Aurora photos, for The Chronicle Review

M y suburban neighborhood is one of those fortunate places inhabited by plenty of animals as well as people. Crows cavort outside my window; down the street is a pond where frogs lurk in the reeds and swallows patrol the surface, and my running path takes me past browsing deer and along a creek where turtles bask and sunfish nest.

I keep an eye out for them all. Animal-watching is like people-watching at a streetside cafe, engrossing me in imagined stories. To watch a chickadee is to live for a moment in the trees. And when I encounter my nonhuman neighbors, I often wonder: What's on their minds?

It's a scientifically exciting moment to ask that question. For most of the past century, the official answer leaned toward: nothing much, really. With a few notable exceptions, scientists defined animals as instinct-driven and incapable of thought, or else governed by simple stimulus-response conditioning. Human intelligence was treated as singular, differing from other animals not merely in degree, as Charles Darwin wrote in The Descent of Man, but in kind. To assert otherwise was to invite the invalidating taint of anthropomorphism: imputing human characteristics to objects that don't have them, not unlike a child playing with stuffed animals. It was unscientific.

How times have changed: What once was considered anthropomorphic thinking is now mainstream science. That's not to say researchers have come to see other animals as simply furred or feathered versions of ourselves. But they are increasingly attentive to the shared biology of human and animal consciousness. A consensus is emerging that to study animals is to appreciate not only their differences from us but also their deep similarities. As the primatologist Frans de Waal writes in Are We Smart Enough to Know How Smart Animals Are? "anthropomorphism is not always as problematic as people think."

Are We Smart Enough is the latest in a profusion of books by scientists and popular-science writers: See also Carl Safina's Beyond Words: What Animals Think and Feel, Nathan H. Lents's Not So Different: Finding Human Nature in Animals, Jonathan Balcombe's What a Fish Knows: The Inner Lives of Our Underwater Cousins, and Jennifer Ackerman's The Genius of Birds, all published in the last year or so. New research describes qualities among nonhuman animals that were once considered exclusive to us: empathy, mental time-travel, language, self-awareness, and altruism. Journals overflow with studies of animal minds, frequently described in language also used to describe human minds, and feats of animal intelligence seem to go viral weekly: an octopus escaping its tank, crows gathering to mourn their dead, fish solving problems, monkeys grieving, and snakes socializing.

Not everyone is excited about it. To some scientists, these celebrations of animal smarts are often held before alternative explanations can be ruled out — "killjoy explanations" that are "less likely to make headlines," as Sara Shettleworth, a University of Toronto psychologist and zoologist, wrote in a 2010 Trends in Cognitive Sciences essay. Clive Wynne, who studies animal cognition at Arizona State University, says that "anthropomorphic descriptions of animal behavior shed more smoke than light." And it's worth remembering that scientific antipathy to animal intelligence emerged partly in response to the carelessness of many early anthropomorphizers.

A Darwin protégé, George Romanes, for example, in the 1880s leapt from secondhand just-so animal stories, such as that of a monkey who supposedly shamed a hunter by proffering his bloodied paw, to conclusions about their mental abilities. Perhaps not surprisingly, Romanes's own acolyte, C. Lloyd Morgan, took a sharp turn toward the empirical; his caution — that animal behavior should never be seen as evidence of "higher psychical faculty" if it could be explained by one "lower on the psychological scale" — would become enshrined as Morgan's Canon, shaping a coming century of research.

While adherence to Morgan's Canon arguably became dogmatic, it's also true that scientists were short on better data and theories. As Shettleworth herself noted, anthropomorphism is now accompanied by scrupulous experiments and sophisticated investigations. These describe not only behavior but neurobiology and draw upon recent research into human psychology and cognition, making it possible to compare the inner workings of animal minds with our own.

Sure, we have some things in common with mammals and birds, but fish?

