12.3: The Fraying of Food Webs

Terrestrial Food Webs: Defaunation and Pollution

It is now known that “ecosystems are built around interaction webs within which every species potentially can influence many other species,” and that the “trophic downgrading” that results from the loss of large apex consumers reduces food chain length and can lead to abrupt state changes in ecosystems “with radically different patterns and pathways of energy and material flux and sequestration” (Estes et al., 2011). Anthropocene defaunation is a more precise name for the phenomenon discussed in the previous section, since the term defaunation can cover loss of individuals, populations, and species of wildlife (Dirzo et al., 2014); it is a term that needs to become as widely recognized as deforestation, since “a forest can be destroyed from within as well as from without” (Redford, 1992), as will be discussed in more detail in Section here . Human hunting is increasingly taking a toll, especially on the larger animals, while other proximate drivers of overall terrestrial defaunation include habitat destruction, the invasion of nonnative species and climate change.

Large-bodied animals that feed at the ‘apex’ of trophic pyramids, like the great cats and other true carnivores, often exert strong top-down regulatory effects on the ecosystems they inhabit (see Ripple et al,. 2014), so the loss of a carnivore at the highest trophic level can “cascade” down through all the trophic levels in an ecosystem. When sea otters were removed from waters off the coast of Alaska, sea urchins, released from otter predation, devastated kelp beds, until they themselves were ‘fished out’ from many parts of the ocean (see Steneck, 2002); likewise, when dam construction in Venezuela created a chain of predator-free islands, leaf-eaters–howler monkeys, iguanas and leaf-cutter ants—were released from predation and there was a subsequent reduction in young canopy trees (Terborgh et al., 2001). Conversely, when an apex predator, the grey wolf, was reintroduced into Yellowstone National Park, ^[4] wolf territories reduced elk grazing pressure on young aspen stands, allowing the forest to regrow and ultimately changing the landscape in a remarkable manner (see Ripple & Beschta, 2011). Large herbivores like bison and elephants are also important components of ecosystems, acting as “ecosystem engineers” by trampling and consuming vegetation (Ripple et al., 2015); they can also be important seed dispersers, and as herbivore populations become depleted around the world, a “wave of recruitment failures” is expected among animal-dispersed trees. While not typically apex consumers, primates are important seed dispersers as well, as are fruit-eating and nectar-feeding bats and many kinds of birds, which are also important in pollination and insect control.

Meanwhile, so far nothing has been said about invertebrate life—“the little things that run the world,” as E. O. Wilson called them more than 30 years ago, when the current situation was barely imaginable; even then, however, he expressed doubt “that the human species could last more than a few months” if they all disappeared (Wilson, 1987). Now several recent studies are highlighting alarming trends. Hallman and colleagues (2017), counting insects in nature reserves surrounded by agricultural fields within a typical Western European landscape, reported a decline in the biomass of flying insects of about 80% over 30 years—an average loss of 2.8% biomass per year that, if continued, could result in a total loss within the century. A parallel decline was observed in larks, swallows, swifts and other insectivorous birds, leading one of the researchers to comment, “if you’re an insect-eating bird” living in the areas studied, “four-fifths of your food is gone in the last quarter-century, which is staggering” (see Vogel, 2017). A similar 60-80% drop in biomass over 36 years was recorded for insects living in the tree canopy of a tropical forest, as well as a 98% drop in insects from the forest floor (Lister & Garcia, 2018), with “synchronous declines” documented in the lizards, frogs and birds dependent upon them for food.

Reviewing of more than 70 reports of insect decline from around the globe, Sanchez-Bayo and Wyckhuys (2019) compiled evidence of “dramatic rates of decline” in insect numbers that, if continued, they projected could “lead to the extinction of 40% of the world’s insect species over the next few decades.” More recently, Seibold and colleagues (2019) reported “widespread declines in arthropod biomass, abundance, and the number of species across trophic levels” in both grassland and forest habitats, finding the major drivers of the declines to be largely associated with agriculture at the landscape level. “Our study confirms that insect decline is real,” Seibold told BBC News, noting that it is occurring in protected areas as well as those that are intensively managed (Briggs 2019). A group of conservation biologists “deeply concerned about the decline of insect populations worldwide” provided a comprehensive overview of the problem and issued a “scientists’ warning to humanity” about the seriousness of this problem as this chapter was undergoing its final edit (Cardoso et al., 2020).

