Download Linking environmental nutrient enrichment and disease

IN V ITE D F E A T U R E
E c o lo g ic a l A p p h c ^ io n s
V o l. 20, N o . 1
Ecological Applications, 20(1), 2010, pp. 16-29
© 2010 by the Ecological Society o f America
Linking en v iro n m en tal n u trie n t e n ric h m e n t and disease em erg en ce
in hu m an s and w ildlife
P ie te r
T. J. J o h n s o n ^ * A l a n R . T o w N S E N o y ^ C o r y C . C l e v e l a n d , ^ P a t r i c i a M . G l i b e r t , " * R o b e r t W . H o w a r t h /
V a l e r i e J. M c K e n z i e , ^ E l i s k a R e j m a n k o v a , ® a n d M a r y H . W a r d ’
^Ecology and Evolutionary Biology, University o f Colorado, Ramaley N122, Campus B ox 334, Boulder, Colorado 80309 USA
Institute fo r Arctic and Alpine Research, 1560 30th Street, University o f Colorado, Boulder, Colorado 80303 USA
^Ecosystem and Conservation Sciences, University o f Montana, Missoula, Montana 59812 USA
‘^University o f M aryland Center fo r Environmental Science, Horn Point Eahoratory, P.O. B ox 775, Cambridge, M aryland 21613 USA
^Ecology and Evolutionary Biology, Cornell University, Corson Hall, Ithaca, New York 14853 USA
^Department o f Environmental Science and Policy, University o f California, One Shields Avenue, Davis, California 95616 USA
''Division o f Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes o f Health,
Department o f Health and Human Services, Bethesda, M aryland 20892 USA
Abstract. W orldw ide increases in h u m an a n d wildlife diseases have challenged ecologists
to u n d ersta n d how large-scale enviro n m en tal changes affect h o st-p a ra site interactions. O ne o f
the m o st p ro fo u n d changes to E a rth ’s ecosystem s is the alte ra tio n o f global n u trie n t cycles,
including those o f p h o sp h o ru s (P) a n d especially nitro g en (N ). A long w ith the obvious direct
benefits o f n u trie n t ap p licatio n fo r fo o d p ro d u ctio n , an th ro p o g en ic in p u ts o f N a n d P can
indirectly affect the ab u n d an ce o f infectious a n d noninfectious pathogens. T he m echanism s
underp in n in g observed co rrelations, how ever, a n d how such p a tte rn s vary w ith disease type,
have long rem ained conjectural. Elere, we highlight recent experim ental advances to critically
evaluate the relatio n sh ip betw een environm ental n u trie n t en richm ent a n d disease. G iven the
interrelated n atu re o f h u m an a n d wildlife disease em ergence, we include a b ro a d range o f
hu m an a n d wildlife exam ples fro m terrestrial, m arine, a n d freshw ater ecosystem s. W e exam ine
the consequences o f n u trie n t p o llu tio n on directly tran sm itted , v ector-borne, com plex life
cycle, a n d noninfectious p athogens, including W est N ile virus, m alaria, h arm fu l algal bloom s,
coral reef diseases, a n d am p h ib ian m alform ations.
O u r synthetic exam in atio n suggests th a t the effects o f en v ironm ental n u trie n t en richm ent on
disease are com plex a n d m ultifaceted, varying w ith the type o f p ath o g en , h o st species a n d
condition, attrib u tes o f the ecosystem , a n d the degree o f enrichm ent; some p athogens increase
in abun d an ce w hereas others decline o r disappear. N evertheless, available evidence indicates
th a t ecological changes associated w ith n u trie n t en richm ent often exacerbate infection a n d
disease caused by generalist parasites w ith direct or simple life cycles. O bserved m echanism s
include changes in h o st/v ecto r density, h o st d istrib u tio n , infection resistance, p ath o g en
virulence o r toxicity, a n d the d irect su p p lem en tatio n o f pathogens. Collectively, these
pathogens m ay be p articu larly d an g ero u s because they can continue to cause m o rtality even as
their hosts decline, p o tentially leading to sustained epidem ics o r chronic pathology. W e
suggest th a t in teractio n s betw een n u trie n t en richm ent an d disease will becom e increasingly
im p o rta n t in tro p ical a n d su b tro p ical regions, w here forecasted increases in n u trien t
applicatio n will occur in an en v ironm ent rich w ith infectious pathogens. W e em phasize the
im portance o f careful disease m an ag e m en t in conju n ctio n w ith co n tin u ed intensification o f
global n u trie n t cycles.
Key words: dead zones; eutrophication; global change; harmful algal blooms (H A B s); host-parasite
interaction; human health; nitrogen; zoonotic disease.
w orldw ide (W orld Elealth O rg an izatio n 2004). W hile
som e p ath o g ens have been elim inated or controlled, the
c o m b in a tio n o f new ly em erg in g diseases a n d th e
resurgence o f e x ta n t diseases engenders a n a n n u al
h u m a n d ea th toll o f ~ 1 2 m illion people. N ew diseases
such as acquired im m unod eficiency syndrom e (A ID S),
L ym e b o rrelio sis, e b o la , su d d e n ac u te re s p ira to ry
D is e a s e E m e r g e n c e in E Iu m an s a n d W i l d l i f e
D espite m a jo r advances in h u m a n medicine, infectious
disease rem ains the largest cause o f h u m a n m o rtality
Manuscript received 3 April 2008; revised 6 October 2008;
accepted 12 Noveniber 2008; final version received 7
2009. Corresponding Editor: N. B. Gnmm. For repnnts 01 this
Invited Feature, see footnote 1, p. 3.
^ E-mail: pieter.johnson@ colorado.edu
syndrom e (SA R S), bovine spongiform encep h alo p ath y
(BSE), a n d h an tav iru s p u lm o n ary syndrom e (H PS) have
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January 2010
PERSPECTIVES O N T H E M O D E R N N CYCLE
em erged, w hile sig n ifican t increases in estab lish ed
infections such as m alaria, tuberculosis, cholera, an d
m easles have also occurred. Im p o rta n tly , how ever, this
tren d is n o t unique to h u m a n p athogens. Em ergence o f
w ildlife diseases h as exhibited a sim ilar p a tte rn in recent
decades, largely ov ertu rn in g the o n ce-d o m in an t p a ra ­
digm th a t disease is n o t an im p o rta n t cause o f wildlife
m o rtality (M ay 1988, D aszak et al. 2000, D o b so n an d
F o u fo p o u lo s 2001). E xam ples are num ero u s a n d include
viral hem orrhag ic septicem ia virus (VHSV) in fishes,
colony collapse d iso rd er in honeybees, m ycoplasm osis in
birds, toxoplasm osis in sea otters, a n d chytridiom ycosis
in am phibians (D aszak et al. 2000, M iller et al. 2002,
Lips et al. 2006). E m erging infections can som etim es
lead to p o p u latio n ex tirp atio n s o r even species extinc­
tions, p articu larly w hen reservoir h o sts, sm all h o st
p o p u latio n sizes, o r frequency-dependent transm ission
are involved (de C astro an d B olker 2005, K . F. Sm ith et
al. 2006).
