RESSALVA Atendendo solicitação do autor, o texto completo desta tese será disponibilizado somente a partir de 12/08/2020 Arturo Angulo Sibaja Gross brain morphology of the Loricariinae (Siluriformes: Loricariidae): Comparative anatomy, ecological implications and phylogenetic analysis São José do Rio Preto 2019 Câmpus de São José do Rio Preto Arturo Angulo Sibaja Gross brain morphology of the Loricariinae (Siluriformes: Loricariidae): comparative anatomy, ecological implications and phylogenetic analysis Tese apresentada como parte dos requisitos para obtenção do título de Doutor em Biologia Animal, junto ao Programa de Pós-Graduação em Biologia Animal, do Instituto de Biociências, Letras e Ciências Exatas da Universidade Estadual Paulista “Júlio de Mesquita Filho”, Câmpus de São José do Rio Preto. Financiadora: PAEC OEA-GCUB / MICITT – PED-017-2015-1 Orientador: Prof. Dr. Francisco Langeani Neto São José do Rio Preto 2019 A594g Angulo, Arturo Gross brain morphology of the Loricariinae (Siluriformes: Loricariidae): Comparative anatomy, ecological implications and phylogenetic analysis / Arturo Angulo. -- São José do Rio Preto, 2019 227 f. : il., tabs., fotos + 1 CD-ROM Tese (doutorado) - Universidade Estadual Paulista (Unesp), Instituto de Biociências Letras e Ciências Exatas, São José do Rio Preto Orientador: Francisco Langeani 1. Zoologia. 2. Ecologia. 3. Peixes de água doce. 4. Cascudo (Peixe). 5. Cérebro. I. Título. Sistema de geração automática de fichas catalográficas da Unesp. Biblioteca do Instituto de Biociências Letras e Ciências Exatas, São José do Rio Preto. Dados fornecidos pelo autor(a). Essa ficha não pode ser modificada. Arturo Angulo Sibaja Gross brain morphology of the Loricariinae (Siluriformes: Loricariidae): comparative anatomy, ecological implications and phylogenetic analysis Tese apresentada como parte dos requisitos para obtenção do título de Doutor em Biologia Animal, junto ao Programa de Pós-Graduação em Biologia Animal, do Instituto de Biociências, Letras e Ciências Exatas da Universidade Estadual Paulista “Júlio de Mesquita Filho”, Câmpus de São José do Rio Preto. Financiadora: PAEC OEA-GCUB / MICITT – PED-017-2015-1 Comissão Examinadora Prof. Dr. Francisco Langeani Neto UNESP – Câmpus de São José do Rio Preto Orientador Prof. Dr. Fabio Müller Pupo USP – Museu de Zoologia, Coleção de Peixes Prof. Dr. Oscar Akio Shibatta UEL – Departamento de Biologia Animal e Vegetal Prof. Dr. Raphaël Covain Muséum d’Histoire Naturelle, Genève Prof. Dr. Vitor Abrahão USP – Museu de Zoologia, Coleção de Peixes Profª. Drª. Lúcia Rapp Py-Daniel INPA – Coleção de Peixes São José do Rio Preto 12 de Fevereiro 2019 ACKNOWLEDGEMENTS To my family, friends, colleagues and teachers (in Brazil and Costa Rica), who supported me and provided me all the necessary tools to successfully complete this academic phase of my life. To Carolina Méndez for her constant support, patience and love in the distance. To Mark Sabaj, Mariangeles Arce (ANSP), Jonathan Armbruster, Dave Werneke (AUM), Armando Ortega (IMCN), Lucia Rapp Py-Daniel (INPA-ICT), Claudio de Oliveira (LBP), Carlos Lucena, Alejandro Londoño (MCP), Raphael Covain (MHNG), Hernan Ortega (MUSM), Aléssio Datovo, Osvaldo Oyakawa (MZUSP), Carla Pavaneli, Sandra Regina (NUP), Flávio Bockmann, Hertz Santos (LIRP), Myrna López, Ana Ramírez (UCR), Luiz Malabarba, Juliana Wingert (UFRGS), Mónica Rodriguez (UFV), Jeff Williams (USNM), Francisco Severo, Fernando Carvalho (ZUFMS) and Marcelo Loureiro (ZVCP) for the loan/donation of specimens for dissection. To the authorities and the administrative staff of the IMCN, MZUSP, LIRP, UCR and DZSJRP (IBILCE – UNESP) for the assistance provided and for the use of facilities during my work and visits to the respective collections. To the Costa Rican Ministerio de Ciencia, Tecnología y Telecomunicaciones (MICITT; PED-017-2015-1) and the Partnerships Program for Education and Training of the Organization of American States in conjunction with the Grupo Coimbra de Universidades Brasileiras (PAEC OEA-GCUB, 2014) for financial support. To Danilo de Oliveira for reviewing and correcting the format of the references. RESUMO A família Loricariidae é a mais diversa dentro do ordem Siluriformes, contendo cerca de 980 espécies válidas. Os membros da família são facilmente reconhecidos por possuírem corpos cobertos por placas dérmicas ossificadas, dentes tegumentares abundantes e um disco oral ventral que facilita a fixação á superfície e a alimentação. A subfamília Loricariinae é a segunda mais diversa dentro de Loricariidae, contendo 31 gêneros e cerca de 243 espécies válidas. Os membros da subfamília são facilmente reconhecidos por ter um pedúnculo caudal alongado e deprimido e por a falta de uma nadadeira adiposa. As espécies de Loricariinae estão amplamente distribuídas pelas principais drenagens da maioria dos