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Reproductive characteristics of characid (Teleostei... 469

Reproductive characteristics of characid fish species (Teleostei, ) and their relationship with body size and phylogeny

Marco A. Azevedo

Setor de Ictiologia, Museu de Ciências Naturais, Fundação Zoobotânica do Rio Grande do Sul, Rua Dr. Salvador França, 1427, 90690-000 Porto Alegre, RS, Brazil. ([email protected])

ABSTRACT. In this study, I investigated the reproductive biology of fish species from the family of the Characiformes. I also investigated the relationship between reproductive biology and body weight and interpreted this relationship in a phylogenetic context. The results of the present study contribute to the understanding of the evolution of the reproductive strategies present in the species of this family. Most larger characid species and other characiforms exhibit a reproductive pattern that is generally characterized by a short seasonal reproductive period that lasts one to three months, between September and April. This is accompanied by total spawning, an extremely high fecundity, and, in many species, a reproductive migration. Many species with lower fecundity exhibit some form of parental care. Although reduction in body size may represent an adaptive advantage, it may also require evolutionary responses to new biological problems that arise. In terms of reproduction, smaller species have a tendency to reduce the number of oocytes that they produce. Many small characids have a reproductive pattern similar to that of larger characiforms. On the other hand they may also exhibit a range of modifications that possibly relate to the decrease in body size and the consequent reduction in fecundity. Examples of changes in the general reproductive pattern include the following: reduction in the size of mature oocytes; increase in fecundity; production of several batches of oocytes; an extended reproductive period or even continuous reproduction that allows individuals to reproduce more than once a year; high growth rates; rapid recruitment of juveniles; presence of more than one reproductive cohort that increases the sexually active population; and multiple independent development of insemination as a reproductive strategy. These changes are possibly associated with adaptive pressures that are related to the reduction in body size. In addition, such reproductive characteristics or novelties may reflect the phylogenetic history of a given species.

KEY WORDS. Neotropical, reproductive period, seasonality, fecundity, type of spawning, mode of reproduction, insemination.

RESUMO. Características da reprodução de espécies de Characidae (Teleostei: Characiformes) e suas relações com tamanho corporal e filogenia. Neste trabalho, as informações sobre reprodução de espécies de peixes da família Characidae, de Characiformes, são avaliadas considerando suas relações de tamanho corporal e interpretadas em um contexto filogenético, contribuindo para a compreensão da evolução das estratégias reprodutivas presentes nas espécies da família. A maioria das espécies de caracídeos de maior porte apresenta, assim como outros Characiformes, um padrão geral de reprodução caracterizado pelo período reprodutivo sazonal e curto, durando de um a três meses, situado entre setembro e abril; desova normalmente total; fecundidade extremamente elevada e muitas espécies apresentam migração reprodutiva. Muitas espécies que têm a fecundidade menor apresentam cuidado parental. A diminuição do tamanho corporal parece ser uma sinapomorfia dos grupos de Characidae que não apresentam o osso supraorbital. A redução no tamanho pode representar uma vantagem adaptativa em diversos aspectos, mas pode exigir respostas evolutivas a novos problemas biológicos decorrentes. Em termos de reprodução, observa-se uma tendência a que espécies de menor porte reduzam também o número de ovócitos produzidos. Muitos caracídeos de pequeno porte mantêm o padrão geral de reprodução dos Characiformes, mas muitos deles exibem diferentes modificações, possivelmente como resposta à diminuição de tamanho e consequente diminuição da fecundidade. A diminuição do tamanho dos ovócitos maduros; a produção de diversos lotes de ovócitos; o prolongamento do período reprodutivo; a presença de mais de uma coorte reprodutiva ou a reprodução contínua, permitindo que os indivíduos reproduzam mais de uma vez no ano; as altas taxas de crescimento e rápido recrutamento de jovens, aumentando a população sexualmente ativa e a inseminação dos ovários são exemplos de modificações no padrão geral de reprodução, possivelmente em resposta às pressões relacionadas à redução de tamanho corporal. Estas características reprodutivas podem refletir as relações de parentesco das espécies.

PALAVRAS-CHAVE. Neotropical, período reprodutivo, sazonalidade, fecundidade, tipo de desova.

Fish represent an estimated 47 to 51% of all interesting point regarding the diversity of Neotropical species in the world, with about 24% occurring fish is related to the varying sizes of different species. in Neotropical freshwaters (GROOMBRIDGE, 1992). Equally Within some families individual species can vary from notable, particularly in the epicontinental waters of the 1.5 cm to more than 1 m in length. Species of similar sizes Neotropics, is the immense diversity of forms, behaviors, can be found in different environments, using different and lifestyles that allow these organisms to inhabit these food resources, and exhibiting different reproductive and diverse environments (VARI & MALABARBA, 1998). One of phylogenetic characteristics. the most interesting features of plasticity exhibited by This study evaluated some of the data available in fish is the number of different reproductive strategies the literature about reproduction in species of the family employed. One can often observe different reproductive Characidae, order Characiformes. The available data were patterns among members of a fish community that inhabit evaluated in relation to the body sizes of the species and the same environment. In some cases, closely allied were interpreted within a phylogenetic context to species exhibit different reproductive strategies, and, in contribute to the understanding of the evolution of the others, phylogenetically distant species converge different reproductive strategies found within the species independently towards a similar strategy. Another of this family.

