EcoHealth DOI: 10.1007/s10393-013-0886-7
Ó 2013 International Association for Ecology and Health
Original Contribution
Aquatic Macroinvertebrate Assemblages of Ghana, West Africa: Understanding the Ecology of a Neglected Tropical Disease M. Eric Benbow,1 Ryan Kimbirauskas,1 Mollie D. McIntosh,2 Heather Williamson,3 Charles Quaye,4 Daniel Boakye,4 Pamela L.C. Small,3 and Richard W. Merritt1 1
Department Department 3 Department 4 Department 2
of of of of
Entomology, Michigan State University, East Lansing, MI 48824 Biology, Xavier University, Cincinnati, OH 45207 Microbiology, University of Tennessee, Knoxville, TN 37996 Parasitology, Noguchi Memorial Institute of Medical Research, Legon, Ghana
Abstract: Buruli ulcer (BU) is an emerging, but neglected tropical disease, where there has been a reported association with disturbed aquatic habitats and proposed aquatic macroinvertebrate vectors such as biting Hemiptera. An initial step in understanding the potential role of macroinvertebrates in the ecology of BU is to better understand the entire community, not just one or two taxa, in relation to the pathogen, Mycobacterium ulcerans, at a large spatial scale. For the first time at a country-wide scale this research documents that M. ulcerans was frequently detected from environmental samples taken from BU endemic regions, but was not present in 30 waterbodies of a non-endemic region. There were significant differences in macroinvertebrate community structure and identified potential indicator taxa in relation to pathogen presence. These results suggest that specific macroinvertebrate taxa or functional metrics may potentially be used as aquatic biological indicators of M. ulcerans. Developing ecological indicators of this pathogen is a first step for understanding the disease ecology of BU and should assist future studies of transmission. Keywords: Mycobacterium ulcerans, Buruli ulcer, wetlands, aquatic macroinvertebrates, disease ecology, Africa
INTRODUCTION Buruli ulcer (BU) is an emerging skin disease caused by an infection of Mycobacterium ulcerans (WHO 2000). Symptoms of the disease are the result of cell necrosis, which may lead to severe ulcerations, disfigurement, and disability in humans (Amofah et al. 1993; Asiedu and Etuaful 1998).
Correspondence to: M. Eric Benbow, e-mail: [email protected]
While BU disease has been reported from temperate regions of Australia (Johnson et al. 2007), the disease is most prevalent in tropical and subtropical climates, with the highest number of new cases being reported from subSaharan West Africa (Merritt et al. 2005; WHO 2008). It is widely accepted that BU is associated with exposure and proximity to freshwater habitats (Barker and Carswell 1973; Portaels et al. 1999; Merritt et al. 2010), yet many questions regarding the ecology of M. ulcerans remain unanswered, including the natural reservoir(s), environmental distribu-
M. Eric Benbow et al.
tion, and transmission of M. ulcerans to humans (Merritt et al. 2010). Merritt et al. (2010) provided a thorough review of published work on the transmission pathways and ecology of BU. Aquatic macroinvertebrates have received a good deal of attention as potential reservoirs and biological vectors of M. ulcerans. Portaels et al. (1999) first suggested that the pathogen may be moved through the aquatic community between trophic levels and feeding groups, and recently Wallace et al. (2010) demonstrated that this was possible in the lab using mosquitoes and biting water bugs (Hemiptera). Merritt et al. (2005) expanded on the Portaels et al. (1999) insect transmission idea with a further developed conceptual framework and provided several hypotheses of M. ulcerans transmission associated with aquatic macroinvertebrate communities: (1) water quality influences biological communities in ways leading to increased growth and proliferation of M. ulcerans; (2) invertebrates and fish concentrate M. ulcerans through feeding, becoming environmental reservoirs; and (3) biting aquatic insects colonized by M. ulcerans may act as transmission vectors to humans. They also reviewed two alternative hypotheses: (1) direct colonization of open lesions by M. ulcerans from the aquatic habitat and (2) aerosol infection from M. ulcerans in water that had been proposed by Hayman (1991). Most recently, the potential for mosquitoes as vectors associated with possum reservoirs has been supported by descriptive studies from Southeast Australia (Johnson et al. 2007; Johnson and Lavender 2009; Fyfe et al. 2010; Lavender et al. 2011). Additionally, the isolation and successful culturing of M. ulcerans from a water strider (Gerris sp. Fabricius) in Benin, West Africa (Portaels et al. 2008) and laboratory experiments demonstrating water bugs (Naucoris sp. Geoffroy) could transmit M. ulcerans to a mammal model have supported the role of aquatic insects in transmission (Marsollier et al. 2002). While these laboratory findings demonstrate a direct association of individual macroinvertebrate species and BU disease, entire aquatic macroinvertebrate communities offer better potential to understand the ecology of this disease through indirect associations with M. ulcerans in the environment. This connection is especially relevant to understanding BU considering that Benbow et al. (2008) and Williamson et al. (2008) reported M. ulcerans associations with multiple aquatic macroinvertebrate taxa from African waterbodies. Recently there have been excellent studies on M. ulcerans and certain aquatic insect species in Africa but these have been limited in spatial extent, defined here as
