Vol. 28: 45–53, 2019 AQUATIC BIOLOGY Published May 2 https://doi.org/10.3354/ab00706 Aquat Biol

OPENPEN ACCESSCCESS Reproductive biology of the armored microps in a coastal Atlantic Forest stream, southeastern Brazil

Víctor de Carvalho Alves1,2,*, Marcelo Fulgêncio Guedes Brito3, Erica Pellegrini Caramaschi1

1Laboratório de Ecologia de Peixes, Departamento de Ecologia, Universidade Federal do Rio de Janeiro, 21941-902 Rio de Janeiro, RJ, Brazil 2Fundação Instituto de Pesca do Estado do Rio de Janeiro, 24030-020 Niterói, RJ, Brazil 3Programa de Pós-Graduação em Ecologia e Conservação, Universidade Federal de Sergipe, 49100-000 Sergipe, SE, Brazil

ABSTRACT: This work aims to analyze reproductive attributes of the Neoplecostomus mi- crops (Steindachner, 1877), a well-known species of the catfish family but little con- templated in ecological studies. We describe the reproductive behavior of the species and compare the patterns identified in 2 different basins. The specimens (117 males and 102 females), collected in the Macaé River, did not present a bias in sex ratio during the year. In the largest length classes, males predominated and attained earlier maturity than females. The length−weight relationship showed positive allometric growth for both sexes. The variation of the gonadosomatic index and frequency of maturation stages indicated a reproductive period of 4 to 6 mo, starting in September and reaching a peak in November. The mean absolute fecundity was 43.83 (SD = 7.62) oocytes, ranging from 32 to 55 oocytes. The frequency distribution of oocyte diameter of mature ovaries revealed 3 clutches, suggesting batch spawning. A prolonged reproductive period, low fecundity, large eggs, possible parental care, and repeated spawns recorded for N. microps suggest a strategy that maximizes parental fitness. The population structure and reproductive characteristics of this species indicate a tendency toward equilibrium. The early maturation in females in the Macaé River population may favor a more rapid replacement of juveniles in the population as a response to the unstable environmental conditions that the population experiences in the rainy season.

KEY WORDS: · Armored catfish · Reproductive biology · Atlantic forest stream · Macaé River

1. INTRODUCTION and digestive processes to exploit sediment and de- bris, wood rasping, and periphyton (Schaefer & Loricariid are important components of the Lauder 1986, Delariva & Agostinho 2001). Loricariids stream ichthyofauna (Buckup 1999) throughout most have a large diversity of reproductive strategies (func- of the Neotropics (Ferraris 2003a). Their representa- tional diversity); there are species with complete tives typically inhabit lotic environments (Sterba & absence of parental care, males that carry adhesive Mills 1983, Sakurai et al. 1993) and consume algae eggs and larvae on the ventral surface, and species and detritus (Flecker 1992, Power 1984). Distinct from with nest protection (Suzuki et al. 2000). other groups, the dispersion of the family occurs Species of the Neoplecostomus are dis - almost exclusively at the primary trophic level, with tributed in rivers and streams in south-central Brazil adaptations involving morphology, feeding behavior, (Ferraris 2003b, Buckup 2007, Zawadzki et al. 2008).

© The authors 2019. Open Access under Creative Commons by *Corresponding author: [email protected] Attribution Licence. Use, distribution and reproduction are un - restricted. Authors and original publication must be credited. Publisher: Inter-Research · www.int-res.com 46 Aquat Biol 28: 45–53, 2019

