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Home , Ancistrus, Hypostomus, Hypostomus plecostomus, Loricariidae, Pterygoplichthys, Suckermouth

BioInvasions Records (2016) Volume 5, Issue 3: 173–183 Open Access DOI: http://dx.doi.org/10.3391/bir.2016.5.3.09 © 2016 The Author(s). Journal compilation © 2016 REABIC

Research Article

Female reproductive biology of an exotic armored () in the San Marcos River, Hays Co., , with observations on environmental triggers

S. Luci Cook-Hildreth1,*, Timothy H. Bonner2 and David G. Huffman2 1Texas Parks & Wildlife Department, 4200 Smith School Rd., Austin, TX 78744, USA 2Department of Biology/Aquatic Station, Texas State University, San Marcos, TX 78666, USA *Corresponding author E-mail: [email protected]

Received: 22 March 2015 / Accepted: 10 March 2016 / Published online: 29 March 2016

Handling editor: Vadim Panov

Abstract

Invasive populations of suckermouth (Loricariidae) are native to Central and , but have become established in US and Mexican waters since the 1950’s and have been reported to have negative impacts on North American freshwater ecosystems. Two genera of loricariids have been reported from Texas waters ( spp. and spp.), both of which have become established in aquatic ecosystems where there are warm-water refugia, or suitable and seasonally stable temperatures. In an effort to better understand the invasive dynamics of these loricariids in novel ecosystems, aspects of their reproductive biology such as fecundity, seasonality of spawning activity, and spawning frequency of the individual were studied for Hypostomus cf. niceforoi living in the spring-fed San Marcos River, Texas. Fecundity was similar to Hypostomus spp. in the native range. There did not appear to be any synchronicity of spawning between individual fish within the invasive population, and there was a hint in the oocyte size-frequency data that some of the fish may be spawning multiple times per year. The timing of spawning activity in the novel range was seasonally inverted compared to the pattern typical of loricariids in the native range. The season of peak reproductive activity was also less distinct in the novel range than in the native range, and the period of reproductive quiescence was more seasonally compressed than in the native range. We provide data and supporting arguments suggesting that photoperiod is the primary proximate factor triggering the onset of reproductive quiescence, as well as a return to reproductive activity for these fish in both their native and novel ranges. Key words: Hypostomus, reproductive triggering, fecundity, GSI, spawning frequency, ovarian dynamics

Introduction Statement of problem The Loricariids Because of their hardy nature and their reputation as The Loricariidae is the most diverse of siluri- cleaners, several genera of loricariids are routinely form , with more than 840 having been imported into North America for the trade described among 90+ genera and 6 subfamilies (Nico (Walker 1968). Interest in loricariids by aquarists et al. 2012). All are native to fresh and brackish has grown substantially in the last several decades. waters of Costa Rica, Panama, and South America Hoover et al. (2014) found only three loricariid genera (Nelson 2006). Loricariids typically consume addressed in the popular aquarium literature between or (Flecker 1992; Power 1984b) and inhabit 1933 and 1935, but found 35 genera addressed between lotic environments (Sakurai et al. 1993; Sterba and 1987 and 2009. Loricariids are also sometimes Mills 1983). Part of their invasiveness is due to them intentionally released into freshwaters outside their being facultative air-breathers that can absorb native range by natural resource managers hoping to oxygen through the stomach, allowing them to control algae and aquatic (TISI 2014). These survive periods of low dissolved oxygen (Graham findings suggest that loricariid introductions are and Baird 1982; Mattias et al. 1998) to which native likely to continue expanding in frequency, taxonomic fish may succumb. diversity, and geographic location, and that the

