11.7: Effect of the Environment - Biology

11.7: Effect of the Environment - Biology

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Learning Outcomes

Identify gene-environment interaction and how this impacts trait expression

Characteristics that are influenced by environmental as well as genetic factors are called multifactorial. The idea of “nature versus nurture” — in other words, the relative influence of genetics versus environmental factors — has been and still is debated. Just looking at the genes of a given organism will not determine how that organism will develop and act. Even identical twins will show different characteristics, depending on the environment in which they live. Everyone is a product of their environment as well as their genetics.

Even when influenced by the environment, phenotypes have a normal range of expression. For instance, human height varies based on nutrition and genetics, but not many people are shorter than 4½ feet or taller than 7 feet. The range of phenotypic possibilities is called the norm of reaction. Hydrangeas, for example, may be blue, pink, or purple, but they are never naturally orange. Hydrangeas are blue in acidic soil with available aluminum, and they are pink in alkaline soil without available aluminum.

You may have heard about PKU, a disorder caused by defects in a single gene coding for an enzyme that converts the amino acid phenylalanine to tyrosine. Newborns are tested for this defect very early in life (Figure 1), so that if the results are positive, they can be given a diet limiting phenylalanine ingestion. That way, the toxic buildup is prevented and the children can develop normally. PKU is an example in which environmental factors can modify gene expression.

Practice Question

Two identical twins (female) live in different parts of the country. One is very committed to a healthy lifestyle: not smoking, exercising regularly, eating a diet rich in fresh produce, and avoiding red meats and processed foods. The other is not as careful: she smokes, is overweight, and often eats fast and processed foods. They are aware that several women in their family have had breast cancer, and decide to consult a doctor about their odds of developing the disease. Which of the following statements by the doctor sounds most correct?

  1. As identical twins, you are genetically the same, so your chances of developing breast cancer are identical.
  2. The twin with the healthy lifestyle should not be terribly concerned, while the one with the unhealthy lifestyle is at a higher risk.
  3. Breast cancer has a genetic component, and the twins have identical genes, so they have the same genetic risk. However, environmental factors such as smoking, obesity, and consumption of red meat have been shown to increase the risk of cancer. While both twins should monitor themselves closely, the twin who smokes and is overweight may want to consider a healthier lifestyle to decrease her risk of breast cancer.

[practice-area rows=”2″][/practice-area]
[reveal-answer q=”41921″]Show Answer[/reveal-answer]
[hidden-answer a=”41921″]Option A is wrong; while it has been shown that certain genes may predispose people to cancer, there are many associations between environmental effects and cancer. Option B is also wrong; familial cancers have a genetic component which may or may not be balanced by a healthy lifestyle. Option C is the most correct answer; lifestyle choices are important, but genetic influences are to be taken seriously, especially if there is a family pattern associated with them.[/hidden-answer]

In Summary: Effect of the Environment

While genes and genetic causes play a large role in health and phenotypes, the environment also plays an important role. Understanding this can enable the treatment of some disorders, such as the case with PKU in which limiting the intake of phenylalanine can prevent toxic build up of this amino acid. Often the norm of reaction is set by genetic factors but ultimately determined by environmental exposures.

Metabolic adaptation to weight loss: implications for the athlete

Optimized body composition provides a competitive advantage in a variety of sports. Weight reduction is common among athletes aiming to improve their strength-to-mass ratio, locomotive efficiency, or aesthetic appearance. Energy restriction is accompanied by changes in circulating hormones, mitochondrial efficiency, and energy expenditure that serve to minimize the energy deficit, attenuate weight loss, and promote weight regain. The current article reviews the metabolic adaptations observed with weight reduction and provides recommendations for successful weight reduction and long term reduced-weight maintenance in athletes.

Investigating the effects of environmental factors on autism spectrum disorder in the USA using remotely sensed data

This study aimed to assess the association between exposures to outdoor environmental factors and autism spectrum disorder (ASD) prevalence in a diverse and spatially distributed population of 8-year-old children from the USA (n = 2,097,188) using the air quality index (AQI) of the US Environmental Protection Agency as well as satellite-derived data of PM2.5 concentrations, sunlight, and maximum heat index. Multivariable logistic regression analyses were performed to determine whether the unhealthy AQI, PM2.5, sunlight, and maximum heat index were related to the odds of ASD prevalence based on gender and race and taking into consideration the confounding factors of smoking and socioeconomic status. The logistic regression odds ratios for ASD per 10% increase in the unhealthy AQI were greater than 1 for all categories, indicating that unhealthy AQI is related to the odds of ASD prevalence. The odds ratio of ASD due to the exposure to the unhealthy AQI was higher for Asians (OR = 2.96, 95% CI = 1.11-7.88) than that for Hispanics (OR = 1.308, 95% CI = 0.607-2.820), and it was higher for Blacks (OR = 1.398, 95% CI = 0.827-2.364) than that for Whites (OR = 1.219, 95% CI = 0.760-1.954). The odds ratio of ASD due to the unhealthy AQI was slightly higher for males (OR = 1.123, 95% CI = 0.771-1.635) than that for females (OR = 1.117, 95% CI = 0.789-1.581). The effects of the unhealthy environmental exposures on the odds ratios of ASD of this study were inconclusive (i.e., statically insignificant p value > 0.05) for all categories except for Asians. The odds ratios of ASD for Asians were increased by 5, 12, and 14% with increased levels of the environmental exposures of 10 μg/m 3 of PM2.5, 1000 kJ/m 2 of sunlight, and 1 °F of maximum heat index, respectively. The odds ratios of ASD prevalence for all categories, except for Asians, were increased with the inclusion of the smoking covariate, reflecting the effect of smoking on ASD prevalence besides the unhealthy environmental factors.

Keywords: Air quality index Autism spectrum disorder Fine particulate matter Heat index Remote sensing Sunlight.

7 Amazing Ways Nanotechnology Is Changing The World

Tiny nanoparticles are a huge part of our lives, for better or for worse.

Wellcome Images

“Everything, when miniaturized to the sub-100-nanometer scale, has new properties, regardless of what it is,” says Chad Mirkin, professor of chemistry (and materials science, engineering, medicine, biomedical engineering and chemical and biological engineering) at Northwestern University. This is what makes nanoparticles the materials of the future. They have strange chemical and physical properties compared to their larger-particle kin. The thing that matters about nanoparticles is their scale.

