Colin D. MacLeod

A review of cephalopod—environment interactions in European Seas

Cephalopods are highly sensitive to environmental conditions and changes at a range of spatial and temporal scales. Relationships documented between cephalopod stock dynamics and environmental conditions are of two main types: those concerning the geographic distribution of abundance, for which the mechanism is often unknown, and those relating to biological processes such as egg survival, growth, recruitment and migration, where mechanisms are sometimes known and in a very few cases demonstrated by experimental evidence. Cephalopods seem to respond to environmental variation both ‘actively’ (e.g. migrating to areas with more favoured environmental conditions for feeding or spawning) and ‘passively’ (growth and survival vary according to conditions experienced, passive migration with prevailing currents). Environmental effects on early life stages can affect life history characteristics (growth and maturation rates) as well as distribution and abundance. Both large-scale atmospheric and oceanic processes and local environmental variation appear to play important roles in species–environment interactions. While oceanographic conditions are of particular significance for mobile pelagic species such as the ommastrephid squids, the less widely ranging demersal and benthic species may be more dependent on other physical habitat characteristics (e.g. substrate and bathymetry). Coastal species may be impacted by variations in water quality and salinity (related to rainfall and river flow). Gaps in current knowledge and future research priorities are discussed. Key research goals include linking distribution and abundance to environmental effects on biological processes, and using such knowledge to provide environmental indicators and to underpin fishery management.

Linking sandeel consumption and the likelihood of starvation in harbour porpoises in the Scottish North Sea: could climate change mean more starving porpoises?

Sandeels are known to be negatively affected by climate change in a number of ways. This study investigated whether these changes are affecting the harbour porpoise (Phocoena phocoena), a species which consumes sandeels. Porpoise diet was examined in spring (March–May), a critical time of year for survival when sandeels are important prey, from 1993 to 2001 to provide baseline information on the proportion of sandeels consumed. When data from spring 2002 and 2003 were compared to these baseline data, the diet was found to be substantially different, with a significant and substantially smaller proportion of sandeels being consumed in March and May. There were also differences in the number of porpoises starving between the two time periods (33% in spring 2002 and 2003 died of starvation, but only 5% in the baseline period). This suggests that a lower proportion of sandeels in the diet of porpoises in spring increases the likelihood of starvation. Therefore, we suggest that the negative effects of climate change on sandeel availability may have serious negative effects on harbour porpoise populations in the North Sea by increasing the likelihood of starvation in spring.

A comparison of approaches for modelling the occurrence of marine animals

Approaches for modelling the distribution of animals in relation to their environment can be divided into two basic types, those which use records of absence as well as records of presence and those which use only presence records. For terrestrial species, presence–absence approaches have been found to produce models with greater predictive ability than presence-only approaches. This study compared the predictive ability of both approaches for a marine animal, the harbour porpoise (Phoceoena phocoena). Using data on the occurrence of harbour porpoises in the Sea of Hebrides, Scotland, the predictive abilities of one presence–absence approach (generalised linear modelling—GLM) and three presence-only approaches (Principal component analysis—PCA, ecological niche factor analysis—ENFA and genetic algorithm for rule-set prediction—GARP) were compared. When the predictive ability of the models was assessed using receiver operating characteristic (ROC) plots, the presence–absence approach (GLM) was found to have the greatest predictive ability. However, all approaches were found to produce models that predicted occurrence significantly better than a random model and the GLM model did not perform significantly better than ENFA and GARP. The PCA had a significantly lower predictive ability than GLM but not the other approaches. In addition, all models predicted a similar spatial distribution. Therefore, while models constructed using presence–absence approaches are likely to provide the best understanding of species distribution within a surveyed area, presence-only models can perform almost as well. However, careful consideration of the potential limitations and biases in the data, especially with regards to representativeness, is needed if the results of presence-only models are to be used for conservation and/or management purposes.

