This article was downloaded by: [University of Florida]On: 16 January 2014, At: 09:57Publisher: Taylor & FrancisInforma Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House,37-41 Mortimer Street, London W1T 3JH, UK

Transactions of the American Fisheries SocietyPublication details, including instructions for authors and subscription information:http://www.tandfonline.com/loi/utaf20

Localized Spatial and Temporal Variation inReproductive Effort of Florida BassS. L. Shaw a & M. S. Allen aa Fisheries and Aquatic Sciences Program , University of Florida , 7922 Northwest 71stStreet, Gainesville , Florida , 32653 , USAPublished online: 09 Jan 2014.

To cite this article: S. L. Shaw & M. S. Allen (2014) Localized Spatial and Temporal Variation in Reproductive Effort of FloridaBass, Transactions of the American Fisheries Society, 143:1, 85-96, DOI: 10.1080/00028487.2013.829123

To link to this article: http://dx.doi.org/10.1080/00028487.2013.829123

PLEASE SCROLL DOWN FOR ARTICLE

Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) containedin the publications on our platform. However, Taylor & Francis, our agents, and our licensors make norepresentations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of theContent. Any opinions and views expressed in this publication are the opinions and views of the authors, andare not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon andshould be independently verified with primary sources of information. Taylor and Francis shall not be liable forany losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoeveror howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use ofthe Content.

This article may be used for research, teaching, and private study purposes. Any substantial or systematicreproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in anyform to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http://www.tandfonline.com/page/terms-and-conditions

Transactions of the American Fisheries Society 143:85–96, 2014C© American Fisheries Society 2014ISSN: 0002-8487 print / 1548-8659 onlineDOI: 10.1080/00028487.2013.829123

ARTICLE

Localized Spatial and Temporal Variation in ReproductiveEffort of Florida Bass

S. L. Shaw* and M. S. AllenFisheries and Aquatic Sciences Program, University of Florida, 7922 Northwest 71st Street, Gainesville,Florida 32653, USA

AbstractFew studies have explored annual reproductive effort of fish populations, yet factors such as skipped spawning could

influence recruitment processes. We estimated the number of broods produced annually as an index of reproductiveeffort for Florida Bass Micropterus floridanus across four lakes in north-central Florida. Snorkel surveys were usedto estimate reproductive effort in the lakes from 2010 to 2012. Mark–recapture methods were used to estimatethe abundance of Florida Bass in each lake during each year. All four lakes contained high-density Florida Basspopulations that showed evidence of relatively slow growth. Average relative weight in all populations was low,ranging from 65.4 to 68.8 for adults (≥25.0 cm TL). Annual reproductive effort (estimated number of broods) variedamong lakes and across years. We found evidence for multiple spawning events per adult and for skipped spawning.Devils Hole Lake produced the highest number of broods in all 3 years, ranging from 1.62 broods/spawner in 2012to 3.72 broods/spawner in 2011 (median = 3.24 broods/spawner in 2010). All other populations exhibited skippedspawning, with the proportion of nonreproductive adults varying across years. Picnic Lake fish had the lowest numberof broods overall (only 0.02 broods/spawner in 2011 and 0.01 broods/spawner in 2012). The other two lakes showedvariable levels of spawning effort. Spawner abundance in these populations was not related to the estimated annualnumber of broods, contrary to the general assumption made for many population models. Variability in annualreproductive effort may be more common than anticipated, potentially clouding the relationship between spawnerabundance and recruitment. Estimation of annual reproductive effort may provide insight into density-dependentpopulation regulation and recruitment processes.

Fish species that are characterized as iteroparous annualspawners are assumed to follow an annual reproductive cy-cle that culminates in spawning each year after a fish reachesmaturity (Rideout et al. 2005). Departure from this cycle,in which a fish does not spawn annually, is commonly re-ferred to as “skipped spawning” and has been noted for manyiteroparous annual spawners in both marine and freshwater sys-tems (Jørgensen et al. 2006; Rideout and Tomkiewicz 2011).Skipped spawning can result from an interruption of gonadmaturation prior to spawning or from retention of ripe gonadsthrough the spawning season. The cycle of normal gonad de-velopment in fishes can be interrupted at multiple points inrelation to different environmental or behavioral factors. In fe-males, interruption of the reproductive cycle can be caused by

*Corresponding author: slshaw@ufl.eduReceived February 14, 2013; accepted July 22, 2013

environmental factors (e.g., low temperature, pollution, or lowdissolved oxygen) or nutritional factors (e.g., low food avail-ability, infestations with parasites, or viral infection) that occurbefore vitellogenesis or during the vitellogenic stage (Rideoutet al. 2005). Behavioral or population-level interactions (i.e.,fish density, mate availability, or habitat availability) can resultin retention of ripe gonads throughout the spawning season byboth sexes (Rideout et al. 2005).

The majority of skipped spawning reported in the literaturehas been described for iteroparous marine species (Rideout et al.2005; Rideout and Tomkiewicz 2011). Skipped spawning hasbeen observed in the freshwater black basses Micropterus spp.,including Smallmouth Bass M. dolomieu and Florida Bass M.floridanus (Swingle 1944; Chew 1973; Barwick and Holcomb

85

Dow

nloa

ded

by [

Uni

vers

ity o

f Fl

orid

a] a

t 09:

57 1

6 Ja

nuar

y 20

14

86 SHAW AND ALLEN

1976; Raffetto et al. 1990; Gillooly et al. 2000). Black basses aregenerally described as iteroparous, annually spawning species,with the male providing parental care to the brood until theschool of fry disperses (Warren 2009). Research in Nebish Lake,Wisconsin, suggested that only female Smallmouth Bass wereiteroparous, while the majority of males sampled during thestudy only reproduced once in their lifetime (i.e., were semel-parous; Baylis et al. 1993). In the same lake, a large proportionof males and females failed to spawn in each year (Raffettoet al. 1990). A male bass may initiate spawning behavior, butif that individual does not produce a brood in a given season(i.e., because he abandons spawning behavior prior to gametedeposition or because he fails to court a female), he would be de-scribed as having exhibited skipped spawning. A male may alsoabandon his brood prior to juvenile independence (i.e., fry dis-persal). These cases could also be considered a form of skippedspawning by males, and such behavior has been observed dur-ing multiple studies (Philipp et al. 1997; Suski and Ridgway2007; Parkos et al. 2011). A long-term study of SmallmouthBass on Lake Opeongo, Ontario, observed that 50.5% of 1,187nesting males did not rear their broods to independence (Suskiand Ridgway 2007).

Skipped spawning by a large proportion of a populationwould result in fewer total broods produced during a seasonthan could be possible if all mature adults spawned. High levelsof skipped spawning in Florida Bass populations have resultedin reproductive failure (i.e., year-class failure) in some cases(Chew 1973; Smith 1976). However, skipped spawning couldbe a mechanism for recruitment compensation, such that lowernumbers of successful broods could increase the juvenile sur-vival rates. This could cause the number of recruits per suc-cessful brood to vary inversely with the number of broods (i.e.,recruitment compensation; Walters and Martell 2004). Chew(1973) found cases in which only a portion of the adult pop-ulation of Florida Bass spawned, but substantial year-classeswere produced. Thus, identifying the conditions under whichskipped spawning occurs is important for understanding recruit-ment processes and mechanisms for density dependence in fishpopulations.

The Florida Bass is an upper-trophic-level species, and thusthe population demographics of Florida Bass are highly influ-enced by changes in resource limitation (Wilbur et al. 1974).The reproductive physiology and behavior of Florida Bass havebeen well described (Carr 1942; Clugston 1966; Chew 1974;Isaac et al. 1998; Warren 2009). Generally, Florida Bass are cat-egorized as iteroparous annual spawners, but few studies haveexplored spatial and temporal differences in adult abundanceand the number of broods produced annually. The objective ofthis study was to quantify Florida Bass reproductive effort (i.e.,the estimated number of broods produced annually) in a seriesof north-central Florida lakes.