Click to launch the photo gallery_

Nanoscale materials are used in everything from sunscreen to chemical catalysts to antibacterial agents–from the mundane to the lifesaving. “I spilled wine at a Christmas party once, and I was terrified. Red wine on a white carpet. And it wipes right up,” Mirkin recalled. “The reason is the nano-particulate used to coat the carpet keeps that material from absorbing into the carpet and staining the carpet.”

On a more sophisticated side, researchers are developing nanoscale assays used to screen for cancer, infection and even genes. Gold nanoparticles that have been doped with DNA can be used to detect bacteria in a person’s bloodstream, determining whether a patient has infection and what kind. Or they can be used to detect changes in a person’s immune system that reflect the presence of cancer. Nano-flares can measure the genetic content of cells, and light up–or flare–when they detect a specific cell of a doctor’s choosing, maybe cancer, stem cells or even the reaction to a small molecule used in a new drug.

So why do nanoscale things act this way? The scale allows for unique interactions among atoms and their constituent parts, and there are a few ways that this happens. For non-biological nanoparticles, it helps to think of a bowling ball, and where all its atoms are located. The vast majority are inside the ball, with a finite number at the surface, interacting with the air or the wooden lanes. Atoms inside the ball interact with atoms just like themselves, but atoms at the surface interact with ones very different than themselves, Mirkin explained. Now shrink that ball to molecular scales.

“The smaller you go, the ratio of surface to bulk atoms goes up,” he said. “At a larger scale, the atoms at the surface are relatively inconsequential. But at nanoscales, you could have a particle that is almost all surface. Those atoms begin to contribute very significantly to the overall properties of the material.”

These interactions play out in electronics, too, making material like graphene and quantum dots useful for tiny computers and communication devices. Nanoscale materials offer a smaller area for electrons to move around. And maybe most importantly for current research, on the nanoscale, you’re on the scale of biology.

Given all these uses and future promises, Mirkin said, most people generally embrace nanotechnology in everyday life, even though most don’t know what that actually means. Even controversial uses like sunscreen are pretty widely used, and often without knowledge of it.

“Much of it is going to be embedded in conventional products that we buy and don’t even think about,” Mirkin said. “There’s nothing inherently good or bad in terms of making things small. The issue ultimately is, what do they do, and what are they used for? Given the application, have we considered the proper safety analyses and implications? And so far, I think we’ve done a pretty good job.”

Nanoparticle-Filled Ink Conducts Electricity

Tiny bits of conductive metal are crucial components of modern electronics, but future generations may not need high-precision machines. Circuit boards could be drawn by hand, enabling paper electronics, disposable antennas and a wide range of other items. Researchers at the University of Illinois at Urbana-Champaign (and many other teams) are making conductive ink from silver nanoparticles, which they shrink using acid. The nanoparticles are suspended in a cellulose solution, so they have a greater viscosity and can flow from a pen, quite literally. A line drawing becomes a silver wire that can carry a current, enough to power an antenna or even a small LED display, like the light bulb at the top of the house in this lovely drawing. The pen allows circuits to be embedded on uneven surfaces–and it enables a new type of creative design.

Cancer Detectors

Gold nanoparticles are used in a variety of new “sniffers” for cancer and other diseases. As cancerous cells grow, genes and proteins within cells change, and this process emits volatile organic compounds that can be detected–this is why some dogs can be trained to “smell” cancer. Nanoparticles can smell it, too, and in tiny concentrations. Israeli researchers a couple of years ago reported new gold nanoparticle sensors that can tell not only whether a person has cancer, but which kind–lung, breast, prostate or colon cancer. The benefit of such a system is its early-warning capability. Doctors could administer a simple breath test, and be able to tell whether a patient has the beginning stages of cancer–well before any tumors would show up on an X-ray or mammogram. And it’s not just cancer patients who can benefit. Chad Mirkin of Northwestern University is developing nanoparticles that can diagnose and treat disease, tracking cancer at earlier stages and even determining whether hospital patients have infections. If someone needs emergency surgery, it may not always be possible for doctors to obtain the person’s medical history, which leaves plenty of unanswered and potentially dangerous questions–does this person have diabetes? Is she at risk for blood clots? Nanoparticles can be used to answer these and other questions. Mirkin points to a relatively new test for sepsis, or blood infection, which has great promise for treating patients better and saving money. Sepsis can be fatal if not treated quickly and thoroughly, but tests to determine a person’s infection level can take three days to complete–meanwhile, the patient is pumped full of antibiotics. But gold nanoparticles functionalized with DNA can identify whether or not someone has sepsis, and which bug is running rampant through his bloodstream, Mirkin said. “It’s the difference between a $20 test and hundreds of thousands of dollars in antibiotics,” he said.


Perhaps no other product demonstrates more clearly the strange behavior at nanoscales than something called Osorb. An accident of chemistry, the swellable glass material was intended to react with trace molecules of explosives, which would have made it a valuable security tool at places like airports. But something very weird happened in the development process, recalled Paul Edmiston, Osorb’s designer and a chemistry professor at the College of Wooster in Wooster, Ohio. He and some graduate students were trying to design nanostructured silica–glass–to change colors in the presence of vapors. “We serendipitously discovered a formulation by which the nanoparticles we were assembling into this porous glass film had become flexible. Instead of being a solid, they had the ability to swell,” he said. “Yeah, we had the color change, but it soaked up the entire volume of the test solution. We put more on and it sucked up more. It just expanded.” (Watch a video of that here). Edmiston was intrigued, but shelved the product in search of something that would satisfy the need for explosives detection, which was the point of his research grant. “It was like, ‘Well, that’s not going to work on a boarding pass,'” he recalled with a laugh. A graduate student resurrected it later and the team realized the material had some very interesting properties–especially its complete lack of reaction to water. Molecules can pass through the empty space between the nanosize silica, but water doesn’t, Edmiston said. This makes it extremely useful for water cleanup. The swellable glass, now named Osorb and marketed commercially by a spinoff called ABS Materials, can soak up oil and other organic material, and you can wring it out afterward and use it again. How does glass swell? “Chemically, it’s halfway between the window pane glass in your house, and the caulk that’s around your sink,” Edmiston explained. “Those type of ingredients, from a chemical level, build them up into a architecture that has the ability to expand and contract.” Osorb is already being used in places like parking lots, where it can absorb oil from leaky cars and prevent it from washing into bodies of water. It can be decorated with other material, like iron, to capture chemicals like phosphate. Edmiston has a new grant to study how this works, because he’s not sure if there’s a biological factor at play. One other weird thing: As it swells, it generates a remarkable amount of force, Edmiston said. It can lift 60,000 times its own weight. “If you had a coffee can of it, that’s enough to lift a car,” he said. “You might imagine we discovered that the hard way. We’ve broken a number of things in the lab because you just cannot contain it.”