173 S.L. Cook-Hildreth et al. consequences of these introductions will likely become (Power 1984a). However, the exotic population of more complex. H. cf. niceforoi living in the thermally stable spring Release of loricariids has led to established run of the San Marcos River would not be influenced populations in several states in the USA (Hoover et al. by the same weather-related proximate factors that 2004), including , , Texas, Arizona, are experienced annually by fish in the surface-fed Colorado, Connecticut, Louisiana, , and waters of their native range. Moreover, seasonal Pennsylvania (Courtenay and Deacon 1982). The variations in the ultimate factors (that originally earliest report of loricariids in Texas waters was in synchronized the reproductive activities of the San Antonio River in 1956 (Barron 1964), and Hypostomus to proximate factors in the native loricariids have since been reported from several habitat) do not occur in the San Marcos River. other Texas drainages (Hubbs et al. 1978; López- During the period of increased reproductive Fernández et al. 2005; Nico and Martin 2001). The activity, some Hypostomus species in South America first record of loricariids in the San Marcos River, a are known to asynchronously, with individual sensitive habitat that is home to several state and females spawning multiple times within the year federally listed endemic taxa, was in the early (Duarte and Araújo 2002; Duarte et al. 2007; Mazzoni 1990’s (Perkin 2009; Perkin and Bonner 2011). The and Caramaschi 1997a,b). feeding preferenda of the San Marcos River The purpose of our study is to provide information Hypostomus was elucidated by Pound et al. (2011). regarding the fecundity and the seasonal patterns of Although the San Marcos River Hypostomus was reproductive activity of the San Marcos River identified as (Linnaeus, population of Hypostomus cf. niceforoi. Our 1758) in some earlier literature, the local loricariid findings are compared to reports from similar studies that we studied from the San Marcos River has been in the Northern and Southern Hemispheres, and help declared to not be H. plecostomus, and has been shed light on whether or not the presumptive tentatively identified (personal communication from proximate factors that have been proposed as triggers Jonathan Armbruster at Auburn University) as for the seasonal reproductive patterns observed for Hypostomus cf. niceforoi (Fowler, 1943). The native loricariids in their native habitats (Duarte and Araújo range of this species is the Japurá River system, 2002; Duarte et al. 2007; Mazzoni and Caramaschi State of Amazonas, Brazil (Froese and Pauly 2015). 1997a,b) are transferrable to exotic populations in We have also recently noted the presence of an the northern hemisphere. We hypothesize that both unidentified species of Pterygoplichthys (Loricariidae) native and exotic populations are responding not to now thriving in the San Marcos River, but this temperature, rainfall, or stream discharge, as suggested species was not included in our study. by other workers, but to another proximate factor (photoperiod) that is a covariate with the ultimate Reproductive biology of loricariids factors in the native range, but not in the novel range in North America. The reproductive biology of loricariids has been studied in their native habitats using such analytical tools as the gonadosomatic index (GSI) and the Methods maturation patterns of ovaries and oocytes (Duarte Study site and Araújo 2002; Duarte et al. 2007; Mazzoni and Caramaschi 1997a,b). Loricariids living in the native The San Marcos River originates at headsprings habitats of South America have developed issuing from the Edwards Aquifer. The headsprings reproductive habits coincident with the seasonal were first impounded in 1848 (Slattery and Fahlquist availability of food and cover for young fish caused 1997) and this resulted in what is now known as by seasonally predictable flooding of the riparian Aquarena Lake, or Spring Lake. The current study was forest floor, sometimes for weeks at a time (Duarte restricted to a 300-meter reach of the San Marcos and Araújo 2002; Duarte et al. 2007; Mazzoni and River spring run immediately downstream from the Caramaschi 1997a,b). Power (1984a) speculated that dam impounding the headsprings (29º53′24.04″N, loricariids in lotic South American habitats had 97º56′4.12″W). This reach is in the USGS 12-digit synchronized their reproductive activity to take Hydrologic Unit HUC 12-121002030302, and includes advantage of the increased food availability and the segment of the river channel shown in Figure 1. cover (the ultimate factors) during these periods, but The exceptional water quality, persistent flow, were probably using increased water temperatures and stable temperatures of the San Marcos River and rainfall rates in spring and summer months as (Groeger et al. 1997) provide a stable habitat for a triggers (proximate factors) to prepare for breeding variety of endemic aquatic life; some species of which

174 Reproductive biology of Hypostomus in Texas

Figure 1. Map of Texas from the USGS “The National Map” (USGS 2015) with insets showing location of study site (29º53′24.04″N, 97º56′04.12″W).

