Category: Effects

What is Behavioral ecology and why should we care?

The natural world is organized into a nested hierarchy; genes are nested within individuals, individuals within populations, populations within communities, etc. As ecologists, we are often interested in understanding how biotic and abiotic components of the environment and their interactions affect the abundance and distribution of living organisms, and in turn, the flows of nutrients and energy through an ecosystem. Consequently, higher levels of organization (populations and communities) have traditionally captivated much of the attention by ecologists, where population- and community-ecology typically treat individuals as being more-or-less ecologically equivalent. However, variation in traits, such as behavior, morphology, physiology, among individuals of the same species, sometimes even within the same population can exceed the variation observed among species by as much as 200%! (Ref). Moreover, because natural selection occurs at the individual level, studying the fitness consequences of individual variation can help bridge the divide between ecological and evolutionary processes (Bolnick et al. 2011). This is precisely the aim of behavioral ecology– to study how natural selection shapes behavior. As many of the ecological processes are explicitly behavioral, including habitat selection, predator-prey interactions, inter- and intra-specific competition, knowledge about how natural selection shapes behavior is critical to understand how the environment shapes, and is shaped by, behavioral interactions among individuals. This knowledge is fundamental to our understanding and ability to mitigate the potential impacts resulting from human-induced rapid ecological changes (HIREC; Robertson et al. 2013; Macdonald 2016).

Ecological novelty and the yin and yang of behavior

are defined as anthropogenically driven changes (e.g. habitat loss, climate change, the spread of exotic/invasive species including diseases) to an ecosystem or biosphere that occur at a historically rapid pace (Sih et al. 2011). Because behavior is the fastest, most flexible, and reversible way for an individual to respond to environmental change, behavior can act to moderate, or amplify the effects of ecological novelty, depending on the predictability of environmental variation (Myers and Bull 2002) and the preference for a behavioral option to increase relative to its fitness value (Roberston et a. 2013). The most apparent way in which behavior can amplify the effects of ecological novelty is through behaviorally mediated trophic cascades (Schmitz et al. 1997) (Fig. 1). For example, when large carnivores are removed from a system, smaller meso-predators are ‘released’ from the fear of being eaten and shift their foraging behaviors, ultimately to the peril of organisms occupying lower trophic levels such as primary producers (vegetation) and consumers (herbivores) (Schmitz et al 1997, Estes et al. XXX). In this example, the ability of meso-predators to perceive and respond to altered cues in the environment by switching their foraging behavior is a form of behavioral flexibility. If this flexibility in foraging behavior confers some kind of fitness advantage to meso-predators, then this example shows how behavior can both amplify (by way of trophic cascade) and moderate (through population enhancement) the effects of ecological novelty, which was in our case the loss of a large carnivores. Alternatively, if behavioral flexibility caused a reduction in fitness, as would be the case if the cues used by meso-predators to sense danger had been altered or removed but the threat still remained, then this maladaptive behavioral flexibility could facilitate ecological novelty through the emergence of an ‘evolutionary trap’ (Sih 2004, Robertson et al. 2013).

Figure 1. Example of a novel ecosystem created from a behaviorally mediated trophic cascade. In the absence of cues from a large predator (gray silhouetted wolf), mesopredator abundance and foraging activity increased (black silhouetted raccoon), leading to a reduction in crabs (gray crab silhouette) which resulted in an increase in sculpin (crab competitor) and snails (crab prey). When predator cues were present (black silhouetted wolf), raccoons decreased foraging activities resulting in an increase in crab populations and a subsequent decrease in snails and sculpin. Figure adapted from Suraci et al. 2016 and inspired by Hobbs et al. 2009.

Ultimately, novel ecosystems exist along a continuum of human-induced rapid ecological change. As highlighted above, the ability of individuals to express different phenotypes (behavioral, physiological or morphological) across a range of environmental conditions – a phenomenon known as phenotypic flexibility – could prove advantageous or maladaptive in novel ecosystems depending on the accuracy of information (cues) that are available for individuals to predict future environmental conditions. Therefore, gradients of novelty can be used as natural ‘titration’ experiments to test theories about adaptive phenotypic plasticity. Such tests could provide valuable insight on the causes and consequences of phenotypic plasticity and generate ‘out-of-the-box’ solutions to conservation problems. A few examples of such creative solutions include: breeding programs that select for plastic genotypes, or training animals (https://www.youtube.com/watch?v=gSCr5OxXN1A) to perform novel behavioral tasks that could help them persist in the face of environmental challenges.

