Toxoplasma gondii finding in beluga whales points same way as sea otter and monk seal studies––& not toward cats
MONTREAL––A new study widely publicized for allegedly linking domestic cats to losses of endangered beluga whales in the St. Lawrence River estuary actually shows almost the opposite, read in context––and contributes to a growing stack of evidence that the original host reservoir for the sometimes deadly Toxoplasma gondii parasite may be not cats, but an as yet unidentified saltwater-dwelling marine species.
Whether the St. Lawrence River estuary beluga whale population is actually declining is also in question. The small beluga colony, isolated since glacial times from the Arctic-dwelling main population, is often said to be declining at the rate of 1% per year.
But beluga counts are not really down
Estimates produced since 1973 from actual counts, however, while ranging from as few as 650 belugas to as many as 1,600, have consistently averaged about 900, according to a 2017 literature review by beluga enthusiast Robert Michaud, scientific director and co-founder of the Group for Research & Education on Marine Mammals.
Thus there is little evidence of either a decline or an increase in the beluga population, attributable to cats or anything else.
Published on September 27, 2018 in the online peer-reviewed journal Diseases of Aquatic Organisms, the new study, by four co-authors, is formally entitled “Toxoplasma gondii infection in stranded St. Lawrence Estuary beluga Delphinapterus leucas in Quebec, Canada.”
Necropsies don’t indict toxo for beluga deaths
“Of 34 beluga tested, 44% (15 beluga) were positive for Toxoplasma gondii,” the co-authors explain in their abstract. “Molecular analyses indicated that all Toxoplasma gondii infecting stranded St. Lawrence Estuary beluga grouped into genotype II, which predominates in humans,” and is usually contracted by humans from consuming undercooked meat.
“While our results indicate that a high prevalence of stranded beluga are positive for Toxoplasma gondii infection,” the co-authors emphasize, “very few deaths are attributed to toxoplasmosis based on published necropsy results. Toxoplasma gondii can cause a range of diseases, including neurological deficits, and more data are needed to investigate this parasite’s effect on [beluga] population recovery.”
“Presence can have an impact”
Restated study co-author Stéphane Lair, a professor of veterinary medicine at the Université de Montréal, to Sidhartha Banerjee of Canadian Press, “It does not mean that belugas died of this parasite. It means there was a presence either in their heart or their brain. We know that it’s a parasite that can kill belugas, so its presence can have an impact on their lives,” Lair acknowledged.
However, Lair continued, “Marine animals in North America have been in contact with this parasite for thousands of years.”
The only animals in whom Toxoplasma gondii is known to produce the oocysts, or eggs, necessary to completing the entire life cycle of the widely distributed parasite, are felids: members of the cat family.
Toxo link to cats raises questions, not answers
But cats were first identified as potential primary hosts only in the 1960s, and the linkage has always raised more questions than it answered.
For starters, Toxoplasma gondii may have existed long before the first felids evolved, about 25 million years ago. And, if felids––few of whom spend much time in or near water––were the original Toxoplasma gondii host species, how did Toxoplasma gondii come to be widely distributed in marine habitats, in regions where there are few felids of any sort––or none?
Why, given the ubiquitous distribution of Toxoplasma gondii, have other land-dwelling hosts not emerged?
Few felids in the Arctic
Why have Toxoplasma gondii strains not evolved who can complete their entire reproductive cycle in species such as foxes, fishers, weasels, mink, or hyenas, whose diets and lifestyles parallel those of felids?
Researchers who identified Toxoplasma gondii in Arctic beluga whales in 2014 speculated that the parasite might have reached the Far North with lynx, bobcats, or pumas.
But even Eurasian and Canadian lynx, the northernmost felid species, rarely reach the Arctic Circle habitat favored by belugas.
Also few felids along the lower St. Lawrence
For the St. Lawrence estuary belugas, whose breeding habitat is off the small city of Tadousac, at the mouth of the Saguenay River, Lair suggested that “The big difference in the last few centuries is the introduction of domestic cats — a new definitive host for the parasite that probably has contributed to an increase in the amount of toxoplasma those mammals are exposed to.”