12 28

10 26

8 24

6 22 Figure 2. Water characteristics of the San Marcos River just downstream from the study 4 20 reach: daily discharge rates for 2005 (USGS 2014), means of temperatureWater (°C) monthly mean discharge rates

Discharge (cubic meters/second) (cubic meters/second) Discharge 2 18 (from 1994–2015, USGS 2014), Mean daily discharge (2005) and water temperatures during Mean monthly mean discharge (1994-2015) 2005 (from local measurements Mean daily water temperature (2005) every 4 hours, compliments of 0 16 BIO-WEST Corporation). Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Month

are listed by the state of Texas and the U.S. federal from the springs fluctuated substantially during that government. Year-round temperature fluctuation of period (2.4–20.6 m3/s, USGS 2014), there are no these waters is minimal compared to local surface annually consistent flood seasons during which the waters, with the mean daily water temperature, stream inundates the flood plain for extended periods. measured every four hours just downstream from the study reach during the study year (2005), varying Study fish between 20.7 and 23.5 with an annual mean of 22.7 °C (Figure 2). The mean annual discharge rate Eighty seven Hypostomus cf. niceforoi were collected of the San Marcos Springs between 1994 and 2014 from the study reach by gigging from January was 5.2 m3/s and, although mean monthly discharge through December of 2005 (≤10 fish/month). Length

175 S.L. Cook-Hildreth et al.

Table 1. Length and weight summary statistics for Hypostomus cf. niceforoi collected from the San Marcos River, TX, during 2005.

Total Length(mm) Body Weight(g) Ovary Weight(g) Females (n=51) Minimum 137 90.7 0.230 Maximum 590 1860 73.4 Mean 338 491 12.9 St. Err. 11.2 45.0 2.70 Males (n=33) Minimum 140 22.7 - Maximum 540 1633 - Mean 280.7 362.5 - St. Err. 20.5 76.9 -