T he parallel em ergence o f h u m a n an d wildlife diseases
reflects the facts th a t (1) each have sim ilar etiologies
involving ecological changes in the enviro n m en t a n d (2)
the division betw een m edical an d veterinary diseases is
largely a n artificial one. M o st em erging diseases of
hum ans are zoonotic, m eaning they involve anim al hosts
a t some stage o f transm ission (T aylor et al. 2001,
W oolhouse an d G ow tage-S equeria 2005). C onsequently,
p attern s o f infection in h u m an s are often linked to the
levels o f infection in wildlife, a n d a th o ro u g h u n d e r­
standing o f disease em ergence th u s requires know ledge
o f the ecological factors th a t influence hu m an s, wildlife
hosts, an d their in teractio n s (N atio n al R esearch C ouncil
2001, Sm ith et al. 2007). A grow ing n u m b er o f exam ples
illu strate the value o f a n ecological a p p ro a c h fo r
u n d e rstan d in g disease a n d collectively suggest th a t
b ro a d p attern s o f em ergence are best u n d e rsto o d by
exam ining h u m a n an d wildlife p o p u latio n s concurrently
(G uernier et al. 2004, Jones et al. 2008). H ere we a d o p t
such a n a p p ro ac h to explore the relationships betw een
environm ental n u trie n t en richm ent a n d disease. R ecog­
nizing th e parallel a n d often in te r-rela te d p a tte rn s
betw een pathogens o f h u m an s an d those o f wildlife,
we do n o t differentiate betw een m edical a n d veterinary
diseases, a n d interw eave exam ples o f each to bro ad ly
exam ine the effects o f n u trien ts o n diseases.
C h a n g in g N a n d
P C y c le s
H u m an activities have driven m assive changes in the
m a jo r biogeoch em ical cycles, p a rtic u la rly th o se o f
nitrogen (N ) a n d p h o sp h o ru s (P). F o r exam ple, N fixed
via fossil fuel com bustion, fertilizer p ro d u ctio n , an d
cultivation o f N -fixing crops now outpaces N inputs
from all n a tu ra l processes o n th e lan d surfaces o f the
planet com bined (G allow ay et al. 2004). Sim ilarly, the
extraction, refining a n d ap p licatio n o f P fertilizer has
am plified the n atu ral P cycle by a b o u t tw o- to threefold
(H o w arth et al. 1995, B ennett et al. 2001). T he regional
v ariatio n in the acceleration o f these n u trien t cycles is
17
rem arkable. W hile som e regions o f the w o rld such as
n o rth e rn C an a d a a n d Siberia have seen little if any
change, o th er regions such as w estern E urope, the
n o rth ea ste rn U n ited States, an d east A sia have seen 10to 15-fold increases in n u trie n t flows in rivers a n d in the
atm o sp h eric d eposition o f nitro g en (H o w arth et al.
2005, H o w a rth 2008). N u trie n t use fo r h u m an e n te r­
prises has a range o f effects on the E a rth system, b o th
positive an d negative. F o r exam ple, m ineral fertilizer
p ro d u c tio n a n d legum e cro p cu ltiv atio n fueled the
G reen R evolution, significantly increasing crop yields
th a t su p p o rt grow ing h u m a n p o p u latio n s, decreasing
m aln u tritio n , a n d enhancing econom ic pro sp erity (Smil
2001, 2002, Sanchez 2002). O n the o th er h an d , en v iro n ­
m en tal N loading can cause a cascade o f negative effects
(sensu G allow ay et al. 2003), including declines in forest
h ealth (Schulze 1989, A b er 1998), changes in species
com p o sitio n a n d losses o f biodiversity (V itousek et al.
1997, Stevens et al. 2004), eu tro p h icatio n a n d loss o f
h a b ita t quality in a q u atic ecosystem s (H o w arth et al.
2000, N a tio n al R esearch C ouncil 2000, S chindler 2006,
V. H . Sm ith et al. 2006), acidification o f soils (H ogberg
et al. 2006), a n d changes to the chem istry an d radiative
balance o f the atm o sp h ere (In tergovernm ental P anel on
C lim ate C hange 2007). P en richm ent has a less diverse
set o f consequences, b u t is a m a jo r driver o f aq u atic
e u tro p h icatio n , p articu larly in freshw aters (C arp en ter et
al. 1998, S chindler 2006, V. H . Sm ith et al. 2006). T hus,
in spite o f the clear benefits to h u m an s o f th e increased
uses o f fertilizer N a n d P, th e w idespread a n d increasing
use o f an th ro p o g en ic n u trien ts is also tran sfo rm in g the
state o f n a tu ra l ecosystem s a n d the m y riad services a n d
functions they provide (V itousek et al. 1997). H ere we
explore the consequences o f such n u trie n t enrichm ent
fo r p attern s o f disease in b o th h u m an an d wildlife
p opu latio n s.
N u t r i e n t E n r i c h m e n t a n d D is e a s e
O u r u n d erstan d in g o f the effects o f n u trie n t enrich­
m en t on p a ttern s o f disease rem ains lim ited. D irect
exposure to n u trien ts (especially n itra te ingestion via
drin kin g w ater) can cause o r co n trib u te to p ath o lo g y in
hu m an s a n d wildlife, w ith exam ples ranging fro m blueb a b y sy n d ro m e (m eth y g lo b in em ia) to re p ro d u ctiv e
problem s to various cancers (W ard et al. 2005). Increases
in fo o d p ro d u ctio n associated w ith fertilizer usage can
also reduce m aln u tritio n a n d enhance h u m an health
(Sanchez a n d S w am in ath an 2005, Sm ith et al. 2005). O u r
goal here, how ever, is to explore th e indirect effects o f
en v ironm ental n u trie n t enrichm ent o n diseases, w hich
are o ften ecologically com plex a n d p o te n tially fa r
reaching. B oth th eoretical a n d em pirical studies suggest
th at, unlike m an y stressors, n u trien t enrichm ent often
enhances p ath o g en ab u n d an ce (L afferty 1997, Lafferty
a n d H o lt 2003, T ow nsend et al. 2003, M cK enzie a n d
T ow nsend 2007, Jo h n so n a n d C arp en te r 2008). A n th ro ­
pogenic in p u ts o f n u trien ts to the en v ironm ent frequently
correlate w ith increases in the prevalence, severity, o r
18
IN V ITE D FE A T U R E
d istrib u tio n o f infectious diseases in n atu re (C oyner et al.
2003, R ejm ankova et al. 2006, Jo h n so n et al. 2007, Voss
a n d R ichard so n 2007). P o stu lated m echanism s fo r these
linkages include changes in h o st a b u n d an ce a n d distri­
b u tio n , shifts in p ath o g en virulence, o r changes in h o st
susceptibility (see reviews by M cK enzie a n d T ow nsend
2007, Joh n so n a n d C arp en te r 2008).
H ow ever, in terp re ta tio n o f these co rrelations is often
confounded by the fact th a t n u trie n t en richm ent is
frequently accom panied by ad d itio n al form s o f en v iro n ­
m ental change (e.g., lan d use changes, chem ical p o llu ­
tion, changes in species com position), precluding precise
identification o f causal m echanism s. M oreover, levels o f
n u trie n t enrichm ent are infrequently m easured directly,
m ak ing it difficult to u n d e rsta n d the range o f enrich­
m e n t v alu es o v e r w h ich p a th o g e n s w ill be m o s t
responsive. The p roblem is fu rth e r co n fo u n d ed by the
tendency o f n u trie n t en richm ent to have no n -lin ear
effects o n ecological resp o n se v ariab les, in clu d in g
p rim ary p ro d u ctio n , d ecom position, h a b ita t quality,
fo o d web structure, a n d species diversity (D o d so n et
al. 2000, H o w a rth et al. 2000, N a tio n a l R esearch
C ouncil 2000). T hus, extrem ely high n u trie n t inputs
m ay induce different effects fo r h o st-p a th o g e n in te r­
actions relative to low or m o d erate levels o f enrichm ent
(Johnson an d C arp en te r 2008).
