Kiesecker+et+al_Amphibian+Disease

Kiesecker+et+al_Amphibian+Disease - Amphibian Decline and...

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Unformatted text preview: Amphibian Decline and Emerging Disease What can sick frogs tench its about new and resurgent diseases in human populations and other species of wildlife? Joseph M. Kiesecker, Lisa K. Belden, Katriona Shea and Michael]. Rubbo Frog 't: length 45 min. There is it shortened left leg that is twisted at the knee. it also does not appear to have a knee joint. Frog 2: length 39 min. The left rear leg on this hog is missing. There are no kiiohliy traces iif'ini nnrtrrdeiiel- oped to; that was found on other frogs. The right leg is bent the inning than. it also has two hone L’t'tttt‘ilttt coiiiiiig out of the .lfni‘e'sl hnrlt. Frog 3: length 45 nini. The only thing inning with this frog is that there is [I tinny projection coming from litsi tliitt. hese are excerpts from the field notebook of Betsy C roon, who was a middle school student in rural Le Sueur, Minnesota when her class stum- bled on the misshapen leopard frogs in the summer of M95. They alerted the lusi'pli M. Kirsc'cia'r ri't'rii'i'r! I'ii'--' l 'liD. in zoology from (tn-gun Shite lliiii'rrsitii in 7997. :Mlt'i'pnst- doctoral research iii init- litttC't't"tl_li. lie ininni tlti‘ liinirileii iii-imi'tnn'nt at lltr' Pennsylvania Stair University as an assistant protrssor iii i‘l‘l‘l. Hr has spent the inst iii nears trying to understand tln' tai‘tiii's n’srmnstiih' for iiisi'tise' tiiitiiir'riks iiiin' how disease mu contribute to the decline at iltt'i'fl'i' one-i spi'i'ic's. iiiior‘i'niiiiiiiphihiiiiis. its] K. HK'JIII'” ‘illitht‘rl lion‘ .‘iir'nmnnrntal sires-tors alter dist-risi- siist‘c'ptillil‘ity iii iiiiiilhii'iiins as it postdoctoi'xil ti't inn' in the liiologn department at Prim Shite. 9hr recently juiin'il the timing};iii'iiiirtinz'nt in Virginia i-‘olutr'rtinir institute and State ttnim‘rsitiras an resistant pruti‘ssm: Kiitri'nmi Stun is (it! assistant professor in the biology .i't'mrtnicnt iit Prim State, where her pt'ttiml’llt research interest is the nsc or u'i'olo‘eirni tiii-‘orn in (anticipation, liiii‘iir'srnix iiinl tlirroiitnil iltiiir'nsitir sprites. Michael l. Riil'ilo is ti' PhD. candidate in biology”! l’rnn Stair strain- inci the intcrfircc l'ctieccn t‘cnsiistrni-lcerl iiiocisscs titltl roniniiriiitli rhininnii's, using ti'iiiihlmi‘li ,tilrrst points as ti nimiri. ,rliiiin‘a's for Kin-art io'r: Deport- "lr'lll Iii “intent. EHH tvtiiclli'r i_ltllllt'ttl'l1t'|i. l’rniir snhriiiin Stair Ulii‘r‘ersitn, lliiit‘t'rsitu Park, PA totttti’. lirtrriirt‘ fink-Eaters" nln 13h“ A merican Scientist, Volume L12 Minnesota Pollution Control Agency, who determined that 30 to 40 percent of the frogs in Ney Pond were de» formed. Nothng like this episode had ever before been seen in Minnesota, and the story shocked the public. Sud- denly, the students were featured in print and broadcast media across the country—including the children's magazine Eiirtli Focus, where this reCord appeared. The problem was not unique to Ney Pond, or to the leopard frogs that the students observed or even to the Mid- western United States. Across the globe hundreds of species of frogs, toads, salamanders and newts are in dramatic decline. At the same time, new and often serious infections dis- eases seem to be sickening people. Might these unhappy developments be connected? Might they indeed share a root cause: the changes in our World brought about by a growing human population? From several lines of in- quiry, evidence is accumulating to sup- port such a conclusion—that envi— ronmental degradation wrought by people is contributing to both trends. The human species no“r mmibers 6.3 billion, and collectively we have altered betWeen one-third and one-half of the Earth‘s land surface. After being stable for millennia, atmospheric carbon dim- ide has increased by 30 percent in the last two centuries. Our actions fix more nitrogen than all natural terrestrial sources, and we utilize over half of all accessible surface freshwater. These are dramatic changes. even though we can't always detennine their long-term significance. The immediate conse— quences seem to be disproportionately borne by frogs, which have suffered massive mortality in recent years. Along with many other scientists around the world, our research group studies this surge in amphibian deaths. While many cases can be linked directly to single, proximate factors such as habi- tat toss, numemus populations have do clined in protected parks and nature re~ serves, even in remote wilderness areasgplaces that are removed from our modern eflluvium and that ought to be insulated from human influence. Yet across the globe, many amphibian species have experienced increased dis- ease— and paras‘ite—prevalence, causing massive mortality. Developmental mal- formations associated with parasitic in— fecti on are also frequent: In some groups 90 Imrcent are severely deformed, with extra or missing limbs. The origins of these catastrophic losses are complex. Several agents can act synergistically to endanger a popu— lation. Depending on the specific lo— cale, forces such as climate change. habitat destruction, environmental chemicals, fertilizer runoff and the in; troduction of exotic species have all been implicated in the threat. So how is the global decline of am— phibians related to increased