Natalie A. Moltschaniwskyj

Phase Shifts, Herbivory, and the Resilience of Coral Reefs to Climate Change

Many coral reefs worldwide have undergone phase shifts to alternate, degraded assemblages because of the combined effects of over-fishing, declining water quality, and the direct and indirect impacts of climate change. Here, we experimentally manipulated the density of large herbivorous fishes to test their influence on the resilience of coral assemblages in the aftermath of regional-scale bleaching in 1998, the largest coral mortality event recorded to date. The experiment was undertaken on the Great Barrier Reef, within a no-fishing reserve where coral abundances and diversity had been sharply reduced by bleaching. In control areas, where fishes were abundant, algal abundance remained low, whereas coral cover almost doubled (to 20%) over a 3 year period, primarily because of recruitment of species that had been locally extirpated by bleaching. In contrast, exclusion of large herbivorous fishes caused a dramatic explosion of macroalgae, which suppressed the fecundity, recruitment, and survival of corals. Consequently, management of fish stocks is a key component in preventing phase shifts and managing reef resilience. Importantly, local stewardship of fishing effort is a tractable goal for conservation of reefs, and this local action can also provide some insurance against larger-scale disturbances such as mass bleaching, which are impractical to manage directly.

Patterns of recruitment and abundance of corals along the Great Barrier Reef

Different physical and biological processes prevail at different scales. As a consequence, small-scale experiments or local observations provide limited insights into regional or global phenomena. One solution is to incorporate spatial scale explicitly into the experimental and sampling design of field studies, to provide a broader, landscape view of ecology. Here we examine spatial patterns in corals on the Great Barrier Reef, across a spectrum of scales ranging from metres to more than 1,700 km. Our study is unusual because we explore large-scale patterns of a process (recruitment by juveniles) as well as patterns of adult abundance, revealing the relationship between the two. We show that coral-reef assemblages that are similar in terms of abundance may nonetheless show profound differences in dynamics and turnover, with major implications for their ecology, evolution and management.

Development of shy/bold behaviour in squid: context-specific phenotypes associated with developmental plasticity

Animals often differ from one another in their willingness to take risks in a number of functional contexts related to fitness (e.g. mating, dispersal, and foraging behaviour). Although several studies have reported life history correlates and selective consequences of this variation in shy/bold behaviour, little attention has been paid to developmental processes resulting in shy/bold phenotypes. Here, we present a lifetime developmental study of shy/bold behaviour in dumpling squid, Euprymna tasmanica. Behaviour was measured in two test contexts, a threat and a feeding test, at five times across the entire life span. Across test contexts, shy/bold behaviour was not correlated at any age; while within a test context, individual shy/ bold phenotypes were consistent both before and after sexual maturity. During sexual maturity, different phenotypes displayed different amounts of developmental variation; shyer animals were more plastic in feeding tests, while bolder animals were more plastic in threat ones. Our results suggest that for some animals shy/bold behaviour throughout development is uncorrelated across different contexts related to risk, while within a context, there may still be developmental constraints to changing shy/bold behaviour. This constraint within a functional context, however, may be phenotype-specific, with some phenotypes able to change more than others. These results indicate that a greater understanding of developmental pathways is needed to determine whether shy/bold phenotypes per se are the sole focus of selection. Differences in developmental plasticity between shy/bold phenotypes may also confer differential fitness in fluctuating environments.

Heritability and fitness-related consequences of squid personality traits

Dumpling squid, Euprymna tasmanica, show consistent individual differences in behaviour that can be classified according to indices reflecting shy–bold, activity and reactivity responses. Using crosses of wild‐caught single males to multiple females with known behavioural phenotypes, this study estimated patterns of additive genetic and residual variance in these behavioural traits from offspring of squid in two contexts, a threat (antipredator) and feeding (foraging) test. Genetic contributions to behavioural expression were dependent on test context. Behaviours in antipredator contexts had significant heritabilities (h2 = 0.2–0.8) while behaviours from foraging contexts had lesser additive genetic and greater residual components (h2 = 0.05–0.08). Personality trait variation in females was not related to her fecundity. Female boldness in foraging situations, which co‐varied with body size, explained small but significant variation (∼21%) in brood hatching success, while successful fertilization was determined by positive assortion of mate pairs according to their shy–bold phenotype. These results are discussed in terms of the ecological and evolutionary significance of animal ‘personality’ traits in wild populations of animals.