rios da América Central e do Sul, sendo geralmente encontradas próximas ao substrato e apresentando uma extraordinária diversidade morfológica e funcional. Tradicionalmente, a maioria dos estudos morfológicos e ecomorfológicos em membros da subfamília e a família, seja sob uma abordagem descritiva/comparativa e/ou cladística, focalizou o uso de caracteres osteológicos. Este estudo descreve e compara a morfologia cerebral superficial dos membros da subfamília e família e explora seu significado ou valor ecológico e filogenético. Mais de 300 espécimes [incluindo representantes de quase todos os gêneros válidos de Loricariinae, bem como de outras sete subfamílias de Loricariidae (Delturinae, Hypoptopomatinae, Hypostominae, Lithogeninae, Neoplecostominae, “Otothyrinae” e Rhinelepinae)] e 89 caracteres foram examinados. Os resultados obtidos sugerem que o tamanho, volume e forma relativa das diferentes estruturas cerebrais examinadas varia principalmente com o comportamento alimentar e o ambiente preferido. Além disso, quando analisados e avaliados em conjunto com hipóteses de relacionamento filogenético, estes resultados podem ser considerados como evidência empírica apoiando o fato de que a diversidade cerebral nos membros atuais da subfamília e a família pode ser o resultado tanto do conservadorismo de nicho filogenético quanto da radiação adaptativa repetida. Finalmente, este trabalho fornece dados adicionais a serem considerados na árvore evolutiva da subfamília e a família, destacando a necessidade de mais estudos integrando informações de diferentes sistemas anatômicos em um contexto filogenético. Além disso, este trabalho representa uma base para futuras investigações sobre as relações entre a anatomia do cérebro e a ecologia dos membros da subfamília, família e ordem em um contexto filogenético. Palavras-chave: Cascudos. Ecomorfologia. Filogenia. Neuroanatomia. Ontogenia. ABSTRACT The family Loricariidae is the most species-rich within the Siluriformes, containing about 980 valid species. Members of the family are easily recognized by having bodies covered by ossified dermal plates, abundant integumentary teeth and a ventral oral disk that facilitates surface attachment and feeding. The subfamily Loricariinae is the second most species rich within the Loricariidae containing 31 genera and about 243 valid species. Members of the subfamily are easily recognized by having an elongate and depressed caudal peduncle and by lacking of adipose fin. Species of the Loricariinae are widely distributed throughout the Central and South American major river drainages, being usually found near the substrate and showing an extraordinary morphological and functional diversity. Traditionally, most of the morphological, and ecomorphological, studies on members of the subfamily and the family, either under a descriptive/comparative and/or cladistic approach, have focused on the use of osteological characters. This study describes and compares the gross brain morphology of the members of the subfamily and the family and explores their ecological and phylogenetic significance. More than 300 specimens [including representatives of almost all valid genera of the Loricariinae, as well as of other seven subfamilies of the Loricariidae (Delturinae, Hypoptopomatinae, Hypostominae, Lithogeninae, Neoplecostominae, “Otothyrinae” and Rhinelepinae)] and 89 characters were examined. The results obtained suggest that the relative size, volume and shape of the different brain structures examined varies mostly with feeding behaviour and preferred environment. Furthermore, when analyzed and evaluated in conjunction with hypotheses of phylogenetic relationships, these results can be considered as empirical evidence supporting the fact that brain diversity in current members of the subfamily, and the family in general terms, could be the result of both phylogenetic niche conservatism and repeated adaptive radiation. Finally, this work provides considerable additional data to the evolutionary tree of the subfamily and the family, highlighting the needing of further studies integrating information from different anatomical systems in a phylogenetic context. Moreover, this work could be a basis for further investigations on the relationships between brain anatomy and the ecology of members of the subfamily, family and order in a phylogenetic frame. Keywords: Ecomorphology. Neuroanatomy. Ontogeny. Phylogeny. Suckermouth armoured catfishes. LIST OF TABLES, FIGURES AND ILLUSTRATIONS Table 1. Body length (SL), mass (We) and brain measurements (28) of examined specimens of Rineloricaria heteroptera (n=42); absolute values and percentages of total brain length, head length or total brain volume, as appropriate. Morphometric measurements (-L=length; -W=width, -H=height), numbered from 1 to 28, are expressed in mm, volumes (“-V”s) are expressed in mm3 and masses (“-We”s) are expressed in mg. Linear measurements refer only to the left lobe or counterpart for those bilateral structures; volumes for these bilateral structures were doubled, assuming brain symmetry ………………………………………………………...