Fighting Cancer At The Source

If cancer does take hold, nanoparticles can help with this, too. The dog in this CT scanner is a prostate cancer patient, undergoing a clinical trial to determine the safety of radioactive gold nanoparticles to treat his disease. Dogs develop an aggressive form prostate cancer much like human men, and a recent study at the University of Missouri could eventually lead to targeted treatment for the human form of the disease. Sandra Axiak-Bechtel, an assistant professor of oncology at the MU College of Veterinary Medicine, said the study’s main goals were to determine whether the gold nanoparticles were safe–and they were. Dogs showed no swelling, toxicity or changes in their livers, kidneys or bone marrow. The dogs underwent CT scans to determine the sizes of their tumors, and then radiologists injected them with a purple liquid containing radioactive gold nanoparticles. The particles were rendered radioactive in MU’s Research Reactor, Axiak-Bechtel said in an interview. Targeting tumors with radioactive particles is not a new concept, but the gold nanoparticles are. Earlier research showed it could be effective in mice, so the team wanted to try it on dogs, too. “A lot of owners that come in are very excited about something new that might be more effective than what we have to offer, and the potential to help men in the future–most people are very excited about that,” Axiak-Bechtel said. Again, nanoparticle treatments can work for diseases beyond just cancer, including bacteria and viruses. At IBM, researchers in California have built degradable nanoparticles that can glom onto drug-resistant bacterial strains and rip them open, draining their contents. The polymer particles break apart when they finish killing bacteria, and flush away with the invaders they destroyed. This is possible because of the particles’ size, which nicely attaches to the exterior wall of a bacterium.

Gene Therapy and Drug Delivery

Practically every week, scientists announce a new breakthrough in the ability of nanoparticles to deliver genes, drugs or chemical messengers inside cells. Nanoparticles of different shapes and chemical makeup can track down and target specific cells of a chemist’s choosing, and perform a variety of tasks. This image depicts DNA molecules (light green), packaged into nanoparticles by using a polymer with two different segments. One segment is positively charged, which binds the polymer to the DNA. This is shown in teal. The brown portion shows a protective coating on the nanoparticle’s surface. By adjusting the solvent surrounding these molecules, researchers at Johns Hopkins and Northwestern universities were able to control the shape of the nanoparticles. The team’s animal tests showed that a nanoparticle’s shape can dramatically affect how well it delivers gene therapy. This is possible because DNA behaves strangely among nanoscale particles, explained Chad Mirkin of Northwestern. Spherical nucleic acids, one of his lab’s inventions and an up-and-coming therapeutic technology, allow DNA to do something it otherwise can’t: Enter cells. To insert gene fragments into cells, researchers have to trick the cell, which is designed to block invasion. This is frequently done using viruses, but those can have a wide range of side effects. Instead, spherical nucleic acids attach short strands of DNA or RNA to a gold or silver nanoparticle’s surface, and the DNA molecules will organize into a spherical shape, Mirkin said. “You arrange a simple molecule in a spherical form, and it naturally enters cells better than anything known to man,” he said. “That is a paradigm shifter for how we think about creating new therapeutics–in this case, involving the world’s most important molecule, and learning how to arrange it in new forms on the nanoscale.”

Protective Coating For Your Skin

Cancer therapy and gene therapy are still largely lab-based uses for nanoparticles, with new papers publishing often, but few if any FDA approvals. That doesn’t mean the tiny particles aren’t ubiquitous, however–one prime example is something you use every day in the summer (or at least should). Sunscreen contains nanoparticles of titanium dioxide and zinc oxide, which are highly reflective and can prevent harmful solar radiation from penetrating your skin. This has been controversial for some time, however, with several environmental groups arguing for a moratorium on nanoparticle-containing sunscreens. But even sunscreens with micro-particles suspended in their lotion may contain nano-ones, inadvertently rendered nano by the manufacturing process. Previous studies have reached conflicting conclusions over whether nanoparticles can penetrate the skin. The debate continues to play out in the scientific literature, but a recent study at the University of Bath in the UK showed the titanium dioxide particles do not penetrate the top layer of skin, where they could theoretically do harm. “Using confocal microscopy has allowed us to unambiguously visualize and objectively assess what happens to nanoparticles on an uneven skin surface. Whereas earlier work has suggested that nanoparticles appear to penetrate the skin, our results indicate that they may in fact have simply been deposited into a deep crease within the skin sample,” said professor Richard Guy from the university’s Department of Pharmacy & Pharmacology, in a press release. Nano-coatings can protect more than your skin–they can make paper waterproof, protect carpets and clothing from stains, and even actively repel dirt from surfaces.

Risk to Wildlife

In several areas of the United States, concentrations of mercury in fish and wildlife are high enough to be a risk to wildlife. It is difficult to prove cause and effect in field studies, however, because other factors that may contribute to the biological effect under study (for example, reproductive success) are often impossible to control. Scientists have discovered toxic effects in the field at concentrations of mercury that are toxic in the lab, and controlled lab studies have found toxic effects at concentrations that are common in certain environments. In studies in Wisconsin, reductions in loon chick production has been found in lakes where mercury concentrations in eggs exceed concentrations that are toxic in laboratory studies. At dietary mercury concentrations that are typical of parts of the Everglades, the behavior of juvenile great egrets can be affected. Studies with mallards, great egrets, and other aquatic birds have shown that protective enzymes are less effective following exposure to mercury. Analyses of such biochemical indicators indicate that mercury is adversely affecting diving ducks from the San Francisco Bay, herons and egrets from the Carson River, Nevada, and heron embryos from colonies along the Mississippi River. Finally, other contaminants also affect the toxicity of mercury. Methylmercury can be more harmful to bird embryos when selenium, another potentially toxic element, is present in the diet.

Mercury can cause deformities in developing animals.

Evolution impacts environment: Fundamental shift in how biologists perceive relationship between evolution and ecology

Biologists have known for long that ecology, the interaction between organisms and their environment, plays a significant role in forming new species and in modifying living ones. The traditional view is that ecology shapes evolution. The environment defines a template and the process of evolution by natural selection shapes organisms to fit that template.

Some specialized theory, a few laboratory experiments and studies of natural populations suggest, however, that evolutionary processes reciprocate by influencing ecology in turn.

Now a team of biologists presents evidence that ecology and evolution are indeed reciprocally interacting processes, presenting a fundamental shift in our understanding of the relationship between evolution and ecology.