METHODSStudy area.—Four neighboring lakes were selected to allow

for the comparison of reproductive effort across a localized spa-tial scale. The lakes were located within a 204-ha area (Figure 1).The four lakes ranged from 2.7 to 26.2 ha in surface area andfrom 2.3 to 3.7 m in mean depth (Table 1). A previous studyby Canfield and Hoyer (1992) measured the limnological char-acteristics and aquatic macrophyte coverage of all four lakes(Table 1). At the time of that study, three of the lakes (KeysPond, Devils Hole Lake, and Picnic Lake) were classified asacidic and clear, with generally low productivity; Keys Pondand Devils Hole Lake were considered mesotrophic, and PicnicLake was considered oligotrophic. Big Fish Lake was classifiedas eutrophic, having a relatively high pH, total nitrogen concen-tration, and chlorophyll-a concentration (Table 1). During thesummer in 2010 and 2011, water quality (i.e., pH, total nitro-gen, total phosphorus, and chlorophyll a) and aquatic vegetation(i.e., percent area covered and percent volume infested) were re-assessed in each lake. The updated measurements were similarto the water quality and aquatic vegetation coverage assessmentsmade in the 1980s by Canfield and Hoyer (1992).

All four lakes are located on private, undeveloped land. Ac-cess to the lakes is restricted, and recreational fishing is negligi-ble. Florida Bass and Bluegills Lepomis macrochirus are abun-dant in all four lakes. The Lake Chubsucker Erimyzon sucetta,

TABLE 1. Limnological characteristics of the four study lakes in Putnam County, north-central Florida. Average adult Florida Bass density (adult density;fish/ha) for each lake and average density of adults by trophic state for 56 Florida lakes (Hoyer and Canfield 1996) are presented.

Mean (max)Mean Mean adult adult densitySecchi Mean Mean Mean density for Florida

Mean (max) depth Mean total P total N chlorophyll a Trophic (fish/ha), lakes byLake depth (m) (m) pH (µg/L) (µg/L) (µg/L) classification 2010–2012 trophic state

Big Fish 2.5 (4.8) 2.9 8.7 15.0 1,496.7 8.0 Eutrophic 63 28 (75)Devils Hole 3.7 (6.9) 4.2 5.5 10.7 333.3 6.6 Mesotrophic 34 18 (56)Keys Pond 2.3 (6.0) 3.0 5.7 5.3 1,850.0 5.6 Mesotrophic 22 18 (56)Picnic 2.6 (4.6) 4.1 4.4 5.0 170.0 1.3 Oligotrophic 23 9 (17)

Dow

nloa

ded

by [

Uni

vers

ity o

f Fl

orid

a] a

t 09:

57 1

6 Ja

nuar

y 20

14

VARIATION IN FLORIDA BASS REPRODUCTIVE EFFORT 87

FIGURE 1. Map of the four study lakes (Picnic Lake, Keys Pond, Devils Hole Lake, and Big Fish Lake) located in Putnam County, north-central Florida.

another important forage species for Florida Bass, is present inthree of the lakes (Devils Hole Lake, Keys Pond, and PicnicLake).

Capture–recapture population estimates.—Fish populationsin all of the study lakes were closed to immigration or emi-gration between water bodies. Florida Bass abundance in eachlake was estimated by using capture–recapture methods. FloridaBass were captured with both electrofishing and hook-and-lineangling. Capture events were conducted via electrofishing sur-veys of the littoral zone of each lake by using a Smith-Root9.0 generator-powered pulsator (GPP) electrofishing unit witha boom-mounted electrode. All of the collected Florida Basswere measured for TL (mm) and weight (kg) and were markedwith a pelvic fin clip. Individuals smaller than 25.0 cm TL wereconsidered juveniles based on previous length-at-age data col-lected by Canfield and Hoyer (1992). These fish were markedwith a left pelvic fin clip. Adult Florida Bass (≥25.0 cm TL)were marked with a right pelvic fin clip, and each adult wasscanned for the presence of a PIT tag (Biomark). If no previoustag was detected, a uniquely numbered PIT tag was implantedby insertion into the body cavity between the pelvic fins (Harveyand Campbell 1989). Hook-and-line angling was accomplishedby using a variety of artificial lures, and fish were marked inthe same manner as those captured by electrofishing. Recapture

events for population estimation included 600-s transects cover-ing the entire perimeter of each lake. The Jolly–Seber populationestimator for multiple recapture events was used to estimate thepopulation size of adult Florida Bass in each lake (Jolly 1965;Seber 1982).

Relative weight (Wr) was used as a general measure of FloridaBass condition among lakes (Wege and Anderson 1978; Ander-son and Neumann 1996). For adult Florida Bass (≥25.0 cm TL)in each lake, Wr was calculated as

Wr = (W/Ws) × 100,

where W is the wet weight (g) of each individual and Ws isthe length-specific standard weight (Wege and Anderson 1978;Anderson and Neumann 1996). To avoid biases resulting fromincreased gonad weight, adults that were collected during theperiod immediately prior to spawning each year (December–February) were not included in Wr calculations.

Brood counts.—To determine the proportion of adults thatspawned in each lake during each spawning season, we quan-tified the number of broods per spawning adult by assuming a1:1 (male : female) sex ratio. Surveys estimating the number ofbroods in each lake were conducted during the spring spawn-ing season in 2010–2012. Water temperatures in the littoral

Dow

nloa

ded

by [

Uni

vers

ity o

f Fl

orid

a] a

t 09:

57 1

6 Ja

nuar

y 20

14

88 SHAW AND ALLEN

zone of each lake were monitored throughout the study periodwith Onset HOBO temperature loggers placed at approximately1.0–1.5-m depth. Temperature loggers were set to record watertemperature (◦C) every 4 h. Average daily water temperaturewas calculated for each lake throughout the year. Boat surveyswere conducted once weekly, starting before water tempera-tures approached the optimum spawning temperatures reportedfor black basses (15–23◦C; Chew 1974; Philipp et al. 1997).Snorkel surveys were initiated when evidence of spawning ac-tivity was observed (i.e., nest building and increased presenceof adults in the littoral zone).

The littoral zone (depth = 0.0–3.0 m) of each lake wasmapped and divided into approximately equal-area transectsby using ArcMap version 9.3. The two smaller lakes (<10 ha;Keys Pond and Big Fish Lake) were divided into four transects,whereas the larger lakes (>10 ha; Picnic and Devils Hole lakes)were divided into 10 transects. Annual changes in water levelwere monitored by using a stationary water level gauge locatedin the littoral zone of each lake. Total lake area and littoral areawere then quantified for each spawning season by adjusting forannual changes in water level.

Snorkel surveys were conducted twice weekly (every 3–4 d)on all four lakes for the duration of the spawning season. Twonew transects were randomly chosen for each survey, resultingin a total of four new transects covered in each lake during eachweek. To cover the littoral zone represented in each transect,snorkelers swam in a tight weaving pattern perpendicular tothe shoreline out to approximately 3.0-m depth. A brood wasdefined as any stage of young that was present (i.e., eggs, larvae,or fry). Reproductive effort was defined as the annual numberof broods; thus, a brood had to be present to be counted. Forexample, an empty nest that did not contain a brood was notcounted. Male Florida Bass construct a nest prior to courting afemale, and it was common—especially early in each season—to see multiple empty nests or “scrapes” present along the surveytransects. Because we were not able to determine whether thesescrapes would eventually result in a spawned brood, they werenot counted. Each observed nest that contained a brood wasmarked with an individually numbered tag to avoid counting thesame nest twice on future surveys. After yolk sac absorption,bass fry will remain in a school rising out of the nest until theyreach approximately 3.0 cm in length, when the school willbegin to disperse (Kramer and Smith 1960; Jackson and Noble1995). Development time from egg to fry is inversely relatedto water temperature (Chew 1974). As temperatures warmedduring the spawning season, it became possible for new broodsto reach the swim-up fry stage prior to being recorded. Thus,new schools of fry (“fry balls”) that were observed during asnorkel survey were counted as new broods and were includedin the annual brood estimate.