…… 27 Table 2. Results of the ANCOVAs evaluating the effect of the body length (SL) and the body mass (BW), as the covariates, and the sex, the developmental stage and the interaction between them (i.e. sex*developmental stage), as the factors, on the scaling of the overall brain length (T-L) and brain mass (T-W) in Rineloricaria heteroptera. Significant p values are denoted with an asterisk (*) …………… 42 Table 3. Slopes or "allometric coeffients" (a) and intercepts or "allometric components" (b), with their respectives ± standard error of mean (SEM) and 95% bootstrapped confidence intervals (CIV; N=1999), and correlation values (r2), with their respective associated "p" value, of the OLS linear regressions lines for the eigth major brain subdivisions volumes (vs. corrected total brain volumes) in Rineloricaria heteroptera .…………..…………………………………...……………………………. 42 Table 4. Results of the ANCOVAs evaluating the effect of the corrected total brain volume, as the covariate, and the sex, the developmental stage and the interaction between them (i.e. sex*developmental stage), as the factors, on the scaling of each brain subdivision volume in Rineloricaria heteroptera. Significant p values are denoted with an asterisk (*) ……………………..………………………………. 43 Table 5. Results for the first four components (PCs) of the PCA of the relative volume of eight brain subdivisions in Rineloricaria heteroptera …………..…. 44 Table 6. Results of the PERMANOVA test for statistical significance between groups of the Loricariidae, based on the PCoA using a total of 88 binary or multistate, non- ordered characters describing its gross brain morphology. Pairwise comparisons; F and Bonferroni-corrected p (Bp) values. Abbreviations: TG=Taxonomic group; De=Delturinae; Hp=Hypoptopomatinae; Hy=Hypostominae; LF=Loricariinae, Loricariini, Farlowellina; LH=Loricariinae, Harttiini; Li=Lithogeninae; LL=Loricariinae, Loricariini, Loricariina; Ne=Neoplecostominae; and Rh=Rhinelepinae. Bold numbers denotes a significant difference between groups ……………………………... 45 Figure 1. Rineloricaria heteroptera; Machado River basin, Madeira River drainage, Rondonia, Brazil; (A) entire specimen (DZSJRP 16730; 75.25 mm SL; female); dorsal (above), lateral (centre) and ventral (below) views; (B, C) ventral detail of head of sexually dimorphic male (B; DZSJRP 14771, 80.15 mm SL) and female (C; DZSJRP 17429, 81.11 mm SL); note the presence (in the male) of shorted, thickened an curved pectoral-fin spines and numerous small odontodes along the sides of the head and the pectoral-fin spines ........................................................................... 31 Figure 2. Topographic brain anatomy of Rineloricaria heteroptera (DZSJPR 014771), 114.42 mm SL; Machado River basin, Madeira River drainage, Rondonia, Brazil; (above) dorsal, (centre) lateral (left side) and (below) ventral views. Pointed lines indicate the anterior and posterior limits of the brain ........................................... 36 Figure 3. Intraspecific variation on the brain of Rineloricaria heteroptera; Machado River basin, Madeira River drainage, Rondonia, Brazil. (A, B, C) DZSJPR 016730, 38.75 mm SL; (D) dorsal, (E) lateral (left side) and (F) ventral views. (D, E, F) DZSJPR 014771, 54.31 mm SL; (D) dorsal, (E) lateral (left side) and (F) ventral views. (G, H, I) DZSJPR 014549, 97.29 mm SL; (G) dorsal, (H) lateral (left side) and (I) ventral views. Scale bar=2 mm ........................................................................... 39 Figure 4. Regression analysis (OLS) of the LOG brain size (length) on the LOG body size (length) in Rineloricaria heteroptera. Developmental stages are denoted with different color symbols (Green=early juveniles, i.e. <60.0 mm SL; Blue=late juveniles, i.e. 60.1–80.0 mm SL; and Red=adults, i.e. >80.0 mm SL); females are represented by closed symbols, males are represented by open symbols ................................ 41 Figure 5. Regression analysis (OLS) of the LOG brain mass on the LOG body mass in Rineloricaria heteroptera. Developmental stages are denoted with different color symbols (Green=early juveniles, Blue=late juveniles and Red=adults); females are represented by closed symbols, males are represented by open symbols .......... 47 Figure 6. Allometric scaling relationships (volume vs. volume OLS regression lines) for the eigth major brain subdivisions in Rineloricaria heteroptera. Developmental stages are denoted with different color symbols (Green=early juveniles, Blue=late juveniles and Red=adults); females are represented by closed symbols, males are represented by open symbols ................................................................................. 