Iheringia, Sér. Zool., Porto Alegre, 100(4):469-482, 30 de dezembro de 2010 470 AZEVEDO

In the order Characiformes, smaller species are less than 40 vertebrae (versus more than 40 vertebrae in concentrated in the Characidae, which is the most more basal characid taxa), among other characters. speciose group of this order. Relationships among family Although the relationships of a large number of members are still controversial, but a series of recent genera remain uncertain or are controversial among the papers, starting with MALABARBA & WEITZMAN (2003), and characid subgroup that includes the species lacking a corroborated by CALCAGNOTTO et al. (2005), MIRANDE supraorbital, monophyly of some ingroups have been (2009, 2010) and JAVONILLO et al. (2010), have corroborated, such as for the Aphyocharacinae, demonstrated that Characidae includes a series of basal Characinae, Cheirodontinae, Rhoadsiinae, Stethaprioninae, taxa and a large internal clade composed of all characid and Tetragonopterinae (sensu stricto, containing only species that share the synapomorphic lack of a Cuvier, 1816) (Figs 1 and 2). The supraorbital bone (Figs 1, 2). MIRANDE (2009, 2010) further Aphyoditeinae and Heterocharacinae were newly defined supported this clade by the synapomorphic presence of by MIRANDE (2009, 2010). The Clade A proposed by

Figure 1. Comparative plots of the body size for the species in each monophyletic group resulting in the phylogeny of Mirande (2010) expressed by Tukey box plots based on percentiles. Shaded portion of the cladogram represents those lineages sharing the lack of a supraorbital bone. Shaded terminals represent those taxa that show both inseminating and externally fertilized species. Body length data extracted from Reis et al. (2003). Genera belonging to each terminal extracted from Mirande (2010), as follows: Acestrorhynchinae (n = 15; ), Agoniatinae (n = 2; ), Aphyocharacinae (n = 20; , Inpaichthys Géry & Junk, , Paragoniates, Phenagoniates, , , and Xenagoniates), Aphyoditeinae (n = 21; , , , Leptobrycon, , Oxybrycon, , and ), clade (n = 31; Astyanax, , , , ), Astyanax paris clade (n = 1), Bramocharax clade (n = 18; Bramocharax and ), scleroparius clade (n = 10; Bryconamericus brevirostris, B. emperador, B. guaytarae, B. loisae, B. multiradiatus, B. peruanus, B. scleroparius, B. simus, B. terrabensis, B. zeteki), Bryconinae (n = 56; , , , Lignobrycon, and ), clade (n = 13; Bryconops), Characinae (n = 71; Acanthocharax, , Bryconexodon, , , Exodon, , , , , and ), Cheirodontinae (n = 48; Acinocheirodon, Amazonspinther, , , , , , , , †Megacheirodon, , , , , , , and ), (n = 14; , , , Rhaphiodon, and ), Gymnocharacinae (n = 4; , , Gymnocharacinus, and ), Heterocharacinae (n = 6; , , Hoplocharax, and Lonchogenys), Iguanodectinae (n = 11; and ), clade (n = 4; and Pseudochalceus), Rhoadsiinae (n = 7; , Nematocharax, Parastremma, and ), Salmininae (n = 3; ), Stevardiinae (n = 214; Acrobrycon, , , Aulixidens, , , Bryconadenos, Bryconamericus, Caiapobrycon, , , Corynopoma, , Cyanocharax, , , , , Hypobrycon, Hysteronotus, Iotabrycon, , Landonia, Lophiobrycon, , , Monotocheirodon, Nantis, Odontostoechus, Othonocheirodus, Phallobrycon, Phenacobrycon, , , , , , Ptychocharax, Rhinobrycon, Rhinopetitia, , , and Xenurobrycon), Tetragonopterinae (n = 252; Bario, , , , , , Hyphessobrycon, , , Myxiops, , Orthospinus, Petitella, , , , , Stichonodon, Tetragonopterus, and ).

Iheringia, Sér. Zool., Porto Alegre, 100(4):469-482, 30 de dezembro de 2010 Reproductive characteristics of characid fish species (Teleostei... 471

MALABARBA & WEITZMAN (2003) to include the Ceratobranchia Eigenmann, 1914, Creagrutus Günther, , the Stevardiinae and several characid 1864, Cyanocharax Malabarba & Weitzman, 2003, genera sharing four teeth in the inner series of the Hemibrycon Günther, 1864, Hypobrycon Malabarba & premaxilla and 2 unbranched plus 8 branched Malabarba, 1994, Microgenys Eigenmann, 1913, rays, was further supported by CALCAGNOTTO et al. (2005) Monotocheirodon Eigenmann & Pearson, 1924, Nantis and JAVONILLO et al. (2010), and later redefined and Mirande, Aguilera & Azpelicueta, 2006, Odontostoechus renamed as the Stevardiinae by MIRANDE (2009, 2010). Gomes, 1947, Othonocheirodus Myers, 1927, Throughout this paper I will continue to refer the lineage Phallobrycon Menezes, Ferreira & Netto-Ferreira, 2009, Clade A, which includes the tribes Corynopomini, Piabarchus Myers, 1928, Piabina Reinhardt, 1867, Diapomini, Glandulocaudini, Stevardiini, and Rhinobrycon Myers, 1944, and Rhinopetitia Géry, 1964. Xenurobryconini, and the genera Attonitus Vari & Ortega, I have included the species of the Serrasalminae in the 2000, Auxilidens Böhlke, 1952, Boehlkea Géry, 1966, comparisons, regardless the fact they have been Bryconacidnus Myers, 1929, Bryconadenos Weitzman, alternately referred as a subfamily (Serrasalminae – Menezes, Evers & Burns, 2005, Bryconamericus JAVONILLO et al., 2010) or as a different family from the Eigenmann, 1907, Caiapobrycon Malabarba & Vari, 2000, Characidae ( – MIRANDE, 2010).