R ecent experim ental research focused o n the n u trie n tdisease linkage offers new a n d d irect insights a b o u t the
m echanism s u n d erp in n ing observed field p attern s. C o l­
lectively, these experim ents encom pass a b ro a d range o f
h u m an an d wildlife disease exam ples, including field an d
lab o ra to ry studies in m arine, freshw ater, a n d terrestrial
ecosystem s. O u r goal is to highlight these recent ex­
perim ental advances a n d use th em to discuss general
m echanism s linking n u trien ts a n d disease. Recognizing
th a t the effects o f n u trien ts will vary w ith the type o f
path o g en an d its m ode o f transm ission, we evaluate the
effects o f n u trien t en richm ent o n directly tran sm itted d is­
eases, vector-borne infections, com plex life cycle p a ra ­
sites, a n d noninfectious diseases. By synthesizing existing
in fo rm atio n from a range o f systems a n d transm ission
m odes, w e aim to elucidate h o w n u trie n t-m ed iate d
changes in disease levels m ay affect h u m a n health,
econom ic sustainability, a n d wildlife conservation.
D irect horizontal transmission
D irectly tran sm itted diseases are caused by parasites
th a t require only one type o f h o st to m ain tain the life
cycle. T hey are usually tran sm itted via d irect co n tac t
betw een hosts o r by the spread o f infective propagules
(e.g., fungal spores, viral particles, eggs, cysts) in the
environm ent. Exam ples include m an y viruses, b acteria,
fungi, protists, an d some m etazo an parasites. N u trie n t
enrichm ent is hypothesized to influence directly tra n s ­
m itted parasites by (1) changing the density o f hosts
(a n d th erefo re th e p a ra site tra n sm issio n rate ), (2)
altering the d u ra tio n o f infectivity by hosts (e.g., by
increasing h o st survival), (3) ex acerbating the p athology
E c o lo g ic a l A p p lic a tio n s
V o l. 20, N o . 1
associated w ith infection, o r (4) by directly o r indirectly
p roviding ad d itio n al resources to the p ath o g en (Jo h n so n
a n d C arp en te r 2008). F o r exam ple, M itchell et al. (2003)
exam ined the response o f fungal foliar p ath o g en s to
experim ental N depo sitio n (as well as elevated c arb o n
dioxide a n d decreased p la n t diversity) o n 16 species o f
h o st plan ts, a n d fo u n d a significant increase in fungal
disease severity in species th a t also displayed increased
foliar N content. The co rrelatio n betw een foliar N an d
disease severity suggests th a t increased N availability
m ay benefit fo lia r p ath o g en s by p ro m o tin g higher
infection establishm ent rates, lesion gro w th (Sander
a n d H eitefuss 1998), a n d spore p ro d u ctio n (Jensen an d
M u n k 1997).
Som e coral p ath o g en s also resp o n d positively to
n u trien t enrichm ent, p erh ap s th ro u g h a sim ilar m ech a­
nism . O u tb reak s o f disease in some coral reefs have been
co rrelated w ith increases in n u trie n t ru n o ff (K im an d
H arvell 2002, S u th erlan d et al. 2004), a n d B runo et al.
(2003) used tim e-release fertilizer pellets to experim en­
tally evaluate the effects o f n u trie n t en richm ent on
n atu rally infected sea fans a n d reef-building corals in
situ. A dded n u trien ts nearly d o u b led the severity o f b o th
aspergillosis a n d yellow b a n d disease (Y B D ) a n d the
rate o f h o st tissue loss (B runo et al. 2003). V oss an d
R ich ardson (2006) used a co m b in atio n o f held an d
lab o ra to ry experim ents to test the effect o f n u trien t
a d d itio n s on black b a n d disease (BBD; Fig. lA ) in
C arib b ea n corals. T heir results also revealed the positive
effects o f n u trien t a d d itio n s o n disease, w ith BBD
progressing appro x im ately 2.5 tim es faster in exper­
im entally exposed corals th a n in u n m an ip u lated controls
(Fig. 2A). C orresp o n d in g la b o ra to ry trials confirm ed
th a t h o st tissue loss increased in a dose-dependent
m an n e r w ith increasing n itrate (Voss a n d R ich ard so n
2006).
T he m echanism (s) linking accelerated p ath o g en spread
a n d n u trien t additions rem ain unclear. BBD, like Y B D ,
is a m icrobial co n so rtiu m o f m o re th a n 50 different
h etero tro p h ic b acteria, as well as som e sulfide-oxidizing
bacteria a n d filam entous cyan o b acteria (C arlto n an d
R ich ard so n 1995, C ooney et al. 2002), m ak in g its
responses to environm ental change difficult to ascertain.
The causal p ath w ay could be sim ilar to th a t observed for
foliar p la n t pathogens discussed above, w hereby n u ­
trien ts benefit the p ath o g e n by directly stim ulating
grow th a n d developm ent. G iven th a t Aspergillus infec­
tions are caused by a single p ath o g en an d th a t Voss et al.
(2007) did n o t find BBD com m unity shifts in response to
nutrients, the m echanism o f direct resource benefits to
the p ath o g en is plausible. E xperim ents by K line et al.
(2006), how ever, suggested th a t the m echanism m ay be
indirect; elevated n u trien ts increase the p ro d u ctio n o f
organic c arb o n (throu g h p rim ary pro d u ctio n ), w hich in
tu rn leads to a n increased ab u n d an ce o f coral-associated
m icro b io ta a n d in o p p o rtu n istic parasitism . In either
case, these exam ples from com pletely different systems
(grasslands a n d coral reefs) suggest the b ro a d p o ten tial
January 2010
PERSPECTIVES O N T H E M O D E R N N CYCLE
19
F ig . 1. Representative diseases or hosts that respond to nutrient enrichment. (A) Black band disease (BBD), a directly
transmitted disease, in reef-building corals (photo courtesy of USGS). (B) Vector-borne pathogens, such as malaria and West Nile
virus, may be enhanced with nutrient enrichment owing to changes in mosquito production or larval habitat. (C) Complex life cycle
parasites, including the trematode (Ribeiroia ondatrae) that causes limb deformities in amphibians, can increase in abundance or
pathology due to changes in intermediate host abundance or parasite production (photo credit: P. Johnson). (D) Noninfectious
diseases such as harmful algal blooms (HABs) may directly or indirectly cause a broad range of pathologies in human and wildlife
populations (photo credit: P. Glibert).
fo r n u trien t enrichm ent to enhance the availability of
resources fo r som e pathogens, thereby facilitating their
rate o f spread an d the resulting h o st pathologies.
In d irect effects associated w ith enviro n m en tal n u ­
trien t enrichm ent can also enhance the p ath o lo g y of
directly tran sm itted parasites. F o r exam ple, hypoxia
caused by eu tro p h icatio n can accelerate p arasite spread
an d enhance pathology. E cto p arasitic copepods an d
m onogenean parasites, w hich colonize the gills a n d skin
o f fishes, can accelerate asphyxiation in oxygen-starved
fish, som etim es leading to large die-offs (M oller 1987,
K u p erm an et al. 2001). Sim ilarly, R o b o h m et al. (2005)
fo u n d th a t experim ental exposure to m o d erate hypoxia
greatly accelerated d ea th in lobsters exposed previously
to pathogenic bacteria.
Indirect transmission: vector-borne
In d ire c t tran sm issio n o f v e c to r-b o rn e p a th o g e n s
requires three com ponents: a disease agent (parasite), a
vector (often an a rth ro p o d such as a m o sq u ito ), an d a
h o st (Fig. IB). W hile an increase in n u trien t availability
could conceivably affect an y o f these co m p o n en ts,
p ublished research has often focused on how n u trien ts
affect the vector, as vector ab u n d an ce strongly affects
overall transm ission. F o r exam ple, changes in lan d use
can alter b o th the type o f h a b ita t a n d the am o u n t o f
fo o d available fo r larval m osquitoes, w ith higher fo o d
resources en h an cin g th e p ro d u c tio n o f a d u lts a n d
increasing disease risk (L aw ler a n d D ritz 2005, M u n g a
e t al. 2006, Y an o v iak et al. 2006). R ecent w o rk on
m a la ria offers a p articu larly com pelling exam ple o f the
relatio n sh ip betw een n u trien t en richm ent an d the vector
com m unity.