48 Figure 7. Scatterplot of the PCA (PC1 vs. PC2), representing the major changes in the composition of the brain along development in Rineloricaria heteroptera. Developmental stages are denoted with different color symbols (Green=early juveniles, i.e. <60.0 mm SL; Blue=late juveniles, i.e. 60.1–80.0 mm SL; and Red=adults, i.e. >80.0 mm SL); females are represented by closed symbols, males are represented by open symbols ........................................................................... 52 Figure 8. Topographic brain anatomy of a generalized member of the Loricariinae (Loricaria cataphracta, type species of the family; MZUSP 014106; 114.70 mm SL); (A) dorsal, (B) lateral (left side) and (C) ventral views. Pointed lines indicate the anterior and posterior limits of the brain. Scale bar=2 mm ................................ 69 Figure 9. Brain of selected species of the Loricariinae, dorsal view; (A) Farlowella oxyrryncha, DZSJRP 014920, female, 124.00 mm SL; (B) Fonchiiloricaria nanodon, MUSM 032153, male, 167.98 mm SL; (C) Harttia novalimensis, DZSJRP 001644, male, 102.53 mm SL; (D) Hemiodontichthys acipenserinus, INPA-ICT 032082, male, 92.34 mm SL; (E) Loricariichthys anus, DZSJRP 010987, female, 158.00 mm SL; (F) Ricola macrops, ZVCP 014035, male, 221.00 mm SL; (G) Rineloricaria cubataonis, DZSJRP 003269, female, 104.53 mm SL; (H) Sturisomatichthys leightoni, ANSP 084177, male, 118.26 mm SL. Scale bar=2 mm ..................................................... 70 Figure 10. Brain of selected species of the Loricariinae, lateral view; (A) Farlowella oxyrryncha, DZSJRP 014920, female, 124.00 mm SL; (B) Fonchiiloricaria nanodon, MUSM 032153, male, 167.98 mm SL; (C) Harttia novalimensis, DZSJRP 001644, male, 102.53 mm SL; (D) Hemiodontichthys acipenserinus, INPA-ICT 032082, male, 92.34 mm SL; (E) Loricariichthys anus, DZSJRP 010987, female, 158.00 mm SL; (F) Ricola macrops, ZVCP 014035, male, 221.00 mm SL; (G) Rineloricaria cubataonis, DZSJRP 003269, female, 104.53 mm SL; (H) Sturisomatichthys leightoni, ANSP 084177, male, 118.26 mm SL. Scale bar=2 mm ........................................... 74 Figure 11. Brain of selected species of the Loricariinae, ventral view; (A) Farlowella oxyrryncha, DZSJRP 014920, female, 124.00 mm SL; (B) Fonchiiloricaria nanodon, MUSM 032153, male, 167.98 mm SL; (C) Harttia novalimensis, DZSJRP 001644, male, 102.53 mm SL; (D) Hemiodontichthys acipenserinus, INPA-ICT 032082, male, 92.34 mm SL; (E) Loricariichthys anus, DZSJRP 010987, female, 158.00 mm SL; (F) Ricola macrops, ZVCP 014035, male, 221.00 mm SL; (G) Rineloricaria cubataonis, DZSJRP 003269, female, 104.53 mm SL; (H) Sturisomatichthys leightoni, ANSP 084177, male, 118.26 mm SL. Scale bar=2 mm ..................................................... 76 Figure 12. Empirical morphospace for members of the Loricariidae, based on the first three principal coordinates (PCos) of the PCoA using a total of 88 binary or multistate non-ordered characters describing its gross brain morphology. (A) PCo1 vs. PCo2 empirical morphospace; (B) PCo1 vs. PCo3 empirical morphospace; (C) Detail of the space occupied by members of the Loricariinae in the PCo1 vs. PCo2 empirical morphospace; (D) Detail of the space occupied by members of the Hypoptopomatinae sensu lato and the Neoplecostominae in the PCo1 vs. PCo2 empirical morphospace (see complete species names in Appendix 3). Yellow symbols represents members of the Delturinae (De); blue symbols represents members of the Hypoptopomatinae (Hp); orange symbols represents members of the Hypostominae (Hy); red symbols represents members of the Neoplecostominae (Ne); green symbols represents members of the Loricariinae [non-filled symbols represents members of the Harttiini (LH); the purple symbol represents the single representative of the Lithogeninae (Li); filled symbols represents members of the Loricariini (LF=Farlowellina, LL=Loricariina)]; the black symbol represents the single representative of the Rhinelepinae …………………………………………..…. 84 Figure 13. Strict consensus of ten maximally parsimonious trees (1154 steps; CI=0.10; RI=0.66), showing the interrelationships among members of the Loricariinae and Loricariidae (gross brain morphology); see part of the consensus tree (i.e., non- Loricariinae members of the Loricariidae) in Fig. 14. Numbers above branches indicate the number of the clade and those below the branches correspond to the Bremer support values (in those clades in which no number is indicated the Bremer support value was equal or greater than 15) …………………………………...