EcoHealth

, Volume 5, Issue 3, pp 268–274 | Cite as

Chytridiomycosis and Amphibian Population Declines Continue to Spread Eastward in Panama

  • Douglas C. Woodhams
  • Vanessa L. Kilburn
  • Laura K. Reinert
  • Jamie Voyles
  • Daniel Medina
  • Roberto Ibáñez
  • Alex D. Hyatt
  • Donna G. Boyle
  • James D. Pask
  • David M. Green
  • Louise A. Rollins-Smith
Short Communication

Abstract

Chytridiomycosis is a globally emerging disease of amphibians and the leading cause of population declines and extirpations at species-diverse montane sites in Central America. We continued long-term monitoring efforts for the presence of the fungal pathogen Batrachochytrium dendrobatidis (Bd) and for amphibian populations at two sites in western Panama, and we began monitoring at three new sites to the east. Population declines associated with chytridiomycosis emergence were detected at Altos de Campana National Park. We also detected Bd in three species east of the Panama Canal at Soberanía National Park, and prevalence data suggests that Bd may be enzootic in the lowlands of the park. However, no infected frogs were found further east at Tortí (prevalence <7.5% with 95% confidence). Our results suggest that Panama’s diverse and not fully described amphibian communities east of the canal are at risk. Precise predictions of future disease emergence events are not possible until factors underlying disease emergence, such as dispersal, are understood. However, if the fungal pathogen spreads in a pattern consistent with previous disease events in Panama, then detection of Bd at Tortí and other areas east of the Panama Canal is imminent. Therefore, development of new management strategies and increased precautions for tourism, recreation, and biology are urgently needed.

Keywords

amphibian Batrachochytrium dendrobatidis chytridiomycosis emerging disease Panama population declines 

The emerging disease chytridiomycosis, caused by the skin fungus Batrachochytrium dendrobatidis (Bd), has resulted in population declines and possible extinctions of hundreds of amphibian species and caused subsequent ecosystem alterations (Lips et al., 2006; Whiles et al., 2006; Finlay and Vredenburg, 2007; Gascon et al., 2007; Skerratt et al., 2007; Verburg et al., 2007). The disease has spread in a predictable pattern southeastward throughout the Cordillera Central mountain range in Central America (Lips et al., 2006; Gagliardo et al., 2008). We continued long-term monitoring of two sites in western Panama: Fortuna Forest Reserve (Fortuna) and General de División Omar Torrijos Herrera National Park (Omar Torrijos) (Lips, 1999; Lips et al., 2006). We began monitoring three additional sites to the east predicted to be affected by chytridiomycosis (Altos de Campana, Soberanía, and Torti) (Lips et al., 2008).

Altos de Campana National Park (Campana, area: 4925 ha; elevational range: 140–1020 m) is a high elevation site just west of the Panama Canal and separated from the Cordillera Central by approximately 35 km of lowlands that include a mosaic of heavily modified land cover. Bordering the canal to the east, Soberanía National Park (Soberanía, area: 19,541 ha; elevational range: 26–332 m) is 30 km north of Panama City. These parks contain a relatively high diversity of amphibian species; 65 species have been recorded at Campana (59 anuran, 4 salamander, and 2 caecilian species) and 56 at Soberanía (53 anuran, 2 salamander, and 1 caecilian species). Generalized drastic amphibian population declines have not previously been reported from these sites, the lowlands along the canal, or anywhere east of the canal in Panama (Condit et al., 2001; Ibáñez et al., 2002), and the fungal pathogen was not previously detected.

