems is primarily limited by supply of labile C sources. We measured short-term respiration responses to addition of glucose, citric acid, gallic acid, phosphate, ammonium (NH4 +), nitrate (NO3 −), urea and glutamic acid to mangrove soils from different tidal positions and soil depths in the laboratory using an adaptation of the MicroResp™ procedure (μg CO2-C g soil−1 hr−1). We also measured short-term respiration responses to added glucose, gallic acid, phosphate, ammonium and urea in the field using an infrared gas analyser (g CO2 m−2 hr−1). Both laboratory and field measurements indicated microbial communities were limited by gallic acid, phosphate and ammonium. Respiration rates were enhanced in both the laboratory and the field after addition of gallic acid but not glucose, suggesting adaptations of the arid microbial community to more complex C sources. Addition of phosphate alone and in combination with other substrates enhanced respiration more than ten-fold in the laboratory. In the field, nutrient addition (ammonium and/or phosphate) generally induced greater respiration responses in the surface soils (0–1 cm) compared to subsurface (>1 cm), which we attribute to more nutrient-limited autotrophic microbes in the surface soils. Addition of phosphate also induced slightly higher activity in the low intertidal fringing forests compared to high intertidal scrub forests. Our results contrast with studies of more productive tropical mangrove systems and demonstrate the critical role of microorganisms in maintaining organic matter turnover and nutrient supply in a relatively pristine and water-limited environment.