That hypothesis, however, overlooks that even today domestic cats are few along the sparsely inhabited banks of the Saguenay River, which flows for 110 miles southeast from Lac St. Jean before entering the St. Lawrence.
Neither are domestic or feral cats, or any other cat species, abundant along either shore of the St. Lawrence River east of Tadousac, by far the greater portion of the St. Lawrence estuary.
Probably more cat feces decades ago
Free-roaming cats undoubtedly shed Toxoplasma gondii oocysts in Montreal, Quebec City, Sherbrooke, Trois Rivieres, St. Jean, Sorel, and other cities whose storm drains flow either directly into the St. Lawrence or into St. Lawrence tributaries, well to the southwest and upstream from Tadousac.
Cat owners may flush Toxoplasma gondii oocysts with cat feces in all of these places.
But almost certainly far more Toxoplasma gondii oocysts reached the St. Lawrence decades ago, before the present Montreal sewage interceptor and treatment system was belatedly completed in 1998, long after most other Quebec cities developed sewage treatment systems, when low-cost cat sterilization programs had yet to reach Quebec and the animal control agencies of Montreal and suburbs annually collected and killed more than 10 times as many free-roaming cats as in recent years.
So how were belugas infected?
If Toxoplasma gondii oocysts from cats are infecting St. Lawrence estuary belugas now, this must have been happening on at least as large a scale for decades without ever before being noticed.
Be that as it may, the infected St. Lawrence estuary belugas, like other infected animals, are believed to have ingested Toxoplasma gondii oocysts somehow.
The most commonly mentioned hypothesis is that the ingested Toxoplasma gondii oocysts infecting any species somehow come from cats. But this is far from the only hypothesis, and reality is that most of the science needed to definitively identify the Toxoplasma gondii host reservoir has yet to be done.
Changing beluga diet
Felids may be the only land animal in whom the entire Toxoplasma gondii occurs, but investigating potential marine animal and avian hosts has barely begun.
Beluga whales consume more than 100 prey species, depending on habitat, including capelin, herring, shrimp, salmon, Arctic cod, halibut, flounder, and crab.
University of Manitoba research fellow David Yurkowski in 2017 reported in the peer-reviewed journal Biology Letters that “beluga whales in parts of the North appear to be shifting away from eating Greenland halibut and are instead targeting capelin — a small, shiny fish that is becoming more common in the Arctic due to climate change,” summarized Bryce Hoye for CBC News.
This may be an effect of global warming.
“Belugas used to eat more Greenland halibut from the 1980s through the early 2000s,” Hoye continued. “But Yurkowski says now, in his research area of Cumberland Sound — an inlet that stretches inland in the southeast of Baffin Island — the whale species is preying on the comparatively smaller capelin.
“Arctic cod have traditionally been a keystone prey item in the area,” Hoye explained, “but they’re becoming less common there. Yurkowski said the cod populations could be dwindling thanks to increased competition for food with capelin or other southerly species that are starting to colonize the Arctic oceans.”
The same observation may apply to the St. Lawrence estuary, where capelin have apparently always been a beluga dietary staple, but maybe more so, since the regional cod stocks crashed due to overfishing more than 30 years ago, and have not recovered.
Could capelin be a primary host for Toxoplasma gondii?
The short answer is, no one really knows yet, but recent study after recent study has hinted that much more research into marine hosts seems to be warranted.
For example, excessively simplified news reports, compounded by hyperbolic alerts from conservation organizations that view cat predation as a threat to wildlife, have established in the public imagination that hardy Toxoplasma gondii oocysts shed by cats are somehow responsible for Toxoplasma gondii infections killing sea otters along the central California coast.
Scientific data, however, has yet to establish any such link.
Toxo cannot flow down a dry gulch
Problem #1 is that there are few year-round streams along the thinly developed stretch of California coast overlooking the sea otter habitat in question which could pollute the waters with Toxoplasma gondii oocysts, even if cats were defecating near the dry flash flood channels in significant numbers––which they are not.
The region, extending roughly from Monterey south to Santa Barbara, is nearly as dry as Death Valley and the Mojave Desert. This is why it is the only major stretch of undeveloped coast between San Francisco and Los Angeles––and why sea otters survived there for decades unobserved, after having been hunted to extirpation everywhere else south of Alaska.