"Ecology for the most part ignores evolution because organisms are treated as constants," said David Reznick, an evolutionary biologist at the University of California, Riverside, who led the study. "This does not mean that ecologists don't believe in evolution. It means the general assumption is that ecological interactions happen on such a short time scale in comparison to evolution that evolution can be ignored -- similar to the way physicists can often safely ignore relativity in the majority of their experiments.

"Our results represent a first significant step in showing that evolution cannot be ignored when studying ecological interactions. In earlier work, we had shown that guppies, our study organism, can evolve very rapidly. In this new study we quantify the ecological consequences of such rapid adaptation."

Study results appear this week in the online early edition of the Proceedings of the National Academy of Sciences.

Reznick's team compared guppies -- small freshwater fish that have been the subject of long-term studies -- that had adapted to two different types of stream communities in Trinidad. One stream community had a diverse group of fish species, some of which were serious predators on guppies. The other type of community included guppies and just one or a few non-predatory species.

Previously, Reznick and colleagues had established that predators cause a substantial increase in guppy mortality rates, resulting in guppies that are younger at maturity, produce more babies, and display different behavior, escape abilities and body shapes.

In the new experiments, the researchers collected guppies from the two different types of communities, and quantified their impact on the stream ecosystem by placing them in replicate, artificial streams built alongside a natural stream. The researchers chose this location for the artificial streams so that they could divert water from a spring that normally flowed into the stream in such a way that it first flowed through the artificial streams, emptying later into the natural stream.

Next, they seeded the artificial streams with organisms such as insect larvae from the natural stream so that all artificial streams had similar ecosystems at the start of the experiment.

They found that guppies from the two types of fish communities had substantially different impacts after only four weeks on the structure and function of their ecosystems.

"Guppies from the more diverse fish communities ate more insect larvae while the low-predation guppies -- guppies from the simple fish communities -- ate more algae," said Ronald Bassar, a graduate student in Reznick's lab and the first author of the research paper. "These differences in diet resulted in the artificial streams with guppies from the diverse communities having substantially more algae and fewer invertebrates than streams stocked with guppies from the simple communities.

"There were corresponding differences in how and at what rate nutrients, like nitrogen or phosphorus, were recycled. The streams with high-predation guppies -- guppies from the more diverse fish communities -- had less plant production and oxygen consumption, a slower breakdown of leaves that had fallen into the water and a slower accumulation of detritus, the breakdown product of leaves."

The researchers found, too, that their findings from their experiments in the artificial streams mirrored their observations in guppies across natural stream communities in Trinidad.

"By doing our experiments in the artificial streams we are able to pin down guppies as a likely cause of what we see in the natural streams," Bassar said. "The experiments show that local adaptation causes the evolution of differences in diet, which, in turn, causes differences in ecosystem structure. Our next step is to characterize how this changed ecosystem, in turn, shapes how the guppies adapt to it."

The National Science Foundation supported this research as part of a five year, multi-investigator grant funded by the Frontiers in Integrative Biological Research initiative.

Environmental Influence on the Developing Brain

Carl Sherman
November 26, 2014

Before birth and early in life, the developing brain is acutely sensitive to its environment. A symposium at the Fifth Annual Aspen Brain Forum, hosted by the New York Academy of Sciences in New York City, explored how certain social and psychological aspects of environment influence biology and behavior.

Tracy L. Bale, of the University of Pennsylvania, noted that maternal stress during pregnancy is associated with increased risk of neurodevelopmental disorders like autism and schizophrenia in offspring, but questions of timing remain unresolved.

Animal research can give insights, she said rodents perceive, process, and react to stress similarly to humans.

In the mouse, very early pregnancy—equivalent to the human first trimester—appears to be a sensitive period for gender-specific effects of maternal stress. Adult male, but not female offspring respond abnormally to stress, and are 10 percent smaller than normal. They pass these characteristics on to their own offspring, suggesting that prenatal stress has altered cells that will develop into sperm.

So early in gestation, maternal stress cannot directly affect the developing brain, Bale said, but it may act through the placenta.

She pointed out that in mice, some sex-linked genes in the placenta produce compounds that switch other genes off and on. “Because of them, the male and female placenta are poised to respond differently to a changing environment.”

Bale described experiments focused on O-linked-N-acetylglucosamine transferase (OGT), an enzyme that is twice as concentrated in normal female as male placenta. Among its functions, OGT helps construct proteins from DNA blueprints. Anything that alters OGT poses a broad threat to normal embryo development.

“We think of OGT as the biochemical canary in the placental coal mine,” she said.

Maternal stress reduces placental OGT in both sexes. Because the male normally has so much less, it may drop below a vulnerability threshold, she proposed.

To test the hypothesis, Bale’s team genetically engineered a mouse to produce no placental OGT in embryo. In adulthood, the males looked and acted very much like the offspring of mothers who had been stressed during pregnancy.

“Just by changing one gene in the placenta, you can dramatically reprogram how the brain is developing,” Bale said.

The prenatal environment should prepare an animal (or human) for its future world, she said. These experiments suggest how maternal stress might derail the process, leading to problems throughout life.

Parenting and Wiring

How early experiences shape a key brain circuit was the subject of a talk by Nim Tottenham, of Columbia University.

“The amygdala is important for learning emotional associations and maintaining vigilance, and strong connections to the prefrontal cortex (PFC) regulate its arousal. We’re interested in what the growth chart of this system looks like,” she said.

The relationship between the amygdala and the PFC is very different in children than in adolescents and adults “This switch interests us as we try to identify sensitive periods in development.”

Tottenham conjectured that because subcortical structures like the amygdala develop earlier than the PFC, to forge a connection the amygdala must “begin the conversation.”

Resting-state amygdala-PFC connectivity is absent in children, slowly developing after age 10, fMRI studies indicate. “This suggests that activations elicited by the environment are a prerequisite for establishing adult functional architecture between these regions,” she said.

Child-parent interactions may be instrumental in shaping the circuit during this period of plasticity, Tottenham said. In rodents, the mother’s presence quiets the amygdala in the first two weeks of life, and inhibits amygdala-based fear learning. When the mother is absent, “the infant acts like an adult.”

Studies in Tottenham’s lab suggested a similar process in young children. Amygdala reactivity declined when children were given pictures of their mothers while in the scanner, and the mother’s presence improved the child’s ability to control emotions like fear of strangers.

“Daily phasic modulations of parental absence and presence may do important toning work for the system, keeping the system plastic longer and determining how it will function,” she said.