The genus comprises 17 species (Eschmeyer et al. stretches of the river using a rectangular frame net 2016), and little is known of their biology and ecol- (1.5 × 1 m; 5 mm mesh), with a standardized effort of ogy. Neoplecostomus microps occurs in the Paraíba 10 bins at each of the sampling points (Brito et al. do Sul basin (Langeani 1990, Bizerril 1995) and adja- 2016). Samples were taken every 2 mo, between cent coastal rivers (Buckup 2007), in fast-flowing March 2004 and March 2005, at the middle course of stretches with stones and boulders (Brito et al. 2016). the Macaé River. The specimens were fixed in 10% Recently, studies on distribution pattern, sexual formalin and later transferred to 70% ethanol. In the dimorphism, nesting sites, and some reproductive laboratory, the specimens were measured, weighed, attributes were published for populations in the and sexed, and the reproductive stages were classi- Paraíba do Sul and Macaé River basins (Braga et al. fied. 2008, Brito et al. 2016). Voucher specimens were deposited in the fish col- The limited number of reports on reproduction of lection of the Museu Nacional do Rio de Janeiro small loricariid catfishes from creeks and streams is (MNRJ 39018). due to sampling difficulties for these studies. In this study, we analyzed the population structure and reproduction characteristics of N. microps in a rocky 2.3. Population structure analysis and forested coastal stream of the state of Rio de Janeiro, Brazil. We focused on population length For each specimen, the standard length (Ls) was structure, length−weight relationship, macroscopic recorded. Standard length structure analyses were characteristics of gonads, reproductive period, size at determined from the number of individuals in differ- first gonad maturation, and fecundity. ent size classes. The classes were established with 0.5 cm intervals. The length−weight relationship, b Wt = aLs , where Wt = total weight, Ls = standard 2. MATERIALS AND METHODS length, a = intercept, and b = isometric coefficient,

was log transformed to Wt = log a + log b × Ls 2.1. Study site (Lleonart et al. 2000). Relationships between stan- dard length and weight were determined by linear We sampled the Macaé River (22° 21’−22° 28’ S and regression. The 95% confidence limits for b were cal- 42° 27’−42° 35’ W), a 110 km long coastal stream culated to determine whether the hypothetical value located in Rio de Janeiro State, south - eastern Brazil. This is a medium- sized river located on the coastal slope of the Serra do Mar. This basin has dense drainage, is located in a humid tropical region, and is sur- rounded by Atlantic Forest vegeta- tion. The headwaters lie between 810 and 1090 m above sea level. The upper and middle courses of the Macaé River and its tributaries are dominated by rapids and waterfalls, with stony beds between sandy pools (Brito 2007). During the study period, the highest rain fall values occurred from November to March.

2.2. Sampling

Specimens of Neoplecostomus mi- crops were collected in rapids at 8 sites (Fig. 1) equally distributed Fig. 1. Sampling sites for Neoplecostomus microps in Macaé River basin, Rio de throughout the upper and middle Janeiro State, southeastern Brazil Carvalho Alves et al.: Reproductive biology of Neoplecostomus microps 47

