Reef manta rays forage on tidally driven, high density zooplankton patches in Hanifaru Bay, Maldives

Abstract

Manta rays forage for zooplankton in tropical and subtropical marine environments, which are generally nutrient-poor. Feeding often occurs at predictable locations where these large, mobile cartilaginous fishes congregate to exploit ephemeral productivity hotspots. Investigating the zooplankton dynamics that lead to such feeding aggregations remains a key question for understanding their movement ecology. The aim of this study is to investigate the feeding environment at the largest known aggregation for reef manta rays Mobula alfredi in the world. We sampled zooplankton throughout the tidal cycle, and recorded M. alfredi activity and behaviour, alongside environmental variables at Hanifaru Bay, Maldives. We constructed generalised linear models to investigate possible relationships between zooplankton dynamics, environmental parameters, and how they influenced M. alfredi abundance, behaviour, and foraging strategies. Zooplankton biomass changed rapidly throughout the tidal cycle, and M. alfredi feeding events were significantly related to high zooplankton biomass. Mobula alfredi switched from non-feeding to feeding behaviour at a prey density threshold of 53.7 mg dry mass m−3; more than double the calculated density estimates needed to theoretically meet their metabolic requirements. The highest numbers of M. alfredi observed in Hanifaru Bay corresponded to when they were engaged in feeding behaviour. The community composition of zooplankton was different when M. alfredi was feeding (dominated by copepods and crustaceans) compared to when present but not feeding (more gelatinous species present than in feeding samples). The dominant zooplankton species recorded was Undinula vulgaris. This is a large-bodied calanoid copepod species that blooms in oceanic waters, suggesting offshore influences at the site. Here, we have characterised aspects of the feeding environment for M. alfredi in Hanifaru Bay and identified some of the conditions that may result in large aggregations of this threatened planktivore, and this information can help inform management of this economically important marine protected area.

Manta and devil ray aggregations: conservation challenges and developments in the field

“…and prey abundance (Notarbartolo-di-Sciara, 1988;Anderson et al, 2011;Jaine et al, 2012;Stevens, 2016;Hacohen-Domenéet al, 2017;Stewart et al, 2017b;Lezama-Ochoa et al, 2019b;Lezama-Ochoa et al, 2020;Harris and Stevens, 2021). In the most closely studied example of large feeding aggregations (M. alfredi), no cooperative grouping behavior was observed (Stevens, 2016;Murray, 2019;Armstrong et al, 2021), indicating that these feeding aggregations are likely site-specific behaviors in which prey availability and site characteristics lead to local enhancement of prey (Silverman et al, 2004;Jourdain and Vongraven, 2017). The co-occurrence of multiple individuals, with prey availability likely also determining the group size (Murray, 2019).…”

“…These mobulid feeding aggregations can be influenced by zooplankton size, species, and concentration. For example, in Hanifaru Bay, Maldives, Armstrong et al (2021) found that M. alfredi formed feeding aggregations when the zooplankton community was dominated by large crustaceans (copepods) and total biomass was greater than a theoretical prey density threshold for net energy gain (25.2 mg m 3 ). At this feeding aggregation site, the foraging opportunities appeared to occur when strong lunar tides overcame the force of the prevailing monsoonal current, drawing plankton-rich water from deep waters outside the atoll into the shallow reef inlet (Harris and Stevens, 2021) attracting up to 250 M. alfredi individuals (Stevens, 2016;Harris et al, 2020) (Table 2).…”

“…During feeding aggregations, social groups can be formed as coordinated feeding strategies emerge (e.g., chain, piggyback and lunge feeding). Here, mobulids use the position of a conspecific to improve their chances of successful feeding, enhancing prey capture, hydrodynamic efficiency, and collision avoidance between individuals (Stevens, 2016;Stevens et al, 2018a;Solleliet-Ferreira et al, 2020;Armstrong et al, 2021;Harris and Stevens, 2021). Such coordinated feeding has been described in M. alfredi, M. birostris, M. kuhlii, M. munkiana, M. hypostoma, M. eregoodoo and M. tarapacana while feeding on zooplankton and shoals of anchovies or mesopelagic lanternfish (Stevens, 2016;Stevens et al, 2018a;Stewart et al, 2018c;Solleliet-Ferreira et al, 2020;Bucair et al, 2021) (Figure 3).…”

Multi-decade catches of manta rays (Mobula alfredi, M. birostris) from South Africa reveal significant decline

“…Manta rays (Family Mobulidae) are pelagic planktivores that aggregate in regions supporting high zooplankton densities and cleaning stations, where symbiotic fish remove parasites from them (Feder, 1966;Couturier et al, 2012;Stevens, 2016;White et al, 2017). Being large filter feeders, manta rays spend their lives in proximity to where plankton blooms occur, these being elicited by temporal and spatial environmental cues (Sims et al, 2005;Armstrong et al, 2021). The great variability and transience of regional plankton likely drive their foraging behavior, prey sources, and habitat use (Stewart et al, 2017;Barr and Abelson, 2019;Putra et al, 2020).…”

Sublethal Injuries and Physical Abnormalities in Maldives Manta Rays, Mobula alfredi and Mobula birostris

“…Mobula alfredi predictably migrate across the archipelago following areas of enhanced zooplankton availability, driven by the biannual reversal of the South Asian Monsoon winds (Anderson et al, 2011b;Harris et al, 2020). Aggregations of M. alfredi occur at locations where food becomes seasonally abundant, often in shallow bays and channels (Armstrong et al, 2016(Armstrong et al, , 2021aHarris et al, 2020). They also visit nearby cleaning stations where cleaner fishes remove parasites and clean wounds (Foster, 1985;Marshall, 2008), and where courtship and mating interactions occur (Stevens, 2016;Stevens et al, 2018b).…”