The most exciting areas now involve moving from obviously intelligent species, like chimpanzees and elephants, into less-understood animals, and figuring out how complex thoughts arise from the interplay of simpler cognitive processes — how to gauge not only intelligence but feeling and inner experience, and what this blooming, buzzing profusion of minds means to Homo sapiens.

"The real job has only now begun," says de Waal. "We are now ready to get into the details."

N ow 67 years old and holding an endowed professorship at Emory University, de Waal began his career in the late 1970s, not long after the zoologist Donald Griffin's seminal The Question of Animal Awareness made waves by suggesting that animals could think and reason. It was a radical idea — Griffin's New York Times obituary in 2003 would say he "broke a scientific taboo" — and the research for which de Waal is now best known, on empathy, altruism and social intelligence in chimpanzees, was initially received with skepticism. De Waal's findings that chimps reconciled after fights and exchanged grooming for food, and that they did so consciously, was "taken to imply impossibly high cognition," he recalls.

Even studying those behaviors was at first difficult. "I learned to go with mainstream topics to get funding, and to test my more speculative ideas simply in the context of such funded work," says de Waal. "I have never received a penny, for example, for research on reconciliation and empathy, even though this is what I am most known for." Though the quality of his science would eventually prevail, it required both inner conviction and a thick skin.

As difficult as it once was for de Waal and other primatologists, though, their task was comparatively easy: Chimpanzees are humanity's closest living relative, and other primates are still part of the evolutionary family. To recognize their intelligence is, in a sense, to recognize our own. In recent years, chimps have been phased out of most medical research, and the National Institutes of Health is reviewing how monkeys are used. But science and society have been slower to acknowledge our similarities with more distantly related species.

Take rats: They are widely underestimated, de Waal says, and exempt from Animal Welfare Act protections, even though findings made in monkeys are frequently then demonstrated in rats. In fact, in a series of experiments conducted over the last several years, rats have also been found to possess empathy, a capacity sometimes said to define humanity.

That research was first described in 2011 in the journal Science by Peggy Mason and Inbal Ben-Ami Bartal, neurobiologists at the University of Chicago and the University of California at Berkeley, respectively, and built on earlier studies of how mice experience "emotional contagion," or a sort of ripple effect in which individuals become distressed when nearby individuals become distressed. So acutely do rats feel for trapped cagemates, found Mason and Ben-Ami Bartal, that they preferred helping them to eating, even choosing helpfulness before chocolate — no small thing to a rat. Further research described the importance of emotion to this response. When the scientists gave rats a drug that blocked their ability to feel stress, they stopped helping.

These findings were notable not just for putting a kinder, gentler face on an oft-loathed rodent, but for underscoring the complexity of empathy. The term encompasses different forms, from the direct response of those rats, to humans who are moved to tears imagining the predicament of someone they know only from a story. Yet much of our everyday empathy does involve caring responses to people in front of us. "Many of the characteristics we value most in ourselves are aspects of our nature that originated in other animals," says Susan Lingle, a behavioral ecologist at the University of Winnipeg, "and are traits that we still share." Being anthropomorphic can mean recognizing the animal in us.

Yet do rats truly experience empathy or do they simply behave in a similar way while possessing a very different internal reality? The question poses what's known as the other-minds problem: The only feelings we can observe directly, and thus be sure about, are our own. Without the ability to ask animals to explain themselves, scientists can only do their best to plot a trajectory from multiple lines of behavioral, neurological, and evolutionary evidence.

Sometimes they disagree on where the lines point. This applies to our understanding of all animals, not just rodents, but an especially instructive example again comes from rats and whether they can imagine themselves in the past and future. Technically known as mental time-travel, this is a bedrock part of human experience; in 1997 two psychologists, Michael Corballis and Thomas Suddendorf, declared that it constituted "a discontinuity between ourselves and other animals," whose mental lives were constrained by the boundaries of the present moment.

