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Feeding Ecomorphologies in the Fish Genus Herichthys (Perciformes: Cichlidae) Based on Stomach Content and Lower Pharyngeal Jaw Shape

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Feeding Ecomorphologies in the Fish Genus Herichthys (Perciformes: Cichlidae) Based on Stomach Content and Lower Pharyngeal Jaw Shape Feeding ecomorphologies in the fish genus Herichthys (Perciformes: Cichlidae) based on stomach content and lower pharyngeal jaw shape Fabian Pérez-Miranda1, Omar Mejía1*, Gerardo Zúñiga1, Eduardo Soto-Galera1 & Oldřich Říčan2 1. Departamento de Zoología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Ciudad de México, México; [email protected], [email protected], [email protected], [email protected] 2. Department of Zoology, Faculty of Science, University of South Bohemia, České Budějovice, Czech Republic; [email protected] * Correspondence Received 08-X-2018. Corrected 01-V-2019. Accepted 20-V-2019. Abstract: Speciation is a multifactorial process with factors acting at different scales of space and time. Trophic niche segregation has promoted the diversification of cichlids fishes in lentic (lacustrine) environments, whether this is also the case in lotic (riverine) systems remains unknown. Herichthys is the genus of cichlids with the most boreal distribution in the Americas comprising 12 currently recognized species, most micro-endemic and only two with a wide distribution. In the present work, we analyzed the stomach content and lower pharyngeal jaw morphologies of the species of the genus to evaluate the possible role of feeding ecology in the diversifica- tion of the group. Trophic strategies varied widely, including omnivores, piscivores, invertivores, molluskivores, detritivores, herbivores and algivores. Low values of Pianka’s index of niche overlap were found in the sym- patric micro-endemic species, while in the widely distributed species the indices ranged from low to very high. The analysis of lower pharyngeal jaw morphologies allowed discriminating a shape associated with piscivorous species from other foraging groups. The results of this study suggest that trophic niche segregation is a factor that could promotes diversification within the genus Herichthys although additional studies need to be performed to fully understand the speciation process in this group of Neotropical cichlid fishes. Key words: diversification; trophic niche; segregation; geometric morphometrics; sympatric species. Pérez-Miranda, F., Mejía, O., Zúñiga, G., Soto-Galera, E., & Říčan, O. (2019). Feeding ecomorphologies in the fish genus Herichthys (Perciformes: Cichlidae) based on stomach content and lower pharyngeal jaw shape. Revista de Biología Tropical, 67(3), 643-653. Feeding ecology is considered a putative (Horstkotte & Strecker, 2005; Joyce et al., driver underlying the diversification of cichlid 2005; Barluenga, Stölting, Salzburger, Mus- fishes in lacustrine environments (Winemiller, chick, & Meyer, 2006). In this way, variation in 1990; Winemiller, Kelso-Winemiller, & Bren- diet can lead to specialization among individu- kert, 1995; Galis & Metz, 1998; Burres et al., als of the same community through the differ- 2013; Burres, 2015). Multiple habitats found in ential use of resources, which in the long term freshwater environments (e.g. pelagic, benthic, can lead to the development of specialized mor- litoral, ...) promote ecological segregation and phologies to exploit a given resource (McKaye sympatric speciation within distribution of the & Marsh, 1983; Liem, 1991; Burres, 2015). range of a species as well as dietary differ- It has been documented that in cichlids, body ences (piscivory, insectivory, detritivory, …) and head shapes are determined by foraging Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 67(3): 643-653, June 2019 643 strategies (Burress 2015, 2016). Thus, head Ciénegas, between the coordinates range shape is closely related with feeding apparatus (20°3’50” - 29°30’8.6” N & 96°52’48” - which in this group of fishes widely differ in 101°19’56” W) (for further details see appen- structure and dentition. Particularly, oral jaws dix 1 or figure 1 in Pérez-Miranda et al. (2018). are likely a structure driving the diversification and radiation in this group (Salzburger, 2009). Stomach content: A total of 367 individu- Besides, in cichlid fishes, the last branchial als from 11 species were analyzed: H. bartoni arch is modified into a second pair of jaws, a (Bean, 1892) (n = 10), H. labridens (Pellegrin, very plastic structure that evolved in response 1903) (n = 10), H. pame (De la Maza-Benignos to foraging function in closely related species & Lozano-Vilano, 2013) (n = 18), H. stein- (Liem, 1973; Burres et al., 2013). Hence, for- dachneri (Jordan & Snyder, 1899) (n = 12), H. aging preferences in cichlids have acted as a pantostictus (Taylor & Miller, 1983) (n = 126), factor promoting changes in head morphology, H. deppii (Heckel, 1840) (n = 20), H. tepehua particularly in oral and pharyngeal jaws as well (De la Maza-Benignos, Ornelas-García, Loza- as in speciation (Fan, Elmer, & Meyer, 2012; no-Vilano, García-Ramírez, & Doadrio, 2015) Tsuboi, Gonzalez-Voyer, & Kolm, 2014). (n = 20), H. tamasopoensis Artigas-Azas, 1993 Herichthys is the most boreal genus among (n = 17), H. cyanoguttatus Baird & Girard, the Neotropical cichlids (Kullander, 2003) with 1854 (n = 10), H. carpintis (Jordan & Snyder, relatively high number of species and with a 1899) (n = 104) and H. minckleyi (Kornfield & high proportion of the various ecomorpholo- Taylor, 1983) (n = 20). For the two widespread gies found among Middle American cichlids species H. pantostictus and H. carpintis a much (Říčan, Pialek, Dragova, & Novak, 2016; larger sample covering their large distribution Peréz-Miranda et al., 2018). Still, there are few areas was analyzed. In the case of H. mol- studies that deal directly with feeding habits ango (De la Maza-Benignos & Lozano-Vilano, in the genus. A few exceptions are: 1) studies 2013), data were taken from Díaz-Pardo & performed on H. minckleyi concluding that Guerra-Magaña (1994). Stomach contents of the species is polymorphic and show different H. pantostictus and H. carpintis were evaluated foraging strategies (Swanson, Gibb, Marks, & for each single locality due to these two species Hendrickson, 2003, Trapani, 2003) and 2) and being widely distributed, while, the other spe- evaluation of the diet through the ontogeny of cies are micro-endemic. The first third of gut’s H. molango (Díaz-Pardo & Guerra-Magaña anterior portion was removed from each indi- 1994). For the rest of the species of the genus, vidual and its content was mixed into a single there are inferences of dietary strategy based sample for each species or locality. Food items on cranial and lower pharyngeal jaw morpholo- were identified to the lower taxonomic level gies (López-Fernández, Arbour, Winemiller, & and the proportion of each one in the pooled Honeycutt, 2013; Říčan et al., 2016) but direct sample was estimated through a volumetric stomach-content analyses are missing. In the method (Hyslop, 1980). To assess trophic over- present work we describe the stomach content lapping, Pianka index of niche overlap (pi) was of the species of the genus Herichthys, analyze used (Pianka, 1974). This is a symmetric index the lower pharyngeal jaw shapes using geomet- that ranges from zero for no niche overlap to ric morphometrics and compare the diet among one for complete niche overlap. Niche overlap- sympatric species to evaluate the existence of ping was estimated only for localities where trophic segregation within the genus. at least two species are sympatric; the species pair H. bartoni - H. labridens in the headwaters MATERIALS AND METHODS of the Río Verde, San Luis Potosí México; H. pame, H. steindachneri and H. tamasopoensis Study sites: Includes most of the Pánuco in the Río Gallinas, San Luis Potosí, México river basin and the endorheic basin of Cuatro and finally, nine sympatric localities for H. 644 Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 67(3): 643-653, June 2019 carpintis and H. pantostictus were examined (Fig. 1). Photographs were digitized in tpsdig throughout their geographic distribution (Digi- (Rohlf, 2005) and Procrustes coordinates were tal Appendix 1). In order to designate trophic estimated in MorphoJ 1.03C (Klingenberg, groups and to represent species in a consump- 2011). To eliminate the allometric effect asso- tion gradient, a principal component analysis ciated with growth, a multivariate regression was performed; with the arc sin standardized analysis was performed, using the Procrustes matrix of the food items proportion to cluster distances as the dependent variable and the each species in a single trophic group. The size of the centroid as the independent variable. analysis was performed in XLSTAT (XLSTAT, The adjusted Procrustes distances were used as 2013). descriptors of the level of differences among lower pharyngeal jaw shapes between the spe- Geometric morphometrics: A total of 303 cies; the significance of the differences was lower pharyngeal jaws (LPJ) were analyzed in evaluated using a permutation test with 10 000 the twelve species of the genus (one image of iterations (Elmer, Kusche, Lehtonen, & Meyer, LPJ per species is available in Digital Appen- 2010) in MorphoJ 1.03C (Klingenberg, 2011). dix 2). Ten LPJs were analyzed for each one of After it, following the criteria established by the restricted distributed species (H. bartoni, Říčan et al. (2016) species were classified into H. labridens, H. pame, H. steindachneri, H. trophic morphs: H. pame, H. tepehua, H. dep- molango, H. deppii, H. tepehua, H. cyanogut- pii, H. labridens, H. bartoni and H. pantostic- tatus, H. minckleyi and H. tamasopoensis). For the widespread H. carpintis and H. pantostictus
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