Since insects are adapted to a very narrow range of temperature variation in the tropics, climate warming may be a factor in insect decline there, but elsewhere the “root cause” of the dramatic decline is thought to be the intensification of agriculture and, in particular, “the widespread, relentless use of synthetic pesticides,” according to Sanchez-Bayo and Wyckhuys (2019). As the most widely used insecticides in the world, neonicotinoid insecticides are highly suspect as a major driver of this decline. They are systemic, meaning that they are absorbed and distributed to all parts of the plants they are applied to, not only leaves and flowers but pollen and nectar. They persist in soils for a year or more, but are water soluble, contaminating up to 80% of surface waters; there they affect a variety of aquatic insect larvae, indirectly reducing populations of fish, frogs, birds, bats and others that feed on them. Along with fipronil, the neonicotinoids are suspected of playing a large role in the decline of honeybees, bumblebees and other wild bees around the world (Sanchez-Bayo, 2014); foraging bees typically take contaminated pollen and nectar back to the hive, where sublethal effects of these neurotoxic insecticides affect movement, olfaction, orientation, and navigation, impairing the mushroom bodies (see Section here) important in bees’ learning and memory, disturbing foraging and homing behavior and disrupting the “waggle dance” ^[5] used to communicate the location of nectar plants to other bees in the colony (van der Sluijs et al. 2013). These synthetic insecticides disrupt biological controls and trigger pest resistance, and they don’t really contribute to crop yields, according to Sanchez-Bayo and Wyckhuys, so there will be “no danger” in reducing their use drastically (2019).

Meanwhile, the escalating use of herbicides–especially glyphosate, the active ingredient in Roundup, widely used around the world now in combination with genetically modified crops—is leading to growing concerns about their effects on soil invertebrates, as well as soil microorganisms, the functioning of below-ground ecological communities, and the aquatic communities downstream of agricultural runoff. According to Benbrook (2016), about 8.6 billion kg have been applied worldwide over the last 40 years, with dramatic increases over the last decade or so. Glyphosate acts by inhibiting the EPSPS enzyme in the shikimate pathway, essential to metabolism in plants, fungi, and some bacteria but absent in vertebrate animals, so it was originally assumed to pose minimal risks, but a potentially serious effect on honeybees has recently been reported, illustrating the complexity of ecological systems: genomes of the beneficial bacteria in honeybee gut flora contain the gene coding for EPSPS, potentially making them susceptible to glyphosate inhibition, possibly increasing mortality and reducing their effectiveness as pollinators around agricultural fields (Motta, Raymann & Moran, 2018).

Glyphosate is absorbed from the leaves of sprayed plants and transported systemically to the roots; it can be released into the rhizosphere, possibly being transferred through the roots of dying plants to living, untreated ones, affecting trees and other plants near treated fields. Kremer and Means (2009) found glyphosate interacted with the below-ground microbial community, and Kremer (2014) reported herbicide-resistant weed infestations release root exudates potentially detrimental to the mycorrhizal fungi, important for plant uptake of nutrients and water. A review article by Annett, Habibi and Hontela (2014) examines the reported effects of glyphosate and formulations with different surfactants on organisms in freshwater ecosystems, noting amphibians seem particularly susceptible to its toxic effects due to their larval dependence on water and frequent location near agricultural fields. There are also growing concerns about its effects on human health, especially since high residue levels are being found on crops subjected to post-season drying (“green burndown”) with glyphosate (Myers et al., 2016); studies on residues, and the concept of “substantial equivalency,” have been criticized as inadequate (Cuhra, 2015). In 2015, the World Health Organization found “sufficient evidence of carcinogenicity in experimental animals” and “limited evidence of carcinogenicity in humans for non-Hodgkins lymphoma” following exposure to glyphosate (WHO, 2015).

Predictably, more than 200 weed species have developed resistance to one or more herbicides, with at least 24 of them resistant to glyphosate (Heap, 2013). In response, biotechnology companies are developing second-generation, “stacked” GM crops with resistance to several herbicides, typically 2,4-D and dicamba, containing synthetic auxins that interfere with the natural plant hormones involved in growth regulation; they are reportedly of low toxicity to vertebrates but extremely toxic to broadleaf plants, and their high volatility and proneness to drift risks injury to both non-GM crops and nontarget plant species, according to Mortensen and colleagues (2012). Noting that the evolution of resistance to both herbicides and insecticides is outstripping our ability to come up with new ones, Gould, Brown and Kuzma (2018) discuss why we “mostly continue to use pesticides as if resistance is a temporary issue,” calling it a “wicked problem” arising from a combination of social, economic and biological factors that decrease incentives for taking a different approach to “pest” control.