Over the next decade, evidence mounted for mental time-travel in other species. Researchers reported conscious planning by chimpanzees selecting tools they'd later need, or western scrub jays caching food for the following day. Corballis and Suddendorf challenged those findings, saying they could be explained by a rote association of action and reward without recourse to high-powered mental projections. Yet over time, Corballis, a professor at the University of Auckland, started to have misgivings.

"I thought we were getting kind of picky in not accepting that evidence and instead trying to pull those experiments apart," he recalls. Meanwhile, studies of rats' brains showed the same neurological networks that in humans underlie mental time-travel and spatial memories. When rats who'd previously earned a treat by navigating a maze later displayed telltale activity patterns in those networks, as if they were actively retracing their steps and plotting a future path, Corballis was swayed.

 "I am among those who have claimed that [mental time-travel] is a uniquely human capacity," he wrote in 2013 in the journal Trends in Cognitive Sciences, "but I now question whether this is so." Suddendorf, a professor at the University of Queensland, dug in his heels: Whatever the rats' experience, he rejoined in his own Trends in Cognitive Sciences letter, it simply couldn't compare to the richness of ours. Invoking the way we "mentally populate spatial scenes with actors and actions, embed scenarios into larger narratives, and reflect on the likelihood or desirability of different options," Suddendorf likened the difference between our experience and a rat's to that between H2O as a solid or a gas. The elements might be the same, but they take radically different forms.

It's presently impossible to adjudicate who is right. Scientists must make judgment calls on those trajectories of evidence, and to Corballis they point unavoidably to mental time-travel. Furthermore, he observes, the ability to remember the past and imagine a future has clear evolutionary benefits. He thinks continuing skepticism reflects not objective rigorousness but a deep-seated desire to prove humans superior.

Corballis does grant that our mental time-travel is probably far richer than rats'. We can expand our mental scenarios with all manner of fantasy and hypotheticals. The rats who live next to a Mexican restaurant's garbage bin probably don't imagine themselves inside with all their friends and extended family, throwing a Ratatouille-style party. Still, they might at least think of the delicious treats awaiting them after closing time. It's a difference of degree, not kind.

I think of that while watching crows, a raucous gang of whom rule the airspace between my building and the next block, and who like to store food in hollows at the tops of telephone poles. Maybe, as Suddendorf would have it, they're acting on instinct and basic learning: a combination of behavioral routines reinforced when crows later rediscover the food they've hidden with no conscious thought of the future. Or, per Corballis, maybe the crows actively plan for a time when they'll be hungry.

It's certainly possible. Like scrub jays, crows are corvids, a family of birds celebrated in books like Bernd Heinrich's classic Mind of the Raven and John Marzluff's 2012 encomium, Gifts of the Crow: How Perception, Emotion, and Thought Allow Smart Birds to Behave Like Humans. They're avian valedictorians, frequently compared to great apes; at this point, feats of corvid intelligence are old hat. What's more intriguing is the study of thought in other, less intellectually celebrated birds, like the black-capped chickadees who live in a patch of forest just down the street.

They too cache food — hundreds of seeds a day, tens of thousands in fall and winter — the locations of which they remember with marvelous accuracy and rely upon to survive. This would at least suggest the possibility of foresight, and indeed some preliminary research supports the notion, though such a capacity might seem beyond their lentil-size brains. Still, it's careless to assume chickadees are simple: Indeed, research into a closely related bird, the great tit, suggests they possess something else that's quite impressive: the fundaments of language.

One of these is "referential communication," or the ability to make sounds that don't just reflect some internal state, like a gasp of surprise or cry of distress, but refer to something specific and external: a crow, for example, or a rat snake, as described in research conducted over the last several years by Toshitaka Suzuki, an ethologist at Japan's Rikkyo University. Then, in a study published this year in Nature Communications, Suzuki and Michael Griesser of the University of Zurich investigated how the meaning of their calls changes depending on the order of sounds. Play a recording of a call sequence that means "scan for danger and come here," and the birds look to the horizon and flock to the loudspeaker, but reversing the chirps occasions no response. Put another way, the birds used syntax.