The number of broods observed was summed by date andtransect for a total brood count (C) each week. The number of

broods for each lake in each week (N ) was estimated as

N =(

C

α p

)

where α is the sampling fraction (i.e., area sampled/total littoralarea; m2), and p is the overall detection probability (Williamset al. 2002). Variance of N for each week was estimated as

var(N

) ≈[

var (C)

E(C)2+ var ( p)

p2

]N 2,

where the expected count (E[C]) is the product of the areasampled (α) and N. The variance in count (var[C]) was estimatedas

var (C) = m[

pS2 (1 − α) + σ2],

where m is the number of counts conducted (e.g., transectssampled) for the week, S2 is the variance in the weekly countestimate, and σ2 is the mean variance for all counts on arealunits within A (Williams et al. 2002). Weekly estimates of thenumber of broods were summed over the spawning season toyield an estimate of the annual number of broods in each lake.Confidence intervals and SDs for the estimated annual numberof broods were generated using parametric bootstrap by con-ducting 1,000 iterations (with replacement) of a random normaldistribution from the weekly N and var(N ) estimates.

To measure the probability of brood detection p, multipledependent observer counts were conducted once weekly in eachlake (Cook and Jacobson 1979; Nichols et al. 2000). Duringthese counts, one snorkeler (the secondary observer) surveyedboth of the randomly chosen transects. The first snorkeler tocover the area (the primary observer) marked each brood ob-served in a nest and counted all free-swimming fry balls thatwere observed during the initial swim of the transect. The sec-ondary observer then swam the transect while recording thesame information. The two observers’ counts of nested broodsand fry balls were compared to determine how many broodswere missed. The observers switched their roles as primary andsecondary when observations were initiated on a new sampleunit. Brood detection probability for each observer ( p1, p2) andthe overall p (Cook and Jacobson 1979) were calculated as

p1 = x11x22 − x12x21

x11x22 + x22x21,

p2 = x11x22 − x12x21

x11x22 + x11x12, and

p = 1 − x12x21

x22x11,

Dow

nloa

ded

by [

Uni

vers

ity o

f Fl

orid

a] a

t 09:

57 1

6 Ja

nuar

y 20

14

VARIATION IN FLORIDA BASS REPRODUCTIVE EFFORT 89

where xij represents the number of broods (i.e., nested broodsand fry balls) counted by observer i (i = 1, 2) on the sample unitswhen observer j (j = 1, 2) was the primary observer. Variance ofp was calculated as described by Cook and Jacobson (1979). Welooked for effects of adult Florida Bass abundance and condition(i.e., Wr) on the estimated number of broods.

RESULTS

Population CharacteristicsAll four lakes contained high-density Florida Bass popula-

tions showing evidence of relatively slow growth. Adult densityin each lake was above the average for corresponding trophicstate as reported by Hoyer and Canfield (1996) in a study of56 Florida lakes (Table 1). Length frequency distributions weresimilar among the lakes, with the majority (range = 84–95%)of adult Florida Bass falling between 25.0 and 35.0 cm TL andwith relatively few individuals growing larger than 40.0 cm TL(Figure 2). Given the lack of fishing mortality in these lakes,the small adult sizes indicate that growth is relatively slow.

Florida Bass abundance in Big Fish Lake, Keys Pond, and Dev-ils Hole Lake remained relatively stable during the study period.However, adult abundance in Picnic Lake decreased 38.2% be-tween the 2011 and 2012 spawning seasons (N = 731 and 452adults, respectively; Table 2). Average Wr of adult Florida Bass(≥25.0 cm TL) varied slightly among lakes (Table 3), but alllakes fell within the range of “poor” Wr values as describedby Bennett (1970; Anderson and Neumann 1996). Thus, allfour lakes had high-density populations characterized by slowgrowth.

Brood Detection ProbabilityBrood detectability rate varied among observers and based

on observer experience level. In 2010 and 2011, overall p was0.97 (SD = 0.0095), while in 2012 p was estimated at 0.65 (SD= 0.0095). The p for individual observers increased with ob-server experience level. For example, a relatively inexperiencedobserver (i.e., first year involved in the study) had an average pof 0.53 in the first half of the spawning season and ended with awhole-season p of 0.74. Observers’ brood detectability carried

FIGURE 2. Relative length frequency distributions of Florida Bass sampled in the four study lakes: (a) Big Fish Lake, (b) Devils Hole Lake, (c) Keys Pond, and(d) Picnic Lake.

Dow

nloa

ded

by [

Uni

vers

ity o

f Fl

orid

a] a

t 09:

57 1

6 Ja

nuar

y 20

14

90 SHAW AND ALLEN

TABLE 2. Abundance and density of adult Florida Bass (≥25.0 cm TL) in the four study lakes (north-central Florida) during 2010–2012. Annual reproductiveeffort in each study lake is summarized as the estimated number of broods produced annually. Also included are the estimated proportion of adults that producedbroods during each spawning season and the number of potential spawners (assuming a 1:1 sex ratio). Values in parentheses represent 95% CIs.

Adult abundance Adult density Estimated number Potential Broods perLake Year (N) (fish/ha) of broods spawners potential spawner

Big Fish 2010 165 (125–238) 56 96 (85–125) 83 1.162011 162 (121–231) 59 4 (2–6) 81 0.052012 171 (127–245) 74 0a 86 0.00

Devils Hole 2010 394 (328–491) 34 639 (584–691) 197 3.242011 397 (343–467) 34 741 (670–817) 199 3.722012 392 (342–444) 35 317 (282–365) 196 1.62

Keys Pond 2010 71 (56–102) 18 9 (8–9) 36 0.252011 70 (57–91) 21 12 (8–16) 35 0.342012b – – 11 (5–16) 35 0.31

Picnic 2011 731 (435–1,419) 28 9 (6–12) 366 0.022012 452 (314–703) 19 3 (1–5) 226 0.01

aNo nests were observed in Big Fish Lake during 2012 due to low visibility throughout the spawning season. Annual reproductive effort was likely low but not zero.bWater levels were too low in Keys Pond during 2012 to estimate population abundance using mark–recapture electrofishing. The potential spawners and broods per spawner estimates

for 2012 were calculated by assuming a relatively stable population (N = 70 adults) as was observed in 2010 and 2011.

over into the next season, with experienced observers (i.e., thosewith two or more years of experience) having higher seasonal p(i.e., p1 = 0.87, p2 = 0.98) than observers in their first season(i.e., p3 = 0.62).

Overall p (i.e., all observers combined) did not vary by broodstage. Average p of broods in nests was 0.74 (SD = 0.31, n =26; all observers, lakes, and years combined). Average p of free-schooling fry balls was also 0.74 (SD = 0.38, n = 20; all ob-servers, lakes, and years combined). However, when consideringobserver experience, the level of detectability differed slightlyby stage, particularly for inexperienced observers (those withless than 1 year of experience). For inexperienced observers,the detectability of fry balls (mean p = 0.48, SD = 0.39, n =10) was lower than the detectability of broods associated witha nest (mean p = 0.63, SD = 0.37, n = 13). For experiencedobservers (i.e., those with two or more years of experience), thedetectability of fry balls averaged 1.0 (SD = 0.0, n = 10) andthe detectability of broods associated with nests averaged 0.86(SD = 0.20, n = 13).