disease prevalence among humans and wild— life? The link is suggestive, not proven, but there are Compelling similarities betwuen recent disease outbreaks in many animals. Amphibians have been hit particularly hard because of their life cycle and physiology: Frogs and salamanders are exquisitely sensitive to environmental changes. This prop— erty casts them in the role of biological Cassandras, prophesying a pessimistic message of enviromnental degradation that we don't want to hear. Like Homer’s Trojans, We've mostly ig- nored their warnings. Figure ‘- Manv an hian species, including the wood t‘rng (Hum: suh‘ufmr, ubuuvi. are up nut. laud rater. M de rmitic‘. or wrinus pnpulaliun dcclin . uvcral studies, includng those of the authurs, alum that this murtalil} is tiu tn a variety of hunmn-mducud environ- mental changes. This: n‘hult is runccrning because amp Iihian‘» are Wt‘l‘l .h‘ im‘limlors ul' envimnnwnlal health—Ehc_\' have permeable skin with- Ulll M'fllt‘m feather“ 0r hair: their thrym are fully expmed tn the em imnmcnt without the benefit of rain-Hr. or other prntm'tinn; and their lift" cycle nftcn empower; them In hmh aquatic and IL‘I‘I‘QMTtdI hazard-u Sn the widespread amphibian decline cnuld he .1 warning of pm'imnmenlat dt‘gmdatinn. furthermore. llu’ rulth force-31h.“ Inn-1' thruatcm‘d amphibian pupulatinm might JIHO be driving the emergence and rcenwrgeme of human infectious [USE-3595 such as West Nile vim-1 and cholera. I -\II plmlngmphs courth of the aullwraJ ‘uu'uJHn-a‘ .tit-\,.'lt'ttli\[.n!:-_“ fill’l '\1.'1r(!'r vancomycin-resistant multidrug-resislant diphtheria Staphylococcus aureus tuberculosis E. coli i. I . . multidrug-resistant cholera 01572H? \ we ospor'as's cryptosporidiosis tuberculosis g dengue ‘i " cryptosporidiosis,-' . - --\I y i, _ r I variant _ _ ?\_ ./ C‘EU'mlm'Jakf’b typhoid drug-resistant 7x . . _ ._ d'sease lever . malaria ovrus . l - may \‘ f); x, _. H5N1 in man I sf 2 I . l . “a” syndrcirne /,,.. ’ /, J y ' ,7" /' .-*‘ ,a /‘ r “I, / I 1‘ '- v multidrug- - / “"9"” 5/ . x resistant 7/ ' If! // tuberculosis hepatitis c” ' f _ - V t,\ /' ' .1 Va yd"- cholera - _I ’- . ' _ i resistant I. w ._ Fl ift Valley * Staphylococcus ,- - F: 1.“ ,‘ l.“ . " . u yellow lever ’ yellow lever _ .-/ x” . k' \. fever " , a revs * I . -' ' x H l I‘ “ If, a E coil hamawrus r ‘ dengue Marburg Chalerag Ebo'a ‘ HIV 3” ' Otto-H? pUlmonaW L I virus _ hemorrhagic I .~ ' '- -..‘ assa ever ‘ , , ‘ a syndrome plague fever human I , \\ J/ monkeypox Nlpah |i‘ Hendra wrus ~. - additional threatened - WUS (endangerd or vulnerable) . extinct, missing or critically endangered enterovirus 71 vancornycin-resistant Staphylococcus aureus Figure 2. Global declines in amphibian populations have coincided with a sharp rise in new and resurgent human infectious diseases. in this map, red bars represent the number of amphibian species that have recently become extinct, missing or critically endangered; orange bars in- dicate the number of endangered or vulnerable species. The ranges and sites of origin for many emerging human diseases are also indicated. Amphibian data are from Here and Shoo 2003. Human disease data are from Fauci 2001. Amphibian Examples The relevance of wildlife (including frog} health to human health has only come to be appreciated recently, as similar patterns began appearing among many species. For people, at least 20 major diseases have reemerged in more virulent forms in the past two decades. Over roughly the same peri‘ od, more than 30 new diseases, in— cluding Ebola, AIDS and SARS, have emerged. Among other animals, sever- al wildlife species have been killed in large numbers in the past it) years by new "epizootics" of diseases such as canine distemper virus, which affects African wild dogs, lions and other car- nivores. 1n the case of amphibians, the toll from microbial and parasitic infec— tion is especially severe, even though the global decline in frogs, toads and salamanders went mostly unnoticed until 1989. Since then, over 115 species of amphibians have become severely threatened or gone extinct. Emerging diseases are those that have increased in incidence, virulence or geographic range, have shifted hosts or have recently evolved new i-lil American Scientist, Volume ‘42 strains. Diseases emerge when a new pathogen is introduced into a naive host population or when an external factor somehow increases the vulnera- bility of current hosts. Understanding the factors that dri- ve emergence of infectious disease in amphibians is central to understand- ing contagion in human and wildlife populations for several reasons. Am— phibians are especially sensitive to subtle changes in their environment. Because the origins of most new frog and toad pathogens have been linked to human-induced environmental change, conditions that cause out— breaks among, am phibians could have similar effects on other organisms. Also, wild and domesticated animals are relevant to human diseases be— cause they serve as reservoirs for pathogens that can be transmitted be- tween humans and animals. These so— called zo'onotic diseases make up many of the emerging infectious agents in humans. Thus, increased pathogenic infection in wildlife pop- ulations could translate into increased risk of human infection. Here we consider a few cases of widespread amphibian mortality and deformity that have been tied to new surges in disease. These examples