The lack of such fluctuations, as in institutionalized children, may result in atypical amygdala-PFC connections, heightened reactivity, and emotional dysregulation, Tottenham suggested. “These profiles may reflect adaptations that the brain makes in response to early environments.”

Disadvantaged Development

Martha J. Farah took a broader perspective, summarizing research on the impact of low socioeconomic status (SES) on the developing brain. “It’s not just about money: nutrition, environmental toxins, prenatal care, neighborhood factors” enter the equation, said Farah, of the University of Pennsylvania, and a Dana Alliance member. “Effects on child development are not a threshold phenomenon, ‘poor vs. non-poor.’ There’s a gradient.”

Numerous behavioral studies have found that SES effects cluster around particular neurocognitive systems, rather than general cognitive capacity: language, executive function, and declarative memory “bear the brunt,” she said.

Brain activity measures show more asymmetry in regions associated with language, in higher SES children. “There was more left hemisphere activation, the normal pattern for language specialization,” Farah said. One study found greater dorsolateral prefrontal cortex activation, corresponding to better executive processing.

In a study of learning and memory, children of lower SES showed less hippocampal activity than those of higher SES. “This is quite consistent with functional data,” Farah said.

Structural imaging told a similar tale. Five studies found a significant association between hippocampal volume and SES. An NIH study of normal brain development linked SES to cortical thickness in regions including the prefrontal cortex, inferior cingulate gyrus and inferior frontal gyrus, she said.

How might SES influence cognitive function? “There are many possible pathways some directly affect the brain and body, others are more psychological,” Farah said.

Longitudinal data based on home visits found that cognitive stimulation promoted language development. “More surprisingly, measures of memory were responsive to parental nurturance” (e.g. attention, affection, and attitude toward discipline), she said.

Other studies link parental nurturance to hippocampal volume, and cognitive stimulation to temporal lobe differences. Much of this data “is highly consistent with the idea that the level of stress, which we know is higher in low SES homes, could be a mediating factor,” Farah said.

The Cost of Neglect
Charles A. Nelson, of Harvard University, discussed development under extreme conditions.

“Postnatal brain development is a heavily experience-dependent period of opportunity or vulnerability. When the brain expects but doesn’t receive input, it doesn’t know how to wire.”

Profound childhood neglect represents a situation in which “the brain is deprived of most expected experiences during sensitive periods,” he said, and institutionalization typically involves such neglect.

Nelson described findings from the ongoing Bucharest Early Intervention Project, a randomized controlled trial involving 136 children abandoned at birth to institutions in Romania. Half were placed in high quality foster homes when they were 6 to 31 months of age, and half remained in institutional care.

Follow-up testing to 12 years, found cognitive, and brain functional and structural differences between the two groups, and between both groups and never-institutionalized children. Age of foster care placement also made a difference.

Overall, “exposure to institutionalization early in life leads to reduction in electroencephalogram (EEG) power, gray and white matter, and connectivity. Foster care remediated some areas,” Nelson said.

EEG findings exemplified the importance of timing. Children placed in foster families before 24 months showed brain activity over the frontal lobe as robust as those who had never been institutionalized, while those placed later “looked like they never left the institution.”

Recently, the researchers analyzed stress response data. Pre-ejection period, a cardiac measure of sympathetic activation, was dramatically different in children who had and hadn’t been institutionalized. “Children placed in foster care showed some recovery, but it was incomplete,” Nelson said.

Cortisol, another stress marker, was more clearly sensitive to timing of family placement. “Those who were placed before 24 months looked just like the never-institutionalized kids,” Nelson said.

The majority of children not randomized to foster care had in fact left their institutions by age 8. That significant deficits endured support the conclusion that “effects are carried by where they lived in the first years of life,” explained Nelson.

Determining environmental causes of biological effects: the need for a mechanistic physiological dimension in conservation biology

The emerging field of Conservation Physiology links environmental change and ecological success by the application of physiological theory, approaches and tools to elucidate and address conservation problems. Human activity has changed the natural environment to a point where the viability of many ecosystems is now under threat. There are already many descriptions of how changes in biological patterns are correlated with environmental changes. The next important step is to determine the causative relationship between environmental variability and biological systems. Physiology provides the mechanistic link between environmental change and ecological patterns. Physiological research, therefore, should be integrated into conservation to predict the biological consequences of human activity, and to identify those species or populations that are most vulnerable.

Conservation Physiology may be defined as the application of physiological theory, approaches and tools to elucidate and address conservation problems with the aim to provide a mechanistic understanding of how environmental disturbances and threatening processes impact physiological responses and thereby ecological function, population persistence, and species survival.

1. Introduction

The importance of addressing conservation issues, such as climate change, emerging diseases and habitat loss, lies in preserving the integrity of ecosystems at local and global scales. Biodiversity is essential to provide utilitarian ecosystems that can sustain human subsistence, as well as cultural values that confer a sense of identity. A well-functioning natural environment and maintenance of biodiversity are thus fundamental to human well-being [1]. Climate change and environmental degradation has already resulted in negative consequences for human subsistence and health and, hence, economic success [2,3]. The regional decline of agriculture [4] and of some fisheries [5–8] are examples of environmental and ecological problems that can be attributed directly to human activity. The most crucial issue is to slow anthropogenic impacts on natural systems and thereby maintain functioning ecosystems. There is good evidence that conservation can work [1,9], and our aim here is to help improve the effectiveness of conservation measures by linking physiology and ecology in a mechanistic framework, thereby providing a stronger knowledge base for decision-making.

Any conservation measure requires sound scientific information of the effects that habitat alterations resulting from human activity have on natural systems [10]. Even if the political will existed to curtail all human impact, this is logistically impossible. Conservation must therefore be selective and pragmatic. Decisions must be based on an understanding of the impacts that particular human activities have on ecosystems, so that the benefits of remedial actions can be maximized, while the costs to society are minimized. In other words, there is an urgent need to understand the link between the cause (i.e. human activity) and its effect on biological function from individuals to ecosystems. We argue here that in many if not most cases, the physiology of individuals provides this link between cause and effect, and can thereby explain ecological patterns. Physiological capacities and responses act as a filter between environmental change and ecological performance of individuals and, hence, populations and species [11,12] (figure 1).