Annual Reproductive EffortReproductive effort varied substantially among lakes. Florida

Bass in Devils Hole Lake exhibited the highest reproductiveeffort during all 3 years, ranging from 317 estimated broods (SD= 21.3) in 2012 to 741 broods (SD = 38.0) in 2011 (medianwas 639 broods [SD = 26.6] in 2010; Table 2). In Big FishLake, Florida Bass produced 96 estimated broods (SD = 10.5)in 2010 and 4 broods (SD = 1.0) in 2011 (Table 2). The numberof broods observed in Big Fish Lake during 2012 was zero.Florida Bass in Keys Pond demonstrated similar nesting effortin all 3 years: 9 broods (SD = 0.3) in 2010; 12 broods (SD = 2.2)in 2011; and 11 broods (SD = 2.7) in 2012 (Table 2). Picnic Lakewas surveyed in 2011 and 2012, and an estimated 9 broods (SD= 1.5) and 3 broods (SD = 1.0), respectively, were produced(Table 2). During each spawning season, the earliest broods wereobserved in Devils Hole Lake. Spawning was initiated when thewater temperature was close to 20◦C in 2011 and 2012. Watertemperatures were slightly colder in 2010 than in the subsequent2 years, and the first nests were observed when the temperature

TABLE 3. Average (SE in parentheses) relative weight (Wr) of adult Florida Bass (≥25.0 cm TL) in each of the four study lakes (2011–2012); and average Wr

of adults sampled during the summer postspawn period through the fall in 2011, with corresponding reproductive effort (broods/potential spawner) estimated forthe 2012 spawning season.

Population Postspawn–fall 2012 broods perLake mean Wr 2011 Wr potential spawner

Big Fish 68.6 (2.56) 68.0 (2.71) 0.00a

Devils Hole 68.8 (1.14) 69.6 (0.95) 1.62Keys Pond 67.5 (4.05) 69.4 (2.78) 0.34Picnic 65.4 (1.07) 64.4 (3.81) 0.01

aNo nests were observed in Big Fish Lake during 2012 due to low visibility throughout the spawning season. Annual reproductive effort was likely low but not zero.

Dow

nloa

ded

by [

Uni

vers

ity o

f Fl

orid

a] a

t 09:

57 1

6 Ja

nuar

y 20

14

VARIATION IN FLORIDA BASS REPRODUCTIVE EFFORT 91

FIGURE 3. Frequency plot of the number of Florida Bass broods observed by snorkelers on each date in each lake and year, with corresponding average dailywater temperature. Picnic Lake is not included because the number of observed broods was very low in both years (i.e., 3 broods in 2011; 1 brood in 2012). Thenumber of broods observed in Big Fish Lake during 2012 was zero, and thus it is not included.

reached 15◦C. During all 3 years, spawning in all lakes ceasedat water temperatures of 27–28◦C.

The proportion of mature adult Florida Bass that spawned(i.e., broods per potential spawner) varied among lakes andacross years within lakes. The annual proportions ranged from0.01 broods/potential spawner in Picnic Lake during 2012 to3.73 broods/potential spawner in Devils Hole Lake during 2011(Table 2; Figure 3). The proportion of adults that spawnedalso varied within lakes across all years. Three lakes (BigFish Lake, Keys Pond, and Picnic Lake) showed some levelof skipped spawning by a percentage of the adult populationduring each year (Table 2; Figure 3). Across years, Keys Pondhad moderate adult spawner proportions ranging from 0.25 to0.34 broods/potential spawner (median = 0.31; Table 2). InBig Fish Lake, the proportion of spawners was relatively highin 2010 at 1.16 broods/potential spawner but then decreasedto 0.05 broods/potential spawner in 2011 (Table 2; Figure 3).Picnic Lake showed consistently low spawner proportions for

the 2 years of observation (0.01–0.02 broods/potential spawner;Table 2; Figure 3). Devils Hole Lake was the only lake thatexhibited no evidence of skipped spawning by adult FloridaBass across all 3 years, with the proportion of spawning adultsranging from 1.62 broods/potential spawner in 2012 to 3.73broods/potential spawner in 2011 (Table 2; Figure 3).

Average Wr was calculated for adults that were sam-pled from the summer postspawn period through the fall in2011 (prior to the 2012 spawning season). Devils Hole Lake,which had the highest observed proportion of spawning adults(broods/potential spawner; in 2012), also had the highest ob-served Wr (Table 3). Picnic Lake, which had the lowest observedproportion of spawning adults, had the lowest observed Wr (Ta-ble 3). However, for this time period, Wr values of Florida Bassfrom all four study lakes would still be considered poor.

Annual reproductive effort of Florida Bass was not relatedto the annual abundance of adults (Figure 4). Although PicnicLake had the highest adult Florida Bass abundance due to its

Dow

nloa

ded

by [

Uni

vers

ity o

f Fl

orid

a] a

t 09:

57 1

6 Ja

nuar

y 20

14

92 SHAW AND ALLEN

FIGURE 4. Annual abundance of adult Florida Bass (≥25.0 cm TL) andestimated annual reproductive effort (estimated annual number of broods) in allfour study lakes, 2010–2012.

large size relative to the other lakes, it consistently had thelowest estimated number of broods (Table 2; Figure 4). The threeother lakes had relatively consistent abundance across years butexhibited variation in the number of broods produced annually(Table 2; Figure 4). Thus, based on these results, the abundanceof adult Florida Bass would not serve as a useful indicator ofannual reproductive effort across lakes.

DISCUSSIONAnnual reproductive effort of a population is difficult to quan-

tify; thus, there is a lack of data on spatial and temporal changesin the reproductive effort of fish populations (Rideout et al.2005). As such, the reproductive strategy of adult fish is gen-erally assumed to be similar across populations, and annualreproductive effort is assumed to be related to the abundanceof mature adults (Walters and Martell 2004). However, vari-ability in reproductive effort has been reported for many fishspecies (Rideout et al. 2005; Jørgensen et al. 2006; Rideout andTomkiewicz 2011). Application of these assumptions to blackbass species has been questioned, and the need for further re-search has been recognized due to the lack of a relationshipbetween adult abundance and reproductive effort (Ridgway andPhilipp 2002). The populations of Florida Bass in this studyexhibited variation in the estimated number of broods producedacross localized spatial and temporal scales. Among neighbor-ing lakes and within a given lake across years, we found evi-dence for multiple spawning events per adult and for skippedspawning. The proportion of adults that skipped spawning inany given year varied from moderate (∼25–50% of the adultsdid not attempt to spawn) to severe (>90% of adults did notattempt to spawn).

The high proportion of spawning adults (broods/potentialspawner) observed in Devils Hole Lake over multiple years indi-cates that both females and males likely spawned multiple times

in a season. In southern latitudes, where the spawning seasonis prolonged, multiple spawning events by individuals of bothsexes have been observed for Largemouth Bass M. salmoides(Dadzie and Aloo 1990; Gran 1995; Isaac et al. 1998; Watersand Noble 2004). Similar to other black bass species, femaleFlorida Bass exhibit asynchronous maturation of ova, suggest-ing that they have the ability to spawn multiple times throughoutthe spawning season and the potential to spawn in the nests ofmultiple males (i.e., batch spawning; Chew 1974; Rosenblumet al. 1991; Tyler and Sumpter 1996; DeWoody et al. 2000).Furthermore, male Florida Bass whose nests failed as a result ofegg removal in a hatchery initiated additional spawning events(Isaac et al. 1998). High rates of nest failure may result in mul-tiple spawning events by males in order to produce a successfulbrood.