demonstrate specific ways in which the global decline in amphibians could re— late to the larger phenomenon of emerging pathogens in humans and wildlife. Although there are many mechanisms leading to the rise in in- fectious diseases, we will focus on en- vimnmontal stressors and introduced pathogens to illustrate how general factors have promoted specific disease outbreaks among many species. A Plague of Frogs Environmental changes can shift the range and distribution of pathogens, and they can increase host susceptibili— ty to disease by altering the ability of hosts to resist infection. Global warm- ing is particularly tl‘lreateninpI to am- phibians. During the past 50 years, so r- face temperatures have risen by about half a degree Celsius, resulting to al- tered precipitation patterns and in- creased frequency and severity of ex— treme weather in many areas. One such event is the El Minn—Southern Oscilla- tion ('ENSOl, a phenomenon that origi- nates over the tropical Pacific Ocean but impacts weather patterns over the entire globe. During an El Nino event, the cold. nutrient—rich water that nor- mally covers most of the equatorial Pt - cific is replaced by warm, nutrient-defi- cient water. This shift happens every two to seven years. La Nina, the oppo- site of El Nine, refers to a blanket of ex- tremely cold water over the equatorial Pacific. In the last quarter—century, ENSO events appear to have increased in frequency, duration and intensity. In the United States, precipitation patterns in the Pacific Northwest are closely tied to ENSO cycles, which decrease winter rain and snowfall in the area. This part of the US. has also experi- enced catastrophic mortality of am- phibian embryos asst'iciated with the pathogen Saprolcguin femx. Several in- vestigators hypothesized that these out- breaks were related to increased expo- sure to ultraviolet radiation caused by depletion of the upper-atnmspheric ozone layer. This scenario is partly true: A particularly harmful component of ultraviolet light, UV~B, may contribute to the decline of amphibian species. However, climate change in the form of altered rainfall patterns may have a greater effect than ozone depletion on the amount of UV-B exposure among aquatic organisms. This is because low- er water levels or reductions in dis- solved organic matter reduce the ab— sorption of ultraviolet wavelengths by the embryos aquatic environment. in the late WSUs, we suggested that amphibians that breed in shallow, high— elevation lakes and ponds might be par- ticularly susceptible to this kind of di- mate—induced change in UV—B exposure. Those embryos that develop in such montane lakes and ponds are often ex- posed to direct sunlight, so they depend on the overlying water column to atten- uate ultraviolet radiation. When there is less precipitation, less water covers the egg clutches. enhancing UV-B exposure. We believed that the increasing frequen— cy and magnitude of El Nino events might have raised the incidence and severity of Stimulation: outbreaks by in- creasing the extent to which embryos are exposai to sunlight in shallow water. To test the theory, the Kiesecker lab along with colleagues at Oregon State University compared pathogen—medi- ated embryo mortality of the western toad, Bulb harms, with climate fluctua- wwiv.ameriranscientistori; tions in Oregon's North Cascades mountain range. For more than 10 years we measured mortality and wa- ter depth at natural egg-deposition sites, and we compared these data with annual precipitation and the Southern Oscillation Index (SOD. Using1 a combi- nation of observation and experimen- tation in the field, we wanted to test how Sapi'oleglain—caused mortality was related to the water depth in which embryos develop, how water depth at oviposition sites is related to ENSO cy- cles and how Sapr‘olegnin outbreaks were related to UV—B exposure. We found that El Nina—induced fluc— tuations in the depth of high-elevation pools did influence the amount of UV- B radiation that reached developing embryos and that higher levels of UV led to greater susceptibility to Supt-nice “in. More than half of the embryos that deVEloped in shallow water (less than 20 centimeters deep) contracted the pathogen, but when toad eggs devel- oped in deeper water (depths greater than 45 ce'i'itimeters), mortality associ— ated with Saprnlegnia was never more than 19 percent. This water depth was related to the amount of winter precip— itation, which was itself a function of the ENSO from 1990 to 1999. We also demonstrated that eggs that were screened from U'V-B radiation showed low levels of Sritn‘nlt'gaia infection— even if they were laid in shallow water. Amphibious Assault The Birth harms results are concordant with other studies that point to recent Pacific warming as a threat to amphib— ians. Because their survival is tied close- ly to water availability, climate changes that alter hydnilogy may set the stage for similar losses in other parts of the world. One example is the Monteverde Cloud Forest of Costa Rica, the site of one of the most notable cases of am- phibian decline. 