M a la ria has once again becom e a global killer, w ith
a n estim ated 2 m illion h u m a n d eath s p er year, m o st o f
w hich involve children u n d er the age o f five (W orld
H e alth O rg an izatio n 2004). U n d erstan d in g the ecology
o f this disease is th erefore a n im p o rta n t public health
p riority. T ransm ission o f m ala ria requires a p ro tist
p arasite {Plasmodium spp.), a m o sq u ito vector, a n d a
p rim ate host. T he presence a n d ab u n d an ce o f m osquito
larvae in aq u atic h a b itats a n d th e resulting n u m b er o f
ad u lts capable o f m a la ria transm ission are reg u lated by
a variety o f ecosystem processes o p eratin g a t several
E c o lo g ic a l A p p lic a tio n s
V o l. 20, N o . 1
IN V ITE D FE A T U R E
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2000
Year
F ig . 2. Select examples o f how nutrient enrichment affects different types of disease conditions. (A) Effects o f experimental
nutrient addition on black band disease in reef-building corals in the Bahamas; (reprinted from Fig. 2 in Voss and Richardson
[2006], with permission of Springer Science+Business Media and the authors). (B) Influence of total nutrients (nutrient
concentration multiplied by water volume) on survival of larval mosquitoes (Culex restuans) (from Reiskind et al. [2004], reprinted
with permission o f the Entomological Society of America). (C) Experimental nutrient additions (N and P) indirectly increased
Ribeiroia infection in larval amphibians through changes in infected snail abundance and per capita parasite release (from Johnson
et al. [2007], reprinted with permission of the National Academy o f Sciences, USA). (D) Trends in nitrogen fertilizer use (solid line)
and the number of red tides (dashed line) reported for Chinese coastal waters through the mid-1990s (sources: Smil [2001] for
fertilizer use and Zhang [1994] for red tide abundance; from Glibert and Burkholder [2006], reprinted with permission o f Springer
Science-f-Business Media and the authors).
o rg a n iz a tio n a l levels a n d s p a tia l/te m p o ra l scales.
A q u atic plants (b o th m icro- a n d m acrophytes) provide
p ro tectio n from p re d a to rs a n d co n trib u te d etritu s th a t
supports the bacterial com m unity, w hich, in tu rn , serves
as fo o d fo r larval m osquitoes. A change in any com ­
p o n e n t w ithin this com plex stru ctu re m ay have a
substantial im pact on the m o sq u ito p o p u la tio n an d
can even lead to a replacem ent o f one species w ith
an o th er. Since n o t all m o sq u ito species are equally
efficient in transm ission o f m alaria, replacem ent o f a
less efficient vector w ith a m o re efficient one w ould
increase the risk o f m ala ria transm ission.
A series o f experim ental a n d correlative studies in the
m alaria-endem ic co u n try o f Belize have revealed the
m echanistic linkages am o n g n u trie n t enrichm ent, w et­
lan d vegetation, a n d vector p ro d u ctio n . O ligotrophic,
lim estone-based w etlands o f the C arib b ean are strongly
p h o sp h o ru s (P) lim ited. In w etland h ab itats, p h o sp h o ­
rus-enriched ru n o ff fro m ag ricu ltu ral lands an d h u m an
settlem ents causes a replacem ent o f sparse m acro p h y te
(rush) vegetation w ith tall dense m acro p h y tes (cattail),
w ith im p o rta n t consequences fo r the larval m osquito
com m unity (Pope et al. 2005, R ejm an k o v a et al. 2008).
R ushes provide typical h a b ita t fo r Anopheles alhimanus
larvae, w hereas cattails rep resen t a typical h a b ita t fo r A.
vestitipennis, w hich is a su p erio r vector o f Plasm odium to
h u m an s (G rieco et al. 2006, 2007). N u trien t-m ed iated
changes in w etlan d p la n t com m unities can thereby lead
to the replacem ent o f A . albimanus by A . vestitipennis,
increasing the risk o f m a la ria transm ission risk in the
region (Achee et al. 2000). Indeed, recent spatial d a ta on
m alaria incidence show ed a w eak b u t positive co rrela­
tio n betw een the d istrib u tio n o f cattail m arshes an d
n u m b er o f m ala ria cases in h u m an s (K. Pope, unpub­
lished data).
O th er m osq u ito -v ecto red diseases m ay also respond
positively to n u trie n t enrichm ent. F o r instance, follow ­
ing its in tro d u ctio n to the U n ited States in 1999, W est
N ile virus has sp read rapidly across N o rth A m erica,
ad ap tin g to endem ic m o sq u ito vectors in the genus
Culex. E xperim ental w o rk has d em o n strated a link
betw een n u trie n t en richm ent a n d breeding success o f
C ulex m osquitoes. R eiskind a n d W ilson (2004) fo u n d
th a t fem ale C ulex restuans oviposited m o re th a n ten
tim es the n u m b er o f egg clutches in containers w ith
ad d ed n u trien ts co m p ared to co n tro l containers. L arval
January 2010
PERSPECTIVES O N T H E M O D E R N N CYCLE
survival an d the m ean size o f em erging adults were
greater in higher n u trie n t treatm en ts com pared w ith
controls (Fig. 2B; R eiskind et al. 2004). Sim ilarly, in
C alifornia rice fields, L aw ler a n d D ritz (2005) rep o rted
th a t n u trien t en richm ent th ro u g h in co rp o ra tio n o f rice
straw led to increased p ro d u c tio n o f C ulex tarsalis,
an o th er im p o rta n t vector o f W est N ile virus (L aw ler an d
D ritz 2005). G iven the im p o rtan ce o f b o th C. restuans
an d C. tarsalis as vectors fo r W est N ile virus in the
U n ited States, these d a ta suggest th a t nu trien t-rich
w ater bodies n earb y to h u m an a n d b ird p o p u latio n s
could increase disease risk.
F o r b o th W est N ile virus a n d m a la ria , n u trie n t
enrichm ent enhanced p ro d u c tio n o f the necessary m o s­
q u ito vector, thereby increasing p o ten tial disease risk.
Flowever, m osqu ito species have diverse h a b ita t req u ire­
m ents fo r breeding a n d larval developm ent, a n d it is
pro b ab le th a t, in o th er cases, com p eten t disease vectors
will respond negatively to n u trien t enrichm ent, u n d e r­
scoring the need fo r m ore experim ental studies th a t
address species-specific ecological responses. M oreover,
the im p o rtan ce o f u n d e rsta n d in g n u trie n t-m o s q u ito
interactions extends b eyond m ala ria an d W est N ile virus;
o th er w idespread tro p ical diseases vectored by m o sq u i­
toes include dengue fever, yellow fever, vector-borne
encephalitis, an d B an cro ftian filariasis, a n d alm ost no
studies have addressed the relative risk o f these diseases
w ith respect to lan d use change a n d n u trie n t enrichm ent.