… 110 Figure 14. Part of the strict consensus of ten maximally parsimonious trees (1154 steps; CI=0.10; RI=0.66), showing the interrelationships among members of the non- Loricariinae subfamilies of the Loricariidae (gross brain morphology); see the complete tree in Fig. 13. Numbers above branches indicate the number of the clade and those below the branches correspond to the Bremer support values (in those clades in which no number is indicated the Bremer support value was equal or greater than 15) ….........................................................................................… 112 Figure 15. Strict consensus of ten maximally parsimonious trees (1459 steps; CI=0.13; RI=0.71), showing the interrelationships among members of the Loricariidae (combined analysis); see part of the consensus tree (i.e., members of the Loricariinae) in Fig. 16. Numbers above branches indicate the number of the clade and those below the branches correspond to the Bremer support values (in those clades in which no number is indicated the Bremer support value was equal or greater than 15) …………………………………………………………………...… 116 Figure 16. Part of the strict consensus of ten maximally parsimonious trees (1459 steps; CI=0.13; RI=0.71), showing the interrelationships among members of the Loricariinae (combined analysis); see the complete tree in Fig. 15. Numbers above branches indicate the number of the clade and those below the branches correspond to the Bremer support values (in those clades in which no number is indicated the Bremer support value was equal or greater than 15) ……………………………... 118 Figure 17. Detail of the olfactory organs and olfactory bulbs of selected species of the Loricariidae, dorsal view. (A) Delturus brevis, NUP 015446, male, 137.66 mm SL; (B) Lamontichthys filamentosus, LBP 000162, male, 184.00 mm SL; (C) Loricariichthys anus, DZSJRP 010987; female, 158.00 mm SL; (D) Farlowella oxyrryncha, DZSJRP 017180, male, 127.00 mm SL. Scale bar=2 mm ……... 149 Figure 18. Detail of the olfactory organs and olfactory bulbs of selected species of the Loricariidae, ventral and lateral views. (A) Farlowella henriquei, MZUSP 014408, male, 120.62 mm SL; (B) Scleromystax barbatus, DZSJRP 005726, female, 63.70 mm SL; (C) Ancistrus sp., DZSJRP 011949, female, 53.80 mm SL; (D) Dentectus barbarmatus, ANSP 198883, male, 100.52 mm SL; (E) Delturus carinotus, MCP 028037, male, 153.10 mm SL. Scale bar=2 mm ………………………………..……. 151 Figure 19. Brain of selected species of the Loricariidae; detail of the olfactory organs, olfactory bulbs and the anterior portion of the brain (telencephalon and mesencephalon), dorsal and lateral views. (A) Corumbataia cuestae, DZSJRP 008027, female, 29.30 mm SL; (B) Megalancistrus parananus, DZSJRP 004845, female, 129.00 mm SL; (C) Limatulichthys petleyi, MZUSP 073995, male, 94.65 mm SL; (D) Loricaria cataphracta, DZSJRP 014499, male, 130.13 mm SL; (E) Otocinclus affinis, DZSJRP 007610, female, 26.00 mm SL. Scale bar=2 mm ……………... 152 Figure 20. Brain of selected species of the Loricaroidea; detail of the antero-medial portion of the brain (telencephalon, diencephalon and mesencephalon), dorsal and lateral views. (A) Kronichthys subteres, MCP 020152, female, 64.10 mm SL; (B) Corydoras aeneus, DZSJRP 015193, female, 44.80 mm SL; (C) Hypostomus regani, DZSJRP 016049, female, 123.00 mm SL, lateral view; (D) Dasyloricaria latiura, USNM 293168, male, 242.00 mm SL; (E) Delturus carinotus, MCP 028037, male, 153.10 mm SL. Scale bar=2 mm …………………………………………………...… 153 Figure 21. Brain of selected species of the Loricariidae, lateral and ventral views. (A) Loricaria cataphracta, MZUSP 014106, male, 114.70 mm SL; (B) Farlowella paraguayensis, DZSJRP 018794, female, 99.55 mm SL; (C) Cteniloricaria platystoma, ANSP 190521, female, 116.71 mm SL; (D) Hemiodontichthys acipenserinus, INPA-ICT 032082, male, 92.34 mm SL; (E) Otothyropsis marapoama, DZSJRP 014108, female, 27.20 mm SL; (F) Paraloricaria vetula, ZVCP 14036, male, 217.00 mm SL; (G) Neoplecostomus selenae, DZSJRP 015331, male, 78.30 mm SL; (H) Neoplecostomus yapo, DZSJRP 013651, female, 74.90 mm SL. Scale bar=2 mm …………………………………………………………………...… 154 Figure 22. Brain of selected species of the Loricaroidea, detail of the anterior and medial portions of the brain (telencephalon, mesencephalon and corpus cerebelli), dorsal and lateral views. (A) Neoplecostomus selenae, DZSJRP 015331, male, 78.30 mm SL; (B) Neoplecostomus yapo, DZSJRP 013651, female, 74.90 mm SL; (C) Rineloricaria cadeae, MCP 009782, male, 123.08 mm SL; (D) Corydoras aeneus, DZSJRP 015193, female, 44.80 mm SL; (E) Harttia novalimensis, DZSJRP 011644, male, 102.53 mm SL; (F) Proloricaria prolixa, DZSJRP 006312, female, 104.51 mm SL. Scale bar=2 mm ……………………………………………………………... 157 Figure 23. Brain of selected species of the Loricariidae, dorsal and lateral views. (A) Pseudohemiodon platycephalus, ZUFMS-PIS 000440, female, 136.26 mm SL; (B) Loricaria luciae, ZUFMS-PIS 003215, male, 120.33 mm SL; (C) Dekeyseria scaphirhynchus, INPA-ICT 036022, male, 85.17 mm SL; (D) Hisonotus insperatus, DZSJRP, 018211, male, 23.20 mm SL; (E) Loricariichthys platymetopon, DZSJRP 004395, female, 241.00 mm SL; (F) Delturus brevis, NUP 015446, male, 137.66 mm SL; (G) Hisonotus insperatus, DZSJRP, 014381, female, 32.30 mm SL. Scale bar=2 mm ……………………………………………………………………………………... 