Diet of Adinobates Bombetes

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Introduction

Poison frogs (Dendrobatidae) have receivedconsiderable attention in the scienti c community

because of their brilliantly colored aposematic patterns,the presence of alkaloids in the skin, and their complexreproductive behaviors (Biavati et al., 2004). Severalstudies have shown that a number of arthropod dietarysources explain the origin of alkaloids sequestered in the

skins of poison frogs (Saporito et al., 2004, 2007a, 2007b,2009; Smith and Jones, 2004). Particularly, dendrobatid

poison frogs have developed an over-expressed systemof alkaloid accumulation that facilitates the sequestrationof alkaloids directly from their diet, such as ants, mitesand millipedes (Daly, 1998, 2000; Saporito et al., 2004,2007a, 2007b, 2009; Takada et al., 2005; Savitzky et al.,2012).

Studies concerning diet and prey consumption areimportant in understanding the relationship betweendiet and alkaloid sequestration in poison frogs, aswell as competition with congenerics. The variation inalkaloid pro les in poison frogs is related to differencesin availability of dietary arthropods consumed among

populations of these frogs (Saporito et al., 2007a).Studies have found geographic variation in alkaloid

pro les related to diet in all species studied (Saporitoet al., 2006, 2007b; Mebs et al., 2008). Few studieshave explored diet patterns across the geographic rangeof a single poison frog species, and how these patternswould correspond to differences in dietary arthropodcommunities and subsequent alkaloid sequestration in

poison frogs.Herein we provide insights to the diet of A. bombetes

from three localities within its range. Andinobates

Herpetology Notes, volume 7: 559-564 (2014) (published online on 3 October 2014)

Geographic variation in the diet of the Cauca Poison Frog Andinobates bombetes

(Anura: Dendrobatidae)in the Andes of Colombia

Diego A. Gómez-Hoyos 1, Margarita M. López-García 2, Carlos A. Soto-Garzón 3, Diana M. Méndez-Rojas 4,Ted R. Kahn 5 and Julián A. Velasco 6,*

1 Wildlife Conservation Society, Colombia Program, Cali, Valledel Cauca, Colombia. E-mail: [email protected]

2 Grupo de Investigación Insectos de Colombia, Instituto deCiencias Naturales, Universidad Nacional de Colombia,Bogotá, Colombia.

3 Fundación Huella Verde, Armenia, Colombia.4 Red de Ecoetología, Instituto de Ecología A.C, Xalapa,

Veracruz, México.5 Integrated Taxonomic Information System, Data Development

contractor, Smithsonian Institution, National Museum of Natural History, Washington, D.C.

6 Laboratorio de Análisis Espaciales, Instituto de Biología,Universidad Nacional Autónoma de México. México. D.F.

*Corresponding author e-mail: [email protected]

Abstract . We describe the diet of Andinobates bombetes (Myers and Daly, 1980) based on stomach contents taken from sixty-nine individuals from three localities in the central northwestern Colombian Andes. 1471 individual prey items were found inthe stomach contents from 16 taxonomic groups: arthropods (14), crustaceans (1) and mollusks (1). Taxonomic groups of preywere identi ed to the lowest taxonomic rank possible. We used the Index of Relative Importance (IRI) and found that Formicidae(ants), and the subclass Acari (mites) dominated the prey taken in our samples. There was not a signi cant correlation betweensnout-vent length (SVL) and prey volume sampled. The dietary ant ratio was different between localities, whereas that of miteswas consistent across the three localities studied. These results indicate that A. bombetes is a dietary ant and mite specialist, similarto other dendrobatid frogs.

Keywords : Trophic ecology, Dendrobatidae, poison frog, ants, mites, diet



Diego A. Gómez-Hoyos et al.560

bombetes is a small-bodied frog and occurs in Centraland Western Andes of Colombia (Suárez-Mayorga,2004; Marín-Gómez and Gómez-Hoyos, 2011). Wequanti ed the diet of A. bombetes at three localities in

the Central and Western Andes of Colombia (Fig. 1),and then compared our ndings of local dietary itemsamong the three study localities.

Materials and Methods

We used visual encounter surveys (VES) (Heyeret al., 1994) during July and October 2009 to collect

A. bombetes individuals for gut content analyses.Sampling occurred at three sites in the Central andWestern Andes of Colombia: 1) La Samaritana farm(SF), Salento municipality, Quindío; secondary forest;1626 m (4°34’N, 75°38’W); 2) Cañón del Río Barbas(CRB), Filandia municipality, Quindío; mature forest;1998 m (4°42’N, 75°38’W); and 3) Reserva Forestal deYotoco (RFY), Yotoco municipality, Valle del Cauca;secondary forest; 1600 m (3°53’N, 76°38’W) (Fig. 1).

All frogs were captured by hand and standard snout-vent (SVL) in millimeters (mm) was measured, exceptfor RFY locality.