According to Hayes and Hansen (2017), “there is probably no place on earth that is not affected by pesticides; they report that an estimated 2.3 billion kilograms of pesticides are being used annually around the world, and they review evidence of alterations in landscapes, populations and gene pools of organisms from both actute toxic and chronic “low dose” effects. Many older, “legacy chemicals” are also still around, contaminating food webs around the world (Matthiessen, Wheeler & Weltje, 2018). The organochlorine insecticides, “hard” pesticides like DDT, were banned in most developed countries years ago but are still in widespread use, with 3.3 million kilograms produced annually (Hayes & Hansen, 2017); these, along with other chemicals such as polychlorinated biphenyls (PCBs), are known as persistent organic pollutants (POPs)– long-lived, fat-soluble compounds that are known to accumulate in animal tissues and biomagnify, increasing in concentration as they move up food chains, often reaching very high levels in apex predators. Many of the POPs have been shown to be toxic, endocrine-disrupting and/or carcinogenic, and long-lived vertebrates occupying high trophic levels not only risk such effects from retaining these chemicals in their own bodies for long periods of time but potentially pass them on to offspring in eggs or milk (Rowe 2008). Kohler and Triebskorn have drawn attention to how little we know about the full extent of unintended impacts of pesticides on wildlife at the higher levels of populations, communities and ecosystems (2013); immunosuppression reportedly can be caused by all the organochlorine, organophosphate, and carbamate insecticides as well as by atrazine and 2, 4-D herbicides.

Moreover, in addition to the biocides—chemicals intentionally designed to kill certain forms of life, the “pesticides” that include rodenticides, insecticides, herbicides, fungicides, and so on—there are over 4000 pharmaceuticals now in global use in human and veterinary medicine continuously being released into the environment through wastewater and sewage sludge; they are generally highly potent at low concentrations, and their modes of action show strong evolutionary conservation across vertebrate species–meaning that what affects us will probably affect many other lifeforms somewhat similarly. An Australian team found over 60 pharmaceutical compounds in the bodies of invertebrates collected from streams and in riparian spiders consuming them, considering them likely to be contaminating other consumers such as frogs, birds and bats (Richmond et al., 2018); they calculated that vertebrate predators on aquatic invertebrates such as the platypus could consume as much as half a human’s therapeutic dose of antidepressants, kilogram for kilogram.

Finally, it should be noted that pollution from small particles of plastic—“microplastics”—which is a growing concern in the world’s oceans, to be discussed in Section here, is problem for terrestrial ecosystems as well. A recent study found that microplastics are being carried by the wind to places far from population centers and are likely distributed widely around the planet; daily counts of atmospheric deposition averaging almost 250 fragments 3 mm or less in size per square meter were found in a remote and supposedly “pristine” mountain area of the French Pyrenees (Allen et al., 2019). “It suggests that this is a far bigger problem than we have currently thought about,” says one of the study’s co-authors; the concern is that it “gives us a background level of microplastic that you probably get pretty much everywhere in the world” (see Thompson, 2019). If there are worries about this atmospheric deposition contaminating soil, however, here’s an even bigger source of that problem: some farmers use treated sewage sludge to fertilize their fields, adding a load of microfibers skimmed off of wastewater along with the nutrients that could add up to tens to hundreds of thousands of tonnes of plastics added to farmlands in Europe and North America every year (Thompson, 2018a); yet another soil additive, moreover, is so-called “mixed waste—a ground-up amalgam of food scraps and unrecyclable material” that, applied thickly on one farm in Australia, added so much plastic to the topsoil that it looked like it was “glistening.” And yes, it’s finally happened—“anthropogenic debris” has been reported in beer, as well as sea salt and tap water (Kosuth, Mason & Wattenberg, 2018). It seems microplastics are now everywhere—they have even been found in human feces (Parker, 2018).