and weight summary statistics for males and females cavity and orange in color with strong vascularization, collected are provided in Table 1. Immediately thin ovarian wall, and containing large yellow oocytes following collection, the fish were euthanized by 5.5 mm in diameter, which is apparently identical to pithing and then weighed and measured for total “Spawning Capable”); and (4) “Recovering” (ovary < length. Each fish was then incised ventrally from the 30% of body cavity and flaccid with slight pharynx to the vent for the study of ovaries. Only 50 vascularization, which is apparently equivalent to females had discernable ovaries and were considered “Regressing”). While other workers have included a to be suitable females for reproductive study. category “Immature,” this category was omitted from our study because only one of the 51 females Reproductive biology collected was considered to be sexually immature. However, we included an additional category Ovaries from the 50 study females were excised, (“Resting”) for six of the females which were large weighed to the nearest milligram, and preserved in enough to be sexually mature (by being larger than 10% buffered formalin for later assessment. The some other females that were obviously sexually preserved ovaries were later assigned to one of four mature), but which had ovaries with no obvious sign stages of ovarian maturity categories based on of past or present oocyte development (perhaps Mazzoni and Caramaschi (1997a,b). This system roughly equivalent to the “Regenerating” category employs an estimate of the percentage of the body of Brown-Peterson et al. (2011)). cavity occupied by the ovary, in combination with a Seasonal variation in reproductive activity of the visual-based classification scale. Subsequent to our females was studied by calculating mean monthly collections and dissections, a new standard for gonadosomatic index (GSI; typically defined as terminology pertaining to reproductive stages of ovary weight divided by total body weight multiplied oocytes in fish ovaries was published by Brown- by 100%) and by examining the relative monthly Peterson et al. (2011). The latter system requires frequencies of the ovarian maturity categories described histological examination for reliable assignment to above. However, the Mature-2 category was so ovarian development categories, and our fish were sparsely represented that, for purposes of exploring not examined histologically. However, the categories seasonal patterns, we pooled Mature-1 and Mature-2 in the system we adapted from Mazzoni and into “Mature,” which corresponds rather well to the Caramaschi (1997a,b) are roughly equivalent to those Developing category of Brown-Peterson et al. (2011). of Brown-Peterson et al. (2011), and we provide the Fecundity was estimated following the McGregor equivalent terms here for future reference. The four (1922) sub-sampling-by-weight technique recom- categories we used from Mazzoni and Caramaschi mended in the International Biological Programme (1997a,b) are: (1) “Mature-1” (ovary <15% of body Handbook No. 3 (Ricker 1968). The majority of cavity and pale cream in color with subtle granulation, oocytes from the 17 Ripe ovaries appeared to be in a which is roughly equivalent to early “Developing” mid- to late-vitellogenic growth phase, as per Patiño of Brown-Peterson et al. 2011); (2) “Mature-2” and Sullivan (2002), which is roughly equivalent to (ovary >15% but <50% of body cavity and yellow in the vitellogenic stages 2 and 3 (Vtg2 and Vtg3) of color with light vascularization and large light-yellow Brown-Peterson et al. (2011). The oocytes from these oocytes discernable, which is roughly equivalent to Ripe ovaries were then set aside and later included late “Developing”); (3) “Ripe” (ovary >50% of body in the oocyte size-frequency study.

176 Reproductive biology of Hypostomus in Texas

%Recovery %Ripe %Mature 1&2 %Resting 100%

14% 13% 90% 20%

33% 33% 80% 40% 25% 70% 67% 75% 60% 40%

50% 100% n/a 71% 20% 100% 33% 100% 38% 40% 50% Percent total Figure 3. Monthly variation 30% in the percent monthly count of Hypostomus cf. niceforoi 20% 40% 40% 33% 33% ovaries assigned to the 25% 25% 10% Resting, Mature 1&2, Ripe, 14% 17% or Recovery categories (no fish were collected in 0% February). Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec n = 1 0 7 8 3 4 5 3 5 3 6 5 Month of collection (2005)

26 24 22 20 18 16 Figure 4. Monthly variation 14 in the mean GSI among all 12 female Hypostomus having ovaries classified as Mature 10 7 3 (n=21), Ripe (n=17), Mean monthly GSI 8 4 Recovery (n=6), and Resting 3 (n=6). No fish were collected 6 in February. Error bars 4 represent upper half of 95% 1 8 confidence intervals 2 5 5 3 6 5   0 X  t0.05( 2 ),df  s X 0  . Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Month of collection (2005)

The spawning pattern of individual Hypostomus All calculations were performed in Excel. Charts in the San Marcos River was investigated by gene- were produced in Excel and some were enhanced in rating oocyte size-frequency charts from the 21 fish PowerPoint. All geographic references are from having ovaries classified as either Mature-2 (n=4) or Google Earth Pro, using the WGS84 datum. Ripe (n=17). Approximately 100 oocytes (as per Hunter and Goldberg 1985) were extracted from each Results of these 21 ovaries and measured under a dissecting microscope to the nearest 100 m with an ocular Seasonal variation in reproductive activity micrometer. These measurements were then cast into The patterns of seasonal variation in the five individual separate size-frequency charts for each of the 21 categories of ovarian maturity (including the Resting fish, and arranged by month of capture. category) are represented by percent monthly totals