123 Figure 24. Brain of selected species of the Loricariidae, dorsal and lateral views. (A) Fonchiiloricaria nanodon, MUSM 032153, female, 166.27 mm SL; (B) Reganella depressa, MZUSP 057936, male, 139.97 mm SL; (C) Brochiloricaria macrodon, NUP 002248, male, 262.00 mm SL; (D) Oxyropsis wrighthiana, MCP 034503, female, 44.00 mm SL; (E) Furcodontichthys novaesi, MZUSP 057726, male, 126.38, mm SL. Scale bar=2 mm ………………………………………………………………...…… 162 LIST OF ABBREVIATIONS AND ACRONYMS Ad Adenohypophysis Ce Corpus cerebelli Ch Chiasma opticum Char Character De Delturinae EG Eminentia granularis Hp Adenohypophysis/Hypoptopomatinae Hy Hypothalamus/Hypostominae I Nervus olfatorius II Nervus opticus III Nervus oculomotorius IV Nervus trochlearis IX Nervus glossopharyngeus La Ofactory lamella LF Loricariinae, Loricarini, Farlowellina LH Lobus inferior hypothalami/Loricariinae, Harttiini Li Lithogeninae LL Loricariinae, Loricarini, Loricarina LLA Nervus linea lateralis anterior LLP Nervus linea lateralis posterior LobVII Lobus facialis LobX Lobus vagi MO Alar portion of the medulla oblongata Me Medulla spinalis Ne Neoplecostominae OB Olfactory bulbs Of Olfactory organ OT Optic tectum Rh Rhinelepinae TC Truncus cerebri SL Standard length Te Telencephalon TG Taxonomic group TL Torus lateralis Tol Nervus tractus olfactorius V Nervus trigeminus VI Nervus abducens VII Nervus facialis VIII Nervus octavus or vestibulares X Nervus vagus TABLE OF CONTENTS 1. GENERAL INTRODUCTION ……………………………………………... 17 1.1. Aims and dissertation structure …………………………………………...… 19 2. CHAPTER 1: GROSS BRAIN MORPHOLOGY OF Rineloricaria heteroptera ISBRÜCKER & NIJSSEN, 1976 AS SPECIES MODEL: A DESCRIPTIVE AND QUANTITATIVE APPROACH ……………....…………………...… 20 2.1. Abstract ……………………………………………………………………... 20 2.2. Keywords …………………………………………………………………..…. 21 2.3. Introduction …………………………………………………………………..…. 22 2.4. Material and methods ……………………………………………………... 24 2.4.1. Species of study ...................................................................................... 24 2.4.2. Material examined ……………………………………………………………... 25 2.4.3. Data acquisition ...................................................................................... 25 2.4.4. Data analyses .............................................................................................. 32 2.5. Results ………………………………………………………………………….… 34 2.5.1. Gross brain morphology of Rineloricaria heteroptera (Descriptive approach) ................................................................................................. 34 2.5.2 Sexual dimorphism and ontogenetic variation in the number of lamellae on the olfactory organs and in the total brain size and mass and brain subdivisions volumes in Rineloricaria heteroptera (Quantitative approach) ..................... 40 2.6. Discussion ………………………………………………………………….….. 47 2.6.1 Sexual dimorphism in the brain of Rineloricaria heteroptera and its ecological implications …………………………………………………………………...… 47 2.6.2 Ontogenetic variation in the brain of Rineloricaria heteroptera and its ecological implications ……………………………………………………... 50 3. CHAPTER 2: GROSS BRAIN MORPHOLOGY OF THE LORICARIINAE: COMPARATIVE ANATOMY AND ECOLOGICAL AND PHYLOGENETIC CONSIDERATIONS …………………………………………………....... 58 3.1 Abstract ...…………………………………………………………………… 58 3.2. Keywords …………………………………………………………...………… 59 3.3. Introduction …………………………………………………………….........…. 60 3.4. Material and methods ……………………………………………………... 62 3.4.1. Group of study …………….……………………………………………….. 62 3.4.2. Material examined ……………………………………………………………... 63 3.4.3. Data acquisition ……………………………………………………………... 64 3.4.4. Data analyses ……………………………………………………………... 65 3.5. Results ………………………………………………………………...…… 66 3.5.1. Gross brain morphology of the Loricariinae (Descriptive anatomy) …...… 66 3.5.2. Gross brain morphological disparity in the Loricariidae (Quantitative approach) ................................................................................................. 80 3.6. Discussion …………………………………………………………….……….. 84 3.6.1. Comparative anatomy and gross ecological correlations and implications …………………………………..………………………….....….. 84 3.6.2. Morphological disparity and phylogenetic considerations …………..…. 95 3.6.3. Additional phylogenetic considerations ………………...…………………… 97 4. CHAPTER 3: A CONTRIBUTION TO THE PHYLOGENY OF THE LORICARIIDAE, WITH EMPHASIS ON THE LORICARIINAE, USING MOSTLY GROSS BRAIN MORPHOLOGICAL CHARACTERS ................ 99 4.1 Abstract ...…………………………………………………………………… 99 4.2. Keywords …………………………………………………………...………… 100 4.3. Introduction …………………………………………………………….........