The habitat preferences of marine mammals west of Scotland (UK)

This study used classification and regression trees (CART) to investigate and compare the habitat preferences of marine mammals in this area. Data were collected in early summer (June/July) in 2004 and 2005 and the distribution of marine mammal species was compared to 10 ecogeographic variables (EGVs). Of 13 species of marine mammals sighted during the study, there were sufficient sightings to examine the habitat preferences of seven. For all species a measure of ‘shelf tendency’ (distance to coast or water depth) was an important variable and the species could be separated into two groups, the deep-water species and the shelf species, with little overlap between them. The occurrence of both deep-water species (long-finned pilot whales and Atlantic white-sided dolphins) was also related to dynamic variables such as sea surface temperature (SST) or primary productivity. Two of the shelf species (northern minke whales and grey seals) were only linked to topographic variables and were limited to quite specific habitats. A third species (harbour porpoise) was primarily related to topographic variables, but in the shallowest waters was also related to local variation in SST. The occurrence of the final two species (common and white-beaked dolphins) was linked to SST and local primary productivity. However, while both species preferentially occurred in areas with higher productivity, the two species differed in their preference for SST, with common dolphins preferentially occurring in warmer waters and whitebeaked dolphins in colder waters.

Breaking symmetry: The marine environment, prey size, and the evolution of asymmetry in cetacean skulls

Skulls of odontocetes (toothed whales, including dolphins and porpoises) are typified by directional asymmetry, particularly in elements associated with the airway. Generally, it is assumed this asymmetry is related to biosonar production. However, skull asymmetry may actually be a by‐product of selection pressure for an asymmetrically positioned larynx. The odontocete larynx traverses the pharynx and is held permanently in place by a ring of muscle. This allows prey swallowing while remaining underwater without risking water entering the lungs and causing injury or death. However, protrusion of the larynx through the pharynx causes a restriction around which prey must pass to reach the stomach. The larynx and associated hyoid apparatus has, therefore, been shifted to the left to provide a larger right piriform sinus (lateral pharyngeal food channel) for swallowing larger prey items. This asymmetry is reflected in the skull, particularly the dorsal openings of the nares. It is hypothesized that there is a relationship between prey size and skull asymmetry. This relationship was examined in 13 species of odontocete cetaceans from the northeast Atlantic, including four narrow‐gaped genera (Mesoplodon, Ziphius, Hyperoodon, and Kogia) and eight wide‐gaped genera (Phocoena, Delphinus, Stenella, Lagenorhynchus, Tursiops, Grampus, Globicephala, and Orcinus). Skulls were examined from 183 specimens to assess asymmetry of the anterior choanae. Stomach contents were examined from 294 specimens to assess prey size. Results show there is a significant positive relationship between maximum relative prey size consumed and average asymmetry relative to skull size in odontocete species (wide‐gape species: R2 = 0.642, P = 0.006; narrow‐gape species: R2 = 0.909, P = 0.031). This finding provides support for the hypothesis that the directional asymmetry found in odontocete skulls is related to an aquatic adaptation enabling swallowing large, whole prey while maintaining respiratory tract protection. Anat Rec, 290:539–545, 2007.

Mass-dependent predation risk and lethal dolphin–porpoise interactions

In small birds, mass-dependent predation risk (MDPR) is known to make the trade-off between avoiding starvation and avoiding predation dependent on individual mass. This occurs because carrying increased fat reserves not only reduces starvation risk but also results in a higher predation risk due to reduced escape flight performance and/or the increased foraging exposure needed to maintain a higher body mass. In principle, the theory of MDPR could also apply to any animal capable of storing energy reserves to reduce starvation and whose escape performance decreases with increasing mass. We used a unique situation along certain parts of coastal Britain, where harbour porpoises (Phocoena phocoena) are pursued and killed but crucially not eaten by bottlenose dolphins (Tursiops truncatus), to investigate whether a MDPR effect can occur in non-avian species. We show that where high levels of dolphin ‘predation’ occur, porpoises carry significantly less energy reserves than would otherwise be expected and this equates to reducing by approximately 37% the length of time that a porpoise could survive without feeding. These results provide the first evidence that a mass-dependent starvation–predation risk trade-off may be a general ecological principle that can apply to widely different animal types rather than, as is currently thought, only to birds.

