North-Western Journal of Zoology 2019, vol.15 (1) - Correspondence: Notes 113
ond location and Chris Raper for additional language correc- tions. This work was supported by Czech grant GA JU 152/2016/P provided by University of South Bohemia and
the Slovak Research and Development Agency under the
contract no. APVV-15-0147.
References Balanger, R.M., Corkum, L.D. (2009): Review of aquatic sex pheromones and
chemical communication in anurans. Journal of Herpetology 43: 184-191. Höble, G. (2005): Rana palustris (Pickerel Frog) and Ambystoma macualtum (Spoted Salamander). Reproductive behavior. Herpetology Review 36: 55-56. Mačát, Z., Jablonski, D. (2017): Pelobates fuscus (Laurenti, 1768) amplexing male Bufo bufo (Linnaeus, 1758). Herpetozoa 30(3/4):222-223. Marco, A., Lizana, M. (2002): The absence of species and sex recognition during mate search by male common toads, Bufo bufo. Ethology, Ecology and
Evolution 14: 1-8. Mollov, I., Popgeorgiev, G.S., Naumov B.Y., Tznakov, N.D., Stoyanov A.Y. (2010): Cases of abnormal amplexus in anurans (Amphibia: Anura) from Bulgaria and Greece. Biharean Biologist 4: 121-125. Oielska, M. (2017) Reproduction of Amphibians. CRC Press LLC., Boca Raton. Reading, C. (1984): Interspecific spawning between common frogs (Rana temporaria) and Common toads (Bufo bufo). Journal of Zoology 203: 95-101. Rojas, B. (2017): Behavioural, ecological, and evolutionary aspects of diversity
in frog colour patterns. Biological Reviews 92: 1059-1080. Simović, A., Anderson, N., Anđelković, M., Gvozdenović, S., Đorđević, S. (2014): Unusual amplexuses between anurans and caudates. Herpetology Notes 7: 25-29. Spareboom, M. (2014): Salamanders of the Old World. KNNV Publishers, Zeist. Strugariu, A., Gherghel, I. (2008): A preliminary report on the composition and distribution of the herpetofauna from the Lower Prut River Basin (Romania). Figure 1. Amplexus observed near the town of Bălan (A) North-Western Journal of Zoology 4 (Suppl. 1): S49-S69. and near the town of Azuga (B). Wells, K.D. (2007): The ecology and behavior of amphibians. The University of Chicago Press Ltd., London. specific females (Marco & Lizana 2002). This can result in Key words: Bombina variegata, Carpathians, Ichtyosaura alpestris, mating behaviour. unproductive forms of amplexus, as described in literature (e.g. Mollov et al. 2010; Simović et al. 2014, Mačát & Jablon- Article No.: e187503 ski 2017). Herein we report two cases of an interspecific am- Received: 15. August 2017 / Accepted: 02. April 2018 Available online: 19. April 2019 / Printed: June 2019 plexus between an adult male of Bombina variegata and an adult female of Ichtyosaura alpestris from Romania. On 16th August 2014 was first observed an amplexing Zdeněk MAČÁT1,2, Michal RINDOŠ3,4,*, male of B. variegata on a female I. alpestris near the town of David MIHALCA5 and Daniel JABLONSKI6 Bălan (N46.679°, E25.803°, 955 m a.s.l., the Inner Eastern Carpathians). The record was obtained near a small tempo- 1. Department of Ecology and Environmental Sciences, Faculty of Science, Palacký University, Šlechtitelů 27, 783 71, Olomouc, Czech Republic. rary flooded puddle. The couple stayed together and the Al- 2. Podyjí National Park Administration, Na Vyhlídce 5, Znojmo, pine newt did not even try to escape during whole process Czech Republic. of photographing and observation. The second observation 3. Biology Centre CAS, Institute of Entomology, Branišovská 31, CZ-37005 České Budějovice, Czech Republic. was made in a permanent pond near the town of Azuga 4. University of South Bohemia, Faculty of Science, Branišovská 31, CZ-37005 (N45.445°, E25.572°, 990 m a.s.l., The Southern Carpathians), České Budějovice, Czech Republic. on May 13, 2017. The observation lasted for 15 minutes 5. Corusu 145B, Cluj, Romania. 