Figure 2. Comparative plots of the body size for the species in each monophyletic group resulting in the phylogeny of Javonillo et al. (2010) expressed by Tukey box plots based on percentiles. Shaded portion of the cladogram represents those lineages sharing the lack of a supraorbital bone. Shaded terminals represent those taxa that show both inseminating and externally fertilized species. Body length data extracted from Reis et al. (2003). Genera belonging to each terminal, as follows: Acestrorhynchinae (n = 15; Acestrorhynchus), Aphyocharacinae (n = 20; Aphyocharax, Inpaichthys, Leptagoniates, Paragoniates, Phenagoniates, Prionobrama, Rachoviscus, and Xenagoniates), Brycon clade (n = 40), Bryconops clade (n = 13), Characinae (n = 70; Acanthocharax, Acestrocephalus, Bryconexodon, Charax, Cynopotamus, Galeocharax, Phenacogaster, Priocharax, Roeboexodon, and Roeboides), Cheirodontinae (n = 48; Acinocheirodon, Amazonspinther, Aphyocheirodon, Cheirodon, Cheirodontops, Compsura, Heterocheirodon, Kolpotocheirodon, Macropsobrycon, †Megacheirodon, Nanocheirodon, Odontostilbe, Prodontocharax, Pseudocheirodon, Saccoderma, Serrapinnus, and Spintherobolus), Clade C (n = 278; Astyanax, Ctenobrycon, Gymnocorymbus, Hasemania, Hemigrammus, Hollandichthys, Hyphessobrycon, Inpaichthys, Jupiaba, Macropsobrycon, Moenkhausia, Nematobrycon, Oligosarcus, Paracheirodon, Poptella, Pristella, Rachoviscus, Thayeria.), Exodon clade (n = 1), (n = 11; , Engraulisoma, , and ), Gnathocharax clade (n = 1), Salminus clade (n = 3), Serrasalminae (n = 68; , , Colossoma, , , , , Ossubtus, , , , Pygopristis, , , and ), Stevardiinae (n = 214; Acrobrycon, Argopleura, Attonitus, Aulixidens, Boehlkea, Bryconacidnus, Bryconadenos, Bryconamericus, Caiapobrycon, Ceratobranchia, Chrysobrycon, Corynopoma, Creagrutus, Cyanocharax, Diapoma, Gephyrocharax, Glandulocauda, Hemibrycon, Hypobrycon, Hysteronotus, Iotabrycon, Knodus, Landonia, Lophiobrycon, Microgenys, Mimagoniates, Monotocheirodon, Nantis, Odontostoechus, Othonocheirodus, Phallobrycon, Phenacobrycon, Piabarchus, Piabina, Planaltina, Pseudocorynopoma, Pterobrycon, Ptychocharax, Rhinobrycon, Rhinopetitia, Scopaeocharax, Tyttocharax, and Xenurobrycon), Tetragonopterinae (n = 2; Tetragonopterus), and Triportheus clade (n = 13).

Iheringia, Sér. Zool., Porto Alegre, 100(4):469-482, 30 de dezembro de 2010 472 AZEVEDO

Reproductive patterns among characid will apomorphic lack of a supraorbital and less than 40 be discussed following the classifications proposed vertebrae, that includes most of the small species of the above. Most characids are externally fertilized, but 69 family, with more than 82% reaching a maximum of 120 species are known to be inseminating, as listed by mm in length, and only about 17% exceeding this length. JAVONILLO et al. (2010). These include all species of the These include the Aphyocharacinae, Aphyoditeinae, tribes Corynopomini, Diapomini, Glandulocaudini, Characinae, Cheirodontinae, Heterocharacinae, Stevardiini, and Xenurobryconini (Clade A), all species Rhoadsiinae, Stethaprioninae, Stevardiinae (sensu of the tribe Compsurini (Cheirodontinae), and a several MIRANDE, 2010), and Tetragonopterinae (sensu stricto, species of uncertain affinities (Figs 1, 2). containing only Tetragonopterus). Thus, this framework allows us also to formulate the hypothesis that there was Body size reduction in Characidae one significant event of body size reduction (miniaturization) in the common ancestor of all species Neotropical freshwater fishes, one of the most sharing the apomorphic lack of a supraorbital and less diverse groups of on the planet, is dominated than 40 vertebrae. According the phylogeny of Mirande by the orders Siluriformes and Characiformes, which (2010), this general body size reduction may have occurred represent approximately 47% and 37%, respectively, of in a common ancestor including Bryconops Kner, 1858 the total number of freshwater species found in the and the Iguanodectinae (Fig. 1), but according to the tree Neotropics (REIS et al., 2003). According to CASTRO (1999), topology of Javonillo et al. (2010) the body size reduction approximately 50% of all Neotropical freshwater species in Bryconops occurred separately from the groups of Characiformes and Siluriformes exhibit small body size, mentioned above (Fig. 2). and many authors claim that smaller fish show reduced Although a number of these groups and small features such as a reduced number of scales, infraorbital species are found in small streams and rapids, many are bones, and fin rays (MYERS, 1958; FINK, 1981; WEITZMAN also found in open areas of larger rivers, backwaters, & VARI, 1988). CASTRO (1999) also reports that freshwater beaches, and lakes. Therefore, body size pedomorphosis (retention of characters of juveniles in reduction may also represent an adaptation to lentic adults) and progenesis (early gonadal maturation that environments, with physical and ecological truncates the ontogenetic process and produces an adult characteristics different from those typical of small that resembles the larval or juvenile stage in general streams, in such a way that we cannot unambiguously appearance and dimensions) are heterochronic processes associate body size reduction with an adaptation to related to reduction of body size, and that heterochronic stream environments, as suggested by CASTRO (1999). events are the main evolutionary processes responsible Although the characteristics of the small stream for faunal size reduction. environments seem more conducive to speciation and In reference to the fish fauna in South American vicariant events, only studies of biogeography, the streams, which are dominated by the small species of the phylogenetic relationships of these species, and the orders Characiformes and Siluriformes, CASTRO (1999) geological history of the waterways where they occur argues that the environments of these streams have will help identify which scenario produced the common exerted a series of selective pressures that favored the ancestor(s) of the small characid species. reduction in size of fish species. CASTRO (1999) also argues that this reduction has allowed for the best use of these Relationships between the reduction in body size and environments. In addition, the author hypothesizes that the biological characteristics of small fishes numerous vicariant events in these environments, associated with the low displacement capacity of these If we assume that a reduced body size is a fish, promoted events of allopatric speciation that were homologous evolutionary novelty that is shared by most responsible for the radiation of these species into streams. of the small sized characid species, one may pose the However, his hypothesis lacks examples and following question: what would be the adaptive phylogenetic support. advantages of a reduced body size for these fish, and In the order Characiformes, the smaller species are what are the secondary or collateral implications of this concentrated in the family Characidae, which is the most characteristic? speciose group of this order. Considering the total length One point raised by CASTRO (1999) and MOYLE & measurements for all species provided by REIS et al. (2003), CECH JR (1996) is that smaller species reach sexual maturity the following patterns of distribution of total length are more rapidly. CASTRO (1999) also states that variable and observed in Characidae. There is a series of basal lineages, ephemeral environmental conditions, such as those all sharing the plesiomorphic presence of a supraorbital found in streams, tend to favor the adaptive success of r- bone, that consist of the largest species of the family, strategist species, which are opportunists that are such as those in the genera Salminus Agassiz, 1829, characterized by their small size, short lifespan, high Brycon Müller & Troschel, 1844, Triportheus Cope, 1872 growth rate, early sexual maturity, elevated natural and the family Serrasalminae, with body lengths similar mortality and fecundity, and the ability to quickly occupy to most other characiform families (e.g., , new or reoccupy habitats whose fish populations , , and ) and were reduced or eliminated by regular or random abiotic reaching up to 1 m in length, and with about 82% environmental fluctuations. Although some studies can exceeding 120 mm in body length. There is also a large corroborate the existence of this pattern, the high internal clade, however, including all species sharing the diversity of the reproductive strategies that are adopted