111 I999, Alan Pounds of the University of Miami and his col- leagues at the Golden Toad Laboratory for Conservation reported massive pop— ulation crashes in approximately ~10 am- phibian species, including the apparent extinction of the golden toad fBHfo pi'riglt'm’sl. They suggested that the deaths were linked to a warmer, drier climate, which raised the altitude at Figure 3. Western toad embryos suffer greater mortality from ultraviolet radiation and infec- tion when rainfall patterns are disrupted. During a decade-long study. years with normal win- ter precipitation (left panel) had a low rate of infection by the pathogenic mold Suproh'gnia fer- nx. But during increasineg frequent E1 Nifio years, less precipitation falls in the Cascade Mountains, 50 the toads lay their eggs in shallower lakes and pools (center panel). The shorter water column above the egg clutches does not screen ultraviolet rays as well as deeper water, and the UV-B wavelength makes embryos more susceptible to infection by S. fernx— causing more than 50 percent mortality during those seasons. However, when the egg clutches were screened from UV-B rays, the embryos developed normally, even when they had been laid in shallow water fright panel). 2004 March—April l-ll iniectad tadpole sporocyst adult nematode nematode eggs Figure 4. Trematodes like Rilwimin cause developmental deformities in several amphibian species. During the life cycle of this flatworm par- asite, adults live and reproduce in the digestive systems of birds (left). Trematodc- eggs are released with the bird's feces, hatching into free- swimming mirtcidia that infect snails and develop into sporocysts. Within the snail hosts, each sporocyst produces many infectious cercariae, which leave the snail and burrow into the bodies of amphibian larvae, where they form cysts in and around the hindlimb buds. This disrupts normal development, producng deformities such as duplication or deletion of the near legs, as seen in wood frogs from central Pennsylvania frighfl. infected animals are readily caught and consumcd by the bird hosts to complete the cycle. which clouds formed, thereby dimin- ishing the amount of moisture: in large portions of the cloud forest. Pounds hy— pothesized that the strcss from their dri- er surmundings made individuals more susceptible to infection. Even as some species shifted their habitat into the re- maining moist areas, tho increased am- phibian density in these oases facilitated the spread of a waterborne pathogen. These associations between disease outbreaks and weather patterns are not limited to amphibians. Global warm- ing also influences the course of certain human diseases. For example, cholera is a water-borne bacterial disease that has reenterng as an epidemic prob— lem. in 1988 there were. approximately 50,000 cases of cholera worldwide. Three years later, that number had in— creased to 600,000. What was the cause of the outbreak? There were many con- tributing factors, but a maior one was the presence of the 1991 El Nino event. The incidence of cholera infection in humans, like Snprolqonia in the western toad, is correlated with global climatic cycles such as ENSO, perhaps because [42 American Scientist. Volume '43 local warming of shallow bodies of wa- ter led to conditions that were more fa- vorable to the transmission of the bac- terium or because of indirect effects on human water usage and sanitation. Among, the important lessons that emerge from these studies is this: The local consequences of large—scale cli— mate shifts—as well as their effects on living systems~arc varied. As a result, the way that changes in the weather impact amphibians (and humans.) will probably be different for each envirorv ment‘ and species. Fluke of Nature A great variety of parasites are depen- dent on freshwater environments. The parasitic. platyhclminlhic t‘latt-vorins called trematodes or tlukes are promi- nent examples. Members of this class usually adopt free-swimming aquatic forms for part of their life cycle, and they later rely on an intcrnnrdiatc host that is ofth a [resin-rater organism. Several well-knm-vn human diseases. including but not limited to schistoso- miasis, cchinostomiasis and cercarial dermatitis, result from infection with various llukcs. Collectively, these dis- cascs affect hundreds of millions of pcoplc around thc world. i towever, trematodes have also rucoivod close attention recently because of their rolc in outbreaks of amphibian doiomtitics. Amphibian deformities, particularly those related to limb development, have been reported in to states in the US, five provinces in Canada, and sev- eral other countries. They aren't a new phenomenon: Reports from the early [7005 document similar specimens. suggesting that whatever cans-3c:- the dc- formitics has been present for centuries. Those historical records describe one or two affected frogs in a population, and scientists usually n'gard a small num— ber of defonnitics, less than five percent of the population, to be normal. flow- evor, the frequency of such malforma- tions has skyrocketed in recent decades. Contemporary reports describe an ex- tremely high incidence of developmen— tal abnormalities in some areas—[mm 15 to 90 percent—often affecting; multi‘ ple spucics at a site. Several studies have shown that in- fection by the trematode Rilu'iroia causes many of these deformities. During its life cycle, Rflwii‘om depends on several hosts. including pond snails. When their snail hosts are present, tree-swimming trematode larvae, called crrrarim’, reach the next step of their life cycle by target- ing tadpoles and burrowing into their bodies. In some cases the cercariae de- velop into Cysts called irii'lacenurial: When the cercariae encvst in develop— ing limb buds, the cysts disrupt the nor- mal growth patterns and cause duplica- tion or deletion of legs in the adult hug. in 2002, Pieter Johnson of the Uni- versity.