Marine transmission cycle?
Reported P.A. Conrada and nine co-authors from six institutions in a much cited 2005 study entitled Transmission of Toxoplasma: Clues from the study of sea otters as sentinels of Toxoplasma gondii flow into the marine environment, “A reasonable and testable hypothesis is that Toxoplasma gondii infection is via ingestion of environmentally resistant oocysts secreted by terrestrial felids, but this rationale presupposes that the intermediate host range for Toxoplasma gondii is restricted to warm-blooded animals.
“The question of whether non-mammal marine species could also serve as intermediate hosts for Toxoplasma gondii replication is unknown. No reports have been published whether it is possible for Toxoplasma gondii to infect and/or replicate in fish, amphibians, invertebrates and/or other aquatic animals in either freshwater or marine ecosystems.
“If these atypical hosts were shown to be sources of infection for otters, then it would be possible to invoke a marine transmission cycle as a potential source for the high rates of Toxoplasma gondii seropositive marine animals.”
California Polytechnic State University at San Luis Obispo researcher Gloeta Massie in 2008 reported having found through laboratory experimentation that about two-thirds of northern anchovies who were exposed to Toxoplasma gondii oocysts became infected.
Anchovies are among the most abundant and widely distributed prey of marine mammals, and have historically been abundant in California sea otter habitat. Anchovies are also abundant in the habitat for several other marine mammals known to have been infected by Toxoplasma gondii, including Hawaiian monk seals, a species living as far from any significant concentrations of felids as Artic belugas.
Canned cat food
The finding that anchovies are susceptible to Toxoplasma gondii also hinted that domestic cats may have been infected by anchovies, first canned and marketed as cat food circa 1930. Domestic cat feces could in turn have infected the other felids in whom Toxoplasma gondii occurs.
The use of anchovies for cat food grew explosively with the rise of keeping pet cats, from the mid-1950s on. The first association of cats with Toxoplasma gondii came about a decade later.
Massie did not establish that northern anchovies are a host for Toxoplasma gondii oocysts. But neither did her research refute that possibility.
Herring––& capelin again
A year later, USDA microbiologist Jitender P. Dubey and eight co-authors published Toxoplasmosis in Captive Dolphins & Walrus, a study examining Toxoplasma gondii infections in eight bottlenose dolphins, seven Pacific walruses, ten California sea lions, seven harbor seals, and two gray seals housed at a Canadian exhibition facility.
“The pinnipeds and dolphins are both fed a diet consisting primarily of herring and capelin,” Dubey et al wrote.
The eight dolphins and seven walruses had become infected, despite extensive precautions taken to prevent any sort of contamination of their food and habitat––a hint that either herring or capelin might harbor Toxoplasma gondii oocysts.
Oysters & mussels
“The mechanism of Toxoplasma gondii infection in marine mammals is most intriguing,” Dubey et al assessed, “because their main staple diet includes fish or invertebrates, i.e., cold-blooded animals, or [e.g. manatees and dugongs] they are exclusively herbivorous. Thus, ingestion of Toxoplasma gondii–infected meat is unlikely. Toxoplasma gondii infection of dolphins is even more intriguing because they drink little or no water; their water requirements are satisfied by consumption of fish, squid, or other cold-blooded sea animals. Accidental ingestion of infected carcasses of birds or rodents, or of water contaminated with cat feces, may occur. This route, however, probably does not play a significant role in the high seropositivity in marine mammals.”
Previous research “suggested that land-based surface runoff was a significant risk for Toxoplasma gondii infection in sea otters,” Dubey et al summarized, “because the Toxoplasma gondii oocysts could be washed into the sea via runoff contaminated by cat excrement. Toxoplasma gondii does not parasitize any cold-blooded vertebrates. However, molluscs (a major food source for dolphins) can filter large quantities of water and, consequently, concentrate Toxoplasma gondii oocysts. This idea is supported by experimental data showing that Toxoplasma gondii oocysts can be concentrated by oysters and mussels.”
But where do the Toxoplasma gondii oocysts come from originally, to be concentrated?
Dubey reported in 2010, overlooking the Massie finding, that “Toxoplasma gondii has never been observed in fishes.”