"We still use ourselves as a measuring stick. If an animal is sufficiently like us, only then are they worthy of being valued."

In human languages, syntax makes it possible to generate ever-more-varied meanings from a limited range of sounds. Scientists have long believed animals lacked both syntax and vocabulary, says Griesser. "The problem was that we didn't listen carefully enough."

So far only one phrase has been deciphered. Many more remain to be translated. If we could understand them, thinks Griesser, we'd mostly overhear conversation of immediate relevance to the birds: "I'm over here." "There might be food." "My territory." "Look out, a hawk!" There are limits, though, to what playback experiments can reveal. It's much easier to decipher "hawk" and "come here," which elicit obvious and easily quantifiable responses, than "How are you feeling?" or "I'm happy to see you."

That sort of chatter could be within the birds' cognitive power, and certainly should be relevant to their highly social life, but would be hard to test experimentally. Which is of a piece with a historical tilt in animal-intelligence studies toward more easily empiricized cognitions: De Waal himself shies away from matters of emotion and subjective experience. "Even with humans," he says, "it's a tricky topic," and in animals, "I'm not sure we'll ever get there." To be clear, de Waal's not asserting that rich animal emotions and feelings don't exist. He's just not optimistic about measuring them rigorously.

Some scientists respond to the other-minds problem by trying to be precise with their terminology. Declaring himself uncomfortable with anthropomorphic language, Hans Hofmann, a neurobiologist at the University of Texas at Austin, prefers to talk of stimuli varying in salience and valence depending on context. He doesn't disbelieve in animal emotion, noting that relevant neural substrates were present in the last common ancestor of all living vertebrates, and that "aspects of affective processing are present in a broad range of species," but he doesn't like the word. It's too vague.

Other researchers are suspicious of the very idea. Joseph LeDoux, a neuroscientist at New York University, sees "a wave of unconstrained mentalism" in language about animal "fear" and "pleasure" and "hunger." Animals might have subjective experiences, LeDoux says, but people shouldn't hasten to understand them in terms of our own. Human cognitive processes may very well produce inner experiences profoundly different from an animal's. Clive Wynne thinks our own experiences are shaped in fundamentally unique ways by human-specific cognition, especially — chickadee syntax not withstanding — our rich language.

That's possible, but it's also a hypothesis. Scientists don't know how language shapes human subjectivity; the foundations may well have been laid while our language still resembled that of chickadees, or for that matter Campbell's monkeys or prairie dogs, two other species in whom syntax has been found. Perhaps language does shape subjectivity, but in such a way that, as with mental time-travel, the basic components produce something recognizably similar if less sophisticated. And Griesser, who hopes to quantify the strength of chickadee affections by measuring how much time they spend watching out for their mates, challenges the very premise that language is of prime importance. "We humans don't think about emotions with words," he says, but, rather, sense feelings and wordless thoughts.

The ethologist and author Marc Bekoff thinks primary emotions — including fear, joy, happiness, jealousy, anger, love, pleasure, sadness and grief — are probably widespread and that hewing too closely to abstract description could become a form of what he calls "anthropo-denial." Take the neuroscientist Jaak Panksepp's experiments in the late 1990s with rats subjected to "playful, experimenter-administered, manual, somatosensory stimulation": If they emit vocalizations associated with positive emotional states, why not say — as Panksepp did — that they laugh when tickled?

I t's hard to imagine rats laughing or chickadees conversing without also imagining they're self-aware. Trying to conceive of experience absent a sense of self is practically a Zen koan: What is you if there is no you? In Not So Different, the molecular biologist Nathan Lents defines animal self-awareness as "a sense of themselves as distinct from other individuals and within the context of their environment and circumstances." It does not sound like a high bar to meet, but the idea remains contested.