6. Department of Zoology, Comenius University in Bratislava, Mlynská dolina, without interruption. In the first case, the male frog held the Ilkovičova 6, 842 15 Bratislava, Slovakia. female newt by axillary amplexus, which is not a typical grip *Corresponding authors, M. Rindoš, E-mail: [email protected] for the family Bombinatoridae (Fig. 1-A). In the second case, the inguinal amplexing grip was used, as typical for the Yel- low-bellied toad (Fig. 1-B). Despite the fact that both species are well known mountain amphibians normally occurring in New upper altitudinal range of anteater same ponds even during the mating season, the potential for species in highlands of South America interspecific interferences seems to be small, as both species have widely different reproductive behaviour. Documented The Myrmecophagidae family has four anteater species, cases of a frog amplexing a newt or salamander are very rare which are insectivorous mammals restricted to the New and described in Höbel (2005) and Simovič et al. (2014). World: the pygmy anteater Cyclopes didactylus (Linnaeus, Nevertheless, the observation of an attempted mating be- 1758), the northern anteater Tamandua mexicana (Saussure, tween Bombina variegata and Ichtyosaura alpestris is another 1860), the giant anteater Myrmecophaga tridactyla Linnaeus, example of mating errors in the biology of amphibians. 1758 and the southern anteater Tamandua tetradactyla (Lin- Acknowledgments. The authors are grateful to Szabolcs naeus, 1758). Of these, the giant anteater and the southern Borbély for providing the photographic record from Bălan, anteater are widely distributed throughout South America, to Mihai Mihalca for providing information about the sec- with their core range in Brazil (Miranda et al. 2014a, b). The
114 North-Western Journal of Zoology 2019, vol.15 (1) - Correspondence: Notes
Table 1 New records of Myrmecophaga tridactyla (giant anteater) and Tamandua tetradactyla (south- ern anteater) in the highland ecosystems of four Protected areas in the Brazilian Atlantic forest (Serra do Papagaio State Park – SPSP, Itatiaia National Park – INP, Caparaó National Park – CNP and Serra dos Órgãos National Park – SONP).
Species Location Date Hour Altitude Geographical Position giant anteater SPSP 11/29/2012 14:10 2,149 m 22º03’14’’S;44º40’29’’W southern anteater CNP 12/26/2004 16:00 2,750 m 20°26’37”S; 41°48'42”W southern anteater SONP 07/15/2007 12:20 2,200 m 22°28’20”S; 43°03’17”W southern anteater SPSP 02/17/2009 13:30 2,206 m 22º03’36’’S; 44º40’34’’W southern anteater SPSP 12/11/2010 11:45 2,173 m 22º02’29’’S; 44º39’04’’W southern anteater SPSP 01/23/2014 15:15 2,065 m 22º17’34’’S; 44º44’17’’W southern anteater INP 11/08/2015 14:00 2,600 m 22°23’59”S; 44°40’10”W southern anteater INP 07/15/2016 12:30 2,500 m 22°23’07”S; 44°40’44”W
Figure 1. Map of the locations of the anteater records in the high-altitude grasslands of southeastern Brazil. Legend of states: RJ= Rio de Janeiro, ES= Espírito Santo, SP= São Paulo and MG = Minas Gerais.