…. 101 4.4. Material and methods ……………………………………………………... 106 4.4.1. Taxon sampling ……………………………………………………………... 106 4.4.2. Character sampling ...................................................................................... 107 4.4.3. Cladistic methodology and phylogenetic analysis ................................ 108 4.4.4. Combined analysis …………………………………………………….……….. 108 4.5. Results ………………………………………………………………...…… 109 4.5.1. Neuroanatomical analysis …………………………………….………..……… 109 4.5.2. Combined analysis ………………………………………………….………….. 113 4.6. Discussion ……………………………………………………………………... 119 5. GENERAL CONCLUSIONS ………………………………………...…… 125 REFERENCES ……………………………………………………………... 126 APPENDIXES ………………………………………………….......……… 145 APPENDIX A. Material examined ………………………………………..……. 145 APPENDIX B. List of characters analyzed (gross brain morphology) ……... 149 APPENDIX C. Data matrix used for the PCoA ………………………..……. 164 APPENDIX D. Data matrix used for the parsimony analyses …………..…. 175 APPENDIX E. List of characters analyzed (osteology and other external characters) ................................................................................................. 188 APPENDIX F. List of synapomorphies and autapomorphies for each clade and terminal taxon, respectively (gross brain morphology) ……………………... 193 APPENDIX G. List of synapomorphies and autapomorphies for each clade and terminal taxon, respectively (combined analysis) ………………….….. 208 17 1. GENERAL INTRODUCTION The family Loricariidae (suckermouth armoured catfishes, armoured catfishes or plecos) is the most species-rich within the Siluriformes (catfishes), containing about 980 valid species (FRICKEE et al., 2018a) as well as several undescribed forms. Members of the family are easily recognized from other fishes by having bodies covered by ossified dermal plates, abundant integumentary teeth (odontodes) and a ventral oral disk that facilitates surface attachment and feeding (REIS et al. 2003; GARG et al., 2010; GEERINCKX et al., 2011; LUJAN et al., 2015). The subfamily Loricariinae is the second most species-rich within the Loricariidae containing 31 genera and about 243 valid species (FRICKEE et al., 2018a) as well as several undescribed forms, corresponding to about 25% of the total known diversity within the family. Members of the Loricariinae are easily recognized from other loricariids by having elongate and depressed caudal peduncles and by lacking of adipose fin, among other distinctive characters (see SCHAEFER, 1987; RAPP PY- DANIEL, 1997; COVAIN & FISCH-MULLER, 2007); they are widely distributed throughout the Central and South American major river drainages, from southern Costa Rica to northern Argentina (REIS et al., 2003; COVAIN & FISCH-MULLER, 2007), showing an extraordinary morphological and functional diversity (see SCHAEFER & LAUDER, 1986; COVAIN & FISCH-MULLER, 2007; COVAIN, 2011; LUJAN & ARMBRUSTER, 2012; LUJAN et al., 2015). Studies focused on the phylogenetic relationships on members of the Loricariinae, and Loricariidae, in general terms, agree, in some measure, with the monophyly of the subfamily and in the recognition of two major lineages, the tribes Harttiini and Loricariini, whose generic composition varies between authors (see for example the contributions of RAPP PY-DANIEL, 1997; MONTOYA-BURGOS et al., 1998; ARMBRUSTER, 2004; COVAIN & FISCH-MULLER, 2007; COVAIN et al., 2008, 2010, 2016; ROXO et al., 2019). Despite of such studies, and as noted by the same authors, a taxonomic synthesis of the subfamily, and the family, in general terms, is still needed in order to provide a foundation for more detailed studies on its members, considering that (1) at lower taxonomic levels, morphological–molecular discordance and homoplasy is still problematic or has not been appropriately evaluated, (2) synapomorphies for many clades at/below the rank of tribe are relatively scarce and (3) the disagreement about the monophyly and taxonomic 18 validity of some genera (see RAPP PY-DANIEL, 1997; COVAIN & FISCH-MULLER, 2007; RAPP PY DANNIEL & FICHBERG, 2008; COVAIN, 2011; LONDOÑO- BURBANO, 2012; COVAIN et al., 2016; ROXO et al., 2019). Most of the morphological, and ecomorphological, studies on members of the Loricariinae, and the Loricariidae, in general terms, either under a descriptive, comparative (e.g., ISBRÜCKER, 1979; RAPP PY-DANIEL, 1997; ARMBRUSTER, 2004; COVAIN & FISCH-MULLER, 2007; LUJAN & ARMBRUSTER, 2012) and/or cladistic approach (e.g., SCHAEFER, 1987; RAPP PY-DANIEL, 1997; ARMBRUSTER, 2004; among others), have focused on the use of osteological characters; this could be understandable given (1) their “pretty well-known” utility for comparative purposes, (2) their relative easy access and (3) the extensive literature available (see for example REGAN, 1904; 1911; LEEGE, 1922; ANGELESCU & GNERI, 1949; ALEXANDER, 1964; 