of isometry (3) fell within these limits (Froese 2006). rainfall values were checked using Shapiro-Wilks In all cases, a significance level (α) of 5% was and Bartlett’s tests to verify normality and homo- adopted. The significance of the regression was tested scedasticity of the data. As these specific conditions by ANOVA to check whether the calculated value of were not satisfied, non-parametric Kruskal-Wallis b is significantly different from 3 (isometric value). analysis of variance followed by the Dunn post hoc test was applied to identify the months that GSI val- ues differed. The non-parametric Spearman’s rank 2.4. Sex and reproductive analysis correlation test was applied between GSI variation and rainfall values to verify possible relationships. For each specimen, the total weight (Wt), gonad For male and female tests, a significance level of 0.05 weight (Wg), sex, and reproductive stage were re - was applied (males: Spearman’s = −0.202, p = 0.281; corded. Sex and reproductive stage were categorized females: Spearman’s = −0.119, p = 0.231). The soft- according to macroscopic features, including color, ware used was BioEstat 5.0 (Ayres et al. 2007). presence of blood vessels, presence of oocytes, and size of the gonad (Vazzoler 1996). The reproductive stages were defined as immature, maturing, mature, 3. RESULTS partially spent, spent, and resting for males and immature, maturing, mature, partially spawned, 3.1. Population structure spawned, and resting for females, according to the macroscopic scale suggested by Núñez & Dupon- A total of 219 specimens of Neoplecostomus mi- chelle (2009), with 5 or 6 stages. The macroscopic cri- crops were captured, including 117 males and 102 teria used in this study were similar to other loricari- females. Standard length ranged from 3.2 to 9.7 cm ids (Agostinho et al. 1991, Menezes & Caramaschi for males and 3.5 to 8.0 cm for females; males were 1994, Dei Tos et al. 1997, Mazzoni & Caramaschi larger than females (Fig. 2). 1997, Guimarães-Cruz et al. 2005), with 6 stages of The sex ratio did not differ from 1:1 (df = 1; χ2 = gonad maturity for both sexes. Reproductive aspects 1.027; p = 0.310), considering months and localities of the N. microps population were characterized by grouped in total, despite the slight predominance of the following: reproductive period, size at first gonad males over females. Considering sex ratio in the maturation, macroscopic analysis of gonads, and different localities, no significant differences were fecundity. The reproductive period was determined observed (all cases: df = 1; χ2 < 3.84; p > 0.05), but dif- through analysis of the variation of the gonadoso- ferences were found in March 2004 (df = 1; χ2 = 2 matic index (GSI = (Wg /Wt) × 100) taken every 2 mo 4.001; p = 0.045) and July 2004 (df = 2; χ = 4.263; p = as well as analyses of the relative frequencies of go- 0.038), with male predominance. For different stan- nadal maturation stages during the sampling period. dard length classes (Fig. 2), the null hypothesis was Size at first gonad maturation was defined as the rejected only for the class 6.5 to 7.0 cm (sexual pro- length class in which 50% of the specimens were portion: df = 1; χ2 = 10.801; p = 0.001) with female adults, estimated according to the distribution of rel- predominance and for the absence of females over ative frequencies of young and adult fish by length size class 7.5 to 8.0 cm. classes (Vazzoler 1996). The equations for the length−weight relationship, Six mature ovaries were dissociated in a modified obtained from the biometric data of males and fe - 3.0485 2 Gilson solution (Vazzoler 1996) to estimate the fecun- males, were Wt = 0.019 L (r = 0.992) and Wt = dity (number of vitellogenic oocytes per ovary), by 0.018 L3.059 (r2 = 0.992), respectively. For both sexes, the volumetric method described by Vazzoler (1996). the increment of weight relative to length was posi- The diameter of oocytes from a random sample of tively allometric (b > 3.0; males and females: ANOVA, each dissociated ovary was obtained under a stereo- p < 0.001). microscope, and their frequency distribution (mm) was determined. 3.2. Reproduction

2.5 Statistical analysis The gonads of both sexes showed variation in size, color, thickness, and angiogenesis, ac cording to the We checked for differences in the sex ratio within reproductive stage. The testes are paired and dor- size classes, by means of the chi-square test. GSI and sally attached by the mesorchium. When immature 48 Aquat Biol 28: 45–53, 2019

30 Females Males 25 *

20

15 Specimens 10

5

0 2.5- 3.0- 3.5- 4.0- 4.5- 5.0- 5.5- 6.0- 6.5- 7.0- 7.5- 8.0- 8.5- 9.0- 9.5- 10- 3.0 3.5 4.0 4.5 5.0 5.5 6.0 6.5 7.0 7.5 8.0 8.5 9.0 9.5 10 10.5 SL classes

Fig. 2. Distribution of the absolute frequencies of occurrence of females and males of Neoplecostomus microps in the standard length (SL) classes (cm) in the Macaé River, southeastern Brazil, from March 2004 through March 2005. *Significantly different chi-square test; p < 0.05

Males A 1.0 or resting, they are filiform and translucent; when maturing, the volume gradually increases until they 0.8 become turgid, when the fish attain the mature stage (Table 1). The morphological changes in the ovaries 0.6 are more remarkable than those in the testes. The ovaries of N. microps are paired, sacculiform organs, 0.4 attached dorsally to the body cavity by the mesovar- Proportion ium and joined at the caudal portion (Table 1). 0.2 Males of N. microps in the Macaé River tended to reach maturity at larger sizes than females. The first 0.0 Mar/04 May/04 Jul/04 Sep/04 Nov/04 Jan/05 Mar/05 gonad maturation was estimated for males at size Immature Maturing Mature Partially spent Spent Resting class 6.6 to 7.0 cm and for females at 5.9 to 6.2 cm. The relative frequencies of gonad maturation stages Females B showed the presence of immature males and females 1.0 in all samples, except males in July 2004 (Fig. 3). The highest numbers of mature individuals of both 0.8 sexes were found in November 2004 (Fig. 3), coincid- ing with the peaks of GSI values (Fig. 4). The distri- 0.6 bution of mature individuals and the variation of GSI values indicated a breeding season starting in 0.4 September and peaking in November. For males, Proportion GSI values varied from 0.015 to 2.610 and for females 0.2 from 0.039 to 16.900. Through the Kruskal-Wallis test, GSI values varied significantly for males (H = 0.0 Mar/04 May/04 Jul/04 Sep/04 Nov/04 Jan/05 Mar/05 14.884; df = 6; p = 0.021) and females (H = 13.014; Immature Maturing Mature Partially spent Spent Resting df = 6; p = 0.041). By the post hoc test, it was verified for males that March 2005 differed significantly from Fig. 3. Distribution of frequency of gonad maturation stages of (A) males and (B) females of Neoplecostomus microps July 2004 (p = 0.016), September 2004 (p = 0.018), in the Macaé River, southeastern Brazil, from March 2004 and November 2004 (p = 0.009); January 2005 dif- through March 2005 fered significantly from July 2004 (p = 0.022), Sep- Carvalho Alves et al.: Reproductive biology of Neoplecostomus microps 49

