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Sound use for orientation by marine fauna, an ecosystem approach considering anthropogenic noise

Final Report Summary - SOUNDMAR (Sound use for orientation by marine fauna, an ecosystem approach considering anthropogenic noise)

'Sound use in the marine ecosystem' (SOUNDMAR) is an international outgoing fellowship project funded by the European Union (EU)'s Marie Curie programme of the Seventh Framework Programme (FP7) for three years (2010 - 2013). SOUNDMAR fellow, Dr Natacha Aguilar de Soto, performed research at the Leigh Marine Laboratory of the University of Auckland (UOA, New Zealand) and at the Faculty of Biology of the University of La Laguna (ULL, Canary Islands, Spain). SOUNDMAR has contributed relevant results about baseline ecology, physiology and behaviour of cetaceans, and about the use of sound and the impact of noise in the marine ecosystem: from invertebrates to whales. For this, the fellow applied a multidisciplinary approach, from using multi-sensor digital tags to study the acoustic behaviour and ecology of whales to performing experiments in the laboratory to investigate the effects of noise exposure on invertebrate larvae. The research involved the collaboration of the fellow with researchers from New Zealand, United Kingdom (UK), Denmark, United States (US), Norway and Spain and resulted in 9 peer-reviewed publications (plus seven more to be submitted in 2013), which are summarised below. The work was presented in 27 contributions to 18 scientific meetings and international conferences in four continents. More information can be found at:

(1) Acoustic behaviour, ecology and ethophysiology of cetaceans (all papers cited are SOUNDMAR results)

Within SOUNDMAR we studied beaked whales and Bryde's whales with suction-cup attached acoustic and movement recording tags (DTAGs). Results were analysed together with data previously gathered by us of beaked and pilot whales and of bottlenose dolphins in the Canary Islands. This resulted in the publication of several papers describing the characteristics and use of the vocalisations of the species. The papers reported for first time the communication sounds of Blainville's beaked whales in the context of their diving behaviour (Aguilar Soto et al. 2012), showing that these whales have a cryptic vocal behaviour, vocalising only when deeper than 200 m. This behaviour limits the ability of shallow-diving predators such as killer whales to track Blainville's acoustically and provide a striking example of the evolutionary in?uence of the risk of predation on animal communication. Moreover, this evolution towards predator-avoidance might explain the strong reactions of these beaked whales to intense sounds like naval sonar, overlapping in frequency with killer whale vocalisations. This work showed that Blainville's beaked whales produce the deepest whistles ever recorded for cetaceans, defying the limits imposed by pressure at depth for a pneumatic sound production system. In contrast, the effects of pressure are evident in the reduction of the duration and source level of pilot whale contact calls at depth (Jensen et al. 2011). We also studied the characteristics of the echolocation clicks of bottlenose dolphins in different areas of the distribution of this cosmopolitan species (Walberg et al. 2011) and the use of clicks and the adaptation of prey search behaviour in the process of echolocation in beaked whales (Madsen et al. 2013). Knowledge about the vocal behaviour of the species allows us to monitor their distribution and abundance using acoustic surveys. Here we contributed important methodological advances to improve the analysis of acoustic survey data of beaked whales (Barlow et al. 2013). The acoustic ecology of beaked whales was the main theme of the PhD of P. Arranz at ULL, supervised by the SOUNDMAR fellow Dr Aguilar de Soto, with co-supervisors Dr Johnson (St. Andrews University, UK), Dr Madsen (Univ. Aarhus, Denmark) and Dr Brito (ULL). We used the clicks produced by tagged Blainville's beaked whales as a bio-echosounder. This provided data about the depth and rate of foraging of the whales, but also about the characteristics of their habitat, showing that these whales feed on mesopelagic and benthopelagic prey with specialised tactics (Arranz et al. 2011). To investigate habitat preferences of beaked whales in El Hierro we combined acoustic surveys of these species (Arranz et al. in prep) with visual surveys from land (Arranz et al. 2013), showing that in the waters around El Hierro beaked whales have a preference for the slope, where both of the foraging habitats of beaked whales (meso and benthopelagic) are readily accessible.