Marine Food Webs: Overfishing, Disruption and Collapse

Ransom Myers and Boris Worm startled the scientific community with their announcement (2003; see SeaWeb, 2003) that “the global ocean has lost 90% of large predatory fishes,” along with “general, pronounced declines of entire communities across widely varying ecosystems.” The decrease in many marine vertebrates has been severe enough that too few of them remain to carry out their normal functional role in many ecosystems, in some places leaving “empty estuaries” and “empty reefs” similar to the “empty forests” in terrestrial systems (McCauley et al., 2015). The striking marine defaunation is recent, since fishing effort intensified only over the last century with the arrival of industrial fishing techniques, the loss of fish being followed by a decline in sea turtles, sea birds, and marine mammals. As Crespo and Dunn (2017) summarize, “the world’s oceans are experiencing an unprecedented level of biotic exploitation, which is altering the abundance and population structure of many species, transforming the composition of biological communities, and threatening the integrity and resilience of entire marine ecosystems.” Marine biologist Daniel Pauly and colleagues explain (1998) that fisheries around the world have shown a pattern over recent decades of “fishing down the food web,” where what is caught is transitioning from “long-lived, high trophic level, piscivorous bottom fish toward short-lived, low trophic level invertebrates and planktivorous pelagic fish,” often with complete collapse of the high trophic level species and replacement with lower trophic level species in fishing catches.

Changes in Chesapeake Bay illustrate how these changes evolved in one coastal community. According to Jackson et al. (2001), “gray whales, dolphins, manatees, river otters, sea turtles, alligators, giant sturgeon, sheepshead, sharks and rays were all once abundant inhabitants of Chesapeake Bay but are now virtually eliminated.” Until the end of the 19^th century, the Bay contained dense concentrations of oysters, filter feeders that consumed phytoplankton so efficiently that algae blooms never occurred, even with agricultural runoff. Introduction of mechanical harvesting in the late 1800s had a serious impact on the oyster reefs by the early 20^th century and decimated them by the 1920s. Eutrophication began to be observed in the Bay by the 1930s. Today, with the oyster reefs essentially destroyed, Chesapeake Bay is now considered a “bacterially dominated ecosystem,” with a trophic structure completely different from what it was a century ago; it is characterized by “population explosions of microbes responsible for increasing eutrophication,” and, in combination with hypoxia, disease, and continued dredging, this now prevents the recovery of oysters and their associated ecological community (Jackson et al., 2001).

Coral reefs are in decline around the world due to global warming-induced coral bleaching, and the combination of higher temperatures and increasing acidification of ocean waters as they absorb \(\ce{CO2}\) may at some point drive them over a ‘tipping point’ into algae-dominated states ^[6]; according to Hoegh-Guldberg et al. (2007), at atmospheric \(\ce{CO2}\) levels nearing 500 ppm, “reefs will become rapidly eroding rubble banks, as are already seen in parts of the Great Barrier Reef.” Australia’s Great Barrier Reef—the world’s largest and most diverse coral reef ecosystem–has undergone mass bleaching events four times over the last twenty years, the northern two thirds being severely damaged by the last two in 2016 and 2017, with the concomitant heat stress killing many reproductive adult corals, leading to nearly a 90% drop in larvae recruited into the population in 2018 (Hughes et al., 2019). Many reefs are also suffering from overfishing, with loss of the larger predatory fish cascading through the system, allowing the escape of smaller fishes and invertebrates that causes booms and busts of algal overgrazing, such that “today, the most degraded reefs are little more than rubble, seaweed, and slime”; these researchers also report that many reefs off the coast of Florida are “well over halfway toward ecological extinction” (Pandolfi et al., 2005).

Perhaps the best-known example of marine defaunation, however, is the ‘crash’ of the Northern Atlantic cod fishery off Newfoundland and Labrador in 1992, which apparently came as quite a surprise to the fishery operators and regulators. Atlantic cod had been harvested for centuries, but with modern harvesting equipment and factory ships arriving in the 1950s, catches went from around 227-327,000 tonnes per year to a peak of 735,000 tonnes in 1968 and then began to diminish, and were down by 80% by 1977. Harvesting was then restricted, but the cod never recovered to anywhere near their previous levels; technological advances in locating and capturing fish allowed increasing catch sizes despite “dramatic declines in catch rate,” concealing the true condition of the cod population throughout the 1980s until its sudden collapse (Hutchings & Myers, 1994). The cod still haven’t come back significantly, and cascading effects within the marine ecosystem have allowed small pelagic fish like herring that principally feed upon zooplankton—which include the eggs and larvae of the cod– increased in biomass by around 900%, effecting a “predator-prey role reversal” that may be largely responsible for preventing cod recovery (Frank et al., 2005; Frank et al,. 2013).