Relatively few of the estimated 25,000 published studies of Toxoplasma gondii, however, have looked at fish as a potential host.
A recent exception was “The zebrafish, Danio rerio, as a model for Toxoplasma gondii: An intial description of infection in fish,” by Justin L. Sanders and eight co-authors, published in the Journal of Fish Diseases in 2015.
Zebrafish, commonly used in laboratory studies, are in the globally distributed minnow family, among the most abundant of freshwater fish.
Sanders et al acknowledged that previous researchers “could not establish Toxoplasma gondii oocysts infections in goldfish,” also a freshwater species. Goldfish, however, are members of the carp family: primarily bottom-feeders, whereas minnows are mostly found near the surface of their habitat.
While goldfish did not become infected by to Toxoplasma gondii, Sanders et al noted that “Two parasites have been reported in fish that show similarities to Toxoplasma gondii oocysts,” albeit that “as no sequence data are available for these parasites, it is not possible to determine their taxonomic affinities with Toxoplasma gondii oocysts or related organisms.”
Nonetheless encouraged, Sanders et al introduced Toxoplasma gondii to zebrafish, finding that it appeared to have killed three of the fish, while others showed “clinical signs” of Toxoplasma gondii infection.
As with the anchovy research, the zebrafish finding does not mean that zebrafish in specific, or minnows in general, have been identified as possible host species for Toxoplasma gondii oocysts.
What it does suggest, though, is that while bottom feeders (goldfish) and saltwater species occupying a similar niche in the marine food chain (anchovies) appear to be capable of harboring Toxoplasma gondii oocysts without suffering immediate harm, a comparable surface-feeding freshwater species (zebrafish) is not only susceptible to Toxoplasma gondii infection but apparently has little resistance to it.
Parasites usually evolve to infect the intermediate hosts of most abundance and proximity. The species most exposed to parasites tend to develop the strongest resistance to whatever infections the parasites transmit, a tendency that benefits the parasites as well as the hosts, since dead hosts can no longer feed the parasites.
If land-dwelling felids were the original hosts of Toxoplasma gondii, logically minnows would have more exposure to Toxoplasma gondii oocysts through runoff than either goldfish or anchovies––and hence would have developed greater rather than lesser resistance to infection.
Accordingly, the anchovy, goldfish, and zebrafish research, examined together, hints at a saltwater marine species having been the original host reservoir for Toxoplasma gondii, not a terrestrial species such as cats.
Yet another recent study, published in 2016 by the Journal of Wildlife Diseases, hinted indirectly that Toxoplasma gondii comes originally from a saltwater marine host. This study found that 21% of the rare nene goose tested on the island of Kauai, Hawaii, had been exposed to toxoplasmosis, and purported to indict cats as a potential cause of the scarcity of nene.
But the findings suggested not that Toxoplasma gondii killed nene, but rather that infected nene tend to recover. This might suggest that nene were first exposed to Toxoplasma gondii long enough ago to have evolved resistance to it––probably beginning long before the first cats arrived in Hawaii in 1778.
HSUS & Vox Felina react
Humane Society of the U.S. senior vice president Andrew Rowan called the toxoplasmosis-and-belugas research “Part of the current anti-cat obsession among wildlife biologists. Cats are the obligate host for toxo,” Rowan said, “but I suspect that toxoplasmosis is pretty low on the list of threats to belugas. Let’s start with PCBs and heavy metals and give humans the pride of place as the invasive species.”
Agreed Vox Felina blogger Peter Wolf, “Some additional context is in order here. The study cited here makes clear that Toxoplasma gondii was identified in just 2% of the mortalities for which cause of death was attributed. One is reminded of the many sensationalist headlines—often promoted by those committed to the ongoing witch-hunt against outdoor cats, of course—blaming cats for the demise of California sea otters and Hawaiian monk seals. Both species are increasing in number, but don’t expect that little detail to be included in the news accounts.”
Time to follow the clues
Both comments, unfortunately, join the anti-catters in reducing the matter to the “Tweety & Sylvester” or “Tom & Jerry” level: whether to blame or not blame cats for the observed phenomena, when what really needs to be done is the scientific research to follow the clues already turned up by the studies of Toxoplasma gondii in marine mammal and fish species to identify the original and primary host.