Personality Traits in Dumpling Squid (Euprymna tasmanica): Context-Specific Traits and Their Correlation With Biological Characteristics

Personality traits are a major class of behavioral variation often observed within populations of animals. However, little is known of the integration between personality and an individuals underlying biology. To address this, the authors measured personality traits in squid (Euprymna tasmanica) in 2 contexts while also describing trait correlates with biological parameters. Four traits (shy avoidance- bold aggression, activity, bury persistence, and reactivity) were reliably measured; however, trait expression between contexts was not correlated and thus was context-specific. Trait variation was not a function of gender or of somatic or reproductive condition but was explained partially by a squids sexual maturity and its size. Results are discussed in terms of the interplay between personality variation and resulting life history strategies in animals.

Detecting regional variation using meta-analysis and large-scale sampling: latitudinal patterns in recruitment

Regional-scale variation of recruitment by marine organisms may reflect geographic patterns in adult stock sizes or fecundities, large-scale hydrodynamic features that influence the transport of larvae (e.g., currents, upwelling), and patterns of early mortality. In turn, recruitment may play a vital role in determining patterns of adult abundance and community structure, from local to biogeographic scales. We examined spatial variation in recruitment by corals at a regional scale, along 3300 km of the tropical and subtropical coast of eastern Australia (10°–31° S). We used two complementary approaches: (1) a metaanalysis of 21 different studies undertaken over a 16-yr period, each of which was generally conducted at a single reef, and (2) a large-scale sampling effort in which recruitment was measured in two years on 33 reefs arrayed along the length of the Great Barrier Reef (GBR). Our goal is to compare the emergent large-scale picture derived from many small-scale studies with patterns revealed by shorter-term regional sampling. The two approaches show very similar large-scale patterns. Recruitment by spawning corals (mainly acroporids) was highest in the central GBR and declined steadily with increasing latitude by up to more than 20-fold. A smaller decline occurred on the northern GBR between Australian and Papua New Guinea. Recruitment by brooding corals (mostly pocilloporids) was greatest in the northern GBR and also declined to the south. The latitudinal decline in brooders was three-to fivefold, i.e., not as great as for spawners. Consequently, the proportion of brooded recruits increased to the south, and they generally exceeded spawners on the southern GBR and on isolated subtropical reefs at higher latitudes. Our meta-analysis shows that fully half of the variation in the ratio of spawners to brooders is attributable to one of 11 variables that we extracted from the published studies: the month when the recruitment panels were deployed. This result suggests that the intensity and timing of spawning have a crucial impact on large-scale patterns of recruitment. Elsewhere, we tested this hypothesis in the field, and confirmed that regional variation in recruitment by spawning acroporid corals was driven by spatial and temporal variation in the extent of mass spawning. Together, large-scale sampling and meta-analyses provide a powerful, combined approach for investigating large-scale patterns and the mechanisms underlying them.

Ethical and welfare considerations when using cephalopods as experimental animals

When using cephalopods as experimental animals, a number of factors, including morality, quality of information derived from experiments, and public perception, drives the motivation to consider welfare issues. Refinement of methods and techniques is a major step in ensuring protection of cephalopod welfare in both laboratory and field studies. To this end, existing literature that provides details of methods used in the collection, handling, maintenance, and culture of a range of cephalopods is a useful starting point when refining and justifying decisions about animal welfare. This review collates recent literature in which authors have used cephalopods as experimental animals, revealing the extent of use and diversity of cephalopod species and techniques. It also highlights several major issues when considering cephalopod welfare; how little is known about disease in cephalopods and its relationship to senescence and also how to define objective endpoints when animals are stressed or dying as a result of the experiment.