We surveyed amphibian assemblages for diversity and disease at five sites ranging across Panama (Fig. 1). Each survey included two people searching along forest and stream transects for approximately 10 hours over 2–3 nights. Amphibians were captured by hand in new plastic bags and swabbed using sterile technique 10 times each on the ventral surface, thighs, and feet according to Hyatt et al. (2007). Diagnosis of Bd infection status was performed by Taqman real-time PCR assay according to Boyle et al. (2004). All samples were analyzed in triplicate (except samples from Campana, June–August 2006, run once) and compared with Australian Animal Health Laboratory zoospore standards.
Figure 1

Elevation map projection of Panama displaying sites and dates of first detection of B. dendrobatidis in amphibian populations. Sites are described in Table 2. Produced by Matthew Becker using ArcGIS Version 9.2, Environmental Systems Research Institute, Inc., Redlands, CA with data available from the United States Geological Survey, EROS Data Center, Sioux Falls, SD based on the World Geodetic coordinate System of 1984 (WGS84).

The mean prevalence of infection and 95% confidence interval based on a binomial distribution are recorded for each site and survey period (Table 1). All site-survey periods were then designated into one of four disease categories: naïve, emerging, epizootic, or enzootic (Table 1). We defined “naïve” as any amphibian assemblage in which Bd was never detected and population declines had not been observed. The “emerging” disease category indicates that Bd infections were recently detected (the first instance) and no signs of chytridiomycosis or population declines were observed. The “epizootic” disease category indicates that Bd infections were detected and associated with disease and population declines. The “enzootic” disease category indicates that Bd infections were present after population declines.
Table 1

Prevalence of Infection with Batrachochytrium dendrobatidis (Bd) in Panamaa

Location

Date

N species sampled

Infection prevalence (%), (N infected/N swabbed)

95% Confidence interval

Disease category

Fortuna

1993–1995

35

0b,c

 

Naïve

Dec 1996

10

c,d

 

Epizootic

Jan 2006

3

18.2 (2/11)

2.3–51.8

Enzootic

Jan 2007

2

42.9 (3/7)

9.9–81.6

Enzootic

Omar Torrijos

Jan 2004

9

0 (0/61)

0–5.9

Naïve

2000–Sept 2004

59

0 (0/1566)e

0–0.0024

Naïve

Oct–Dec 2004

48

49.2 (432/879)e

45.8–52.5

Epizootic

Jan 2005

6

23.8 (5/21)

8.2–47.2

Enzootic

Jan 2006

3

0 (0/3)

0–70.8

Enzootic

Jan 2007

1

0 (0/10)

0–30.9

Enzootic

Aug 2007

11

5.1 (3/59)

1.1–14.2

Enzootic

Barrigon–Omar Torrijos

Jan 2005

1

100.0 (12/12)

73.5–100

Epizootic

Rio Blanco–Omar Torrijos

Jan 2007

1

60.0 (6/10)

26.2–87.8

Epizootic

El Valle

Jan 2005

2

25.0 (1f/4)

0.6–80.6

Naïve

Apr 2006

 

g

 

Epizootic

Chica/Campana

Jan 2005

1

0 (0/32)

0–10.9

Naïve

Campana

Jan 2005

14

0 (0/145)

0–2.5

Naïve

Jan 2006

4

0 (0/27)

0–12.8

Naïve

June–Aug 2006

25

12.8 (34/266)

9.0–17.4

Emerging

Jan 2007

4

47.1 (8/17)

23.0–72.2

Epizootic

Aug 2007

3

5.0 (1/20)

0.1–24.9

Enzootic

Soberanía

Jan 2007

3

30.0 (9/30)

14.7–49.4

Possibly enzootic

Tortí

Aug 2007

8

0 (0/49)

0–7.25

Naïve

aSites are categorized as naïve, emerging, epizootic, or enzootic based on Bd presence, disease occurrence, and population declines (see text).

bNo indications of Bd.

cLips, 1999.

dBerger et al., 1998.

eLips et al., 2006.

fSuspicious positive.

gGagliardo et al., 2008.