 

~by Chris Latimer~

Adaptation to ecological novelty: Can species keep pace?

 

“…I’m simply saying that life… finds a way.” -Dr. Ian Malcolm, Jurassic Park (1993)

 

Novelty is not new to life on Earth. Organisms have been adapting to novel challenges for millennia. But the key difference between adaptation over the evolutionary history of Earth and adaptation in recent history is the pace of change organisms have had to keep up with.

 

Populations can adapt to novel conditions by three principle means (Figure 1): 1) niche tracking, 2) phenotypic plasticity, and 3) adaptive evolution.

Figure 1. Modes of adaptation:

• Niche tracking involves avoiding the new environment, and could be generalized to any behavior that moderates the effect of a novel environment on fitness.
• Phenotypic plasticity occurs when phenotypic expression is flexible and can maintain fitness in either environment.
• Adaptive evolution involves changes in allele frequencies at loci that result in increased fitness in the new environment, often at the expense of fitness in the original environment.
• Note: Niche tracking and phenotypic plasticity do not involve any evolutionary change, whereas adaptive evolution arises when populations become locally adapted to the new environment.

The ability to genetically adapt hinges on one thing: the availability of standing genetic variation on which natural selection can act. Adaptation over evolutionary time scales (thousands to millions of years) can occur by the generation of beneficial traits by gradual genomic changes ranging from whole genome duplications to point mutations. But adaptation on ecological time scales (tens to hundreds of years) requires adaptive genetic variation to already be available prior to the environmental shift, clearly presenting a challenge for adaptation to novelty on ecological timescales. This challenge can be overcome by species with large population sizes and short generation times, such as some arthropods, marine species, microbes, and plants, because adaptive mutations arise more frequently, and are less likely to be lost due to demographic changes (Figure 2). But many species, particularly those of conservation concern, will not have the genetic capacity to keep pace with ecological change.

 

Despite the rapid pace of changes in biotic and abiotic factors, many contemporary evolutionary success stories have emerged. A significant proportion of these stories involve species that are considered invasive or pests, but many less negatively-charged examples also exist. For example:

• Eurasian blackcaps have exhibited genetic changes in migratory behavior to utilize more northerly wintering habitat (Berthold et al. 1992) while great tits have evolved greater plasticity of reproductive timing to better synchronize with changing seasonal food availability (Nussey et al. 2005);
• Peppered moths and field mice have rapidly evolved color polymorphisms to avoid predation in novel environments (Grant & Wiseman 2002, Linnen et al. 2009)
• Marine phytoplankton evolved higher heat tolerances under experimental warming conditions (Listmann et al. 2016) while rapid evolution of salt-tolerance in marine zooplankton has facilitated expansion into freshwater habitats (Lee 2016);
• Several plant species have rapidly evolved heavy-metal tolerance, enabling colonization of polluted mine tailings (Wu et al. 1975, Baker et al. 1986).

 

Among drivers of rapid change, climate change is particularly concerning, as the majority of adaptive responses thus far have not involved genetic changes in thermal physiology, but rather, thermal niche tracking (Bradshaw & Holzapfel 2006). If trends continue, species with long generation times, poor dispersal abilities, and small population sizes may not be able to adapt to warming temperatures, particularly in the tropics (Parmesan 2006, Huey et al. 2012), and cold-adapted species may run out of niche space to track. Life as we know it may not always be able to find a way.

 

In addition to the challenge of the pace of contemporary environmental change, overall loss of habitat in human-dominated landscapes has exerted downward pressure on population sizes, making adaptive evolution in many species highly unlikely. For these species, persistence may require substantial conservation effort. Facilitated migration and habitat conservation and restoration may buy species time to evolve. Controlled breeding may help maintain effective population sizes, though some have raised concerns over the potential for outbreeding depression (Frankham 2010), and some species may already have crossed the point of no return.

 

More controversial actions such as facilitating “adaptive introgression” (Hamilton & Miller 2016), the genetic exchange from adapted to maladapted species, may be necessary to increase standing genetic variation for adaptive evolution. Much excitement now surrounds emergent technologies once relegated to science fiction novels, such as genome editing facilitated by CRISPR/Cas9, which could enable direct insertion of adaptive alleles into struggling populations. However, we must be cautious of “techno-arrogance” that addresses symptoms while ignoring causes of species declines, and ultimately promises more than it can deliver (Meffe 1993).