Iheringia, Sér. Zool., Porto Alegre, 100(4):469-482, 30 de dezembro de 2010 Reproductive characteristics of characid fish species (Teleostei... 473 by different characid species and fish in general suggest generation time that usually coincides with the that there could be other, more complex, patterns that reproductive cycle and with large clutches and low levels have not yet been explored. It is indisputable, however, of care for the offspring. The opportunistic strategy is that in any type of environment, the smaller fish are able characterized by a short generation time, low fecundity, to occupy niches that are not available to the larger fish and minimum offspring care. According to the author, and that a reduced size could represent an adaptive the latter strategy is associated with small species that solution for some species. exhibit high rates of reproduction despite the apparent high mortality rate of young adults as a result of Reproductive biology of small characids unfavorable conditions and predation during the dry season. The opportunistic and seasonal strategies share In recent years, several studies on the reproduction many of the characteristics of a typical r-strategist of small characids have been conducted in different (PIANKA, 1970). drainage basins in the state of Rio Grande do Sul, Brazil Most characids studied by WINEMILLER (1989) (GELAIN et al., 1999; AZEVEDO, 2000; AZEVEDO et al., 2000; exhibited seasonal reproductive strategies with a OLIVEIRA et al., 2002; AZEVEDO, 2004; LAMPERT et al., 2004, reproductive period that lasted from one to three months 2007; GONÇALVES et al., 2005; OLIVEIRA et al., 2010; for the large species and from one to six months for the AZEVEDO et al., 2010). These studies, in addition to the smaller species. Some small characids species used an information synthesized by VAZZOLER & MENEZES (1992) opportunistic reproductive strategy, with the reproductive and VAZZOLER (1996), and those presented by KRAMER period varying between 10 and 12 months. Other small (1978), WINEMILLER (1989) and MENI & ALMIRÓN (1994) species used reproductive strategies exhibiting provide a set of reproductive data for a large number of opportunistic/seasonal characteristics, with reproductive characid species. Many of these species were of a smaller periods lasting between five and eight months. size and were residing in different environments. Despite KRAMER (1978) studied the reproductive the limited amount information, these data allow us to characteristics of six characid species in Panama and draw a general conclusion about the evolution of characid discussed the influence of seasonality on the time and reproductive traits, the involved phylogenetic aspects, duration of the breeding and spawning periods. He and the relationship between these characteristics and a presents five hypotheses to explain which factors reduced body size. determine the time and duration of the breeding period: VAZZOLER & MENEZES (1992) analyzed the data that 1) the reproductive period is controlled by the availability were available in the literature about the reproduction of of food for the young and adults; 2) the reproductive South American characiform species. In this study they period is controlled by interspecific competition among evaluated the following reproductive tactics: spawning the young for food; 3) the reproductive period is period, fecundity, type of spawning, and rate of first controlled by competition for breeding locations; 4) the gonadal maturation. The species were separated reproductive period is a mechanism of reproductive according to the large basins in which they were studied isolation; and 5) the reproductive period is not related to and according to the respective reproductive strategies. local conditions but was related to the evolution of Analyzing the data reported by VAZZOLER & MENEZES previously primitive reproductive specializations and to (1992), I observed that all characid species reproduced those specialization that limit a species to spawning under seasonally during the spring and summer, independent particular conditions. of size, reproductive strategy, and location, with variations In terms of the last hypothesis, KRAMER (1978) in reproductive period lengths. The establishment of the argues that the seasonality of reproduction may be a reproductive period of these characiform species during characteristic with a strong phylogenetic inertia. He also the spring and summer months was attributed to both states that body size may be another factor that is the increase in temperature and level of rainfall. In both involved in reproduction, and that there is a tendency cases, the climatic and environmental conditions during for smaller species to have long reproductive periods. this time period favored the development of larvae. According to the author, smaller species, which do not However, correlations between the reproductive have proportionally reduced ova [oocyte size] must have characteristics and body size or phylogenetic reduced fecundity unless able to produce multiple relationships were not discussed in this work. clutches within a season. WINEMILLER (1989) provided data on the life history MENNI & ALMIRÓN (1994) evaluated the reproductive and reproduction of roughly 72 freshwater fish species period of fourteen fish species in , eight of from various drainages in Venezuela, including 24 which were characids. The authors also identified three characid species, characterizing three reproductive distinct species groups that were based on the duration strategies: equilibrium, opportunistic and seasonal. In of spawning or according to the presence of spawning the equilibrium strategy, generation time is intermediate specimens: 1) species that spawned throughout most or or long, there is a large investment in individual offspring, all of the year; 2) species that did not during the maturation is delayed, reproduction is aseasonal and winter, avoiding temperatures lower than 20ºC, and 3) breeding prolonged. According WINEMILLER (1989), to species with short spawning periods that were restricted some extent these life history traits agree with the relative to the last months of the winter or spring, spawning “K-strategy” as originally proposed by PIANKA (1970). during the time when the temperature varied between The seasonal strategy is characterized by reproduction minimum and maximum values. In all three groups, small that is cyclical and annual, with a relatively long characid species were present.