Amphibian declines associated with Bd were well documented at three sites where amphibian diversity (richness and abundance) remains low: Fortuna, Omar Torrijos, and El Valle (Lips, 1999; Lips et al., 2006; Gagliardo et al., 2008). Our sampling revealed that Bd persists at Fortuna 11 years after disease emergence, and is now enzootic at these sites (Table 1). At Campana, we monitored amphibian populations for 3 years. Our results showed sharp population declines occurred after the detection of Bd in June 2006, and sometime between August 2006 and January 2007 (Fig. 2A). A decline in species richness after the epizootic was also evident (Appendix). Koch’s postulates were fulfilled for the common rocket frog Colostethus panamensis sampled from Campana (Lips et al., 2006). Thus, the timing of disease emergence and associated population declines at Campana is on a similar scale to that shown for Omar Torrijos (Lips et al., 2006).
Figure 2

(A) Population trends of six amphibian species at Altos de Campana National Park. Infection of amphibians with B. dendrobatidis was first detected at this site in June 2006. A survey includes two people × 2–3 nights search effort. (B) Mean prevalence of infection with B. dendrobatidis across sites categorized as naïve, emerging, or enzootic (see Table 1). Infection prevalence at Soberanía in January 2007 is displayed for comparison. Contributing to the variation shown here, overall infection prevalence may be influenced by species, elevation, and season sampled.

We detected infections on three species at Soberanía in a January 2007 survey. These species persisted at the site and we did not detect a population decline upon repeat survey in February 2008. Earlier surveys for disease at Soberanía are not known, but comparisons to infection prevalence and disease category of other sites suggests that Bd may already be enzootic at Soberanía (Fig. 2B). Bd was not detected (actual prevalence <7.5% with 95% confidence) at Parque Natural San Francisco (area: 1500 ha; elevational range: 120–415 m) near Tortí (Tortí), bordering the Darién Province as of August 2007 (Table 1).

Based on the sequential geographic pattern of Bd detection and amphibian declines, we calculated the putative rate of pathogen spread between adjacent sites (Table 2). By our most conservative estimate, amphibian declines are not predicted to occur at Tortí until September 2012. However, it is equally plausible that Bd is already present at Tortí if it disperses at a rate equivalent to that calculated for Campana. Without knowing the dispersal mechanism or other factors underlying disease emergence, it is not possible to make more precise predictions.
Table 2

Theoretical Rates of Spread of B. dendrobatidis in Panama Assuming That the Pathogen Is Introduced from Adjacent Sitesa

Site

Name (date B. dendrobatidis first detected)

Latitude

Longitude

Distance from previous site (km)

Months before next epizootic

Rate of spread (km/month)

1

Fortuna (Dec 1996)

N08°43′30.0

W082°14′0.0

  

2.75b

2

Omar Torrijos, El Copé (Sept 2004)

N08°40′12.8

W080°35′36.1

182

94

1.9

3

El Valle (Apr 2006)

N08°34′48.0

W080°10′12.0

48

19

2.5

4

Altos de Campana (June 2006)

N08°40′30.1

W079°55′39.2

29

2

14.5

5

Soberanía (Jan 2007)

N09°40′30.7

W079°39′32.4

54

7

7.7

6

Parque Natural San Francisco, Tortí (not detected)

N08°56′20.0

W078°27′44.2

134

9–69c

1.9–14.5

aDate that Bd was first detected is an estimate for Bd appearance in amphibians at a given site; pre-decline data on the prevalence of Bd is not available from Fortuna.

bPrevious amphibian population declines caused by chytridiomycosis were reported from 1993 at Las Tablas, Puntarenas Province, Costa Rica (8”55’N, 82’44’W) (Lips, 1998; Lips et al., 2008).

cAmphibian population declines are predicted to occur at Parque Natural San Francisco upon arrival of B. dendrobatidis . Depending upon the rate of spread, an epizootic may occur as late as September 2012 or as early as September 2007.

