Two mistletoes are too many?: Interspecific occurrence of mistletoes on the same host tree

SHORT COMMUNICATION

Two mistletoes are too many? Interspecific occurrence of mistletoes on the same host tree

Rafael Arruda^I,*; Caroline Lunardelli^II; Clóvis Kitagawa^II, Claudenir Simões Caires^III; Grazielle Sales Teodoro^IV; Fabiana Alves Mourão^V

^IUniversidade Federal de Mato Grosso, Instituto de Ciências Naturais, Humanas e Sociais, Sinop, MT, Brazil

^IIUniversidade Federal de Mato Grosso, Instituto de Ciências Agrárias e Ambientais, Sinop, MT, Brazil

^IIIUniversidade de Brasília, Instituto de Ciências Biológicas, Departamento de Botânica, Brasilia, DF, Brazil

^IVUniversidade Estadual de Campinas, Instituto de Biologia, Departamento de Botânica, Campinas, SP, Brazil

^VUniversidade Federal de Minas Gerais, Instituto de Ciências Biológicas, Departamento de Biologia Geral, Belo Horizonte, MG, Brazil

ABSTRACT

Mistletoe can have a major impact on the fitness of the host plant. If there is more than one species of mistletoe on the same host tree, the overall impact might be amplified. We report the occurrence of more than one species of mistletoe on the same host tree. Although it is not a rule in the field, to our knowledge, there have been no studies of this topic. In most cases, two species of mistletoe were recorded on the same host tree, although we recorded three species of mistletoe on one occasion. This demonstrates that different species of mistletoe can be compatible with the same host species. Therefore, compatibility (structural and physiological) might be an important factor for the occurrence of mistletoe. Recent studies have shown that if the mistletoe does not "recognize" the host species, the deposited seeds will germinate but the haustorium will not penetrate the host branch. This is probably the primary mechanism in the establishment of more than one species of mistletoe on the same host, which can trigger a cascade of harmful effects for the host species.

Key words: parasite-host relationship, compatibility, specificity, parasitic plants, Red Queen hypothesis

The first step toward improving our understanding of mistletoe-host interactions is to determine the pattern of host specificity on various spatial scales (Norton & Carpenter 1998; Blick & Burns 2009, Arruda et al. 2012). Empirical data show that some species of mistletoe that locally specialize on certain host species (e.g., Psittacanthus plagiophyllus on Anacardium occidentale L.; Fadini 2011) are generalists on a regional scale (Caires & Proença 2008). Therefore, changes in mistletoe demographics can be expected on the basis of host compatibility, which ultimately affects the spatial pattern of specificity. In addition, the host ranges of many sympatric species of mistletoe can overlap in a given area, and, ultimately, the same host individual can support more than one species of mistletoe.

Here, we present our observations regarding the occurrence of more than one species of mistletoe on individual host trees of various species in the Brazilian savanna (cerrado). Although this is not the norm in the field, there is a lack of data on this subject in the literature and our knowledge of the particularities of mistletoe-host interactions is therefore limited. Mistletoe can have a major impact on the development of host plants (Press & Phoenix 2005, Arruda et al. 2009; Mourão et al. 2009, Arruda et al. 2012). Because mistletoe draws nutrition from its host-either by intercepting the xylem, as is the case for Struthanthus spp. (Arruda et al. 2006; Mourão et al. 2006) and Psittacanthus spp. (Fadini et al. 2009; Teodoro et al. 2010), or by intercepting the phloem, as in the case of Tristerix spp. (Martínez del Rio et al. 1995; Medel et al. 2002)-it can have harmful effects on the host, sometimes even causing the death of the parasitized individual.

Through observations at various sites in the Brazilian cerrado, we recorded occurrences of two or more species of mistletoe on the same host individual. The host species and the hemiparasites found on it were recorded, as were the geographic coordinates of the sampled location. Although mistletoe occurs in all regions of Brazil, collection efforts are primarily concentrated in the cerrado. This can be explained by the ease in sampling material in the cerrado when compared with forest habitats like the Amazon, due to the lower canopy in the cerrado, which facilitates the detection of mistletoe. The pertinent mistletoe and host species identified in our study are shown in Tab. 1.