Figure 1. Physiology acts as a filter between environmental changes, and ecology and biodiversity. Environmental changes result from global change and habitat destruction, for example, which lead to changes in physical variables such as temperature, pH, etc. The physiological response of organisms to these changes will determine fitness-related functions, such as metabolism, growth, behaviour and ultimately reproduction. These functions are key elements that determine ecological relationships and the persistence of species in particular habitats, and thereby biodiversity. Photos J. Smith (left panels, with permission) and F. Seebacher (right panel).

2. Human activity modifies the abiotic and biotic environments

Environmental change is natural and occurs at different time scales. For example, natural forcing can cause regional climate change at time scales of 1–10 years [13], and palaeoclimate records around the globe show that regional climate fluctuation of as much as 8–16°C occurred repeatedly at periods of less than 10 years [14]. These regional climate changes have had a direct impact on human societies [2]. Importantly, forcing by human activity accelerates climate change at regional and global scales. Human activity such as extensive deforestation may have affected climate since prehistoric times in Europe [15]. However, the recent climate change induced by increased CO2 emissions starting in the late twentieth century remains unprecedented [15,16]. The resulting increases in temperature and acidification of marine systems are global [16], although temperature increases can be much more pronounced in climate change ‘hotspots’. For example, sea temperatures in southeastern Australia have increased much more rapidly (by 2–3°C since the mid-twentieth century) than the global average [17]. Regional and small-scale changes in the environment are also driven by local land-use practices [18]. Deforestation and land clearing affect biodiversity by direct removal of species. Direct removal of species, either as a result of land clearing or of exploitation for human use, alters resource availability, such as shelter and food, for higher trophic levels. Land clearing causes climate warming by adding CO2 to the atmosphere and decreasing evaporation, but it may also have a cooling effect by changing the surface albedo [18]. Removal of vegetation cover affects the hydrologic dynamics of the soil and may contribute to increased salinization of freshwater systems [19,20].

Other major impacts on the physical environment at global or regional scales result from pollution. Dumping or spillage of industrial chemicals has a direct impact on the environment. Examples of negative effects on biodiversity are chemical spillages from mine tailing dams, such as in the otherwise relatively pristine rivers of New Guinea [21]. The military strategy of defoliation, whereby American forces dumped hundreds of thousands of tonnes of herbicides on forests in Vietnam in the 1960s and 1970s, has caused large-scale deforestation and pollution, the effects of which are still present today [22]. At a global scale, the increase in ultra-violet (UV) radiation as a result of hydrofluorocarbon release can affect ecosystems by disrupting different life-history stages of vulnerable species, and its effect may be compounded by other stressors such as pollution [23,24].

3. Ecological success is coupled to environmental conditions via the sensitivity of physiological systems

It is well established that changes in the abiotic environment affect the physiology of organisms at multiple levels. A large proportion of reproductive success and individual fitness is determined by physiology, so that environmental change affects fitness by its effect on physiology. Time to sexual maturity depends on growth rate and therefore on the capacity of energy assimilation and metabolism [25]. Foraging, competition and reproductive behaviour of animals are a function of locomotor performance and therefore of muscle physiology and metabolism [26,27].

The efficacy of metabolism and muscle physiology as well as most other physiological systems depends on the cellular environment (temperature, pH, acid–base balance, etc.), which is influenced by the external environment. Changes in body temperature, for example, affect biochemical reaction rates and most organisms function best within a relatively narrow range of body temperatures. Because the thermal sensitivities of individual reaction rates vary, the challenge for organisms lies in maintaining the stoichiometry of their complex cellular biochemistry, which will be disrupted by a change in the thermal environment. Increases or decreases in means or variability of operative environmental temperatures change body temperature directly in those organisms that do not thermoregulate, or change the environmental context within which animals thermoregulate [28]. In endotherms, a decrease in environmental temperatures will elicit an increase in metabolic heat production and, conversely, increases in temperature decrease metabolic heat production. Ectotherms may respond to changes in environmental temperature by selecting different microhabitats, such as increased shelter use to minimize absorption of solar radiation in warming environments [29]. In addition to behavioural responses, many ectotherms modulate their cellular biochemistry to compensate for thermal effects by, for example, quantitatively or qualitatively changing the expression of rate-limiting enzymes [30,31]. In all cases, the change in physiological need that ensues from a change in the environment will alter the resource use of individuals. In the examples above, energy requirements and the utilization of the structural environment change, both of which have important ecological consequences by changing foraging and predation, and competition for particular microhabitats. Similar relationships as discussed briefly above for temperature exist for changes in other abiotic environmental variables, such as UV-B radiation, CO2 levels, rainfall and dehydration, hypoxia and salinity. Hence, physiological requirements are at the interface between environmental change and ecology (figure 1).

Importantly, physiology also mediates biotic interactions. These interactions may be nested within the effect of abiotic drivers as in the example above where energetic needs for thermoregulation change in different environmental contexts. Nutrition, with respect to both energetic and macronutrient requirements, in particular determines interactions between organisms [32,33]. At a quantitative level, density of prey will determine predator numbers [34], but this relationship will change with environmentally driven changes in energy requirements, such as for thermoregulation. Different abiotic contexts can also change the macronutrient requirements of individuals and therefore change the need for prey quality in addition to quantity. For example, temperature affects the relative macronutrient requirements in trout, and fish at warm temperatures require relatively more protein than at cooler temperatures [35]. As a result, foraging behaviour must be adjusted to meet intake targets, and predation pressures shift to different prey species, potentially leading to a change in community structure and interactions [33].

Similarly, decreases in aquatic oxygen levels in freshwater river systems can impact on the diving ecology of bimodally respiring turtles, requiring them to expend greater energy to surface more frequently to acquire oxygen from the air, but also increasing the risk of predation, especially in hatchlings as they swim through the water column [36]. Changes in salinity of freshwater systems also change the activities of ATPases for ion regulation [37] and therefore modulate energy intake, and thereby the impact that individuals have on their ecological community.

Most species possess a degree of plasticity that permits persistence across a range of environmental conditions. However, there is a limit to physiological compensation for environmental variability [38,39]. If environmental conditions become too extreme, direct cellular damage may ensue and animals will become more susceptible to disease [40], and ultimately extinctions will occur.

4. Physiological systems can compensate for environmental change—up to a point

The effect of environmental variation on physiological function (phenotype) may be modulated by compensatory responses. Such responses can occur at different time scales: between generations (genetic adaptation) [41], during development (developmental plasticity) [42,43] so that phenotypes are matched to prevailing environmental conditions, and within the adult lifespan as reversible plasticity (acclimation and acclimatization) [44–46] and migration [47,48].