Indirect transmission: com plex life cycle
Parasites w ith com plex life cycles require m ultiple
hosts to com plete th e ir life cycles a n d rep ro d u ce,
frequently alte rn a tin g betw een free-living infectious
stages (e.g., cercariae, zoospores, m iracidia) a n d endoparasitic form s. These life cycles are com m on to m any
helm inths, such as trem ato d es (flatw orm s), cestodes
(tapew orm s), nem atodes (roundw orm s), acan th o cep h alans (spiny-headed w orm s), as well as som e m yxozoans
an d chytridiom ycetes. Im p o rtan tly , because infection
m u st progress sequentially a m o n g hosts, the parasites
c an n o t generally reinfect the sam e hosts, as m ig h t occur
w ith a virus living inside its host. As a result, the n u m b er
o f parasites in a h o st— w hich determ ines the risk of
pathology— is a fu n ctio n o f how m an y tim es the h o st
has been independently infected (intensity-dependent
pathology). Because com plex life cycle parasites are
sensitive to changes in the d istrib u tio n a n d /o r a b u n ­
dance o f all req u ired h osts, predicting the effects of
environm ental change o n infections is often challenging
(L afferty an d H o lt 2003). D epending u p o n the p arasite’s
specificity, th e loss o f even one h o st species can
effectively elim inate the parasite fro m the system, even
w hen the rem aining hosts persist. F ield d a ta suggest th a t
m any com plex life cycle parasites (especially trem atodes)
increase in abun d an ce w ith low to m o d erate levels of
eu tro p h icatio n (L afferty 1997, Jo h n so n a n d C arp en ter
2008). This often occurs because o f (1) increases in
interm ediate h o st density follow ing nutrien t-m ed iated
21
changes in p rim ary a n d secondary p ro d u c tio n a n d (2) an
increased ability o f interm ediate hosts to w ith stan d
infection u n d er nu trien t-rich conditions (i.e., decrease in
p arasite-in d u ced m ortality). M a n y o f these parasites
d ep en d on in v erteb rate interm ed iate hosts, such as
snails, w orm s a n d cru stacean s, w hich can resp o n d
quickly an d strongly to n u trie n t inputs (Z an d er a n d
R eim er 2002, Jo h n s o n a n d C a rp e n te r 2008). T he
resulting increase in infection can enhance disease a n d
p ath o lo g y in som e h o st species.
Because o f the difficulties inh eren t in m an ip u latin g
com plex life cycle p a ra site s, ex p erim en tal research
involving m ore th a n one h o st species o r p arasite stage
in the life cycle are rare. H ow ever, a recent com bin atio n
o f field surveys a n d experim ents suggest a link betw een
a q u atic e u tro p h icatio n an d infection by the digenetic
trem ato d e Ribeiroia ondatrae. Ribeiroia uses freshw ater
snails as first in term ediate h osts, larval am phibians as
second in term ediate hosts, a n d birds as definitive hosts
(Jo h n so n et al. 2004). In am phibians, Ribeiroia infection
can cause high frequencies (> 5 0 % ) o f severe limb
m alform atio n s, including m issing, m isshapen, a n d extra
lim bs (Fig. 1C; Sessions a n d R u th 1990, Jo h n so n et al.
1999, 2002). Such deform ities, w hich are considered a
m a jo r d etrim en t to a m p h ib ian survival, are widely
suspected to have increased in recent decades (Johnson
e t al. 2003), b u t the reasons fo r the a p p a re n t increase
rem ain speculative. P revious field surveys suggested a
link betw een w etlands w ith deform ed am phibians a n d
n u trie n t ru n o ff fro m a g ric u ltu ra l fertilizers, ca ttle
grazing, a n d u rb an izatio n (Jo h n so n et al. 2002, Jo h n so n
a n d C hase 2004). Jo h n so n a n d C hase (2004) h y p o th e ­
sized th a t, by stim ulating algae gro w th in w etland
h ab itats, n u trie n t ru n o ff enhanced the p o p u latio n o f
h erbivorous snails, providing g reater in term ediate h o st
availability fo r Ribeiroia.
Jo h n so n et al. (2007) tested this hypothesis by m a ­
n ip u latin g n u trie n t in p u ts into a series o f o u td o o r
m esocosm s stocked w ith snails, larval am phibians, a n d
parasites. E u tro p h ic atio n indirectly increased infection
th ro u g h changes in the a q u atic fo o d web. E xperim en­
tally elevated n u trie n t levels led to a n increase in
periphytic algal grow th, w hich enhanced gro w th a n d
rep ro d u ctio n o f snail hosts (Planorbella trivolvis). H ig h ­
er snail densities increased the likelihood th a t hatching
parasites (m iracidia) successfully fo u n d a snail host,
th ereby leading to a larger n u m b er o f infected snails.
Infected snails from the h ig h -n u trien t co n d itio n also
produced, o n average, twice as m an y parasites p er 24
h o u rs relative to snails in the lo w -n u trien t treatm en t,
likely as a result o f higher fo o d (algae) availability a n d
low er m o rtality (Jo h n so n et al. 2007). T he com bin atio n
o f m ore infected snails an d a g reater p er snail release o f
parasites led to a three- to fivefold increase in am p h ib ian
infection (Fig. 2C), w hich is a d irect p red icto r o f disease
risk (Jo h n so n et al. 2007). O th er experim ents have
d e m o n strated sim ilar increases in parasite p ro d u ctio n in
22
T a ble 1.
E c o lo g ic a l A p p lic a tio n s
V o l. 20, N o . 1
IN V ITE D FE A T U R E
Overview of human illnesses and associated symptoms caused by harmful algae.
Illness
Major vector
Symptoms
Amnesic shellfish poisoning
domoic acid from Pseudo-nitzschia sp. in shellfish
Diarrhetic shellfish poisoning
Neurotoxic shellfish poisoning
okadaic acid from Dinophysis sp. in shellfish
brevetoxin from Karenia sp. in shellfish, aerosolized
toxins
saxitoxin from Alexandrium sp. and other species
in shellfish
microcystins and other toxins from Microcystis and
other cyanobacteria in water
gambiertoxins/ciguatoxins from Gambierdiscus sp.
that accumulate in reef fish
Paralytic shellfish poisoning
Cyanotoxin poisoning
Ciguatera fish poisoning
response to food q u an tity a n d q u ality (K eas a n d Esch
1997, S andland an d M inchella 2003).
R esults from various u n p lan n ed “n a tu ra l” experi­
m ents fu rth er su p p o rt links betw een n u trie n t enrichm ent
a n d elevated infection by com plex life cycle parasites.
F o r exam ple, C oyner et al. (2003) fo u n d a strong
a ss o c ia tio n betw een sew age tre a tm e n t ru n o f f a n d
infection by the nem ato d e Eustrongylides ignotus, w hich
can increase nestling m o rtality in w ading birds. In p u ts
o f N an d P w ere positively correlated w ith the density o f
first interm ediate hosts (a tubificid w orm ) a n d w ith
infection in second interm ediate hosts (m osquitofish).
Follow ing diversion o f the sewage a n d a corresponding
re d u c tio n in n u trie n t c o n c e n tra tio n s, in fectio n s in
m osquitofish declined from 54% in 1990 to 0% in 1998
(C oyner et al. 2003; see also W eisberg et al. 1986 an d
M u zzall 1999 fo r a d d itio n a l exam ples). S im ilarly,
sewage inputs into G ull F ake, M ichigan, were linked
to a fourfold increase in infection o f mayflies by the
trem ato d e Crepidostom um cooperi (M arcogliese et al.
1990). D eep-w ater h y poxia caused by nutrien t-m ed iated
e u tro p h icatio n o f the lake altered the d istrib u tio n o f
oxygen-sensitive mayflies, forcing them in to shallow er
w ater a n d into closer p roxim ity w ith sphaeriid clam s,
w hich are the first in term ediate hosts o f Crepidostomum.
A fter the lak e’s sewage system w as im proved in 1984,
infection prevalence in m ayflies declined by 70% w ithin
five years (M arcogliese et al. 1990), presum ably ow ing to
the m ovem ent o f mayflies in to deeper w ater.