We registered an occurrence of two species of mistletoe on the same host individual in the Salto Magessi Environmentally Protected Area (13º34'39.30"S; 55º15'57.73"W), located in the community of Boa Esperança, 200 km from the city of Sinop, in the state of Mato Grosso, where we found Psittacanthus acinarius and Phoradendron mucronatum on the same branch of the host species Aspidosperma sp.1 (Tab. 1 and Fig. 1A). We also recorded mistletoe individuals in the ironstone outcrops area of the Serra do Rola Moça State Park, located 35 km from the city of Belo Horizonte (20º03'60"S; 44º02'00"W), in the northwestern portion of the Iron Quadrangle, in the state of Minas Gerais. We found Tripodanthus acutifolius and Struthanthus flexicaulis simultaneously on the host Mimosa calodendron (Tab. 1). We made another record at the edge of a forest fragment of tropical semideciduous forest near the city of Lavras (ca. 21º14'43''S; 44º59'59''W), in the state of Minas Gerais. In this record, two Phoradendron species (P. perrottetii and Phoradendron sp.) were found on the host Tapirira obtusa (Tab. 1).

We recorded six occurrences of multiple mistletoe species on the same host in the Federal District of Brasília:

Passovia ovata and Dendrophthora warmingii on the host species Vochysia pyramidalis (ca. 15º31'09"S; 48º01'08"W)

Phoradendron mucronatum and Passovia ovata on the host species Aspidosperma subincanum (ca. 15º33'05"S; 48º11'07"W)

Phoradendron mucronatum and Passovia stelis on the host species Aspidosperma subincanum (ca. 15º33'05"S; 48º11'07"W)

Phoradendron tunaeforme and Phoradendron andersonii on the host species Myrcia tomentosa (ca. 15º56'08"S; 47º58'09"W)

Phoradendron apiciflorum and Phoradendron mucronatum on the host species Senegalia polyphylla (ca. 15º31'09"S; 48º06'07"W)

Phoradendron crassifolium,Dendrophthora warmingii and Phoradendron strongyloclados on the host species Miconia ferruginata (ca. 15º30'07"S; 48º10'08"W)

We registered three occurrences in the state of Mato Grosso do Sul:

Psittacanthus acinarius and Phoradendron affine on the host species Guazuma ulmifolia (ca. 20º13'57"S, 56º28'59"W)

Psittacanthus cordatus and Phoradendron bathyoryctum on the host species Anadenanthera sp.1 (ca. 20º14'25"S; 56º23'39"W)

Psittacanthus cordatus and Psittacanthus acinarius on an unidentified species of the family Malpighiaceae (ca. 20º14'51"S; 56º22'56"W)

In the state of Mato Grosso, we recorded the joint occurrence of Oryctanthus florulentus and Passovia pyrifolia on the host species Citrus sp.1 (ca. 09º14'02"S; 56º59'24"W). In the community of Cáceres, also in the state of Mato Grosso, Psittacanthus acinarius and Struthanthus sp. were recorded on the host Triplaris sp. (Fig. 1B), although the geographic coordinates of the location were not recorded.