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Studies conducted on the reproduction of small fecundity and body size (rPearson)=-0,6280; p<0,0162) (Fig. characids in southern Brazil evaluated reproductive 16). These data indicate that, whereas larger species may characteristics, such as the timing and duration of the increase the absolute number of oocytes produced, the reproductive period, absolute and relative fecundity, relative fecundity, which represents the average number spawning mode and diameter of mature oocytes. These of oocytes per gram of body weight, actually decreases as studies included species of inseminating characids body size increases, suggesting that the smaller species distributed in different groups within the family. In some may actually spend more energy on individual oocyte cases, it was possible to establish correlations between production. Available oocyte diameter measurements for 15 certain reproductive characteristics and phylogenetic species show a significant correlation between oocyte relationships of these same species. Some results for diameter and body size (rPearson)=0,6484; p<0,0121) (Fig. 17). species of Cheirodontinae in northeastern Brazil are also informative. Based on the data compiled here (Tab. I), it is possible to detect some general patterns in characid reproduction. More than 90% of the characid species that have the supraorbital bone, which are named the “large species,” reproduce seasonally (Fig. 3). For the species lacking a supraorbital bone, which are named the “small species,” over 80% reproduce seasonally, and approximately 18% show some variation of this pattern (Fig. 4). Over 50% of the large species have a reproductive period that is restricted to one, two, or three months, approximately 30% reproduce for four to six months, and only about 8% prolong reproduction for up to seven or eight months (Fig. 5). For the small species, just over 15% restrict reproduction to three months, more than 50% reproduce in four to six months, and more than 20% extend the reproductive period beyond six months. Approximately 13% of the small species reproduce for ten to twelve months (Fig. 6). For the large species, roughly 70% reproduce between the months of September and April, and only 8% also reproduce in other months (Fig. 7). For the small species, about 36% reproduce between September and April, and 33.3% are found to reproduce in other months (Fig. 8). Figures 3, 4. Relative frequencies (%) of species showing seasonal, The absolute fecundity of the large species varies opportunistic or continuous reproductive strategies in large (3) from 100 to 500,000 oocytes, and that of small species and small size (4) characid species. Source data given in Table I. varies from 94 to 10,000 oocytes. Approximately 27% of “?” means unknown. the large species produce more than 5,000 oocytes, 19% produce between 2,500 and 5,000 oocytes, and only two species produce between 100 and 400 oocytes (Fig. 9). For the small species, only 11% produce more than 5,000 oocytes, and the same percentage produces 1,000 to 5,000 oocytes. Approximately 21% of these species produce 500 to 1,000 oocytes, and more than 36% produce from 90 to 500 oocytes (Fig. 10). Of the large species that produce an extremely high number of oocytes (more than 5,000), more than 57% of these do not provide offspring care (Fig. 11), and more than 42% migrate (Fig. 12). Of the smaller species that produce up to 500 oocytes, 50% are inseminated (Fig. 13), and within those that produce up to 1,000 oocytes, more than 43% break up spawning events or have more than one courtship during the breeding period (Fig. 14). The four smaller species that produce between 3,000 and 9,500 oocytes are above 80 mm in standard length. The other species, which produce a maximum of approximately 1,000 oocytes, are between 28 and 69 mm in length. There is a statistically significant positive Figures 5, 6. Relative frequencies (%) of species showing different correlation between absolute fecundity and body size reproductive period lengths (months) in large (5) and small size (rPearson)=0,7074; p<0,0001) (Fig. 15). Moreover, there is (6) characid species. Source data given in Table I. “?” means also a significant negative correlation between relative unknown.

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(2003). The (2003). ENEZES ENEZES ENEZES ENEZES ENEZES ENEZES ENEZES ENEZES ENEZES ENEZES ENEZES ENEZES Data source Data , 1978 & M & M & M & M & M & M & M & M & M & M & M & M & M et al. RAMER AZZOLER AZZOLER AZZOLER AZZOLER AZZOLER AZZOLER AZZOLER AZZOLER AZZOLER AZZOLER AZZOLER AZZOLER AZZOLER INEMILLER INEMILLER INEMILLER V V V V EIS AZZOLER AZZOLER AZZOLER AZZOLER AZZOLER AZZOLER AZZOLER AZZOLER AZZOLER AZZOLER AZZOLER AZZOLER AZZOLER

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migration, Parental care, Parental parental careparental careparental care V V V parental care V parental care V parental care V parental care non-migratory, V non-migratory, V non-migratory, V

with parental care V migratory, withoutmigratory, V migratory, withoutmigratory, V withoutmigratory, without V migratory, V without migratory, migratory, withoutmigratory, V

without parental care V without parental care V

maturation Length of 1ª of Length

130 without migratory, V 306- 210- 320-

oocytes (mm) oocytes Size of mature of Size 1.6- K

from the reference given for each species or R Spawning total total 1.9 total 1.5 251 total 156 total total

multiple multiple multiple

apparently W apparently apparently

body weight) body

(nº oocytes/mg (nº

Relative fecundity Relative

(nº oocytes) (nº Total fecundity Total

4,303 apparently3,048 apparently W W 2,600 total 1.3

52,000 36,700– 171,545 100,000 309,290 325 427,000 25,500–

(months) Length reproduction Length

and 2 and 2 and 2 and 2 Time of year of Time January January 411 January 230 February February 2

October to 3 60,000 – October to 4

February and 2 November to 4 100 September to 8 98- November to 5 November to 5

seasonality Reproductive

seasonal seasonal seasonal

Size difference ( difference Size ) /

of species (mm) species of Maximum length Maximum (1992) were compiled from several publications by those authors. 220 seasonal December 313 seasonal 1 995 500,000 V 350625156 seasonal females seasonal200 December 250710 seasonal405 November and seasonal 2 seasonal 500147 seasonal December seasonal 400,000 3 V 300 seasonal December ENEZES & M = 248 seasonal 3 = 1000 = 221 seasonal AZZOLER = 776 seasonal TAXONS melanopterus cf. SPECIES WITH SUPRAORBITAL BONE SPECIES WITH SUPRAORBITAL Brycon cephalus Meek & Hildebrand, 1913B. whitei larger and March S. brasiliensis Myers & Weitzman, 1960 Weitzman, Myers & Colossoma macropomum (Humboldt 1821) Salminus brevidens Peters, 1877 S. marginatus data from V (Agassiz, 1829)(Cuvier, 1818)(Jardine 1841) December March March (Günther, 1869)(Cope, 1872) 1850)(Valenciennes, January (Cuvier, 1818) (Holmberg, 1887) January (Cuvier, 1816) S. brasiliensis 1837Valenciennes, December April 116 (Cuvier, 1818) Table I. Summary of published data about reproductive traits and life history characid species. Maximum length was extracted Table B. henni B. B. orbignianus B. petrosus Milossoma aureum M. duriventris Myleus mesopotamicus P. Pygocentrus notatus S. hilarii 1850 Valenciennes, S. maxilosus (Cuvier, 1816) Serrasalmus irritans Eigenmann, 1913 November