N oninfectious diseases
Finally, environm ental n u trien t en richm ent can influ­
ence levels o f noninfectious diseases. N o ninfectious
disease represents a b ro a d category o f h ealth conditions
ranging from cancer to hypoxia; etiological factors can
include chem ical exposure, tem p eratu re, oxygen av ail­
ability, an d biotoxins p ro d u ced by algae, plan ts, fungi,
a n d bacteria. In a q u a tic systems, the m o st com m on
noninfectious con d itio n associated w ith environm ental
n u trie n t enrichm ent is hypoxia, w hich can result from
n u trient-induced eu tro p h icatio n . Excess fertilizer ru n o ff
in to rivers an d coastal systems has been linked to
expanding “dead zones” in the E a rth ’s oceans, w ith
short-term memory loss; vomiting,
cramps
diarrhea, vomiting, cramping
nausea, diarrhea, respiratory
distress, eye irritation
numbness around lips and
mouth, respiratory paralysis, death
skin irritation, respiratory irritation,
tumor promotion, liver cancer, failure
gastrointestinal distress, numbness
around mouth, reversal o f hot and
cold sensations, hypotension
serio u s co n seq u en ces fo r fisheries p ro d u c tio n a n d
ecosystem process (see D iaz a n d R osenberg 2008).
U n lik e w ith in fe c tio u s d iseases, th e d y n am ic s o f
“ p a th o g e n s” resp o n sib le fo r n o n in fe c tio u s diseases
m ay have lim ited o r no dependency on the dynam ics
o f the species experiencing pathology. Som e allergic
diseases, fo r exam ple, have exhibited su b stan tial in ­
creases in recent decades, an d currently affect m illions o f
peoples in developed countries (e.g.. Sly 1999). H igh
pollen co u n ts cause hayfever, allergenic rhinitis, an d
allergenic asth m a, a n d fo r those already suffering from
o th er p u lm o n ary ailm ents, these p o llen-induced re ­
sponses can be especially serious (N atio n al In stitu tes
o f H e a lth 1993). P o llen co u n ts have in creased in
m u ltiple highly p o p u la te d regions (e.g.. C lo t 2003,
Spieksm a et al. 2003), fo r reasons th a t m ay be related
clim ate change, shifts in species co m p o sitio n , a n d
increased atm o sp h eric C O 2 a n d environm ental n u trien t
en richm ent (W ayne et al. 2002). Pollen p ro d u ctio n in
m an y w eedy species freq u en tly increases follow ing
n u trien t en richm ent (F a n et al. 1995). F o r exam ple, N
fe rtiliz a tio n c au sed su b s ta n tia l in creases in p o llen
p ro d u c tio n o f ragw eed, one o f the m o st p roblem atic
sources o f allergenic pollen (T ow nsend et al. 2003), an d
recent evidence suggests th a t pollen grains in p olluted
atm o sp h eres— to w hich reactive N is an im p o rta n t
c o n trib u to r— display an altered surface structure an d
chem istry th a t led to enhanced allergenicity (M ajd et al.
2004).
Increased in p u ts o f n u trien ts in to a q u atic ecosystem s
can also cause p ro n o u n ced changes in h arm fu l algal
bloom s (H ABs), w hich are p roliferations o f algae an d
cy an o b acteria th a t can cause m assive fish kills, m arine
m am m al kills, co n tam in ate seafood o r drin k in g w ater
w ith toxins, o r a lte r ecosystem s in w ays th a t are
d etrim en tal (G lib ert a n d P itch er 2001, B acker a n d
M cG illicuddy 2006). A lgae p roduce a w ide range o f
toxins (Table 1) w hich m ay accum ulate in p red ato rs an d
organism s higher in the fo o d web, ultim ately affecting
h u m an s w hen seafood is consum ed, w hen toxin-laden
aerosols are inhaled, or w hen c o n tam in ated w ater is
consum ed. Toxic syndrom es include p aralytic, am nesic,
diarrheic, n eurotoxic, a n d cyanotoxic shellfish p o iso n ­
January 2010
PERSPECTIVES O N T H E M O D E R N N CYCLE
ing, am on g others. Evidence is also m o u n tin g th a t
H A B s can elicit subtle effects on fish an d wildlife (Fig.
ID ). F o r exam ple, dom oic acid, a n eu ro to x in p ro d u ced
by the d iato m Pseudo-nitzschia spp., induces seizure an d
m em ory loss in la b o ra to ry an im als (T iedeken an d
R am sdell 2007). Toxins fro m dinoflagellates can cause
reproductive dysfunction in w hales (e.g., D o u cette et al.
2006), an d em bryonic deform ities in oysters (G lib ert et
al. 2007a). In ad d itio n , aerosolized red tide toxins can
exacerbate resp ira to ry sym ptom s am o n g asth m atics
(M ilian et al. 2007). E x p o su re to p ep tid e to x in s
pro d u ced by cy an o b acteria have also been suggested
as co ntributing to increased rates o f liver cancer in
po p u latio n s consum ing w ater fro m n u trie n t rich lakes
(G rosse et al. 2006).
T h ro u g h o u t m an y p a rts o f the w orld, m arine an d
freshw ater H A B s are increasing in geographic extent, in
d u ra tio n o f occurrences, in num bers o f toxins a n d toxic
species identified, in nu m b ers o f fisheries affected, a n d in
eco n o m ic co sts (A n d e rso n 1989, H a lle g ra e ff 1993,
A nderson et al. 2002, G lib ert et al. 2005). W hile m any
factors likely influence these increases, n u trie n t ru n o ff in
freshw ater a n d m arine ecosystem s is likely a n im p o rta n t
co n trib u to r (N atio n al R esearch C ouncil 2000, V. H .
Sm ith et al. 2006). F o r exam ple, in the G u lf o f M exico, the
sedim entary reco rd o f p o tentially toxic d iato m s {Pseudonitzschia spp.) has increased in parallel w ith increased
n itrate loading over the p a st several decades (T u rn er an d
R ab alais 1991, P arso n et al. 2002). Sim ilarly, bloom s of
toxic H A B s o ff the co ast o f C h in a have expanded in recent
years in geographic extent (square kilom eters to tens of
square kilom eters), d u ra tio n (days to m o n th s), a n d in
harm ful im pacts. These changes are strongly correlated to
increases in fertilizer use over the p a st tw o decades (Fig.
2D ; A nderson et al. 2002, Z h o u et al. 2003, F i et al. 2009).
M oreover, the B altic Sea, A egan Sea, N o rth e rn A driatic,
an d B lack Seas have all experienced increased H A B
occurrences in relatio n to n u trie n t loading (e.g., F arsson
et al. 1985, B odeanu 1993, M onch ev a et al. 2001, H eisler
et al. 2008).
C hanges in the type o f n u trien ts o r th eir relative
p ro p o rtio n s c an also influence th e freq u en cy a n d
severity o f H A B s. O ff the co ast o f G erm any, tim e series
analysis o f n u trie n t co n cen tratio n s over several decades
has revealed th a t a fo u rfo ld increase in the ra tio of
nitrogen: silicate (N:Si) coincided w ith a n increase in the
H A B Phaeocystis (R ad ach et al. 1990). The specific
form s o f available N a n d P, p articu larly w ith respect to
organic nutrients, also play a n im p o rta n t role in the
n u tritio n o f m an y H A B s (G libert a n d F eg ran d 2006).
F o r exam ple, bloom s o f the H A B species Aureococcus
anophagefferens, w hich have been linked to reductions in
shellfish rep ro d u ctio n (T racey 1988, G allag h er et al.
1989), correlate w ith increases in organic co m p ared to
inorganic loading (F aR o ch e et al. 1997, G lib ert et al.