Skipped spawning has been observed in many fish popula-tions in both marine and freshwater systems. The proportion ofthe population that forgoes spawning in a season often remainselusive due to the difficulty in defining, and thus quantifying,annual reproductive effort by individual fish over successiveyears (Rideout et al. 2005). In this study, skipped spawning wasthe more common reproductive strategy among the neighboringFlorida Bass populations. Proportions of each population thatdid not spawn in a given season varied among lakes and withinlakes across years. Populations exhibiting skipped spawningwere generally described as having shortened and highly in-consistent spawning effort relative to the populations with highreproductive effort (e.g., Devils Hole Lake in all years and BigFish Lake in 2010). We defined reproductive effort as the esti-mated number of broods; however, broods vary in size. Thus, thenumber of individuals in a brood can provide a more detailedindicator of total reproductive effort. Future studies could in-crease the detail associated with quantifying reproductive effortby incorporating brood size at the earliest stages (i.e., numberof eggs) prior to compounding mortality effects related to theenvironment and predation.

The selection of the four study lakes from among the manylakes in the area was based on a combination of relatively smallsize, water clarity, a defined depth profile, and little anthro-pogenic disturbance (via recreational angling or shoreline de-velopment). The closed Florida Bass populations in these studylakes allowed for more confidence in population and broodestimates and likely more homogeneous populations. How-ever, the results reported here are probably not transferable tolarge systems with greater heterogeneity in environmental andpopulation-level factors (Baylis et al. 1993).

The probability of detection p is an important parameterthat needs to be addressed when using count-based abundanceestimators (Williams et al. 2002). In visually based surveys, de-tection is typically assumed to differ based on environmentalconditions that would affect visibility. In this study, we notedthat the variation in p was more closely related to observers—particularly observer experience level—than to environmentalconditions. This highlights the importance of quantifying p to

Dow

nloa

ded

by [

Uni

vers

ity o

f Fl

orid

a] a

t 09:

57 1

6 Ja

nuar

y 20

14

VARIATION IN FLORIDA BASS REPRODUCTIVE EFFORT 93

account for heterogeneity among observers as well as the envi-ronment. It also suggests that future studies may benefit fromincluding observers in their levels of stratification of samplingeffort so as not to confound potential observer effects with otherpredictor variables.

Our estimates of annual reproductive effort should be con-sidered underestimates when considering the true annual repro-ductive effort (i.e., total number of broods spawned). We wereunable to account for some environmental effects on observa-tions and behavioral aspects of Florida Bass reproduction thatwould result in an underestimation of reproductive effort. Thestudy lakes were chosen in part for their relatively high aver-age Secchi depths (Table 1). However, water clarity in Big FishLake during the 2012 spawning season was the lowest observedamong the 3 years, and no broods were detected by any of theobservers. Age-1 recruits that would have been spawned dur-ing that season were observed in early 2013 (S.L.S., personalobservation); therefore, it is clear that reproduction occurred,although we were unable to quantify it due to low visibility.Water clarity levels for Big Fish Lake in 2010 and 2011 and forall other lakes during all study years were close to the averagereported and likely had little effect on estimates of the numberof broods. Studies of black bass reproduction have observed thatschooling fry balls will combine into larger schools, with one ormultiple males guarding them until dispersal (Carr 1942; Allanand Romero 1975; Warren 2009). In our study, a fry ball wascounted as a single brood because we were unable to determinewhether multiple fry balls were schooling together. Another po-tential bias arose because we did not count nests in which abrood was not observed. We were unable to determine whetheran empty nest (1) had contained a brood that was abandoned andlost or (2) was a newly constructed nest in which a brood wouldbe produced in the future. Thus, these nests were not counted,possibly resulting in the underestimation of annual reproductiveeffort. However, the effect of this bias would not be expectedto vary among lakes or among years, so the relative differencesin reproductive effort among lakes were probably indicative ofreal differences.

We did not determine the sex ratio of the population in eachlake; therefore, our estimates of reproductive effort were madeunder a general assumption of a 1:1 (male : female) sex ratio.This assumption meant that the estimate of reproductive effortwas reliant on male nesting behavior, as it was assumed thateach brood was produced by only one male and only one fe-male. This may not be the case, particularly in systems wheremortality rates and age at maturity vary by sex. In Nebish Lake,Wisconsin, female Smallmouth Bass were found to mature laterthan males, resulting in a male-biased adult sex ratio (Raffettoet al. 1990; Baylis et al. 1993). Previous studies have also ob-served that multiple females may contribute to the brood of onemale (DeWoody et al. 2000). Our results assumed that eachmale had a potential female, but we were unable to verify thisassumption. Limited availability of mates would likely have agreater impact on annual reproductive effort if female numbers

were biased low, resulting in a higher number of males that areunable to produce a brood. A sex ratio that is skewed toward fe-males may be less limiting because multiple females may spawnin the nest of a single male, thus reducing the potential for a highnumber of females to retain gametes (i.e., due to an inability tofind a mate).

Annual reproductive effort varied among lakes and withinlakes across years, but the mechanisms influencing effort dur-ing a given year were unclear. Previous research on skippedspawning in fish populations indicates that environmental, nu-tritional, and population-level effects can influence reproductiveeffort (Rideout et al. 2005). Environmental factors (i.e., pollu-tion, habitat, and water temperature) were unlikely to have im-pacted the reproductive effort of the four study populations. Allof the study lakes are located on private, undeveloped land withhighly restricted access and can be described as pristine Floridalakes. A broad littoral zone containing suitable spawning habi-tat (i.e., structure and vegetation) was available in each lake.Fluctuating water levels affected the amount of littoral area thatwas available across years in each lake, but due to the prolongedspawning season, spawning habitat availability would not havebeen restricted. Cold spells can delay or interrupt the spawn-ing behavior of Florida Bass (Chew 1974; Mesing and Wicker1986), but no large swings in temperature occurred during thespawning seasons over the duration of this study. The lowestwater temperatures were observed early in the 2010 spawningseason, but no interruption of spawning behavior or reduction ofannual reproductive effort was observed for Devils Hole Lake, inwhich spawning was most common. Considering the prolongedspawning seasons for Florida Bass in their native range (Rogersand Allen 2009), cold spells may interrupt spawning behaviorbriefly but would be unlikely to affect the annual reproductiveeffort of a population.

Picnic Lake, which had the lowest estimated number ofFlorida Bass broods in all seasons, was also the most acidicof the study lakes. Increasing acidity in George Lake, Ontario(e.g., pH was 6.5 during 1961 and ranged from 4.8 to 5.3 in1971–1972), and in other northern lakes has resulted in fishmortality events and failure to spawn (Beamish et al. 1975;Haines 1981). Unlike the increasing acidification reported innorthern lakes, evidence suggests that the pH in Picnic Lakehas been consistently low for the past 20 years and that the lakelikely undergoes small seasonal changes in water chemistry,similar to other lakes in north-central Florida (Brezonik et al.1982; Canfield and Hoyer 1992). Naturally acidic, clear, olig-otrophic lakes comprise about 10–15% of Florida’s lakes (Can-field et al. 1985). The persistence of Florida Bass populationsin these acidic lakes may reflect a difference in acid tolerancecompared with northern Largemouth Bass populations (Can-field et al. 1985). However, we cannot rule out the hypothesisthat low pH contributed to skipped spawning at Picnic Lake.