177 S.L. Cook-Hildreth et al. in Figure 3. Fish with Ripe ovaries only occurred species (as per Brown-Peterson et al. 2011) and will March through September, and four of the six fish likely spawn at least twice during the reproductive with Resting ovaries were observed September season. However, we cannot be certain that these through November. Fish with Mature ovaries were individual fish are actually spawning more than once observed throughout the 11 months we collected fish, per season because we did not conduct any real-time except for August. spawning observations of individual fish. Although no definitive peak in reproductive activity All of the oocyte size-frequency charts in Figure 5 was noted for the San Marcos River Hypostomus, show most of the oocytes within an ovary clustered the fluctuations in mean monthly GSI’s appeared to rather tightly around one or two length values. correspond seasonally with photoperiod. All elevated However, while the central lengths around which the mean monthly GSI’s (greater than 2%) occurred oocytes clustered varied from ovary to ovary, there from March through August, and five of the six was no consistent seasonal increase in oocyte size lowest mean monthly GSI’s (less than 2%) occurred among the fish as the seasons progressed, as one September through January (Figure 4). As with the would expect if these fish were determinate Pterygoplichthys population in Volusia Springs, synchronous spawners. These observations are con- Florida (Gibbs et al. 2008), there appeared to be a sistent with patterns of oocyte development reported period of reproductive quiescence, with five of the for loricariids in South America that are asynchronous six GSI values below 2% occurring during the five spawners (Macchi and Acha 2000; Wallace and months between when day length had declined Selman 1981). Therefore, the observed lack of seasonal more than half way to minimum value, until just progression in the oocyte size frequencies for the after the day length had begun to increase again. San Marcos Hypostomus could be an indication of a similar asynchronous spawning pattern for our fish Fecundity estimates in the invaded Northern Hemisphere habitat. The fecundity estimates for the 17 Ripe ovaries varied from 871 to 3,367 oocytes per ovary, with a Factors affecting ovarian dynamics mean estimate of 2,124 per ovary ( ). sX  217 Seasonal patterns Spawning frequency within a breeding season The highest individual GSI values (Figure 4), and also the highest monthly percentages of fish with Oocyte size-frequency distributions for each of the Ripe ovaries (Figure 3), were recorded from early ovaries classified as Mature (n=4) and Ripe (n=17) spring (March) through late summer (August), though are plotted in separate charts for each ovary in as females appeared to be reproductively active Figure 5. In at least three of the charts for Ripe through most months of the spring, summer, and ovaries (charts P, R, and T), two distinct and separate early fall, we could not reliably estimate the exact cohorts of oocytes are discernible. seasonal peak in breeding activity. However, we were able to discern the seasonal period of minimal Discussion reproductive activity (reproductive quiescence). The low and progressively declining GSI values recorded Spawning frequency in the last quarter of 2005 suggest decreasing levels Native Hypostomus populations in South America of spawning activity for the population at that time. have been reported to spawn multiple times per year Even though 30% of the females that were rated for (Duarte and Araújo 2002; Mazzoni and Caramaschi ovarian maturity were collected during the months 1997a,b). Multiple-batch spawning has also been of Oct-Jan, not one of these 15 females had ovaries reported for an introduced population of classified as Ripe (Figure 3). In addition, the lowest Pterygoplichthys disjunctivus in Volusia Blue four mean monthly GSI values in the study, involving Spring, Florida (Gibbs et al. 2008). We investigated 40% of the 50 fish rated for GSI, occurred in the pattern of spawning frequency of individual fish progressively declining order from September through in our study by examining the size-frequency charts December (Figure 4). portraying oocyte development within individual These findings are consistent with those for an ovaries. We found some evidence of bimodality, exotic population of Pterygoplichthys disjunctivus indicating two different oocyte-size cohorts (Figure 5; established in Volusia Blue Spring Florida charts P, R, & T). The ovaries of these three females (28º56′51.00″N, 81º20′22.50″W; Gibbs et al. 2008), suggest that the Hypostomus in the San Marcos and also for a different population of P. disjunctivus River system is a determinate batch spawning at El Infiernillo Reservoir in (18º16′21.27″N,

178 Reproductive biology of Hypostomus in Texas

Figure 5. Hypostomus cf. niceforoi oocyte size frequency distributions for 17 Ripe (green, down right) and 4 Mature (red, up right) ovaries, including total length (TL) and gonadosomatic index (GSI) of each fish (San Marcos River, TX, 2005).

