From coast to slope: Zooplankton communities shift in the Northern Alboran Sea

Highlights

• The SSL relative frequency response change according to its zooplankton composition.

• Strong scatterers as fish larvae mask the detection of weak scatterers as crustaceans.

• The main SSL environmental forcing were the distance to the coast and the thermocline.

• Acoustic data were verified as indicator of the secondary production.

Abstract

The zooplankton composition of the Sound Scattering Layer (SSL) detected at multiples frequencies, 18, 38, 120 and 200 kHz, along the continental shelf of the Northern Alboran Sea (Mediterranean Sea) has been identified in July 2013 and 2014 by means of different plankton nets and the SSL dominant scatterers have been identified using zooplankton scattering models.

Three acoustic patterns, based on their distinctive relative frequency response (r(f)), have been detected along the continental shelf, matching with three zooplankton communities; in coastal areas (25–40 m bottom depth), a homogeneous community composed by Fluid-like zooplankton, mainly crustaceans, exhibiting a r(f) peak at 120 kHz, (ii) in intermediate areas (40–190 m) a heterogeneous community composed by Fluid-like (crustaceans, chaetognaths, larvaceans, doliolids, Calycophora siphonophores), Elastic-shelled (heteropods) and Gas-bearing (fish larvae) zooplankton, exhibiting a r(f) peak at 38 kHz (iii) in the continental shelf edge (180–250 m), a zooplankton community dominated by Maurolicus muelleri fish larvae, exhibiting a r(f) peak at 18 kHz. Scattering models results showed that stronger scatterers as fish larvae (Gas-bearing), although scarce in samples, dominated the backscattering energy at almost all frequencies and locations. Fluid-like zooplankton contribution was only significant in coastal areas at high frequencies (120 and 200 kHz).

The application of these findings to all echograms collected over the study area made it possible to obtain, the macro scale spatial distribution of the zooplankton communities as well as the SSL backscatter energy all over the continental shelf, highlighting the suitability of the use of acoustic data as an indicator of secondary production.

Introduction

Plankton and micronekton form dense and geographically extensive layers, which are observed acoustically using echosounders, known as Sound Scattering Layers (SSLs). These layers may present a monospecific composition such as occurs with euphausiids aggregations (Everson, 2000; Everson et al., 2007; Ventero et al., 2019); they may be composed by organisms belonging to the same taxonomic family such as copepods (Mutlu, 2003) or mesopelagic fishes (Peña et al., 2014) or they may present a heterogeneous and multispecific organisms composition (Lavery et al., 2007). Echosounders let us determine the vertical (Benoit-Bird et al., 2010) and the horizontal (Moline et al., 2010) structure of the SSLs in a remote, no invasive and synoptically way (Simmonds and MacLennan, 2005) and enable the collection of information simultaneously from different pelagic communities (plankton and nekton) on a spatial and temporal scale, an almost impossible task with the use of traditional sampling methods (Godo et al., 2014).

Technology evolution from single to multiple frequency systems (Chu, 2011) has provided scientists with an additional capability to characterize or classify the scattering targets according to the strong frequency dependence of signals backscattered by marine animals (Chu et al., 1992; Holliday et al., 1989). Planktonic organisms can be classified, based on the dispersion model that explains their acoustic reflection, according to the categorization principle (Fernandes et al., 2006). This principle discriminates organisms in three different categories, namely: Fluid-like, Elastic-shelled, and Gas-bearing (Martin et al., 1996; Simmonds and MacLennan, 2005; Stanton et al., 1996). The Fluid-like class includes organisms with tissues composition causing a low contrast of density and sound speed compared to sea water; e.g., copepods, euphausiids, or chaetognaths. The Elastic-shelled class is composed by organisms with an external shell made of calcium carbonate, such as pteropodes. Finally, in the Gas-bearing class are included organisms with gaseous vesicles, such as some siphonophores, adult jellyfish, and fish larvae. The relative frequency response measured at different acoustic frequencies is an important acoustic feature used to characterize the acoustic targets (Korneliussen and Ona, 2003). Fluid-like zooplankton backscatter is characterized by increasing the acoustic backscatter from low to high frequencies considering the frequency range (18–200 kHz) commonly employed during acoustic surveys focus on stock assessment. All Gas-bearing zooplankton displays resonant scattering at a frequency that depends on the depth and the size of the gas inclusion. Backscatter from Elastic-shelled zooplankton is characterized by the smooth transition between low frequencies and high frequencies.

Fisheries acoustic water-column data is a currently underused data source for monitoring changes in pelagic ecosystem state, in particular for deriving indicators making use of the distinctive acoustic frequency response of different organism groups (Trenkel et al., 2011). Routine assessment acoustic surveys data contain information about the entire water column and can provide large scale reference maps of the distribution of acoustic scattering groups (Trenkel and Berger, 2013). In addition, knowledge of the spatial and temporal variation of the distribution of different pelagic communities (mainly fish and plankton) is essential to achieve efficient management of fishery resources based on the ecosystem approach (Bertrand et al., 2014; FAO, 2008).

The main difficulty when several frequencies are used to characterize zooplankton is the diverse array of organisms present in the water column (Lavery et al., 2007). Direct identification of organisms, by means of biological samples, is needed in order to interpret correctly the echotraces (Simmonds and MacLennan, 2005). The zooplankton is composed by a multitude of organisms that live their entire life (holoplankton) or part of it (meroplankton) suspended in the water column, presenting an extraordinary diversity of taxa (Alcaraz and Calbet, 2007) shapes, sizes (Sieburth et al., 1978) and body structures that prevent their sinking. The high degree of biodiversity and sizes makes it difficult to determine its composition using a single sampling device, so it is necessary to use several of them to know the global composition of the community (Skjoldal et al., 2013). Moreover, the distribution of the zooplankton community is strongly influenced by climatic factors (Fernández de Puelles et al., 2004, 2008; Siokou-Frangou et al., 2010), thus the SSLs has to be framed into their environmental context to determine its principal environmental forcing.

In this study, our main objective was to determine the macroscale spatial distribution of the different zooplankton communities present in the Northern Alboran Sea. The achievement of this objective was carried out by verifying our working hypothesis which implied that the changes in the acoustic frequency response (Korneliussen and Ona, 2003) observed along the continental shelf (from coast to the edge) were due to changes in the composition of the zooplankton community. In order to be able to interpret the echograms collected at different frequencies (18, 38, 120 and 200 kHz) in terms of zooplankton communities, the SSL biological composition was determined by analyzing zooplankton samples collected by plankton nets. In addition, the suitability of acoustic methods for generating secondary production indicator maps is discussed.

The main contribution of this study is the application of acoustic methods, for the first time in the Mediterranean Sea, to obtain the spatial distribution of different zooplankton communities. This fact has a great ecological importance because it shows the different levels of complexity and organization of zooplanktonic communities on the continental shelf. The scope of this work does not subscribe only to the limits of the study area but also gives the keys to interpret echograms in terms of the zooplankton community collected in previous years in the same area and/or in adjacent areas. In addition, the distribution of zooplankton determines the presence and distribution of upper links of the trophic chain thus having a map of the distribution of possible prey can help to understand the distribution and behavior of potential predators. With the results provided, it is possible to interpret the data collected in acoustic stock assessment surveys, such as MEDIAS (MEDiterranean International Acoustic Survey) in a global context, integrating the main components of the ecosystem, fish and zooplankton.