Only a few species, including dolphins, elephants, orangutans, magpies and most recently manta rays, are able to recognize themselves in a mirror, which since the 1970s has been considered a foundational test of self-awareness. Human children usually pass it by the time they're 3 years old. Yet some researchers say reliance on the mirror test is misguided. Lori Marino, formerly a neurobiologist at Emory University who in 2001 was part of the research team that demonstrated dolphin self-awareness, thinks the emphasis placed on the test has made it a tool of exclusion: Animals who don't demonstrate our own particular form of self-awareness are denied the capacity altogether.

"We still use ourselves as a measuring stick," says Marino. "If an animal is sufficiently like us, only then are they worthy of being valued." De Waal shares some of her misgivings, arguing in Are We Smart Enough that every animal "needs to set its body apart from its surroundings and to have a sense of agency." Mirrors measure only one form of self-awareness, he says; many animals spend their entire lives without ever encountering a reflection and may rely on other cues, such as smell.

Joel Sartore

"This is certainly the case in fishes," wrote Culum Brown, a behavioral ecologist at Macquarie University, in a 2014 review of fish intelligence published in the journal Animal Cognition. "Chemical cues play a very important role in aquatic ecosystems. There is compelling evidence that fish are capable of self-recognition using chemical cues." Even fish recognize themselves and other individuals, then — creatures whose expressionless faces and alien habits so predispose people to thinking them unfeeling that even "vegetarians" eat them.

Fish are an especially interesting example of animal cognition studies expanding not only beyond species of evident intelligence, but beyond entire evolutionary groups and into parts of the animal kingdom where many scientists remain reluctant to posit similarities with humans. Or, to put it casually: Sure, we have some things in common with mammals and birds, but fish?

That tension was on full display in a recent debate held in the journal Animal Sentience on whether fish feel pain. The argument that they don't, championed by Brian Key, a neuroscientist at the University of Queensland, rests on neurological differences: Fish can have aversive experiences, but their brains are just too different to produce the emotional resonance crucial to what we understand as pain. Brown and others responded that, despite the anatomical dissimilarities, fish brains and chemistries could still generate something similar, and that behavioral studies certainly showed them acting like they felt pain. Key rejoined that fish brains are still poorly understood and the behaviors overinterpreted.

In some ways the debate felt like a litmus test for how different researchers weigh evidence. Georg Striedter, a neurobiologist at the University of California at Irvine, took a middle ground: "The debate cannot be settled yet," he wrote, and he noted that fish have demonstrated many other cognitive feats. These include what seems to be fear; the ability to count, as described in angel fish who differentiate between schools with different numbers of individuals; physiological stress responses considered markers of consciousness in other species; long-term memories; and even culture, described experimentally in nine-spined sticklebacks who learn feeding strategies from their compatriots.

Pain aside, there's clearly some extraordinary cognition going on underwater. While it can be misleading to talk generally of fish, of which there are roughly 30,000 species, Brown thinks that findings from model organisms, like those made in zebrafish or sticklebacks, can be extrapolated broadly. Gordon Burghardt, a University of Tennessee at Knoxville ethologist who in the 1980s coined the term "critical anthropomorphism" to describe how scientists could formulate hypotheses about other species by trying to imagine life from their perspective, has long lamented that turtles and other reptiles are, like fish, underestimated by virtue of their seemingly expressionless faces and unfamiliar habits. Many basic aspects of reptile life history remain unknown, and research in turtles has been skewed by a tendency to notice mostly what they do out of water, ignoring the social interactions that occur beneath its surface.

Aurora Photos

In the 1990s, Burghardt described turtles playing — or, in his careful language, engaging in "incompletely functional behavior differing from more serious versions structurally, contextually, or ontogenetically, and initiated voluntarily when the animal is in a relaxed or low stress setting." (Komodo dragons also seem to play; sped up on video, Burghardt notes, they look like dogs.) More recently he and Karen Davis, a doctoral student at the time, also found evidence of long-term memory in American red-bellied turtles, as well as an ability to learn by watching others. What might their emotional lives be like? "Although the nature of subjective experience is only partially accessible to objective science," Burghardt wrote this year in Animal Sentience, "we must keep trying to understand it." Certainly neurological networks fundamental to social interaction and emotional reward are present in them, as they are across all vertebrates.