Stomach contents were sampled immediately after

capture (from 9:00 to 16:00 h) by stomach ushingusing a small blunt needle (Popper® 3.048 mm gauge).This procedure is effective to ush stomach contentswithout producing injury (Solé et al., 2005). Stomachcontents were preserved in 70% ethanol. We identi edeach prey item to the lowest taxonomic rank possible.We measured length and width in mm of each intact

prey item. These measurements were used to calculate prey volume using the spheroid volumetric equation asfollows:

V = 4/3 π * (length/2) * (width/2) 2

We quanti ed the number of each prey item in the dietusing the Index of Relative Importance (IRI) described

by Pinkas et al. (1971) with the following equation:

IRI t =[%O t * (%N t + %V t)]

Figure 1. Study area in the Central and Western Andes of Colombia. Solid circle: Cañón del Río Barbas; Square: La SamaritanaFarm; Triangle: Reserva Forestal de Yotoco.



Geographic variation in the diet of the Cauca Poison Frog in the Andes of Colombia 561

where %O t is the occurrence percentage (i.e. thenumber of stomachs containing each prey categoryde ned as t ), %N t is the percentage of the number of titems in all stomachs, and %V t is the percentage of the

volume of t items in all stomachs examined.We also calculated the trophic niche breadth using

Levins´ standardized formula (Hurlbert, 1978):

BA=[(1/ Σ p i2)-1]/ n-1

where p i is the proportion in volume of each preyitem with respect to the total volume of prey in eachlocation; n is the number of prey items in the diet of thefrogs. The index produces values ranging from zero to1; B A=1 means that all prey categories were consumed

in equal proportions and that selection of prey was notsigni cant, whereas a value near zero indicates thatone or few prey were consumed in large quantitiesindicating intentional prey selection (Valderrama-Vernaza et al., 2009). After testing for normality and

homogeneity of variances, we applied a Spearman rankcorrelation to examine the relationships between SVLand prey volume consumed in each locality. We testedfor differences in proportions of prey items between

localities using a Kruskal-Wallis test. All statisticalanalyses were conducted with Deducer package on Rlanguage v. 3.0.2 (R Core Team, 2013).

Results

A total of 69 stomach contents were analyzed fromlive A. bombetes : 18 from CRB (6 males, meanSVL=19.24±0.89; 6 females, mean SVL=18.67±1.51;6 immatures), 27 from FS (11 males, mean

SVL=17.44±0.83; 10 females, mean SVL=19.24±0.89;6 immatures) and 24 from RFY. We identi ed 16

prey taxa to the subphylum, class, subclass, order andfamily level (Table 1). We identi ed 1471 individual

prey items with a mean of 4.43 (±1.90) prey categories

Cañón Río Barbas Samaritana Farm Reserva Forestal Yotoco

Dietary SampleClassification N %F %V IRI N %F %V IRI N %F %V IRI

Arthropoda

Arachnida

Araneae 2 11.11 4.8 60.26 4 14.81 0.41 16.08 8 25 0.87 57.53

Acari 164 88.89 46.58 8695.89 283 88.89 13.55 5460.59 286 100 29.5 8057.11

Pseudoscorpionida 1 5.56 0.47 4.36 1 3.7 0.13 1.09 5 20.83 1.44 48.51

Insecta

Coleoptera(includes larvae) 12 38.89 9.38 510.7 23 44.44 6.49 461.38 30 66.67 12.48 1189.39

Collembola 18 33.33 8.84 482.08 12 22.22 0.17 48.89 61 50 3.87 738.13

Diptera(includes larvae) 12 50 3.84 379.44 17 40.74 0.69 145.37 42 62.5 4.51 750.87

Hemiptera 21 55.56 0.84 411.04 5 14.81 3.31 61.53 9 29.17 0.93 74.01

Hymenoptera(Formicidae) 82 77.78 19.71 3525.89 208 77.78 71.92 8331.29 84 58.33 41.5 3295.63

Hymenoptera(non Formicidae) 1 5.56 0.06 2.07 22 55.56 2.11 324.08 6 20.83 1.79 59.55

Orthoptera 1 5.56 1.95 12.55 0 0 0 0 0 0 0 0

Thysanoptera 3 16.67 0.54 24.55 12 33.33 0.45 82.85 17 33.33 1.55 152.98

Psocoptera 0 0 0 0 3 7.41 0.63 8.46 1 4.17 0.1 1.15

Diplura 0 0 0 0 0 0 0 0 1 4.17 0.16 1.42

Malacostraca

Isopoda 0 0 0 0 0 0 0 0 1 4.17 0.01 0.79

Myriapoda 0 0 0 0 0 0 0 0 6 20.83 0.96 42.42

Mollusca

Gasteropoda 3 11.11 3 43.8 1 3.7 0.14 1.14 3 4.17 0.32 3.58

Table 1. Diet of Andinobates bombetes from three localities in the Central and Western Andes of Colombia. N: number of prey;%F: percentage of frequency of each prey item; %V: percentage of volume of prey; IRI: Index of Relative Importance.