Table 1. Gonad development of males and females of Neoplecostomus microps, macroscopically characterized. GSI: gonado- somatic index; SL: standard length

Stage Development of testes Development of ovaries

Immature Filamentous and transparent; occupies less Occupies less than 10% of the abdominal cavity; than 5% of the volume of the abdominal translucent; oocytes not visible to the naked eye, cavity; sometimes difficult to see. GSI mean irrigation not visible. GSI mean = 0.06; SL mean = = 0.21; SL mean = 4.58 4.78

Maturing Form is still filamentous but organs are more Occupies between 20 and 25% of the abdominal conspicuous; occupies between 5 and 10% of cavity; beige color; some oocytes visible to the the abdominal cavity; whitish color, weak naked eye; moderate irrigation and turgid. GSI irrigation and slightly flaccid. GSI mean = mean = 1.97; SL mean = 6.67 0.22; SL mean = 7.11

Mature Flat tubular form and maximum size; Maximum size, occupying more than 70% of the occupies between 20 and 25% of the abdominal cavity; yellowish; oocytes visible to the abdominal cavity; white, evident irrigation naked eye in 3 different size classes (smallest size and turgid. GSI mean = 1.07; SL mean = 8.88 corresponds to young oocytes of reserve stock, intermediate corresponds to developing oocytes, and largest corresponds to mature vitellogenic oocytes); oocytes yellow or beige; ovaries with intense irrigation in blood vessels and very turgid. GSI mean = 10.57; SL mean = 7.11

Partially spent/ Flat tubular form; occupies between 10 and Occupies between 30 and 40% of the abdominal partially spawned 15% of the abdominal cavity; whitish, and cavity; yellowish; oocytes visible to the naked eye evident irrigation with hemorrhagic and in smaller quantities and translucent; intense flaccid appearance. GSI mean = 0.42; SL irrigation with hemorrhagic and flaccid appear- mean = 8.29 ance. GSI mean = 5.91; SL mean = 6.96

Spent/spawned Flat filamentous and filamentous form; Occupies approximately 30% of the abdominal occupies less than 10% of the abdominal cavity; few unspawned oocytes visible in possible cavity; whitish; intense irrigation with very resorption process; hemorrhagic appearance and hemorrhagic appearance and very flaccid. very flaccid. GSI mean = 1.99; SL mean = 6.70 GSI mean = 0.30; SL mean = 8.05

Resting Testes still large as a stage 4 but flaccid; Ovaries similar to immature stage but usually empty-like. GSI mean = 0.09; SL mean = 7.04 larger, wider, and pink to dark red in color; ovarian wall also thicker. GSI mean = 0.65; SL mean = 5.97

Fig. 4. Individual (black dots) and average (line) values of gonadosomatic index (GSI) of (A) males and (B) females of Neo- plecostomus microps, captured in the Macaé River, southeastern Brazil, from March 2004 through March 2005 50 Aquat Biol 28: 45–53, 2019