Iheringia, Sér. Zool., Porto Alegre, 100(4):469-482, 30 de dezembro de 2010 476 AZEVEDO , 1992 , 1992; , 1992; , 1992; , 1992; , 1992; , 1992; , 1992; , 1992; , 1992; , 1992; , 1992; , 1994 , 1994 , 2005 , 1989 , 1989 , 1989 , 1989 , 1989 , 1989 , 1989 , 1989 , 1996 , 1996 , 1996 , 1996 , 1996 , 1996 , 1996 , 1996 , 1996 , 1996 , 1996 , 1996 ENEZES ENEZES ENEZES ENEZES ENEZES ENEZES ENEZES ENEZES ENEZES ENEZES ENEZES ENEZES et al.

LMIRÓN LMIRÓN & M & M & M & M & M & M & M & M & M & M & M & M & A & & A AZZOLER AZZOLER AZZOLER AZZOLER AZZOLER AZZOLER AZZOLER AZZOLER AZZOLER AZZOLER AZZOLER AZZOLER INEMILLER INEMILLER INEMILLER INEMILLER INEMILLER INEMILLER INEMILLER INEMILLER V V V W ONÇALVES ENNI ENNI AZZOLER AZZOLER M M AZZOLER AZZOLER AZZOLER AZZOLER AZZOLER AZZOLER AZZOLER AZZOLER AZZOLER AZZOLER azzoler & Menezes, 1992; V V V parental care V parental care V non-migratory, V non-migratory, V non-migratory, V non-migratory, V non-migratory, V non-migratory, V non-migratory, V with parental care V with parental care V migratory, withoutmigratory, V without parental care V without parental care V without parental care V without parental care V 124- 108- 60-78 17 V 0.78 52 0.77 total total total 41 multiple multiple multiple multiple multiple multiple multiple apparently W apparently W apparently W 0.68 G 300 600– 600– 300– 3,048 apparently W 8,400 apparently W 344.8 9,528 7,800 4,303 apparently3,175 apparently4,287 W W 10,000 3,200 April 138 with parental care V to May November 6 January to 6 multiple November 7 October to 4 October to 7 and autumn and February November to 6 November toSeptember to 5 5 400 September to 7 150 without migratory, V seasonal 6 280 seasonal September 6 seasonal October and about 7 seasonal spring, much larger December larger of the summer females females 9 2 seasonal 1 3 7 seasonal 3 617 6 9 seasonal 46 9 1 seasonal85 females 2 6 4 seasonal 1 800 140 seasonal 3 132 seasonal 190 seasonal 106 seasonal 333 seasonal 106 seasonal 1 195210151 seasonal163242 seasonal seasonal seasonal December 3 seasonal 1195 seasonal 120 66.3 1125 , 1903 January 1858 April Pygocentrus A. dentatus 1903 larger sp. 120 seasonal 2 = Eigenmann 32.31 = Kner, Tab. I (cont.) Tab. S. medinai A. integer A. fasciatus Ramírez, 1965 S. nattereri (Linnaeus, 1766) S. serrulatus BONE SUPRAORBITAL SPECIES WITHOUT Aphyocharax alburnus (Günther, 1869) A. anisitsi Myers, 1930 A. metae A. schubarti Myers, 1942 Charax gibbosus (Linnaeus, 1758) Eigenmann, 1914 A. metae A. difficilis & Kennedy, & Kennedy, Eigenmann & Kennedy (Linnaeus, 1758)(Cuvier, 1819) March Britski, 1964April to to May nattereri 1850Valenciennes, Kner, 1858 Cope, 1872 Agassiz, 1829)(Spix & Aphyocharax dentatus June March 127 (Günther, 1864) January S. rhombeus S. spilopleura albus Triportheus angulatus T. elongatus T. Triportheus A. nasutus = Eigenmann & Kennedy 1903 Astyanax bimaculatus A. bimaculatus A. eigenmanniorum (Cope, 1894) A fasciatus A. superbus

Iheringia, Sér. Zool., Porto Alegre, 100(4):469-482, 30 de dezembro de 2010 Reproductive characteristics of characid fish species (Teleostei... 477 , 1992; , 1992; , 1992; , 1992; , 1992; , 1992; , 1992; , 1992; , 1992; , 1992; , 1994 , 1994 2002 , 2010 , 1989 , 1989 , 1989 , 1989 , 1989 , 1996 , 1996 , 1996 , 1996 , 1996 , 1996 , 1996 , 1996 , 1996 , 1996; ENEZES ENEZES ENEZES ENEZES ENEZES ENEZES ENEZES ENEZES ENEZES ENEZES , 1978 , 1978 , 1978 , 1978 et al. LMIRÓN LMIRÓN et al.