giant anteater is the only species of anteater listed on the biology in these high altitude areas remain unknown. The IUCN Red List, being categorized as Vulnerable (Miranda et study of mammalian habitat use in highland areas can pro- al. 2014a). In Central America, it is considered to be extinct vide new and useful information on their ecology and habi- in several countries, while in other countries of South Amer- tat preferences (Aximoff 2015, Abreu et al. 2016, Aximoff & ica it is considered rare (Superina et al. 2010). In Brazil, the Vaz 2016, Aximoff & Rosa 2016, Ramos et al. 2018). giant anteater occurs at low population densities in some re- In this paper, we report records of Tamandua tetradactyla gions, where it is also considered to be rare (Superina et al. and Myrmecophaga tridactyla in high-altitude grasslands, and 2010), and it is threatened by deforestation, fragmentation, therefore extend the known upper limit of their altitudinal fire, road-kill, attacks from domestic animals and hunting distribution to more than 2,000 m, representing novel habitat (Miranda et al. 2015). use by both species in the Brazilian Atlantic Forest. The giant anteater and the southern anteater are known to occur in a wide variety of habitats, such as open fields, Our records were made between 2004 and 2016 in protected areas lo- grasslands, savannas, flooded forests, mangroves, tropical cated in the Serra da Mantiqueira Mountains (Serra do Papagaio State Park – SPSP, Itatiaia National Park – INP, Caparaó National moist forest, dry forest and dense forests (Miranda et al. Park – CNP) and in the Serra do Mar Mountains (Serra dos Órgãos 2014a, b). However, little is known about their altitudinal National Park – SONP) (Table 1, Fig. 1). These two mountain ranges distributions, with the highest occurrence records up to ca. are located in southeastern Brazil and are the largest and highest At- 1,600 m (Hayssen 2011, Aximoff et al. 2015, Passos et al. lantic Forest Mountains, considered irreplaceable for global biodi- 2016, Mazza et al. 2018). Many aspects of their ecology and versity conservation (Le Saout et al. 2013). North-Western Journal of Zoology 2019, vol.15 (1) - Correspondence: Notes 115
All records were made in the daylight and above the tree line (1,800-2,000 m) in high-altitude grasslands with a predominance of herbs, shrubs and small trees (up to 4 m in height) (Fig. 2a) that show a remarkable richness of plant species, including some endemic and endangered species (Aximoff 2011). This ecosystem is restricted to the top of the highest mountains of the Brazilian Atlantic Forest. The greatest threat to this ecosystem is the occurrence of man-made fires, which are most frequent during the winter, between June and Sep- tember (Aximoff 2011). The area has a mesothermal climate: a mean annual temperature is ~11.5°C and mean annual precipitation is ~2,150 mm, with precipitation concentrated in the rainy season, dur- ing spring and summer (September to March) and the winter being dry. During the winter, minimum temperatures were below zero for more than half of the days in 2016, and the lowest recorded tempera- ture was -11.8ºC (Wunderground 2016).
We recorded the presence of a single giant anteater at 2,149 m, which was observed walking in an area of high-altitude grassland in the SPSP. Startled by our presence, the individ- ual ran way into the vegetation, adjacent to a high-altitude swamp. Seven records were made of southern anteater in four protected areas, above 2,000 m. In the SONP, an individual was observed on a rock outcrop above 2,200 m (Fig. 2b), while in the CNP, we observed one individual on the high- altitude grasslands at 2,750 m (Fig. 2c). Three records oc- curred in the SPSP, where an individual was observed mov- ing between rocks at 2,206 m, another individual was ob- served climbing a small tree at an altitude of 2,173 m, and a third individual was observed walking along a trail on the edge of a forest to high-altitude grassland at 2,065 m. In all three cases, the animals walked away into the vegetation Figure 2. (a) High-altitude grasslands of Itatiaia National Park. (b) Southern anteater on rocky outcrops in Serra dos Órgãos National when they detected our presence. The last two records were Park. (c) Southern anteater moving across the high-altitude grass- made in the INP at 2,600 m, where an individual was ob- lands of Caparaó National Park. (d) Southern anteater feeding on served moving on rocks and another individual was ob- ants in Itatiaia National Park. (e) An anthill of Camponotus sp., served at an anthill at 2,500 m (Fig. 2d – 2e). When the latter commonly found in the high-altitude grasslands where the ant- individual detected our presence, it moved away into the eater records were made. vegetation less than 15 m away. In addition to representing an increase in the altitudinal extent of both species, their presence in high-altitude grass- grasslands as has been previously observed in the Cerrado lands reveals the use of a new habitat restricted to the cold- (Rosa CA, personal observation). est peaks of some of the highest mountains of the Atlantic Although studies of the effect of climate change on