250 18

16.551 16 15.001 200 14 12 150 10 9.395 9.091 8.562 8 GSI 100 6.191 6 Number oocytes of 50 4 2 Fig. 5. Distribution of the relative frequencies of oocyte diameter 0 0 classes in 6 mature females of 6.0 7.17.5 7.5 7.6 8.0 Neoplecostomus microps in the Standard length (cm) Macaé River, southeastern Brazil. Number of oocytes per ovary Number of vitellogenic oocytes GSI GSI: gonadosomatic index tember (p = 0.029), and November 2005 (p = 0.014). rapids) between the sexes in the studied sections of For females, it was verified that November 2004 dif- the Macaé River. Males also reaching the largest fered significantly from September 2004 (p = 0.013), sizes in other species of Loricariidae were found by January 2005 (p = 0.001), and March 2005 (p = 0.041). Mazzoni & Caramaschi (1995, 1997) for Hypostomus The higher values of rainfall and GSI for males and affinis and H. luetkeni and by Suzuki et al. (2000) for females occurred in November but were not signif - H. ternetzi and Megalancistrus aculeatus. Nikolsky icantly correlated for the sampling period. Vi tello - (1963) reported that males tend to be larger than genic oocytes presented diameters between 2.017 females in species that defend their eggs, larvae, and and 3.448 mm. The absolute fecundity from 6 fe- young in the nest against other fish and predators. males (6.02−8.00 cm standard length) of N. microps Although females and males present similar growth, presented a range of 32 to 55 oocytes (mean ± SD = larger body size in males of Neoplecostomus microps 43.83 ± 7.62) (Table 1). The distribution of oocyte dia - may be a useful strategy to defend and/or compete meter classes (Fig. 5) revealed the existence of 3 oocyte for appropriate spawning sites and also to protect the groups. The first was composed of reserve oocytes, offspring in development in the eggs, as shown by with diameters between 0.068 and 0.948 mm. The Brito et al. (2016). second consisted of developing oocytes, with diame- The size at first gonadal maturation is an impor- ters between 1.034 and 1.896 mm. The third was com- tant reproductive tactic because it is closely related posed of mature oocytes, which probably would be to growth, presenting spatial−temporal intraspecific spawned, measuring between 2.063 and 3.448 mm. varia tions related to biotic and abiotic conditions of the occupied area or the period when the population is subject to these factors (Vazzoler 1996). The matu- 4. DISCUSSION ration expresses the interaction between the genetic background and environmental influences and pro- The sex ratio can show temporal variation as a vides evidence of geographic and/or reproductive result of successive events that affect males and isolation of fish populations (Begg 2005). The length females differently (Vazzoler 1996). In this study, the of maturation may be directly affected through sex ratio did not differ from 1:1 during the study changes in the quantity of energy reserves available period, conforming to the expected null hypothesis. for gonad development (Morgan 2004) or indirectly For the same species, Braga et al. (2008) found a sex via changes in growth, which in turn influence the ratio of approximately 1:3 favoring females, but sam- triggering of maturation (Engelhard & Heino 2004). ples were collected at 4 different rivers, which may In this study, the size at sexual maturity found for N. have influenced the result. Considering the sex ratio microps was consistent with that registered by Braga among the length classes, we found only males in the et al. (2008) for the same species in the upper largest length classes, suggesting differential mor - stretches of the Paraíba do Sul river basin, located in tality (e.g. higher energetic cost to produce oocytes) São Paulo State, southeastern Brazil, which seems to or activity (e.g. higher exposure of males in the be a conservative parameter for the species. Carvalho Alves et al.: Reproductive biology of Neoplecostomus microps 51