For Burghardt, who remembers "when you couldn't even talk about animals being hungry because it was too anthropomorphic," the present moment is a tremendously exciting one. "In the period right after Darwin, scientists were looking for commonalities between humans and other animals, but they didn't have good tools or experimental designs," he says. "Now people are doing experiments on phenomena that 20 or 30 years ago nobody even looked at. They're finding abilities that we never thought animals would have."

In recent years scientists have even found that insects possess evolutionarily ancient brain structures responsible for creating mental maps of one's own place in space. Some researchers consider these structures foundational to human awareness; if they are, then insects, too, would appear to be conscious. Whatever it feels like to be a bee, it feels like something.

W hat that something is, how instinct and awareness interact, how different forms of memory shape experience, how evolution's convergences and divergences have shaped the development of cognition across time and circumstance — these are frontier questions now being asked. Science has come a long way from a reflexive adherence to C. Lloyd Morgan's wariness of "higher psychical faculty," or the famed behaviorist B.F. Skinner's insistence that other animals are "conscious in the sense of being under stimulus control" and experience pain with no more conscious resonance than "they see a light or hear a sound."

Other questions involve capacities like morality: Might its biological building blocks be widespread in the animal kingdom? Or what about motivation? After all, a human whose every physical need is provided for, but who doesn't actually do anything except sit in a room, won't be very happy. Beyond seeking pleasure, avoiding pain and procreating, what might an animal find fulfilling?

"I don't think I can understand that unless I try, with a whole lot of humility, to imagine what it would be like to be that animal," says Becca Franks, a cognitive psychologist at the University of British Columbia. "Then you take those insights to create an experimental, data-driven paradigm. That's how science proceeds."

Franks sometimes has misgivings about the emphasis placed on experimentation with animal brains. Even as scientists learn more about the depth of animal thoughts and feelings, they continue to treat animals as means to human ends. It's a concern shared by Lori Marino, whose research led to her present role as an animal advocate and activist, marshalling the science to argue for better ethics. "There's a lot of stuff I'd like to know," says Marino, "but I'm not going to kill a dolphin or stick electrodes in their brains or do invasive work just because I want to satisfy my curiosity."

Yet a great deal can still be learned in ethical ways; as with research on humans, ethical constraints can spur greater ingenuity. And as this research proceeds, Frans de Waal has called for a "moratorium" on claims of human uniqueness. "We are still facing the mindset that animal cognition can be only a poor substitute of what we humans have," he writes in Are We Smart Enough. Only by setting aside that preconception for a few decades may we "then return to our species's particular case" with a deeper basis for understanding what truly distinguishes us.

As for what to make of the animals I encounter while running along the creek, I think of research by Winnipeg's Susan Lingle. She describes how white-tailed deer mothers respond to distress calls from infants belonging to other mammal species, including marmots and cats and Homo sapiens. It's an automatic behavior, says Lingle, but probably accompanied by conscious awareness and concern. Those moms care about the distressed.

It calls to mind another line of research, on what's called "mental state attribution." If those deer mothers can respond to a human baby's cry, might they be imagining how that baby feels?

As described last year in the journal Animal Behaviour by two University of Vienna behavioral biologists, Esmeralda Urquiza-Haas and Kurt Kotrschal, mental state attribution refers to the tendency of animals to project thoughts and feelings onto other animals. The cognitive underpinnings of this, they say, are found across the animal kingdom. It seems to have been an evolutionarily favored way of making sense of the living world.

We're biologically predisposed to anthropomorphize, then, as are other creatures in their own species-specific ways. Turtles may turtle-pomorphize, frogs frog-pomorphize, and so on. As I'm watching a mother deer, making sense of her mind in terms of my own, she's probably doing the same to me.

Brandon Keim is a freelance journalist who writes about science, nature, and animals.