Chytridiomycosis epizootics caused by Bd are continuing to spread among Central American amphibians resulting in population declines and extirpations at montane sites. Amphibian species extirpations and reduced population sizes can have cascading effects on both aquatic and terrestrial ecosystems (Whiles et al., 2006; Finlay and Vredenburg, 2007; Verburg et al., 2007). Chytridiomycosis is clearly an emerging disease of amphibians, but many questions remain (McCallum, 2005). Is chytridiomycosis caused by novel introductions and subsequently spread in epizootic waves (Lips et al., 2006, 2008), or are changing environmental conditions or other cofactors causing Bd to emerge as an amphibian pathogen (Pounds et al., 2006)? Our data suggest that, at montane sites, Bd may emerge as a novel pathogen, cause population collapse of multiple species, and then become locally enzootic. This transition in disease category is consistent with a study attributing a chytridiomycosis outbreak in Rana muscosa to possibly a single Bd genotype (Morgan et al., 2007). At tropical lowland sites, chytridiomycosis may not be as severe (e.g., Woodhams and Alford, 2005; Puschendorf et al., 2006; Whitfield et al., 2007). Thus, we suspect that amphibians in the lowlands along the Panama Canal may carry Bd without developing clinical signs of chytridiomycosis.

We detected Bd at Soberanía, a lowland site east of the Panama Canal. Because this site was not previously surveyed for Bd, it is difficult to determine when or how it may have arrived. Evidence including infection prevalence (Fig. 2B) and repeat surveys indicates that Bd at Soberanía is possibly enzootic. Tropical lowland sites in which populations remain relatively stable may be reservoirs for Bd. Puschendorf et al. (2006) showed that Bd was present in lowlands and highlands and appears to be enzootic throughout most of Costa Rica, but population declines occurred most frequently in the highlands. In South America, detection of chytridiomycosis associated population declines was most common at high elevations (Lips et al., 2008). Similarly, the emergence of chytridiomycosis in the Australian wet tropics may have impacted amphibian diversity at highland sites more severely than in the lowlands (McDonald and Alford, 1999). Consistent access to high temperatures or behavioral modification may inhibit infections from developing into chytridiomycosis in tropical lowlands (Woodhams et al., 2003).

For Campana, we demonstrated that Bd was probably not present before detection in June 2006 (0 of 204 swabs were positive) (Fig. 2B). Bd may have been present before our surveys at Soberanía, and examination of museum specimens would be informative. The theoretical rate of spread (Table 2) to Soberanía and Campana when calculated from adjacent epizootic sites was nearly an order of magnitude higher than that to Omar Torrijos and El Valle. This may indicate a separate introduction (e.g., Lips et al., 2008) rather than spread from a single source. Alternatively, changing environmental conditions may be partly responsible for chytridiomycosis emergence at high elevations (Pounds et al., 2006), although this has not been investigated in Panama. The proximity of Soberanía and Campana to Panama City (human population approximately 1 million) and the many tourists visiting the parks suggests human introduction is a strong possibility. Although the mechanism of dispersal between sites is not known, infection can be transmitted between amphibians by direct contact or exposure to water or substrates with infectious zoospores. Movement patterns of several species of amphibians, mainly forest floor and understory frogs, are related to seasonal rainfall in central Panama. Seasonal drying conditions of the forest floor and vegetation induce frogs to move in search of moist places, resulting in frog congregations along stream margins and drying pools (Toft et al., 1982; Ibáñez et al., 1995 [1997]; Ibáñez et al., 2002). If chytridiomycosis emergence is density dependent, these concentrations of individuals of various species of amphibians in moist areas may increase the probability of Bd transmission, and could partly explain a rapid rate of spread of Bd in central Panama. The mature sporangia stage can attach and grow on sterile moist soil and bird feathers (Johnson and Speare, 2005). Reptile and fish scales or invertebrates have not been ruled out as possible reservoirs. Zoospores can survive for hours to days depending on temperature, and a sudden drop in temperature can induce zoospore release (Woodhams et al., 2008).