‘. of Wisconsin and his colleagues suggested that Ril'i'iroin occurrence and limb deformities were associated with highly productive artificial ponds situ- ated near agricultural areas. These pools were extremely nutrient dense because of fertilizer runoff and cattle manure, leading, to increased algal growth and greater snail density. Am“ phibians and birds—the other neces- sary hosts for Rilwiroia—also used these environmean readily. This type of artificial Wetland has become much more common with changes in agricul- tural land-Lise patterns assi‘iciatecl with the so—called “green rei-‘olution" in the Ittnlls and the current trend toward la rge—sca 1e corporate fa rmin g. Farm ponds aren't the oiin sites where habitat manipulation is altering the incidence. of trematode diseases. Most epidemiologists, parasitologists and health pnifessionals now recognire that several human parasites have thrived after anthropogenic changes Were made to freshwater ecosystems. An example is schistosomiasis, a tremas tode disease that contributes to the death of about a million people each year. The incidence of this parasitic in- fection is growing because various hu- man activities, including dam construc- tion, deforestation and irresponsible agricultural practices, have multiplied the amount of suitable habitat for the parasite’s snail hosts. This is a common theme: Many emerging-disease hot- spots have been linked with changes that led to population booms in critical hosts. These findings illustrate how hu- man beings have altered the environ- ment in. ways that have inadvertently increased the risk to our own health. Chemical Compromise The same kinds of environmental degradation that result in increased snail densities can also increase am: phibian exposure to pollutants such as pesticides. Many deformed frogs have been found in agrimltural areas where, in addition to fertilizer, herbicides and enclosures of 75 um Nitex mesh insecticides accumulate. Such chemi- cals are nearly ubiquitous in modern agriculture: Since their early use in the mid-10405, the worldwide application of pesticides has grown from Ell mil- lion kilograms per tear to approxi— maler 2.5 billion kilograms per year. Our research group recently investi- gated the role of chemical contamina» tion in nematode-mediated limb defor- mities among Wnud frogs (Rana syl- zntioil in central Pennsylvania. As ex- pected, We found that the parasites caused limb deformities in the frogs: When we prevented trematode cercari— ae from getting to the developing tad- poles. the. malformations never oc- curred. However, in the wild popula— tions there was great variation in the in- cidence of limb deformities depending on which pond the frogs came from. The animals that lived in ponds receiv‘ ing pesticide runoff developed abnor— malities much more often that animals from ponds without agricultural runoff—even though all the ponds had comparable levels of Rilii'fr'oia, We thought that stress, in the form of pesticide exposure. might have de— creased the host tadpoles ability to re- sist infection. resulting in higher para- site loads and higher risk of limb deformities. To test the idea, We put R. syltrtlt‘i‘tt tadpoles in a contmlled labora- enclosures of 500 pm Nltex mesh deformities, higher prevalance at sites exposed to ‘ for agricultural k " runoff .fi 5_\ .. cs _. Figure 5. Tremainde infection leads to limb deformities, but the infection rate is higher at sites that receive agricultural runoff. The authors reared groups of tadpoles inside screened enclosures (left) at six ponds where Ribs-iron: was present. Three of the ponds were contaminated by runoff containing agricultural pesticides. Different mesh sizes were used to exclude the parasite from some groups and pennit access to others fright). For the frogs housed behind finer mesh, the absence of cercariae prevented developmental abnormalities at all six locations. As expected, frogs that were reared in the larger-mesh enclosures were exposed to the parasite and developed limb deformities. However, the infection rates were significantly higher in the ponds that received agricultural runoff—despite the fact that the densities of Rilwiroia were comparable. wu'warm-tiednscienlisl .t In; El ill-l Mn rch—A pril 1-13 exposed to pesticides not exposed to pesticides _. 40 g 3 E 30 g 15 st i:— c 20 e 8. m to 5 a 10 e '63 9, 0 \ \ \° 0 e .56 . 9.3% Go“ {an 4’49 e139 :9 q“ if” metacercariae 80— 20- assayed the number of cercariae ‘ that successfully encyste O Figure 6. In the laboratory, tadpoles exposed to even low levels of pesticides (the US. Envi- ronmental Protection Agency maximum for human drinking water) had fewer ensinophils, a type of white blood cell—potentially indicating a weakened immune system—and much higher rates of parasitic infection than controls. tow environment and exposed them to one of three different pesticides (atrazine, malathion or esfenvaleratcl at concentrations equal to the US. Envi- ronmental Protection Agency maxi- mum for drinking water. W'e measured the immunocompetenq’ of each group of animals by challenging them with cercariae and by examining, a blood sample for the number of wsinophils, a 14-! American Scientist. Volume ‘42 cell type that may help resist macropar- asite infection. For the atrazine and es- feiwalerate groups. even these suppos- edly safe levels had dramatic effects on the wood frogs, and malathion had sim- ilar consequences at higher concentra- tions. The animals that were exposed to these pesticides showed sharp increases in the proportion of encrsted cercariae and significantly fewer eosinophils. These findings parallel other analy- ses of disease outbreaks in the midst of environmental stress. An example is the [988 introduction of phocine dis- temper virus into North Sea pinnipeds. The virus is endemic to its usual host, the harp seal, which lives on the Arctic pack ice. However, as the host popula- tion shifted its range southward in re- sponse to overfishiug, the virus passed to the native seal species of northern Europe and inflicted catastrophic loss- es. bro separate hivestieations into the animal epidemic, or epiaootic, suggest- ed that the seab might have been par- ticularly vulnerable because their im— mune systems had been compromised by exposure to pollutants such as polvv chlorinated biphenvls (I‘Cle. Other studies of marine vertebrates have also indicated that some pt’illutants, partic- ularly pesticides, can have immuno- toxic properties, which impair the abil- ity to rebuff infectious agents. Old Fungi, New Hosts One of the consequences of our domi- nation of the Earth is massive biotic ho— mogeniration. Worldwide transport of people, plants and animals has become routine, resulting in the breakdown of biogeographic boundaries that histori- cally maintained distinctive flora and fauna in different regions. People move organisms for Cllttfit-‘t‘\"alitit‘t, agriculture and hunting, in addition to accidental transport, on a global nt‘dlt‘. This steady traffic represents a constant inf l us of exotic infectious agents to humans and wildlife. Such foreiin introductions are often referred to as "biological pollu- tion." and they have unix'ersally di- minished local biodiversity. One example of this kind of intro duced pathogen is a newly discovered fungal disease of amphibians, chytrids ionn'cosis, caused by infection with Ba- lruclmcliiitrimn .it'iitinilmtidis, The Cliv- trids are the oldest fungi we knot-v of, based on fossils from the Rhynie Cheri in northern Scotland (see i’i-lareiimlfa, page 12th. 'l'hese ancient, still ubiqui~ tous fungi are found in moist soil and aquatic habitats where they act primar- ily as detritivores. Parasitic members of this group infect plants. protists and invertebrates, but B. t'ft‘ll'lfl'tif’tilftffS is the first chvtrid known to infect vertev brates. [t has caused mass die-offs of juvenile and adult frogs from Aus tralia, Central America and the west- ern United btates The pathogen was first described in l998 from dead and Figure 7'. Amphibians are particulariy sensitive to the erwirnnmenl‘al changes responsible for emerging diseases, a property that also makes them ideal models for understanding the mechanisms ot intectinn. Amphibians are amenable to experimental manipulation, not on];' in wet— land settings, but also in well-controlled laboratory; environments (left) and readily manipulated "meant-05m" experiments night). This flexi- bility allows investigators to combine natural settings with precise control of environmental variables and fipecified levels of infection to probt' disease dynamics in the most realistic and powerful way. dying amphibians in Australia and l‘anania. lntected animals develop gross lesions and hemorrhages ol the skin, which has led some st‘ientists to suggest that the liru‘nit‘liet'lrutrium has spL'L‘lali/L'Ll to use amphibian keratin as a prime nutrient. The epidemiologival patterns ot rhvtridiontveosis intection are charar- teristit' of a virulent pathogen spread- ing through a naive host. In Central America and Australia the mortality has been severe. ra\ aging, entire puptl‘ lations over the course of a few months and leaving:I l'en' survivors. Such high death rates are often assoL‘iated with introduced pathogens, and other signs also point to a novel agent as the cause ol this. outbreak. lior example, l‘eter Das/alx ol the Universilv ot Georgia and his L‘olteagues shim-ed that spL-t'it‘ie DNA sequences ti'oni ehytrid isolates from around the world were much less divergent than expected tor a wild strain, and some samples LUllL’Utt’Ll in opposite hemispheres were identical. liltll'll'tt‘l' evidence that ii. rlt'iitlrtlltrtlidls‘ has revently emerged comes from pre- served amphibian specimens collected prior to the onslaught. Not one Aus- tralian or Central :‘\nierican specimen examined in the llt tears belon- lot'al crises. showed evidence ol Chvtrid inv \\ \\'\\ .tl!tL‘t'h'aI'Ht'ti‘t!ltf~t.n|'g J'er'tion. But in a strange twist to the hit" r_\-‘, an examination ot preserved frogs that were collected during, population collapses in the western United States during; the 'l‘JTHs has lound evidence ol a type ot Burrm'lior'liuliirim infection. ll this is true, it raises a number or press- ing t'plestions. Did the new strain emerge twice? If so, where has it been all this time? Most importantly. \vhv did it subside? l‘he animal pandemic, or littttirtctltt‘. ol chytrid inlettion is relatively recent, and the field of amphibian biology is still struggling to understand the phe- nomenon. So while the findings to date are eonsistt-nt with a novel, introduced pathogen. other factors can't yet be ex- cluded from an e\planation or these massive crashes. So the t‘hvtrid hy— pothesis. which states that the t‘lL‘L‘lines ot highland amphibians in Central Arneriea and .