 

On a hopeful note, many species likely already possess the standing genetic variation necessary to maintain fitness in the increasingly novel environmental space they occupy. Whether these are the species we want to be the evolutionary “winners” in the era of ecological novelty, however, remains an open question. Life may yet find a way, but the fate of some species may ultimately be in our hands.

~By Michael Crossley~

References

Baker et al. (1986) Induction and loss of cadmium tolerance in Holcus lanatus L. and other grasses. New Phytologist 102, 575-587.

Berthold et al. (1992) Rapid microevolution of migratory behavior in a wild bird species. Nature 360, 668-670.

Bradshaw & Holzapfel (2006) Evolutionary response to rapid climate change. Science 312, 1477-1478.

Frankham (2010) Challenges and opportunities of genetic approaches to biological conservation. Biological Conservation 143, 1919-1927.

Grant & Wiseman (2002) Recent history of melanism in American peppered moths. Journal of Heredity 93, 86-90.

Hamilton & Miller (2016) Adaptive introgression as a resource for management and genetic conservation in a changing climate. Conservation Biology 30, 33-41.

Huey et al. (2012) Predicting organismal vulnerability to climate warming: roles of behavior physiology and adaptation. Philosophical Transactions of the Royal Society of Britain 367, 1665-1679.

Lee (2016) Evolutionary mechanisms of habitat invasions, using the copepod Eurytemora affinis as a model system. Evolutionary Applications 9, 248-270.

Linnen et al. (2009) On the origin and spread of an adaptive allele in deer mice. Science 325, 1095-1098.

Listmann et al. (2016) Swift thermal reaction norm evolution in a key marine phytoplankton species. Evolutionary Applications (in press)

Meffe GK (1993) Techno-arrogance and halfway technologies: Salmon hatcheries on the Pacific Coast of North America. Conservation Biology 6, 350-354.

Nussey et al. (2005) Selection on heritable phenotypic plasticity in a wild bird population. Science 310, 304-306.

Parmesan (2006) Ecological and evolutionary responses to recent climate change. Annual Reviews of Ecology, Evolution, and Systematics 37, 637-669.

Wu et al. (1975) The potential for evolution of heavy metal tolerance in plants. III. The rapid evolution of copper tolerance in Agrostis tenuis. Heredity 34, 165-187.

Trying to see the invisible: what are the consequences of behavioral changes along gradients of novelty?

Abstract: Ecological novelty can be both cause and result of behavioral changes in animals. These behavioral changes can be subtle, but are likely widespread, and could have large effects on communities and ecosystems. While animal behavior can vary tremendously across space and time, I highlight three general themes regarding novelty and behavior. First, animal behavior can either create novelty, or respond to other drivers of novelty. Second, behavioral responses to novelty can either harm or benefit humans. Third, it is difficult to predict behaviors in high-novelty systems, because of the emergence of new behaviors in very novel systems. While there is considerable uncertainty surrounding the relationship of animal behavior and novelty, conducting behavioral ecology experiments across novelty gradients, and integrating known behavioral responses to novelty into forecasts of ecological change could improve predictions of the consequences of animal behavior in future habitats.

 

Most ecological research is based on observing and counting organisms. For example, if we know that there are 50 deer in Area A, but 10 deer in Area B, we might hypothesize that the 50 deer in Area A have a larger impact on their habitat than the 10 deer in Area B, perhaps by eating more plants or excreting more nitrogen.

However, abundance can provide a misleading measure of a population’s impact, because individuals within a species can behave very differently. In our deer example, the presence of a predator in Area A would lead deer there to spend more time watching for potential threats and less time eating. Similarly, the presence of a competitor in Area A could cause deer to avoid high-quality food patches, creating differences in diet and space use between habitats. While behavioral variation can complicate ecological monitoring and data collection, properly considering animal behavior has the potential to improve conservation efforts (Caro 2007).

Ecological novelty is not only changing where organisms are or how many organisms there are—novelty can also change how organisms behave, and behavioral novelty may precedes taxonomic novelty. Ecological novelty can alter behavior, regardless of whether populations increase, decrease, or stay the same. In turn, behavioral changes can alter community composition and ecosystem function. Below, I explore three general themes regarding ecological novelty and animal behavior, using examples from multiple study systems to illustrate the widespread links between novelty and behavior.