101º53′34.13″W; Rueda-Jasso et al. 2013). Findings by Gibbs et al. (2008) suggest that the period of Abiotic factors covarying with ovarian dynamics reproductive quiescence for P. disjunctivus in The period of reproductive quiescence for Hypostomus Volusia Blue Springs starts in the last quarter of the populations in the river Paraiba do Sul in South calendar year and continues through January (lowest America near the Tropic of Capricorn (at approxi- numbers of large oocytes Oct, 2005 – Jan, 2006 and mately 21º43′7.10″S, 42º16′29.25″W) typically occurs Nov, 2006 – Jan, 2007; lowest mean GSI and lowest in the second quarter of the year (Duarte and Araújo variation in GSI during same periods). In addition, 2002; Mazzoni and Caramaschi 1997a,b). This is Rueda-Jasso et al. (2013) reported the lowest raw almost exactly one half year out of phase with what fecundity and lowest egg number/wt. of females in we observed for the three North American January, and also reported lowest GSI values from populations, which straddle the Tropic of Cancer November through January (Figure 6). (from about 18ºN to 30ºN). In contrast to the South

179 S.L. Cook-Hildreth et al.

Figure 6. Comparison of periods of reproductive quiescence (based on declining GSI) reported for loricariids in southern North America (Florida, Texas, and Mexico) vs. South America (Rio de Janeiro), with the annual photoperiod cycles for the latitudes of interest. A – Based on Rueda-Jasso et al. (2013), GSI values less than 0.8%, lowest GSI in January (0.36%); B – Based on Mazzoni and Caramaschi (1997b), GSIs were reported by these authors with resolution of 2 months, so beginning and ending of indicated quiescent period is represented herein as middle of 2-month periods reported by the authors (GSIs<2%); C – Based on our study (San Marcos River, TX, 2005); GSIs during indicated quiescent period were all less than 2% and declining until increase in January; D – Based on Gibbs et al. (2008); quiescent period was compressed by two months during the second year of study, so quiescent period represented herein is bounded by median of two beginning months and two ending months reported by authors. Day lengths determined from USNO (2015).

American populations, there were no apparent all become reproductively quiescent during the relationships between patterns of reproductive second half of the period of waning day length at quiescence for Hypostomus in the San Marcos River their respective localities. Moreover, the end of the and local rainfall rates, spring discharge, or ambient period of reproductive quiescence (increase in air temperature. Gibbs et al. (2008) noted that P. reproductive activity) occurs shortly after the photo- disjunctivus spread out into the connecting St. period begins to lengthen again (arrows between John’s River in warmer months, but returned to the dotted lines in Figure 6). Note that the Mexico site is warmer spring run in large numbers during the at a lower latitude than the other sites under winter. Temperature may therefore have played a comparison and experiences less seasonal amplitude role in influencing the fourth quarter period of in photoperiod (Figure 6), perhaps explaining why reproductive quiescence in the Volusia Blue Springs the quiescent period in Mexico is not as seasonally population, even though that period of quiescence distinct as for the Volusia Blue Springs and San coincided well with the San Marcos Springs popu- Marcos Springs populations. lation, which was not exposed to temperature swings. Our suggestion that photoperiod is the main Rueda-Jasso et al. (2013) noted that the rainy season proximate stimulus triggering the onset of reproductive happened to be coincident with the peak of repro- quiescence for these loricariids does not eliminate ductive activity in a population of P. disjunctivus the possibility that other proximate factors, such as they studied in Mexico. However, the single common rainfall and water temperature, originally played a factor that ties all these periods of reproductive role in the evolution of patterns of reproductive quiescence together in both hemispheres is that they activity for loricariids in their native habitat.