Inter-annual plasticity of squid life history and population structure: ecological and management implications

Population size and structure, as well as individual growth rates, condition, and reproductive output, respond to environmental factors, particularly in short-lived and fast-growing squid species. We need to understand the mechanisms through which populations respond to environmental conditions, to predict when or if established relationships, used as management tools to forecast recruitment strength, might break down completely. Identifying characteristics of successful recruits who have grown under different environmental scenarios may improve our understanding of the mechanistic connections between environmental conditions and the temporal variation in life history characteristics that ultimately affect recruitment. This 5-year study sought to determine the association between key life history characteristics of southern calamary Sepioteuthis australis (growth rate, body size, and patterns of repro-somatic energy allocation) and the environmental conditions experienced by individuals on the east coast of Tasmania, Australia. Among years, all population and individual parameters examined were highly variable, despite the environmental regime during the study not encompassing the extremes that may occur in this dynamic region. Temperature was not clearly associated with any of the individual or population differences observed. Populations of apparently similar abundance were composed of individuals with strikingly different biological characteristics, therefore seeking relationships between abundance and environmental parameters at gross levels did not shed light on the mechanisms responsible for population size. Importantly, inter-annual differences in squid size, condition, reproductive investment, and possibly growth rate, were sex-specific, indicating that males and females responded differently to similar factors. Among years differences in body size were extreme, both among the male component of the population and between genders. The relative importance of many size-based processes that contribute to population size and structure (e.g. predation, starvation, competition, and reproductive success) will therefore vary inter-annually.

Multiple spawning in the tropical squid Photololigo sp.: what is the cost in somatic growth?

This study assesses the potential of the tropical loliginid squid Photololigo sp. to lay multiple batches of eggs and examines changes in somatic growth during reproduction. Histological analysis of the ovary and the relative size of the oviduct to mantle weight and ovary weight were used to determine the potential for multiple spawning. Ovaries of mature females always had immature and mature oocytes present, suggesting that not all the oocytes were maturing simultaneously and that multiple batches of eggs were being produced. Furthermore, poor correlations of oviduct weight with body size and ovary weight indicated that mature oocytes were not accumulating in the oviduct for a single spawning event. Both these observations supported the hypothesis that Photololigo sp. has the potential to lay multiple batches of eggs throughout its life. Specific growth rates, length-weight relationships, relative growth of somatic and reproductive tissue and microscopic assessment of muscle tissue were compared between immature and mature females. Growth rates of immature females were almost twice as fast as those of mature females. Mature females also had no large muscle fibres present, suggesting that energy for reproduction was mobilised from the muscle tissue.

Are behavioral syndromes invariant? Spatiotemporal variation in shy/bold behavior in squid

Behavioral syndromes are correlated suites of behavior, analogous to human personality traits. Most work to date has been taken from limited “snapshots” in space and time, with the implicit assumption that a behavioral syndrome is an invariant property, fixed by evolutionary constraints or adaptations. However, directional selection on two mechanistically independent traits (selective covariance) could also result in correlated behaviors. Previously, we have shown that shy/bold behavior in Southern dumpling squid (Euprymna tasmanica) across predator encounter and feeding risk contexts is genetically and phenotypically uncoupled, and hence potentially free to vary independently. Here, we collected data on shy/bold behaviors from two independent wild populations of squid in two different years to test whether behavioral correlations across these same two functional contexts vary through time and space. We detected significant influences of population, sex, and body size on the expression of boldness in squid within each functional context, and this was coupled with significant differences in relative population density and adult sex ratio. Despite these changes in behavior and demographic parameters, we found that correlations between boldness scores across the two functional contexts were largely absent in both wild populations of squid in both years. Our work suggests that some animal groups may be largely characterized by context-specific behavioral expression. A theoretical framework which conceptualizes behavioral syndromes resulting from context-specific behavioral rules may be needed to fully understand why behaviors are sometimes correlated, and why sometimes they are not.