To our knowledge, this is the first study to present records of multiple species of mistletoe on the same host individual. Most of the cases involved the simultaneous occurrence of two species of mistletoe, although three species of mistletoe were involved on one occasion. The activity of these hemiparasites can have harmful effects on the host, including changes to the anatomy, physiology and behavior of the host, as well as altering their role in the community (Press & Phoenix 2005; Wood et al. 2007; Arruda et al. 2009; Mourão et al. 2009; Cuevas-Reyes et al. 2011; Milanello do Amaral & Ceccantini 2011; Arruda et al. 2012). Recent results show that mistletoe can affect the reproductive success of its host, because parasitized individuals produce less fruit and present reduced seed weight (Mourão et al. 2009). In addition to the physiological effects, significant host mortality has been observed (Mourão et al. 2009; Teodoro 2010). Mistletoe drains water from its host, the former having high rates of transpiration, which might be related to the increased availability of nutrients, provided by the host (Glatzel & Geils 2009). At lower mistletoe densities, it is unlikely that mortality will occur, because there is no competition for water and nutrients between the mistletoe and the host. However, a higher density of a given species of mistletoe, or even increased density due to the occurrence of more than one mistletoe species, can be expected to diminish the fitness of the host individual, which may be reflected in both the competitive and reproductive ability of the hosts.

In parasite-host relationships, the Red Queen hypothesis proposes that parasites affect certain genotypes of the hosts and, because the hosts can make rapid evolutionary adjustments, sexual reproduction in hosts would guarantee that future generations become resistant to parasites (Van Valen 1973). If the presence of only one species of mistletoe can cause deleterious effects in various biological attributes of hosts, the synergistic effects of two or more species can increase the scale of negative impacts on the host. Therefore, multiple species of mistletoe could break the co-evolutionary cycle predicted by the Red Queen hypothesis and, in the long term, increase the mortality of the host species or add a new host in the range of potential hosts of a particular species of mistletoe. However, compared with traditional parasite-host relationships, the mistletoe-host interaction does not yet have any clear general patterns in Brazil, where the collection effort for this group is still incipient (Arruda et al. 2009; Arruda et al. 2012; Fadini, Caires & Arruda, unpublished data).

The occurrence of mistletoe species can be determined by their compatibility with their hosts. If any one species of host is compatible with more than one species of mistletoe, the tendency would be to increase the density at the local level (individual host) and at the regional level (host species). Our results show that various host species support more than one species of mistletoe, suggesting that, if we increase the sampling effort, we will find more examples of multiple mistletoe species sharing a host tree (Arruda & Carvalho 2004; Arruda et al. 2006; Mourão et al. 2006; Caires & Proença 2008; Fadini 2011; Arruda et al. 2012). Consequently, compatibility (structural and physiological) is perhaps an important factor for the occurrence of multiple mistletoe species on a single host. This is probably the primary mechanism that favors the establishment of more than one species of mistletoe and also determines the degree of specificity, which can trigger a cascade of harmful effects for the host species, such as reduced reproductive fitness and increased mortality.

Acknowledgments

We would like to thank the two anonymous referees who reviewed the manuscript and whose suggestions led to extensive improvements. We would also like to thank the Brazilian Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio, Chico Mendes Institute for the Conservation of Biodiversity) for providing the necessary research permits, as well as the Federal University of Mato Grosso, Federal University of Minas Gerais, Federal University of Lavras and University of Brasília for the logistical and financial support provided. This study received additional financial support in the form of grants from the following Brazilian agencies: the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Office for the Advancement of Higher Education; Graduate Fellowship Grant to CSC); the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, National Council for Scientific and Technological Development; Graduate Fellowship Grants to CSC, FAM and GST; and Postdoctoral Fellowship Grant no. 35.0201/2009-9 to RA); and the Fundação de Amparo à Pesquisa do Estado de Mato Grosso (FAPEMAT, Mato Grosso State Foundation for the Support of Research; Grant no. 40810/2009 to RA). This is Núcleo de Estudos da Biodiversidade da Amazônia Mato-Grossense (NEBAM, Center for the Study of Biodiversity in the Mato Grosso Amazon Region of the state of Mato Grosso) publication 24 and publication 06 in the Parasitic Plants Research Group technical series.

Submitted: 27 March, 2012.

Accepted: 30 October, 2012

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Publication Dates

• Publication in this collection
  08 May 2013
• Date of issue
  Mar 2013

History

• Received
  27 Mar 2012
• Accepted
  30 Oct 2012