180 Reproductive biology of Hypostomus in Texas

Proximate factors have often been implicated in populations in lentic and lotic habitats of South determining the evolution of behavioral patterns America. For example, in the native Brazilian range (Brown and Lawson 2010; Hoar 1976; Kramer 1987; of H. affinis, Duarte and Araújo (2002) reported Sorensen and Stacey 1999). While water temperature mean fecundity to be 2,373 in a lentic habitat, while is typically thought to influence hormonal cycles in Mazzoni and Caramaschi (1997b) reported a mean fish more so than photoperiod (Vlaming 1972), fecundity of 1,784 for P. disjunctivus in a lotic habitat. mean daily water temperatures during periods of The mean fecundity estimate for the Hypostomus cf. reproductive quiescence for the Hypostomus niceforoi of the San Marcos River was intermediate, population in the San Marcos River were not more with approximately 2,124 oocytes per Ripe ovary. than 3 °C lower than during the extended period of Our fecundity data are also consistent with those reproductive activity during the summer (Figure 2). reported for other species of loricariids, which Therefore, while proximate factors other than typically have less than 2,500 oocytes per ovary photoperiod might covary with reproductive behavior (Azevedo 1938; Rueda-Jasso et al. 2013). However, in the native and novel habitats, the proximate factor if H. cf. niceforoi in the San Marcos River is, indeed, that actually stimulates the onset of increasing a multiple-batch spawner, then our fecundity reproductive activity of these fishes in the Northern estimates for this species are probably low. Hemisphere appears to be lengthening photoperiod following the annual minimum. Conclusions and implications for future Gibbs et al. (2008) observed that the period of research reproductive quiescence in the Volusia Blue Springs population was shorter than the period of repro- Our findings indicate that the San Marcos River ductive quiescence reported for native populations, Hypostomus population is probably batch-spawning i.e. the period of reproductive activity had apparently asynchronously, and that the seasonal onset and lengthened at the expense of the quiescent period. cessation of reproductive activity are likely triggered Moreover, even during their two-year study, the by photoperiod. quiescent period was compressed in the second year Because the variance in such measures as GSI is compared to the first (Gibbs et al. 2008). They very high for asynchronous spawners having conjectured that, while the day-length cycle may extended spawning periods, it may be more useful to have served as an adaptive trigger for the South study the seasonality of reproductive behavior for American populations signaling the onset of favorable such fishes by describing the period of reproductive breeding conditions, that trigger has no adaptive quiescence rather than attempting to estimate the value for the exotic populations in the seasonally seasonal peak in reproductive activity. The quiescent constant spring habitat. Photoperiod seems to be the period in both the Northern and Southern Hemi- proximate factor that is most likely to be triggering spheres for the loricariids considered herein begins the observed seasonal spawning cycle in Northern during the period of declining day length at Hemisphere populations at this time, but is probably approximately the equinox, and the resumption of also doing so for populations in their native ranges reproductive activity occurs at or shortly after the as well. For populations of loricariids established in minimum day length, even for invasive populations environmentally stable spring runs in the Northern in spring-dominated physicochemically stable Hemisphere there is no obvious selection pressure environments. Thus, loricariids in both hemispheres that would discourage spawning during the season of are probably using photoperiod as triggers of repro- waning day length. Therefore, while there may be ductive activity, rather than seasonal changes in residual (but seasonally inverted) patterns of other covarying environmental factors such as river reproductive activity in newly introduced popu- discharge, water temperature, rainfall, etc. lations in the Northern Hemisphere, with time, Since this study was conducted, there have been reproductive activity in these exotic populations several anecdotal reports and personal observations might become more seasonally uniform as the period of invasive loricariids in Texas River systems not of reproductive quiescence is gradually compressed influenced by thermally constant spring runs, such and ultimately disappears. as the Guadalupe River some 12 km downstream from the confluence with the spring-fed Comal Fecundity River. The fish in these thermally ambient waters have been observed to survive winter thermal Our fecundity data for the Hypostomus in the lotic minima by crowding into thermally stable refugia habitat of the San Marcos River are similar to those formed by hyporheic flows in which winter thermal reported for Hypostomus affinis (Steindachner, 1877) minima remained above 17 °C (personal obs., DGH).