-'\ustralia are doe solely to rhytrid intettion, is lil~‘.el_\-~ to be an oversiniplit‘it'ation. l-iven the popula- tion declines in amphibians or the Monteverde vloud torests—which were strongly linked to climatic warm- ing—have ocvurred synchronously with nearby t-vaves ot' chvtrid intm‘tion. even as the specilic palluieen in Mon- teverde has yet to be it'tenlil'ied. Anoth— er purzling detail is that some of the mortality among Lentral American trogs has been m'mmpanied by simul- taneous dedines in reptiles and birds. The aquatic Cll_\-'ll'l\l tungus is unliker to attack terrestrial verteiwates, so the relatitflnship between these deaths res mains a mystery. l’uttin' the Flam in I‘lavivirus' Despite the unvertaintv that remains, R hvtrid intt-etion has tollmvet‘l the par- adigm ol novel pathogen, naive host in an ewrnplarv \Vav. \-\"e're lamiliar with the script tor this kind of onslaught be— cause the pattern has been repeated so manv times, The template was tol- lmved when Spanish e\plorers intro— dut'ed smallpoit and measles to the Amerit'as, and it is still being played out in today's. neu'spaper headtines Among u'ildlite, chronic wasting dis— ease is spreading through wild ungtr late populations .is' ll'tlt‘L'lk‘L‘l elk are transported among; game ranrhes, and dork plague threatens the Future of North American wildton'l alter being introduced repeated]; lrom abroad lior humans. the l-Ves‘t Nile virus provides a more urgent example, This mierobe is a mosthito-horne tlavivirus that infects people, horses and birds. Altht’iueh it is \-\-‘idespread in Atrial. .-\s‘ia and the Middle East. its appears ZItl'l Klart'h April l4; year in which .1999 ' West Nile virus I 2000 was first 2001 detected I Figure 8.1112 outbreak of West Nile virus in North America illustrates the rapidity with which a rowel pathogen can infect a naive population. This "zoonotic" virus infects birds, mosqui- toes, humans and horses In the five years since it was first detected, it has spread to all but one of the 43 contiguous United States. ance in North America is quite recent, with the first human cases diagnosed in 1999. initial cases in the northeast- ern United States coincided with a large epizootic in captive exotic and native wild birds. West Nile virus 'could have entered through a number of avenues, including travel by infect- ed humans, importation of infected do- mesticated birds or the unintentional transfer of infected mosquitoes. In the four years since its introduction, the virus has spread extremely quickl}r and now covers most of North America. During 2002 and 2003, 13,000 cases of West Nile infection were reported to the Centers for Disease Control and Prevention, resulting in nearly 500 hu- man deaths. West Nile Virus illustrates the rapid rate at which a novel path- ogen can spread once it encounters a fresh host population. Low Biodiversity, High Disease Risk Biodiversity advocates often argue that animals, plants and microbes are valu- able as sources for new medicines or other useful products. Seldom men— tioned is the benefit of species diversity in mitigating human disease risk, a hy— pothesis called the "dilution effect," which was proposed by Richard Ost- feid and his colleagues at the institute of Ecosystem Studies in Millbrook, New York. Their model evolved to ex: plore the relationship betwrzen hu- mans, wild mammals and the deer Mn American Scientist, Volume ‘12 tick, which transmits the spirochetal bacterium that causes Lyme disease. in a 2000 article. theyr explained that in dis verse communities, many licks do not carry the disease because some verte- brate hosts that offer perfectly good blood meals are inefficient at transmit~ ting the spirochete to the feeding ticks. However, degraded habitats lose many species of tick-hosts, leaving the ticks to feast on the few remaining mammals that are well adapted to disturbed ar- eas. One of these species, the white- footed mouse Pt’t‘tltlll/SL'HS trump-us. also happens to be the most effective reser- voir for the spirochete. in 2003, the same group demonstrated that in- creased species diversity could buffer the risk of Lyme disease transmission by providing hosts other than white— footed mice for licks to feed on. More diversity in macrofauna would, pre— sumably, lead to lower rates of tick in- fection and therefore lower risk of hu- man exposure. The proposed relation between species diversity and infection risk is new, but we have seen similar patterns in our own most recent work with em- phibians. We observed that variany urbanized wetlands showed an inverse relation between the diversity of am- phibians, trematodes and snails, and the degree of urbanization. At the same time, snail density and the number of trematode infections among individ ual amphibians was higher in the more disturbed ponds. Although these data are preliminary, the mechanism re- sponsible for this pattern could be sim- ilar to the dilution effect. However, we cannot rule out the contribution of oth— er factors that might co—vary with di- versity in explaining the data. Con- sequently, the higher trematode sus- ceptibility may not be driven by a loss of diversity per sr if the same factors that decrease diversity also increase