1: Behavior can either drive novelty or respond to novelty

Introduced animals might possess novel behaviors that rapidly change an ecosystem. For example, invasive Pacific lionfish hunt by herding their prey into corners and producing jets of water to disorient them. Prey in the native range of lionfish have evolved behavioral responses to this unique predator over many generations, but prey in the introduced range of lionfish are naïve to these tactics. Hence, prey often experience rapid population declines in habitats invaded by lionfish (Albins 2013). Alternatively, native animals may alter their behavior in response to novelty. For example, the dense growth of invasive shrubs reduces the predation risk experienced by deer, leading deer to select invaded forests over uninvaded forests. As deer aggregate under invasive shrub cover, tick survival increases, potentially posing risks to human health (Allan et al. 2010). Whether animal behavior causes novelty, or represents a response to other drivers of novelty could be an important distinction for managers trying to limit novelty. Animals whose behavior creates novelty may need to be eradicated or reduced to reach management goals, whereas animals whose behavior is a response to novelty may be left in place, if the driver of novelty is addressed.

2: Behavioral responses to novelty can either increase or decrease ecosystem services

Species vary tremendously in their functional roles and behavioral responses to novelty. In a New Mexico forest, novel noise pollution from natural gas wells reduced the efficiency of many predators, which has mixed results for human society (Francis et al. 2012). Hummingbirds respond to gas wells by increasing pollination, benefitting flowering plants. At the same time, mice respond by increasing seed predation, which limited pine regeneration. Novelty might also have no effect on animal behavior: migratory birds in Jamaica suppress insect pests even as forest conversion to agriculture intensifies (Kellermann et al. 2008). Idiosyncratic responses to novelty may frustrate land managers when they present difficult trade-offs between opposing ecosystem services. Consequently, it will be important to identify the species primarily responsible for key ecosystem services, and to quantify behavioral changes in these species along gradients of novelty. With more studies, it may be possible to generalize which services increase, decrease, or stay the same along novelty gradients.

Figure 1. Comparison of a forest understory invaded by Lonicera maackii, or bush honeysuckle (left) and an understory with the invasive shrub removed. Invasive shrubs shade out many native wildflowers and tree seedlings, but can also drastically change animal behavior, because their dense growth creates a safe refuge from predators. Photo credit: The Nature Conservancy of Kentucky

3: Behavior in high-novelty systems cannot be inferred from behavior in low-novelty systems

Some species are widely distributed along gradients of novelty, but might exhibit unique behaviors under highly novel conditions. For example, invasive Argentine ants expand their diet to include plants, creating colonies with a lower trophic position than in their native range (Tillberg et al. 2007). Similarly, an exotic predator causes waterfowl in Poland to form larger breeding colonies and nest in developed areas, behaviors that were historically rare (Brzezinski et al. 2012). These abrupt changes make it is unwise to predict behavior in highly novel habitats using data collected under low-novelty conditions.

Figure 2. Animals exhibit variable responses to novelty. Because of this, as novelty increases, ecosystem services may increase, decrease, or remain constant.

Where do we go from here?

The potential for behavioral changes to produce rapid and unanticipated ecological change in highly novel systems is daunting for many ecologists and conservationists. I highlight two approaches that could be used to better understand the relationship between behavior and novelty.

1: Use experiments to measure behavioral responses to novelty

Observational data is valuable, but may not fully capture high degrees of novelty expected in future habitats. Rather, experimental manipulations may be better suited to explore behavioral responses to increased novelty, particularly when control treatments are carefully selected. Examples of possible experiments (reviewed by Knowlton and Graham 2010) include exposing organisms to novel stimuli (playback experiments), novel climates (translocation experiments), or novel habitat structure (constructing/removing corridors). Integrating behavioral experiments into research programs conducted at a large spatial or temporal extent (NEON, LTER, Nutrient Network) could be particularly valuable for advancing our understanding of how behavioral changes might influence communities and ecosystems.

2. Incorporate behavioral mechanisms in species distribution models

Communities will change substantially over the next century as novelty increases. A common approach taken to predict these changes is to project species distributions onto future climate or land-use scenarios, but this approach ignores the potential for unprecedented animal behavior to emerge when novelty is high (Conley et al. 2011). Instead, a more fruitful (yet challenging) approach would be to measure behavioral changes along gradients of novelty, and then explicitly account for these behavioral changes in species distribution and disease risk models. Doing so could improve our ability to forecast the novel species assemblages of the Anthropocene, and the ecosystem services they provide.

 

References

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