(2) Human impacts and conservation measures: from acoustic pollution to ship collisions

While behavioural or acute effects of underwater sound have been widely reported, for example by Science and Nature in cases of whales stranding in coincidence with naval sonar and seismic activities, there is little or no knowledge about possible long-term or population impacts, or about the impact of noise on the base levels of marine trophic webs, with potential consequences on the maintenance of ecosystem balance. Understanding the impact of noise on marine fauna at the population level requires knowledge about the vulnerability of different life stages. In SOUNDMAR we performed an experiment on the effect of low frequency noise on the development of marine larvae and provided, to our knowledge, the first evidence that noise exposure during larval development produces body malformations in marine invertebrates (Aguilar Soto et al. in press in Scientific Records). The experiment was performed as a response to strongly voiced concerns by Australian fishermen relating seismic surveys to mortality of scallops resulting in USD 70 million worth loses in scallop fisheries. Fishermen also reported scallop population declines a year after seismic surveys and claimed that it was due to decreased recruitment following the surveys. To investigate potential biological basis of these observations, we exposed scallop larvae to pre-recorded seismic pulses and monitored their development at the Leigh Marine Laboratory of University of Auckland. Noise-exposed larvae showed a significant developmental delay with respect to larvae in the non-exposed control group. In addition, at the end of the experiment 46 % of the exposed larvae showed body malformations, while no malformations were found in the control groups (4 881 larvae examined). Abnormalities may be caused by different mechanisms including mechanical or physiological stress and our results will stimulate research to identify noise-induced mechanisms that may be similar across different taxa. Underwater human activities such as seismic surveys, pile-driving, low-frequency sonar and blasting regularly introduce into the environment noise exceeding the levels tested in this study (160 dB re 1 µPa, 4-6 mm s-1 RMS), at spatial ranges that will vary for different sources and oceanographic conditions (e.g. c.10 km for blasting). In addition, the strong effects observed here suggest that abnormalities and growth delays may also result from lower sound levels or discrete exposures during the D-stage, increasing the potential for routinely-occurring anthropogenic noise sources to affect recruitment of wild scallop larvae in natural stocks. These results call for further research to define exposure thresholds and conditions at which noise may affect stock recruitment of wild scallops with important economic and ecological values. Shellfish and other invertebrates provide an important food source for different taxa and yield annually 12 million tons of fishing catches. It is important to define thresholds of effects of acoustic pollution on marine invertebrate populations and provide a scientific basis for the design of impact mitigation measures of human activities.

Noise also affects emblematic marine macrofauna such as beaked whales. Beaked whales live in small social groups and do not tend to mass strand under natural circumstances. However, mass strandings of beaked whales related to naval exercises have been recorded in many places of the world. Whales die with a characteristic pattern of multi-organic haemorrhages consistent with decompression sickness. The most accepted hypothesis explaining the strandings is a behavioural reaction of these extreme deep-diving whales to intense sonar used to detect submarines. The researcher participated in a collaborative effort aimed to uncover the physiological bases of decompression sickness in beaked whales (Hooker et al. 2011) and characterised the communication sounds of Blainville's whales, showing that they overlap in frequency range with mid-frequency sonar related to strandings (Aguilar Soto et al. 2012). It is unknown if mass strandings related to sonar may pose a population level threat for beaked whales. To assess this it is necessary to obtain abundance and connectivity data of local populations. The fellow in SOUNDMAR discovered the existence of rare coastal populations of beaked whales off El Hierro, in the Canary Islands. This has allowed a longitudinal population study showing that both Cuvier´s and Blainville's beaked whales populations in El Hierro are formed by transient and island-associated individuals. The populations are small (some 100 whales) and thus could be seriously compromised by a mass-mortality resembling that recorded in 2002 in the eastern Canary Islands. The SOUNDMAR fellow was part of the collaborative scientific and political effort that ended these mortalities in 2004, when the Spanish Ministry of Defence adopted a voluntary moratorium to the use of naval sonar within 50 nm of the archipelago. Now, the fellow is part of an ACCOBAMS (United Nations Agreement for the Conservation of Small Cetaceans in the Black and Mediterranean Seas) initiative to prevent mass mortalities of beaked whales in the Mediterranean in relation to naval exercises (Aguilar de Soto et al. in prep).

Ship strikes are another important factor of anthropogenic impact on cetaceans. Passive acoustic monitoring of whale vocalisations is used to inform ships of the position of the whales. In SOUNDMAR we performed a study with acoustic tags of Brydes' whales in the Hauraki Gulf (New Zealand) where ship collisions constitute the highest factor of human impact for this protected species. Results provided the first quantification of the foraging behaviour of this species (Aguilar de Soto et al. in prep.) and based the design of impact-risk mitigation measures for ship-strikes in the Gulf. These measures are being developed in a social forum involving stakeholders from the government, academy, shipping companies and social groups (Constantine et al. in prep.).