Tunas are another group of particular concern. More than 60% of the tuna harvest is captured in purse seines, giant nets that pull up from below to encircle entire schools of tuna and other schooling fish once they are located with sophisticated sensing technologies, taking a significant amount of ‘bycatch,’ other species that are (usually) unintentionally caught up in the seine nets, such that “tuna fisheries are directly responsible for endangering a wide range of oceanic pelagic sharks, billfishes, seabirds, and turtles” (Juan-Jorda et al., 2011) as well as marine mammals, killing around 1000 dolphins a year and harming many more (see Brown, 2016). Unlike the cod, overall tuna catches have continued to increase since the 1950s, but this continuing increase “was achieved by halving global tuna biomass in half a century” (Juan-Jorda et al., 2011). Tunas and their relatives, along with the billfish–swordfish and marlins–are apex predators of pelagic food webs, so they very likely exert important trophic effects within the whole ocean ecosystem; unfortunately, some of them are highly valued economically and thereby increasingly threatened with extinction, with the biomass of the Southern Bluefin tuna is now said to be about five percent of its original size, so its population “has already essentially crashed,” paralleling the trend of the western Atlantic Bluefin, whose population has not rebuilt since it plummeted in the 1970s (Colette et al., 2011). Individual Bluefin tunas were selling at over $100,000 five years ago, making them among the “rhinos of the ocean”—for those of a certain mindset, they will “never be too rare to be hunted” (McCauley et al., 2015).

And it is clear all is not well with marine fisheries globally. Daniel Pauly, attempting to reconstruct the historical sizes of fish populations, concluded that most of his colleagues had fallen prey to the “shifting baselines syndrome,” ^[7] whereby each new generation of scientists takes the stock sizes that prevailed at the beginning of their careers as the ‘baseline’ and evaluates changes in relation to it, not noticing that the baseline itself has been gradually shifting downward (Pauly, 1995), a phenomenon he has described in a (2010) TED talk. ^[8] In a recent interview (Schiffman, 2018), Pauly called the global industrial fishing industry “a Ponzi scheme,” explaining, “a Ponzi scheme is where you pay your old investors money from new investors, not from any actual profit.” That’s what’s been happening as industrial fisheries have developed over the last 50 or 60 years, he charges—“we fish out one place, European or North American waters, for example, then we go to Southeast Asia or Africa, now even Antarctica.” With the new technologies that have become available, “we’ve destroyed all the protections that fish populations once enjoyed”—“depth was a protection, cold was a protection, ice was a protection because we couldn’t fish in those areas”—but “we can now go everywhere the fish once sheltered.” Global catches have been declining by one to two million tonnes a year since the mid-1990s, he reports; we’re getting up against the limits of the Earth now, it seems, and when you run out of new fishing stocks to exploit, “the whole [Ponzi] scheme collapses.”

But what’s happening to populations of deep-sea organisms may be cause for even more concern. Most deep-sea fisheries utilize bottom trawls, fishing gear that drags a net along the ocean floor and that can weigh several tonnes and do tremendous damage to the benthic habitat. One study found that, compared with the impacts of oil and gas drilling, submarine communications cables, marine scientific research, and the historical dumping of radioactive wastes, munitions and chemical weapons, “the extent of bottom trawling is very significant and, even on the lowest possible estimates, is an order of magnitude greater than the total extent of all the other activities” (Benn et al., 2010). Moreover, bottom trawling activities can be concentrated on ocean ridges and seamounts, which are particularly vulnerable to the effects of such disturbance. Seamounts are “true mountains under the sea,” usually 2-3 kilometers in height, that have become covered with sessile invertebrates including octocorals, hard corals, sponges, crinoids, and other suspension feeders that structure the habitat for fish but that are very fragile and easily broken (Watling & Auster, 2017). Daniel Pauly tries to describe what was “encountered” by a trawler in his “shifting baselines” TED talk: “Well,” he says, at the time “we didn’t have words for it,” but now he knows, “it was the bottom of the sea”; 90% of the catch was made up of sponges and other organisms that had been attached to the bottom, while any fish that were caught were just “little spots on the piles of debris.” The “most rational decision,” according to Watling and Auster, is to simply protect seamounts in perpetuity; meanwhile, Pauly advocates closing off the “high seas”—the open ocean outside the control of the coastal countries, which extends out to 200 miles offshore—from fishing, allowing many fish populations to rebuild and very likely increasing the harvestable catch of many less-developed coastal nations, while Eileen Crist has called for declaring the whole “area” of the high seas off limits to all extractive activity, for fish and fossil fuels as well as for minerals, renaming it “the common heritage of all Life” (Crist ,2019).