in- fection. If future data can substantiate the connection between species diver- sity and disease risk, then the biodiver— sity debate will become much more tangible and pressing. Conclusion Species extinction and the emergence of infectious disease are two of the most serious global concerns we face. These processes are tightly inter— twined, with parasitic and microbial infection acting as a cause for and con» sequence of biodiversity loss. There is no doubt that the world's climate patterns are changing. Al- though some scientists maintain that these alterations cannot yet be conclu- sively linked to human actions, none contest that global biodiversity has sharply decreased in recent decades. However, not all organisms are nega- tively affected by such environmental changes. indeed, many organisms, in» cluding hundreds of pathogens and parasites, have been great beneficiaries of these alterations. if current trends continue, these life forms are likely to experience continued prosperity. Un- forttmatelv, the outlook for animals, in- cluding people, is somewhat dimmer. The rapid global declines in amphib- ian populations have led some obs servers to believe that such massive decimation of fmgs and toads is some- how separate from the overall biodiver— sity This is a fa [lac—v it is now clear that the loss of amphibians is part of a larger phenomenon that is also increas- ing the prevalence of infectious disease in human and Wildlife populations. If we hope to extricate ourselves from this situation, we must gain greater insight into the origins and mechanisms of future disease out; breaks. The complexity of the problem presents a daunting obstacle to the task of reversing the trend of accelerating emergence of infectious disease. How- ever, it seems clear to us that we need a better understanding of the environ- mental cofactors that facilitate the spread at t'liHmse or the susceptibility «It limb. A! the HT}; least we need a much better Lindursmm'ling of how hu- manu intentionally or inml‘.'t'i't'9ntly Llif-pk‘fr-it" diauahc-t‘.1u.~,.tng nrganimm. Amphibit-ins make ideal subjects to investigate these issuuh became they lmu: prm't-tl tn be particularly hcl'lsi- lix'v to the environmental mtactnra that trigger disease outbreaks. This ut-nuit'ix'ity makes them (In early warn- ing system (it envirunnu'ntdl dc};de- tinn and L'lihk'dht‘ cmurguncc—tl‘tc ca— nnriu: in nLlr pldnctary (uni mine. In addition, {rugs are amenable to experi- nwnlal nmnipulatitms. allowing mn- trnllud mpurinwntatiun to assess the inllum‘tct' of key um'irtmnwntnl \‘étl‘i- ables; (in disease cmergt‘ncc. In many ways it SL'DFHS fitting that dlthuugh muphibians have liven Sn severely at- fcctud by thu cunditiuns that prumutc t‘linmse cnwrgenw, they might alsn servv as a must prumising tool In un- derstanding this pmccss. Bibliography “lam-tutu. A. R. and I. \‘I. l'\|L".~L'(l\L‘l‘. 2WD t nmplt-utt‘ in run-whatnot}; lc-Hfiuns tram tht- glnlml \ll‘LllIIL‘ n-t amphibian pnpulm Hunk" l. vinyl: ft'lll'l'"; 3597-1-45. IL mun. I’: tth. lint}; data .intl nlwvrmtluns l'.w.‘l: lu. au. u'mlvr IJJVJL. l‘.. .\. .-‘\. Lunninghgnn and A. l‘l. Hy- .nl Illllll. Inn-signing nifvutimm CllHl‘dHl'S nl n Iltillll'illll't'dl‘w to l‘ltklfl-‘t‘WtH and human l‘iunlth ‘Rt 1m. :' 237314144” liulci. -\. b. 2W1. Inl'uctlum difix-dw»: L'unxid‘ urnnnna tar llu- 2N crntnrt. Uilunn‘ I'lllt't' tii'm l.‘-‘.'.--t':l~:'.~ Eff? 063. l'lL'l'l I. l.-\‘1.,and L. ‘i-hun. IIIUF. Lunwruitiun Hl amphibians in thy Old World tropic-s thin— mg unith prublunh JSHI‘L‘It-Ill‘tl with re- gimml lawn. in .'tnnlliil'm.u Curiwrmmw, ed. It. I). Hmnhtfich. \\'a.~‘hinglm1, UL: Smith— wnmn Inslitutmn l‘rm-i. Klee-wt kvr, ]. \l.. .-\. R [lltmstcin nml l. K. llL'ltlt'n. JIM]. L'umplm (.nlkt‘x tit dmpl'nhiun [amputation rlm‘linn-‘fi. Mrtmr 4 ilkhfll—hH-l. Kira-mkt-r, J. \1. JUNE. Synerghm twin‘t‘en tn-matmlv inhrtiun .1an pwtit'itiv minimum: A link tn amphibian limb tlvtnrmitiva in rm- turt’n‘ l’rutt‘t‘ii‘in_-.;.~ u! Uic' Minimal :lurdt’m}; 1'! 5mm c; m :M' t..' .5 .'l. ‘.P-J:L|‘tlltl-J'Utlnl. ktzffit‘t'lx'i‘l'. ]. \t. ZUIH. lm'.‘::~i\t' ~pm'iuk .15 .‘J glulml problem: limanl undt-ratmulang lt'u- HI‘I’lLlH'iLli‘ le‘lim- ul .1Inplnl'11.inr‘~. In .tmr umlufln t‘uim‘rrritmn, ml. l\‘. [3 hvmlitwh. “flay-hingtun. I'M. .. Finithmnian Instilutiun I’l‘k'ffi. (Mt’vld, R. and F Ruining. llttllt. Hit It‘li\'t‘1“hl- tv and Llihi'twv rials: The mm- nl l__\-'m:- dis-7 mw. L‘n-m-nnttivn timing-II: 14:722—723. l‘m.:.nti.~., ‘I. r\.. .\-1 I' 1.. i‘ngtlt-n am] I. l-i.L'.-1mp— lJK'll. l‘N‘P. Bit-lsigicnl Ti'HpUl‘lbL‘ tn climate change on .1 tropical mountain Nirtmr "\UHN‘I l 4.: l '3 l‘\-'t‘iuhnld, lx’. EllU-l. lnh't't'imb LIN-aw: Thu hu- man rust: u1 uttl' um'immncntnl t'rI'UIS. Fu- .‘H'Illttlh'lllrl.’ “tutti: l‘rnpm mu“. llZl [1 All—A W. Fur relevant Wet-I tints, consult um issue ut rtmcrk‘an Scientist Onlimr: 11rtpitmumquigwgnum LegueTDC im} 5&1 Tilt; 9351' o MoDeRN Bananas-lint. ScneNceS ‘-\ \‘\' “fit[Ht'l'lfitlltl'it'lt'l‘lll‘it All}: ZIIU-l March—April I47 Copyright of American Scientist is the property of Sigma XI Science Research Society and its content may not be copied or emailed to multiple sites or posted to a listsenr without the copyright holder's express written permission. 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Kiesecker+et+al_Amphibian+Disease - Amphibian Decline and...

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