Poor condition (i.e., insufficient energy reserves) is the mostcommonly reported cause of skipped spawning (Rideout et al.2005; Rideout and Tomkiewicz 2011). Spawning of fish in

Dow

nloa

ded

by [

Uni

vers

ity o

f Fl

orid

a] a

t 09:

57 1

6 Ja

nuar

y 20

14

94 SHAW AND ALLEN

captivity can be interrupted when diets are controlled (Hislopet al. 1978; Burton and Idler 1987; Rijnsdorp 1990; Maddockand Burton 1994; Bunnell et al. 2007). Adults in the wild thatare classified as being in a nonreproductive state have been ob-served to exhibit poorer condition than reproductive individuals(Burton and Idler 1987; Rideout et al. 2000). If condition is acause, females are able to enter a resting stage, and the annualreproductive cycle is interrupted prior to vitellogenesis (Ride-out et al. 2005; Rideout and Tomkiewicz 2011). Females mayalso complete their annual reproductive cycle but retain and ul-timately reabsorb their eggs via follicular atresia (Scott 1962;Hislop et al. 1978; Ma et al. 1998; Kennedy et al. 2008). Lessis known about the possible effect of poor condition on skippedspawning in males (Rideout and Tomkiewicz 2011). Conditionof adult Florida Bass in the four study lakes would be consid-ered “poor” in comparison with other populations of FloridaBass and Largemouth Bass (Bennett 1970; Anderson and Neu-mann 1996). It is likely that condition alone did not drive thedifferences in annual reproductive effort among lakes becauseFlorida Bass in all lakes displayed poor condition, but the de-gree of skipped spawning varied widely. It is not known whetherthe growth, age structure, and mortality of the populations var-ied substantially. Length frequency data indicated only minordifferences, but future studies should estimate all vital rates andevaluate whether they are related to spawning frequency.

The best methods for determining the mechanisms that af-fect spawning frequency would likely require monitoring atthe level of the individual. Tracking of uniquely tagged adultsduring the spawning season (as per Waters and Noble 2004)coupled with brood monitoring surveys would provide a robustapproach for differentiating physical versus environmental vari-ables that may influence spawning frequency. Gonad samplingbefore, during, and after the spawning period would provide im-portant information regarding size and age at maturity, changesin gonad maturation through time, and the number of adultsthat have entered resting or retaining stages without spawning(Swingle 1943; Chew 1973). Gonad sampling methods in mostcases would require mortality of sampled individuals, which hasthe potential to influence population dynamics, particularly insmall systems like those in this study. Another potential methodof tracking individual reproductive stage involves the quantifi-cation of steroid concentrations that influence gonad maturationand spawning behavior (i.e., testosterone, 11-ketotestosterone,estradiol, progesterone, and vitellogenin). Steroid concentra-tions cycle seasonally and drive gonad maturation processes;thus, they can allow the sex and maturity stage of individualsto be determined. Blood sample collection is generally non-lethal, and individuals can be resampled through time. Quan-tification of steroid concentrations in black bass species, par-ticularly Largemouth Bass and Florida Bass, has typically beenused to examine the influence of environmental contaminantson physiology (Sepulveda et al. 2001; Gross et al. 2002; Mar-tyniuk et al. 2009). Studies conducted on sturgeons often usesteroid concentrations as indicators of the reproductive stage

of individuals during the spawning season (Webb et al. 2002;Webb and Doroshov 2011; Shaw et al. 2013).

Skipped spawning could be a mechanism for recruitmentcompensation in fish populations, but few studies have consid-ered this factor in recruitment processes. Compensation refersto a negative feedback interaction that would stabilize a popu-lation by offsetting the losses of individuals via mortality (i.e.,natural or fishing mortality; Rose et al. 2001). Recruitment com-pensation implies that the number of offspring recruiting to apopulation per mature adult increases at low population sizesbecause the resources available to individuals would be greaterat a low density (DeAngelis et al. 1991). Stable average recruit-ment has been noted in many fish species across a wide range ofspawner abundances (Hilborn et al. 1995; Walters and Martell2004). Per-capita recruitment rates (i.e., number of recruits peradult) in fish species are often inversely related to populationsize (Cushing 1995; Myers et al. 1999; Rose et al. 2001; Allenet al. 2011). We found that annual reproductive effort was notpositively related to spawner abundance. However, lower annualreproductive effort through skipped spawning could provide amechanism for compensatory recruitment, possibly increasingjuvenile survival during years when the number of broods pro-duced is low. Additionally, recruitment models for many speciesmay be ineffective because they fail to incorporate data on stockdemography and individual variability in spawner quality (Trip-pel 1999; Marshall et al. 2003; Tomkiewicz et al. 2003; Rideoutet al. 2005). This is true of the black basses, as there is no clear re-lationship between spawner abundance and recruitment for anyof these species (Parkos and Wahl 2002; Ridgway and Philipp2002), leading to much debate (Allen et al. 2013; Parkos et al.2013). In the case of black basses, variability in annual repro-ductive effort may be more common than anticipated, therebyclouding the relationships between spawner abundance and re-cruitment. Thus, attempts to understand recruitment processesshould consider variable reproductive effort as a mechanism in-fluencing juvenile survival rates, and the lack of a stock–recruitrelationship should not be viewed as definitive proof that adultpopulation dynamics are irrelevant.

ACKNOWLEDGMENTSThis study was funded by the Sport Fish Restoration Program

through the Florida Fish and Wildlife Conservation Commis-sion. We thank W. Porak, C. Suski, D. Philipp, and J. Dotsonfor input on study design and approach.

REFERENCESAllan, R. C., and J. Romero. 1975. Underwater observations of Largemouth Bass

spawning and survival in Lake Mead. Pages 104–112 in R. H. Stroud andH. E. Clepper, editors. Black Bass biology and management. Sport FishingInstitute, Washington, D.C.

Allen, M. S., M. W. Rogers, M. J. Catalano, D. C. Gwinn, and S. J. Walsh. 2011.Evaluating the potential for stock size to limit recruitment in LargemouthBass. Transactions of the American Fisheries Society 140:1093–1100.

Dow

nloa

ded

by [

Uni

vers

ity o

f Fl

orid

a] a

t 09:

57 1

6 Ja

nuar

y 20

14

VARIATION IN FLORIDA BASS REPRODUCTIVE EFFORT 95

Allen, M. S., M. W. Rogers, M. J. Catalano, D. C. Gwinn, and S. J. Walsh.2013. Assessing the potential for the angling of nesting males to influenceLargemouth Bass recruitment should consider the quality of nesting individ-uals: response to comment. Transactions of the American Fisheries Society142:419–421.

Anderson, R. O., and R. M. Neumann. 1996. Length, weight, and associatedstructural indices. Pages 447–482 in B. R. Murphy and D. W. Willis, editors.Fisheries techniques, 2nd edition. American Fisheries Society, Bethesda,Maryland.

Barwick, D. H., and D. E. Holcomb. 1976. Relation of Largemouth Bass repro-duction to crowded sunfish populations in Florida ponds. Transactions of theAmerican Fisheries Society 105:244–246.

Baylis, J. R., D. D. Wiegmann, and M. H. Hoff. 1993. Alternating life histories ofSmallmouth Bass. Transactions of the American Fisheries Society 122:500–510.

Beamish, R. J., W. L. Lockhart, J. C. Van Loon, and H. H. Harvey. 1975. Long-term acidification of a lake and resulting effects on fishes. Ambio 4:98–102.

Bennett, G. W. 1970. Management of lakes and ponds. Van Nostrand Reinhold,New York.

Brezonik, P. L., C. D. Hendry Jr., E. S. Edgerton, R. L. Schulze, and T. L.Crisman. 1982. Acidity, nutrients, and minerals in atmospheric precipita-tion over Florida: deposition patterns, mechanisms and ecological effects.U.S. Environmental Protection Agency, Environmental Research Laboratory,Project 805560, Corvallis, Oregon.