20076). O th er w o rk has show n th a t n u trien t availability
o r com position m ay even alter the toxin c o n ten t of
individual species w ith o u t altering th eir to ta l a b u n ­
23
dance. F o r the d ia to m Pseudo-nitzschia australis, the
fo rm o f N influences b o th the gro w th ra te as well as the
tox in content. Cells grow n o n urea, fo r exam ple, h a d
h igher levels o f the toxin, dom oic acid, relative to those
grow n o n n itra te o r am m o n iu m (A rm stro n g -H o w ard et
al. 2007). Sim ilarly, the tox in c o n ten t o f u rea-grow n cells
o f the dinoflagellate A lexandrium tamarense, w hich
causes p araly tic shellfish poisoning, w as significantly
h igher th a n cells grow n on n itrate (F eong et al. 2004).
Sum m ary o f nutrients and disease
W hile the effects o f n u trien ts vary w ith enrichm ent
levels, the types o f h o st a n d p ath o g en , a n d the c h a ra c te r­
istics o f ecosystem s, the above exam ples illustrate th a t
e u tro p h icatio n can have im p o rta n t indirect effects on
h u m a n a n d wildlife diseases. R ecent experim ents have
shed new light o n the m echanism s u n d erp in n in g the
observed links betw een n u trie n t en richm ent a n d disease.
D epending on the m ode o f transm ission, these m ech a­
nism s m ay affect th e p a th o g e n , th e h o st, o r th eir
in te ra c tio n , a n d include changes in th e d en sity o r
d istrib u tio n o f suitable h o sts/v ecto rs, a lte ra tio n s in
p h y sical h a b ita t, in creases in p a ra s ite p ro d u c tio n ,
selection fo r m o re v irulent o r toxic p athogens, a n d the
p rovisioning o f path o g en s w ith supplem ental resources.
It is im p o rta n t to n o te th a t the effects o f n u trie n t
en richm ent vary am ong p ath o g en s a n d d o n o t alw ays
elicit higher disease risk; exacerbation o f a b ro a d suite o f
d iseases does a p p e a r p ossible, b u t th e decline o r
e lim in a tio n o f o th ers is also po ssib le. M o re o v e r,
increases in p arasite species richness o r a b u n d an ce do
n o t alw ays reflect a n increase in disease risk, as disease is
also a fu n ctio n o f the h o st’s response to infection.
C u rre n t evidence suggests th a t n u trien t in p u ts will fav o r
generalist o r o p p o rtu n istic p ath o g en s w ith d irect o r
simple life cycles. Im p o rta n tly , how ever, because these
p ath o g en s are generalists w ith little dependency o n the
dynam ics o f any one h o st species, they m ay cause
sustained epidem ics or h o st extirp atio n s w ith o u t suffer­
ing a red u ction in transm ission. N o ninfectious diseases
such as H A B s, pollen allergies, a n d avian botulism
rep resen t the extrem e p o sitio n in this g rad ien t in th a t the
dynam ics o f the “p ath o g e n ” (e.g., a h arm fu l alga) are
com p letely d iv o rced fro m th e species experiencing
p athology. T hus, declines in “h o sts” do n o t necessarily
lead to declines in the p athogen. P arasites w ith com plex
life cycles th a t depend o n m ultiple, interacting species
w ithin a com m unity to com plete transm ission are often
m o re sensitive to en v ironm ental d isturbance, as losses in
an y one h o st can reduce or elim inate the infection cycle
(see H u d so n et al. 2006). H ow ever, if interm ediate hosts
are to le ra n t o f (or thriv e u n d er) elevated n u trie n t
conditions, such as som e h y p o x ia-to leran t snails a n d
tubificid w orm s, infection a n d p ath o lo g y can respond
positively to inputs o f N a n d P. Such situations can lead
to increased disease w ithin o th er hosts in the life cycle
(e.g., am p h ib ian m alform ations).
24
IN V ITE D FE A T U R E
A lth o u g h m any exam ples discussed here focus on
wildlife diseases, we argue th a t the sam e p attern s,
interactions an d co ntrols are relevant fo r u n d erstan d in g
the effects o f n u trien t en richm ent on m an y zoon o tic
h u m an diseases. F o r exam ple, as discussed fo r m alaria
a n d W N V , n u trien t ru n o ff into freshw ater h a b itats can
increase m o sq u ito oviposition, larval gro w th rate, an d
a lter the vector com m unity to fav o r disease transm ission
in hum ans. W hile vector ab u n d an ce is a n im p o rtan t
p red icto r o f disease transm ission, m o re w o rk is needed
to definitively lin k n u tr ie n t in p u ts w ith in fec tio n
incidence in hum an s from endem ic areas. Sim ilarly, in
a d d itio n to affecting wildlife, H A B s can cause significant
disease in hum ans a n d costly econom ic losses. Collec­
tively, there are > 6 0 0 0 0 incidents o f h u m a n exposure to
algal toxins annually in the U SA , resulting in ~ 6 5 0 0
d eaths (H o ag lan d et al. 2002). C osts associated w ith
public health, shellfish recalls, a n d decreased tourism
a p p ro a c h U S$50 m illion annually. (H u b b a rd et al.
2004). F inally, com plex life cycle parasites o f m edical
a n d v e te rin a ry im p o rta n c e m ay be in flu en ced by
changing n u trien t levels. In livestock, the ru m in a n t liver
fluke (Fasciola hepatica) has caused m ore th a n U S$2
billion in livestock in d u stry losses (B oray a n d M u n ro
1998). Infected snail hosts resp o n d strongly to food
q uality a n d qu an tity , altering the o u tp u t o f infectious
p a ra s ite s by n early sev en fo ld o v e r sta rv e d snails
(K endall 1949). Infections by som e schistosom es (h u ­
m a n b lo o d flukes), w hich continue to afflict 200 m illion
people in A frica, S o u th A m erica, a n d A sia, have also
been associated w ith increased algal gro w th a n d organic
n itro g en in w etland h ab itats (G arcia 1972). C onsidering
the strong response o f Ribeiroia infection to elevated
n u trie n t conditions a n d the ecological parallels betw een
the life cycles o f Ribeiroia a n d Schistosom a, these results
m ay have im p o rta n t epidem iological im plications.
A look to the fu tu re
M an y diseases th a t affect b o th h u m an s a n d wildlife
have increased in incidence o r severity in recent decades,
freq u en tly resu ltin g fro m changes in th e ecological
in te ra c tio n s am o n g a p a th o g e n , its h o sts, a n d th e
en v iro n m en t in w hich they co-occur (D aszak et al.
2000). The im portance o f in co rp o ratin g ecology in to the
study o f p arasite s a n d em erging diseases h as been
em phasized w ith increasing urgency in recen t years
(N atio n al R esearch C ouncil 2001, M illennium Ecosystem
A ssessm ent 2005). In th e ir synthesis o f th e G ra n d
C hallenges in E n v iro n m en tal Sciences, the N a tio n a l
R esearch C ouncil (2001) listed infectious disease as one
o f the eight m o st pressing en v ironm ental issues, a d v o c a t­
ing a “ systems-level” a p p ro a c h to u n d erstan d in g disease
em ergence. N evertheless, the ecology o f zoon o tic diseases
is often rem arkab ly com plex, rendering predictions o f
th eir responses to an th ro p o g en ic change n o tab ly difficult
(D aszak et al. 2000, P atz et al. 2004). Such challenges are
exacerbated by the fact th a t hum an -in d u ced changes to
the environm ent rarely occur in isolation; fo r exam ple.