The optimal ‘adaptive strategy’ of organisms depends on the patchiness or ‘grain’ of the environment [49]. A coarse-grained environment fluctuates between distinct states, and an individual is exposed to only one. Performance and fitness in a coarse-grained environment may be maximized by genetic adaptation if environmental conditions remain stable across generations, and by developmental plasticity if the environment remains stable during the lifetime of the organism [49,50]. In a fine-grained environment, an individual experiences numerous patches, so that total fitness will be the sum of the individual fitness components of each patch, and reversible acclimation would enhance performance and fitness [30,51]. In theory [49,52], coarse-grained environments will produce phenotypes that are specialized (adapted) to the relatively stable conditions experienced, while fine-grained environments produce generalists that perform well over a wider range of environmental conditions albeit at a reduced level in other words, generalists trade-off maximal performance for performance breadth. However, this need not be the case if reversible acclimation can compensate for environmental variation experienced during the lifetime, effectively leading to ‘specialized generalists’ in which the conditions at which performance optima occur track changes in environmental conditions without loss of performance [51,53].

Most species experience both fine- and coarse-grained variation at several temporal (e.g. day, season and geological) and spatial (e.g. microhabitat and latitude) dimensions, as well as the interaction of the two resulting from animal movement within habitats [54], between geographically separated habitats [48], or as a consequence of life-history stages occupying different habitats [55]. Hence, fine-scale patchiness at a short temporal scale is added to coarse scale variation at longer periods. Patchiness of the environment changes naturally, for example, with season or latitude. However, conservation issues may arise when human activities alter patchiness and thereby disrupt evolutionary strategies. Local land-use patterns such as deforestation and agricultural activities, and anthropogenic climate change, for example, can alter fine- and coarse-grained patchiness of the environment, respectively.

The relative importance of plasticity and adaptation will depend firstly on the relationship between lifespan and rate of environmental change and, secondly, on the rate of phenotypic change relative to environmental change. The importance of lifespan is that species with very short lifespans may experience only one distinct (coarse-grained) environment, so that genetic adaptation between generations and possibly developmental plasticity will be the most important responses. Many species, however, will also experience at least some variation within their lifetime. In this case, the optimal adaptive strategy will be a plastic phenotype that can acclimate to each of the predictable extremes, in addition to genetic adaptation to latitudinal and altitudinal gradients [12,56,57].

Ideally, fitness is maximized when organisms can perform at a constant level despite environmental variability. It is impossible, however, that the phenotype can change at the same time as the environment, if the environmental change provides the signal for phenotypic change. Hence, there will always be a lag between the two. The lag in the phenotypic response may preclude plasticity, when the rate of environmental change is greater than the potential for phenotypic change. Hence, an environmental fluctuation with a period that is much shorter than the physiological response time could not act as a stimulus for phenotypic change. For example, it will take several weeks for changes in metabolic gene expression and enzyme activities to compensate for a chronic change in temperature [58,59] so that daily temperature fluctuation will not affect metabolic capacity. Generally, acute changes in temperature resulting from movement through different microclimates, weather changes and diurnal fluctuations may affect real-time physiological rates, but do not affect capacities. Similarly, genetic adaptation will occur only when the rate of environmental change is slower than that of genotypic change. Human activity is often rapid relative to the rate of adaptive processes and even relative to the lifespan of many organisms. Hence, genetic adaptation may play a lesser role in responding to human-induced environmental changes than developmental- and reversible plasticity. This means that capacity for acclimation will play a predominant role in determining the vulnerability of organisms to environmental change. Human activity will affect species within the same habitat differentially, depending on their capacity for physiological plasticity and lifespan the latter characteristics alone can provide valuable background data informing conservation decisions.

Even in the most plastic organisms, however, the capacity to compensate for environmental change has it limits [38]. These limits may be set by inadequate environmental resources such as energy and nutrient supply, which may curtail growth, locomotion and other energy-consuming processes [32,60,61]. Limits may also be set by biochemical constraints such as an increased inefficiency of mitochondria in producing chemical energy (ATP), or by the production of reactive oxygen species, which cause damage to membranes and proteins [31,62,63]. Beyond these limits, fitness will decrease as a result of declining performance, and accumulated damage and disease. Successful conservation must predict these limits and, if possible, maintain the range of environmental fluctuations within the limits of effective organismal responses. An understanding of the capacity for individual plasticity that may compensate for human-induced changes is of particular importance in the light of rapidly changing environments. It is unlikely that all species or populations within a region will have the same capacities and limitations. However, knowing the limits of physiological responses to environmental perturbations will make it possible to identify the elements of the ecosystem that are most vulnerable to particular human activities.

5. Physiology can detect cause and effect to determine vulnerabilities to environmental change

To date, most information regarding biological responses to anthropogenic environmental changes, and in particular to climate change, consists of correlations between environmental and biological variables [64,65]. For example, northward shifts in the distributions of marine and terrestrial organisms in the Northern Hemisphere have been associated with the avoidance of increasing temperatures at lower latitudes caused by anthropogenic climate change [66,67]. Shorter winters and mild springs resulting from global warming have been correlated with the earlier flowering of plants and other shifts in phenology [68]. These correlational data are essential to understanding the potential impact of climate change on biological systems. However, correlations are not sufficient to determine whether climate change has caused the observed changes in distribution or phenology. Invariably, any biological pattern will be correlated with a large number of abiotic and biotic patterns—some known, many unknown. To determine whether or not a change in the environment can cause the observed change in pattern requires experimental evidence [69]. It would be necessary to demonstrate experimentally, with adequate controls, replication and elucidation of the underlying pathways, that the environmental variable in question can effect the observed biological changes.