1965; CHARDON, 1968; LUNDBERG & BASKIN, 1969; ISBRÜCKER, 1979; SCHAEFER, 1987; RAPP PY-DANIEL, 1997; COVAIN & FISCH-MULLER; 2007). On the other hand, descriptive, comparative and/or cladistic studies considering alternative body systems, such as the brain anatomy (neuroanatomy), in both members of the Loricariinae and Loricariidae, as well as in other teleost fish taxa, in general terms, have been rarely addressed, and/or when undertaken, rarely carried on in an organized fashion [see FREIHOFER, 1978; HOWES, 1983; RAPP PY-DANIEL, 1997; PUPO, 2011, 2015; DATOVO & VARI, 2014; ROSA, 2015; PEREIRA & CASTRO, 2016; among others (see below), for examples and a more detailed discussion]. This “extensive” exploration of osteological characters demonstrated to be “rather efficient” for the delimitation of most major clades within the Teleostei; however, as noted by DATOVO & VARI (2014) and PEREIRA & CASTRO (2016), among other authors, it also resulted in the “relatively minor attention” of alternative, and (possibly) equally or more informative, anatomical systems. The first investigations on the neuroanatomy of members of the Siluriformes date to the end of the 19th century (see PUPO & BRITTO, 2018); one of the first attempts was the work of HERRICK & HERRICK (1891) who used members of the family Ictaluridae (bullhead catfishes) as subject of study. In the middle of the 20th century, several studies on the external morphology of the brain took place, followed by many papers published on the general anatomy, physiology, cytoarchitecture, hodology and embryology of the brain and the peripheral nervous system of, mainly, 19 Neartic species (see KOTRSCHAL et al., 1998; FINGER, 2000 for an overview). On the other hand, studies on Neotropical fishes, and members of the Siluriformes, specifically, are relatively scarce and have focused only in a few species or supraspecific groups; e.g., members of the Callichthyidae (PUPO, 2011; PUPO & BRITO, 2018), Heptapteridae (TRAJANO, 1994; ABRAHÃO et al., 2018a), Loricariidae (ROSA et al., 2014; ROSA, 2015; ANGULO & LANGEANI, 2017; CHAMON et al., 2018) and Pseudopimelodidae (ABRAHÃO & SHIBATTA, 2015; ABRAHÃO et al., 2018b). Furthermore, in these essentially descriptive (mainly anatomical) contributions, the potential ecological (and phylogenetic) inferences and correlations have been, in most cases, only superficially addressed (see ROSA, 2015; PEREIRA & CASTRO, 2016; ANGULO & LANGEANI, 2017; ABRAHÃO et al., 2018a). 1.1. Aims and dissertation structure In accordance with the above, the main objective of this work is to describe the general gross morphology of the brain of the armoured catfish subfamily Loricariinae, as a baseline for comparative anatomical, taxonomic, phylogenetic and ecological studies. Moreover, four specific objectives, corresponding each one of them (in general terms) with one or more of the three chapters presented below, were raised. These four specific objectives are: (1) to explore and evaluate (quantitatively and qualitatively) the sexual and ontogenetic (post-larvae) intraspecific variation in the gross brain morphology of members of the Loricariinae (chapter one); (2) to explore andevaluate and describe (quantitatively and qualitatively) the intergeneric (considering the major suprageneric taxonomic divisions) variation in the gross brain morphology in members of the Loricariinae, also comparing it with some external taxa within the Loricariidae, Siluriformes and Ostariophysi (chapter two); (3) to explore and evaluate and discuss the possible correlations between the general brain patterns observed and the sensory and behavioral ecology of the species and supraspecific groups (chapters one and two); and (4) to evaluate the phylogenetic significance of the neuroanatomy, in members of the Loricariinae and the Loricariidae, following a cladistic approach (chapter three). 125 5. GENERAL CONCLUSIONS The results obtained in this study suggest that the relative size, volume and shape of the different brain structures examined, in members of the Loricariinae and Loricariidae, varies mostly with feeding behaviour and preferred environment; including changes possibly related to a ontogenetic shift in the habitat/resources use. Furthermore, when analyzed in conjunction with hypotheses of phylogenetic relationships, the results of this study also can be considered as empirical evidence supporting the fact that brain diversity in current members of the subfamily and family could be the result of both phylogenetic niche conservatism and repeated adaptive radiation. This work also provides considerable additional data to the evolutionary tree of the subfamily and family, highlighting the needing of further studies integrating information from different anatomical systems in a phylogenetic context. 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