& M & M & M & M & M & M & M & M & M & M RAMER RAMER RAMER RAMER & A & A & AZZOLER AZZOLER AZZOLER AZZOLER AZZOLER AZZOLER AZZOLER AZZOLER AZZOLER INEMILLER INEMILLER INEMILLER AZZOLER INEMILLER INEMILLER K V V V V V LIVEIRA LIVEIRA ENNI ENNI M M AZZOLER AZZOLER AZZOLER AZZOLER AZZOLER AZZOLER AZZOLER AZZOLER AZZOLER AZZOLER V V non-migratory, V non-migratory,non-migratory, V V with parental care V without parental care V without parental care V without parental care V 0.7-0.8 K 1.2-1.5 K 0.85-1.0 K total total total total V multiple 0.7 5 5 multiple multiple multiple multiple 0.9multiple 3 7 V O apparently W apparently W apparently apparently W 0.71 O 3,398 apparently1,108 apparently W V 3,398 apparently W 500 non-migratory, V June months summer summer summer pring and 6 513 0.5 February Spring and November 8 November late winter, 8 400 January and rainy season and February December to 3 1.1 9 6 V November to 6 September to 4 November to 6 145 September and 4 722 March and April March and January seasonal seasonal seasonal s seasonal seasonal seasonal seasonal October to 4 males seasonal larger larger April larger October, January larger larger spring and females females females seasonal ? seasonal October and 2 41 females 45 100 95 sazonal October to 6 8 3 seasonal2 8 1 to 2 seasonal 2 56 females 109 opportunistic 12 to 7 280 104 400 V 580 seasonal 2 to 3 755 141 males seasonal 880 seasonal 933 seasonal130 2 non-seasonal every 12 61.4 44.6 2222 103.2 44.97 1844) 240 seasonal sp. 33 opportunistic/ 8 to 7 282 Ringuelet, larger December Tab. I (cont.) Tab. C. stenopterus Cheirodon interruptus Eigenmann, 1915 R. dayi meridionalis Miquelarena & Menni, 1978 H. panamensis Durbin, 1908 Markiana geayi Gill, 1877Pristella maxillaris (Günther, 1864) larger (Steindachner, 1882) (Cope, 1894) panamensis (Valenciennes, 1850) (Valenciennes, Galeocharax knerii Hyphessobrycon Moenkhausia intermedia (Steindachner, 1878) R. paranensis (Cuvier, 1816) CHEIRODONTINAE Cheirodon ibicuhiensis (Steindachner, 1879) 1894) (Ulrey, (Jenyns, 1842) (Pellegrin, 1908) Eigenmann, 1908(Müller & Troschel, (Günther, 1864) Pignalberi, 1975 to Serrapinnus piaba Schultz, 1944 March Cheirodon piaba = Hemigrammus M. geayi asterias Oligosarcus jenynsii Roeboides guatemalensis argenteus Tetragonopterus (Lütken, 1875) Cheirodontops geayi Odontostilbe pequira

Iheringia, Sér. Zool., Porto Alegre, 100(4):469-482, 30 de dezembro de 2010 478 AZEVEDO , 1994 , 2010 , 2000 , 2010 , 2007 , 2007 , 2003 , 1999 , 2007 , 1989 , 1989 , 1989 , 1989 , 1989 , 1989 , 2004 , 2004 , 2004 , 1978 , 1978 LMIRÓN et al. et al. et al. et al. et al. et al. et al.

et al.

RAMER RAMER ZEVEDO ZEVEDO ZEVEDO & A & INEMILLER INEMILLER INEMILLER INEMILLER INEMILLER INEMILLER ELAIN ERRIS ILVANO LIVEIRA ZEVEDO ZEVEDO AMPERT AMPERT ENNI Filipe Melo, comm. pes.; Carlos Machado, comm. pes. inseminating O inseminating A inseminating W inseminating A inseminating W inseminating A inseminating K inseminating A inseminating A inseminating inseminating F inseminating M 26-36.5 0.6711 24 0.7-0.8 1.2-1.5 K al 0.8375 multiple G multiple multiple multiple multiple multiple multiple apparently apparently W apparently apparently W apparently W 0.55 0.36 L 0.35 L 0.27 0.356 0.565 tot 0.539 total 0.631 0.507 0.4101 0.3412 1,108 apparently W 371.3 491.1 421.05 322.63 933.71 191.08 109.33 1286.42 ) ) and) 441 0.74 S about 6 980 about 10 135 ) ) 12( ust to 4 January winter season January 4 434 months months months months summer summer summer April ( spring and spring and 4 spring and 4 spring and 4 406 November every year October to 5 months ( cold months early autumn )/ January to( 4 ) every and ( seasonal seasonal Aug seasonal seasonal September 5 seasonal seasonal autumn and 4 seasonal seasonal seasonal seasonal seasonal seasonal late winter about 6 continuous seasonal ( non-seasonal every continuous non-seasonal continuous larger larger larger larger every larger larger larger to April largerlarger to February larger larger larger females females females females females females females 3 6 seasonal 5 43 opportunistic almost 44 opportunistic every 12 796 37 opportunistic/ 5 734 53 males non-seasonal every 12 46 females 3 97 6 males seasonal seasonal dry 6 243 67.5 52.6 males 66.3 40.2 males 48.7 68.9 34.14 54.85 males 54.58 34.04 30.18 1907) eitzman, 1990 sp. 28 opportunistic/ 6 94 Tab. I (cont.) Tab. O. pulcher = COMPSURINI Compsura heterura STEVARDIINAE D. terofali (Steindachner, 1876) Mimagoniates rheocharis W Menezes & 1964) (Géry, CLADE A B. beta D. terofali uruguayanae Eigenmann, 1915 Cope, 1894 B. iheringii valencia G. (Eigenmann & Ogle, Meek & Hildebrand, 1912 larger Eigenmann, 1915 Macropsobrycon (Boulenger, 1887) Bryconamericus stramineus Eigenmann, 1908 Creagrutus Gephyrocharax atracaudata (Lütken, 1875) Serrapinus piaba (Boulenger, 1900) GLANDULOCAUDINAE M. microlepis Diapoma speculiferum Pseudocorynopoma doriae Odontostilbe pulchra (Gill, 1858) Serrapinnus calliurus Eigenmann, 1914 B. deuterodonoides Eigenmann, 1914 B. emperador Gill, 1858 Eigenmann, 1920 Perugia, 1891 doriae P.

Iheringia, Sér. Zool., Porto Alegre, 100(4):469-482, 30 de dezembro de 2010 Reproductive characteristics of characid fish species (Teleostei... 479

Figures 11, 12. Relative frequencies (%) of parental care (11) and Figures 7, 8. Relative frequencies (%) of species with the migratory behavior (12) in large size characid species with high reproductive period lasting between September and April, and of fecundity (more than 5,000 oocytes). Source data given in Table I. species showing reproductive activity outside this period, in large “?” means unknown. (7) and small size (8) characid species. Source data given in Table I. “?” means unknown.