181 S.L. Cook-Hildreth et al.

Loricariids have also been captured along Texas Gibbs MA, Shields JH, Lock DW, Talmadge KM, Farrell TM (2008) coastal habitats in brackish and salt water bays and Reproduction in an invasive exotic catfish Pterygoplichthys disjunctivus in Volusia Blue Spring, Florida, USA. Journal of estuaries (Chilton et al. 2011). Outside of spring-run Fish Biology 73: 1562–1572, http://dx.doi.org/10.1111/j.1095-8649.200 habitats, it is unclear what influence abiotic factors 8.02031.x may be having on loricariid reproductive behaviors Graham JB, Baird TA (1982) The transition to air breathing in fishes: I. Environmental effects on the facultative air breathing of (Nico et al. 2012). The more or less random spawning chagresi and Hypostomus plecostomus Loricariidae. of individual fish over a protracted spawning period Journal of Experimental Biology 96(1): 53–67 of several months has also been reported for Groeger AW, Brown PF, Tietjen TE, Kelsey TC (1997) Water loricariids in the native habitat of South America, quality of the San Marcos River. Texas Journal of Science 49(4): 279–294 but this behavior in the novel habitat of North Hoar WS (1976) Smolt transformation: Evolution, behavior, and America, coupled with the hardy nature of these physiology. Journal of the Board of Canada 33: fishes, will undoubtedly lead to continued colonization 1233–1252, http://dx.doi.org/10.1139/f76-158 of new habitats. Hoover JJ, Killgore KJ, Cofrancesco AF (2004) Suckermouth catfishes: Threats to aquatic ecosystems of the United States? Aquatic Nuisance Species Research Program Bulletin 4(1): 1–9 Acknowledgements Hoover JJ, Murphy CE, Killgore J (2014) Ecological impacts of suckermouth catfishes (Loricariidae) in North America: A This paper is based on a Masters of Science thesis at Texas State conceptual model. Aquatic Nuisance Species Research Program University by SLC, and we are indebted to the Department of 14(1): 1–20 Biology at Texas State University for the provision of materials, Hubbs C, Lucier T, Garrett GP, Edwards RJ, Dean SM, Marsh E, lab space, and resources to complete this project. There were Belk D (1978) Survival and abundance of introduced fishes near many students that participated in the collection of specimens for San Antonio, Texas. Texas Journal of Science 30(4): 369–376 this project and without their help this project would have been Hunter JR, Goldberg SR (1985) Spawning incidence and batch nearly impossible. Thanks also to the Texas Parks & Wildlife fecundity in northern , Engraulis mordax. National Department, where SLC was employed during the end phase of Oceanographic and Atmospheric Administration, NOAA this study, for their encouragement and patience as the project Technical Report, Report No. 36, 67–78 pp required SLC to make many excursions from the office. We Kramer DL (1987) Dissolved oxygen and fish behavior. especially appreciate the helpful suggestions of a reviewer who Environmental Biology of Fishes 18: 81–92, http://dx.doi.org/10.10 helped us to correlate our reproductive terminology with 07/BF00002597 emerging standards. López-Fernández H, Winemiller KO, Bestgen K (2005) Status of Dionda diaboli and report of established populations of exotic References fish species in lower San Felipe Creek, Val Verde County, Texas. 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