E c o lo g ic a l A p p lic a tio n s
V o l. 20, N o . 1
n u trie n t lo ad in g to surface w aters is n early alw ays
co m b in ed w ith su b sta n tia l la n d use changes in the
su rro u n d in g w atersh ed s, w ith co n c o m ita n t shifts in
species ab u n d an ces. T hus, p arsing o u t the p o ten tial
effects o f a single fac to r such as n u trie n t loading is often
a tall order, one w hich typically requires controlled,
m echanistic studies to begin the co n stru ctio n o f m ore
pro g n o stic m odels. F o r exam ple, lim ited evidence has
linked cholera to coastal e u tro p h icatio n a n d seasonal
p la n k to n bloom s. T he b acte riu m responsible. Vibrio
cholerae, can becom e co n cen trated in fishes, shellfishes,
a n d especially in biofllms o n the surface o f crustacean
zo o p lan k to n (E pstein 1993, Colwell 1996). H ow ever,
p a ttern s o f h u m an behavior, clim ate, a n d ocean circu­
la tio n also influence in fectio n dynam ics, m ak in g it
difficult to identify the relative im p o rtan ce o f n u trien t
in p u ts (C olw ell a n d H u q 2001, R o d o et al. 2002,
C o ttin g h am et al. 2003).
W e have sum m arized a few experim ental studies th a t
focused o n n u trie n t effects, b u t such experim ents rem ain
rare a n d are thus a p rio rity in ad vancing o u r ability to
forecast the future o f b o th h u m a n a n d wildlife infectious
disease (M cK enzie a n d T ow nsend 2007, Jo h n so n an d
C arp en te r 2008). B ased o n the evidence to date, we
expect th a t en v iro n m en tal n u trie n t en rich m en t will
rem ain a n im p o rta n t facto r in the etiology o f h u m an
a n d wildlife diseases fo r decades to come. A lth o u g h
aw areness a n d technological inn o v atio n s have slowed
the p ro b lem in som e regions, ongoing p attern s o f
atm o sp h eric d eposition o f reactive nitrogen, losses o f
w etland a n d rip a ria n areas, increasing use o f fertilizers
in developing natio n s, grow ing livestock popu latio n s,
a n d an increasing h u m a n p o p u la tio n all suggest th a t
e u tro p h icatio n will continue to exp an d (M illennium
Ecosystem A ssessm ent 2005). M oreover, even if the
co n trib u tin g drivers are reversed, e u tro p h icatio n tends
to be a p ersistent co n d itio n because o f feedback loops
a n d the in tern al recycling o f n u trien ts (e.g.. C arp en ter
2005, V. H . Sm ith et al. 2006).
T he disease-related outcom es o f n u trie n t enrichm ent
are likely to exhibit p ro n o u n ced regional variation. O ur
grow ing u n d erstan d in g o f spatial a n d tem p o ral p attern s
in b o th em erging infectious diseases (e.g., Jones et al.
2008) a n d in rapidly changing n u trie n t cycles (G allow ay
et al. 2004) allows a focus on regionally targ eted efforts
th a t m ay pose the g reatest risks. F o r exam ple, in heavily
industrialized regions such as the U n ited States, E urope,
a n d p a rts o f A sia, an th ro p o g en ic in p u ts o f N a n d P to
th e en v iro n m en t have been excep tio n ally h ig h fo r
decades, resulting in ecosystem s already d em o n stratin g
significant change in response to such disturbance. F ro m
the perspective o f h u m an infectious diseases, the overall
risk o f n u trien t-d isease interactions m ay be low er in
these tem perate regions sim ply because the diversity o f
infectious diseases responsive to n u trien ts is low er th a n
th a t in tro p ical regions (e.g., G u ern ier et al. 2004).
H ow ever, a w arm in g clim ate a n d g lobal tra n sp o rt
systems continue to increase the p o ten tial fo r a suite o f
January 2010
PERSPECTIVES O N T H E M O D E R N N CYCLE
v ecto r tra n sm itte d diseases to ex p a n d in to h ig h er
latitude zones (P atz an d O lson 2006, Sm ith et al.
2007). N oninfectio u s diseases, including H A B s a n d
pollen-based allergies, are already intensifying in tem ­
perate regions w ith ongoing n u trie n t deposition. In the
sh o rt term , som e o f the m o st pressing th rea ts from
elev a ted n u trie n ts m a y be to w ildlife: in heavily
industrialized tem p erate regions, m an y critical h ab itats
are already greatly reduced in size a n d subject to a suite
o f o th er disturbances from invasive species to acidic
precipitation; here, increased disease prevalence from
n u trien t loading m ay fu rth er com plicate conservation
efforts.
C onservation challenges are also rising in tropical
regions, w hich in recent decades have exhibited the m ost
d ram atic increases in lan d clearing a n d industrialization.
Follow ing the precedents observed in higher latitudes,
such changes are causing ra p id increases in the loading
o f excess N an d P to the environm ent; over the next 50
years, the tropical latitudes will see the m o st significant
increases in fertilizer use a n d atm o sp h eric depo sitio n of
N (G allow ay et al. 2004, D en ten er 2006). A t the same
tim e, these regions su p p o rt the highest diversity of
h u m an p athogen s w ith the p o ten tial to resp o n d to
n u trien t enrichm ent (see G u ern ier et al. 2004, M cK enzie
an d T ow nsend 2007). G iven this high degree o f overlap
in tropical regions, the p o ten tial fo r n u trien ts to affect
p attern s o f h u m a n disease in the fu tu re is p redicted to be
very high (M cK enzie a n d T ow nsend 2007). Som e o f the
m ajo r plagues o f low latitudes, such as m ala ria an d
schistosom iasis, show w orrisom e signs o f elevated risk in
m ore eutro p h ic conditions, suggesting th a t forecasted
increases in env ironm ental n u trie n t en richm ent could
incur increases in h u m a n disease risk. T ak en as a w hole,
the intersection o f a high diversity o f h u m an p arasitic
an d infectious diseases w ith ra p id changes in the en ­
vironm ent, including those to n u trien t cycles, suggests
th a t som e o f the g reatest nu trien t-d riv en risks to hum ans
from infectious diseases are likely to be in low latitude
countries. In a recent analysis o f global trends in
em erging infectious diseases, Jones et al. (2008) e m p h a­
sized b o th the risks a n d challenges o f the tropics by
pointing o u t th a t n o t only are such zones a likely
h o tsp o t fo r em erging diseases o f h u m an s an d wildlife,
b u t are also typified by p o o r h ea th in frastru ctu res an d
lim ited reporting o f disease outbreaks.
T hus, while a b etter u n d erstan d in g o f links betw een
n u trien ts a n d disease is needed o n a global basis, we
em phasize its p artic u la r im portance in tro p ical an d
subtropical A frica, A sia, a n d L atin A m erica. All three
c o n tin e n ts c o n ta in re g io n s ex p erie n c in g ex plosive
grow th an d developm ent, while still conten d in g w ith
ra m p a n t poverty, w idespread en v ironm ental dam age,
an d a huge disease b urden. W ith o u t question, increases
in fertilizer applicatio n a n d fo o d p ro d u c tio n in these
regions will likely have substantially positive effects on
h u m an h ealth by reducing m a ln u tritio n a n d im proving
quality o f life. H ow ever, a significant concern lies w ith
25
the u n in ten d ed side effects o f such efforts: will increases
in the a lteratio n o f en v ironm ental n u trien t co n cen tra­
tions in cu r a n d increased risk o f disease? Ecologists,
epidem iologists, an d agronom ists are collectively ch al­
lenged to determ ine (1) u n d e r w h a t con d itio n s n u trien t
en richm ent will enhance disease risk a n d (2) th ro u g h
w h a t strategies ag ricu ltu ral intensification can be ac­
co m panied by careful m an ag em en t o f disease-related
outcom es.
A c k n o w le d g m en t s
We thank L. Martinelli and all those who organized and
supported the N2007 conference for providing the forum that
led to this manuscript. This is contribution number 4224 from
the University of Maryland Center for Environmental Science.
P. Johnson was supported by a fellowship from the David and
Lucille Packard Foundation.
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