Bunnell, D. B., S. E. Thomas, and R. A. Stein. 2007. Prey resources beforespawning influence gonadal investment of female, but not male, White Crap-pie. Journal of Fish Biology 70:1838–1854.

Burton, M. P., and D. R. Idler. 1987. An experimental investigation of the non-reproductive, post-mature state in Winter Flounder. Journal of Fish Biology30:643–650.

Canfield, D. E., Jr., and M. V. Hoyer. 1992. Aquatic macrophytes and theirrelation to the limnology of Florida lakes. Florida Department of NaturalResources, Bureau of Aquatic Plant Management, Tallahassee.

Canfield, D. E., Jr., M. J. Maceina, F. G. Nordlie, and J. V. Shireman. 1985.Plasma osmotic and electrolyte concentrations of Largemouth Bass fromsome acidic Florida lakes. Transactions of the American Fisheries Society114:423–429.

Carr, M. H. 1942. The breeding habits, embryology and larval development ofthe Large-mouthed Black Bass in Florida. Proceedings of the New EnglandZoological Club 20:43–77.

Chew, R. L. 1973. The failure of Largemouth Bass, Micropterus salmoidesfloridanus (LeSueur), to spawn in eutrophic, over-crowded environments.Proceedings of the Annual Conference Southeastern Association of Gameand Fish Commissioners 26(1972):306–319.

Chew, R. L. 1974. Early life history of the Florida Largemouth Bass. FloridaGame and Fresh Water Fish Commission, Fishery Bulletin 7, Tallahassee.

Clugston, J. P. 1966. Centrarchid spawning in the Florida Everglades. QuarterlyJournal of the Florida Academy of Sciences 29:137–143.

Cook, R. D., and J. O. Jacobson. 1979. A design for estimating visibility biasin aerial surveys. Biometrics 35:735–742.

Cushing, D. 1995. Population production and regulation in the sea: a fisheriesperspective. Cambridge University Press, Cambridge, UK.

Dadzie, S., and P. A. Aloo. 1990. Reproduction of the North AmericanBlackbass, Micropterus salmoides (Lacepede), in an equatorial lake, LakeNaivasha, Kenya. Aquaculture Research 21:449–458.

DeAngelis, D. L., L. Godbout, and B. J. Shuter. 1991. An individual-based ap-proach to predicting density-dependent dynamics in Smallmouth Bass popu-lations. Ecological Modelling 57:91–115.

DeWoody, J. A., D. E. Fletcher, S. D. Wilkins, W. S. Nelson, and J. C. Avise.2000. Genetic monogamy and biparental care in an externally fertilizing fish,the Largemouth Bass (Micropterus salmoides). Proceedings of the RoyalSociety of London B 267:2431–2437.

Gillooly, J. F., T. C. O’Keefe, S. P. Newman, and J. R. Baylis. 2000. A long-term view of density-dependent recruitment in Smallmouth Bass from NebishLake, Wisconsin. Journal of Fish Biology 56:542–551.

Gran, J. E. 1995. Gonad development and spawning of Largemouth Bass in atropical reservoir. Master’s thesis. North Carolina State University, Raleigh.

Gross, T. S., C. M. Wieser, M. S. Sepulveda, J. J. Wiebe, T. R. Schoeb, and N.D. Denslow. 2002. Characterization of annual reproductive cycles for pond-reared Florida Largemouth Bass Micropterus salmoides floridanus. Pages205–212 in D. P. Philipp and M. S. Ridgway, editors. Black Bass: ecology,conservation, and management. American Fisheries Society, Symposium 31,Bethesda, Maryland.

Haines, T. A. 1981. Acidic precipitation and its consequences for aquatic ecosys-tems: a review. Transactions of the American Fisheries Society 110:669–707.

Harvey, W. D., and D. L. Campbell. 1989. Retention of passive integratedtransponder tags in Largemouth Bass brood fish. Progressive Fish-Culturist51:164–166.

Hilborn, R., C. J. Walters, and D. Ludwig. 1995. Sustainable exploitationof renewable resources. Annual Review of Ecology and Systematics 26:45–67.

Hislop, J. R. G., A. P. Robb, and J. A. Gauld. 1978. Observations on effectsof feeding level on growth and reproduction in Haddock, Melanogrammusaeglefinus (L.) in captivity. Journal of Fish Biology 13:85–98.

Hoyer, M. V., and D. E. Canfield Jr. 1996. Largemouth Bass abundance andaquatic vegetation in Florida lakes: an empirical analysis. Journal of AquaticPlant Management 34:23–32.

Isaac, J., Jr., T. M. Kimmel, R. W. Bagley, V. H. Staats, and A. Barkoh. 1998.Spawning behavior of Florida Largemouth Bass in an indoor raceway. Pro-gressive Fish-Culturist 60:59–62.

Jackson, J. R., and R. L. Noble. 1995. Selectivity of sampling methods forjuvenile Largemouth Bass in assessments of recruitment processes. NorthAmerican Journal of Fisheries Management 15:408–418.

Jolly, G. M. 1965. Explicit estimates from capture-recapture data with bothdeath and immigration-stochastic model. Biometrika 52:225–247.

Jørgensen, C., B. Ernande, Ø. Fiksen, and U. Dieckmann. 2006. The logic ofskipped spawning in fish. Canadian Journal of Fisheries and Aquatic Sciences63:200–211.

Kennedy, J., P. R. Witthames, R. D. M. Nash, and C. J. Fox. 2008. Is fecundityin Plaice (Pleuronectes platessa L.) down-regulated in response to reducedfood intake during autumn? Journal of Fish Biology 72:78–92.

Kramer, R. H., and L. L. Smith Jr. 1960. First-year growth of the LargemouthBass, Micropterus salmoides (Lacepede), and some related ecological factors.Transactions of the American Fisheries Society 89:222–233.

Ma, Y., O. S. Kjesbu, and T. Jørgensen. 1998. Effects of ration on the matura-tion and fecundity in captive Atlantic Herring (Clupea harengus). CanadianJournal of Fisheries and Aquatic Sciences 55:900–908.

Maddock, D. M., and M. P. M. Burton. 1994. Some effects of starvation onthe lipid and skeletal muscle layers of the Winter Flounder, Pleuronectesamericanus. Canadian Journal of Zoology 72:1672–1679.

Marshall, C. T., L. O’Brien, J. Tomkiewicz, F. W. Koster, G. Kraus, G. Marteins-dottir, M. J. Morgan, F. Saborido-Rey, J. L. Blanchard, D. H. Secor, P. J.Wright, N. V. Mukhina, and H. Bjornsson. 2003. Developing alternative in-dices of reproductive potential for use in fisheries management: case studiesfor stocks spanning an information gradient. Journal of Northwest AtlanticFishery Science 33:161–190.

Martyniuk, C. J., K. J. Kroll, W. F. Porak, C. Steward, H. J. Grier, and N.D. Denslow. 2009. Seasonal relationship between gonadotropin, growth hor-mone, and estrogen receptor mRNA expression in the pituitary gland ofLargemouth Bass. General and Comparative Endocrinology 163:306–317.

Mesing, C. L., and A. M. Wicker. 1986. Home range, spawning migrations,and homing of radio-tagged Florida Largemouth Bass in two central Floridalakes. Transactions of the American Fisheries Society 115:286–295.

Myers, R. A., K. G. Bowen, and N. J. Barrowman. 1999. Maximum reproductiverate of fish at low population sizes. Canadian Journal of Fisheries and AquaticSciences 56:2404–2419.