Figures 13, 14. Relative frequencies (%) of insemination and external fertilization in species with absolute fecundity up to 500 Figures 9, 10. Relative frequencies (%) of species per absolute oocytes (13) and of species showing complete or partial spawning fecundity classes in large (7) and small size (8) characid species. with absolute fecundity up to 1000 oocytes (14). Source data given Source data given in Table I. “?” means unknown. in Table I. “?” means unknown.

In one of these species, however, the average diameter formulate some initial hypotheses about the reproductive of the oocytes is the largest observed, regardless of its characteristics of the family Characidae that can be further small body size (Fig. 17 - B. emperador (Eigenmann & tested as more data are accumulated in the future. Ogle, 1907)). This particular case suggests that this 1) Characid species sharing a supraorbital bone species compensates the low oocyte production by tend to be larger than those without a supraorbital bone. increasing the diameter of the oocytes. A larger size is also observed in the majority of the species from the other characiform families. Interpretations of the patterns of reproduction of 2) Most of the species with a supraorbital bone characid species have a general reproductive pattern that is characterized by a short seasonal reproductive season that lasts from In spite of the fact that these data represent a very one to three months and that rarely exceeds six months. limited number of characid species, and that possible Reproduction in these species normally occurs between errors in data analysis or species identification by the September and April. Spawning in these species is researchers may have occurred, it is still possible to generally complete, their absolute fecundity can be

Iheringia, Sér. Zool., Porto Alegre, 100(4):469-482, 30 de dezembro de 2010 480 AZEVEDO extremely high, and several species are migratory. Many of the oocytes (maximizing offspring survival), multiple species with lower fecundity present some form of spawning to produce several batches of oocytes in one parental care, providing a higher chance for and larval breeding season, extended reproductive periods, the survival. presence of more than one reproductive cohort during 3) There may have been a single event of body size the year or continuous reproduction, high growth and reduction (miniaturization) in the common ancestor of all recruitment rates (quickly increasing sexually active characid species that share the apomorphic lack of a population), the insemination and all of the morphological, supraorbital and less than 40 vertebrae. Body size physiological, and behavioral adaptations known to exist reduction may have independently appeared in other for inseminating species (see BURNS & WEITZMAN, 2005). lineages of Characiformes, as for example the Similar selective pressures may lead to the emergence of , Gasteropelecidae, and . Size these independent adaptations in different lineages of reduction possibly represented an adaptive advantage small characids and at different times in evolutionary in several aspects related to the occupation of new history. environments and niches, but can, moreover, have Some specific trends are observed in Clade A required new evolutionary responses to new biological species, particularly in the inseminating species. The problems arising. majority of species belonging to Clade A, and particularly 4) In terms of reproduction, the most direct the inseminating species, have lower relative fecundity consequence of a reduced body size is the reduction of values than other characid species (data available only the absolute number of oocytes produced by smaller to small size species, Fig. 16). Among small size species, species. lower relative fecundity values may be associated with 5) Many small characid species retain some or most the presence and efficiency of insemination. In the same of the reproductive traits of the larger species, with a manner, some species considered to be highly adapted seasonal reproductive period between September and to the mode of insemination, such as the genera April, a relatively high fecundity, and total spawning. Mimagoniates Regan, 1907 and Pseudocorynopoma However, many of these species, especially those Perugia, 1891, are able to reproduce during a major part belonging to Clade A (sensu MALABARBA & WEITZMAN, of the year or during months outside of spring and summer 2003), exhibit changes in this reproductive pattern, such (Tab. I), which may represent an adaptation related to the as extended reproductive period, reproducing during the efficiency of insemination. Protracted reproduction may colder months, reduced fecundity, and multiple spawning. also have arisen independently in other inseminating These changes are possibly in response to a decrease in characid lineages. size and subsequent decrease in fecundity. Large species have oocytes with diameters that 6) The following changes in the general are larger than those of smaller species (Fig. 17). Among reproductive patterns of characiforms are found in small the smaller species, however, the oocyte diameter varies species and may constitute novelties in response to very little. For example, Diapoma terofali (Géry, 1964) environmental pressures that are related to the reduction (Stevardiinae) engages in insemination and has low of body size and fecundity: size reduction of mature absolute fecundity, but the diameter of the oocytes is oocytes (increasing fecundity) or an increase in the size very similar to that of the other small species that are externally fertilizing and with higher fecundity (AZEVEDO, 2004). However, the inseminating cheirodontine, Macropsobrycon uruguayanae Eigenmann, 1915, has a reduced oocyte diameter and a high relative fecundity (AZEVEDO et al., 2010). The decrease in oocyte size in M. uruguayanae does not seem to be present in the inseminating Stevardiinae species, suggesting that the reproductive traits of both groups have evolved under different selective pressures. This finding supports the hypothesis that insemination has independent origins in both groups (BURNS et al., 1995, 1997, 1998; AZEVEDO, 2004; WEITZMAN et al., 2005).

Figures 15, 16. Scatter plot of absolute fecundity (15) and relative fecundity (16) versus body length in small characid species. Source Figure 17. Scatter plot of oocyte diameter versus body length in data given in Table I. “?” means unknown. characid species. Source data given in Table I. “?” means unknown.

Iheringia, Sér. Zool., Porto Alegre, 100(4):469-482, 30 de dezembro de 2010 Reproductive characteristics of characid fish species (Teleostei... 481

Although the information from the literature that Reproductive biology of Pseudocorynopoma doriai (Pisces: was compiled in this study represent an advance in Characidae) in the High Basin of the Samborombón River, province of Buenos Aires, Argentina. Journal of Applied studies on reproductive strategies of characid species, Ichthyology 23(3):226-230. the available data are extremely fragmented and represent FINK, W. L. 1981. Ontogeny and Phylogeny of tooth attachment only some aspects of reproduction for a limited number modes in Actinopterygian fishes. Journal of Morphology of species. Further research aiming to test the hypotheses 167:167-184. and trends reported in the present study are required. The GELAIN D.; FIALHO, C. B. & MALABARBA, L. R. 1999. 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Recebido em dezembro de 2010. Aceito em dezembro de 2010. ISSN 0073-4721 Artigo disponível em: www.scielo.br/isz Impresso e distribuído em 2011.

Iheringia, Sér. Zool., Porto Alegre, 100(4):469-482, 30 de dezembro de 2010