Lips et al. (2008) hypothesized that certain habitats may slow the spread of Bd or prevent invasion. Because the fungus dies at temperatures exceeding 30°C and in salt water (Longcore et al., 1999; Johnson et al., 2003), hot deforested lowlands, the freshwater Panama Canal, and the marine coastal environment may be physical barriers that could slow the spread of Bd in Panama. We did not test these barriers to dispersal specifically, but suggest that human movement of the pathogen would easily overcome these barriers.

The significance of our results is that amphibian population declines associated with chytridiomycosis are continuing in Panama. Amphibian populations, species, and by extension ecosystems naïve to Bd, particularly at high elevation sites east of the Panama Canal, may be at risk. In addition, the detection of Bd in Colombian museum specimens (Ruiz and Rueda-Almonacid, 2008) raises the potential for disease spread from the south (Lips et al., 2008). Future studies should focus greater sampling effort in eastern Panama.

A range of management options should be considered. Captive breeding programs such as at the El Valle Amphibian Conservation Center in Panama and at zoos associated with the amphibian ark project (http://www.amphibianark.org, March 5, 2008) have already been successful at preserving some species in captivity (Gagliardo et al., 2008). However, repatriation is complicated by enzootic Bd at all sites with a history of disease. Thus, development of local conservation management options is urgently needed to preserve a significant portion of Panama’s large and not fully described amphibian diversity and functions within their natural ecosystems. Presently, biosecurity should be increased for scientists and ecotourism, including bleaching boots and cleaning field gear between sites, and providing information at eco-lodges about the spread of epizootics.

Notes

Acknowledgments

We thank Santana Arcia, Arquímides Batista, Forrest Brem, Roberto Brenes, James Coronado, Iván Domínguez, Aurelio González, César Jaramillo, Fr. Wally Kasuboski, Karen Lips, Julie Ray, Corrine Richards, and Manuel Rivera. This research was supported by NSF IRCEB grant DEB-0213851 (James P. Collins, P.I.; subcontracts to L.A. Rollins-Smith and A.D. Hyatt) and grants IOB-0520847 and IOB-0619536 to L.A. Rollins-Smith and a NSERC Canada Discovery Grant to D.M. Green. Scientific collecting permits from the government of Panama (Autoridad Nacional del Ambiente) were arranged with the assistance of the Smithsonian Tropical Research Institute (STRI). We gratefully acknowledge the assistance of STRI for logistical support for the all of the studies in Panama.

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Copyright information

© International Association for Ecology and Health 2008

Authors and Affiliations

  • Douglas C. Woodhams
    • 1
  • Vanessa L. Kilburn
    • 2
    • 3
  • Laura K. Reinert
    • 4
  • Jamie Voyles
    • 5
  • Daniel Medina
    • 3
  • Roberto Ibáñez
    • 3
    • 6
    • 7
  • Alex D. Hyatt
    • 8
  • Donna G. Boyle
    • 8
  • James D. Pask
    • 4
  • David M. Green
    • 2
  • Louise A. Rollins-Smith
    • 4
  1. 1.Institute of ZoologyUniversity of ZürichZürichSwitzerland
  2. 2.Department of Biology, Redpath MuseumMcGill UniversityMontrealCanada
  3. 3.Smithsonian Tropical Research InstitutePanamáRepublic of Panamá
  4. 4.Departments of Microbiology and Immunology and of PediatricsVanderbilt UniversityNashvilleUSA
  5. 5.School of Public Health, Tropical Biology and Rehabilitation Sciences, Amphibian Disease Ecology GroupJames Cook UniversityTownsvilleAustralia
  6. 6.Departamento de ZoologíaUniversidad de PanamáPanamáRepublic of Panamá
  7. 7.Círculo Herpetológico de PanamáPanamáRepublic of Panamá
  8. 8.Australian Animal Health LaboratoryCSIRO Livestock IndustriesGeelongAustralia

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