and 21.45 (±18.08) prey items per individual frog.Formicidae and Acari had the highest IRI scores (Table1). Only Acari and Formicidae were consumed in a

higher proportion than other prey categories. Pheidole were consumed most commonly (79.03% of total ants)and other ant genera were rarely found ( Solenopsis ,Carebara, Cyphomyrmex , Strumygenis , Crematogaster ,Octostruma , Linepithema , Discothyrea , Pyramica ,

Brachymyrmex ). For example, the formicine genus Brachymyrmex was represented by only a single record(0.26% of total ants). Niche breadth was close to zero(CRB=0.1774; FS=0.1631; RFY=0.1624).

We found no signi cant correlation between poisonfrog SVL and prey volume (R=0.10, p > 0.05) inthe individuals we examined. We found signi cantdifferences in the dietary percentage of ants consumed

between localities (Kruskal-Wallis Chi 2 = 6.8, df = 2, p = 0.03), with a higher proportion of ants consumedat FS than at RFY (Fig. 2, A). The percentage of mitesconsumed for poison frogs did not vary among sites(Kruskal-Wallis Chi 2 = 1.72, df = 2, p = 0.42; Fig. 2,B).

Discussion

The diet of Andinobates bombetes is primarilycomposed of ants and mites, which occur at a higher

percentage than other prey items at our study sites. Thisresult is well-supported by our very small niche breadth

values. Our data suggest that A. bombetes is a dietary antand mite specialist as many other dendrobatid speciesfrom several genera (e.g., Ameerega , Andinobates ;

Kahn et al., 2014 in press). Ants and mites are anabundant prey resource in Neotropical the leaf litterhabitat where dendrobatid frogs live (Daly et al., 1999:Hölldober and Wilson, 1990; Franklin et al., 2006).

Andinobates bombetes usually is found in microhabitats(e.g., bromeliads, leaf litter, soil substrate) (Myers andDaly, 1980) where many of the prey items were found.Variation in ant and mite consumed by A. bombetes across the study sites is consistent with ndings inother dendrobatid frog species (Valderrama-Vernaza et

al., 2009; Lieberman, 1986; Daly, 1998; Biavati et al.,2004; Darst et al., 2005; Saporito et al., 2004, 2007a,2009; Forti et al., 2011).

Ants and mites are primary sources of dietary alkaloidsin a number of poison frog species (Daly et al., 1999:Hölldober and Wilson, 1990; Franklin et al., 2006).Variation in alkaloid pro les of A. bombetes has beenobserved over broad geographic areas (Myers and Daly,1980) and can be attributed to differences in the kinds ofarthropods, and their respective alkaloids, consumed bythe frogs. A previous study of A. bombetes conducted attwo sites in Colombia, revealed a total of 22 piperidinealkaloids sequestered in the skins of these poison frogs;little variation occurred in the 15 and 17 compoundsevaluated from the two localities (Myers and Daly,1980). Since the time of that study, the link between diet

Figure 2. Proportion of ants (A) and mites (B) consumed by Andinobates bombetes in three localities in the Central and WesternAndes of Colombian Andes (CRB: Cañon Río Barbas; FS: Finca La Samaritana; RFY: Reserva Forestal Yotoco). Solid circle:mean; error bars: 95% con dence interval.




and alkaloid sequestration has been demonstrated (Dalyet al., 1999; Saporito et al., 2011). However, with theaim to elucidate the relationship between toxicity anddiet in dendrobatid poison frogs further studies will be

necessary to characterize the alkaloid pro les of thevaried prey consumed by A. bombetes, principally antsand mites.

Acknowledgments. This study was funded by an internship grantfrom the Wildlife Conservation Society for Colombia Program(ONE WCS grant). The authors are grateful to Jennifer Pramuk(Woodland Park Zoo), Catalina Silva (Cali Zoo), and BeatrizVelásquez (Cali Zoo) for their support during our eldwork.A special thanks to Carlos Jaramillo (Director of the ReservaForestal de Yocoto) for logistic support during our eldwork.

We are grateful for the insightful and encouraging review of ourmanuscript by Anna J. Phillips (Dept. of Invertebrate Zoology,

NMNH), Mason Ryan (University of New Mexico), and ananonymous reviewer. This work was also made possible by agraduate scholarship from the Consejo Nacional de Ciencia yTecnología (Conacyt) to JAV and a scholarship from the U.S.Fish and Wildlife Service to DAG-H.

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Geographic variation in the diet of the Cauca Poison Frog in the Andes of Colombia 563



Accepted by Diogo Provete; Managing Editor: Diogo Provete

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