Ó 2013 International Association for Ecology and Health
Original Contribution
Aquatic Macroinvertebrate Assemblages of Ghana, West Africa: Understanding the Ecology of a Neglected Tropical Disease M. Eric Benbow,1 Ryan Kimbirauskas,1 Mollie D. McIntosh,2 Heather Williamson,3 Charles Quaye,4 Daniel Boakye,4 Pamela L.C. Small,3 and Richard W. Merritt1 1
Department Department 3 Department 4 Department 2
of of of of
Entomology, Michigan State University, East Lansing, MI 48824 Biology, Xavier University, Cincinnati, OH 45207 Microbiology, University of Tennessee, Knoxville, TN 37996 Parasitology, Noguchi Memorial Institute of Medical Research, Legon, Ghana
Abstract: Buruli ulcer (BU) is an emerging, but neglected tropical disease, where there has been a reported association with disturbed aquatic habitats and proposed aquatic macroinvertebrate vectors such as biting Hemiptera. An initial step in understanding the potential role of macroinvertebrates in the ecology of BU is to better understand the entire community, not just one or two taxa, in relation to the pathogen, Mycobacterium ulcerans, at a large spatial scale. For the first time at a country-wide scale this research documents that M. ulcerans was frequently detected from environmental samples taken from BU endemic regions, but was not present in 30 waterbodies of a non-endemic region. There were significant differences in macroinvertebrate community structure and identified potential indicator taxa in relation to pathogen presence. These results suggest that specific macroinvertebrate taxa or functional metrics may potentially be used as aquatic biological indicators of M. ulcerans. Developing ecological indicators of this pathogen is a first step for understanding the disease ecology of BU and should assist future studies of transmission. Keywords: Mycobacterium ulcerans, Buruli ulcer, wetlands, aquatic macroinvertebrates, disease ecology, Africa
INTRODUCTION Buruli ulcer (BU) is an emerging skin disease caused by an infection of Mycobacterium ulcerans (WHO 2000). Symptoms of the disease are the result of cell necrosis, which may lead to severe ulcerations, disfigurement, and disability in humans (Amofah et al. 1993; Asiedu and Etuaful 1998).
Correspondence to: M. Eric Benbow, e-mail: [email protected]
While BU disease has been reported from temperate regions of Australia (Johnson et al. 2007), the disease is most prevalent in tropical and subtropical climates, with the highest number of new cases being reported from subSaharan West Africa (Merritt et al. 2005; WHO 2008). It is widely accepted that BU is associated with exposure and proximity to freshwater habitats (Barker and Carswell 1973; Portaels et al. 1999; Merritt et al. 2010), yet many questions regarding the ecology of M. ulcerans remain unanswered, including the natural reservoir(s), environmental distribu-
M. Eric Benbow et al.
tion, and transmission of M. ulcerans to humans (Merritt et al. 2010). Merritt et al. (2010) provided a thorough review of published work on the transmission pathways and ecology of BU. Aquatic macroinvertebrates have received a good deal of attention as potential reservoirs and biological vectors of M. ulcerans. Portaels et al. (1999) first suggested that the pathogen may be moved through the aquatic community between trophic levels and feeding groups, and recently Wallace et al. (2010) demonstrated that this was possible in the lab using mosquitoes and biting water bugs (Hemiptera). Merritt et al. (2005) expanded on the Portaels et al. (1999) insect transmission idea with a further developed conceptual framework and provided several hypotheses of M. ulcerans transmission associated with aquatic macroinvertebrate communities: (1) water quality influences biological communities in ways leading to increased growth and proliferation of M. ulcerans; (2) invertebrates and fish concentrate M. ulcerans through feeding, becoming environmental reservoirs; and (3) biting aquatic insects colonized by M. ulcerans may act as transmission vectors to humans. They also reviewed two alternative hypotheses: (1) direct colonization of open lesions by M. ulcerans from the aquatic habitat and (2) aerosol infection from M. ulcerans in water that had been proposed by Hayman (1991). Most recently, the potential for mosquitoes as vectors associated with possum reservoirs has been supported by descriptive studies from Southeast Australia (Johnson et al. 2007; Johnson and Lavender 2009; Fyfe et al. 2010; Lavender et al. 2011). Additionally, the isolation and successful culturing of M. ulcerans from a water strider (Gerris sp. Fabricius) in Benin, West Africa (Portaels et al. 2008) and laboratory experiments demonstrating water bugs (Naucoris sp. Geoffroy) could transmit M. ulcerans to a mammal model have supported the role of aquatic insects in transmission (Marsollier et al. 2002). While these laboratory findings demonstrate a direct association of individual macroinvertebrate species and BU disease, entire aquatic macroinvertebrate communities offer better potential to understand the ecology of this disease through indirect associations with M. ulcerans in the environment. This connection is especially relevant to understanding BU considering that Benbow et al. (2008) and Williamson et al. (2008) reported M. ulcerans associations with multiple aquatic macroinvertebrate taxa from African waterbodies. Recently there have been excellent studies on M. ulcerans and certain aquatic insect species in Africa but these have been limited in spatial extent, defined here as