For example, in one of the first studies that related global warming to a change in distribution, Parmesan et al. [66] showed a northward shift in distribution of butterflies in Britain between 1910 and 1997. However, over that time frame, there were many changes in the British landscape, and one very obvious one was the decline and collapse of the coal industry in northern England and Scotland (figure 2). Plotting the abundance of butterflies in Scotland (i.e. the northernmost distribution) given in fig. 1 of Parmesan et al. [66] against the number of coalmines in the area (data from the UK Coal Authority) gives a perfect correlation of r = 1 (figure 2). Apart from the inherent limitation of only three data-points, figure 2 clearly presents an alternative hypothesis explaining distributional range shifts of butterflies in the UK in the last century. Which explanation is correct, global warming or coal pollution, if any? The only way to determine the correct answer is by experimentation. Another example is the perceived northward shift of fish in the North Sea [67] as a result of mean water temperature increases in the southern North Sea. At least for some species such as cod (Gadus morhua), published data [70–72] show that the fish are well able to acclimate to temperatures over the observed temperature increase in mean surface temperature from 11.7°C to 13.0°C in the North Sea between 1980 and 2006. In fact, the fish are more likely to be limited by cold at those temperatures than to be heat stressed. Hence, what is known about the physiology of the fish does not support the conclusions drawn from the correlational study that temperature per se caused shifts in distribution. Plausible alternative explanations that could explain the changed distribution pattern include overfishing, and a decline in copepod abundance which is the main food source of larval cod [73]. Cod are a good example of the challenges facing marine conservation, because the complex responses to environmental variability within individuals and between populations [8] make it difficult to manage the resource. Conservation physiology can make a significant contribution, because understanding the plasticity of physiological responses of the species will permit modelling of ecological responses [8] and predictions of the impact of future environmental change. Finally, correlations between climate change and bird distribution patterns lack predictive power and are unlikely to reveal the mechanistic basis of changes in distribution [74].

Figure 2. Correlation between butterfly distribution and coal mining. Butterfly distributions (from Parmesan et al. [66]) in Scotland were plotted against the number of coalmines in the area during the same time periods (inset). The strong correlation presents the alternative hypothesis that butterfly distributions are constrained by coal pollution rather than by climate change as suggested by Parmesan et al. [66]).

Correlations are essential to propose hypotheses that could explain the observed patterns. Hence, the studies cited above and many other correlational studies are extremely important. Over-interpretations of correlations, however, are detrimental to conservation because a misrepresentation of the cause underlying a biological pattern means that conservation efforts are misguided. This is where the importance of physiology lies: it can detect the cause. Even in the absence of a positive result, fairly standard physiological studies can eliminate possible explanations. In the cod example above, physiological studies have shown that locomotor performance [72], metabolism and growth of larvae [70,72], and even food supply [75] are not negatively affected by the observed temperature increase. Hence, temperature increases per se can be ruled out in explaining the observed distributional shift. It is now clear that overfishing is the most likely candidate to have caused the pattern [5]. We would like to emphasize that we do not wish to downplay the importance of climate change. Instead, we advocate a more stringent assessment of its effects to increase the efficacy of conservation measures. Physiological research provides a tool to identify causes of biological change, and to eliminate others that may be correlated but not causative.

The environment interacts with physiological capacities of individuals. Growth rates, as well as other fitness-related functions such as locomotion [76], are directly dependent on individual physiological capacities such as for aerobic metabolic energy production. Population growth—either positive or negative—is the sum total of the growth and performance of individuals. A shift in the environment that causes a mismatch between environmental conditions and optimal temperatures for individual physiological performance can therefore cause population declines and extinctions if performance optima are fixed within populations. Hence, there is a need to understand individual responses to changing environments and then translate these to populations, species and communities [8,11,12].

A Real-Life Stress Example

Consider Sue's story, which illustrates the impact that prolonged stress can have on health. Sue was a bright and talented high school student. She had always been healthy and done well in school. In the past year, she added more activities, including early morning swim practice, a college prep class, a role in the school play, and work on the school yearbook. She knew her schedule would be really busy, but she enjoyed all of the activities.

What happened?

Because of her busy schedule, Sue seldom ate dinner with her family. Her meals often consisted of fast food. She started drinking soda to boost her energy. At night, even though she was exhausted, she couldn't sleep because her mind was racing. She started getting sick and missing school, first because of strep throat and then mono. She also started having severe stomachaches.

How were Sue's health issues addressed?

Sue's pediatrician diagnosed her with irritable bowel syndrome and offered her some medication to relax her gut. But Sue's mother felt strongly that she didn't want her to take medication.

Instead, she began to work with Sue on her schedule and habits. She insisted that Sue cut one after-school activity and be home for dinner at least four nights a week. She took Sue to a yoga class, where Sue began learning how to work with her breath, and to focus on the moment without fixating on worries about things that were out of her control. In the mornings before swim practice, she began doing 10 minutes of seated meditation with her mother.

After addressing the stress, Sue was still very busy, but she slept better, had more energy, and her stomach problems disappeared.

Straw breathing exercise

Keep a pack of straws in your car and do this exercise whenever you're stuck in traffic.

  • Inhale normally and naturally.
  • Exhale fully through a plastic drinking straw, making sure you have exhaled all of the air out of your lungs.
  • Inhale normally (not through the straw).
  • Exhale fully out of the straw.
  • Repeat this exercise for 5 minutes.
  • Ideally, do this twice a day.

What is the evidence?

There is a great deal of very rigorous research that links the physical environment of hospitals to health outcomes. According to Ulrich and Zimming, authors of the 2004 report, The Role of the Physical Environment in the 21st Century Hospital, there are more than 600 credible studies that show how aspects of healthcare design can influence medical outcomes.

Essentially, this research shows that the conventional ways hospitals have been designed contribute to stress and adverse patient and staff outcomes. Poor design can adversely impact health and wellbeing, as well as staff productivity and ability to deliver great patient care. For example, because of poor design, nurses in most hospitals spend a great deal of time just gathering the material they need for care. One study showed that almost one-third of nursing staff time was spent walking. (Ulrich, p5.)

On the other hand, improving the physical environment can make healthcare settings less stressful, safer, and better places to work.

Experts in the new area of evidence-based design have identified five environmental factors that can have a large impact on health outcomes. Changes in these areas help create a healing environment that is psychologically supportive for patients, families, and staff. And many hospitals and healthcare settings are applying these findings.

Bees in decline

At the same time, the practice of spraying pesticides on almond plantations to deter pests has other unwanted side-effects. Almond trees require pollination in order to flourish, so vast armies of bees are often brought in to help with the process. However, the bees cannot cope with the substances sprayed on the crops and so, just like human armies sent off to war, many of them do not survive the ordeal.

This is grave news not just for the survival of bees themselves, but also myriad other species, since the deterioration of pollination habits can have serious repercussions for all manner of other plants and animals. Indeed, cultivation of almost all human crops (not just almonds) rely on pollinators to aid with the process, meaning that a drop-off in bee populations can have a keenly felt effect on food security, as well.

So should almonds be shunned altogether? Well, the nuts are a great source of protein, fibre and other important nutrients and when consumed in moderation, can form part of a healthy diet. However, those concerned about their almond footprint should look to buy only organically produced ones, which don&rsquot employ the pesticides so dangerous to bees. Meanwhile, almond milk is far preferable to dairy &ndash but oat milk and soy milk both represent more eco-friendly alternatives.