Forest. High availability of food, lower competition and mountain areas are scarce, species are expected to colonize shelter resources has been suggested as an explanation for previously unsuitable areas quickly (Chen et al. 2011). The new records of mammals at higher elevations in tropical metabolism and habitat use of anteaters in the high-altitude habitats (e.g. Aximoff 2015, Abreu et al. 2016, Andrade- grasslands of the Atlantic Forest, where temperatures de- Ponce & Angarita-Sierra 2017, Ramos et al. 2018). Anteaters crease below 10ºC in summer and become negative during spend much of their energy and time searching for social in- winter, need to be studied. Our records were all made in sects and have a specialized diet, feeding mainly on insects daylight, which could indicate that individuals of these spe- but also on fruits and seeds (Brown 2011, Cunha et al. 2014). cies are not active in these habitats at night, in order to pre- The high altitude grasslands of the INP appear to offer re- vent loss of body heat. However, it could also be a result of sources in abundance (Aximoff 2015, Abreu et al. 2016), and non-random sampling, with no directed effort made to find indeed we registered a southern anteater feeding on an ant- these species, but rather sporadic records being by observers hill of Camponotus sp. (Fig. 2e), which is the richest and most walking during the day. abundant ant genera in the area (Martins 2011). Another possible explanation for increased habitat use at Anteaters require arboreal habitats as shelter from heat higher altitudes by these species is the frequency of human or extreme cold where temperatures range outside of 15 to impacts on lowland forests, compared with relatively low 36°C (Camilo-Alves and Mourão 2006). As such, the indi- human pressure in these high altitude ecosystems (Cunha viduals that we recorded could be seeking shelter in the 2010, Aximoff 2015). Teasing apart these drivers will be key small remnants of high montane forest scattered in the high to understanding the importance of high altitude areas in altitude grasslands. Alternatively, they may descend to alti- ensuring the survival of species’ in the face of global warm- tudes where temperatures are more moderate (< 1,800 m), or ing and continued degradation of native environments at even seek shelter in cracks of the rocky areas or high-altitude lower altitudes. 116 North-Western Journal of Zoology 2019, vol.15 (1) - Correspondence: Notes
The record of the giant anteater is also the first for the (Pilosa, Myrmecophagidae) regarding the termite defense strategies. Serra do Papagaio State Park, meaning that the species has Bioscience Journal 31 :234-241. Hayssen, V. (2011): Tamandua tetradactyla (Pilosa: Myrmecophagidae). now been recorded in 10 protected areas of the Atlantic For- Mammalian Species 43(1): 64-74. est (see Passos et al. 2016). This is especially important since Le Saout, S., Hoffmann, M., Shi, Y., Hughes, A., Bernard, C., Brooks, T.M., the giant anteater is now considered almost extinct in the At- Bertzky, B., Butchart, S.H.M., Stuart, S.N., Badman, T., Rodrigues, A.S.L. (2013): Protected areas and effective biodiversity conservation. Science. 342: lantic Forest biome, especially in the Brazilian coastal plain 803-805. (Superina et al. 2010). The records reported here supplement Martins, L. (2011). Estrutura de comunidades de formigas (Hymenoptera: those recently reported by Passos et al. (2016) for the giant Formicidae) do planalto do Itatiaia, Rio de Janeiro, Brasil. Dissertação (mestrado) – Universidade Federal Rural do Rio de Janeiro, Programa de anteater, and extend the known altitudinal limit of the giant PósGraduação em Biologia Animal. <83p.https://tede.ufrrj.br/bitstream/ anteater by 800 m, and of the southern anteater by 1,250 m. jspui/1139/2/2011%20-%20Luciano%20Martins.pdf> They also supplement records for other mammals species, Mazza, I., da Rosa, C. A., de Souza, A. C., Aximoff, I., & Passamani, M. (2018). Mamíferos de médio e grande porte registrados em florestas dominadas por recently reported to be using areas at higher altitudes than Araucaria angustifolia na RPPN Alto-Montana, Serra da Mantiqueira. previously known (e.g. Aximoff 2015, Abreu et al. 2016, Axi- Oecologia Australis 22(1): 74–88. moff & Vaz 2016, Aximoff & Rosa 2016, Ramos et al. 2018). Miranda, F., Bertassoni, A., Abba, A.M. (2014a): Myrmecophaga tridactyla. The Taken together, these studies highlight the importance of the IUCN Red List of Threatened Species 2014: e.T14224A47441961. Accessed 12 December 2016. continuous Atlantic Forest and its highland areas in main- Miranda, F., Fallabrino, A., Arteaga, M., Tirira, D.G., Meritt, D.A., Superina, M. taining populations of mammal species in protected areas in (2014b): Tamandua tetradactyla. The IUCN Red List of Threatened Species southern Brazil. 2014: e.T21350A47442916. Accessed 12 December 2016 Miranda, F.R., Chiarello, A.G., Röhe, F., Braga, F.G., Mourão, G.M., Miranda, G.H.B. (2015): Avaliação do risco de extinção de Myrmecophaga tridactyla Acknowledgments. We thank the administration of the Itatiaia Linnaeus 1758 no Brasil.
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