Gray whale ( Eschrichtius robustus ) in the Mediterranean Sea: anomalous event or early sign of climate-driven distribution change?

On 8 May 2010, a gray whale was sighted off the Israeli Mediterranean shore and twenty-two days later, the same individual was sighted in Spanish Mediterranean waters. Since gray whales were last recorded in the North Atlantic in the 1700s, these sightings prompted much speculation about this whales population origin. Here, we consider three hypotheses for the origin of this individual: (1) it represents a vagrant individual from the larger extant population of gray whales found in the eastern North Pacific; (2) it represents a vagrant individual from the smaller extant population found in the western North Pacific; or (3) it represents an individual from the previously thought extinct North Atlantic population. We believe that the first is the most likely, based on current population sizes, on known summer distributions, on the extent of cetacean monitoring in the North Atlantic and on the results of a performed route analysis. While it is difficult to draw conclusions from such singular events, the occurrence of this individual in the Mediterranean coincides with a shrinking of Arctic Sea ice due to climate change and suggests that climate change may allow gray whales to re-colonize the North Atlantic as ice and temperature barriers to mixing between northern North Atlantic and North Pacific biomes are reduced. Such mixing, if it were to become widespread, would have implications for many aspects of the marine conservation and ecology of these two regions.

Sustainable whale-watching tourism and climate change: towards a framework of resilience

Whale-watching tourism, currently worth

Cultural transmission of tool use by Indo-Pacific bottlenose dolphins (Tursiops sp.) provides access to a novel foraging niche

1 billion p.a. worldwide, depends upon the continued presence of whale, dolphin and porpoise species (collectively called cetaceans) within a specific area. Current evidence suggests that the distribution and/or abundance of cetaceans is likely to alter in response to continued changes in sea surface temperature with global climate change (GCC). This paper reviews how such changes may affect the sustainability of whale-watching operators from a resilience perspective. Potential implications include changes to the presence and frequency of cetacean species targeted and changes to lengths of tourism seasons to coincide with shifts in migration patterns. The review presents an interdisciplinary framework for evaluating the resilience of whale watching to changes in species occurrence, whereby resilience is the degree of change in cetacean occurrence experienced before tourist numbers fall below a critical threshold. The framework combines likelihood of observing a cetacean, trip type and tourist type, which when quantified could identify which operators are likely to experience a change in tourist numbers given a specific scenario of changing cetacean occurrence. In doing so, a step is taken towards providing a means by which resilience to GCC effects on cetacean species could potentially be provided.

Temperature-based summer habitat partitioning between white-beaked and common dolphins around the United Kingdom and Republic of Ireland

Culturally transmitted tool use has important ecological and evolutionary consequences and has been proposed as a significant driver of human evolution. Such evidence is still scarce in other animals. In cetaceans, tool use has been inferred using indirect evidence in one population of Indo-Pacific bottlenose dolphins (Tursiops sp.), where particular dolphins (‘spongers’) use marine sponges during foraging. To date, evidence of whether this foraging tactic actually provides access to novel food items is lacking. We used fatty acid (FA) signature analysis to identify dietary differences between spongers and non-spongers, analysing data from 11 spongers and 27 non-spongers from two different study sites. Both univariate and multivariate analyses revealed significant differences in FA profiles between spongers and non-spongers between and within study sites. Moreover, FA profiles differed significantly between spongers and non-spongers foraging within the same deep channel habitat, whereas the profiles of non-spongers from deep channel and shallow habitats at this site could not be distinguished. Our results indicate that sponge use by bottlenose dolphins is linked to significant differences in diet. It appears that cultural transmission of tool use in dolphins, as in humans, allows the exploitation of an otherwise unused niche.