The reproductive period of N. microps was associ- spawns recorded for N. microps suggest a strategy ated with the spring and summer period (until 6 mo). that maximizes parental fitness. These attributes The large reproductive period of N. microps in the indicate an equilibrium strategist sensu Winemiller Serra do Mar stream was not different from that of (1989) and may also increase juvenile survivor - the Serra da Mantiqueira population in São Paulo ship and reduce fluctuations in local population State (Braga et al. 2008). The Serra do Mar is exposed density. to frequent and strong orogenic rains, and the pluvio- The absolute fecundity estimated for N. microps metric index in Macaé River localities reaches annual in the Macaé River ranged from 42 to 55 oocytes, means exceeding 2000 mm, according to the Agência with mature oocytes having a mean diameter of Nacional de Águas (2006). A prolonged reproductive 2.72 mm. These values were very close to those period, with increased reproductive activity coinciding reported by Braga et al. (2008). This corroborates with the rainy season, was observed by Brito (2007) the hypothesis of more than 1 female spawning on for other species of the Macaé River (e.g. Characid- the same stone by Brito et al. (2016), where up to ium cf. vidali, Astyanax cf. intermedius, and Schi - 375 eggs per stone were registered. The low fecun- zolecis guntheri). N. microps shows a sharp increase dity in loricariid species was reported in several in reproductive effort and spawning in November publications (Mazzoni & Caramaschi 1997, Suzuki that coincides with the onset of rains, but a signifi- et al. 2000, Schmidt 2001, Braga et al. 2009), de - cant correlation in the tests between pluviometric monstrating that egg size in fluences offspring qual- data and GSI was not observed. In the stretches that ity (Sargent et al. 1987), since both correlative and N. microps inhabits, the incidence of flash floods in experimental evidence has shown that several spring and summer is probably the seasonal factor measures of fitness are positively related to egg that most influences the reproductive patterns of the size (Kolm & Ahnesjö 2005). For species that reside ichthyofauna. A continuous or extensive reproduc- in spatially limited and unstable environments, tive period could increase the probability of success such as stream and river channels, the increase in in recruiting (Matthews 1998) and be a useful strat- oocyte diameter and the reduction of fecundity can egy to overcome hydrologically unstable environ- be understood as tactical advantages for larval sur- ments such as streams and rivers of the Brazilian vival. The pattern of at least 2 batches of oocytes Atlantic Forest. recruited for vitellogenesis was similar to the lori- The variations in the stages of gonad maturity and cariids Pseudotothyris obtusa (Menezes et al. 2000) GSI values showed higher frequencies of mature and rudolphi (Braga et al. 2009), both individuals and higher values of GSI in November, smaller than N. microps. suggesting a reproductive peak of N. microps in the Considering N. microps populations in the Serra do Serra do Mar stream. Braga et al. (2008) verified Mar (present study) and the Serra da Manti queira higher GSI values in samples from October and Feb- (Braga et al. 2008), we observed similar reproductive ruary in the Serra da Mantiqueira. It seems plausible behavior. It is possible that in environments with sea- to assume that the 2 populations have their repro - sonal variation that is less predictable and strongly ductive periods at similar times. According to Lowe- influenced by short-duration events, such as oro- McConnell (1987), in the tropics, where the annual genic rains and subsequent flash floods, the immedi- changes in photoperiod and temperature are not very ate conditions are more important than regional sea- noticeable, the influence of these factors on repro- sonal changes for reproduction in small streams. duction are minimal or nonexistent. In tropical re - gions, such as in southeastern Brazil, the level of the Acknowledgements. We thank all the members of the Labo- rivers determines the availability of habitat and food, ratório de Ecologia de Peixes (UFRJ) who helped us with the and rainfall seems to be the factor that most influ- field and laboratory work. We are also grateful to the inhab- ences the reproductive cycles of fish (Vazzoler 1983, itants of the Macaé River basin for their hospitality, espe- Vazzoler & Menezes 1992, Vazzoler et al. 1997, Ago - cially Sérgio Almeida, Geraldo Craik, Joceline Craik, Már- cio Nascimento Silva and Renaldo, Morais and Gracinha. stinho et al. 2004, Bailly et al. 2008, Freitas et al. We thank CNPq and FAPERJ for scholarships. The authors 2011). In the Macaé River, N. microps exhibits high thank Bruno Eleres Soares for statistical support. The study reproductive effort in the rainy season, from Novem- was part of the project entitled ‘Estrutura da comunidade e ber to March, when the river is subjected to sudden estratégias reprodutivas e tróficas de peixes da bacia do rio Macaé, RJ’, partially financed by CNPq and FAPERJ (grant changes in water volume (Brito 2007). The prolonged nos. 479257/2004-3 and E-26/171.672/2001, respectively). reproductive period, low fecundity, large eggs, posi- We also thank IBAMA for a collecting permit (Authorization tive allometry, possible parental care, and repeated 004/2004). 52 Aquat Biol 28: 45–53, 2019

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Editorial responsibility: Victor Benno Meyer-Rochow, Submitted: June 29, 2018; Accepted: February 6, 2019 Oulu, Finland Proofs received from author(s): March 29, 2019