Nichols, J. D., J. E. Hines, J. R. Sauer, F. W. Fallon, J. E. Fallon, and P. J. Heglund.2000. A double-observer approach for estimating detection probability andabundance from point counts. Auk 117:393–408.

Dow

nloa

ded

by [

Uni

vers

ity o

f Fl

orid

a] a

t 09:

57 1

6 Ja

nuar

y 20

14

96 SHAW AND ALLEN

Parkos, J. J., III, and D. H. Wahl. 2002. Towards an understanding of recruit-ment mechanisms in Largemouth Bass. Pages 25–45 in D. P. Philipp and M.S. Ridgway, editors. Black Bass: ecology, conservation, and management.American Fisheries Society, Symposium 31, Bethesda, Maryland.

Parkos, J. J., III, D. H. Wahl, and D. P. Philipp. 2011. Influence of behavior andmating success on brood-specific contribution to fish recruitment in ponds.Ecological Applications 21:2576–2586.

Parkos, J. J., III, D. H. Wahl, and D. P. Philipp. 2013. Comment: assessingthe potential for the angling of nesting males to influence Largemouth Bassrecruitment should consider the quality of nesting individuals. Transactionsof the American Fisheries Society 142:416–418.

Philipp, D. P., C. A. Toline, M. F. Kubacki, D. B. F. Philipp, and F. J. S. Phelan.1997. The impact of catch-and-release angling on the reproductive success ofSmallmouth Bass and Largemouth Bass. North American Journal of FisheriesManagement 17:557–567.

Raffetto, N. S., J. R. Baylis, and S. L. Serns. 1990. Complete estimates ofreproductive success in a closed population of Smallmouth Bass (Micropterusdolomieui). Ecology 71:1523–1535.

Rideout, R. M., M. P. M. Burton, and G. A. Rose. 2000. Observations on massatresia and skipped spawning in northern Atlantic Cod from Smith Sound,Newfoundland. Journal of Fish Biology 57:1429–1440.

Rideout, R. M., G. A. Rose, and M. P. M. Burton. 2005. Skipped spawning infemale iteroparous fishes. Fish and Fisheries 6:50–72.

Rideout, R. M., and J. Tomkiewicz. 2011. Skipped spawning in fishes: morecommon than you might think. Marine and Coastal Fisheries: Dynamics,Management, and Ecosystem Science 3:176–189.

Ridgway, M. S., and D. P. Philipp. 2002. Current status and future directionsfor research in the ecology, conservation, and management of Black Bass inNorth America. Pages 719–724 in D. P. Philipp and M. S. Ridgway, editors.Black Bass: ecology, conservation, and management. American FisheriesSociety, Symposium 31, Bethesda, Maryland.

Rijnsdorp, A. D. 1990. The mechanism of energy allocation over reproductionand somatic growth in female North Sea Plaice, Pleuronectes platessa L.Netherlands Journal of Sea Research 25:279–289.

Rogers, M. W., and M. S. Allen. 2009. Exploring the generality of recruitmenthypotheses for Largemouth Bass along a latitudinal gradient of Florida lakes.Transactions of the American Fisheries Society 138:23–37.

Rose, K. A., J. H. Cowan Jr., K. O. Winemiller, R. A. Myers, and R. Hilborn.2001. Compensatory density dependence in fish populations: importance,controversy, understanding and prognosis. Fish and Fisheries 2:293–327.

Rosenblum, P. M., H. Horne, N. Chatterjee, and T. M. Brandt. 1991. Influenceof diet on ovarian growth and steroidogenesis in Largemouth Bass. Pages265–267 in A. P. Scott, J. P. Sumpter, D. E. Kime, and M. S. Rolfe, edi-tors. Proceedings of the fourth international symposium on the reproductivephysiology of fish. University of Sheffield Press, Sheffield, UK.

Scott, D. P. 1962. Effect of food quantity on fecundity of Rainbow Trout, Salmogairdneri. Journal of the Fisheries Research Board of Canada 19:715–731.

Seber, G. A. F. 1982. The estimation of animal abundance and related parame-ters. Edward Arnold, London.

Sepulveda, M. S., D. S. Ruessler, N. D. Denslow, S. E. Holm, T. R. Schoeb, andT. S. Gross. 2001. Assessment of reproductive effects in Largemouth Bass(Micropterus salmoides) exposed to bleached/unbleached kraft mill effluents.Archives of Environmental Contamination and Toxicology 41:475–482.

Shaw, S. L., S. R. Chipps, S. K. Windels, M. A. H. Webb, and D. T. McLeod.2013. Influence of sex and reproductive status on seasonal movement ofLake Sturgeon in Namakan Reservoir, Minnesota–Ontario. Transactions ofthe American Fisheries Society 142:10–20.

Smith, S. L. 1976. Behavioral suppression of spawning in Largemouth Bass byinterspecific competition for space within spawning areas. Transactions ofthe American Fisheries Society 105:682–685.

Suski, C. D., and M. S. Ridgway. 2007. Climate and body size influence nestsurvival in a fish with parental care. Journal of Animal Ecology 76:730–739.

Swingle, H. S., and E. V. Smith. 1943. Factors affecting the reproduction ofBluegill Bream and Largemouth black bass in ponds. Alabama PolytechnicInstitute, Agricultural Experiment Station, Circular 87, Auburn.

Tomkiewicz, J., M. J. Morgan, J. Burnett, and F. Saborido-Rey. 2003. Avail-able information for estimating reproductive potential of northwest Atlanticgroundfish stocks. Journal of Northwest Atlantic Fishery Science 33:1–21.

Trippel, E. A. 1999. Estimation of stock reproductive potential: history and chal-lenges for Canadian Atlantic gadoid stock assessments. Journal of NorthwestAtlantic Fishery Science 25:61–81.

Tyler, C. R., and J. P. Sumpter. 1996. Oocyte growth and development in teleosts.Reviews in Fish Biology and Fisheries 6:287–318.

Walters, C. J., and S. J. D. Martell. 2004. Fisheries ecology and management.Princeton University Press, Princeton, New Jersey.

Warren, M. L., Jr. 2009. Centrarchid identification and natural history. Pages375–534 in S. J. Cooke and D. P. Philipp, editors. Centrarchid fishes: diversity,biology and conservation. Blackwell Publishing, Chichester, UK.

Waters, D. S., and R. L. Noble. 2004. Spawning season and nest fidelity ofLargemouth Bass in a tropical reservoir. North American Journal of FisheriesManagement 24:1240–1251.

Webb, M. A. H., and S. I. Doroshov. 2011. Importance of environmental en-docrinology in fisheries management and aquaculture of sturgeons. Generaland Comparative Endocrinology 170:313–321.

Webb, M. A. H., G. W. Feist, E. P. Foster, C. B. Schreck, and M. S. Fitzpatrick.2002. Potential classification of sex and stage of gonadal maturity of wildWhite Sturgeon using blood plasma indicators. Transactions of the AmericanFisheries Society 131:132–142.

Wege, G. J., and R. O. Anderson. 1978. Relative weight (Wr): a new index ofcondition for Largemouth Bass. Pages 79–91 in G. D. Novinger and J. G.Dillard, editors. New approaches to the management of small impoundments.American Fisheries Society, North Central Division, Special Publication 5,Bethesda, Maryland.

Wilbur, H. M., D. W. Tinkle, and J. P. Collins. 1974. Environmental certainty,trophic level, and resource availability in life history evolution. AmericanNaturalist 108:805–817.

Williams, B. K., J. D. Nichols, and M. J. Conroy. 2002. Analysis and manage-ment of animal populations. Academic Press, San Diego, California.

Dow

nloa

ded

by [

Uni

vers

ity o

f Fl

orid

a] a

t 09:

57 1

6 Ja

nuar

y 20

14